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ECUADOR

PARAGUAY

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1000 miles

1000 kilometers

Major Fossil Hominin Sites

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TOGO

Toros-Menalla

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Hadar Middle Awash (Aramis, Bouri,

Herto, Dikika)

Sangiran Trinil

Niah Cave

Flores

Ngandong

Jinniushan

Lantian Ordos

MabaLiujiang

Dali

Hexian

Zhoukoudian

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Neander Valley

Heidelberg (Mauer)

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Skhul/Tabun

Amud Jebel Qafzeh

Teshik Tash

Okladnikov Cave/Denisova Cave

Sungir

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East and West Turkana Kanapoi

Olduvai/Laetoli

Omo

Kabwe

Sterkfontein/Swartkrans/Drimolen/Malapa Taung

Border Cave

Klasies River Mouth

Florisbad Lake Mungo

Kow Swamp

Tugen Hills

IntroductIon to

Physical Anthropology

About the Cover ImAge

Our closest evolutionary cousins, the nonhuman

primates are among the most endangered animals

on earth. The book cover shows four of the most

endangered species, all of which are close to extinction

due to destructive human practices.

robert Jurmain Professor Emeritus, San Jose State University

Lynn Kilgore University of Colorado, Boulder

Wenda trevathan Professor Emerita, New Mexico State University

russell L. ciochon University of Iowa

Australia • Brazil • Japan • Korea • Mexico • Singapore Spain • United Kingdom • United States

2013–2014 Edition

IntroductIon to

Physical Anthropology

This is an electronic version of the print textbook. Due to electronic rights restrictions, some third party content may be suppressed. Editorial review has deemed that any suppressed content does not materially affect the overall learning experience. The publisher reserves the right to remove content from this title at any time if

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Introduction to Physical Anthropology, 2013–2014 Edition

Robert Jurmain, Lynn Kilgore, Wenda Trevathan, Russell L. Ciochon

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1 2 3 4 5 6 7 17 16 15 14 13

chAPter 1 Introduction to Physical Anthropology 3

heredity and evolution chAPter 2 The Development of Evolutionary Theory 25 chAPter 3 The Biological Basis of Life 49 chAPter 4 Heredity and Evolution 77 chAPter 5 Macroevolution: Processes of Vertebrate and Mammalian Evolution 107

Primates chAPter 6 Survey of the Living Primates 135 chAPter 7 Primate Behavior 175 chAPter 8 Overview of the Fossil Primates 217

hominin evolution chAPter 9 Paleoanthropology: Reconstructing Early Hominin Behavior and Ecology 255 chAPter 10 Hominin Origins in Africa 277 chAPter 11 The First Dispersal of the Genus Homo: Homo erectus and Contemporaries 307 chAPter 12 Premodern Humans 331 chAPter 13 The Origin and Dispersal of Modern Humans 363

contemporary human evolution chAPter 14 Modern Human Biology: Patterns of Variation 389 chAPter 15 Modern Human Biology: Patterns of Adaptation 413 chAPter 16 Legacies of Human Evolutionary History and the Human Life Course 441 chAPter 17 The Human Disconnection 469

Appendix A: Atlas of Primate Skeletal Anatomy 484

Appendix B: Sexing and Aging the Skeleton 492

Glossary 497

Bibliography 506

Index 532

Brief contents

vii

contents

Preface xvi Acknowledgments xix Supplements xx

Chapter 1

Introduction to Physical Anthropology 3 Introduction 3 The Human Connection 5 Biocultural Evolution 6 What Is Anthropology? 10

Cultural Anthropology 11 Archaeology 11 Linguistic Anthropology 11 Physical Anthropology 12 Applied Anthropology 18 Physical Anthropology and the Scientific Method 19 A Closer Look Forensic Anthropology in Practice 21 The Anthropological Perspective 22 Summary of Main Topics 23 Critical Thinking Questions 23

heredity and evolution Chapter 2

The Development of Evolutionary Theory 25 A Brief History of Evolutionary Thought 26

The Scientific Revolution 27 Precursors of the Theory of Evolution 29

The Discovery of Natural Selection 33 In Darwin’s Shadow 37

Natural Selection 38 Natural Selection in Action 39 Constraints on Nineteenth-Century Evolutionary

Theory 42 Opposition to Evolution Today 42

A Brief History of Opposition to Evolution in the United States 43

At a glance The Mechanism of Natural Selection 45 How Do We Know? 46 Summary of Main Topics 46 Critical Thinking Questions 47 Media Resources 47

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Chapter 3

The Biological Basis of Life 49 Cells 50 The Structure of DNA 51 A Closer Look Rosalind Franklin: The Fourth (but

Invisible) Member of the Double Helix Team 52 DNA Replication 52 Protein Synthesis 53 What Is a Gene? 57 Regulatory Genes 58 A Closer Look Noncoding DNA—Not Junk

After All 59 At a glance Coding and Noncoding DNA 61 Mutation: When Genes Change 61 Chromosomes 63

Karyotyping Chromosomes 66

Cell Division 67 Mitosis 67 Meiosis 68

New Frontiers 71 How Do We Know? 74 Summary of Main Topics 75 Critical Thinking Questions 75 Media Resources 75

Chapter 4

Heredity and Evolution 77 The Genetic Principles Discovered by Mendel 78

Segregation 78 Dominance and Recessiveness 79

Mendelian Inheritance in Humans 83 Misconceptions about Dominance and Recessiveness 83 Patterns of Mendelian Inheritance 85

Non-Mendelian Inheritance 89 Polygenic Inheritance 89

At a glance Mendelian vs. Polygenic Traits 92 Mitochondrial Inheritance 92 Pleiotropy 93

Genetic and Environmental Factors 93 Modern Evolutionary Theory 94

The Modern Synthesis 94 A Current Definition of Evolution 94

Factors That Produce and Redistribute Variation 95 Mutation 95 Gene Flow 96 Genetic Drift and Founder Effect 97

Natural Selection Is Directional and Acts on Variation 100

Review of Genetics and Evolutionary Factors 102 How Do We Know? 104 Summary of Main Topics 105 Critical Thinking Questions 105

Chapter 5

Macroevolution: Processes of Vertebrate and Mammalian Evolution 107 How We Connect: Discovering the Human Place in the

Organic World 108 Principles of Classification 108 Making Connections: Constructing Classifications and

Interpreting Evolutionary Relationships 110 Comparing Evolutionary Systematics with Cladistics 111

A Closer Look Evo-Devo: The Evolution Revolution 112–113

An Example of Cladistic Analysis: The Evolutionary History of Cars and Trucks 114

Using Cladistics to Interpret Real Organisms 114

At a glance Comparing Two Approaches to Interpretation of Evolutionary Relationships 117

Definition of Species 117 Interpreting Species and Other Groups in the Fossil

Record 119 Recognition of Fossil Species 120 Recognition of Fossil Genera 121

What Are Fossils and How Do They Form? 122 Humans Are Vertebrates: Distant Connections 124 A Closer Look Deep Time 126–127 Humans Are Also Mammals: Closer Connections 128 The Emergence of Major Mammalian Groups 130 Processes of Macroevolution 130

Adaptive Radiation 130 Generalized and Specialized Characteristics 131

Working Together: Microevolution and Macroevolution 132

How Do We Know? 133 Summary of Main Topics 133 Critical Thinking Questions 133

contents ix

Primates Chapter 7

Primate Behavior 175 The Evolution of Behavior 176

Some Factors That Influence Social Structure 178

A Closer Look Types of Nonhuman Primate Social Groups 180

Why Be Social? 181 Primate Social Behavior 182

Dominance 182

At a glance Primate Social Strategies 183 Communication 184

Aggressive and Affiliative Behaviors within Groups 186 Aggression 186 Affiliative Behaviors 187

Reproduction and Reproductive Behaviors 188 Reproductive Strategies 189 Sexual Selection 189 Infanticide as a Reproductive Strategy? 190

Mothers, Fathers, and Infants 192 Nonhuman Primate Models for the Evolution of Human

Behavior 194 Brain and Body Size 195

Language 197 The Evolution of Language 200

Primate Cultural Behavior 202

At a glance Evolution of Human Language 203 Conflict between Groups 207 Prosocial Behaviors: Affiliation, Altruism, and

Cooperation 210 Altruism 210

The Primate Continuum 212 How Do We Know? 213 Summary of Main Topics 214 Critical Thinking Questions 215

Chapter 6

Survey of the Living Primates 135 Primate Characteristics 136 Primate Adaptations 139

Evolutionary Factors 139

A Closer Look Primate Cranial Anatomy 140–141 Geographical Distribution and Habitats 141 Diet and Teeth 144 Locomotion 145 Primate Classification 146

A Survey of the Living Primates 148 Lemurs and Lorises 148 Tarsiers 150 Anthropoids: Monkeys, Apes, and Humans 151 Hominoids: Apes and Humans 158

Endangered Primates 166 A Closer Look Aye-Ayes: Victims of Derived

Traits and Superstition 168 The Bushmeat Trade 169

How Do We Know? 172 Summary of Main Topics 172 Critical Thinking Questions 173

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Chapter 8

Overview of the Fossil Primates 217 Background to Primate Evolution: Late Mesozoic 218 Primate Origins 218 A Closer Look Building Family Trees from

Genes 220 Made to Order: Archaic Primates 221 Eocene Euprimates 222

Lemur Connections? The Adapoids 223

At a glance Key Early Primate Names 226

Closer Connections to Living Primates: The Evolution of True Lemurs and Lorises 226

Tarsier Connections? The Omomyoids 228 Evolution of True Tarsiers 229 Eocene and Oligocene Early Anthropoids 229

Oligocene Primates 231

A Closer Look Primate Diversity in the Fayum 232 True Anthropoids 233 Early Platyrrhines: New World Anthropoids 234

A Closer Look Island Hopping and Primate Evolution 236

Miocene Primates 237 Monkeying Around 237

At a glance Key Early Anthropoid Names 239 Aping Monkeys 240 True Apes 244

At a glance Key Fossil Ape Names 244 Evolution of Extant Hominoids 250

How Do We Know? 252 Summary of Main Topics 253 Critical Thinking Questions 253

hominin evolution Chapter 9

Paleoanthropology: Reconstructing Early Hominin Behavior and Ecology 255 Understanding Our Direct Evolutionary Connections:

What’s a Hominin? 256 What’s in a Name? 256

Biocultural Evolution: The Human Capacity for Culture 257

Discovering Human Evolution: The Science of Paleoanthropology 259

A Closer Look What Were Early Hominins Doing, and How Do We Know? 260–261

Connecting the Dots through Time: Paleoanthropological Dating Methods 264

A Closer Look Chronometric Dating Estimates 267 Experimental Archaeology 268

Stone Tool (Lithic) Technology 268 Analysis of Bone 270

Reconstruction of Early Hominin Environments and Behavior 270

Why Did Hominins Become Bipedal? 271

How Do We Know? 275 Summary of Main Topics 275 Critical Thinking Questions 275 Media Resources 275

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Chapter 10

Hominin Origins in Africa 277 Walking the Walk: The Bipedal Adaptation 278

The Mechanics of Walking on Two Legs 278

A Closer Look Major Features of Bipedal Locomotion 280–281

Digging for Connections: Early Hominins from Africa 282

Pre-Australopiths (6.0+ to 4.4 mya) 283 At a glance Key Pre-Australopith Discoveries 288 Australopiths (4.2 to 1.2 mya) 288

Australopithecus afarensis 289

A Closer Look Cranial Capacity 293 A Contemporaneous and Very Different Kind of

Hominin 293 Later More Derived Australopiths (3.0 to 1.2 mya) 294 New Connections: A Transitional Australopith? 297

Closer Connections: Early Homo (2.0 to 1.4 mya) 299 Interpretations: What Does It All Mean? 301 Seeing the Big Picture: Adaptive Patterns of Early

African Hominins 304 How Do We Know? 305 Summary of Main Topics 305 Critical Thinking Questions 305 Media Resources 305

Chapter 11

The First Dispersal of the Genus Homo: Homo erectus and Contemporaries 307 A New Kind of Hominin 310 The Morphology of Homo erectus 310

Body Size 311 Brain Size 311 Cranial Shape 311

The First Homo erectus: Homo erectus from Africa 311 At a glance Key Homo erectus Discoveries from

Africa 315 Who Were the Earliest African Emigrants? 315 Homo erectus from Indonesia 317 A Closer Look In Search of Ancient Human

Ancestors—and a Little Shade 318–319 Homo erectus from China 319

Zhoukoudian Homo erectus 319 Cultural Remains from Zhoukoudian 320 Other Chinese Sites 321

A Closer Look Dragon Bone Hill: Cave Home or Hyena Den? 322–323

Asian and African Homo erectus: A Comparison 323

At a glance Key Homo Erectus Discoveries from Asia 324

Later Homo erectus from Europe 325 At a glance Key Homo erectus and Contemporaneous

Discoveries from Europe 326 Technological Trends During Homo erectus Times 327 Seeing the Connections: Interpretations of Homo

erectus 328 How Do We Know? 329 Summary of Main Topics 329 Critical Thinking Questions 329

Chapter 12

Premodern Humans 331 When, Where, and What 332

The Pleistocene 332 Dispersal of Middle Pleistocene Hominins 333 Middle Pleistocene Hominins: Terminology 333

Premodern Humans of the Middle Pleistocene 334 Africa 334 Europe 335

At a glance Key Premodern Human (H. heidelbergensis) Fossils from Africa 335

At a glance Key Premodern Human (H. heidelbergensis) Fossils from Europe 336

Asia 337

At a glance Key Premodern Human (H. heidelbergensis) Fossils from Asia 337

A Review of Middle Pleistocene Evolution 340 Middle Pleistocene Culture 340 Neandertals: Premodern Humans of the Late

Pleistocene 341 Western Europe 345 Central Europe 346 Western Asia 347 Central Asia 349

At a glance Key Neandertal Fossil Discoveries 350 Culture of Neandertals 350

Technology 350 Subsistence 351 Speech and Symbolic Behavior 351

A Closer Look The Evolution of Language 352–353 Burials 354

Molecular Connections: The Genetic Evidence 354 A Closer Look Are They Human? 356–357 Seeing Close Human Connections: Understanding

Premodern Humans 357 How Do We Know? 360 Summary of Main Topics 361 Critical Thinking Questions 361

contentsxii

Chapter 13

The Origin and Dispersal of Modern Humans 363 Approaches to Understanding Modern Human

Origins 364 The Regional Continuity Model: Multiregional

Evolution 364 Replacement Models 365

The Earliest Discoveries of Modern Humans 368 Africa 368 The Near East 371

At a glance Key Early Modern Homo sapiens Discoveries from Africa and the Near East 373

Asia 373 Australia 375 Central Europe 375 Western Europe 377

Something New and Different: The “Little People” 378 At a glance Key Early Modern Homo sapiens

Discoveries from Europe and Asia 378 Technology and Art in the Upper Paleolithic 380

Europe 380

A Closer Look Maybe You Can Take It with You 384 Africa 384

Summary of Upper Paleolithic Culture 385 How Do We Know? 387 Summary of Main Topics 387 Critical Thinking Questions 387

contemporary human evolution Chapter 14

Modern Human Biology: Patterns of Variation 389 Historical Views of Human Variation 390 The Concept of Race 391 A Closer Look Racial Purity: A False and Dangerous

Ideology 392–393 Contemporary Interpretations of Human Variation 396

Human Polymorphisms 397 Polymorphisms at the DNA Level 398

At a glance Genetic Polymorphisms Used to Study Human Variation 399

A Closer Look What DNA Tells Us about Ancient Human Migrations 400–401

Population Genetics 402 Calculating Allele Frequencies 404

At a glance Population Genetics Research 405 A Closer Look Calculating Allele Frequencies: PTC

Tasting in a Hypothetical Population 406 Evolution in Action: Modern Human Populations 407

Nonrandom Mating 407

Human Biocultural Evolution 408 How Do We Know? 411 Summary of Main Topics 411 Critical Thinking Questions 411 Media Resources 411

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Chapter 15

Modern Human Biology: Patterns of Adaptation 413 The Adaptive Significance of Human Variation 413

Solar Radiation and Skin Color 415 The Thermal Environment 419

A Closer Look Skin Cancer and UV Radiation 422–423

High Altitude 425

Infectious Disease 427 The Continuing Impact of Infectious Disease 430 At a glance Zoonoses and Human Infectious

Disease 431 Human Skeletal Biology: What Bones Can Tell Us about

Ancient Diseases, Trauma, and Lifestyles 433 Evidence of Prehistoric Diseases 433 Reconstruction of Prehistoric Behavioral Patterns 436

How Do We Know? 438 Summary of Main Topics 439 Critical Thinking Questions 439 Media Resources 439

Chapter 16

Legacies of Human Evolutionary History and the Human Life Course 441 Evolved Biology and Contemporary Lifestyles—Is There

a Mismatch? 442 Biocultural Evolution and the Life Course 442 From Embryo to Adult: Human Growth and

Development Today and in the Past 443 Nutritional Effects on Growth, Development, and Later-Life

Health 444

A Closer Look Diabetes 448 At a glance Diet, Lifestyle, and Consequences 449

Other Factors Affecting Growth and Development: Genes, Environment, and Hormones 450

Life History Theory and the Human Life Course 453 Pregnancy, Birth, Infancy, and Childhood 454 Onset of Reproductive Functioning in Humans 458 Mothers and Grandmothers 459 Aging and Longevity 461

Effects of Technology on the Brain 464 Are We Still Evolving? 465 How Do We Know? 466 Summary of Main Topics 467 Critical Thinking Questions 467 Media Resources 467

Chapter 17

The Human Disconnection 469 Human Impacts on the Planet and Other Life-

Forms 470 Humans and the Impact of Culture 470 Global Climate Change 472 Impact on Biodiversity 476 Acceleration of Evolutionary Processes 479

Looking for Solutions 480 Is There Any Good News? 481 How Do We Know? 482 Summary of Main Topics 483 Critical Thinking Questions 483

appendix a Atlas of Primate Skeletal Anatomy 484

appendix B Sexing and Aging the Skeleton 492

Glossary 497 Bibliography 506 Index 532

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A Closer Look Forensic Anthropology in Practice 21

Rosalind Franklin: The Fourth (but Invisible) Member of the Double Helix Team 52

Noncoding DNA—Not Junk After All 59

Evo-Devo: The Evolution Revolution 112–113

Deep Time 126–127

Primate Cranial Anatomy 140

Aye-Ayes: Victims of Derived Traits and Superstition 168

Types of Nonhuman Primate Social Groups 180

Building Family Trees from Genes 220

Primate Diversity in the Fayum 232

Island Hopping and Primate Evolution 236

What Were Early Hominins Doing, and How Do We Know? 260–261

Chronometric Dating Estimates 267

Major Features of Bipedal Locomotion 280–281

Cranial Capacity 293

In Search of Ancient Human Ancestors— and a Little Shade 318–319

Dragon Bone Hill: Cave Home or Hyena Den? 322–323

The Evolution of Language 352

Are They Human? 356–357

Maybe You Can Take It with You 384

Racial Purity: A False and Dangerous Ideology 392–393

What DNA Tells Us about Ancient Human Migrations 400–401

Calculating Allele Frequencies: PTC Tasting in a Hypothetical Population 406

Skin Cancer and UV Radiation 422–423

Diabetes 448

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At a Glance The Mechanism of Natural Selection 45

Coding and Noncoding DNA 61

Mendelian vs. Polygenic Traits 92

Comparing Two Approaches to Interpretation of Evolutionary Relationships 117

Primate Social Strategies 183

Evolution of Human Language 203

Key Early Primate Names 226

Key Early Anthropoid Names 239

Key Fossil Ape Names 244

Key Pre-Australopith Discoveries 288

Key Homo erectus Discoveries from Africa 315

Key Homo Erectus Discoveries from Asia 324

Key Homo erectus and Contemporaneous Discoveries from Europe 326

Key Premodern Human (H. heidelbergensis) Fossils from Africa 335

Key Premodern Human (H. heidelbergensis) Fossils from Europe 336

Key Premodern Human (H. heidelbergensis) Fossils from Asia 337

Key Neandertal Fossil Discoveries 350

Key Early Modern Homo Sapiens Discoveries from Africa and the Near East 373

Key Early Modern Homo Sapiens Discoveries from Europe and Asia 378

Genetic Polymorphisms Used to Study Human Variation 399

Population Genetics Research 405

Zoonoses and Human Infectious Disease 431

Diet, Lifestyle, and Consequences 449

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Preface

This textbook is about where we come from and the sci- entific ways we can explore our beginnings. Our species, like all species on earth, evolved from earlier life-forms. As a result of this long shared ancestry, we and all other life are connected in a variety of ways: genetically, ana- tomically, physiologically, and even behaviorally. These connections are the main focus of the book and are high- lighted in every chapter.

Physical anthropology, also called “biological anthro- pology,” is the study of human adaptation, variability and evolution as well as of our living and fossil relatives from a biological perspective. Consequently, throughout this text, you will encounter topics that emphasize basic bio- logical concepts. This broad biological framework allows us to connect our evolutionary history with that of other life-forms in order to better understand the evolutionary pressures that shaped our species.

In the last few years scientific knowledge in many fields has accumulated amazingly fast. What’s more, the bio- logical sciences are certainly among the most rapidly expanding areas of knowledge as information increases dramatically every year—indeed, every month. This edi- tion has been updated to reflect these changes and to pro- vide the most current information available.

But, in reality, our presentation is just a beginning for students new to this field of study. It is our goal to give students a strong foundation relating to the key aspects of evolutionary biology, which includes physical anthro- pology. Our aim is to provide fundamental informa- tion which will allow you to better understand some of the dramatic scientific advances that almost surely will directly affect you in coming years.

Because genetic mechanisms lie at the heart of under- standing evolution, in the early chapters (2 though 5) we address the basic aspects of life, cells, DNA, and the ways species change. In Chapters 6 and 7, we turn to an explo- ration of our evolutionary cousins, the nonhuman pri- mates, and show how they are closely connected to us genetically, physically and behaviorally. In Chapters 8 through 13, we first discuss the evolutionary history of early primates and how they relate to living nonhuman primates and our own earliest ancestors (Chapter 8). In Chapters 9–13, we turn to a more detailed exploration of

our specific human evolutionary history over the past 6 million years. This evolutionary journey begins with our small-brained, apelike ancestors in Africa and follows the development of their descendants through time and over an expanding geographical range into Asia and Europe, and much later into Australia and the Americas.

In the last section of this book (Chapters 14–17), we cover the most recent part of our evolutionary jour- ney with a discussion of modern human biology, and we trace the ongoing evolution of our species. Major top- ics include the nature of human variation (including an anthropological discussion of the concept of “race”), pat- terns of adaptation in recent human populations, and the developmental changes experienced by humans through the course of their lives. In our new concluding chapter, “The Human Disconnection,” we discuss how contemporary humans are severely altering the planet. We compare these recent and sudden developments with our species’ long evolutionary past, when humans were not so numerous or so dependent on nonrenewable resources.

What’s new in the 2013–2014 edition First, as previously mentioned, we have incorporated the unifying concept of our “connection” to all life as the framework for presenting material throughout the text. To further reinforce this central focus, each chapter now opens with a pedagogical aid that clearly shows students the biological connections as they are organized within and between chapters. Students are also now presented with the learning objectives they are expected to mas- ter after reading the chapter. In addition, at the end of each chapter we have included a new section (How Do We Know?) which briefly summarizes the basic scien- tific information that allows physical anthropologists and other biologists to draw accurate conclusions regarding our evolutionary history.

As genetic technology continues to grow at an unprec- edented pace, it is our task to present the most rele-

Preface xvii

vant new discoveries in as simple a manner as possible. Chapter 3 includes a new discussion of the ENCODE (Encyclopedia of DNA Elements) project that involves more than 400 geneticists from around the world. The goal of the project is to identify the functions of the “non- coding” DNA that comprises about 98 percent of the human genome. This discussion is important because some of this DNA is involved in regulatory functions and changes in regulatory genes are critical to the evolution- ary process. We also increased our discussion of regu- latory DNA and types of regulatory genes to emphasize their role in evolution.

A major change to this edition is the reduction of the number of nonhuman primate chapters from 3 to 2. This change was in response to reviewer comments that there be somewhat less coverage. However, all major topics have been retained, and there is added material on cooperation and empathy in nonhuman primates. We have also added more information emphasizing the endangered status of many nonhuman primates, both in the text, and in a new table (Table 6.1) that lists some of the 25 species consid- ered most endangered by the IUCN (International Union for the Conservation of Nature). The table includes esti- mated numbers and the major threats to these species.

Chapter 8 (formerly Chapter 9) has been trimmed and extensively updated to include new discoveries as well as ongoing reinterpretations of fossil primates. These changes include a reassessment of molecular dating for primate origins and the evolution of all groups, as well as an updated and streamlined treatment of lower pri- mates. This new approach relies less on nomenclature and instead emphasizes key trends in primate adaptation and relation to living groups. Three new “At a Glance” boxes call attention to significant transitional primate groups and act as handy study tools. A complete revision of ape origins is supplemented by a detailed map showing the dispersal patterns of early apes from Africa to Europe and Eurasia and then back into Africa. The chapter, as a whole, includes attractive new art emphasizing important primate traits and differences between groups in an easy- to-understand visual format.

Remarkable new discoveries of fossil hominins and evidence of their behavior are discussed in Chapters 9 through 13. In Chapter 9 we provide further informa- tion that sheds light on the controversial interpretation of what some researchers have claimed are the earliest stone tools (ostensibly used for butchering) as well the latest chemical evidence used to reconstruct early hom- inin diets. Chapter 10 covers the earliest hominins and presents varied interpretations, including further infor-

mation about Ardipithecus as well as a new find of foot remains that suggest many of these early hominins were likely bipedal, but in a very different way from us or even some other contemporary hominin species.

Our coverage of Homo erectus in Chapter 11 covers a new find from Java as well as new and more precise dating of several key sites. Chapter 12 contains a new framework for understanding premodern humans, especially as they occupied wider areas of the Old World with some popu- lations becoming more isolated. In addition, we cover the amazing new DNA results obtained from a finger bone found in Siberia that have allowed researchers to deter- mine not only that the individual was female but also her hair, skin, and eye color. Chapter 13 concludes the sec- tion on fossil hominins with a discussion of the origins of modern humans. Updates include further evidence showing more precisely the evolutionary relationships of Homo floresiensis as well as new archaeological dis- coveries pushing back the dates of cave painting in west- ern Europe and the development of sophisticated tools in southern Africa.

In Chapters 14 through 16, our focus turns to modern human biology. Our understanding of human variation (discussed in Chapter 14) has been completely trans- formed by more complete DNA data, published in just the last five years. We have updated and modified our main perspective in this chapter to reflect the remarkable new findings contributed by molecular biology. New data from contemporary hunter-gatherer populations in Africa tell us about human origins; other very recent research fur- ther clarifies how migrations outside of Africa led to the peopling of Eurasia, Australia, and the New World.

In Chapter 15, there’s a new discussion of recent research demonstrating a population-wide genetic muta- tion in Tibetan highlanders that increases their ability to adapt to living at high altitude. We have also included a major new section on “Human Skeletal Biology: What Bones Can Tell Us about Ancient Diseases and Lifestyles.” The discussion of diseases found in bone is linked to the overall human adaptation theme of the chapter and is heavily illustrated with new photos.

In Chapter 16, now titled “Legacies of Human Evolutionary History: Effects on the Individual,” we focus on ways in which our biology, resulting from millions of years of evolution, seems to be mismatched with the lives we lead today, leading in some cases to compromised health. For example, the biology of women may not be well suited to the highly frequent menstrual cycling that results from the use of modern forms of birth control. Some health disorders that we are dealing with today may

Prefacexviii

stem from the dramatic differences between the diets of our ancestors and the foods we eat today.

Finally, in the new concluding Chapter 17 (“The Human Disconnection”), we focus on another theme that runs through the book—why it is so crucial that we know and understand human evolutionary history, its impact on the world today, and how we have distanced ourselves from other living species with which we share so many connections. We humans and the consequences of our activities are probably the most important influences on evolution today, causing the extinction or near- extinction of thousands of other life-forms and threatening the very planet on which we live. Our disconnection from other species and from our own evolutionary past pose the biggest challenges our species has ever faced. Only by understanding how we got to this point can we begin to respond to the challenges that are in our future and the futures of our children and grandchildren.

We also expanded our treatment of climate change in Chapter 17, including two new figures. The discussion provides current information from the National Snow and Ice Data Center showing that in September 2012, the Arctic sea ice minimum was 49 percent less than the average figure for the years 1979 to 2000. We point out that there has been a steady decline in Arctic sea ice since the year 2000 and we briefly deal with the likely conse- quences of continued melting.

In-chapter Learning Aids Connections graphic at the beginning of each chap- ter shows the biological relationships emphasized in the chapter in the context of topics in other chapters.

Student Learning Objectives are listed on the opening page of each chapter.

A Closer Look boxes are high-interest features found throughout the book. They supplement chapter material and include more in-depth discussion of selected stimu- lating topics.

How Do We Know? chapter concluding sections sum- marize the basic scientific information used in drawing accurate conclusions about our evolutionary history.

Video Media Resources are now listed at the end of half of the chapters. Students are referred to the anthropology CourseMate at www.cengagebrain.com for access.

A running glossary in the margins provides definitions of terms immediately adjacent to the text where the term is first introduced. A full glossary is provided at the back of the book.

At a Glance boxes found throughout the book briefly summarize complex or controversial material in a visually simple fashion.

Figures, including numerous photographs, line drawings, and maps, most in full color, are carefully selected to clar- ify text materials and directly support the discussion in the text.

Critical Thinking Questions at the end of each chapter reinforce key concepts and encourage students to think critically about what they have read.

Full bibliographical citations throughout the book pro- vide sources from which the materials are drawn. This type of documentation guides students to published, peer- reviewed source materials and illustrates for students the proper use of references. All cited sources are listed in the comprehensive bibliography at the back of the book.

xix

xxxx

Over the years, many friends and colleagues have assisted us with our books. For this edition we are espe- cially grateful to the reviewers who so carefully com- mented on the manuscript and made such helpful suggestions: Jerusha Achterberg, Harvard University; Autumn Cahoon, Sierra College; Meredith Dorner, Saddleback College; Samantha Hens, California State University Sacramento; Melissa Remis, Purdue University West Lafayette; Kathleen Rizzo, University of Illinois at Chicago; Patricia Vinyard, University of Akron; and Brita Wynn, Sacramento City College.

We wish to thank the team at Cengage Learning: Aileen Berg, Lin Marshall Gaylord, Liz Rhoden, Michelle Williams, Mallory Ortberg, John Chell, Caryl Gorska, and Cheri Palmer. Moreover, for their unflagging exper- tise and patience, we are grateful to our copy editor, Heidi Thaens, our production coordinator, Gary Hespenheide, and his skilled staff at Hespenheide Design: Patti Zeman, Randy Miyake, and Bridget Neumayr.

To the many friends and colleagues who have gen- erously provided photographs, we are greatly apprecia- tive: Zeresenay Alemsegel, Nanette Barkey, Chris Beard, Günter Bechly, David Begun, Brenda Benefit, Lee Berger, Jonathan Bloch, C. K. Brain, Günter Bräuer, Peter Brown, Ray Carson, Desmond Clark, Ron Clarke, Bill Clemens, Raymond Dart, Henri de Lumley, Louis de Bonis, Didier Descouens, Michael Donnenberg, John Fleagle, Diane France, Robert Franciscus, David Frayer, Kathleen Galvin, Philip Gingerich, Gregg Gunnell, David Haring, Terry Harrison, John Hodgkiss, Almut Hoffman, Pat Holroyd, Ellen Ingmanson, Fred Jacobs, Don Johanson, Peter Jones, Mushtaq Kahn, John Kappelman, Richard Kay, William Kimbel, Charles Knowles, Arlene Kruse, Yutaku Kunimatsu, Julie Lesnik, Linda Levitch, Thomas J. Loebel, David Lordkipanidze, Carles Lalueza-Fox, Giorgio Manzi, Tetsuro Matsuzawa, Monte McCrossin, National Museums of Kenya, Gerald Newlands, Xijum Ni, John Oates, Bonnie Pedersen, David Pilbeam, Gul Reyman, Charlotte Roberts, Duane Rumbaugh, Sastrohamijoyo Sartono, Peter Schmid, Rose Sevick, Elwyn Simons, Meredith Small, Fred Smith, Thierry Smith, Kirstin Sterner, Masanaru Takai, Heather Thew, Nelson Ting, Phillip Tobias, Erik Trinkaus, William Turnbaugh, Alan Walker, Carol Ward, Wally Wecker, Dietrich Wegner,

James Westgate, Randy White, Milford Wolpoff, Xinzhi Wu, and João Zilhão.

Over the years, many students have pledged their time and expertise to help improve Chapter 8. We would especially like to thank K. Lindsay Eaves for her invalu- able help editing and researching this and earlier edi- tions of the manuscript and for facilitating coordination of the text and art within the context of the Ciochon Lab. We also thank Kiran Patel for her unfailing atten- tion to detail, Toby Avalos for his research on fossil apes and Mike Hussey for help with photographs. For the cur- rent and past three editions, John Fleagle has made ana- tomical diagrams available that were originally used in his book, Primate Adaptation and Evolution (Academic Press, 1999). Others who have assisted in forming the concepts that we have put into written form include David Begun, Eric Delson, John Fleagle, Terry Harrison, Pat Holroyd, Gregg Gunnell, Andrew Kitchen, Philip Rightmire, Nelson Ting, Kirstin Sterner, Iyad Zalmout, and Tim White.

Robert Jurmain Lynn Kilgore Wenda Trevathan Russell Ciochon December 2012

Acknowledgments

In memory of Phillip Tobias

Je ffr

ey M

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1925–2012

Supplements

Introduction to Physical Anthropology 2013–2014 comes with an outstanding supplements program to help instructors create an effective learning environment so students can more easily master the latest discoveries and interpretations in the field of physical anthropology.

Supplements for the Instructor Online Instructor’s Manual with Test Bank for Introduction to Physical Anthropology 2013–2014 Edition This online resource includes a sample syllabus showing how to integrate the Anthropology Resource Center with the text, as well as chapter outlines, learning objectives, key terms and concepts, lecture suggestions, and enrich- ment topics, as well as 40–60 test questions per chapter.

PowerLecture™ with Exam View® (Windows/ Macintosh) for Introduction to Physical Anthropology 2013–2014 Edition This easy-to-use, one-stop digital library and presenta- tion tool includes the following book-specific resources as well as direct links to many of Wadsworth’s highly valued electronic resources for anthropology:

▶ Ready-to-use Microsoft® PowerPoint® lecture slides with photos and graphics from the text, make it easy for you to assemble, edit, publish, and present custom lectures for your course.

▶ ExamView® testing software, which provides all the test items from the text’s test bank in electronic format, enabling you to create customized tests of up to 250 items that can be delivered in print or online.

▶ The text’s Instructor’s Resource Manual and Test Bank in electronic format.

Anthropology CourseMate This website for Introduction to Physical Anthropology 2013–2014 Edition brings chapter topics to life with inter- active learning, study, and exam preparation tools includ- ing quizzes and flashcards for each chapter’s key terms

and concepts. The site also provides an eBook version of the text with highlighting and note-taking capabili- ties. For instructors this text’s CourseMate also includes Engagement Tracker, a first-of-its-kind tool that monitors student engagement in the course. Go to login.cengage. com to access these resources.

WebTutor™ for Blackboard® and WebCT™ Jump-start your course with customizable, rich, text- specific content within your Course Management System.

▶ Jump-start—Simply load a WebTutor cartridge into your Course Management System.

▶ Customizable—Easily blend, add, edit, reorganize, or delete content.

▶ Content—Rich, text-specific content, media assets, quizzing, weblinks, discussion topics, interactive games and exercises, and more.

The Wadsworth Anthropology Video Library Vol. 1, 2, and 3 The Wadsworth Anthropology Video Library drives home the relevance of course topics through short, pro- vocative clips of current and historical events. Perfect for enriching lectures and engaging students in discussion, many of the segments on this volume have been gathered from BBC Motion Gallery. Ask your Cengage Learning representative for a list of contents.

Supplements for the Student Anthropology CourseMate This website for Introduction to Physical Anthropology 2013–2014 Edition brings chapter topics to life with inter- active learning, study, and exam preparation tools, includ- ing quizzes, flash cards, videos, animations, and more! The site also provides an eBook version of the text with highlighting and note-taking capabilities. You can access this new learning tool and all other online resources through www.cengagebrain.com.

Supplements xxi

Telecourse Course Student Guide for Introduction to Physical Anthropology, 2013–2014 Edition Entitled “Physical Anthropology: The Evolving Human,” this distance-learning course provides online and print companion study guide options that include quizzing, study aids, interactive exercises, video, and more.

Classic and Contemporary Readings in Physical Anthropology Edited by Mary K. Sandford and Eileen Jackson, this accessible reader presents primary articles with intro- ductions and questions for discussion, helping students to better understand the nature of scientific inquiry. Students will read highly accessible classic and contem- porary articles on key topics, including the science of physical anthropology, evolution and heredity, primates, human evolution, and modern human variation.

Lab Manual and Workbook for Physical Anthropology, Seventh Edition Written by Diane L. France, this edition of the workbook and lab manual includes a new “Introduction to Science and Critical Thinking” that precedes the first. Using hands-on exercises, this richly illustrated full-color lab manual balances the study of genetics, human osteology, anthropometry, and forensic anthropology with the study of primates and human evolution. In addition to provid- ing hands-on lab assignments that apply the field’s per- spectives and techniques to real situations, this edition provides more explanatory information and sample exer- cises throughout the text to help make the concepts of physical anthropology easier to understand. Contact your Cengage sales representative to package with the text.

Physical Anthropology Lab Manual by John Kappelman offers a focused sampling of laboratory exer- cises that range across the breadth of the discipline, from examples of heredity and evolution to primate behavior, the fossil record of apes and early humans, and questions about human biology that are linked to environmental change. Exercises are designed with a succinct focus on particular problems, and the labs follow a fixed format with the introduction of a problem followed by the collec- tion of data that are in turn used to test and evaluate the hypothesis. Students who complete the labs will greatly expand their knowledge of physical anthropology.

Basic Genetics in Anthropology CD-ROM: Principles and Applications, Version 2.0 by Jurmain/Kilgore/ Trevathan This student CD-ROM expands on basic biological con- cepts covered in the book, focusing on biological inher- itance (such as genes and DNA sequencing) and its applications to modern human populations. Interactive animations and simulations bring these important con- cepts to life so that students can fully understand the essential biological principles underlying human evolu- tion. Also available are quizzes and interactive flash cards for further study.

Hominid Fossils CD-ROM: An Interactive Atlas by James Ahern This CD-based interactive atlas includes over 75 key fos- sils that are important for a clear understanding of human evolution. The QuickTime® Virtual Reality (QTVR) “object” movie format for each fossil will enable students to have a near-authentic experience working with these important finds by allowing them to rotate the fossil 360°. Unlike some VR media, QTVR objects are made using actual photographs of the real objects and thus better preserve details of color and texture. The fossils used are high-quality research casts and real fossils.

The organization of the atlas is nonlinear, with three levels and multiple paths, enabling students to start with a particular fossil and work their way “up” to see how the fossil fits into the map of human evolution in terms of geography, time, and evolution. The CD-ROM offers stu- dents an inviting, authentic learning environment, one that also contains a dynamic quizzing feature that will allow students to test their knowledge of fossil and species identification as well as provide more detailed informa- tion about the fossil record.

hormones Substances (usually pro- teins) that are produced by specialized cells and that travel to other parts of the body, where they influence chemical reactions and regulate various cellular functions.

amino acids Small molecules that are the components of proteins.

Connections

Physical anthropology is a biological science that investigates

how humans have evolved and continue to do so.

Evolutionary theory, par- ticularly natural selection,

explains how life forms have changed over time

and how new species are produced.

Connections

Cr is

tin a

G. M

itt er

m ei

savanna (also spelled savannah) A large flat grassland with scattered trees and shrubs. Savannas are found in many regions of the world with dry and warm-to- hot climates.

hominins Colloquial term for members of the evolutionary group that includes modern humans and now-extinct bipedal relatives.

species A group of organisms that can interbreed to produce fertile offspring. Members of one species are reproductively isolated from members of all other species (i.e., they cannot mate with them to pro- duce fertile offspring).

bipedally On two feet; walking habitu- ally on two legs.

After mastering the material in this chapter, you should be able to:

▶ �Describe the discipline of anthropology as it is practiced in the United States, its subfields, and the general anthropological perspective on how humans are biologically and behaviorally connected to other species.

▶ �Provide a brief description of the major subfields of physical or biological anthropology.

▶ �Understand the fundamentals of the scientific method and the importance of hypothesis testing.

▶ �Explain why scientific theories are not simply guesses or hunches, as the term (theory) is often incorrectly used and interpreted.

▶ �Appreciate how understanding the nature of scientific research can lead to the development of critical thinking skills, which, in turn, are an extremely important outcome of a college education.

Introduction

One day, perhaps during the rainy season some 3.7 million years ago, two or three animals walked across a grassland savanna in what is now northern Tanzania, in East Africa. These individuals were early hominins, members of the same evo- lutionary lineage that includes our own species, Homo sapiens. Fortunately for us, a record of their passage on that long-forgotten day remains in the form of fossilized footprints, preserved in hardened volcanic deposits. As chance would have it, shortly after heels and toes were pressed into the damp soil, a nearby volcano erupted. The ensu- ing ash fall blanketed everything on the ground. In time, the ash layer hardened into a deposit that remarkably pre- served the tracks of numerous animals, including those early hominins, for nearly 4 million years (Fig. 1-1).

These now famous prints indicate that two individuals, one smaller than the other, perhaps walking side by side, left parallel sets of tracks. But because the larger individual’s prints are obscured, possibly by those of a third, it’s unclear how many actually made that journey so long ago. What is clear is that the prints were made by an ani- mal that habitually walked bipedally (on two feet), and that fact tells us that those ancient travelers were hominins.

In addition to the footprints, scien- tists working at this site (called Laetoli) and at other locations have discovered many fossilized parts of skeletons of an animal we call Australopithecus afar

1Introduction to Physical Anthropology

ensis. Because the remains have been extensively studied, we know that these hominins were anatomically similar to ourselves, although their brains were only about one-third the size of ours. They may have used stones and sticks as simple tools, but there is no evidence that they actually made stone tools. In fact, they were very much at the mercy of nature’s whims. They certainly could not outrun most predators, and their canine teeth were fairly small, so compared to many other animals, they were pretty much defenseless.

We’ve asked hundreds of questions about the Laetoli hominins, but we will never be able to answer them all. They walked down a path into what became their future, and their journey ended so long ago that we cannot really grasp how much time has passed since that

Student Learning Objectives

ChApter 1 Introduction to Physical Anthropology 4

day. But it remains for us to learn as much as we can about them, and as we continue to do this, their greater jour- ney continues.

On July 20, 1969, a television audi- ence numbering in the hundreds of millions watched as two human beings stepped out of a spacecraft onto the surface of the moon. People born after that date have always lived in an age of space exploration, and many may now take that first moon landing more or less for granted. But the significance of that first moonwalk can’t be overstated, because it represents humankind’s pre- sumed mastery over the natural forces that govern our presence on earth. For the first time ever, people actually walked upon the surface of a celestial body that, as far as we know, has never given birth to biological life.

As the astronauts gathered geologi- cal specimens and frolicked in near weightlessness, they left traces of their fleeting presence in the form of foot- prints in the lunar dust (Fig. 1-2). On the surface of the moon, where no rain falls and no wind blows, the footprints remain undisturbed to this day. They survive as silent testimony to a brief visit by a medium-sized, big- brained creature that pre- sumed to challenge the very forces that cre- ated it.

You may wonder why anyone would care about early hominin footprints and how they can possibly be relevant to your life. You may also wonder why a physical anthropology textbook would begin by discussing two such seemingly unrelated events as ancient hominins walking across an African savanna and a moonwalk. But the fact is, these two events are very closely connected.

Physical, or biological, anthropology (both terms are used) is a scientific discipline concerned with the biologi- cal and behavioral characteristics of human beings; our closest relatives, the nonhuman primates (apes, mon- keys, tarsiers, lemurs, and lorises); and our ancestors. This kind of research helps us explain what it means to be human and how we came to be the way we are. This is an ambitious goal and it probably isn’t fully attain- able, but it’s certainly worth pursuing. We’re the only species to ponder our own existence and question how we fit into the spectrum of life on earth. Most people view

▶�Figure 1-1 Early hominin footprints at Laetoli, Tanzania. The tracks to the left were made by one individual, while those to the right appear to have been made by two individuals, the second stepping in the tracks of the first.

anthropology the field of inquiry that studies human culture and evolutionary aspects of human biology; includes cultural anthropology, archaeology, linguistics, and physical, or biological, anthropology.

primates Members of the mammalian order primates (pronounced “pry-may´- tees”), which includes lemurs, lorises, tarsiers, monkeys, apes, and humans. Pe

te r J

on es

The Human Connection 5

evolution A change in the genetic structure of a population. the term is also frequently used to refer to the appearance of a new species.

adaptation An anatomical, physi- ological, or behavioral response of organ- isms or populations to the environment. Adaptations result from evolutionary change (specifically as a result of natural selection).

genetic having to do with the study of gene structure and action and the pat- terns of inheritance of traits from parent to offspring. Genetic mechanisms are the foundation of evolutionary change.

behavior Anything organisms do that involves action in response to internal or external stimuli; the response of an indi- vidual, group, or species to its environment. Such responses may or may not be deliber- ate, and they aren’t necessarily the result of conscious decision making (which is absent in single-celled organisms, insects, and many other species).

humanity as quite separate from the rest of the animal kingdom. But at the same time, many are curious about the similarities we share with other species. Maybe, as a child, you looked at your dog and tried to figure out how her front legs might correspond to your arms. Or perhaps during a visit to the zoo, you recognized the simi- larities between a chimpanzee’s hands or facial expressions and your own. Maybe you wondered if he also shared your thoughts and feelings. If you’ve ever had thoughts and questions like these, then you’ve indeed been curious about humankind’s place in nature.

How did Homo sapiens, a result of the same evolutionary forces that pro- duced all other forms of life on this planet, gain the power to control the flow of rivers and even alter the cli- mate on a global scale? As tropical ani- mals, how were we able to leave the tropics and eventually occupy most of the earth’s land surfaces? How did we adjust to different environmental con- ditions as we dispersed? How could our species, which numbered fewer than 1 billion until the mid-nineteenth cen- tury, come to number more than 7 bil- lion worldwide today and, as we now do, add another billion people approxi- mately every 11 years?

These are some of the many ques- tions that physical anthropologists try to answer through the study of human evolution, variation, and adaptation. These issues, and many others, are cov- ered in this textbook, because physical anthropology is, in large part, human biology seen from an evolutionary per- spective. On hearing the term evolu tion, most people think of the appear- ance of new species. Certainly new species are one important consequence of evolution, but not the only one. Evolution is an ongoing biological process with more than one outcome. Simply stated, evolution is a change in the genetic makeup of a population from one generation to the next, and it can be defined and studied at two lev- els. Over time, some genetic changes in populations do result in the appear-

ance of a new species (or spe ciation), especially when those populations are isolated from one another. Change at this level is called macroevolution. At the other level, there are genetic altera- tions within populations; and though this type of change may not lead to speciation, it does cause popu- lations of a species to differ from one another in the frequency of certain traits. Evolution at this level is referred to as microevolution. Evolution at both these levels will be discussed in this book.

The Human Connection

The unifying theme of this textbook is how human beings are linked to all other life on earth. We can see how we are connected to other organisms in countless ways, as you will learn throughout this book. For example, our DNA is structurally identical to that of every living thing. Indeed, we share genes that are involved in the most fun- damental life processes with even the simplest of animals, such as sponges. These genes have changed very little over the course of several hundred mil- lion years of evolution. With few excep- tions, our cells have the same struc- ture and work the same way as in all life forms. Anatomically, we have the same muscles and bones as other ani- mals. What’s more, many aspects of our behavior have direct connections to nonhuman species, especially other primates.

The countless connections we share with other organisms show that

NA SA

▲�Figure 1-2 Human footprints left on the lunar surface during the Apollo mission.

ChApter 1 Introduction to Physical Anthropology 6

amino acids Small molecules that are the components of proteins.

humans are a product of the same evo- lutionary forces that produced all liv- ing things. But, clearly we aren’t iden- tical to any other species. In fact, all species are unique in some ways. We humans are one contemporary compo- nent of a vast biological continuum at a particular point in time; and in this regard, we aren’t really all that special. Stating that humans are part of a con- tinuum doesn’t imply that we’re at the peak of development on that contin- uum. Depending on the criteria used, humans can be seen to exist at one end of the spectrum or the other, or some- where in between, but we don’t occupy a position of inherent superiority over other species (Fig. 1-3).

However, human beings are unques- tionably unique regarding one highly significant characteristic, and that is intellect. After all, humans are the only species, born of earth, to stir the lunar dust. We’re the only species to develop language and complex culture as a means of buffering nature’s chal- lenges, and by doing so we have gained the power to shape the planet’s very destiny.

Biocultural Evolution

Biological anthropologists don’t just study physiological and biological systems. When these topics are con- sidered within the broader context of human evolution, another factor must be considered, and that is culture. Cul- ture is an extremely important con- cept, not only as it relates to modern humans but also because of its critical role in human evolution. Quite sim- ply, and in a very broad sense, culture can be defined as the strategy by which humans adapt to the natural environ- ment. In fact, culture has so altered and dominated our world that it’s become the environment in which we live. Culture includes technologies ranging from stone tools to computers; subsis- tence patterns, from hunting and gath- ering to global agribusiness; housing types, from thatched huts to skyscrap-

ers; and clothing, from animal skins to high-tech synthetic fibers (Fig. 1-4). Technology, religion, values, social organization, language, kinship, mar- riage rules, gender roles, dietary prac- tices, inheritance of property, and so on are all aspects of culture. Each cul- ture shapes people’s perceptions of the external environment, or worldview, in particular ways that distinguish a particular society from all others.

One important point to remember is that culture isn’t genetically passed from one generation to the next. We aren’t born with innate knowledge that leads us to behave in ways appropriate to our own culture. Culture is learned, and the process of learning one’s cul- ture begins, quite literally, at birth. All people are products of the culture they’re raised in, and since most human behavior is learned, it follows that most human behaviors, perceptions, values, and reactions are shaped by culture.

It’s important to emphasize that even though culture isn’t genetically determined, the human predisposi- tion to assimilate culture and func- tion within it is very much influenced by biological factors. Most nonhuman animals rely to varying degrees on learned behavior. This is especially true of the great apes (gorillas, chimpan- zees, bonobos, and orangutans), which exhibit several aspects of culture.

The predisposition for culture is perhaps the most critical component of human evolutionary history, and it was inherited from our early hominin or even prehominin ancestors. In fact, the common ancestor we share with chimpanzees may have had this pre- disposition. But during the course of human evolution, the role of culture became increasingly important. Over time, as you will see, culture influ- enced many aspects of our biologi- cal makeup; in turn, aspects of biol- ogy influenced cultural practices. For this reason, humans are the result of long-term interactions between biology and culture. We call these interactions biocultural evolution; and in this respect, humans are unique.

continuum A set of relationships in which all components fall along a single integrated spectrum (for example, color). All life reflects a single biological continuum.

culture Behavioral aspects of human adaptation, including technology, tradi- tions, language, religion, marriage patterns, and social roles. Culture is a set of learned behaviors transmitted from one generation to the next by nonbiological (i.e., nongenetic) means.

worldview General cultural orientation or perspective shared by the members of a society.

biocultural evolution the mutual interactive evolution of human biology and culture; the concept that biology (anatomy, neurological attributes, etc.) makes culture possible and that developing culture further influences the direction of biological evolu- tion; this is a basic concept in understanding the unique components of human evolution.

Biocultural Evolution 7

amino acids Small molecules that are the components of proteins.

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▶�Figure 1-3 Traditional and recent technologies. (a) An early stone tool from East Africa. This artifact repre- sents one of the oldest types of stone tools found anywhere. (b) The Hubble Space telescope, a late twentieth- century tool, orbits the earth every 96 minutes at an altitude of 360 miles. Because it is above the earth’s atmo- sphere, it provides distortion-free images of objects in deep space. (c) A cuneiform tablet. Cuneiform, the earliest form of writing, involved pressing symbols into clay tablets. It originated in southern Iraq some 5,000 years ago. (d) Text messaging, a fairly recent innovation in satellite communi- cation, has generated a new language of sorts. Today, more than 500 million text messages are sent every day worldwide. (e) A Samburu woman in East Africa building a traditional but complicated dwelling of stems, small branches, and mud. (f) These Hong Kong skyscrapers are typical of cities in industrialized countries today.

amino acids Small molecules that are the components of proteins.

C H A P T E R 1

C H A P T E R 2Physical anthropology is a biological science that investigates how humans have evolved and continue to do so.

Human development and adaptation is best

understood from an evolutionary perspective.

Modern human variation is best under- stood by examining similarities and dif-

ferences in DNA among populations.

Humans have recently become disconnected from

other life and are rapidly altering the planet.

Modern humans first evolved in Africa and later spread to other

areas of the world, where they occa- sionally interbred with Neandertals

and other pre-modern humans.

Through natural selection, humans have and continue to adapt to environmental factors including solar radiation, cold, altitude, and, most importantly,

infectious disease.

Evolutionary theory, particularly natural selection, explains how life forms have

changed over time and how new species are produced.

Figure 1-4 Humans are biologically connected to all forms of life. This central theme will be addressed in every chapter of this textbook as shown in this figure.

C H A P T E R 1 3

C H A P T E R 1 5

C H A P T E R 1 4

C H A P T E R 1 6

C H A P T E R 1 7

The immedi- ate predeces- sors of modern humans, including the Neandertals, were much like us, but had some anatomical and behavioral differences.

C H A P T E R 1 2

Connections

amino acids Small molecules that are the components of proteins.

The DNA molecule is the basis of all life.

Evolution occurs when DNA changes and genetic variation is further influenced by natural

selection and other factors.

Fossil evidence indicates our primate origins date to at

least 65 million years ago.

The first more human-like ani- mals (hominins) appeared in Africa around 6 mya ago

and evolved into a variety of different

species.

Partly because of common evolutionary history, many human

behaviors are also seen in other primates.

Paleoanthropology, which includes physical anthro- pology, archaeology, and geology, provides the scien-

tific basis to understand hominin evolution.

C H A P T E R 3 C H A P T E R 4

C H A P T E R 7

C H A P T E R 9

Humans are both ver- tebrates and mammals, and their evolutionary history over many mil- lions of years explains our early roots.

C H A P T E R 5

Humans are primates and share many bio-

logical characteristics with other primates.

Hominins began to disperse out of Africa around 2 million years ago, and during the next 1 million years

inhabited much of Eurasia.

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ChApter 1 Introduction to Physical Anthropology 10

applied anthropology the practi- cal application of anthropological and archaeological theories and techniques. For example, many biological anthropolo- gists work in the public health sector.

Biocultural interactions have result- ed in many anatomical, biological, and behavioral changes during the course of human evolution. Alterations in the shape of the pelvis, increased brain size, reorganization of neurological struc- tures, smaller teeth, and the devel- opment of language are some of the results of the evolutionary process in our lineage. Today biocultural inter- actions are as important as ever, espe- cially with regard to health and disease. Air pollution and exposure to dan- gerous chemicals have increased the prevalence of respiratory disease and cancer. While air travel makes it pos- sible for people to travel thousands of miles in just a few hours, we aren’t the only species that can do this. Millions of disease-causing organisms travel on airplanes with their human hosts, mak- ing it possible for infectious diseases to spread within hours across the globe.

Many human activities have changed the patterns of such infec- tious diseases as tuberculosis, influ- enza, and malaria. After the domes- tication of nonhuman animals, close contact with chickens, pigs, and cat- tle greatly increased human expo- sure to some of the diseases these ani- mals carry. Through this contact we’ve also changed the genetic makeup of disease-causing microorganisms. For example, the H1N1 “swine flu” virus that caused the 2009 pandemic actu- ally contains genetic material derived from bacteria that infect three differ- ent species: humans, birds, and pigs. As it turned out, that pandemic wasn’t as serious as had originally been feared, but the next one could be. Because we have overused antibiotics, we’ve made many bacteria resistant to treatment and many are even deadly. Likewise, although we’re making progress in treating malaria, the microorganism that causes it has developed resistance to some treatments and preventive medications. We’ve also increased the geographical distribution of malaria- carrying mosquitoes through agri- cultural practices and global climate

change. But while it’s clear that we humans have influenced the develop- ment and spread of infectious disease, we still don’t know the many ways that changes in infectious disease pat- terns are affecting human biology and behavior. Anthropological research in this one area alone is extremely rel- evant to all of us, and there are many other critical topics that biological anthropologists explore.

What Is Anthropology?

Many anthropology students con-template this question when their parents or friends ask, “What are you studying?” The answer is often fol- lowed by a blank stare or a comment about dinosaurs. So, what is anthropol- ogy, and how is it different from several related disciplines?

Like physical anthropologists, biologists investigate human adap- tation and evolution. Similarly, his- torians and sociologists also study aspects of human societies past and present. But when biological or social research also considers the interactions between evolutionary and cultural fac- tors, it’s included in the discipline of anthropology.

In the United States, anthropology is divided into four main subfields: cul- tural, or social, anthropology; archaeol- ogy; linguistic anthropology; and physi- cal, or biological, anthropology. Each of these, in turn, is divided into several specialized areas of interest. This four- field approach concerns all aspects of humanity across space and time. Each subdiscipline emphasizes different aspects of the human experience, but together they offer a means of explain- ing variation in human biological and behavioral adaptations. In addition, each of these subfields has practical applications, and many anthropologists pursue careers outside the university environment. This kind of anthropolo- gy is called applied anthropology, and it’s extremely important today.

Linguistic Anthropology 11

ethnographies Detailed descrip- tive studies of human societies. In cultural anthropology, an ethnography is tradition- ally the study of a non-Western society.

artifacts Objects or materials made or modified for use by hominins. The earliest artifacts are usually tools made of stone or occasionally bone.

Cultural Anthropology

Cultural, or social, anthropology is the study of patterns of belief and behavior found in modern and histori- cal cultures. The origins of cultural anthropology can be traced to the nine- teenth century, when travel and explo- ration brought Europeans into contact (and sometimes conflict) with vari- ous cultures in Africa, Asia, and the New World.

This contact sparked an interest in “traditional” societies and led many early anthropologists to study and record lifestyles that are now mostly extinct. These studies produced many descriptive ethnographies that cov- ered a range of topics such as reli- gion, ritual, myth, the use of symbols, diet, technology, gender roles, and child-rearing practices. Ethnographic accounts, in turn, formed the basis for comparative studies of numerous cul- tures. By examining the similarities and differences among cultures, cul- tural anthropologists have been able to formulate many hypotheses regard- ing fundamental aspects of human behavior.

The focus of cultural anthropol- ogy shifted over the course of the twentieth century. Cultural anthro- pologists still work in remote areas, but increasingly they’ve turned their gaze toward their own cul- tures and the people around them. Increasingly, ethnographic tech- niques have been applied to the study of diverse subcultures and their interactions with one another in con- temporary metropolitan areas (urban anthropology). The population of any city is composed of many subgroups defined by economic status, religion, ethnic background, profession, age, level of education, and so on. Even the student body of your own col- lege or university is made up of many subcultures, and as you walk across campus, you see students of many nationalities and diverse religious and ethnic backgrounds.

Archaeology

Archaeology is the study of ear-lier cultures by anthropologists who specialize in the scientific recov- ery, analysis, and interpretation of the material remains of past societ- ies. Archaeologists obtain informa- tion from artifacts and structures left behind by earlier cultures. The remains of earlier societies, in the form of tools, structures, art, eating implements, frag- ments of writing, and so on, provide a great deal of information about many important aspects of a society, such as religion and social structure.

Unlike in the past, sites aren’t exca- vated simply for the artifacts or “trea- sures” they may contain. Rather, they’re excavated to gain information about human behavior. For example, patterns of behavior are reflected in the disper- sal of human settlements across a land- scape and in the distribution of cultural remains within them. Archaeological research may focus on specific localities or peoples and attempt to identify, for example, various aspects of social orga- nization, subsistence techniques, or fac- tors that led to the collapse of a civiliza- tion. Alternatively, inquiry may reflect an interest in broader issues relating to human culture in general, such as the development of agriculture or the rise of cities.

Linguistic Anthropology

Linguistic anthropology is the study of human speech and language, including the origins of language in general as well as specific languages. By examining similarities between contemporary languages, linguists have been able to trace historical ties between particular languages and groups of languages, thus facilitating the identification of language families and perhaps past relationships between human populations.

chapter 1 Introduction to Physical Anthropology 12

paleoanthropology the interdis- ciplinary approach to the study of earlier hominins—their chronology, physical structure, archaeological remains, habitats, and so on.

primate paleontology the study of fossil primates, especially those that lived before the appearance of hominins.

Because the spontaneous acquisi- tion and use of language is a uniquely human characteristic, it’s an important topic for linguistic anthropologists, who, along with specialists in other fields, study the process of language acquisition in infants. Because insights into the process may well have implica- tions for the development of language in human evolution as well as in grow- ing children, it’s also an important sub- ject in physical anthropology.

Physical Anthropology

As we’ve already said, physical anthropology is the study of human biology within the framework of evolution with an emphasis on the interaction between biology and cul- ture. This subdiscipline is also referred to as biological anthropology, and you’ll find the terms used interchangeably. Physical anthropology is the original term, and it reflects the initial inter- ests anthropologists had in describing human physical variation. The Ameri- can Association of Physical Anthro- pologists, its journal, many college courses, and numerous publications retain this term. The designation bio- logical anthropology reflects the shift in emphasis to more biologically ori- ented topics, such as genetics, evolu- tionary biology, nutrition, physiological adaptation, and growth and devel- opment. This shift occurred large- ly because of advances in the field of genetics and molecular biology since the late 1950s. Although we’ve contin- ued to use the traditional term in the title of this textbook, you’ll find that all of the major topics we discuss pertain to biological issues.

The origins of biological anthro- pology can be traced to two principal areas of interest among nineteenth- century European and American scholars: the ancestry of modern spe- cies, including humans; and human variation. Although most of these scholars held religious convictions,

they were beginning to doubt the literal interpretation of the biblical account of creation and to support explanations that emphasized natu- ral processes rather than supernatural phenomena. Eventually, the sparks of interest in biological change over time were fanned into flames by the publica- tion of Charles Darwin’s On the Origin of Species in 1859.

Today, paleoanthropology, the study of anatomical and behavioral human evolution as revealed in the fos- sil record, is a major subfield of physical anthropology (Fig. 1-5). Thousands of fossilized remains of early pri- mates, including human ancestors, are now kept in research collections. Taken together, these fossils span at least 7 million years of human prehis- tory. Although most of these fossils are incomplete, they provide us with a significant wealth of knowledge that increases each year. It’s the ultimate goal of paleoanthropological research to identify the various early human and humanlike species, establish a chron- ological sequence of relationships among them, and gain insights into their adaptation and behavior. Only then will we have a clear picture of how and when modern humans came into being.

To some extent, primate paleontol- ogy can be viewed as a subset of paleo- anthropology. Primate paleontology is the study of the primate fossil record, which extends back to the beginning of primate evolution some 65 million years ago (mya). Virtually every year, fossil-bearing geological beds around the world yield important new discov- eries. By studying fossil primates and comparing them with anatomically similar living species, primate paleon- tologists are learning a great deal about factors such as diet or locomotion in earlier forms. They can also try to iden- tify aspects of behavior in some extinct primates and attempt to clarify what we know about evolutionary relation- ships between extinct and modern spe- cies, including ourselves.

Physical Anthropology 13

Visible physical variation was the other major area of interest for early physical anthropologists. Enormous effort was spent in measuring, describ- ing, and explaining visible differ- ences among various human popula- tions, with particular attention being focused on skin color, body propor- tions, and the shape of the head and face. Although some approaches were misguided and even racist, they gave birth to many body measurements that are sometimes still used. They’ve been used to design everything from wheel- chairs to office furniture. They have also been used to determine the abso- lute minimum amount of leg room a person needs in order to remain sane during a 3-hour flight on a com- mercial airliner. Lastly, they are also

very important to the study of skele- tal remains from archaeological sites (Fig. 1-6).

Today, physical anthropologists are concerned with human variation because of its possible adaptive signifi cance and because they want to identify the factors that have produced not only visible physical variation but genetic variation as well. In other words, many traits that typify certain populations evolved as biological adaptations, or adjustments, to local environmental conditions such as sunlight, altitude, or infectious disease. Other characteris- tics may be the result of geographical isolation or the descent of populations from small founding groups.

Since the early 1990s, the focus of human variation studies has shifted

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▲�Figure 1-5 (a) Paleoanthropologist Meave Leakey and crew exca- vate an early hominin skull at Lake Turkana in northern Kenya. (b) Primate paleon tologist Russell L. Ciochon (left) and Le Trang Kha (right), a verte- brate paleontologist, examine the fossil remains of Gigantopithecus from a 450,000-year-old site in Vietnam. Gigantopithecus is the name given to the largest apes that have ever lived. In the background is a reconstruction of this enormous animal.

chapter 1 Introduction to Physical Anthropology 14

ulations and individuals of any species helps to explain biological change over time, which is precisely what the evolu- tionary process is all about.

Modern population studies also examine other important aspects of human variation, including how dif- ferent groups respond physiologically to different kinds of environmentally induced stress (Fig. 1-7). Such stresses may include high altitude, cold, or heat. Nutritional anthropologists study the relationships between various dietary components, cultural practices, phys- iology, and certain aspects of health and disease (Fig. 1-8). Investigations of human fertility, growth, and devel- opment are also closely related to the topic of nutrition. These fields of inquiry, which are fundamental to studies of adaptation in modern human populations, can also provide insights into hominin evolution.

It would be impossible to study evolutionary processes without some knowledge of how traits are inherited. For this reason and others, genetics is a crucial field for physical anthro- pologists. Modern physical anthro- pology wouldn’t exist as an evolution- ary science if it weren’t for advances in the understanding of genetic mechanisms.

Molecular anthropologists use cutting-edge technologies to inves- tigate evolutionary relationships between human populations as well as between humans and nonhuman primates. To do this, they examine similarities and differences in DNA sequences between individuals, pop- ulations, and species. What’s more, by extracting DNA from certain fos- sils, these researchers have contribut- ed to our understanding of evolution- ary relationships between extinct and living species. As genetic technologies continue to be developed, molecular anthropologists will play a key role in explaining human evolution, adapta- tion, and our biological relationships with other species (Fig. 1-9).

completely away from the visible dif- ferences we see in people to the under- lying genetic factors that influence these and many other traits. This shift occurred partly because the examina- tion of genetic variation between pop-

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◀ Figure 1-6 An anthropol- ogy student using spread- ing calipers to measure the length of a human cranium.

▶ Figure 1-7 This researcher is using a treadmill test to assess a subject’s heart rate, blood pressure, and oxy- gen consumption.

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Physical Anthropology 15

osteology the study of skeletal material. human osteology focuses on the interpretation of skeletal remains from archaeological sites, skeletal anatomy, bone physiology, and growth and devel- opment. Some of the same techniques are used in paleoanthropology to study early hominins.

However, before genetic and molec- ular techniques became widespread, osteology, the study of the skeleton, was the only way that anthropolo- gists could study our immediate ances- tors. In fact, a thorough knowledge of skeletal structure and function is still critical to the interpretation of fossil

material today. For this reason, oste- ology has long been viewed as central to physical anthropology. In fact, it’s so important that when many people think of biological anthropology, the first thing that comes to mind is bones!

Bone biology and physiology are of major importance to many other

◀�Figure 1-8 Dr. Kathleen Galvin measures the upper arm circum- ference of a young Maasai boy in Tanzania. Data derived from various body measurements, including height and weight, were used in a health and nutrition study of groups of Maasai cattle herders.

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◀�Figure 1-9 Molecular anthro- pologist Nelson Ting collecting red colobus fecal samples for a study of genetic variation in small groups of monkeys isolated from one another by agricultural clearing.

ChApter 1 Introduction to Physical Anthropology 16

bioarchaeology the study of skel- etal remains from archaeological sites.

paleopathology the branch of osteology that studies the evidence of disease and injury in human skeletal (or, occasionally, mummified) remains from archaeological sites.

forensic anthropology An applied anthropological approach dealing with legal matters. Forensic anthropolo- gists work with coroners and others in iden- tifying and analyzing human remains.

aspects of physical anthropology besides human evolution. Many oste- ologists specialize in the measure- ment of skeletal elements, essential for identifying stature and growth pat- terns in archaeological populations. In the last 30 years or so, the study of human skeletal remains from archaeo- logical sites has sometimes been called bioarchaeology.

Paleopathology, the study of disease and trauma in ancient skele- tal populations, is a major component of bioarchaeology. Paleopathologists investigate the prevalence of trauma, certain infectious diseases (such as syphilis and tuberculosis), nutrition- al deficiencies, and numerous other conditions that may leave evidence in bone (Fig. 1-10). This research can tell us a great deal about the lives of indi- viduals and populations in the past. Paleopathology also yields informa- tion regarding the history of certain disease processes, and for this reason it’s of interest to scientists in biomedi- cal fields.

Forensic anthropology is directly related to osteology and paleopatholo- gy and has become popular among the public because of forensic TV shows like Bones (based on a character cre- ated by a practicing forensic anthropol- ogist) and Crime Scene Investigation. Technically, this approach is the appli- cation of anthropological (usually osteological and sometimes archae- ological) techniques to legal issues. Forensic anthropologists help iden- tify skeletal remains in mass disasters or other situations in which a human body has been found. They’ve been involved in numerous cases having important legal, historical, and human consequences (Fig. 1-11). They were instrumental in identifying the skel- etons of most of the Russian imperi- al family, executed in 1918, and many participated in the overwhelming task of trying to identify the remains of vic- tims of the September 11, 2001, terror- ist attacks in the United States.

Anatomy is yet another important area of interest for physical anthropol-

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▶�Figure 1-10 Two examples of pathological conditions in human skel- etal remains from the Nubian site of Kulubnarti in Sudan. These remains are approximately 1,000 years old. (a) A partially healed fracture of a child’s left femur (thigh bone). This child died around the age of 6, prob- ably of an infection that resulted from this injury. (b) Very severe congenital scoliosis in an adult male. The curves are due to developmental defects in individual vertebrae. (This is not the most common form of scoliosis.)

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Physical Anthropology 17

ogists. In living organisms, bones and teeth are intimately linked to the soft tissues that surround and act on them. Consequently a thorough knowledge of soft tissue anatomy is essential to understanding the biomechanical rela- tionships involved in movement. Such relationships are important in assessing the structure and function of limbs and other components of fossilized remains. For these reasons and others, many physical anthropologists specialize

in anatomical studies. In fact, several physical anthropologists are professors in anatomy departments at universities and medical schools (Fig. 1-12).

Given our evolutionary focus and the fact that we ourselves are primates, it’s natural that primatology, the study of the living nonhuman primates, has become increasingly important since the late 1950s (Fig. 1-13). Today, doz- ens of nonhuman primate species have been and are being studied. Because

◀�Figure 1-11 (a) Forensic anthro- pologists Vuzumusi Madasco (from Zimbabwe) and Patricia Bernardi (from Argentina) excavating the skel- etal remains and clothing of one of many victims of a civil war massacre in El Salvador. The goal is to identify as many of the victims as possible. (b) These forensic anthropologists, working in a lab near Baghdad, are examining the skeletal remains of Kurdish victims of genocide. They cataloged the injuries of 114 individu- als buried in a mass grave, and some of their evidence was used against Saddam Hussein during his trial in 2006.

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primatology the study of the biol- ogy and behavior of nonhuman primates (lemurs, lorises, tarsiers, monkeys, and apes).

ChApter 1 Introduction to Physical Anthropology 18

science A body of knowledge gained through observation and experimenta- tion; from the Latin scientia, meaning “knowledge.”

hypotheses (sing., hypothesis) A provisional explanation of a phenomenon. hypotheses require verification or falsifica- tion through testing.

empirical relying on experiment or observation; from the Latin empiricus, meaning “experienced.”

scientific method An approach to research whereby a problem is identified, a hypothesis (provisional explanation) is stated, and that hypothesis is tested by collecting and analyzing data.

data (sing., datum) Facts from which conclusions can be drawn; scientific information.

nonhuman primates are our closest living relatives, identifying the under- lying factors related to their social behavior, communication, infant care, reproductive behavior, and so on helps us develop a better understanding of the natural forces that have shaped so many aspects of modern human behavior. Nonhuman primates are also important to study in their own right. This is particularly true today because the majority of primate spe- cies are threatened or seriously endan- gered. For this reason many primatolo- gists have become actively involved in primate conservation. Only through study will scientists be able to rec- ommend policies that can better ensure the survival of many nonhu- man primates as well as thousands of other species.

Applied Anthropology

Applied anthropology is the practical use of anthropological theories and methods outside the academic setting,

but applied and academic anthropology aren’t mutually exclusive approaches. In fact, applied anthropology relies on the research and theories of academic anthropologists and at the same time has much to contribute to theory and techniques.

Within biological anthropolo- gy, forensic anthropology is a good example of the applied approach. But the practical application of the techniques of physical anthropol- ogy isn’t new. During World War II, for example, physical anthropolo- gists were extensively involved in designing gun turrets and airplane cockpits. Since then, many physical anthropologists have pursued careers in genetic and biomedical research, public health, evolutionary medi- cine, medical anthropology, and the conservation of nonhuman primates, and many hold positions in muse- ums and zoos. In fact, a background in physical anthropology is excellent preparation for almost any career in the medical and biological fields (Fig. 1-14).

▶�Figure 1-12 Dr. Linda Levitch teaching a human anatomy class at the University of North Carolina School of Medicine.

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Physical Anthropology and the Scientific Method 19

Physical Anthropology and the Scientific Method

Science is a method of explain-ing natural phenomena. It involves observation, developing hypotheses to explain what has been observed, and developing a research design or series of experiments to test these hypoth- eses. This is an empirical approach to gaining information. Because biological anthropologists are engaged in scien- tific research, they adhere to the princi- ples of the scientific method by iden- tifying a research problem and then gathering information to solve it.

Once a question or problem has been identified, the first step is usually to explore the existing literature (books and journals) to determine what other people have done to resolve the issue. Based on this preliminary research and

other observa- tions, one or even sever- al tentative explana- tions (hypotheses) are then proposed. The next step is to develop a research design or methodology to test the hypothesis. These methods involve col- lecting information, or data, that can

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▲�Figure 1-13 (a) Primatologist Emmanuelle Grundmann using ropes and a harness to observe an orang- utan in Borneo. (b) Primatologist Jill Pruetz follows a chimpanzee in Senegal, West Africa.

ChApter 1 Introduction to Physical Anthropology 20

then be studied and analyzed. Data can be analyzed in many ways, most of them involving various statistical tests. During the data collection and analy- sis phase, it’s important for scientists to use a strictly controlled approach so that they can precisely describe their techniques and results. This precision is critical because it enables others to repeat the experiments and allows sci- entists to make comparisons between their study and the work of others.

For example, when scientists collect data on tooth size in hominin fossils, they must specify which teeth are mea- sured, how they’re measured, and the results of the measurements (expressed numerically, or quantitatively). Then, by analyzing the data, the investiga- tors try to draw conclusions about the meaning and significance of their mea- surements. This body of information then becomes the basis of future stud- ies, perhaps by other researchers, who can compare their own results with those already obtained.

Hypothesis testing is the very core of the scientific method, and although it may seem contradictory at first, it’s based on the potential to falsify the hypothesis. Falsification doesn’t mean that the entire hypothesis is untrue, but it does indicate that the hypothesis may need to be refined and subjected to fur- ther testing.

Eventually, if a hypothesis stands up to repeated testing, it may become part of a theory or perhaps a theory itself. There’s a popular misconception that a theory is nothing more than con- jecture, or a “hunch.” But in science, theories are proposed explanations of relationships between natural phenom- ena. Theories usually concern broad- er, more universal views than hypoth- eses, which have a narrower focus and deal with more specific relationships between phenomena. But like hypoth- eses, theories aren’t facts. They are test ed explanations of facts. For example, it’s a fact that when you drop an object, it falls to the ground. The explanation for this fact is the theory of gravity. But, like hypotheses, theories can be altered

over time with further experimenta- tion and by using newly developed technologies in testing. The theory of gravity has been tested many times and qualified by experiments showing how the mass of objects affects how they’re attracted to one another. So far, the theory has held up.

Scientific testing of hypoth- eses may take several years (or lon- ger) and may involve researchers who didn’t participate in the original work. What’s more, new methods may per- mit different kinds of testing that weren’t previously possible; this is a strength, not a weakness, of scien- tific research. For example, since the 1970s, primatologists have reported that male nonhuman primates (as well as males of many other species) some- times kill infants. One hypothesis has been that infanticidal males only killed the offspring of other males and not their own. But many scientists have objected to this hypothesis and have proposed several alternatives. For one thing, there was no way to know for certain that the males weren’t kill- ing their own offspring; if they were, this would argue against the hypoth- esis. However, in a fairly recent study, scientists collected DNA samples from dead infants and the males who killed them. The evidence showed that most of the time, the males were not related to their victims. This result doesn’t prove that the original hypoth- esis is accurate but it does strengthen it. This study is described in more detail in Chapter 7, but we mention it here to emphasize that science is an ongoing process that builds on pre- vious work and benefits from newly developed techniques (in this case, DNA testing) in ways that constantly expand our knowledge.

Throughout this book we pre- sent several examples of how differ- ent approaches to research and new technologies (especially in the field of genetics) have helped support or alter numerous hypotheses. Scientific research is frequently ridiculed and/or dismissed by the general public, politi-

▲�Figure 1-14 Nanette Barkey, a medical anthropologist involved in a repatriation project in Angola, photographed this little girl being vaccinated at a refugee transit camp. Vaccinations were being administered to Angolan refugees returning home in 2004 from the Democratic Republic of Congo, where they had fled to escape warfare in their own country.

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quantitatively pertaining to mea- surements of quantity and including such properties as size, number, and capac- ity. When data are quantified, they’re expressed numerically and can be tested statistically.

theory A broad statement of scientific relationships or underlying principles that has been substantially verified through the testing of hypotheses.

scientific testing the precise repetition of an experiment or expansion of observed data to provide verification; the procedure by which hypotheses and theo- ries are verified, modified, or discarded.

Physical Anthropology and the Scientific Method 21

cians, and some members of the press. (Particularly good current examples of this relate to climate change research and evolution.) These anti-science positions have been quite successful because the majority of people don’t understand the nature or goals of sci- entific research.

There’s one more extremely impor- tant fact about hypotheses and the- ories: Any proposition that is stated as absolute or does not allow the pos- sibility of falsification is not a scien-

tific hypothesis and should never be considered as such. For a statement to be considered a scientific hypoth- esis, there must be a way to evalu- ate its validity. A statement such as “Heaven exists” may be true, but there is no rational, empirical means (based on experience or experiment) of test- ing it. Therefore acceptance of such a view is based on faith rather than sci- entific verification. The purpose of sci- entific research is not to establish abso- lute truths; rather, it is to generate ever

Forensic Anthropology in Practice

Forensic anthropology is the application of the principles of physical anthropol- ogy and archaeology to the legal system, especially as they relate to the study of the human skeleton. Forensic anthropolo- gists are often called on to assist local law enforcement with crime scene recovery and analysis of human remains. Because of their specialized knowledge and training in physical anthropology, archaeology, and forensic science, they are ideally suited to assist with cases involving badly decomposed or skeletonized remains. Although many forensic anthropolo- gists are employed by universities, there is a growing number who work in museums, state and federal law enforcement agencies, human rights organizations, and for mass disaster agencies (Fig. 1).

The first step in a potential forensic investigation is to determine if the remains are human or nonhuman. If they are human it is then necessary to ascertain if they are of recent origin. A skeletal analysis initially begins with establishing a biological profile of the person whose remains are under investigation. This involves the estima-

tion of the person’s sex, age at death, ancestry, and living height (stature). These characteristics aid in narrowing down the pool of missing persons to consider for comparison. A positive identification of an unknown individual can be made through comparisons of antemortem (con- ditions that affected the skeleton during life) records, such as medical and dental x-rays, with unique biological characteris- tics observed on the skeleton. These may include genetic anomalies, such as unusual or atypical skeletal or dental features, or

pathological conditions, such as bone infec- tions or healed fractures. Multiple points of similarity between antemortem and post- mortem records (i.e., information collected on the deceased individual) can then help to establish identity. Finally, an analysis involves a comprehensive assessment of skeletal trauma, usually classified as blunt- force, sharp-force, or projectile trauma. Forensic anthropologists carefully document trauma that occurred at or around the time of death (perimortem trauma) to provide investigators with information regarding the circumstances of death. They also study postmortem alterations, such as damage to bone caused by exposure to the sun or by scavenging animals. It is critical to be able to differentiate this damage from trauma caused by interpersonal violence.

Ultimately, forensic anthropologists provide services that may help to resolve a case and provide closure to families. They are sometimes called into court as expert witnesses to testify regarding the identity of an individual and to describe traumatic inju- ries identified on skeletal remains that may pertain to the cause and manner of death. It is strongly recommended that people who wish to practice forensic anthropology receive a doctorate in physical anthropol- ogy and undergo certification through the American Board of Forensic Anthropology (see: www.theabfa.org). Currently there are over 70 active board certified forensic anthropologists in North America.

A Closer Look

▲ Figure 1 Heather Thew, who was trained as an anthropologist, is shown working at the Armed Forces DNA Laboratory where remains of missing soldiers are identified.

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ChApter 1 Introduction to Physical Anthropology 22

quadrupedal Using all four limbs to support the body during locomotion; the basic mammalian (and primate) form of locomotion.

ethnocentric Viewing other cultures from the inherently biased perspective of one’s own culture. ethnocentrism often causes other cultures to be seen as inferior to one’s own.

relativistic Viewing entities as they relate to something else. Cultural relativism is the view that cultures have merits within their own historical and environmental contexts.

more accurate and consistent expla nations of phenomena in our universe based on observation and testing. At its very heart, scientific methodology is an exercise in rational thought and critical thinking.

The development of critical think- ing skills is an extremely important benefit of a college education. Such skills enable people to evaluate, com- pare, analyze, critique, and synthe- size information so that they won’t accept everything they hear at face value. Critical thinking skills are per- haps most needed when it comes to advertising and politics. People spend billions of dollars every year on “nat- ural” dietary supplements based on marketing claims that may not have even been tested. So when a salesper- son tells you that, for example, echi- nacea helps prevent colds, you should ask if that statement has been scientifi- cally tested, how it was tested, when, by whom, and where the results were published. Similarly, when politicians make claims in 30-second sound bites, check those claims before you accept them as truth. Be skeptical, and if you do check the validity of advertising and political statements, you’ll find that frequently they’re either misleading or just plain wrong.

The Anthropological Perspective

Perhaps the most important benefit you’ll receive from this textbook and this course is a wider appreciation of the human experience. To under- stand human beings and how our spe- cies came to be, we must broaden our viewpoint through both time and space. All branches of anthropology funda- mentally seek to do this in what we call the anthropological perspective.

Physical anthropologists, for exam- ple, are interested in how humans both differ from and are similar to other animals, especially nonhuman pri-

mates. For example, we’ve defined hominins as bipedal primates, but what are the major anatomical components of bipedal locomotion and how do they differ from, say, those in a quadrupe- dal ape? To answer these questions, biological anthropologists have studied the anatomical structures involved in human locomotion (muscles, hips, legs, and feet) and compared them with the same structures in various nonhuman primates.

Through a perspective that is broad in space and time, we can begin to grasp the diversity of the human expe- rience within the context of biological and behavioral connections with other species. In this way, we may better understand the limits and potentials of humankind. And by extending our knowledge to include cultures other than our own, we may hope to avoid the ethnocentric pitfalls inherent in a more limited view of humanity.

This relativistic view of culture is perhaps more important now than ever before because, in our interde- pendent global community, it allows us to understand other people’s con- cerns and to view our own culture from a broader perspective. Likewise, by examining our species as part of a wide spectrum of life, we realize that we can’t judge other species using only human criteria. Each species is unique, with needs and a behavioral repertoire not exactly like that of any other. By recognizing that we share many sim- ilarities (both biological and behav- ioral) with other animals, perhaps we may come to recognize that they have a place in nature just as surely as we our- selves do.

We hope that after reading the following pages, you will have an increased understanding not only of the similarities we share with other biological organisms but also of the processes that have shaped the traits that make us unique. We live in what may well be the most crucial time for our planet in the past 65 million years. We are members of the one species

23Critical Thinking Questions

that, through the very agency of cul- ture, has wrought such devastating changes in ecological systems that we must now alter our technologies or face potentially unspeakable consequences. In such a time, it’s vital that we attempt

to gain the best possible understand- ing of what it means to be human. We believe that the study of physical anthropology is one endeavor that aids in this attempt, and that is indeed the goal of this textbook.

Summary of Main Topics

▶▶ The major subfields of anthro- pology are cultural anthro- pology, linguistic anthropol- ogy, archaeology, and physical anthropology.

▶▶ Physical anthropology is a dis- cipline that seeks to explain how and when human beings evolved. This requires a detailed examination of the primate and particularly the hominin fossil record (primate paleontology). Another major topic of physical anthropol- ogy is human biological varia- tion, its genetic basis, and its adaptive significance. In addi- tion, physical anthropologists

study the behavior and biology of nonhuman primates, partly as a method of understanding humans but also because non- human primates are important in their own right.

▶▶ Because physical anthropol- ogy is a scientific approach to the investigation of all aspects of human evolution, variation, and adaptation, research in this field is based on the sci- entific method. The scientific method is a system of inquiry that involves the development of hypotheses to explain phe- nomena. To determine the validity of hypotheses, scien-

tists develop research designs aimed at collecting informa- tion (data) and testing the data to see if they support the hypothesis. If the hypothesis is not supported by the data, it may be rejected or modified and retested. If it is supported, it may also be modified or refined over time and further tested. Further tests frequently use new technologies that have been developed since the origi- nal hypothesis was proposed. If a hypothesis stands up to continued testing, it may even- tually be accepted as a theory or part of a theory.

1. Given that you’ve only just been introduced to the field of physical anthropology, why do you think subjects such as anatomy, genetics, nonhuman primate behavior, and human evolution are inte- grated into a discussion of what it means to be human?

2. Is it important to you, personally, to know about human evolution? Why or why not?

3. Do you see a connection between hominin foot- prints that are almost 4 million years old and human footprints left on the moon in 1969? If so, do you think this relationship is important? What does the fact that there are human footprints on the moon say about human adaptation? (Consider both biological and cultural adaptation.)

Critical Thinking Questions

Connections

Evolutionary theory, particularly natural selection, explains

how life forms have changed over time.

DNA molecule is the basis of all life.

Connections

Physical anthropology

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After mastering the material in this chapter, you should be able to:

▶ �Trace the major developments in scientific thinking that led to the discovery of evolutionary processes.

▶ �Compare Darwin’s and Wallace’s theory of natural selection to earlier explanations of how species came to exist.

▶ �Understand how natural selection operates on biological variation in species to cause evolutionary change over time.

▶ �Define the term fitness as it relates to reproductive success.

▶ �Explain how science and religion differ in their explanations of natural phenomena.

▶ �Discuss the history of opposition to the teaching of evolution in the United States.

Has anyone ever asked you, “If humans evolved from mon-keys, why do we still have mon- keys?” Or maybe, “If evolution happens, why don’t we ever see new species?” These are the kinds of questions people sometimes ask if they don’t understand evolutionary processes or don’t believe that evolution occurs. Evolution is one of the most fundamental of all biologi- cal processes and one of the most mis- understood. The explanation for this misunderstanding is simple: Evolution is not taught in most primary and sec- ondary schools. In fact, it’s frequently avoided. Even in colleges and universi- ties, it receives the most detailed treat- ment in biological anthropology. If you’re not an anthropology or biology major and you’re taking a class in bio- logical anthropology mainly to fulfill a science requirement, you’ll probably never study evolution again.

By the end of this course, you’ll know the answers to the questions in the preceding paragraph. Briefly, no one who understands evolution would ever say that humans evolved from monkeys, because we didn’t. We didn’t evolve from chimpanzees either. The earliest human ancestors evolved from a species that lived some 6 to 8 million years ago (mya). That ancestral species was the last common ancestor we share with chimpanzees. In turn, the lineage that eventually gave rise to apes and humans separated from a monkey-like ancestor some 20 mya, and monkeys are still around because as early pri- mate lineages diverged from one anoth-

2The Development of Evolutionary Theory

er, each went its separate way. Over millions of years, some of these groups became extinct while others evolved into the species we know today. Thus all living species are the current results of processes that go back millions of years. The evolution of new species takes time, a lot of time, which is why we don’t witness the appearance of new species except microorganisms. But we do see microevolutionary changes in many species, including humans.

The subject of evolution is contro- versial, especially in the United States, because some religious views hold that evolutionary statements run counter to biblical teachings. In fact, as you’re probably aware, there is strong opposi- tion in the United States to the teach- ing of evolution in public schools. Opponents of teaching evolution often say, “It’s just a theory,” meaning that

Student Learning Objectives

Dorine Essumang

chapter 2 The Development of Evolutionary Theory26

evolution is just an idea or hunch. As we pointed out in Chapter 1, scientific theories aren’t just ideas, although that’s how the word theory is com- monly used in everyday conversation. But when dealing with scientific issues, referring to a concept as “theory” sup- ports it. Theories have been tested and subjected to verification through accumulated evidence, and they have not been disproved, sometimes after decades of experimentation. It is abso- lutely true that evolution is a theory, one supported by a mounting body of genetic evidence that grows daily. It’s a theory that explains how biological change occurs in species over time, and it has stood the test of time. Today, evolutionary theory stands as the most fundamental unifying force in biologi- cal science, and evolutionary biolo- gists can explain many evolutionary processes in ways that were impossible even 10 years ago.

Because physical anthropology is concerned with all aspects of how humans came to be and how we adapt physiologically to the external environ- ment, the details of the evolutionary process are crucial to the field. Given the central importance of evolution to biological anthropology, it’s help- ful to know how the mechanics of the process came to be discovered. Also, if we want to understand and make criti- cal assessments of the controversy that surrounds the issue today, we need to explore the social and political events that influenced the discovery of evolu- tionary principles.

A Brief History of Evolutionary Thought

The discovery of evolutionary prin-ciples first took place in west- ern Europe and was made possible by advances in scientific thinking that date back to the sixteenth century. Having said this, we must recognize that West- ern science borrowed many of its ideas from other cultures, especially the

Arabs, Indians, and Chinese. In fact, intellectuals in these cultures and in ancient Greece had developed notions of biological evolution centuries before Charles Darwin did (Teresi, 2002), but they never formulated them into a cohesive theory.

Charles Darwin was the first per- son to explain the basic mechanics of the evolutionary process. But while he was developing his theory of natural selection, a Scottish naturalist named Alfred Russel Wallace independently reached the same conclusion. That nat- ural selection, the single most impor- tant force of evolutionary change, was proposed at more or less the same time by two British men in the mid- nineteenth century may seem like a strange coincidence. But actually if Darwin and Wallace hadn’t made their simultaneous discoveries, someone else soon would have, and that someone would probably have been British or French. That’s because the groundwork had already been laid in Britain and France, and many scientists there were prepared to accept explanations of bio- logical change that would have been unacceptable even 25 years before.

In science as in other human endeavors, knowledge is usually gained through a series of small steps rather than giant leaps. And just as techno- logical change is based on past achieve- ments, scientific knowledge builds on previously developed theories. Therefore, it’s informative to exam- ine the development of ideas that led Darwin and Wallace to independently arrive at the theory of evolution by nat- ural selection.

Throughout the Middle Ages, one predominant feature of the European worldview was that all aspects of nature, including all forms of life and their relationships to one another, never changed. This view was partly shaped by a feudal society that was itself a rigid class system that had barely changed for centuries. But the most important influence was an extremely powerful religious system in which the teachings of Christianity

natural selection the most critical mechanism of evolutionary change, first described by charles Darwin; the term refers to genetic change or changes in the frequencies of certain traits in populations due to differential reproductive success between individuals.

Dorine Essumang

A Brief History of Evolutionary Thought 27

were held to be the only “truth.” Consequently it was generally accepted that all life on earth had been created by God exactly as it existed in the pres- ent and the belief that life-forms could not and did not change, came to be known as fixity of species. Anyone who questioned the assumptions of fix- ity, especially in the fifteenth and six- teenth centuries, could be accused of challenging God’s perfection, which was heresy. Generally it was a good idea to avoid being accused of heresy, because this was a crime that could be punished by a particularly unpleasant and often fiery death (Fig. 2-1).

The plan of the entire universe was viewed as God’s design. In what is called the “argument from design,” anatomical structures were held to have been engineered to meet their intended purpose. Limbs, internal organs, and eyes all fit the functions they performed; and they, along with the rest of nature, were part of the Grand Designer’s deliberate plan. Also, the Grand Designer was thought to have completed his works as recently as 4004 b.c. The prevailing belief in the

earth’s brief existence, together with fixity of species, was a virtually insur- mountable obstacle to the development of evolutionary theory. The idea of immense geological time, which today we take for granted, simply didn’t exist. In fact, until the concepts of fixity and time were fundamentally altered, it was impossible to conceive of evolution by means of natural selection.

The Scientific Revolution So what transformed this centuries- old belief in a rigid, static universe into a view of worlds in continuous motion? How did the earth’s brief his- tory become an immense expanse of incomprehensible time? How did the scientific method as we know it today develop? These are important ques- tions, but we could also ask why it took so long for Europe to break away from traditional beliefs. After all, scholars in India and the Arab world had devel- oped concepts of planetary motion, for example, centuries earlier.

The development of evolution- ary theory came about as a result of a

◀ Figure 2-1 Portion of a Renaissance painting that depicts the execution of Father Girolamo Savonarola in 1498 in Florence, Italy, (artist unknown). Savonarola wasn’t promoting scientific arguments, but he did run afoul of church leaders. His execution by burning was a common punishment for those, including many scientists and philosophers, who promoted scientific explanations of natural phenomena.

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fixity of species the notion that species, once created, can never change is diametrically opposed to theories of biological evolution.

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chapter 2 The Development of Evolutionary Theory28

series of discoveries that led to major paradigm shifts. For example, the discovery of the New World and cir- cumnavigation of the globe in the fifteenth century overturned some very basic European ideas about the planet. Among other things, the earth could no longer be thought of as flat. Also, as Europeans began to explore the New World, encountering plants and animals they’d never seen before, their awareness of biological diversity expanded.

There were other attacks on tradi- tional beliefs. In 1514, a Polish math- ematician named Copernicus chal- lenged a notion proposed more than 1,500 years earlier, in the fourth- century b.c., by the Greek philosopher Aristotle. Aristotle had taught that the sun and planets existed in a series of concentric spheres that revolved around the earth (Fig. 2-2), a system that was, in turn, surrounded by the stars. Thus it came to be accepted that the earth was the center of the solar system. In fact, scholars in India had figured out that the earth orbited the sun long before Copernicus did; but

Copernicus is generally credited with removing the earth as the center of all things.

Copernicus’ theory was discussed in intellectual circles, but it didn’t attract much attention from the Catholic Church. (Catholicism was the only form of Christianity until the 1520s.) Nevertheless, the theory did contradict a major premise of church doctrine, which at that time wholeheartedly embraced the teachings of Aristotle. By the 1300s, the church had accepted these teachings as dogma because they reinforced the notion that the earth, and the humans on it, were the cen- tral focus of God’s creation and must therefore have a central position in the solar system.

However, in the early 1600s, an Italian mathematician named Galileo Galilei restated Copernicus’ views, using logic and mathematics to support his claim. To his misfortune, Galileo was eventually confronted by the highest-ranking officials of the Catholic Church (including the pope, his one- time friend), who sentenced him to house arrest for the last nine years of

▶�Figure 2-2 This beautifully illus- trated seventeenth-century map shows the earth at the center of the solar system. Around it are seven con- centric circles depicting the orbits of the moon, the sun, and the five planets that were known at the time. (Note also the signs of the zodiac.)

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paradigm shift a transition from one conceptual framework or prevailing and widely accepted viewpoint to another. the acceptance of the discovery that the sun is the center of our solar system is an example of a paradigm shift.

A Brief History of Evolutionary Thought 29

his life. Nevertheless, in intellectual cir- cles there had been a paradigm shift. The solar system had changed; the sun was now at its center, and the earth and other planets revolved around it as the entire system journeyed through space.

Throughout the sixteenth and sev- enteenth centuries, European scientists developed other methods and theories that revolutionized scientific thought. The seventeenth century, in particu- lar, saw the discovery of the principles of physics (such as motion and gravity) and the invention of numerous scien- tific instruments, including the micro- scope. These advances made it possible to investigate many previously misun- derstood natural phenomena. But even with these advances, the idea that liv- ing forms could change over time sim- ply didn’t occur to people.

Precursors of the Theory of Evolution Before early naturalists could begin to understand the many forms of organic life, they had to list and describe them. And as research progressed, scholars were increasingly impressed with the amount of biological diversity they saw.

The concept of species, as we think of them today, wasn’t proposed until the seventeenth century, when John Ray, a minister educated at the University of Cambridge, developed it. He recognized that groups of plants and animals could be differentiated from other groups by their ability to mate with one another and produce fertile offspring. He placed such groups of reproductively isolated organisms into categories, which he called spe- cies (sing., species). Thus, by the late 1600s, the biological criterion of repro- duction was used to define species, much as it is today (Young, 1992). Ray also recognized that species frequently share similarities with other species, and he grouped these together in a sec- ond level of classification he called the genus (pl., genera). He was the first to use the labels genus and species in this

way, and these terms are still in use today.

Carolus Linnaeus (1707–1778) was a Swedish naturalist who developed a method of classifying plants and ani- mals. In his famous work Systema Naturae (The System of Nature), first published in 1735, he standardized Ray’s use of genus and species terminol- ogy and established the system of bino- mial nomenclature. He also added two more categories: class and order. Linnaeus’ four-level system became the basis for taxonomy, the system of clas- sification we still use today.

Linnaeus also included humans in his classification of animals, placing them in the genus Homo and species sapiens. (Genus and species names are always italicized.) Including humans in this scheme was controversial because it defied the idea that humans should be considered unique and separate from the rest of the animal kingdom. Unfortunately for other species, most people still have this view, in spite of all the research that has demonstrated biological and behavioral continuity among all animals including ourselves.

For all his progressive tendencies, Linnaeus still believed in fixity of spe- cies, although in later years, faced with mounting evidence to the contrary, he came to question it. Indeed, fixity was being challenged on many fronts, especially in France, where voices were being raised in favor of a uni- verse based on change and, more to the point, in favor of a biological relation- ship between similar species based on descent from a common ancestor.

Georges-Louis Leclerc de Buffon (1707–1788), a French natural- ist, recognized the dynamic relation- ship between the external environ- ment and living forms. In his Natural History, first published in 1749, he rec- ognized that different regions have unique plants and animals. He also stressed that animals had come from a “center of origin,” but he never dis- cussed the diversification of life over time. Even so, Buffon recog- nized that alterations of the external

reproductively isolated pertaining to groups of organisms that, mainly because of genetic differences, are prevented from mating and producing off- spring with members of other such groups. For example, dogs cannot mate and pro- duce offspring with cats.

binomial nomenclature (bino- mial, meaning “two names”) In taxonomy, the convention established by carolus Linnaeus whereby genus and species names are used to refer to living things. For example, Homo sapiens refers to human beings.

taxonomy the branch of science concerned with the rules of classifying organisms on the basis of evolutionary relationships.

Dorine Essumang

chapter 2 The Development of Evolutionary Theory30

environment, including the climate, were agents of change in species.

Today, Erasmus Darwin (1731–1802) is best known as Charles Darwin’s grandfather. But he was also a physi- cian, poet, and leading member of an important intellectual community in England. In fact, Darwin counted among his friends some of the most important figures of the industrial rev- olution—a time of rapid technological and social change. In his most famous poem, Darwin expressed the view that life had originated in the seas and that all species had descended from a com- mon ancestor. Thus he introduced many of the ideas that his grandson would propose 56 years later. These concepts include vast expanses of time for life to evolve, competition for resources, and the importance of the environment in evolutionary processes. From letters and other sources, we know that Charles Darwin read his grandfather’s writings, but we don’t know how much they influenced him.

Neither Buffon nor Erasmus Darwin attempted to explain the evolutionary process, but a French naturalist named Jean-Baptiste Lamarck (1744–1829) did. Lamarck (Fig. 2-3) suggested a dynamic relationship between spe- cies and the environment such that if the external environment changed, an animal’s activity patterns would also change to accommodate the new cir- cumstances. This would result in the increased or decreased use of certain body parts; consequently those body parts would be modified. According to Lamarck, the parts that weren’t used would disappear over time. However, the parts that continued to be used, perhaps in different ways, would change. Such physical changes would occur in response to bodily “needs,” so that if a particular part of the body felt a certain need, “fluids and forces” would be directed to that point, and the structure would be modified. Because the alteration would make the animal better suited to its habitat, the new trait would be passed on to off- spring. This theory is known as the

inheritance of acquired characteristics, or the use-disuse theory.

One of the most frequently given hypothetical examples of Lamarck’s theory is the giraffe, which, hav- ing stripped all the leaves from the lower branches of a tree (environmen- tal change), tries to reach the leaves on upper branches. As “vital forces” move to tissues of the neck, it becomes slightly longer and the giraffe can reach higher. The longer neck is then trans- mitted to offspring, with the eventual result that all giraffes have longer necks than their predecessors had (Fig. 2-4). So, according to this theory, a trait acquired by an animal during its life- time can be passed on to offspring. Today we know that this explana- tion is wrong because only those traits that are influenced by genetic infor- mation contained within sex cells (eggs and sperm) can be inherited (see Chapter 3).

Because Lamarck’s explanation of species change isn’t genetically correct, he is frequently scorned even today. But in fact Lamarck deserves a great deal of credit because he emphasized the importance of interactions between organisms and the external environ- ment in the evolutionary process. He also coined the term biology to refer to the study of living organisms, and a central feature of this new discipline was the idea of species change.

Lamarck’s most vehement oppo- nent was a French vertebrate paleon- tologist named Georges Cuvier (1769– 1832). Cuvier introduced the concept of extinction to explain the disappear- ance of animals represented by fos- sils. Cuvier was a brilliant anatomist, but he never grasped the dynamic con- cept of nature and continued to insist on the fixity of species. So, rather than assuming that similarities between fos- sil forms and living species indicate evolutionary relationships, Cuvier pro- posed a variation of a doctrine known as catastrophism.

Catastrophism was the belief that the earth’s geological features are the results of sudden, worldwide cataclys-

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▲�Figure 2-3 Portrait of Jean- Baptiste Lamarck. Lamarck believed that species change was influenced by environmental change. He is best known for his theory of the inheritance of acquired characteristics. Oil on canvas, Thevenin, Charles (1764–1838) / Private Collection / The Bridgeman Art Library International.

catastrophism the view that the earth’s geological landscape is the result of violent cataclysmic events. cuvier pro- moted this view, especially in opposition to Lamarck.

Dorine Essumang

A Brief History of Evolutionary Thought 31

mic events. Cuvier’s version of cata- strophism suggested that a series of regional disasters had destroyed most or all of the local plant and animal life in many places. These areas were then restocked with new, similar forms that migrated in from unaffected regions. In order to be consistent with emerging fossil evidence, which indicated that organisms had become more complex over time, Cuvier proposed that after each disaster, the incoming migrants were more similar to living species because they had been produced by more recent creation events. In this way, Cuvier’s explanation of increased complexity over time avoided any notion of evolution, but it still managed to account for the evidence of change so well preserved in the fossil record.

In 1798, an English economist named Thomas Malthus (1766–1834) wrote An Essay on the Principle of Population. This important essay inspired both Charles Darwin and Alfred Russel Wallace in their sepa- rate discoveries of natural selection. It’s interesting that, although Malthus had an enormous influence on these two men, he wasn’t interested in species change at all. Instead, he was arguing for limits to human population growth. He pointed out that in nature, there is a tendency for animal populations to increase in size, but the amount of resources (food and water) remains relatively the same. Therefore popula- tion size is held in check by resource availability. Even though humans can reduce constraints on population

Original group exhibiting variation in neck length

Natural selection favors longer necks

The favored characteristic is passed on to next generation in greater proportion than the shorter neck

Keeps stretching neck to reach leaves higher up on tree

Long-necked descendant after many generations

After many, many generations, group is still variable, but shows a general increase in neck length

Original, short-necked ancestor

And continues stretching until neck becomes progressively longer

(a) Lamarck’s view

The Darwin-Wallace view

▲�Figure 2-4 Contrasting ideas about the mechanism of evolution. (a) Lamarck’s theory held that acquired characteristics can be passed to offspring. Short-necked giraffes stretched to reach higher into trees for food; therefore their necks grew longer. According to Lamarck, this acquired trait was then passed on to offspring, who were born with longer necks. (b) The Darwin-Wallace theory of natural selection states that there is variation in neck length among giraffes. If having a longer neck provides an advantage for feeding, the trait will be passed on to a greater number of offspring, leading to an overall increase in the length of giraffe necks over many generations.

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chapter 2 The Development of Evolutionary Theory32

size by producing more food, Malthus argued that the lack of sufficient food and water would always be a constant source of “misery” and famine for human- kind if our numbers contin- ued to increase. Unfortunately we are now testing Malthus’ hypothesis, as the number of humans on earth reached 7 bil- lion in 2011!

Both Darwin and Wallace extended Malthus’ principles to all organisms, not just humans. Moreover, they recognized the important fact that when popu- lation size is limited by resource availability, there is constant competition. This is a crucial point, because competition

among individuals is the ultimate key to understanding natural selection.

Charles Lyell (1797–1875) is consid- ered the founder of modern geology (Fig. 2-5). He was a lawyer, a geologist, and, for many years, Charles Darwin’s friend and mentor. Before meeting Darwin in 1836, Lyell had earned acceptance in Europe’s most prestigious scientific circles, thanks to his highly praised Principles of Geology, first pub- lished during the years 1830–1833.

In this extremely important work, Lyell argued that the geological processes we see today are the same as those that existed in the past. This theory, called geological uniformi- tarianism, didn’t originate entirely with Lyell, having been proposed by James Hutton in the late 1700s. Even so, it was Lyell who demonstrated that forces such as wind, water erosion, local flooding, frost, decomposition of veg- etable matter, volcanoes, earthquakes, and glacial movements had all contrib- uted in the past to produce the geologi- cal landscape that we see today. What’s more, these processes were ongoing, indicating that geological change was still happening and that the forces driv- ing such change were consistent, or uniform, over time. In other words, various aspects of the earth’s surface (mountain ranges, rivers, the position of

continents, and so forth) vary through time, but the underlying processes that influence them are constant.

Lyell also emphasized the obvious: namely, that for such slowly acting forces to produce momentous change, the earth must be far older than any- one had previously suspected. By pro- viding an immense time scale and thereby changing perceptions of the earth’s history from a few thousand to many millions of years, Lyell changed the framework within which scientists viewed the geological past. Thus the concept of “deep time” (Gould, 1987) remains one of Lyell’s most significant contributions to the discovery of evolu- tionary principles, because the immen- sity of geological time permitted the necessary time depth for the inherently slow process of evolutionary change (Fig. 2-6).

As you can see, the roots of evolu- tionary theory are deeply embedded in the late eighteenth and early nine- teenth centuries. During that time, many lesser-known but very important people also contributed to this intellec- tual movement. One such person was Mary Anning (1799–1847), who lived in the town of Lyme Regis on the south coast of England.

Anning’s father died when she was 11 years old, leaving his wife and two children destitute. Fortunately, he had taught Mary to recognize marine fos- sils embedded in the cliffs near the town. Thus she began to earn a living by collecting and selling fossils to col- lectors who were becoming increas- ingly interested in the remains of crea- tures that many people believed had been killed in the Noah flood.

After Anning’s discovery of the first complete fossil of Ichthyosaurus, a large marine reptile, and the first Pleiosaurus fossil (another ocean-dwelling reptile), some of the most famous scientists in England repeatedly visited her home. Eventually she became known as one of the world’s leading “fossilists.” And by sharing her extensive knowledge of fos- sil species with the leading scientists of the day, she contributed to the under-

▲�Figure 2-5 Portrait of Charles Lyell.

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uniformitarianism the theory that the earth’s features are the result of long- term processes that continue to operate in the present just as they did in the past. elaborated on by Lyell, this theory opposed catastrophism and greatly contributed to the concept of immense geological time.

Dorine Essumang

The Discovery of Natural Selection 33

standing of the evolution of marine life, which spanned over 200 million years. But because she was a woman and of low social position, Anning wasn’t acknowledged in the numerous sci- entific publications she facilitated. In recent years, however, she has achieved the recognition she deserves; her por- trait hangs prominently in the British Museum (Natural History) in London.

The Discovery of Natural Selection

Having already been introduced to Erasmus Darwin, you shouldn’t be surprised to learn that his grandson Charles grew up in an educated fam- ily with ties to the intellectual circles of the time. Charles Darwin (1809–1882) was one of six children of Dr. Robert and Susanna Darwin (Fig. 2-7). Being the grandson not only of Erasmus Darwin but also of the wealthy Josiah Wedgwood (of Wedgwood china fame), Charles grew up enjoying the comfort- able lifestyle of the landed gentry in rural England.

As a boy, Darwin had a keen interest in nature, but this interest did little to dispel the generally held view among family and friends that he was in no way remarkable. In fact, his per- formance at school was no more than ordinary.

After his mother’s death when he was 8 years old, Darwin was raised by his father and older sisters. Because he showed little interest in anything except hunting, shooting, and per- haps science, his father sent him to Edinburgh University to study medi- cine. It was there that Darwin first became acquainted with the evolution- ary theories of Lamarck and others.

During that time (the 1820s), notions of evolution were becoming feared in England and elsewhere. Anything identified with postrevolu- tionary France was viewed with sus- picion by the established order in England, and Lamarck, partly because he was French, was especially vilified by British scientists.

It was also a time of growing polit- ical unrest in Britain. The Reform Movement, which sought to undo the

◀�Figure 2-6 (a) These limestone cliffs in southern France were formed around 300 million years ago from shells and the skeletal remains of countless sea creatures. (b) Part of a block of stone cut from the same limestone containing fossilized shells.

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chapter 2 The Development of Evolutionary Theory34

though he hated medicine and left Edinburgh after two years, his experi- ence there was a formative period in his intellectual development.

Although Darwin was fairly indif- ferent to religion, he next went to Cambridge to study theology. It was during his Cambridge years that he cultivated interests in natural science and immersed himself in botany and geology. Following his graduation in 1831, he was invited to join a scien- tific expedition that would circle the globe. And so it was that Darwin set sail aboard HMS Beagle on December 17, 1831 (Fig. 2-8). The famous voyage of the Beagle would take almost five years and would forever change not only the course of Darwin’s life but also the history of biological science (Fig. 2-9).

Darwin went aboard the Beagle believing in the fixity of species. But during the voyage he privately began to have doubts. For one thing, he came across fossils of ancient giant animals that, except for size, looked very much like species that still lived in the same vicinity. The similarities he saw caused

many inequalities of the tradi- tional class system, was under way, and like most social move- ments, it had a radical faction. Because many of the radicals were atheists and socialists who also supported Lamarck’s ideas, many people came to associate evolution with athe- ism and political subversion. The growing fear of evolution- ary ideas led many to believe that if these ideas were gen- erally accepted, “the Church would crash, the moral fabric of society would be torn apart, and civilized man would return to savagery” (Desmond and Moore, 1991, p. 34). It’s unfortu- nate that some of the most out- spoken early proponents of spe- cies change were so vehemently

anti-Christian, because their rhetoric helped to establish the entrenched sus- picion and misunderstanding of evolu- tionary theory that persists today.

While at Edinburgh, Darwin stud- ied with professors who were outspo- ken supporters of Lamarck. So, even

▲�Figure 2-7 Charles Darwin, photo- graphed five years before the publica- tion of On the Origin of Species.

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NORTH AMERICA

SOUTH AMERICA

AFRICA

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AUSTRALIA

INDIA

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British Isles

Azores Islands

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Mauritius

King George’s Sound

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Galápagos Islands Marquesas

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Falkland Islands

Montevideo Port Desire

Rio de Janeiro

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Valparaiso

Tierra del Fuego

JAPAN

Outward voyage Return voyage

A T L A N T I C P A C I F I C P A C I F I C

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▼�Figure 2-8 The route of HMS Beagle.

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Dorine Essumang

The Discovery of Natural Selection 35

him to speculate that the fossils repre- sented ancestors of those living forms.

During the now famous stopover at the Galápagos Islands, off the coast of Ecuador, Darwin noticed that the veg- etation and animals (especially birds) shared many similarities with those on the South American mainland. But they weren’t identical to them. What’s more, the birds varied from island to island. Darwin collected 13 varieties of Galápagos finches, and it was clear that they represented a closely related group; but some of their physical traits

were different, particularly the shape and size of their beaks (Fig. 2-10). Darwin also collected finches from the mainland, and these appeared to repre- sent only one group, or species.

The insight that Darwin gained from the finches is legendary. But, contrary to popular misconception, it wasn’t until after he returned to England that he recognized the signifi- cance of the variation in beak struc- ture. In fact, during the voyage, he had paid little attention to the finches. It was only later that he considered the

◀�Figure 2-9 A painting by John Chancellor of HMS Beagle sail- ing through the Galápagos Islands in 1835.

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▼�Figure 2-10 Beak variation in Darwin’s Galápagos finches.

Ground finch

Tree finch

Tree finch (called woodpecker finch)

Ground finch (known as warbler finch)

Main Food: seeds Main food: leaves, buds, blossoms, fruits

Main food: insects Main food: insects

Beak: heavy Beak: thick, short Beak: stout, straight Beak: slender

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factors that could lead to the modifica- tion of one species into many (Gould, 1985; Desmond and Moore, 1991). He realized that the various Galapagos finches had all descended from a com- mon mainland ancestor and had been modified over time in response to different island habitats and dietary preferences.

Darwin returned to England in October 1836 and was immediately accepted into the most prestigious sci- entific circles. He married his cousin Emma Wedgwood and moved to the village of Down, near London, where he spent the rest of his life writing on topics ranging from fossils to orchids (Fig. 2-11). But the question of species change was his overriding passion.

At Down, Darwin began to develop his views on what he called natural selection. This concept was borrowed from animal breeders, who choose, or “select,” as breeding stock those ani- mals that possess certain traits that the breeders want to emphasize in off- spring. Animals with undesirable traits are “selected against,” or prevented from breeding. A dramatic example of the effects of selective breeding can be seen in the various domestic dog breeds shown in Figure 2-12. Darwin applied his knowledge of domesticated

species to naturally occurring ones, and he recognized that in undomes- ticated organisms, the selective agent was nature, not humans.

By the late 1830s, Darwin had real- ized that biological variation within a species (that is, differences among individuals) was crucial. Furthermore, he realized that sexual reproduc- tion increased variation, although he didn’t know why. Then, in 1838, he read Malthus’ essay; and there he found the answer to the question of how new spe- cies came to be. He accepted Malthus’ idea that populations increase at a faster rate than resources do, and he recognized that in nonhuman animals, population size is always limited by the amount of available food and water. He also recognized that these two facts lead to a constant “struggle for exis- tence.” The idea that in each generation more offspring are born than survive to adulthood coupled with the notions of competition for resources and biologi- cal diversity was all Darwin needed to develop his theory of natural selection. He wrote: “It at once struck me that under these circumstances favourable variations would tend to be preserved, and unfavourable ones to be destroyed. The result of this would be the forma- tion of a new species” (F. Darwin, 1950,

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▶�Figure 2-11 Down House as seen from the rear. Darwin wrote On the Origin of Species and numerous other publications here.

Dorine Essumang

The Discovery of Natural Selection 37

pp. 53–54). Basically, this quotation summarizes the entire theory of natu- ral selection.

By 1844, Darwin had written a short summary of his natural selec- tion hypothesis but he didn’t think he had enough data to support it, so he continued his research without pub- lishing. He also had other reasons for not publishing what he knew would be a highly controversial work. He was deeply troubled that his wife, Emma, saw his ideas as running counter to her strong religious convictions (Keynes, 2002). Also, as a member of the estab- lished order, he knew that many of his friends and associates were concerned with threats to the status quo, and evo- lutionary theory was viewed as a very serious threat indeed.

In Darwin’s Shadow Unlike Darwin, Alfred Russel Wal- lace (1823–1913) was born into a family of modest means (Fig. 2-13). He went to work at the age of 14 and, with lit- tle formal education, moved from one job to the next. Eventually he became interested in collecting plants and ani- mals and joined expeditions to the Amazon and Southeast Asia, where he acquired firsthand knowledge of many natural phenomena.

In 1855, Wallace published an arti- cle suggesting that current species were descended from other species and that the appearance of new ones was influenced by environmental factors (Trinkaus and Shipman, 1992). This article caused Lyell and others to urge

▲�Figure 2-12 All domestic dog breeds share a common ancestor, the wolf. The extreme variation exhib- ited by dog breeds today has been achieved in a relatively short time through artificial selection. In this situ- ation, humans allow only certain dogs to breed in order to emphasize spe- cific characteristics. (We should note that many traits desired by human breeders are detrimental to the dogs themselves.)

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chapter 2 The Development of Evolutionary Theory38

▲ Figure 2-14 Charles Darwin’s Origin of Species, the book that revo- lutionized biological science.

Darwin to publish, but he continued to hesitate.

Then, in 1858, Wallace sent Darwin another paper, “On the Tendency of Varieties to Depart Indefinitely from the Original Type.” In it, Wallace described evolution as a process driven by competition and natural selection. When he received Wallace’s paper, Darwin realized that if he continued to wait, Wallace might get credit for a theory (natural selection) that he him- self had developed. He quickly wrote a paper presenting his ideas, and both papers were read before the Linnean Society of London. Neither author was present. Wallace was out of the country and Darwin was mourning the recent death of his young son.

The papers received little notice at the time. But in December 1859, when Darwin completed and published his greatest work, On the Origin of Species,* the storm broke, and it still hasn’t abat- ed (Fig. 2-14). Although public opinion was negative, there was much scholarly praise for the book, and scientific opin- ion gradually came to Darwin’s sup- port. The question of species was now

* The full title is On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life.

explained: Species could change, they weren’t fixed, and they evolved from other species through the mechanism of natural selection.

Natural Selection

Early in his research, Darwin had realized that natural selection was the key to evolution. With the help of Malthus’ ideas, he saw how selection in nature could be explained. In the strug- gle for existence, those individuals with favorable variations would survive and reproduce, but those with unfavorable variations would not. For Darwin, the explanation of evolution was simple. The basic processes, as he understood them, are as follows:

1. All species are capable of produc- ing offspring at a faster rate than food supplies increase.

2. There is biological variation in all species.

3. In each generation more offspring are produced than survive, and because of limited resources, there is competition among individu- als. (Note: This statement does not mean that there is constant fierce fighting.)

4. Individuals who possess favorable variations or traits (for example, speed, resistance to disease, pro- tective coloration) have an advan- tage over those who don’t. In other words, they have greater fitness, because favorable traits increase the likelihood that they will sur- vive to adulthood and reproduce.

5. The environmental context deter- mines whether or not a trait is beneficial. What is favorable in one setting may be a liability in another. Consequently the traits that become most advantageous are the results of a natural process.

6. Traits are inherited and passed on to the next generation. Because individuals who possess favorable traits contribute more offspring to the next generation than do oth-

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▲ Figure 2-13 Alfred Russel Wallace independently identified natural selec- tion as the key to the evolutionary process. Oil on canvas by Evstafieff (19th century) Down House, Downe, Kent, UK/ © English Heritage Photo Library / The Bridgeman Art Library.

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Dorine Essumang

Natural Selection in Action 39

ers, over time those favorable traits become more common in the pop- ulation. Less favorable character- istics aren’t passed as frequently, so they become less common over time and are “weeded out.” Indi- viduals who produce more off- spring in comparison to others are said to have greater reproductive success, or fitness.

7. Over long periods of time, success- ful variations accumulate in a pop- ulation, so that later generations may be distinct from ancestral ones. Thus, in time, a new species may appear.

8. Geographical isolation also con- tributes to the formation of new species. As populations of a spe- cies become geographically isolated from one another, for whatever rea- sons (for example, distance or nat- ural barriers such as rivers), they begin to adapt to different environ- ments. Over time, as populations continue to respond to different selective pressures (that is, dif- ferent ecological circumstances), they may become distinct species. The 13 species of Galápagos finch- es are presumably all descended from a common ancestor that lived on the South American mainland. Thus, they provide an example of the role of geographical isolation.

Before Darwin, individual mem- bers of species were not considered important, so they weren’t studied. But as we’ve seen, Darwin recognized the uniqueness of individuals and real- ized that variation among them could explain how selection occurs. Favorable variations are selected, or chosen, for survival by nature; unfavorable ones are eliminated. Natural selection oper- ates on individuals, either favorably or unfavorably, but it’s the population that evolves. It’s important to emphasize that the unit of natural selection is the individual; the unit of evolution is the population. This is because individuals don’t change genetically but, over time, populations do.

Natural Selection in Action

One of the most frequently cited examples of natural selection relates to changes in the coloration of a species of moth. In recent years, the moth story has come under some criti- cism; but the premise remains valid, so we use it to illustrate how natural selec- tion works.

Before the nineteenth century, the most common variety of the peppered moth in England was a mottled gray color. During the day, as the moths rested on lichen-covered tree trunks, their coloration provided camouflage (Fig. 2-15). There was also a dark gray variety of the same species, but because the dark moths were not as well cam- ouflaged, they were more frequently eaten by birds; therefore they were less common. (In this example, the birds are the selective agents, and they apply selective pressures on the moths.) Yet by the end of the nineteenth century, the darker form had almost completely replaced the common gray one.

The cause of this change was the changing environment of industrialized nineteenth-century England. Coal dust from factories and fireplaces settled on the trees, turning them dark gray and killing the lichen. The moths contin- ued to rest on the trees, but the light gray ones became more conspicuous as the trees became darker, and they were increasingly targeted by birds. Thus, the light gray moths began to contrib- ute fewer genes to the next generation than the darker moths, and the propor- tion of lighter moths decreased while the dark moths became more common. A similar color shift also occurred in North America. But the introduction of clean air acts in both Britain and the United States reduced the amount of air pollution (at least from coal), and the predominant color of the peppered moth once again became the light mottled gray. This kind of evolution- ary shift in response to environmental change is called adaptation.

fitness pertaining to natural selection, a measure of the relative reproductive success of individuals. Fitness can be mea- sured by an individual’s genetic contribution to the next generation compared with that of other individuals. the terms genetic fit- ness, reproductive fitness, and differential net reproductive success are also used.

reproductive success the num- ber of offspring an individual produces and rears to reproductive age, or an individual’s genetic contribution to the next generation.

selective pressures Forces in the environment that influence reproductive success in individuals.

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chapter 2 The Development of Evolutionary Theory40

The medium ground finch of the Galápagos Islands provides another example of natural selection. In 1977, drought killed many of the plants that produced the smaller, softer seeds favored by these birds. This forced a population of finches on one of the islands to feed on larger, harder seeds. Even before 1977, some birds had smaller, less robust beaks than others (that is, there was variation). During the drought, because they were less able to process the larger seeds, more smaller-beaked birds died than larger-beaked birds. So, although over- all population size declined, average

beak thickness in the survivors and their offspring increased, simply because larger-beaked individuals were surviving in greater numbers and pro- ducing more offspring. In other words, they had greater reproductive success. But during heavy rains in 1982–1983, smaller seeds became more plenti- ful again and the pattern in beak size reversed itself, demonstrating again how reproductive success is related to environmental conditions (Boag and Grant, 1981; Ridley, 1993).

The best illustration of natural selection, however—and certainly one with potentially grave consequences for humans—is the recent increase in resistant strains of disease- causing microorganisms. When antibiotics were first introduced in the 1940s, they were seen as the cure for bacte- rial disease. But that optimistic view didn’t take into account that bacteria, like other organisms, possess genetic variability. Consequently, though an antibiotic will kill most bacteria in an infected person, any bacterium with an inherited resistance to that par- ticular therapy will survive. In turn, the survivors reproduce and pass their drug resistance to future generations, so that eventually, the population is mostly made up of bacteria that don’t respond to treatment. What’s more, because bacteria produce new genera- tions every few hours, antibiotic-resis- tant strains are continuously appearing. As a result, many types of infection no longer respond to treatment. For exam- ple, tuberculosis was once thought to be well controlled, but there’s been a resurgence of TB in recent years because some strains of the bacterium that causes it are resistant to most of the antibiotics used to treat it.

These examples (moths, finches, and bacteria) provide the following insights into the fundamentals of evo- lutionary change produced by natural selection:

1. A trait must be inherited if natural selection is to act on it. A charac-

▶�Figure 2-15 Variation in the pep- pered moth. (a) The dark form is more visible on the light, lichen-covered tree. (b) On trees dark- ened by pollution, the lighter form is more visible.

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Natural Selection in Action 41

teristic that isn’t hereditary (such as a temporary change in hair color produced by the hairdresser) won’t be passed on to offspring. In finches, for example, beak size is a hereditary trait.

2. Natural selection cannot occur without population variation in inherited characteristics. If, for example, all the peppered moths had initially been light gray and the trees had become darker, the survival and reproduction of the moths could have been so low that the population might have become extinct. Selection can work only with variation that already exists.

3. Fitness is a relative measure that changes as the environment changes. Fitness is simply differ- ential net reproductive success. In the initial stage, the lighter moths were more fit because they pro- duced more offspring. But as the environment changed, the dark gray moths became more fit. Later, a further change reversed the pat- tern again. Likewise, the major- ity of Galápagos finches will have larger or smaller beaks, depend- ing on external conditions. So it should be obvious that statements regarding the “most fit” don’t mean anything without reference to spe- cific environments.

4. Natural selection can act only on traits that affect reproduction. If a characteristic isn’t expressed until later in life, after organisms have reproduced, natural selection can’t influence it. This is because the trait’s inherited components have already been passed on to off- spring. Many forms of cancer and cardiovascular disease are influ- enced by hereditary factors, but because these diseases usually affect people after they’ve had chil- dren, natural selection can’t act against them. By the same token, if a condition usually kills or com- promises the individual before he

or she reproduces, natural selec- tion is able to act against it because the trait won’t be passed on.

So far, our examples have shown how different death rates influence natural selection (for example, moths or finches that die early leave fewer off- spring). But mortality is only part of the picture. Another important aspect of natural selection is fertility, because an animal that gives birth to more young contributes more genes to the next generation than an animal that produces fewer. But fertility isn’t the entire story either, because the crucial element is the number of young raised successfully to the point where they themselves reproduce. We call this differential net reproductive success. The way this mechanism works can be demonstrated through another example.

In swifts (small birds that resem- ble swallows), data show that produc- ing more offspring doesn’t necessarily guarantee that more young will be suc- cessfully raised. The number of eggs hatched in a breeding season is a mea- sure of fertility. The number of birds that mature and are eventually able to leave the nest is a measure of net repro- ductive success, or successfully raised offspring. The following table shows the correlation between the number of eggs hatched (fertility) and the number of young that leave the nest (reproduc- tive success), averaged over four breed- ing seasons (Lack, 1966):

Number of eggs hatched (fertility) 2 eggs 3 eggs 4 eggs Average number of young raised (reproductive success) 1.92 2.54 1.76 Sample size (number of nests) 72 20 16

As you can see, the most efficient number of eggs is three, because that number yields the highest reproductive

fertility the ability to conceive and pro- duce healthy offspring.

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chapter 2 The Development of Evolutionary Theory42

success. Raising two offspring is less beneficial to the parents, because the end result isn’t as successful as with three eggs. Trying to raise more than three is actually detrimental, as the parents may not be able to provide enough nourishment for any of the offspring. Offspring that die before reaching reproductive age are, in evo- lutionary terms, equivalent to never being born. Moreover, an offspring that dies can be a minus to the parents, because before it dies it drains paren- tal resources. It may even inhibit their ability to raise other offspring, thus reducing their reproductive success even further. Selection favors those genetic traits that yield the maximum net reproductive success. If the num- ber of eggs laid is a genetic trait in birds (and it seems to be), natural selection in swifts should act to favor laying three eggs as opposed to two or four.

Constraints on Nineteenth-Century Evolutionary Theory

Darwin argued for the concept of evolution in general and the role of natural selection in particular. But he didn’t understand the exact mecha- nisms of evolutionary change. As we’ve already seen, natural selection acts on variation within species; but what Dar- win didn’t understand was where the variation came from. In the nineteenth century, this remained an unanswered question, plus no one understood how offspring inherited traits from their parents. Almost without exception, nineteenth-century scientists believed inheritance to be a blending process in which parental characteristics were mixed together to produce intermedi- ate expressions in offspring. Given this notion, we can see why the true nature of genes was unimaginable; and, with no alternative explanation, Darwin accepted the blending theory of inheri- tance. As it turns out, a contemporary

of Darwin’s had actually worked out the rules of heredity. However, the work of this Augustinian monk, named Gregor Mendel (whom you’ll meet in Chapter 4), wasn’t recognized until the begin- ning of the twentieth century.

The first three decades of the twen- tieth century saw the merger of natural selection theory and Mendel’s discov- eries. This was a crucial development because until then, scientists thought these concepts were unrelated. Then, in 1953, the structure of DNA was dis- covered. This landmark achievement has been followed by even more amaz- ing advances in the field of genetics. The human genome was sequenced in 2003, followed by the chimpanzee genome in 2005. The genomes of many other species have also now been sequenced. By comparing the genomes of different species (a field called com- parative genomics), scientists can examine how genetically similar or dif- ferent they are. This can explain many aspects of how these species evolved. Also, since the early 1990s, several sci- entists have merged the fields of evo- lutionary and developmental biology into a new field called “evo-devo.” This approach, which compares the actions of different developmental genes and the factors that regulate them, is mak- ing it possible to explain evolution in ways that were impossible even 15 years ago. Scientists are truly on the threshold of revealing many secrets of the evolutionary process. If only Darwin could know!

Opposition to Evolution Today

More than 150 years after the pub-lication of Origin of Species, the debate over evolution is far from over, especially in the United States and, increasingly, in several Muslim coun- tries. For most biologists, evolution is indisputable. The genetic evidence for it is solid and accumulates daily. Any- one who appreciates and understands

genome the entire genetic makeup of an individual or species.

Opposition to Evolution Today 43

genetic mechanisms can’t avoid the conclusion that populations and spe- cies evolve. What’s more, the majority of Christians don’t believe that biblical depictions should be taken literally. But at the same time, some surveys show that about half of all Americans don’t believe that evolution occurs. There are a number of reasons for this.

The mechanisms of evolution are complex and do not lend themselves to simple explanations. Understanding them requires some familiarity with genetics and biology, a familiarity that most people don’t have unless they took related courses in school. What is more, many people want definitive, clear-cut answers to complex ques- tions. But as you learned in Chapter 1, science doesn’t always provide defini- tive answers to questions; it doesn’t establish absolute truths; and it doesn’t prove facts. Another thing to consider is that regardless of their culture, most people are raised in belief systems that don’t emphasize biological continu- ity between species or offer scientific explanations for natural phenomena.

The relationship between science and religion has never been easy (remember Galileo), even though both serve in their own ways to explain natural phenomena. As you read in Chapter 1, scientific explanations are based on data analysis, hypothesis testing, and interpretation. Religions, meanwhile, are systems of faith-based beliefs. A major difference between science and religion is that religious explanations aren’t amenable to scien- tific testing. Religion and science con- cern different aspects of the human experience, but they aren’t inherently mutually exclusive approaches. That is, belief in God doesn’t exclude the occurrence of biological evolution; and acknowledgment of evolutionary processes doesn’t preclude the exis- tence of God. What’s more, evolution- ary theories aren’t rejected by all reli- gions or by most forms of Christianity.

Some years ago, the Vatican hosted an international conference on human evolution; in 1996, Pope John Paul II

issued a statement that “fresh knowl- edge leads to recognition of the the- ory of evolution as more than just a hypothesis.” Today, the official position of the Catholic Church is that evo- lutionary processes do occur, but that the human soul is of divine cre- ation and not subject to evolution- ary processes. Likewise, mainstream Protestants don’t generally see a con- flict. Unfortunately those who believe in an absolutely literal interpretation of the Bible (called fundamentalists) accept no compromise.

A Brief History of Opposition to Evolution in the United States There are historical reasons for the opposition to the teaching of evolu- tion in the United States. Reacting to rapid cultural change after World War I, conservative Christians sought a revival of what they considered to be “traditional values.” In their view, one way to achieve this was to prevent any mention of Darwinism in public schools. One result of this effort was a state law, passed in Tennessee in 1925, that banned the teaching of any theo- ry (particularly evolution) that did not support the biblical version of the cre- ation of humankind. To test the valid- ity of this law, the American Civil Lib- erties Union persuaded a high school teacher named John Scopes to submit to being arrested and tried for teach- ing evolution (Fig. 2-16). The subse- quent trial, called the “Scopes Mon- key Trial” was a 1920s equivalent of current celebrity trials. In the end, Scopes was convicted and fined $100, though the conviction was later over- turned. Although most states didn’t actually forbid the teaching of evolu- tion, Arkansas, Tennessee, and a few others continued to prohibit any men- tion of it until 1968, when the U.S. Supreme Court struck down the ban against teaching evolution in public schools. (One coauthor of this text- book remembers when her junior high

biological continuity a bio- logical continuum. When expressions of a phenomenon continuously grade into one another so that there are no discrete categories, they exist on a continuum. color is one such phenomenon, and life-forms are another.

Dorine Essumang

chapter 2 The Development of Evolutionary Theory44

school science teacher was fired for mentioning evolution in Little Rock, Arkansas.)

By the mid-1960s, coverage of evo- lution in textbooks had increased. As a result, Christian fundamentalists renewed their campaign to eliminate evolution from public school curricula and to introduce antievolutionary material into public school classes. The creation science movement was born out of this effort.

Proponents of creation science are called “creationists” because they explain the existence of the universe as the result of a sudden creation event that occurred over the course of six 24-hour days, as described in the book of Genesis. The premise of creation sci- ence is that the biblical account of the earth’s origins and the story of Noah and the flood can be supported by sci- entific evidence.

Creationists have insisted that what they used to call “creation science” and now call “intelligent design” (ID) is a valid scientific explanation of the

earth’s origins. They’ve argued that in the interest of fairness, a balanced view should be offered in public schools: If evolution is taught as science, then cre- ationism should also be taught as sci- ence. Sounds fair, doesn’t it? But ID isn’t science at all, for the simple reason that creationists insist that their view is absolute and infallible. Therefore cre- ationism is not a hypothesis that can be tested, nor is it amenable to falsifi- cation. And because hypothesis testing is the basis of all science, creationism by its very nature cannot be considered science.

Since the 1970s, creationists have become increasingly active on local school boards and in state legisla- tures, promoting laws that mandate the teaching of creationism in pub- lic schools. However, state and fed- eral courts have consistently over- ruled these laws because they violate the “establishment clause” of the First Amendment of the U.S. Constitution, which states that “Congress shall make no law respecting an establishment of

▶�Figure 2-16 Photo taken at the “Scopes Monkey Trial.” The well- known defense attorney Clarence Darrow is sitting on the edge of the table. John Scopes, wearing a white shirt, is sitting with his arms folded behind Darrow.

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Christian fundamentalists adherents to a movement in american protestantism that began in the early twentieth century. this group holds that the teachings of the Bible are infallible and should be taken literally.

Dorine Essumang

Opposition to Evolution Today 45

religion, or prohibiting the free exer- cise thereof.” This statement guaran- tees the separation of church and state, and it means that the government can neither promote nor inhibit the prac- tice of any religion. Therefore the use of public institutions (including schools), paid for by taxes, to promote any particular religion is unconstitu- tional. Of course this does not mean that individuals can’t have private reli- gious discussions or pray in publicly funded institutions; but it does mean that such places can’t be used for orga- nized religious events. This hasn’t stopped creationists, who encourage teachers to claim “academic freedom” to teach creationism. To avoid objec- tions based on the guarantee of sepa- ration of church and state, proponents of ID claim that they don’t empha- size any particular religion. But this argument doesn’t address the essen-

tial point that teaching any religious views in a way that promotes them in publicly funded schools is a violation of the U.S. Constitution.

It is curious that the biological process that has led to the appearance of millions of plants and animals on our planet should generate such con- troversy. Our current understanding of evolution is directly traceable to developments in intellectual thought over the past 400 years. Many people contributed to this shift in perspec- tive; we’ve named only a few to pro- vide a short historical view. It is quite likely that, in the next 20 years, scien- tists will identify many of the secrets of our evolutionary past through advances in genetic technologies and the continued discovery of fossil material. For evolutionary science, the early twenty-first century is indeed an exciting time.

The Mechanism of Natural Selection

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At a Glance

Individuals in a population vary in most inherited characteristics (i.e., they don’t all express these traits in the same way)

Some individuals have higher reproductive success than others because they possess advantageous expressions of certain traits

Increase in the proportion of individuals with the advantageous expression of the trait; decrease in the proportion having a less beneficial expression

Environment (selective agents)

chapter 2 The Development of Evolutionary Theory46

Summary of Main Topics

▶▶ Our current understanding of evolutionary processes is directly traceable to develop- ments in intellectual thought in western Europe and the East over the past 400 years. Darwin and Wallace were able to dis- cover the process of natural selection and evolution because of the discoveries of numer- ous scientists who had laid the groundwork for them. Among others, Galileo, Lyell, Lamarck, Linnaeus, and Malthus all con- tributed to a dramatic shift in how people viewed the planet and themselves as part of a system governed by natural processes.

▶▶ Charles Darwin and Alfred Russel Wallace recognized that there was variation among individuals in any population (human or nonhuman). Having come to understand how ani- mal breeders selected for cer-

tain traits in cattle, pigeons, and other species, Darwin was able to formulate the theory of natural selection. Stated in the simplest terms, natural selec- tion is a process whereby indi- viduals who possess favorable traits (characteristics that per- mit them to survive and repro- duce in a specific environment) will produce more offspring than individuals who have less favorable traits. Over time, the beneficial characteristics will become more frequent in the population, and the makeup of the population (or even a spe- cies) will change.

▶▶ As populations of a species become reproductively iso- lated from one another (per- haps because of distance or geographical barriers), they become increasingly differ- ent as each population adapts, by means of natural selec-

tion, to its own environment. Eventually, the populations may become distinct enough that they can no longer inter- breed; at this point, they are considered separate species.

▶▶ In the United States, and increasingly in some Muslim countries, the teaching of evolutionary processes is denounced because they are seen as contradictory to cer- tain religious views. In recent years, Christian fundamental- ists in the United States have argued in favor of teaching “creation science” or “intelli- gent design” in public schools. So far, courts have ruled against various attempts to promote “creation science” because the U.S. Constitution provides for the separation of church and state.

During the last 150 years, biologists have gathered overwhelming evidence to support evolutionary the- ory. In this chapter we have emphasized the role of natural selection, which is demonstrated by studying the effects of human selective breeding on such spe- cies as domestic dogs. We can see how natural selec- tion causes microevolutionary change by observing alterations over a few decades in many species. And evolutionary change, including speciation, can also be documented much faster (just a few weeks) in rapidly reproducing species such as bacteria.

Within the past 20 years, scientists have developed many techniques that allow them to directly compare different species genetically. In fact, they can now pro- vide reliable estimates as to when two related species

last shared a common ancestor, or when they became separate species. For example, Hailer et al (2012) used genetic evidence to suggest that polar bears diverged from their close relative, the European brown bear around 600 kya.*

Prior to the development of recent innovations in genetic research, it was impossible to estimate when speciation events occurred. But by combining fos- sil and genetic evidence we are now in a position to explain microevolution and the appearance of new species (speciation) in ways that, until recently, were only dreamed of.

*kya = thousand years ago

How Do We Know?

47Media Resources

1. After having read this chapter, how would you respond to the question, “If humans evolved from monkeys, why do we still have monkeys?”

2. We live in an age of unprecedented technological change that is rapidly altering almost all aspects of our lives. Can you think of a paradigm shift that has occurred because of technological innovations in the past 30 years or so?

3. Given what you’ve read about the scientific method in Chapter 1, how would you explain the differ-

ences between science and religion as methods of explaining natural phenomena? Do you personally see a conflict between evolutionary and religious explanations of how species came to be?

4. Can you think of some examples of artificial and natural selection that were not discussed in this chapter? For your examples, what traits have been selected for? In the case of natural selection, what was the selective agent?

Critical Thinking Questions

Video See the video “Natural Selection” to learn

more about topics covered in this chapter. Login to your Anthropology CourseMate at www.cengagebrain.com to access videos.

Media Resources

Connections

DNA is the basis of all life.

Connections

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Evolutionary theory, particularly natural selection, explains

how life forms have changed over time.

Heredity is based on the transmission

of DNA from one generation to the

next.

After mastering the material in this chapter, you should be able to:

▶ �Discuss why DNA is the biological basis of life and explain some of the scientific evidence showing how all species are ultimately related to one another.

▶ �Understand in general what DNA does.

▶ �Explain why DNA replication has been important to evolutionary processes.

▶ �Discuss what genes do.

▶ �Outline the steps involved in DNA replication and protein synthesis.

▶ �Understand why regulatory genes are important to the evolutionary process.

▶ �Discuss the genetic evidence demonstrating how humans are connected to other species, that is, how we are part of a biological continuum.

▶ �Understand why the study of genetics is critical to biological anthropology today.

You’ve just gotten home after a rotten day, and you’re watching the news on TV. The first story, after around 20 minutes of commer- cials, is about genetically modified foods, synthetic DNA, or the contro- versy over stem cell research. What do you do? Change the channel? Press the mute button? Go to sleep? Or do you follow the story? If you watch it, do you understand it, and do you think it’s important to you personally? In fact, all of these topics are impor- tant to you because you live in an age when genetic discoveries and geneti- cally based technologies are advanc- ing daily, and one way or another, they’re going to profoundly affect your life.

At some point, you or someone you love will probably need lifesaving med- ical treatment, perhaps for cancer, and this treatment will almost certainly be based on genetic research. Like it or not, you already eat genetically modi- fied foods, and you may eventually take advantage of developing reproductive technologies. Sadly, you may also see the development of biological weapons based on genetically altered bacteria and viruses. But fortunately, you’ll also live to see many of the secrets of evolu- tion revealed through genetic research. So even if you haven’t been particu- larly interested in genetic issues, you should be aware that they affect your life every day.

As you already know, this book is about human evolution, variation, and adaptation, all of which are ultimately

3 The Biological Basis of Life

linked to life processes that involve cells, the duplication and decoding of genetic information, and the trans- mission of this information between generations. So before we go any fur- ther, we must examine the basic prin- ciples of genetics. Genetics is the study of how genes work and how traits are passed from one generation to the next. Although most physical anthro- pologists don’t specialize in this field, they’re very familiar with it because the various subdisciplines of biological anthropology are ultimately connected by genetics.

Student Learning Objectives

Dorine Essumang

chapter 3 The Biological Basis of Life 50

Cells

In order to discuss genetic and evo-lutionary principles, it’s first nec- essary to understand the basic func- tions of cells. Cells are the fundamental units of life in all organisms. In some life-forms, such as bacteria, the entire organism consists of only a single cell (Fig. 3-1). However, more com- plex multicellular forms, such as plants, insects, birds, and mammals, are composed of billions of cells. In fact, an adult human body may be composed of as many as 1 trillion (1,000,000,000,000) cells, all function- ing in complex ways that ultimately promote the survival of the individual.

Life on earth began more than 3.5 billion years ago in the form of single-celled organisms, represented today by bacteria and blue-green algae. Structurally more complex cells, called eukaryotic cells, appeared approx- imately 1.2 billion years ago, and because they are the kind of cell found in multicellular organisms, they will be the focus of this chapter. Despite the numerous differences among various forms of life, it’s important to under- stand that the cells of all living organ- isms share many similarities because of their common evolutionary past. In

this way, all living things are ultimately connected.

In general, a eukaryotic cell is a three-dimensional structure composed of carbohydrates, lipids (fats), nucleic acids, and proteins. It also contains several kinds of substructures called organelles, one of which is the nucleus (pl., nuclei), a discrete unit surrounded by a thin membrane called the nuclear membrane (Fig. 3-2). Inside the nucleus are two kinds of molecules that contain the genetic informa- tion that controls the cell’s functions.

▲�Figure 3-1 Each one of these pink sausage-shaped structures is a single- celled bacterium.

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Nuclear membrane

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Nucleus ▶�Figure 3-2 Structure of a gener- alized eukaryotic cell, illustrating its three-dimensional nature. Various organelles are shown; but for simplic- ity, only those we discuss are labeled.

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proteins three-dimensional mol- ecules that serve a wide variety of func- tions through their ability to bind to other molecules.

nucleus a structure (organelle) found in all eukaryotic cells. the nucleus contains DNa and rNa, among other things.

molecules Structures made up of two or more atoms. Molecules can combine with other molecules to form more complex structures.

Dorine Essumang

The Structure of DNA 51

Actually, these two mol- ecules, DNA (deoxyribo- nucleic acid) and RNA (ribonucleic acid), are fun- damental not only to cel- lular activities but also to life itself.

The nucleus is sur- rounded by a gel-like sub- stance called cytoplasm, which contains many other types of organelles involved in activities related to the function of the cell and organism. These activities include breaking down nutrients and converting them to other substances, storing and releasing energy, elimi- nating waste, and manufacturing pro- teins through a process called protein synthesis.

Two of these organelles, mito- chondria (sing., mitochondrion) and ribosomes, require further men- tion. Mitochondria (Fig. 3-3) pro- duce energy and can be thought of as the cell’s engines. Mitochondria are structures enclosed within a folded membrane and contain their own dis- tinct DNA, called mitochondrial DNA (mtDNA), which directs mitochon- drial activities. Mitochondrial DNA has the same molecular structure and function as nuclear DNA (that is, DNA found in the nucleus), but it’s orga- nized somewhat differently. In recent years, mtDNA has attracted a lot of attention because of the traits it influ- ences and because it can be used to study certain evolutionary processes. For these reasons, we’ll discuss mito- chondrial inheritance in more detail later. Ribosomes, which will also be discussed later, are partly composed of RNA. They’re important because they’re essential to protein synthesis.

There are basically two types of cells: somatic cells and gametes. Somatic cells make up the body tissues, such as muscles, bones, organs, and the brain. Gametes, or sex cells, are spe- cifically involved in reproduction and are not important as structural com- ponents of the body. There are two types of gametes: egg cells, produced in female ovaries, and sperm cells,

which develop in male testes. The sole function of a sex cell is to unite with a gamete from another individual to form a zygote, which has the poten- tial of developing into a new individual. In this way, gametes transmit genetic information from parent to offspring.

The Structure of DNA

DNA is the very basis of life because it directs all cellular activities. So if we want to understand these activi- ties and how traits are inherited, we must know something about the struc- ture and function of DNA. The exact physical and chemical properties of DNA were unknown until 1953, when, at the University of Cambridge, in Eng- land, an American researcher named James Watson and three British scien- tists, Francis Crick, Maurice Wilkins, and Rosalind Franklin, developed a structural and functional model of DNA (Watson and Crick, 1953a, b). It’s impossible to overstate the impor- tance of this achievement because it completely revolutionized the fields of biology and medicine and forever altered our understanding of biologi- cal and evolutionary mechanisms (see “A Closer Look: Rosalind Franklin: The Fourth [but Invisible] Member of the Double Helix Team”).

The DNA molecule is composed of two chains of even smaller units called nucleotides. A nucleotide, in turn, is made up of three components: a sugar molecule (deoxyribose), a phosphate group (a molecule composed of phos- phorus and oxygen), and one of four nitrogenous bases (Fig. 3-4). In DNA, nucleotides are stacked on top of one

◀�Figure 3-3 Scanning electron micrograph of a mitochondrion.

DNA (deoxyribonucleic acid) the double-stranded molecule that con- tains the genetic code. DNa is a main com- ponent of chromosomes.

RNA (ribonucleic acid) a single- stranded molecule similar in structure to DNa. three forms of rNa are essential to protein synthesis: messenger rNa (mrNa), transfer rNa (trNa), and ribosomal rNa (rrNa)

cytoplasm the semifluid, gel-like sub- stance contained within the cell membrane. the nucleus and numerous structures involved with cell function are found within the cytoplasm.

protein synthesis the manufacture of proteins; that is, the assembly of chains of amino acids into functional protein mole- cules. protein synthesis is directed by DNa.

mitochondria (sing., mitochondrion) Structures contained within the cytoplasm of eukaryotic cells that convert energy, derived from nutrients, to a form that can be used by the cell.

ribosomes Structures composed of a form of rNa called ribosomal rNa (rrNa) and protein. ribosomes are found in a cell’s cytoplasm and are essential to the manu- facture of proteins.

mitochondrial DNA (mtDNA) DNa found in the mitochon- dria. Mitochondrial DNa is inherited only from the mother.

somatic cells Basically, all the cells in the body except those involved with reproduction.

gametes reproductive cells (eggs and sperm in animals) developed from precur- sor cells in ovaries and testes.

zygote a cell formed by the union of an egg cell and a sperm cell. It contains the full complement of chromosomes (in humans, 46) and has the potential of developing into an entire organism.

nucleotides Basic units of the DNa molecule, composed of a sugar, a phos- phate, and one of four DNa bases.

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Dorine Essumang

Rosalind Franklin: The Fourth (but Invisible) Member of the Double Helix Team

In 1962, three men, James Watson, Francis crick, and Maurice Wilkins, won the Nobel prize for medicine and physiolo- gy. they earned this most prestigious of all scientific honors for their discovery of the structure of the DNa molecule, which they had published in 1953. But due credit was not given to a fourth, equally deserving but unacknowledged person named rosalind Franklin, who had died of ovarian cancer in 1958. But even if she had been acknowl- edged in 1962, Franklin still wouldn’t have been a Nobel recipient because the Nobel prize isn’t awarded posthumously.

Franklin was a chemist who went to the University of cambridge in 1951, after being invited to study the structure of DNa. Before that, she’d been in paris using a technique called x-ray diffraction, a process that reveals the positions of atoms in crys-

talline structures. What Franklin didn’t know was that a colleague in her cambridge lab, Maurice Wilkins, was working on the same DNa project. to make matters worse, Wilkins hadn’t been told what her position was, so he thought she’d been hired as his assistant. Needless to say, this was hardly a good way to begin a working relationship, and as you might expect, there were a few tense moments between them.

Franklin soon produced some excellent x-ray diffraction images of some DNa fibers that Wilkins had provided, and the images

clearly showed that the structure was heli- cal. Furthermore, she worked out that there were two strands, not one. Wilkins inno- cently (but without Franklin’s knowledge) showed the images to Watson and crick, who were working in another laboratory, also at cambridge. Within 2 weeks, Watson and crick had developed their now famous model of a double-stranded helix without Franklin’s knowledge.

Desperately unhappy at cambridge, Franklin took a position at King’s college, London, in 1953. In april of that year, she and a student published an article in the journal Nature that dealt indirectly with the helical structure of DNa. the article by Watson and crick was published in the same issue.

During her lifetime, Franklin gained recognition for her work in carbons, coal, and viruses, topics on which she pub- lished many articles; and she was happy with the reputation she achieved. after her death, Watson made many derogative comments about rosalind Franklin, includ- ing several in print. even so, it appears that they remained on friendly terms until she died at the age of 37. She also remained friendly with crick, but she never knew that their revolutionary discovery was partly made possible by her photographic images.

A Closer Look

▲�Figure 1 Rosalind Franklin

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another to form a chain that is bonded by its bases to another nucleotide chain. Together the two chains twist to form a spiral, or helical shape. Thus, the DNA molecule is double-stranded and is described as forming a double helix that resembles a twisted ladder. If we follow the twisted ladder analogy, the sugars and phosphates represent the two sides while the bases and the bonds that join them form the rungs.

The four bases are the key to how DNA works. These bases are adenine, guanine, thymine, and cytosine, usu- ally referred to by their initial letters: A, G, T, and C. When the double helix

is formed, one type of base is able to pair, or bond, with only one other type: A can pair only with T, and G can pair only with C (Fig. 3-4). This specificity is absolutely essential to the DNA mol- ecule’s ability to replicate, or make an exact copy of itself.

DNA Replication

Cells multiply by dividing to make exact copies of themselves. This, in turn, enables organisms to grow and injured tissues to heal. There are two kinds of cell division. In the simpler

replicate to duplicate. the DNa mol- ecule is able to make copies of itself.

Dorine Essumang

Protein Synthesis 53

form, a cell divides one time to produce two “daughter” cells, each of which receives a full set of genetic material. This is important, because a cell can’t function properly without the right amount of DNA. But before a cell can divide, its DNA must replicate.

Replication begins when enzymes break the bonds between bases throughout the DNA molecule, sep- arating the two previously joined strands of nucleotides and leaving their bases exposed (Fig. 3-5). These exposed bases then attract unattached DNA nucleotides that have been made by DNA elsewhere in the cell nucle- us. Because each base can pair with only one other, the attraction between bases occurs in a complementary way. This means that the two pre- viously joined parental nucleotide chains serve as models, or templates, for forming new strands of nucleo- tides. As each new strand is formed, its bases are joined to the bases of an original strand. When the process is complete, there are two double- stranded DNA molecules exactly like

the original one. Importantly, each newly formed molecule consists of one original nucleotide chain joined to a newly formed chain.

Protein Synthesis

One of the most important activ-ities of DNA is to direct the assembly of proteins (protein synthe- sis) within cells. Proteins are com- plex three-dimensional molecules that function through their ability to bind to other molecules. For example, the protein hemoglobin (Fig. 3-6), found in red blood cells, is able to bind to oxy- gen, which it carries to cells through- out the body.

Proteins function in countless ways. Some, such as collagen (the most com- mon protein in the body), are structur- al components of tissues. Enzymes are also proteins, which regulate chemi- cal reactions. For example, a digestive enzyme called lactase breaks down lactose, or milk sugar, into two sim- pler sugars. Another class of proteins

BASES

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= Thymine

= Cytosine

= Phosphate

= Sugar

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Strand 1 Strand 2

Nucleotide

◀�Figure 3-4 Part of a DNA mol- ecule. The illustration shows the two DNA strands with the sugar (green) and phosphate (purple) molecules forming the sides of the strands and the bases (labeled T, A, G, and C) joined together in the middle.

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enzymes Specialized proteins that initiate and direct chemical reactions in the body.

complementary In genetics, refer- ring to the fact that DNa bases form pairs (called base pairs) in a precise manner. For example, adenine can bond only to thymine. these two bases are said to be comple- mentary because one requires the other to form a complete DNa base pair.

hemoglobin a protein molecule that occurs in red blood cells and binds to oxy- gen molecules.

Dorine Essumang

chapter 3 The Biological Basis of Life 54

includes many types of hormones. Hormones are produced by specialized cells and then released into the blood- stream to circulate to other parts of the body, where they produce specific effects in tissues and organs. Insulin, for example, is a hormone produced by cells in the pancreas, but it func- tions in the liver where it causes cells in the liver to absorb energy-producing glucose (sugar) from the blood. People

whose pancreatic cells fail to produce sufficient amounts of insulin have one of the two types of diabetes. Lastly, many kinds of proteins can enter a cell’s nucleus and attach directly to its DNA. This is very important because when these proteins bind to the DNA, they can regulate its activity. From this brief description, you can see that pro- teins make us what we are. So pro- tein synthesis must occur accurate- ly, because if it doesn’t, physiological development and cellular activities can be disrupted or even prevented.

Proteins are made up of chains of smaller molecules called amino acids. In all, there are 20 amino acids, 8 of which must be obtained from foods (see Chapter 16). The remain- ing 12 are produced in cells. These 20 amino acids are combined in different amounts and sequences to produce at least 90,000 different proteins. What makes proteins different from one another is the number and sequence of their amino acids.

▲�Figure 3-5 DNA replication. During DNA replication, the two strands of the DNA molecule (purple) are separated, and each strand serves as a template for the formation of a new strand (brown). When replication is complete, there are two DNA mol- ecules, each consisting of one new strand and one original strand.

T A

T T

G C

C C

C G

T A

T AT

A T

C G

T A

C G C G

C G

A T

DNA double helix

Original double-stranded DNA molecule

Two identical double- stranded DNA molecules

New strands

Original strands

Replication under way

Unattached nucleotides are attracted to their complementary nucleotides and thereby form a new strand

Replication complete

new old old new

▶�Figure 3-6 Diagrammatic repre- sentation of a hemoglobin molecule. Hemoglobin molecules are composed of four chains of amino acids (two alpha chains and two beta chains).

Beta chain Beta chain

Alpha chain Alpha chain

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amino acids Small molecules that are the components of proteins.

Dorine Essumang

Protein Synthesis 55

In part, DNA is a recipe for making a protein, because it’s the sequence of DNA bases that ultimately determines the order of amino acids in a protein. In the DNA instructions, a triplet, or group of three bases, specifies a par- ticular amino acid. For example, if a triplet consists of the base sequence cytosine, guanine, and adenine (CGA), it specifies the amino acid arginine (Table 3.1). Therefore, a small portion of a DNA recipe might look like this (except that there would be no spaces between the triplets): AGA CGA ACA ACC TAC TTT TTC CTT AAG GTC.

Protein synthesis actually takes place outside the cell nucleus, in the cytoplasm at the ribosomes. But the DNA molecule can’t leave the cell’s nucleus. Therefore the first step in pro-

tein synthesis is to copy the DNA mes- sage into a form of RNA called mes- senger RNA (mRNA), which can pass through the nuclear membrane into the cytoplasm. RNA is similar to DNA but it differs in some important ways:

1. It’s single-stranded. (This is true for the forms we discuss here but not true for all forms of RNA.)

2. It contains a different type of sugar.

3. It contains the base uracil as a sub- stitute for the DNA base thymine. (Uracil binds to adenine in the same way thymine does.)

The mRNA molecule forms on the DNA template in pretty much the same way that new DNA molecules do. As

Table 3.1 The Genetic Code Amino Acid Symbol Amino Acid mRNA Codon DNA Triplet

Ala Alanine GCU, GCC, GCA, GCG CGA, CGG, CGT, CGC

Arg Arginine CGU, CGC, CGA, CGG, AGA, AGG GCA, GCG, GCT, GCC, TCT, TCC

Asn Asparagine AAU, AAC TTA, TTG

Asp Aspartic acid GAU, GAC CTA, CTG

Cys Cysteine UGU, UGC ACA, ACG

Gln Glutamine CAA, CAG GTT, GTC

Glu Glutamic acid GAA, GAG CTT, CTC

Gly Glycine GGU, GGC, GGA, GGG CCA, CCG, CCT, CCC

His Histidine CAU, CAC GTA, GTG

Ile Isoleucine AUU, AUC, AUA TAA, TAG, TAT

Leu Leucine UUA, UUG, CUU, CUC, CUA, CUG AAT, AAC, GAA, GAG, GAT, GAC

Lys Lysine AAA, AAG TTT, TTC

Met Methionine AUG TAC

Phe Phenylalanine UUU, UUC AAA, AAG

Pro Proline CCU, CCC, CCA, CCG GGA, GGG, GGT, GGC

Ser Serine UCU, UCC, UCA, UCG, AGU, AGC AGA, AGG, AGT, AGC, TCA, TCG

Thr Threonine ACU, ACC, ACA, ACG TGA, TGG, TGT, TGC

Trp Tryptophan UGG ACC

Tyr Tyrosine UAU, UAC ATA, ATG

Val Valine GUU, GUC, GUA, GUG CAA, CAG, CAT, CAC

Terminating triplets UAA, UAG, UGA ATT, ATC, ACT

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messenger RNA (mRNA) a form of rNa that’s assembled on a sequence of DNa bases. It carries the DNa code to the ribosome during protein synthesis.

Dorine Essumang

chapter 3 The Biological Basis of Life 56

in DNA replication, the two DNA strands separate, but only partially, and one of these strands attracts free-floating RNA nucleotides (also pro- duced in the cell), which are joined together on the DNA template. The formation of mRNA is called transcription because, in fact, the DNA code is being copied, or transcribed (Fig. 3-7). Transcription con- tinues until a section of DNA called a terminator region (composed of one of three spe- cific DNA triplets) is reached and the process stops (see

Table 3-1). At this point, the mRNA strand, comprising anywhere from 5,000 to per- haps as many as 200,000 nucleotides, peels away from the DNA model, and a por- tion of it travels through the nuclear membrane to the ribo- some. Meanwhile, the bonds between the DNA bases are reestablished and the DNA molecule is once more intact.

As the mRNA strand arrives at the ribosome, its message is translated, or decoded (Fig. 3-8). Just as each DNA triplet specifies

A T

mRNA

DNA template strand

G C

C G

G C C

A A

▼ Figure 3-7 Transcription. In this illustration, the two DNA strands have partly separated. Messenger RNA (mRNA) nucleotides have been drawn to the template strand and a strand of mRNA is being made. Note that the mRNA strand will exactly complement the DNA template strand except that uracil (U) replaces thymine (T).

(a) As the ribosome binds to the mRNA, tRNA brings a particular amino acid, specified by the mRNA codon, to the ribosome.

(b) The tRNA binds to the first codon while a second tRNA–amino acid complex arrives at the ribosome.

(c) The ribosome moves down the mRNA, allowing a third amino acid to be brought into position by another tRNA molecule. Note that the first two amino acids are now joined together.

Ribosome

Transfer RNA

mRNA Codon 5

Codon 4

Codon 3

Codon 2

Codon 1

Codon 5

Codon 4

Codon 3

Codon 2

Codon 1

U A C

Amino acid

Second tRNA and amino acid

G C C U A C

U A C

Third tRNA and amino acid

G C C

AA 1

AA2

AA 2

AA 1

AA3

A U G G A U G G C C U U A

A U G GGC

A U G G C C U U A

Codon 5

Codon 4

Codon 3

Codon 2

Codon 1

▲ Figure 3-8 Assembly of an amino acid chain in protein synthesis.

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What Is a Gene? 57

one amino acid, so do mRNA triplets, which are called codons. Therefore the mRNA strand is “read” in codons, or groups of three mRNA bases at a time (see Table 3-1). Subsequently, another form of RNA, called transfer RNA (tRNA), brings each amino acid to the ribosome. The ribosome then joins that amino acid to another amino acid in the order dictated by the sequence of mRNA codons (or, ultimately, DNA triplets). In this way, amino acids are linked together to form a molecule that will eventually be a protein or part of a protein. But it’s important to men- tion that if a DNA base or sequence of bases is changed through muta- tion, some proteins may not be made or they may be defective. In this case, cells won’t function properly, or they may not function at all.

What Is a Gene?

The answer to this question is com-plicated, and the definition of the term gene is currently the subject of some debate. In the past, textbooks compared genes to a string of beads, with each bead representing one gene on a chromosome. For 50 years or so, biologists considered a gene to be an uninterrupted sequence of DNA bases responsible for the manufacture of a protein or part of a protein. Or, put another way, a gene could be defined as a segment of DNA that specifies the sequence of amino acids in a particular protein. This definition, based on the concept of a one gene‒one protein rela- tionship, was a core principle in biology for decades, but it’s been substantially modified, partly in recognition of the fact that DNA codes not only for pro- teins but also for RNA and other DNA nucleotides.

Moreover, when the human genome was sequenced in 2001, sci- entists determined that humans have only about 25,000 genes (International Human Genome Sequencing Consor- tium, 2001; Venter et al., 2001). This number has now been revised to

approximately 21,000 (Pennisi, 2012). Yet we produce as many as 90,000 pro- teins! Furthermore, protein-coding genes (also called coding sequences), the DNA segments that are tran- scribed into proteins, make up only about 2 to 3 percent of the entire human genome! The rest is composed of noncoding DNA, or what used to be called “junk DNA” (see A Closer Look: Noncoding DNA—Not Junk After All). Thus gene action is much more compli- cated than previously believed and it’s impossible for every protein to be coded for by a specific gene. This shift in perspective is a good example of something we discussed in Chapter 1, that hypotheses and theories can and do change over time as we continue to acquire new knowledge.

Geneticists have also learned that only some parts of genes, called exons, are actually transcribed into mRNA and thus code for specific amino acids. In fact, most of the nucleotide sequences in genes are not expressed during protein synthesis. (By expressed we mean that the DNA sequence is actually making a product.) Many sequences, called introns, are ini- tially transcribed into mRNA and then clipped out (Fig. 3-9). Therefore introns aren’t translated into amino acid sequences. Moreover, the intron segments that are snipped out of a gene aren’t always the same ones. This means that the exons can be combined in different ways to make segments that code for more than one protein. That’s how 21,000 coding sequences can make 90,000 proteins. Genes can also overlap one another, and there can be genes within genes (Fig. 3-10). But they’re still a part of the DNA mole- cule, and it’s the combination of introns

Unit of transcription in DNA strand

Mature mRNA transcript

Intron snipped out Intron snipped out

Transcription into pre-mRNA

Exon Intron Exon Intron Exon

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▲ Figure 3-9 Diagram of a DNA sequence being tran- scribed. The introns are deleted from pre-mRNA before it leaves the cell’s nucleus. The remaining mature RNA contains only exons, which will code for a protein or part of a protein.

codons Triplets of messenger RNA bases that code for specific amino acids during protein synthesis.

transfer RNA (tRNA) A type of RNA that binds to specific amino acids and transports them to the ribosome during protein synthesis.

mutation A change in DNA. The term can refer to changes in DNA bases (specifi- cally called point mutations) as well as to changes in chromosome number and/or structure.

gene A sequence of DNA bases that specifies the order of amino acids in an entire protein, a portion of a protein, or any functional product, such as RNA. A gene may be composed of thousands of DNA bases.

genome The entire genetic makeup of an individual or species. In humans, it’s estimated that the human genome com- prises about 3 billion DNA bases.

noncoding DNA DNA that does not direct the production of proteins. However, such DNA segments produce thousands of molecules (for example, RNA) that are involved in gene regulation. Thus the term noncoding DNA is misleading.

exons Segments of genes that are transcribed and are involved in protein synthesis. (The prefix ex denotes that these segments are expressed.)

introns Segments of genes that are ini- tially transcribed and then deleted. Because introns are not expressed, they aren’t involved in protein synthesis.

Dorine Essumang

chapter 3 The Biological Basis of Life 58

Regulatory Genes

Some genes act solely to control the expression of other genes. Basically these regulatory genes make various kinds of RNA, proteins, and other mol- ecules that switch other DNA segments (genes) on or off. Also, many regulatory genes diminish or enhance the expres- sion of other genes. They play a funda- mental role in embryological develop- ment, cellular function, and evolution. In fact, without them, life as we know it could not exist. The study of regulatory genes and their role in evolution is still in its infancy; but as information about them continues to accumulate, we will eventually be able to answer many of the questions we still have about the evolution of species.

DNA deactivation during embry- onic development is one good exam- ple of how regulatory genes work. As you know, all somatic cells contain the same genetic information; but in any given cell, only a fraction of the DNA is actually involved in protein synthesis. For example, like the cells of the stom- ach lining, bone cells have DNA that codes for the production of digestive enzymes. But bone cells don’t produce digestive enzymes. Instead, they make collagen, the main organic component of bone. This is because cells become

and exons, interspersed along a DNA strand, that makes up the unit we call a gene. So much for beads on a string.

Clearly, the answer to the question “What is a gene?” is complicated, and a completely accurate definition may be a long time coming. However, a pro- posed and more inclusive definition simply states that a gene is “a complete chromosomal segment responsible for making a functional product” (Snyder and Gerstein, 2003).

In spite of all the recently obtained information that has changed some of our views and expanded our knowledge of DNA, there is one fact that doesn’t change. The genetic code is universal, and at least on earth, DNA is the mole- cule that governs the expression, inher- itance, and evolution of biological traits in all forms of life. The DNA of all organisms, from bacteria to oak trees to fruit flies to human beings, is com- posed of the same molecules using the same kinds of instructions. The DNA triplet CGA, for example, specifies the amino acid alanine regardless of spe- cies. These similarities imply biologi- cal relationships between all forms of life—and a common ancestry as well. What makes fruit flies distinct from humans isn’t differences in the DNA material itself, but differences in how that material is arranged and regulated.

Gene

DNA

mRNA after deletion of introns

Mature RNA with segments produced by different exons rearranged into new sequences

Exon 1 Intron 1 Intron 2 Intron 3Exon 2 Exon 3 Exon 4

Exon 1 Exon 2 Exon 3 Exon 1 Exon 2

Exon 2Exon 1 Exon 3 Exon 4

Alternative Splicing

Translation

Protein A Protein B

Exon 4

▶�Figure 3-10 Diagrammatic rep- resentation of how our views of gene function have changed. According to the traditional view, genes are discrete segments of DNA, each coding for a specific protein. (a) We now know that genes are composed of some DNA segments that are expressed (exons), and others that are not (introns). (b) Introns aren’t expressed because they’re deleted during the formation of mRNA. (c) The remaining exons can be rearranged to form several different coding sequences, each of which pro- duces a different protein.

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regulatory genes Genes that influ- ence the activity of other genes. regulatory genes direct embryonic development and are involved in physiological processes throughout life. they are critically important to the evolutionary process.

Dorine Essumang

Regulatory Genes 59

specialized during embryonic devel- opment to perform only certain func- tions, and most of their DNA is perma- nently switched off by regulatory genes. In other words, they become specific types of cells, such as bone cells.

There are thousands of kinds of reg- ulatory genes and one crucially impor- tant group is referred to as homeobox genes. The best known homeobox genes are the Hox genes, which direct the early segmentation of embryonic tissues. They also determine the iden-

tity of individual segments, by speci- fying what they will become, such as part of the head or thorax. Hox genes interact with other genes to deter- mine the characteristics of developing body segments and structures but not their actual development. For example, they determine where, in a develop- ing embryo, limb buds will appear; and they establish the number and overall pattern of the different types of verte- brae, the bones that make up the spine (Fig. 3-11).

Noncoding DNA— Not Junk After All

In all fields of inquiry, important discover-ies always raise new questions that even- tually lead to further revelations. there’s probably no statement that could be more appropriately applied to the field of genet- ics. For example, in 1977, geneticists rec- ognized that during protein synthesis, the initially formed mrNa molecule contains many more nucleotides than are represent- ed in the subsequently produced protein. this finding led to the discovery of introns, portions of genes that don’t code for pro- teins. In the 1980s, geneticists learned that only about 2 percent of human DNa is contained within exons, the segments that actually provide the code for protein synthe- sis. We also know that a human gene can specify the production of as many as three different proteins by using different combi- nations of the exons interspersed within it (pennisi, 2005).

as discussed earlier, with only 2 percent of the human genome directing protein synthesis, humans have more non- protein coding DNa than any other species so far studied. Invertebrates and some vertebrates have only small amounts of noncoding sequences, and yet they’re fully functional organisms. So just what does all

this noncoding DNa (originally called “junk DNa”) do in humans? apparently much of it codes for different forms of rNa that act to regulate gene function, but it does not directly participate in protein synthesis (pennisi, 2012; the eNcODe project con- sortium, 2012).

almost half of all human DNa consists of noncoding segments that are repeated over and over and over. Depending on their length, these segments have been referred to as tandem repeats, satellites, or microsatellites, but now they’re frequently lumped together and called copy number variants (cNVs). Microsatellites have an extremely high mutation rate and can gain or lose repeated segments and then return to their former length. But this tendency to mutate means that the number of repeats in a given microsatellite varies between individuals. and this tremendous variation has been the basis for DNa fingerprint- ing, a technique commonly used to pro- vide evidence in criminal cases. actually, anthropologists are now using microsatellite variation for all kinds of research, from trac- ing migrations of populations to paternity testing in nonhuman primates.

Some of the variations in microsatellite composition are associated with various disorders, so we can’t help wondering why these variations exist. One answer is that some microsatellites influence the activities of protein coding DNa sequences. also, by losing or adding material, they can alter

the sequences of bases in genes, thus becoming a source of mutation in functional genes. and these mutations are a source of genetic variation.

Lastly, there are transposable elements (tes), the so-called jumping genes. these are DNa sequences that can make thou- sands of copies of themselves, which are then scattered throughout the genome. One family of tes, called alu, is found only in primates. about 5 percent of the human genome is made up of alu sequences, and although most of these are shared with other primates, about 7,000 are unique to humans (chimpanzee Sequencing and analysis consortium, 2005).

tes mainly code for proteins that enable them to move about, and because they can land right in the middle of coding sequences (exons), tes cause mutations. Some of these mutations are harmful, and tes have been associated with numerous disease conditions, including some forms of cancer (Deragon and capy, 2000). But at the same time, tes essentially create new exons, thereby generating variations on which natural selection can act. Moreover, they also regulate the activities of many genes, including those involved in develop- ment. So rather than being junk, tes are increasingly being recognized as serving extremely important functions in the evolu- tionary process, including the introduction of genetic changes that have led to the origin of new lineages.

A Closer Look

homeobox genes an evolutionarily ancient family of regulatory genes that directs the development of the overall body plan and the segmentation of body tissues. there are at least 20 families of homeobox genes.

Dorine Essumang

chapter 3 The Biological Basis of Life 60

All homeobox genes are highly conserved, meaning that they’ve been maintained throughout much of evo- lutionary history. They’re present in all invertebrates (such as worms and insects) and vertebrates, and they don’t vary greatly from species to spe- cies. This type of conservation means not only that these genes are vitally important but also that they evolved from genes that were present in some of the earliest forms of life. Moreover, changes in the behavior of homeobox genes are responsible for various physi- cal differences between closely related species or different breeds of domes- ticated animals. For these reasons, homeobox genes, and the many other kinds of regulatory genes, are now a critical area of research in evolutionary and developmental biology.

The finches of the Galápagos Islands provide an excellent example of how regulatory genes influence evo- lutionary change. In Chapter 2, we saw how Charles Darwin came to rec- ognize that variation in these finch- es was an example of natural selec- tion. Scientists have now explained the genetic basis for some of the finch variation by identifying two of the reg- ulatory genes involved in the shape and size of bird beaks (Abzhanov et al., 2004, 2006). One of these genes (also involved in bone formation) is expressed to a greater degree during the embryonic development of wide-

beaked ground fiches than in that of finches with narrower beaks. Likewise, another gene is more active during beak development in finches that have longer, narrower beaks. Therefore the length and width of bird beaks are controlled by the activity of at least two different regulatory genes, allow- ing each aspect of beak size to evolve separately.

There are many other types of highly conserved genes as well. For example, recent sequencing of the sea sponge genome has shown that humans share many genes with sea sponges (Srivastava et al., 2010). This doesn’t mean that sponges were ances- tral to humans, but it does mean that we have genes that were already in existence some 600 mya. These genes ultimately laid the foundation for the evolution of complex animals, and they’re crucial to many of the basic cellular processes that are funda- mental to life today. These processes include a cell’s ability to recognize for- eign cells (immunity), the develop- ment of specific cell types, and signal- ing between cells during growth and development.

We cannot overstate the importance of regulatory genes in evolution. The fact that these genes, with little modi- fication, are present in all complex (as well as in some not so complex) organ- isms, including humans, is the basis of biological continuity between species.

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▲�Figure 3-11 The differences in these three vertebrae, from different regions of the spine, are caused by the action of Hox genes during embryonic development. (a) The cervical (neck) vertebrae have characteristics that dif- ferentiate them from (b) thoracic ver- tebrae, which are attached to the ribs, and also from (c) lumbar vertebrae of the lower back. Hox genes determine the overall pattern not only of each type of vertebra but also of each indi- vidual vertebra.

Mutation: When Genes Change 61

Mutation: When Genes Change

The best way to understand how genes function is to see what hap- pens when they change, or mutate. Normal adult hemoglobin is made up of four amino acid chains (two alpha chains and two beta chains) that are the direct products of gene action. Each beta chain is in turn composed of 146 amino acids. There are several hemoglobin disorders with genetic ori- gins, and perhaps the best known of these is sickle-cell anemia, which results from a defect in the beta chain. People with sickle-cell anemia inherit, from both parents, a mutated form of the gene that directs the formation of the beta chain. This mutation is caused by the substitution of one amino acid (valine) for the amino acid that’s nor- mally present (glutamic acid). This sin- gle amino acid substitution on the beta chain results in the production of a less efficient form of hemoglobin called hemoglobin S (HbS) instead of the nor-

mal form, which is called hemoglobin A (HbA). In situations where the avail- ability of oxygen is reduced, such as at high altitude or when oxygen require- ments are increased through exer- cise, red blood cells with HbS collapse and become sickle-shaped (Fig. 3-12). What follows is a cascade of events, all of which result in severe anemia and its consequences (Fig. 3-13). Briefly, these consequences include impaired cir- culation from blocked capillaries, red blood cell destruction, oxygen depri- vation to vital organs (including the brain), and, without treatment, death.

People who inherit the altered form of the gene from only one parent don’t have sickle-cell anemia, but they do have what’s called sickle-cell trait. Fortunately for them, they’re much less severely affected because only about 40 percent of their hemoglobin is abnormal.

The cause of sickle-cell ane- mia is a very slight change in the Hb gene. Remember that hemoglo- bin beta chains each have 146 amino acids. What’s more, to emphasize the

Coding and Noncoding DNA

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Coding DNA Noncoding DNA

codes for sequences of amino acids (i.e., functional proteins) or rNa molecules

Function not well known, but some (perhaps many) noncoding segments regulate the activities of protein- coding genes. this terminology may change as more discoveries are made.

comprises approximately 2% of human nuclear DNa

comprises about 98% of human nuclear DNa

Includes exons within functional genes Includes introns within functional genes and multiple repeated segments elsewhere on chromosomes

At a Glance

sickle-cell anemia a severe inherited hemoglobin disorder in which red blood cells collapse when deprived of oxygen. It results from inheriting two cop- ies of a mutant allele. the type of mutation that produces the sickle-cell allele is a point mutation.

chapter 3 The Biological Basis of Life 62

importance of a seemingly minor alter- ation, consider that triplets of DNA bases are required to specify amino acids. Therefore it takes 438 bases (146 × 3) to produce the chain of 146 amino acids that forms the adult hemoglobin beta chain. But a change in only one of these 438 bases produces the life- threatening complications seen in sick- le-cell anemia. Figure 3-14 shows the DNA base sequence and the resulting amino acid products for both normal and sickling hemoglobin. As you can see, a single base substitution (from CTC to CAC) can result in an altered amino acid sequence, from

. . . proline—glutamic acid—glutamic acid . . .

to . . . proline—valine—glutamic acid . . .

This kind of change in the genetic code is referred to as a point mutation or base substitution. In evolution, these changes are important sources of new genetic variation in populations. Point mutations, like the one that causes sickle-cell anemia, probably occur fair- ly frequently. But for a new mutation to be evolutionarily significant, it must be passed on to offspring and eventually become more common in a population.

▶�Figure 3-12 Scanning electron micrographs of (a) a normal, fully oxy- genated red blood cell and (b) a col- lapsed, sickle-shaped red blood cell that contains HbS.

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Decreased lung

capacity Paralysis Kidney

failure

Slight changes in skull bones

Impaired mental

function Heart failure

Impaired musculoskeletal

function

Abdominal pain

Enlargement, then fibrosis

of spleen

Lung damage

Clumping of cells and interference with blood circulation

Sickling of red blood cells

Abnormal hemoglobin

Collection of sickle cells in the spleen

Fewer functional red blood cells

Anemia Local failures in blood supply

Heart damage

Muscle and joint damage

Gastrointestinal tract damage

Brain damage

Kidney damage

Dilation of heartIncrease in amount

of bone marrow

Overactivity of bone marrow

Weakness and fatigue

Poor physical development

A Person With Two Mutated Genes for the Hemoglobin Beta Chains

▼�Figure 3-13 Diagram showing the cascade of symptoms that can occur in people with sickle-cell anemia.

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Chromosomes 63

Once point mutations occur, their fate in populations depends on the other evolutionary forces, especially natural selection. Depending on how benefi- cial a mutation is, it may become more common over time; if it’s disadvanta- geous, it probably won’t. Sickle-cell ane- mia is one of the best examples of natu- ral selection acting on humans; it shows us how a disadvantageous mutation can become more frequent in certain envi- ronments. This last point will be con- sidered in Chapter 4.

Chromosomes

Throughout much of a cell’s life, its DNA (all 6 feet of it!) directs cellu- lar functions and exists as an uncoiled, granular substance. However, at vari- ous times in the life of most types of cells, normal activities cease and the cell divides. Cell division produces

new cells, and at the beginning of this process, the DNA becomes tightly coiled and is visible under a micro- scope as a set of discrete structures called chromosomes (Fig. 3-15).

Chromosomes are composed of a DNA molecule and proteins (Fig. 3-16). During normal cell func- tion, if the DNA were organized into chromosomes, they would be single- stranded structures. However, during the early stages of cell division when they become visible, they’re made up of two strands, or two DNA mole- cules, joined together at a constricted area called the centromere. The rea- son there are two strands is simple: The DNA molecules have replicat- ed, and one strand is an exact copy of the other.

Every species has a specific num- ber of chromosomes in somatic cells (Table 3.2). Humans have 46, while chimpanzees and gorillas have 48. This

Point Mutation

Normal Hemoglobin

DNA sequence Amino acid

• • • • • T G A

G G A

C T C

T T T • • • • •

#4 Threonine

#5 Proline

#6 Glutamic acid

#7 Glutamic acid

#8 Lysine

• • • • • #146

Sickling Hemoglobin

Amino acid DNA sequence

#4 Threonine

#5 Proline

#6 Valine

#7 Glutamic acid

#8 Lysine

• • • • • #146

• • • • • T G A

G G A

C A C

C T C

T T T • • • • •

#1652 #1652 (including intron sequences)

◀�Figure 3-14 Substitution of one base at position 6 produces sickling hemoglobin.

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point mutation a change in one of the four DNa bases.

chromosomes Discrete structures composed of DNa and proteins found only in the nuclei of cells. chromosomes are vis- ible under magnification only during certain phases of cell division.

chapter 3 The Biological Basis of Life 64

doesn’t mean that humans have less DNA than chimpanzees and gorillas. It just means that the DNA is packaged differently.

There are two basic types of chro- mosomes: autosomes and sex chromosomes. Autosomes carry information that governs all physi-

cal characteristics except primary sex determination. The two sex chromo- somes are the X and Y chromosomes; in mammals, the Y chromosome is directly involved in determining male- ness. Although the X chromosome is called a sex chromosome, it actu- ally functions more like an autosome

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▶�Figure 3-15 Colorized scan- ning electronmicrograph of human chromosomes.

autosomes all chromosomes except the sex chromosomes.

sex chromosomes In mammals, the X and Y chromosomes.

Table 3.2 Standard Chromosomal Complement in Various Organisms

Organism

Chromosome Number in Somatic Cells

Chromosome Number in Gametes

Human (Homo sapiens) 46 23

Chimpanzee (Pan troglodytes)

48 24

Gorilla (Gorilla gorilla) 48 24

Dog (Canis familiaris) 78 39

Chicken (Gallus domesticus) 78 39

Frog (Rana pipiens) 26 13

Housefly (Musca domestica) 12 6

Onion (Allium cepa) 16 8

Corn (Zea mays) 20 10

Tobacco (Nicotiana tabacum) 48 24

Source: Cummings, 2000, p. 16.

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Chromosomes 65

because it’s not involved in primary sex determination and it influences sev- eral other traits. Among mammals, all genetically normal females have two X chromosomes (XX), and they’re female only because they don’t have a Y chro- mosome. (Female is the default set- ting.) All genetically normal males have one X and one Y chromosome (XY).

Chromosomes occur in pairs, so all normal human somatic cells have 22 pairs of autosomes and one pair of sex chromosomes (23 pairs in all). With few exceptions, abnormal numbers of autosomes are fatal—usually soon after conception. Although abnormal num- bers of sex chromosomes aren’t usual- ly fatal, they may result in sterility and frequently have other consequences. So to function normally, it’s essential for a

human cell to possess both members of each chromosomal pair, or a total of 46 chromosomes.

Offspring inherit one member of each chromosomal pair from the father (the paternal chromosome) and one member from the mother (the mater- nal chromosome). Members of chro- mosomal pairs are alike in size and position of the centromere, and they carry genetic information governing the same traits. However, this doesn’t mean that partner chromosomes are genetically identical; it just means that they influence the same traits. For example, on both copies of a person’s ninth chromosome, there’s a locus, or gene position, that determines which of the four ABO blood types (A, B, AB, or O) he or she will have. However, these

A A

G G

T A

T C

A T

AC G

C T

Each of the more than 1 trillion somatic cells in the body consists of a cell membrane, cytoplasm, and a nucleus.

(d) To form the chromosome, the DNA is coiled into higher and higher levels of organization.

(f) A specific sequence of nucleotide base pairs constitutes a gene.

(a) Each somatic cell nucleus contains 46 chromosomes— 23 contributed by the mother and 23 by the father. The chromosomes consist of protein and DNA.

(c) A chromosome consists of two DNA molecules joined at a constricted area called the centromere. A chromosome is seen in this form only during cell division.

(e) The DNA is coiled around specialized proteins that provide structure to the chromosome. These proteins also interact with the DNA.

◀�Figure 3-16 A model of a human chromosome illustrating the relation- ship of DNA to chromosomes.

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locus (pl., loci) (lo’-kus, lo-sigh’) the position or location on a chromo- some where a given gene occurs. the term is sometimes used interchangeably with gene.

chapter 3 The Biological Basis of Life 66

two ninth chromosomes might not have identical DNA segments at the ABO locus. In other words, at numer- ous genetic loci, there may be more than one possible form of a gene, and these different forms are called alleles (Fig 3-17).

Alleles are alternate forms of a gene that can direct the cell to pro- duce slightly different forms of a prod- uct, and ultimately, different expres-

sions of a trait—as in the hemoglobin S (HbS) example. At the ABO locus, there are three possible alleles: A, B, and O. However, since individuals have only two ninth chromosomes, only two alleles are present in any one person. And the variation in alleles at the ABO locus is what accounts for the variation among humans in ABO blood type.

Karyotyping Chromosomes One method frequently used to exam- ine chromosomes in an individual is to produce a karyotype. (An exam- ple of a human karyotype is shown in Fig. 3-18.) The chromosomes used in karyotypes are obtained from divid- ing cells. White blood cells can be cul- tured, chemically treated, and micro- scopically examined to identify the ones that are dividing. These cells are then photographed through a micro- scope to produce photomicrographs of intact, double-stranded chromo- somes. Partner chromosomes are then matched up, and the entire set is arranged in descending order by size so that the largest chromosome appears first.

Karyotyping has had numerous practical applications. Physicians and

Members of a pair of chromosomes. One chromosome is from a male parent, and its partner is from a female parent.

Gene locus. The location for a specific gene on a chromosome.

Pair of alleles. Although they influence the same characteristic, their DNA varies slightly, so they produce somewhat different expressions of the same trait.

Three pairs of alleles (at three loci on this pair of chomosomes). Note that at two loci the alleles are identical (homozygous), and at one locus they are different (heterozygous).

▶�Figure 3-17 As this diagram illus- trates, alleles are located at the same locus on paired chromosomes, but they aren’t always identical.

▼�Figure 3-18 A karyotype of a human male with the chromosomes arranged by size, position of the cen- tromere, and banding patterns.

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alleles alternate forms of a gene. alleles occur at the same locus on paired chromosomes and thus govern the same trait, but because they’re different, their action may result in different expressions of that trait.

karyotype the chromosomes of an individual, or what is typical of a species, viewed microscopically and displayed in a photograph. the chromosomes are arranged in pairs and according to size and position of the centromere.

mitosis Simple cell division; the process by which somatic cells divide to produce two identical daughter cells.

meiosis cell division in specialized cells in ovaries and testes. Meiosis involves two divisions and results in four daughter cells, each containing only half the original number of chromosomes. these cells can develop into gametes.

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Cell Division 67

genetic counselors use karyotypes to help diagnose chromosomal disorders in patients, and they’re used in prena- tal testing to identify chromosomal abnormalities in developing fetuses. Karyotype analysis has also revealed many chromosomal similarities shared by different species, including humans and nonhuman primates. But, now that scientists can directly compare the genomes of species, karyotyping prob- ably won’t continue being used for this or several other purposes.

Cell Division

As we mentioned earlier, normal cellular function is periodically interrupted so that the cell can divide. Cell division in somatic cells is called mitosis, and it’s the way somatic cells reproduce. Mitosis occurs during growth and development; it also plays a role in the repair of injured tissues; and it replaces older cells with newer ones. But while mitosis produces new somatic cells, another type of cell division, called meiosis, may lead to the development of new individuals, since it produces reproductive cells, or gametes.

Mitosis In the early stages of mitosis, a human somatic cell has 46 double-stranded chromosomes, and as the cell begins to divide, these chromosomes line up along its center and split apart so that the two strands separate (Fig. 3-19). Once the two strands are apart, they pull away from each other and move to opposite ends of the dividing cell. At this point, each strand is a dis- tinct chromosome, composed of one DNA molecule. Following the sepa- ration of chromosome strands, the cell membrane pinches in and seals, so that there are two new cells, each with a full complement of DNA, or 46 chromosomes.

Mitosis is referred to as “simple cell division” because a somatic cell divides

The cell is involved in metabolic activities. DNA replication occurs, but chromosomes are not visible.

The nuclear membrane disappears, and double- stranded chromosomes are visible.

The chromosomes align themselves at the center of the cell.

The chromosomes split at the centromere, and the strands separate and move to opposite ends of the dividing cell.

The cell membrane pinches in as the cell continues to divide. The chromosomes begin to uncoil (not shown here).

After mitosis is complete, there are two identical daughter cells. The nuclear membrane is present, and chromosomes are no longer visible.

◀�Figure 3-19 Diagrammatic representa- tion of mitosis. The blue images next to some of these illustrations are photomicrographs of actual chromosomes in a dividing cell.

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chapter 3 The Biological Basis of Life 68

one time to produce two daughter cells that are genetically identical to each other and to the original cell. In mitosis, the original cell possesses 46 chromosomes, and each new daugh- ter cell inherits an exact copy of all 46. This precision is made possible by the DNA molecule’s ability to replicate. Therefore DNA replication ensures that the amount of genetic material remains constant from one generation of cells to the next.

We should mention here that cer- tain types of somatic cells don’t divide. Red blood cells are produced continu- ously by specialized cells in bone mar- row, but they can’t divide because they have no nucleus and no nuclear DNA. Once the brain and nervous system are fully developed, brain and nerve cells (neurons) stop dividing, although there is some debate about this issue. Liver cells also do not divide after growth has stopped unless this vital organ is damaged through injury or disease. With these three exceptions (red blood cells, mature neurons, and liver cells), somatic cells are regularly duplicated through the process of mitosis.

Meiosis While mitosis produces new cells, mei- osis can lead to the development of a new organism because it produces reproductive cells (gametes). Although meiosis is similar to mitosis, it’s more complicated. In meiosis, there are two divisions instead of one. Also, meio- sis produces four daughter cells, not two, and each of these four cells con- tains only half the original number of chromosomes.

During meiosis, specialized cells in male testes and female ovaries divide and eventually develop into sperm and egg cells. Initially, these cells contain the full complement of chromosomes (46 in humans); but after the first divi- sion (called reduction division), the number of chromosomes in the two daughter cells is 23, or half the original number (Fig. 3-20). This reduction of chromosome number is crucial because

the resulting gamete, with its 23 chro- mosomes, may eventually unite with another gamete that also has 23 chro- mosomes. The product of this union is a zygote, or fertilized egg, in which the original number of chromosomes (46) has been restored. In other words, a zygote inherits the exact amount of DNA it needs (half from each parent) to develop and function normally. If it weren’t for reduction division in meio- sis, it wouldn’t be possible to maintain the correct number of chromosomes from one generation to the next.

During the first division, part- ner chromosomes come together to form pairs of double-stranded chro- mosomes that line up along the cell’s center. Pairing of partner chromo- somes is essential because while they’re together, members of pairs exchange genetic information in a process called recombination. Pairing is also impor- tant because it ensures that each new daughter cell receives only one member of each pair.

As the cell begins to divide, the chromosomes themselves remain intact (that is, double-stranded), but members of pairs pull apart and move to opposite ends of the cell. After the first division, there are two new daughter cells, but they aren’t iden- tical to each other or to the parental cell. They’re different because each cell contains only one member of each chromosome pair (that is, only 23 chromosomes), each of which still has two strands. Also, because of recom- bination, each chromosome now con- tains some combinations of alleles it didn’t have before.

The second meiotic division is simi- lar to division in mitosis. (For a com- parison of mitosis and meiosis, see Fig. 3-21.) In the two newly formed cells, the 23 double-stranded chro- mosomes line up at the cell’s center and, as in mitosis, the strands of each chromosome separate and move apart. Once this second division is completed, there are four daughter cells, each with 23 single-stranded chromosomes, or 23 DNA molecules.

recombination the exchange of genetic material between paired chro- mosomes during meiosis; also called crossing over.

Cell Division 69

Chromosomes are not visible as DNA replication occurs in a cell preparing to divide.

Double-stranded chromosomes become visible, and partner chromosomes exchange genetic material in a process called recombination or crossing over.

Chromosome pairs migrate to the center of the cell.

First Division (reduction division) Partner chromosomes separate, and members of each pair move to opposite ends of the dividing cell. This results in only half the original number of chromosomes in each new daughter cell.

After the first meiotic division, there are two daughter cells, each containing only one member of each original chromosomal pair, or 23 nonpartner chromosomes.

Second Division

In this division, the chromosomes split at the centromere, and the strands move to opposite sides of the cell.

After the second division, meiosis results in four daughter cells. These may mature to become functional gametes, containing only half the DNA in the original cell.

A t c e o

Detailed representation of results of exchange of genetic material during recombination. of genetic material d recombination.

In th o

◀�Figure 3-20 Diagrammatic representation of meiosis.

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chapter 3 The Biological Basis of Life 70

The Evolutionary Significance of Meiosis Meiosis occurs in all sexually repro- ducing organisms and is an extremely important evolutionary innovation because it increases genetic variation in populations. Members of sexually reproducing species aren’t genetically identical clones of other individuals because they receive genetic contribu- tions from two parents. Just from the random assortment of chromosome pairs during the first division of meio- sis, each parent can produce around 8 million genetically different gametes. In human matings, literally trillions of genetic combinations can result in the offspring of two parents. Consequently every individual represents a unique combination of genes that, in all like- lihood, has never occurred before and will never occur again.

As you can see, genetic diversity is considerably enhanced by meiosis, and this diversity is essential if species are to adapt to changing selective pres- sures. As we mentioned in Chapter 2, natural selection acts on genetic varia- tion in populations; thus if all individ- uals were genetically identical, natu- ral selection would have nothing to act

upon and evolution couldn’t occur. In all species, mutation is the only source of new genetic variation because it pro- duces new alleles. But sexually repro- ducing species have an additional advantage because recombination pro- duces new arrangements of genetic information, potentially providing additional material for selection to act on. In fact, the influence of meiosis on genetic variation is the main advantage of sexual reproduction. Thus, sexual reproduction and meiosis are of major evolutionary importance because they contribute to the role of natural selec- tion in populations.

Problems with Meiosis For fetal devel- opment to occur normally, the process of meiosis must be exact. If chromo- somes or chromosome strands don’t separate during either of the two divi- sions, serious problems can develop. This failure to separate is called non- disjunction; when it happens, one of the daughter cells receives two copies of the affected chromosome while the other daughter cell receives none. If such an affected gamete unites with a normal gamete containing 23 chromo-

▲�Figure 3-21 Mitosis and meiosis compared. In mitosis, one division produces two daughter cells, each of which contains 46 chromosomes. In meiosis, there are two divisions. After the first, there are two cells, each containing only 23 chromosomes (one member of each original chromosome pair). Each daughter cell divides again, so that the final result is four cells, each with only half the original number of chromosomes.

223 23

46 46 chromosomes (single-stranded)

46 46 double-stranded chromosomes arranged into 23 pairs

Two daughter cells, each containing 23 double-stranded chromosomes (one member of each pair)

Four daughter cells, each containing 23 single-stranded chromosomes

Four each 23 s chro

233 23 23

46 double-stranded chromosomes

46 chromosomes (single-stranded)

4646

46 do chrom46

46 ch (sing46

Replication

Two daughter cells, each containing 46 single-stranded chromosomes

First Cell Division (reduction division)

Second Cell Division

Cell Division

Mitosisa Meiosisb

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clones Organisms that are genetically identical to another organism. the term may also be used to refer to genetically identical DNa segments, molecules, or cells.

random assortment the chance distribution of chromosomes to daughter cells during meiosis. along with recombina- tion, random assortment is an important source of genetic variation (but not new alleles).

Dorine Essumang

New Frontiers 71

somes, the resulting zygote will have either 45 or 47 chromosomes. If there are 47, then there will be three copies of one chromosome instead of two, a situ- ation called trisomy.

You can appreciate the potential effects of an abnormal number of chro- mosomes if you remember that the zygote, by means of mitosis, ultimately gives rise to all the cells in the devel- oping body. Consequently every one of those cells will inherit an incorrect number of chromosomes. And since most abnormal numbers of autosomes are lethal, the embryo is usually spon- taneously aborted, frequently before the pregnancy is even recognized.

Trisomy 21 (formerly called Down syndrome) is the only example of an incorrect number of autosomes that’s compatible with life beyond the first few years after birth. Trisomy 21 is caused by the presence of three copies of chromosome 21. It occurs in approx- imately 1 out of every 1,000 live births and is associated with various devel- opmental and health problems. These problems include congenital heart defects (seen in about 40 percent of affected newborns) as well as increased susceptibility to respiratory infections and leukemia. However, the most wide- ly recognized effect is mental impair- ment, which is variably expressed and ranges from mild to severe.

Trisomy 21 is partly associated with advanced maternal age. For example, the risk of a 20-year-old woman giv- ing birth to an affected infant is just 0.05 percent (5 in 10,000). However, 3 percent of babies born to mothers aged 45 and older are affected (a 60-fold increase). Actually, most affected infants are born to women under the age of 35, but that’s because the major- ity of women who have babies are less than 35 years old. The increased preva- lence of trisomy 21 with maternal age is thought to be related to the fact that meiosis actually begins in females dur- ing their own fetal development and then stops, only to be resumed and completed at ovulation. This means that a woman’s gametes are as old as she is, and age-related changes in the

chromosomes themselves appear to increase the risk of nondisjunction, at least for some chromosomes.

Nondisjunction also occurs in sex chromosomes (see Table 3.3). For example, a man may have two X chro- mosomes and one Y chromosome (XXY) or one X chromosome and two Y chromosomes (XYY). Likewise, a woman may have only one X chro- mosome (X0), or she may have more than two (XXX). Although abnormal numbers of sex chromosomes don’t always result in spontaneous abor- tion or death, they can cause sterility, some mental impairment, and other problems. And while it’s possible to live without a Y chromosome ( roughly half of all people do), it’s impossible for an embryo to survive without an X chromosome. (Remember, X chromo- somes carry genes that influence many traits.) Clearly normal development depends on having the correct number of chromosomes.

New Frontiers

Since the discovery of DNA struc-ture and function in the 1950s, the field of genetics has revolutionized biological science and reshaped our understanding of inheritance, genetic disease, and evolutionary processes. For example, a technique developed in 1986, called polymerase chain reac- tion (PCR), enables scientists to make thousands of copies of small samples of DNA, which can then be analyzed. In the past, DNA samples from crime scenes or fossils were usually too small to be studied. But PCR makes it pos- sible to examine DNA sequences in, for example, Neandertal fossils and Egyp- tian mummies, and it has limitless potential for many disciplines, includ- ing forensic science, medicine, and paleoanthropology.

Another application of PCR allows scientists to identify DNA fingerprints, so called because they appear as pat- terns of repeated DNA sequences that are unique to each individual (Fig. 3-22 on p. 73). For example, one person

polymerase chain reaction (PCR) a method of producing thousands of copies of a DNa sample.

chapter 3 The Biological Basis of Life 72

might have a segment of six bases such as ATTCTA repeated 3 times, while another person might have 20 copies of the same sequence. DNA finger- printing is perhaps the most powerful tool available for human identification. Scientists have used it to identify scores of remains, including members of the Russian royal family murdered in 1918 and victims of the September 11, 2001, terrorist attacks. Moreover, the tech- nique has been used to exonerate many innocent people wrongly convicted of crimes, in some cases decades after they were imprisoned.

Over the last two decades, scientists have used the techniques of recombi- nant DNA technology to transfer genes from the cells of one species into those of another. One common method has been to insert human genes that direct the production of various pro- teins into bacterial cells in laborato- ries. The altered bacteria can then pro- duce human gene products, such as insulin. Until the early 1980s, people with diabetes relied on insulin derived from nonhuman animals. However, this insulin wasn’t plentiful, and some patients became allergic to it. But since

1982, abundant supplies of human insulin, produced by bacteria, have been available, and insulin derived from bacteria doesn’t cause allergic reactions.

In recent years, genetic manipulation has become increasingly controversial owing to questions related to product safety, environmental concerns, animal welfare, and concern over the experi- mental use of human embryos. For example, the insertion of bacterial DNA into certain crops has made them toxic to leaf-eating insects, thus reducing the need for pesticides. Cattle and pigs are commonly treated with antibiotics and genetically engineered growth hormone to increase growth rates. (There’s no concrete evidence that humans are sus- ceptible to the insect-repelling bacteri- al DNA or harmed by consuming meat and dairy products from animals treat- ed with growth hormone. But there are concerns over the unknown effects of long-term exposure.)

Cloning has been one of the most controversial of all the new genetic technologies. But cloning isn’t as new as you might think. Anyone who has ever taken a cutting from a plant and rooted it to grow a new one has produced a

Table 3.3 Examples of Nondisjunction in Sex Chromosomes Chromosomal Complement

Condition

Estimated Incidence

Manifestations

XXX Trisomy X 1 per 1,000 female births Affected women are usually clinically normal, but there is a slight increase in sterility and mental impairment compared to the general population. In cases with more than three X chromosomes, mental impairment can be severe.

XYY XYY syndrome 1 per 1,000 male births Affected males are fertile and tend to be taller than average.

XO Turner syn- drome

1 per 10,000 female births Affected females are short-statured, have broad chests and webbed necks, and are sterile. There is usually no mental impairment, but concepts relating to spatial relationships, including mathematics, can pose difficul- ties. Between 95 and 99 percent of affected fetuses die before birth.

XXY Klinefelter syn- drome

1 per 1,000 male births Symptoms are noticeable by puberty: reduced testicu- lar development, reduced facial and body hair, some breast development in about half of all cases, and reduced fertility or sterility. Some individuals exhibit lowered intelligence. Additional X chromosomes (XXXY) are associated with mental impairment.

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Dorine Essumang

New Frontiers 73

clone. Many mammalian species have now been cloned, and researchers have even produced clones of dead mice that were frozen for as long as 16 years. This gives rise to hopes that eventu- ally it may be possible to clone extinct animals, such as mammoths, from the frozen bodies of animals that died sev- eral thousand years ago (Wakayama et al., 2008). But don’t count on visiting a Jurassic Park type zoo anytime soon.

As exciting as these innovations are, probably the single most impor- tant advance in genetics has been the progress made by the Human Genome Project (International Human Genome Sequencing Consortium, 2001; Venter et al., 2001). The goal of this interna- tional effort, begun in 1990, was to sequence the entire human genome, which consists of some 3 billion bases making up approximately 21,000 protein-coding genes. This extremely important project was completed in 2003. Since that time, the genomes of hundreds of species have been sequenced, including those of chim- panzees (Chimpanzee Sequencing and Analysis Consortium, 2005), rhesus macaques (Rhesus Macaque Genome Sequencing and Analysis Consortium, 2007), western lowland gorillas (Scally et al., 2012), Orangutans (Locke et al., 2011), and bonobos (Prüfer et al., 2012). By comparing different primate genomes, including that of humans, molecular anthropologists are reveal- ing more details regarding phylogenetic relationships among all primate species.

Since the publication of the human genome, DNA sequencing technolo- gies have become increasingly inexpen- sive, more widely available, and much faster. In May 2010, researchers fin- ished sequencing the entire Neandertal genome (Green et al., 2010). To date, the most exciting announcement stem- ming from this research is that mod- ern Europeans and Asians (but not Africans) inherited 1 to 4 percent of their genes from ancient Neandertal ancestors. This finding sheds light on debates concerning whether or not early modern humans interbred with Neandertals. These debates have been

ongoing in physi- cal anthropology for more than 50 years, and while this new genetic evidence does not conclusively end the discussion, it strongly supports the argument that inter- breeding did indeed take place and that many of us carry a few Neandertal genes (see Chapter 13).

Equally exciting was the sequencing of the entire genome of another pre-modern human group called the Denisovans (Reich et al., 2010; Meyer et al., 2012). This group is dated to around 50,000 ya and the entire col-lection of Denisovan skeletal remains consists of a tiny finger bone and two teeth discovered in Siberia. Yet, in a feat that would have been unimagina- ble just ten years ago, researchers have been able to obtain high quality DNA from the finger bone and sequence the entire genome of this population! The Denisovan genome has now been compared to that of their Neandertal cousins and to the genomes of modern human populations (see Chapter 12).

Eventually, comparative genome analysis should provide a thorough assessment of genetic similarities and differences and thus of the evolution- ary relationships between humans and other primates. What’s more, we can already look at human varia- tion in an entirely different light than was possible just 10 years ago (see Chapter 15). Among other things, genetic comparisons between human groups can inform us about popu- lation movements in the past and what selective pressures may have been exerted on different popula- tions to produce some of the variabil- ity we see.

▲�Figure 3-22 Eight DNA finger- prints, one of which is from a blood sample left at an actual crime scene. The other seven are from suspects. By comparing the banding patterns, it’s easy to identify the guilty person.

① ② ➂ ➃ ➄ ➅ ➆From blood at crime scene

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Human Genome Project an international effort aimed at sequencing and mapping the entire human genome, completed in 2003.

Dorine Essumang

chapter 3 The Biological Basis of Life 74

The Encyclopedia of DNA Elements, or ENCODE, is a project initially con- ceived to follow up on the progress made by the Human Genome Project. This huge study, begun in 2003, now involves an international consortium of more than 400 researchers who, in September 2012, simultaneously pub- lished 30 articles in several scientific journals. Initially, the project set out to catalog the functional DNA sequences contained within the vast stretches of non-protein coding DNA, determine what they do, and examine how the human genome is regulated (Maher, 2012; Pennisi, 2012; The ENCODE Project Consortium, 2012).

The current results of the ENCODE project are far too numerous to men- tion here. But the some of the most important ones include the discov- ery that as much as 80 percent of the human genome is involved in some form of biochemical function. That estimate may be high and most of the biochemical functions have not been identified. In fact, some of them are probably not even important. But some of these activities include the manu- facture of non-coding RNA (RNA that is not involved in protein syn- thesis but that regulates gene func- tion), and binding sites where regula- tory proteins attach, In short, some of what used to be called “junk DNA” is active in gene regulation. It is also of great interest that many regulatory fac-

tors have been shown to be involved in disease, including autoimmune con- ditions such as rheumatoid arthritis, Crohn’s disease, and multiple sclerosis (Maurano, et al., 2012). This discovery will radically alter future approaches to the diagnosis and treatment of geneti- cally caused diseases.

The ENCODE project has deter- mined that at least 9 percent (and probably much more) of the human genome has regulatory functions. It has also determined that the regula- tion of protein coding genes is more complex and has evolved more quickly in humans than in most other species. Moreover, evolution occurs more rap- idly in regulatory elements. These facts may partly explain the acceler- ated pace of evolutionary change in modern humans compared to that of other animals. Ultimately the detailed understanding of how gene regulation works will revolutionize how we view evolutionary processes. The focus of many genetic and evolutionary stud- ies will shift away from protein cod- ing genes and toward regulatory ele- ments. The factors that regulate gene activity in embryonic development are also the basis of evolutionary change. It follows that if we are going to reveal the secrets of our evolutionary past, we must first examine how DNA function is regulated in the present. Certainly the term “junk DNA” will be laid to rest.

There are thousands of DNA coding sequences (genes) that have functions which have not been identified. One way geneticists determine what specific genes do is to study what happens when they aren’t functioning. Using various techniques, scientists can insert prod- ucts into mouse embryos very early in development. These products can then “knock out” a target gene so that it doesn’t function. This means that virtually every cell in the developing embryo will have a disabled gene at the locus under investigation. Then, when these knockout mice are born, the results can be detected.

One of the many uses of knockout mice has been to identify which Hox genes influence the develop- ment of specific vertebrae. This information has many

clinical applications because the Hox genes that deter- mine vertebral identity in mice have human counter- parts. Therefore many defects of the spine can now be traced to the gain, loss, or alteration of the function of specific genes during early embryonic development. Subsequent investigations can then search for causes of gene malfunction, including substances in the envi- ronment or in food that might influence DNA activity in embryos. For example, it is known that vitamin A can attach to DNA and cause vertebral anomalies. In the future, it is likely that many developmental defects will be detected and treated very early in embryonic development, partly because of the use of knockout techniques.

How Do We Know?

Dorine Essumang

75Media Resources

Summary of Main Topics

▶▶ Cells are the fundamental units of life, and in multicellular organisms, there are basically two types. Somatic cells make up body tissues, while gametes (eggs and sperm) are reproduc- tive cells that transmit genetic information from parents to offspring.

▶▶ Genetic information is con- tained in the DNA molecule, found in the nucleus of cells and in mitochondria. The DNA molecule is capable of replica- tion, or making copies of itself. Replication makes it possible for daughter cells to receive a full complement of DNA (con- tained in chromosomes). DNA also controls protein synthesis by directing the cell to arrange amino acids in the proper sequence for each protein. Also involved in the process of pro- tein synthesis is another, simi- lar molecule called RNA.

▶▶ There are many genes that regulate the function of other genes. One class of regulatory genes, the homeobox genes, direct the development of the overall body plan. Other reg- ulatory genes turn genes on and off.

▶▶ Cells multiply by dividing and when they do, the DNA within them is visible microscopically in the form of chromosomes. In humans, there are 46 chro- mosomes (23 pairs). If the full complement isn’t precisely dis- tributed to succeeding genera- tions of cells, there can be seri- ous consequences.

▶▶ Somatic cells divide dur- ing growth or tissue repair or to replace old worn-out cells. Somatic cell division is called mitosis. A cell divides one time to produce two daughter cells, each possessing a full and iden- tical set of chromosomes.

▶▶ Sex cells are produced when specialized cells in the ovaries and testes divide during meio- sis. Unlike mitosis, meiosis is characterized by two divisions that produce four nonidentical daughter cells, each containing only half the amount of DNA (23 chromosomes).

▶▶ About 98 percent of our DNA doesn’t actually code for pro- tein production.

▶▶ Some noncoding sequences, called introns, are contained within genes. Introns are ini- tially transcribed into mRNA but are then deleted before the mRNA leaves the cell nucleus.

▶▶ A high percentage of non- protein coding DNA is involved in gene regulation. In fact, humans have more regulatory DNA than any other species so far studied.

1. Before you read this chapter, were you aware that the DNA in your body is structurally the same as that in all other organisms? Do you see this fact as having potential to clarify some of the many ques- tions we still have regarding biological evolution? Why?

2. Do you think proteins are exactly the same in all species? If not, how do you think they would dif- fer in terms of their composition, and why might

these differences be important to biological anthropologists?

3. How can regulatory genes, especially Hox genes, play an important role in biological evolution?

Video See the video “Natural Selection in Action”

to learn more about topics covered in this chapter. Login to your Anthropology CourseMate at www.cengagebrain.com to access videos.

Critical Thinking Questions

Media Resources

Connections

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Evolution occurs when DNA changes and genetic variation is further influenced by natural

selection and other factors. DNA is the basis

of all life.

Humans are both vertebrates and

mammals and we’ve shared evolutionary history for millions

of years.

After mastering the material in this chapter, you should be able to:

▶ Explain the principles of inheritance, first discovered by Gregor Mendel.

▶ Explain why, when Mendel did his experiments with pea plants, he observed three tall plants for every short plant in the F2 generation.

▶ Describe how dominant and recessive traits are inherited and how these modes of inheritance differ from one another.

▶ Summarize why mutation is important to the evolutionary process.

▶ Discuss how natural selection works and why there must be genetic variation in a population for natural selection to occur. You should also be able to provide some examples of natural selection in humans.

▶ Discuss how mutation, genetic drift, gene flow, and natural selection interact over time to produce evolutionary change in populations and species.

Have you ever had a cat with five, six, or even seven toes? Even if you haven’t, you may have seen one, because extra toes are fairly com- mon in cats. Or, maybe you’ve known someone with an extra finger or toe, because some people have extra dig- its too. Anne Boleyn, mother of Eng- land’s Queen Elizabeth I and the first of Henry VIII’s wives to lose her head, apparently had at least part of an extra little finger. (Of course, this had noth- ing to do with her early demise; that’s another story.)

Having extra digits (fingers and toes) is called polydactyly, and it’s pretty certain that one of Anne Boleyn’s parents was also polydacty- lous (Fig. 4-1). It’s also likely that any polydactylous cat has a parent with extra toes. But how do we know this? Actually, it’s fairly simple. It’s because polydactyly is a Mendelian trait inher- ited in a predictable way, and its pat- tern of inheritance, among others, was discovered almost 150 years ago by a monk named Gregor Mendel (Fig. 4-2).

For at least 10,000 years, people have raised domesticated plants and ani- mals. However, it wasn’t until the twen- tieth century that scientists under- stood how selective breeding could increase the frequency of desirable characteristics. From the time when

4 Heredity and Evolution

ancient Greek philosophers considered the question of how traits were inher- ited until well into the nineteenth cen- tury, the most common belief was that the traits seen in offspring resulted from the blending of parental traits. There were different explanations of how this happened, but numerous scholars, including Charles Darwin, accepted some aspects of this explana- tion focused on blending.

Student Learning Objectives

selective breeding A practice whereby animal or plant breeders choose which individual animals or plants will be allowed to mate based on the traits (such as coat color or body size) they hope to produce in the offspring. Animals or plants that don’t have the desirable traits aren’t allowed to breed.

chApter 4 Heredity and Evolution 78

The Genetic Principles Discovered by Mendel

It may seem strange that, after dis-cussing recent discoveries about DNA, we now turn our attention to the middle of the nineteenth century, but that’s when the science of genetics was born. By examining how the basic principles of inheritance were discov-

ered, we can more easily understand them. It wasn’t until Gregor

Mendel (1822–1884) con- sidered the question of

heredity that it began to be resolved. Men-

del was living in an abbey in what is now the Czech Republic. At the time he began his research, he’d already studied bot- any at the University

of Vienna. He had also performed vari-

ous experiments in the monastery gardens, and

this background led him to investigate how physical traits,

such as color or height, could be expressed in plant hybrids.

Mendel worked with garden peas, concentrating on seven different traits, each of which could be expressed in two ways (Fig. 4-3). You may think it’s unusual that we’re discussing peas in

an anthropology book, but they provide a simple example of the basic rules of inheritance. The principles Mendel dis- covered apply to all biological organ- isms, including humans—another fact illustrating the biological connections among all living things.

Segregation First, Mendel grew groups of pea plants that were different from one another with regard to at least one trait. For example, in one group all the plants were tall, while in another all were short. To see how the expression of height would change from one gen- eration to the next, he crossed tall plants with short plants, calling them the parental generation. According to traditional views, all the hybrid off- spring, which he called the F1 genera tion, should have been intermediate in height. But they weren’t. Instead they were all tall (Fig. 4-4).

Next, Mendel let the F1 plants self- fertilize to produce a second genera- tion (the F2 generation). But this time, only about three quarters of the off- spring were tall; the remaining one quarter were short. One expression (short) of the trait (height) had com- pletely disappeared in the F1 generation and then reappeared in the F2 genera- tion. Moreover, the expression that was present in all the F1 plants was more common in the F2 plants, occurring in

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▲ Figure 4-2 Portrait of Gregor Mendel.

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hybrids Offspring of parents who differ from each other with regard to certain traits or certain aspects of genetic makeup; also known as heterozygotes.

The Genetic Principles Discovered by Mendel 79

a ratio of approximately 3:1 (three tall plants for every short one).

These results suggested that dif- ferent expressions of a trait were con- trolled by discrete units (we would call them genes) occurring in pairs and that offspring inherited one unit from each parent. Mendel realized that the mem- bers of a pair of units controlling a trait somehow separated into different sex cells and were again united with anoth- er member during fertilization of the egg. This is Mendel’s first principle of inheritance, known as the principle of segregation.

Today we know that meiosis explains Mendel’s principle of segre- gation. During meiosis, paired chro- mosomes, and the genes they carry,

separate from each other and end up in different gametes. However, in the zygote, the full complement of chro- mosomes is restored, and both mem- bers of each chromosome pair are pres- ent in the offspring.

Dominance and Recessiveness Mendel also realized that the “unit” for the absent characteristic (short- ness) in the F1 plants hadn’t actually disappeared. It was still there, but for some reason it wasn’t expressed. Mendel described the expression that seemed to be lost as “recessive,” and the expressed trait “dominant.” Thus,

◀ Figure 4-3 The traits Mendel studied in peas.

Seed shape round wrinkled

yellow green

inflated wrinkled

green yellow

purple white

along stem at tip

tall short

Seed color

Pod shape

Pod color

Flower color

Flower position

Stem length

Trait Studied Dominant Form Recessive Form

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principle of segregation Genes (alleles) occur in pairs because chromo- somes occur in pairs. During gamete for- mation, the members of each pair of alleles separate, so that each gamete contains one member of each pair.

recessive Describing a trait that isn’t expressed in heterozygotes; it also refers to the allele that governs the trait. For a recessive allele to be expressed, an indi- vidual must have two copies of it (i.e., the individual must be homozygous).

dominant In genetics, describing a trait governed by an allele that’s expressed in the presence of another allele (i.e., in het- erozygotes). Dominant alleles prevent the expression of recessive alleles in hetero- zygotes. (This is the definition of complete dominance.)

Dorine Essumang

chapter 4 Heredity and Evolution 80

the principles of dominance and reces- siveness were developed, and they remain important concepts in genet- ics today.

As it turns out, height in garden peas is controlled by two different alleles at the same genetic locus; we’ll call it the height locus. The allele that specifies tall is dominant to the allele for short. (It’s worth mentioning that height isn’t controlled this way in all plants.) In Mendel’s experiments, all the parent plants had two copies of the same allele, either dominant or recessive, depending on whether they were tall or short. When two copies of the same allele are present, the indi- vidual is said to be homozygous. Thus all the tall parent plants were homozy- gous for the dominant allele and all the

short parent plants were homozygous for the recessive allele. This explains why crossing tall plants with tall plants produced only tall offspring. Likewise, all the crosses between short plants produced only short offspring. All the plants in the parent generation had the same allele—that is, they lacked genetic variation at the height locus. However, all the F1 plants (hybrids) inherited one allele from each parent plant: a tall allele from one parent and a short allele from the other. Therefore they all inherited two different alleles at the height locus. Individuals that have two different alleles at a locus are heterozygous.

Figure 4-5 illustrates the crosses that Mendel initially performed. By convention, letters that represent

All tall plants Tt

F1 Generation

Genotype

3/4 tall Genotypes TT or Tt tt

Pure-breeding tall plant Pure-breeding short plant

Parent Generation

Genotype tt

F2 Generation

1/4 short

▶ Figure 4-4 Results of crosses when only one trait (height) at a time is considered.

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homozygous having the same allele at the same locus on both members of a pair of chromosomes.

heterozygous having different alleles at the same locus on members of a pair of chromosomes.

Dorine Essumang

The Genetic Principles Discovered by Mendel 81

alleles or genes are italicized, with uppercase letters referring to dominant alleles (or dominant traits) and lower- case letters referring to recessive alleles (or recessive traits). Therefore,

T = the allele for tallness t = the allele for shortness

The same symbols are combined to describe an individual’s actual genetic makeup, or genotype. The term geno type usually refers to the alleles at a specific genetic locus in an organism. Thus the genotypes of the plants in Mendel’s experiments were

TT = homozygous tall plants Tt = heterozygous tall plants tt = homozygous short plants

Figure 4-5 also shows the different ways alleles can be combined when the F1 plants are self- fertilized to produce an F2 generation. Therefore the figure shows all the genotypes that are pos- sible in the F2 generation and, statisti- cally speaking, it shows that we would expect one quarter of the F2 plants to be homozygous dominant (TT), half to be heterozygous (Tt), and the remain- ing one quarter to be homozygous recessive (tt).

You can also see the proportions of F2 phenotypes, the observed physi- cal manifestations of genes, illustrat- ing why Mendel saw approximately three tall plants for every short plant in the F2 generation. One quarter of

the F2 plants are tall because they have the TT genotype. Furthermore, an additional half, which are hetero- zygous (Tt), are also tall because T is dominant to t, so it’s expressed in the phenotype. The remaining one quar- ter are homozygous recessive (tt), and they’re short because no domi- nant allele is present. It’s important to understand that the only way a reces- sive allele can be expressed is if it occurs with another recessive allele— that is, if the individual is homozy- gous recessive at the particular locus in question.

Independent Assortment Mendel also demonstrated that different charac- teristics aren’t necessarily inherited together by showing that plant height and seed color are independent of each other. That is, any tall pea plant had a 50-50 chance of producing either yel- low or green peas. Because of this fact, he developed the principle of inde- pendent assortment. According to this principle, the units (genes) that code for different traits (in this exam- ple, plant height and seed color) sort out independently of each other dur- ing gamete formation (Fig. 4-6). Today we know that this happens because the genes that control plant height and seed color are located on different, nonpartner chromosomes and, dur- ing meiosis, the chromosomes travel to newly forming cells independently

T t

TT Tall

Tt Tall

tt Short

Tt Tall

Parental gametes ◀ Figure 4-5 Punnett square repre- senting possible genotypes and phe- notypes and their proportions in the F2 generation. The circles across the top and at the left of the Punnett square represent the gametes of the F1 par- ents. Each square receives one allele from the gamete above it and another from the gamete to the left. Thus the square at the upper left has two domi- nant (T ) alleles. Likewise the upper right square receives a recessive (t) allele from the blue gamete above it and a dominant (T ) allele from the orange gamete to its left. In this way, the four squares illustrate that, statisti- cally, one quarter of the F2 plants can be expected to be homozygous tall (TT ); another half of the plants can also be expected to be tall but will be heterozygous (Tt); and the remaining quarter can be expected to be short because they are homozygous for the recessive “short” allele (tt). Thus, three quarters of the plants can be expected to be tall and one quarter short.

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genotype the genetic makeup of an individual. Genotype usually refers to an organism’s genetic makeup (or alleles) at a particular locus.

phenotypes the observable or detectable physical characteristics of an organism; the detectable expressions of genotypes, frequently influenced by envi- ronmental factors.

principle of independent assortment the distribution of one pair of alleles into gametes does not influ- ence the distribution of another pair. the genes controlling different traits are inher- ited independently of one another.

chApter 4 Heredity and Evolution 82

of one another in a process called ran- dom assortment.

But if Mendel had used just any two traits, his results would have been dif- ferent at least some of the time. This is because genes on the same chro- mosome aren’t independent of each other, and they usually stay together during meiosis. Even though Mendel didn’t know about chromosomes, he certainly knew that all characteristics weren’t independent of one another. But because he wanted to emphasize independence, he reported only on those traits that illustrated indepen- dent assortment.

Mendel’s results were published in 1866, but the methodology and statisti- cal nature of the research were beyond the thinking of the time and their sig- nificance was overlooked and unap- preciated. However, by the end of the nineteenth century, several investiga- tors had made important contributions to the understanding of chromosomes and cell division. These discoveries paved the way for the acceptance of Mendel’s work in 1900, when three dif- ferent groups of scientists came across his paper. Regrettably, Mendel had died 16 years earlier and never knew how greatly his work came to be appreciated.

▶ Figure 4-6 Results of a cross when two traits (height and seed color) are considered simultaneously. These two traits are independent of each other; that is, they aren’t neces- sarily inherited together. Also shown are the genotypes associated with each phenotype. Notice that the ratio of tall plants to short plants is three quarters to one quarter, or 3:1, the same as in Figure 4-4. Likewise, the ratio of yellow seeds to green seeds is 3:1. Thus, the phenotypic ratio in the F2 generation is 9:3:3:1. F1

Generation

Genotype

Genotypes

Pure-breeding short plant with green seeds (Recessive traits)

× TTYY

Pure-breeding tall plant with yellow seeds (Dominant traits)

3/16 short with yellow seeds

9/16 tall with yellow seeds

1/16 short with green seeds

TTYY TTYy TtYY TtYy

ttyy

3/16 tall with green seeds

TTyy Ttyy

ttyY ttYy

All tall plants with yellow seeds

Genotype

Phenotype

ttyy

TtYy

F2 Generation

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random assortment the chance distribution of chromosomes to daughter cells during meiosis. Along with recombina- tion, random assortment is an important source of genetic variation (but not new alleles).

Mendelian Inheritance in Humans 83

Mendelian Inheritance in Humans

Mendelian traits, also called discrete traits, are controlled by alleles at only one genetic locus (or, in some cases, two or more very closely linked loci). The most comprehensive listing of Mendelian traits in humans is available on the Internet. Online Men delian Inheritance in Man (www.ncbi. nlm.nih.gov/omim/) currently lists more than 21,000 human character- istics that are inherited according to Mendelian principles.

Although some Mendelian charac- teristics have readily visible phenotypic expressions (such as polydactyly), most don’t. The majority of Mendelian traits are biochemical in nature, and many genetic disorders result from harmful alleles inherited in Mendelian fashion (Table 4.1 on page 84). So if it seems as though textbooks overly empha- size genetic disease in discussions of Mendelian traits, it’s because many of the known Mendelian characteristics result from harmful alleles.

A number of genetic disorders are caused by dominant alleles (see Table 4-1). This means that if a person inher- its only one copy of a harmful domi- nant allele, the condition it causes will be present regardless of the presence of a different, recessive allele on the part- ner chromosome.

Recessive conditions are commonly associated with the lack of a sub- stance, usually an enzyme (see Table 4-1). For a person actually to have a recessive disorder, he or she must have two copies of the recessive allele caus- ing it. People who have only one copy of a harmful recessive allele are unaf- fected. But even though they don’t actually have the recessive condi- tion, they can still pass the allele that causes it on to their children. For this reason they’re frequently called car riers. (Remember, half their gametes will carry the recessive allele.) If such a person’s mate is also a carrier, it’s possible for them to have a child who

will be homozygous for the allele, and that child will be affected. In fact, in a mating between two carriers, the risk of having an affected child is 25 per- cent (refer back to Fig. 4-5).

Blood groups, such as the ABO sys- tem, provide some of the best exam- ples of Mendelian traits in humans. The ABO system is governed by three alleles, A, B, and O, found at the ABO locus on the ninth chromosome. These alleles determine a person’s ABO blood type by coding for the production of molecules called antigens on the sur- face of red blood cells. If only antigen A is present, the blood type (phenotype) is A; if only B is present, the blood type is B; if both are present, the blood type is AB; and when neither is present, the blood type is O (Table 4.2 on page 85).

The O allele is recessive to both A and B; therefore if a person has type O blood, he or she must have two cop- ies of the O allele. However, since both A and B are dominant to O, an indi- vidual with blood type A can actu- ally have one of two genotypes: AA or AO. The same is true of type B, which results from the genotypes BB and BO (see Table 4-2). However, type AB presents a slightly different situation, called codominance, where two dif- ferent alleles are present and both are expressed. Therefore when both A and B alleles are present, both A and B anti- gens can be detected on the surface of red blood cells.

Misconceptions about Dominance and Recessiveness Most people have the impression that dominance and recessiveness are all- or-nothing situations. This miscon- ception especially pertains to recessive alleles. The general view is that when these alleles occur in carriers (hetero- zygotes), they have no effect on the phenotype; that is, they are completely inactivated by the presence of another (dominant) allele. Certainly this is how it appeared to Gregor Mendel.

Mendelian traits characteristics that are influenced by alleles at only one genetic locus. examples include many blood types, such as ABO. Many genetic disorders, including sickle-cell anemia and tay-Sachs disease, are also Mendelian traits.

antigens Large molecules found on the surface of cells. Several different loci govern various antigens on red and white blood cells. (Foreign antigens provoke an immune response.)

codominance the expression of two alleles in heterozygotes. In this situation, neither allele is dominant or recessive, so they both influence the phenotype.

chApter 4 Heredity and Evolution 84

However, various biochemical tech- niques available today show that many recessive alleles actually do have some effect on the phenotype, although these effects aren’t usually detect- able through simple observation. It turns out that in heterozygotes, the products of many recessive alleles are

reduced but not completely eliminated. Therefore our perception of recessive alleles greatly depends on whether we examine them at the directly observ- able phenotypic level or the biochemi- cal level.

There are also a number of mis- conceptions about dominant alleles.

Table 4.1 Some Mendelian Traits in Humans Dominant Traits Condition

Manifestations

Recessive Traits Condition

Manifestations

Achondroplasia

Brachydactyly

Familial hyper- cholesterolemia

Neurofibromatosis

Marfan syndrome

Huntington disease

Camptodactyly

Hypodontia of upper lateral incisors

Cleft chin

PTC tasting

Dwarfism due to growth defects involving the long bones of the arms and legs; trunk and head size usually normal.

Shortened fingers and toes.

Elevated cholesterol levels and cholesterol plaque deposition; a lead- ing cause of heart disease, with death frequently occurring by middle age.

Symptoms range from the appear- ance of abnormal skin pigmentation to large tumors resulting in severe defor- mities; can, in extreme cases, lead to paralysis, blindness, and death.

The eyes and cardiovascular and skeletal systems are affected; symp- toms include greater than average height, long arms and legs, eye prob- lems, and enlargement of the aorta; death due to rupture of the aorta is common. Abraham Lincoln may have had Marfan syndrome.

Progressive degeneration of the ner- vous system accompanied by demen- tia and seizures; age of onset variable but commonly between 30 and 40 years.

Malformation of the hands whereby the fingers, usually the little finger, is permanently contracted.

Upper lateral incisors are absent or only partially formed (peg-shaped). Pegged incisors are a partial expres- sion of the allele.

Dimple or depression in the middle of the chin; less prominent in females than in males.

The ability to taste the bitter sub- stance phenylthiocarbamide (PTC). Tasting thresholds vary, suggesting that alleles at another locus may also exert an influence.

Cystic fibrosis

Tay-Sachs disease

Phenylketonuria (PKU)

Albinism

Sickle-cell anemia

Thalassemia

Absence of permanent dentition

Among the most common genetic (Mendelian) disorders among European Americans; abnormal secretions of the exocrine glands, with pronounced involvement of the pancreas; most patients develop obstructive lung disease. Until the recent development of new treatments, only about half of all patients survived to early adulthood.

Most common among Ashkenazi Jews; degeneration of the ner- vous system beginning at about 6 months of age; lethal by age 2 or 3 years.

Inability to metabolize the amino acid phenylalanine; results in men- tal impairment if left untreated dur- ing childhood; treatment involves strict dietary management and some supplementation.

Inability to produce normal amounts of the pigment melanin; results in very fair, untannable skin, light blond hair, and light eyes; may also be associated with vision problems. (There is more than one form of albinism.)

Abnormal form of hemoglobin (HbS) that results in collapsed red blood cells, blockage of capillar- ies, reduced blood flow to organs, and, without treatment, death.

A group of disorders character- ized by reduced or absent alpha or beta chains in the hemoglobin molecule; results in severe anemia and, in some forms, death.

Failure of the permanent dentition to erupt. The primary dentition is not affected.

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Mendelian Inheritance in Humans 85

Many people think of dominant alleles as somehow “stronger” or “better,” and there is always the mistaken notion that dominant alleles are more com- mon in populations because natural selection favors them. These miscon- ceptions undoubtedly stem from the label “dominant” and its connotations of power or control. But in genetic usage, this view is misleading. Just think about it. If dominant alleles were always more common, then a majority of people would have conditions such as achondroplasia and Marfan syn- drome (see Table 4-1). But obviously that’s not true.

Previously held views of dominance and recessiveness were influenced by available technologies, and as genetic technologies continue to change, new theories will emerge and our percep- tions will be further altered. (This is another example of how new tech- niques and continued hypothesis test- ing can lead to a revision of hypotheses and theories.) In fact, although domi- nance and recessiveness will remain important factors in genetics, it’s clear that the ways in which these con- cepts will be taught will be adapted to accommodate new discoveries.

Patterns of Mendelian Inheritance It’s important to be able to establish the pattern of inheritance of genetic traits, especially those that cause serious disease. Also, in families with a his- tory of inherited disorders, it’s impor- tant to determine an individual’s risk of

inheriting harmful alleles or express- ing symptoms. The technique tradi- tionally used to assess risk of genetic disease has been the construction of a pedigree chart, a diagram of matings and offspring in a family over the span of a few generations. Pedigree analysis helps researchers determine if a trait is Mendelian and also helps establish the mode of inheritance. By determin- ing whether the gene that influences a particular trait is located on an auto- some or sex chromosome and whether a particular allele is dominant or reces- sive, researchers have identified six different modes of Mendelian inheri- tance in humans: autosomal dominant, autosomal recessive, X-linked recessive, X-linked dominant, Y-linked, and mito- chondrial. We’ll discuss the first three in some detail.

Standardized symbols are used in pedigree charts. Squares and cir- cles represent males and females, respectively. Horizontal lines con- necting individuals indicate matings, and offspring are connected to hori- zontal mating lines by vertical lines. Siblings are joined by a horizontal line connected to a vertical line that descends from the parents (Fig. 4-7).

Autosomal Dominant Traits As the term implies, autosomal dominant traits are governed by dominant alleles located on autosomes (that is, any chromosome except X or Y). One example of an autosomal dominant trait is achondro- plasia, a form of dwarfism character- ized by a normal-sized trunk and head but shortened arms and legs (see Table

Table 4.2 ABO Genotypes and Associated Phenotypes Genotypes

Antigens on Red Blood Cells

ABO Blood Type (Phenotype)

AA, AO A A

BB, BO B B

AB A and B AB

OO None O

Parents

Offspring (siblings)

▲ Figure 4-7 Typical symbols used in pedigree charts. Circles and squares represent females and males respec- tively. Horizontal lines connecting two individuals indicate mating. Vertical lines connect generations.

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pedigree chart A diagram showing family relationships. It’s used to trace the hereditary pattern of particular genetic (usually Mendelian) traits.

chApter 4 Heredity and Evolution 86

almost everybody) are homozygous recessive (aa).

Figure 4-9 is a partial pedigree chart for achondroplasia. It’s appar- ent from this pedigree that all affected members have at least one affected par- ent, so the condition doesn’t skip gen- erations. This pattern is true for all autosomal dominant traits. Another characteristic of autosomal domi- nant traits is that males and females are more or less equally affected. Also important regarding dominant traits is that approximately half the offspring of affected parents are also affected (Fig. 4-10). This proportion is what we

4-1 and Fig. 4-8). Achondroplasia occurs in approximately 1 out of every 10,000 live births. It is usually caused by a spontaneous point mutation in a gene that influences the development of cartilage and thus bone growth.

Because achondroplasia is caused by a dominant allele, anyone who inherits just one copy of it will have the trait. In this discussion, the sym- bol A refers to the dominant allele that causes the condition and a represents the recessive, normal allele. Since the allele is rare, virtually everyone who has achondroplasia is a heterozygote (Aa). Unaffected individuals (that is,

▲ Figure 4-8 Ellie Simmonds who has achondroplasia, won two gold medals for Great Britain in swimming events at both the 2008 and 2012 Paralympic Games. She inherited one copy of the dominant allele that causes achondroplasia by inhibiting bone growth during fetal develop- ment. As a result, her legs and arms are disproportionally short. People with achondroplasia are also unable to fully extend their arms—something that has not inhibited her swimming abilities.

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Unaffected male

Unaffected female

Affected male

Affected female

1 2

3 4 5 6 7 8

9 10 11 12 13 14 15 16 17 18 19

▲ Figure 4-9 Inheritance of an autosomal dominant trait as illustrated by a human pedigree for achondroplasia. How can individuals 5, 11, 14, 15, and 17 be unaffected? What is the gen- otype of all affected individuals? (To answer the second question, let A = the dominant allele and a = the recessive allele.)

aaAa

aA aa Gametes

Parent with achondroplasia

Normal parent

(a)

Aa aaa

Parental gametes

Aa aa

Genotypes of offspring

(b)a b

▲ Figure 4-10 The pattern of inheritance of autosomal dominant traits is the direct result of the distribution of chromosomes and the alleles they carry into gametes during meiosis. (a) A diagram of possible gametes produced by two parents, one with achondroplasia and another with normal development of the extremities. The achondroplastic individual can produce two types of gametes: half with the dominant allele (A) and half with the recessive allele (a). All gametes produced by the normal-height parent will carry the recessive allele. (b) A Punnett square depicting the possible genotypes in the offspring of one parent with achondroplasia (Aa) and one with normal extremities (aa). Statistically, we would expect half the offspring to have the Aa genotype and thus have achondroplasia. The other half would be homozygous recessive (aa) and their extremities would grow normally.

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Mendelian Inheritance in Humans 87

would predict for an autosomal dom- inant trait where only one parent is affected, because half of that parent’s gametes will have the dominant but harmful allele.

Autosomal Recessive Traits Autosomal recessive traits are also influenced by genes on autosomes, but they show a different pattern of inheritance. A good example is shown in Figure 4-11, a pedigree chart for albinism. The most common form of albinism is a meta- bolic disorder caused by an autosomal recessive allele that prevents the pro-

duction of a pigment called melanin (see Chapter 15). Thus albinos have unusually light hair, skin, and eyes (Fig. 4-12). The frequency of this type of albinism varies widely among popu- lations, with a prevalence of about 1 in 37,000 people of European ancestry; but approximately 1 in 200 Hopi Indi- ans are affected.

Pedigrees for autosomal recessive traits show obvious differences from those for autosomal dominant char- acteristics. For one thing, an affected offspring can be produced by two phe- notypically normal parents. In fact,

◀ Figure 4-11 Partial pedigree for albinism, an autosomal recessive trait. Why are some of the offspring of affected individuals unaffected? Individuals 6 and 7, children of unaf- fected parents, are affected. Why? Four individuals are definitely unaf- fected carriers. Which ones are they? Why is individual 11 affected when his parents aren’t?

Unaffected male

Unaffected female

Affected male

Affected female

1 2

5 63 4

12 139 10 11

7 8

14 15 16

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Bi ld

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▼ Figure 4-12 (a) A Tanzanian woman with her young albino son. (Because of the social stigma attached to albinism, there has been, since the mid-2000s, a dramatic increase in the trade of albino body parts, which are used in witchcraft, especially in Tanzania.) (b) This albino horse may be beautiful, but it should not be kept outdoors all the time. With virtually no pigmentation, it would be highly susceptible to sunburn and various forms of skin cancer, including melanoma.

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most people who express recessive conditions have unaffected parents. In addition, the proportion of affected off- spring from most matings is less than half. But when both parents have the trait, all their offspring will be affected. As in the pattern for autosomal dom- inant traits, males and females are equally affected.

The Mendelian principle of segrega- tion explains the pattern of inheritance of autosomal recessive traits. In fact, this pattern is the very one Mendel first described in his pea experiments (look back at Fig. 4-5). Unaffected par- ents who produce an albino child must

both be carriers, and their child will be homozygous for the recessive allele causing the abnormality. The Punnett square in Figure 4-13 shows how such a mating produces both unaffected and affected offspring in predictable proportions—the typical phenotypic ratio of 3:1.

Sex-Linked Traits Sex-linked traits are controlled by genes located on the X and Y chromosomes. Almost all of the more than 1,000 sex-linked traits list- ed in Online Mendelian Inheritance in Man are influenced by genes on the X chromosome (Table 4.3). Most of the

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▶ Figure 4-13 A cross between two phenotypically normal parents, both carriers of the albinism allele. From a mating such as this between two carriers, statistically we would expect the following possible proportions of genotypes and phenotypes in the off- spring: homozygous dominants (AA) with normal phenotype, 25 percent; heterozygotes, or carriers (Aa) with nor- mal phenotype, 50 percent; and homo- zygous recessives (aa) with albinism, 25 percent. This yields the phenotypic ratio of three with normal pigmentation to one albino.

Table 4.3 Some Mendelian Disorders Inherited as X-linked Recessive Traits in Humans Condition Manifestations

G-6-PD (glucose-6-phos- phate) deficiency

Lack of an enzyme (G-6-PD) in red blood cells; produces severe, sometimes fatal anemia in the presence of certain foods (e.g., fava beans) and/or drugs (e.g., the antimalarial drug primaquin).

Muscular dystrophy One form is X-linked; other forms can be inherited as autosomal recessives. Progressive weakness and atrophy of muscles beginning in early childhood; continues to progress throughout life; some female carriers may develop heart problems.

Red-green color blindness Actually, there are two separate forms, one involving the perception of red and the other involving the perception of green. About 8 percent of European males have an impaired ability to distinguish green.

Lesch-Nyhan disease Impaired motor development noticeable by 5 months; progressive motor impairment, dimin- ished kidney function, self-mutilation, and early death.

Hemophilia There are three forms; two (hemophilia A and B) are X-linked. In hemophilia A, a clotting fac- tor is missing; hemophilia B is caused by a defective clotting factor. Both produce abnormal internal and external bleeding from minor injuries; severe pain is a frequent accompaniment; without treatment, death usually occurs before adulthood.

Ichthyosis There are several forms; one is X-linked. A skin condition due to lack of an enzyme; character- ized by scaly, brown lesions on the extremities and trunk. In the past, people with this condi- tion were sometimes exhibited in circuses and sideshows as “the alligator man.”

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Non-Mendelian Inheritance 89

coding sequences (that is, those seg- ments that actually specify a protein) on the Y chromosome are involved in determining maleness and testis function.

Hemophilia, one of the best known of the X-linked traits, is caused by a recessive allele on the X chromo- some. This allele prevents the forma- tion of a clotting factor in the blood, and affected individuals suffer bleed- ing episodes and may actually bleed to death from injuries that most of us would consider trivial.

The most famous pedigree illus- trating this condition is that of Queen Victoria (1820–1901) of England and her descendants (Fig. 4-14). The most striking feature shown by this pat- tern of inheritance is that almost all affected people are males, because males have only one X chromosome and therefore only one copy of X-linked genes. This means that any allele, even a recessive one, located on their X chromosome will be expressed, because there’s no possibility of a dominant allele on a partner chromo- some to block it. Females, on the other hand, show the same pattern of expres- sion of X-linked traits as for autoso- mal traits, because they have two X chromosomes. That is, just as with any other pair of chromosomes, the only way an X-linked recessive allele can be expressed in a female is if she has two copies of it. However, females who have one copy of the hemophilia allele are carriers, and they may have some ten- dency toward bleeding, even though they aren’t severely affected.

Non-Mendelian Inheritance

Polygenic Inheritance Mendelian traits are described as dis crete, or discontinuous, because their phenotypic expressions don’t overlap; instead, they fall into clearly defined categories (Fig. 4-15a). For example,

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chApter 4 Heredity and Evolution 90

in the ABO system, the four pheno- types are completely distinct from one another; that is, there is no intermedi- ate form between type A and type B. In other words, Mendelian traits don’t show continuous variation.

However, many traits do have a wide range of phenotypic expressions, which form a graded series. These are called polygenic, or continuous, traits (Fig. 4-15b and c). While Mendelian traits are governed by only one genetic locus, polygenic characteristics are governed by alleles at two or more loci, and each

locus has some influence on the pheno- type. Throughout the history of biolog- ical anthropology, the most frequently discussed examples of polygenic inher- itance in humans have been skin, hair, and eye color (Fig. 4-16).

Coloration is determined by mela- nin, a pigment produced by special- ized cells called melanocytes (see Chapter 16), and the amount of mela- nin that is produced determines how dark or light a person’s skin will be. Melanin production is influenced by interactions between several differ-

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polygenic referring to traits influ- enced by genes at two or more loci. examples include stature, skin color, eye color, and hair color. Many polygenic traits are influenced by environmental factors such as nutrition and exposure to sunlight.

pigment In this context, molecules that influence the color of skin, hair, and eyes.

Non-Mendelian Inheritance 91

ent loci that have now been identi- fied. A study by Lamason and col- leagues (2005) showed that one single, highly conserved gene (called MC1R) with two alleles makes a greater con- tribution to melanin production than some other melanin- producing genes. Moreover, geneticists know of at least four other pigmentation genes. This is very important because they can now examine the complex interactions between these genes and also how their functions are influenced by regulatory genes. So the story of melanin produc- tion is a complicated one, but it’s excit- ing that many long-standing questions about variation in human skin color will be answered in the not too distant future.

As we stated earlier, eye color is influenced by more than one gene, and some of the genes that influence skin color are also involved. However, a gene called OCA2, located on chromosome 15, is apparently the most important gene in the development of blue eyes (Fig. 4-16). OCA2 is involved in pigmen- tation of the iris of the eye, and muta- tions in this gene lead to a form of albi- nism. Sturm and colleagues (2008) demonstrated that this gene accounts for 74 percent of the variation in human eye color in European populations. (Northern European populations and their descendants exhibit more variabil- ity in eye color than is seen in any other human populations, and they’re the only ones in which significant numbers of people have blue eyes.) Moreover, specific variations of the OCA2 gene were found in virtually 100 percent of blue-eyed people from Denmark, Turkey, and Jordan. In addition, point mutations in one of several genes that regulate OCA2 are also “perfectly asso- ciated” with blue eyes (Eiberg et al., 2007). Thus when we examine any trait, we must look not only at the genes tra- ditionally associated with it but also at the DNA sequences that regulate it. Indeed, it’s looking more and more like genes don’t really do much by them- selves; they just follow orders, and if the orders vary, their effects will also vary.

Polygenic traits actually account for most of the readily observable pheno- typic variation in humans, and they’ve traditionally served as a basis for racial classification. In addition to skin, hair, and eye color, there are many other polygenic characteristics—including stature, shape of the face, and finger- print pattern—to name a few. Because they exhibit continuous variation, most polygenic traits can be measured on a scale composed of equal increments. For example, height (stature) is mea- sured in feet and inches (or meters and centimeters). If we were to measure height in a large number of individu- als, the distribution of measurements would continue uninterrupted from the shortest extreme to the tallest (see Fig. 4-15b and c). That’s what is meant by the term continuous traits.

Because polygenic traits can usually be measured, physical anthropologists can analyze them using certain statis- tical tests. The use of simple summary statistics, such as the mean (average) or standard deviation (a measure of variation within a group), permits basic descriptions of populations and com- parisons between them. For example, a physical anthropologist might be inter- ested in average height in two different populations, whether or not differences between the two are statistically sig- nificant, and if so, why. (Incidentally, all physical traits measured and statis- tically treated in fossils are polygenic in nature.)

Mendelian traits can’t be measured in the same way because they’re either present or absent—expressed one way or another. But this doesn’t mean that they provide less information about genetic processes. They can be described in terms of frequency within populations, which makes it possible to compare groups for differences in prev- alence. For example, one population may have a high frequency of blood type A while type A may be almost completely absent in another group. Also, Mendelian traits can be analyzed for mode of inheritance (dominant or recessive).

▲ Figure 4-16 Eye color is a polygenic characteristic and is a good example of continuous variation.

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chApter 4 Heredity and Evolution 92

Last, for many Mendelian traits, the approximate or exact positions of genetic loci are known, which makes it possible to examine the mechanisms and patterns of inheritance at these loci. This type of study isn’t yet possi- ble for polygenic traits because they’re influenced by several genes that are only now being traced to specific loci.

Mitochondrial Inheritance Another component of inheritance involves the organelles called mito chondria (see Chapter 3). All cells con- tain several hundred of these oval structures, which convert energy (derived from the breakdown of nutri- ents) to a form that can be used to per- form cellular functions.

Each mitochondrion contains sev- eral copies of a ring-shaped DNA mol- ecule, or chromosome. While mito chondrial DNA (mtDNA) is distinct

from chromosomal DNA, its molec- ular structure and functions are the same. The entire molecule has been sequenced and is known to contain around 40 genes that direct the conver- sion of energy within the cell.

Like the DNA in a cell’s nucleus, mtDNA is subject to mutations, some of which cause certain genetic disor- ders resulting from impaired energy conversion. Importantly, animals of both sexes inherit all their mtDNA, and thus the expression of all mito- chondrial traits, from their mothers. Because mtDNA is inherited from only one parent, meiosis and recombination don’t occur. This means that all the variation in mtDNA among individu- als is caused by mutation, which makes mtDNA extremely useful for study- ing genetic change over time. So far, geneticists have used mutation rates in mtDNA to investigate evolution- ary relationships between species, to

Mendelian vs. Polygenic Traits

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At a Glance

Mendelian Traits

expression not usually influenced by environment

Distribution of phenotypes into just a few discrete

categories (for example, in complete dominance with two alleles, there are just

two phenotypes)

Polygenic Traits

expression may be influenced by environment

Distribution of phenotypes is continuous with no discrete

categories (many phenotypes can be distinguished)

Influenced by one gene Influenced by more than one gene

Genetic and Environmental Factors 93

trace ancestral relationships within the human lineage, and to study genetic variability among individuals and/or populations. While these techniques are still being refined, it’s clear that we have a lot to learn from mtDNA.

Pleiotropy While polygenic traits are governed by the actions of several genes, pleiotropy is a situation where a single gene influ- ences more than one characteristic. Although this might seem unusual, pleiotropic effects are probably the rule rather than the exception.

The autosomal recessive disorder phenylketonuria (PKU) provides one example of pleiotropy (see Table 4-1). Individuals who are homozygous for the PKU allele don’t produce the enzyme involved in the initial conver- sion of the amino acid phenylalanine to another amino acid, tyrosine. Because of this block in the metabolic pathway, phenylalanine breaks down into sub- stances that accumulate in the cen- tral nervous system; without dietary management, these substances lead to mental deficiencies and several other consequences. Tyrosine is ultimately converted to several other substances, including the pigment melanin; there- fore numerous other systems can also be affected. Thus another manifesta- tion of PKU, owing to a diminished ability to produce melanin, is that affected people usually have blue eyes, fair skin, and light hair. There are many examples of pleiotropic genes, includ- ing the allele that causes sickle-cell anemia. Thus the action of one gene can influence a number of seemingly unrelated traits.

Genetic and Environmental Factors

By now you may have the impres-sion that phenotypes are entirely the expressions of genotypes; but that’s

not true. (Here the terms genotype and phenotype are used in a broader sense to refer to an individual’s entire genetic makeup and all observable or detect- able characteristics.) Genotypes set limits and potentials for development, but they also interact with the environ- ment, and many (but not all) aspects of the phenotype are influenced by this genetic-environmental interaction. For example, adult stature is influenced by both genes and the environment. Even though the maximum height a person can achieve is genetically determined, childhood nutrition (an environmental factor) is also important. Other impor- tant environmental factors include exposure to sunlight, altitude, tem- perature, and both toxic waste and air- borne pollutants, which unfortunately are increasing almost everywhere. These and many other factors contrib- ute in complex ways to the continuous phenotypic variation seen in traits gov- erned by several genetic loci. However, for many characteristics, it’s not pos- sible to identify the specific environ- mental components that influence the phenotype.

Mendelian traits are less likely to be influenced by environmental fac- tors. For example, ABO blood type is determined at fertilization and remains fixed throughout an individual’s life- time, regardless of diet, exposure to ultraviolet radiation, temperature, and so forth.

Mendelian and polygenic inheri- tance show different patterns of phe- notypic variation. In the former, vari- ation occurs in discrete categories, while in the latter, it’s continuous. However, it’s important to understand that even for polygenic characteris- tics, Mendelian principles still apply at individual loci. In other words, if a trait is influenced by six loci, each one of those loci may have two or more alleles, with some perhaps being dominant to others. It’s the combined action of the alleles at all six loci, inter- acting with the environment, that pro- duces the phenotype.

pleiotropy A situation where the action of one gene affects several different traits.

chApter 4 Heredity and Evolution 94

Modern Evolutionary Theory

By the beginning of the twentieth century, the foundations for evo- lutionary theory had already been developed. Darwin and Wallace had described natural selection 40 years earlier, and the rediscovery of Mende- lian genetics in 1900 contributed the other major component: a mechanism for inheritance. We might expect that these two basic contributions would have been combined into a consistent theory of evolution, but they weren’t. For the first 30 years of the twentieth century, some scientists argued that mutation was the main factor in evolu- tion, while others emphasized natural selection. What they really needed was a merger of the two views rather than an either-or situation, but this didn’t happen until the mid-1930s.

The Modern Synthesis In the late 1920s and early 1930s, biolo- gists realized that mutation and natural selection weren’t opposing processes: They both contributed to biological evolution. The two major foundations of the biological sciences had finally been brought together in what is called the Modern Synthesis. From such a “modern” (that is, the middle of the twentieth century onward) perspec- tive, evolution is defined as a two-stage process:

1. The production and redistribution of variation (inherited differences among organisms)

2. Natural selection acting on this variation, whereby inherited differ- ences, or variations, among indi- viduals differentially affect their ability to successfully reproduce

A Current Definition of Evolution As we discussed in Chapter 2, Darwin saw evolution as the gradual unfold- ing of new varieties of life from pre-

existing ones. Certainly this is one result of the evolutionary process. But these long-term effects can come about only through the accumulation of many small genetic changes occur- ring over the generations. Today we can demonstrate how evolution works by examining some of the small genetic changes seen in populations and how they increase or decrease in frequency. From this perspective, we define evo- lution as a change in allele frequency from one generation to the next.

Allele frequencies are indicators of the genetic makeup of a population, the members of which share a com- mon gene pool. To show how allele frequencies change, we’ll use a simpli- fied example of an inherited trait, again the ABO blood types. (Note: There are several blood groups, not just the ABO system, and they’re all controlled by different genes.)

Let’s assume that the students in your anthropology class represent a population and that we’ve determined everyone’s ABO blood type. (To be considered a population, individuals must choose mates more often from within the group than from outside it. Obviously your class won’t meet this requirement, but we’ll overlook that.) The proportions of the A, B, and O alleles are the allele frequencies for this trait. If 50 percent of all the ABO alleles in your class are A, 40 percent are B, and 10 percent are O, the frequencies of these alleles are A = 0.50, B = 0.40, and O = 0.10.

Since the frequencies of these alleles represent proportions of a total, it’s obvious that allele frequencies can refer only to groups of individuals, or populations. Individuals don’t have allele frequencies; they have either A, B, or O in any combination of two. Also, from conception onward, a per- son’s genetic makeup is fixed.* If you start out with blood type A, you will

* Although a person’s genetic makeup is determined at conception, certain environmental factors, over time, can alter gene expression. However the nucleotide sequences themselves remain the same.

variation In genetics, inherited differ- ences among individuals; the basis of all evolutionary change.

allele frequency In a population, the percentage of all the alleles at a locus accounted for by one specific allele.

population Within a species, a com- munity of individuals where mates are usu- ally found.

gene pool All of the genes shared by the reproductive members of a population.

Factors That Produce and Redistribute Variation 95

always have type A. Therefore only a population can evolve over time; indi- viduals can’t.

Assume that 20 years from now we calculate the frequencies of the ABO alleles for the offspring of our class- room population and find the follow- ing: A = 0.30, B = 0.40, and O = 0.30. We can see that the relative propor- tions have changed: A has decreased, O has increased, and B has remained the same. This would not be a big deal, but in a biological sense, minor changes such as this constitute evolution. Over the short span of just a few generations, changes in the frequencies of inherited traits may be very small; but if they continue to happen, and particularly if they go in one direction as a result of natural selection, they can produce new adaptations and even new species.

Whether we’re talking about the short-term effects (as in our classroom population) from one generation to the next, which is sometimes called micro- evolution, or the long-term effects through time, called speciation or mac- roevolution, the basic evolutionary mechanisms are similar. But how do allele frequencies change? Or, to put it another way, what causes evolution? As we’ve already said, evolution is a two- stage process. Genetic variation must first be produced by mutation, so that natural selection can then act upon it.

Factors That Produce and Redistribute Variation

Mutation You’ve already learned that a mutation is a change in DNA. There are many kinds of mutations, but here we focus on point mutations, or substitutions of one DNA base for another. ( Actually, alleles are the results of point muta- tions.) Point mutations must occur in sex cells if they’re to have evolution- ary consequences. This is because, in order for evolutionary change to occur, the mutation must be passed from one

generation to the next. If a mutation takes place in a person’s somatic cells but not in gametes, it won’t be passed on to offspring. If, however, a genetic change occurs in the sperm or egg of one of the students in our classroom (A mutates to B, for instance), the off- spring’s blood type will be different from that of the parent, causing a min- ute shift in the allele frequencies of the next generation.

Actually, except in microorgan- isms, it’s rare for evolution to take place solely because of mutations. Mutation rates for any given trait are usually low, so we wouldn’t really expect to see a mutation at the ABO locus in a popu- lation as small as your class. In larg- er populations, mutations might be observed in 1 individual out of 10,000, but by themselves they would have no impact on allele frequencies. However, when mutation is combined with natu- ral selection, evolutionary changes can occur more rapidly.

It’s important to remember that mutation is the basic creative force in evolution, because it’s the only way to produce new genes (that is, variation). Its role in the production of variation is key to the first stage of the evolution- ary process.

In Chapter 3, we discussed the importance to the evolutionary process of mutations in regulatory genes. We also mentioned that many DNA sequences contain variable numbers of certain segments called copy number variants (CNVs) (see A Closer Look: “Noncoding DNA—Not Junk After All” in Chapter 3). Individuals and spe- cies have different numbers of certain segments within their genes, and these differences influence a gene’s overall effect. When CNVs occur in regulatory genes, particularly those involved in development, they can cause dramatic phenotypic changes.

CNVs occur as a result of dele- tions or duplications of DNA segments within a gene. Tandem repeats are a type of duplication that has attracted a great deal of attention in recent years because they have much higher mutation rates than single alleles do

microevolution Small changes occurring within species, such as changes in allele frequencies.

macroevolution changes produced only after many generations, such as the appearance of a new species.

tandem repeats Short, adjacent segments of DNA within a gene that are repeated several times.

chApter 4 Heredity and Evolution 96

and therefore could have a signifi- cant influence on rates of evolution. In one study, Fondon and Garner (2004) examined the relationship between tandem repeats in regulatory genes and phenotypic expression. Among other things, they showed how a tandem repeat in a regulatory gene involved in bone growth has dramatically influ- enced the shape of the cranium of bull terriers (Fig. 4-17).

The changes in bull terrier crania are the results of artificial selection for a specific trait (the long droop- ing snout), influenced by variation in a regulatory gene. While this is not speciation, it is dramatic evidence of how tandem repeats in protein-coding genes can produce significant pheno- typic variation for natural selection to act on. Indeed, tandem repeats have played, and continue to play, a highly significant role in evolution.

Gene Flow Gene flow is the exchange of genes between populations. The term migra tion is also sometimes used; but strictly

speaking, migration refers to the move- ment of people. In contrast, gene flow refers to the exchange of genes between groups, which can happen only if the migrants interbreed. Also, even if indi- viduals move temporarily and have offspring in the new population, they don’t necessarily stay there. For exam- ple, the children of U.S. soldiers and Vietnamese women represent gene flow. Even though the fathers returned to the United States after the Vietnam War, some of their genes remained behind, although not in sufficient numbers to appreciably change allele frequencies.

In humans, mating patterns are mostly determined by social factors, and cultural anthropologists can work closely with biological anthropologists to isolate and measure this aspect of evolutionary change. Human popula- tion movements (particularly in the last 500 years) have reached previously unheard of proportions, and very few breeding isolates remain. But migra- tion on a smaller scale has been a con- sistent feature of human evolution since the first dispersal of our genus,

▶ Figure 4-17 (a) Selective breeding in bull terriers has produced dramatic changes in the shape of the head, resulting in a concave profile and downward-turning nose. (b) These three purebred bull terrier crania clearly illustrate how the shape of the head changed in this breed in just 35 years. The dates for the crania, from top to bottom, are 1931, 1950, and 1976. (The 1931 specimen, from a Swiss lab, provided DNA for use in comparisons with modern bull terriers DNA.)

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gene flow exchange of genes between populations.

Factors That Produce and Redistribute Variation 97

and gene flow between populations (even though sometimes limited) helps explain why speciation has been rare during the past million years or so.

An interesting example of how gene flow influences microevolutionary changes in modern human populations is seen in African Americans. African Americans are largely of West African descent, but there has also been con- siderable genetic admixture with European Americans. By measuring allele frequencies for specific genetic loci, we can estimate the amount of migration of European alleles into the African American gene pool. Data from northern and western U.S. cities (including New York, Detroit, and Oakland) have shown that the pro- portion of non-African genes in the African American gene pool is 20 to 25 percent (Cummings, 2000).

Gene flow occurs for reasons other than large-scale movements of pop- ulations. In fact, significant changes in allele frequencies can come about through long-term patterns of mate selection whereby members of a group traditionally obtain mates from cer- tain other groups. This is especially true if mate exchange consistently occurs in one direction over a long period of time. For example, if group A chooses mates from group B but group B doesn’t reciprocate, eventu- ally group A will have an increased proportion of group B alleles. If, how- ever, mate exchange between groups is reciprocal, over time the two groups will become more alike genetically (Fig. 4-18).

Genetic Drift and Founder Effect Genetic drift is the random factor in evolution, and it’s a function of popula- tion size. Drift occurs solely because the population is small. If an allele is rare in a small population, it may disappear because, just by chance, it isn’t passed on to offspring (Fig. 4-19a). Thus

genetic drift reduces genetic variability in small populations.

One particular kind of genetic drift, called founder effect, is seen in many modern human and nonhuman popula- tions. Founder effect can occur when a small band of “founders” leaves its par- ent group and forms a colony some- where else. Over time, a new popula- tion will be established, and as long as mates are chosen only from within this population, all of its members will be descended from the small origi- nal group of founders. Therefore all the genes in the expanding group will have come from the original colonists. In such a case, an allele that was rare in the founders’ parent population but was carried by even one of the founders can eventually become common among the founders’ descendants (Fig. 4-19b). This is because a high proportion of people in later generations will all be descended from that one founder.

Colonization isn’t the only way founder effect can happen. Small founding groups may be the survivors of a larger group that was mostly wiped out by some type of disaster. But like the small group of colonists, the sur- vivors possess only a sample of all the alleles that were present in the original population.

Therefore, just by chance alone, some alleles may be completely lost from a population’s gene pool while others may become the only alleles at loci that previously had two or more. Whatever the cause, the outcome is a reduction in genetic diversity, and the allele frequencies of succeeding gen- erations may be substantially differ- ent from those of the original, larger population. The loss of genetic diver- sity in this type of situation is called a genetic bottleneck, and the effects can be highly detrimental to a species.

There are many known examples (both human and nonhuman) of spe- cies or populations that have passed through genetic bottlenecks. (In fact, many species are going through genetic bottlenecks right now.)

genetic drift Evolutionary changes, or changes in allele frequencies, produced by random factors in small popula- tions. Genetic drift is a result of small population size.

founder effect A type of genetic drift in which allele frequencies are altered in small populations that are taken from larger populations or are remnants of the latter.

chApter 4 Heredity and Evolution 98

Genetically, cheetahs (Fig. 4-20) are an extremely uniform species, and biol- ogists believe that at some point in the past these magnificent cats suffered a catastrophic decline in numbers. For unknown reasons related to the species-wide loss of numerous alleles, male cheetahs produce a high percent- age of defective sperm compared to other cat species. Decreased reproduc- tive potential, greatly reduced genetic diversity, and other factors (includ- ing human hunting) have combined to jeopardize the continued existence of this species. Other species that have passed through genetic bottlenecks include California elephant seals, sea

otters, and condors. Indeed, humans are much more genetically uniform than chimpanzees, and it appears that all modern human populations are the descendants of a few small groups.

One human example of genetic drift is provided by a fatal recessive condi- tion called Amish microcephaly, in which a mutation results in abnormally small brains and heads in fetuses. The disorder is found only in the Old Order Amish community of Lancaster County, Pennsylvania, where it occurs in approximately 1 in 500 births (Kelley et al., 2002; Rosenberg et al., 2002). Genealogical research showed that affected families have all been traced

The red allele is more common in population A than in population B. Meanwhile,the green allele is less common in population A.

Gene flow going in one direction because population A is supplying mates to population B. The result is that, over time, there is an increase in the red allele in population B.

Gene flow going in both directions and the populations are becoming more genetically alike.

a b

▶ Figure 4-18 Gene flow. In this illustration, the colored dots repre- sent different alleles and the circles that contain them represent two populations.

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Factors That Produce and Redistribute Variation 99

back nine generations to a single cou- ple. One member of this couple carried the deleterious recessive allele that, because of customs promoting mar- riage within (what was then) a small group, has greatly increased in frequen- cy with very serious consequences.

Much insight into the evolution- ary factors that have acted in the past can be gained by understanding how such mechanisms continue to operate on human populations today. In small populations, drift plays an important evolutionary role because fairly sudden fluctuations in allele frequency occur solely because of small population size. Likewise, throughout a good deal of

human evolution, at least the last 4 to 5 million years, hominins probably lived in small groups, and drift probably had a significant impact.

Additional insight concerning the relative influences of the different evo- lutionary factors has emerged in recent studies of the early dispersal of modern Homo sapiens. Evidence suggests that in the last 100,000 to 200,000 years, our species experienced a genetic bot- tleneck that considerably influenced the pattern of genetic variation seen in all human populations today.

As we’ve seen, both gene flow and genetic drift can produce some evolutionary changes by themselves.

▲ Figure 4-19 Small populations are subject to genetic drift, where rare alleles can be lost because, just by chance, they weren’t passed to offspring. Also, although more common alleles may not be lost, their frequencies may change for the same reason. (a) This diagram represents six alleles (different-colored dots) that occur at one genetic locus in a small population. You can see that in a fairly short period of time (three or four generations), rare alleles can be lost and genetic diversity consequently reduced. (b) This diagram illustrates the founder effect, a form of genetic drift where diversity is lost because a large population is drastically reduced in size and consequently passes through a genetic “bottleneck.” Founder effect also happens when a small group leaves the larger group and “founds” a new population elsewhere. (In this case, the group of founders is represented by the bottleneck.) Those individuals that survive (the founders) and the alleles they carry represent only a sample of the variation that was present in the original popula- tion. And future generations, all descended from the survivors, will therefore have less variability.

Time

Population size

A small population with considerable genetic variability. Note that the dark green and blue alleles are less common than the other alleles.

After just a few genera- tions, the population is approximately the same size but genetic variation has been reduced. Both the dark green and blue alleles have been lost. Also, the red allele is less common and the frequency of the light green allele has increased.

Original population with considerable genetic variation

A small group leaves to colonize a new area, or a bottleneck occurs, so that population size decreases and genetic variation is reduced.

Population size restored but the dark green and purple alleles have been lost. The frequencies of the red and yellow alleles have also changed.

Population size

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chapter 4 Heredity and Evolution 100

However, these changes are usually microevolutionary ones; that is,

they produce changes within species over the short term.

To produce the kind of evo- lutionary changes that ulti- mately result in new spe- cies (for example, the diversification of the first primates or the appear- ance of the earliest homi- nins), natural selection

is necessary. But natural selection can’t operate inde-

pendently of the other evolu- tionary factors: mutation, gene

flow, and genetic drift.

Recombination As we saw in Chap- ter 3, members of chromosome pairs exchange segments of DNA dur- ing meiosis. By itself, recombina- tion doesn’t change allele frequencies or cause evolution. However, when paired chromosomes exchange DNA, genes sometimes find themselves in different genetic environments. (It’s as if they had moved to a new neigh- borhood.) This fact can be important because the functions of some genes can be influenced simply by the alleles they’re close to. Thus recombination not only changes the composition of

parts of chromosomes but can also affect how some genes act, and slight changes of gene function can become material for natural selection to act on. (The levels of organization in the evolutionary process are summarized in Table 4.4.)

Natural Selection Is Directional and Acts on Variation

The evolutionary factors just dis-cussed (mutation, gene flow, genetic drift, and recombination) inter- act to produce variation and to dis- tribute genes within and between pop- ulations. But there is no long-term direction to any of these factors, and for adaptation and evolution to occur, a population’s gene pool must change in a specific direction. This means that some alleles must consistently become more common while others become less common, and natural selection is the one factor that can cause this kind of directional change in allele frequen- cy relative to specific environmental factors. If the environment changes, selection pressures change and allele

▲ Figure 4-20 Cheetahs, like many other species, have passed through a genetic bottleneck. Consequently they have little genetic variation as a species.

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Table 4.4 Levels of Organization in the Evolutionary Process Evolutionary Factor

Level

Evolutionary Process

Technique of Study

Mutation DNA Storage of genetic information; ability to rep- licate; influences phenotype by production of proteins

Biochemistry, recombinant DNA

Mutation Chromosomes A vehicle for packaging and transmitting genetic material (DNA)

Light or electron microscope

Recombination (sex cells only)

Cell The basic unit of life that contains the chro- mosomes and divides for growth and for production of sex cells

Light or electron microscope

Natural selection

Organism The unit, composed of cells, that reproduces and that we observe for phenotypic traits

Visual study, biochemistry

Drift, gene flow Population A group of interbreeding organisms; changes in allele frequencies between generations; it’s the population that evolves

Statistical analysis

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Natural Selection Is Directional and Acts on Variation 101

frequencies shift. Such shifts in allele frequencies are called adaptation.

In humans, the best-documented example of natural selection involves hemoglobin S (HbS), an abnormal form of hemoglobin that results from a point mutation in the gene that produces part of the hemoglobin molecule. As you learned in Chapter 3, if an indi- vidual inherits the hemoglobin S (HbS) allele from both parents, he or she will have sickle-cell anemia. Worldwide, sickle-cell anemia causes an estimated 100,000 deaths each year; in the United States, approximately 40,000 to 50,000 people, mostly of African descent, have this disease (Ashley-Koch et al., 2000).

The HbS mutation (see Chapter 3) occurs occasionally in all human pop- ulations, but usually the allele is rare. However, in some populations, espe- cially in western and central Africa, it’s more common than elsewhere, with

frequencies as high as 20 percent. The HbS allele is also fairly common in parts of Greece and India (Fig. 4-21). Given the devastating effects of hemo- globin S in homozygotes, you may wonder why it’s so common in some populations. It seems as though natu- ral selection would eliminate it, but it doesn’t. In fact, natural selection has actually increased its frequency, and the explanation for this situation can be summed up in one word: malaria.

Malaria is an infectious disease caused by a single-celled parasitic organism known as Plasmodium (its genus name). It is transmit- ted to humans by mosquitoes, and it kills an estimated 1 to 3 million people worldwide every year. After an infected mosquito bite, plasmo- dial parasites invade red blood cells, where they obtain the oxygen they need for reproduction (Fig. 4-22). The

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.08–.10

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.04–.06

Frequencies of the sickle-cell allele:

.02–.04

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◀ Figure 4-21 The distribution of the sickle-cell allele in the Old World.

chapter 4 Heredity and Evolution 102

consequencesofthisinfectiontothe humanhostincludefever,chills,head- ache,nausea,vomiting,andfrequently death.Inpartsofwesternandcentral Africa,wheremalariaisalwayspres- ent,asmanyas50to75percentof2- to9-year-oldsareafflicted.

Inthemid-twentiethcentury,the geographicalcorrelationbetween malariaandthedistributionofthe sickle-cellallele(HbS)wastheonly evidenceofabiologicalrelation- shipbetweenthetwo.Butnowwe knowthatpeople(heterozygotes)with sickle-cell traithavegreaterresis- tancetomalariathanpeoplewithonly normalhemoglobin.Thisisbecause peoplewithsickle-celltraithavesome redbloodcellsthatcontainhemoglo- binS,andthesecellsdon’tprovidea suitableenvironmentforthemalarial parasite.Inotherwords,havingsome hemoglobinSisbeneficialbecauseit affordssomeprotectionfrommalaria. Soinareaswheremalariaispresent, itactsasaselectiveagentfavoringthe heterozygousphenotypebecausepeo- plewithsickle-celltraithavehigher netreproductivesuccessthanthose withonlynormalhemoglobin,who oftendieofmalaria.Butselection forheterozygotesmeansthattheHbS allelewillbemaintainedinthepopu-

lation.Thustherewillalwaysbesome peoplewithsickle-cellanemia,and they,ofcourse,willhavethelowest reproductivesuccess,sincemost,with- outtreatment,willdiebeforereaching adulthood.

Review of Genetics and Evolutionary Factors

Inthischapter,discussionfocusedonhowgeneticinformationispassed fromonegenerationtothenext.We alsoreviewedevolutionarytheory, emphasizingthecrucialroleofnatural selection.Thevariouslevels(molec- ular,cellular,individual,andpopu- lational)aredifferentcomponentsof theevolutionaryprocess,andthey’re relatedtoeachotherinawaythat caneventuallyproduceevolutionary change.Astep-by-stepexamplewill makethisclear.

Considerapopulationinwhich almosteveryonehashemoglobinA. Forallpracticalpurposes,there’s almostnovariationregardingthis trait,andwithoutsomesourceofnew variation,evolutionisnotpossible.

(d) Merozoites enter blood, invade red blood cells, and reproduce by dividing. They can do this often, over a prolonged period. Disease symptoms (fever, chills, shaking) become more and more severe.

(f) Others develop into male and female gametocytes (precursors to sex cells) that are released into the bloodstream.

(e) Some of the merozoites enter the liver, causing more malaria episodes.

(a) In the female mosquito gut, Plasmodium zygotes develop into sporozoites, which migrate to the insect’s salivary gland. (b) The mosquito bites another

human, whose bloodstream carries sporozoites to the liver.

Sporozoite

(g) A female mosquito bites and ingests blood from an infected human. Gametocytes in the blood enter her gut and mature into gametes, which fuse to form zygotes. Male gametocyte in red blood cell

Sporozoites

Merozoite

▲ Figure 4-22 The life cycle of the parasite that causes malaria.

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sickle-cell trait heterozygous con- dition where a person has one HbA allele and one HbS allele. thus they have some normal hemoglobin.

Review of Genetics and Evolutionary Factors 103

However, in every generation, a few people carry a spontaneous mutation that changes just one DNA base in the HbA gene. This single point mutation, or base substitution, actually creates a new allele (HbS) in the DNA sequence, slightly altering the protein product (the hemoglobin molecule) and ulti- mately the phenotype of the individ- ual. But for the mutated allele to have any evolutionary potential, it must be present in the gametes and transmitted to offspring.

Once a mutation has occurred, it will exist within a chromosome, which, along with other chromosomes, may be inherited by offspring. And if a person has the mutation on only one mem- ber of a pair of chromosomes, there’s a 50-50 chance that the mutation will be passed on to each child he or she has.

But what does all this have to do with evolution? To repeat an earlier definition, evolution is based on a change in allele frequency in a popula- tion from one generation to the next. The key point here is that we are con- sidering populations, because it’s the populations that change over time.

We can determine if allele frequen- cies have changed in a population where sickle-cell hemoglobin is found by determining the percentage of indi-

viduals with the HbS allele versus those with the normal allele (HbA). If the rela- tive proportions of these alleles change with time, the population is evolv- ing at the HbA locus. But in addition to knowing that evolution is occuring, it’s important to know why, and there are several possible explanations. First, the only way the new HbS allele could have arisen is by mutation, and we’ve shown how this can happen in a single indi- vidual. But this isn’t an evolutionary change, since the alteration of one per- son’s genes in a relatively large popula- tion won’t change the allele frequencies of the entire population. Somehow, this new allele must spread in the popula- tion; and in the case of HbS, the allele spread because it was favored by nat- ural selection. And the reason it was favored is because it conferred some advantage in an environment where malaria was present.

As you learned earlier, genetic drift can also greatly alter the frequencies of alleles in small populations. Just by chance, some alleles may not be passed on, and after a few generations, they’re completely lost. Other alleles, mean- while, may end up being the only allele at a particular locus. This situation represents a loss of variation in the population.

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O C E A N

Areas where malaria is present

◀ Figure 4-23 The distribution of malaria in the Old World.

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chApter 4 Heredity and Evolution 104

In the course of human evolution, drift has probably played a significant role; it’s important to remember that at this microevolutionary level, drift and/or gene flow can (and will) pro- duce evolutionary change, even in the absence of natural selection. However, such change will be random because natural selection is the only factor that can cause allele frequencies to change in a particular direction.

The way natural selection has worked in the past and still operates today (as with sickle-cell hemoglobin) is through differential net reproduc-

tive success. That is, individuals who carry a particular allele or combination of alleles produce more offspring than other individuals with different alleles. Hence if a certain allele is beneficial in a particular environment, its frequency should increase slowly from genera- tion to generation. Likewise alleles that are detrimental should become less common. When this process is com- pounded over hundreds of generations at numerous loci, the result is signifi- cant evolutionary change. The levels of organization in the evolutionary process are summarized in Table 4-3.

In Table 4-1 we listed Tay-Sachs disease as an example of an autosomal recessive trait, most commonly seen in Ashkenazi Jews (Jews of eastern European descent). Tay-Sachs is actually a good example of why the inheri- tance and expression of dominant and recessive char- acteristics in populations is not as simple as textbooks (including this one) sometimes make it seem.

Tay-Sachs disease is a fatal disorder caused by the lack of an enzyme produced by the HEXA gene— an enzyme that breaks down lipids (molecules made of fats and other substances). In the absence of the enzyme, these substances accumulate in the brain. Resulting neurological symptoms usually appear by the age of 6 months and include blindness, deafness, paral- ysis, and death, usually before the age of 3 years. This description applies to the most common manifestation of the disease, infantile Tay-Sachs disease. The other two forms, juvenile and late onset, are much less com- mon and are caused by other mutations in the HEXA gene. In fact there are more than 100 mutations in the gene; all of them affect how the enzyme functions (Kaback, 2000) and they cause different expressions of the disease. But scientists began to be aware of the many different mutations only in the 1970s, and more are still being discovered.

As we stated, infantile Tay-Sachs is most com- monly seen in Ashkenazi Jews. But Cajun popula- tions of southern Louisiana also exhibit Tay-Sachs in much higher frequencies than other populations. As it turns out, the cause is the same mutation in both populations. A different mutation causes higher than normal frequencies in French Canadians. In all three groups, founder effect is the principal explanation for the increased frequency of the mutations in the HEXA gene. Indeed, researchers have traced the Cajun muta- tion back to a single couple that lived in France in the eighteenth century (McDowell et al, 1992).

Likewise, French Canadians are mostly descendants of a small founder population. In addition, they tended to marry other French Canadians because they were isolated from the general population by geographic, language, and cultural differences.

As you can see from this one briefly described con- dition, patterns of genetic disease result from the inter- actions of several factors. In the case of Tay-Sachs, multiple recessive mutations in one gene have inter- acted with population movement and social factors to produce the distribution of Tay-Sachs disease we see today.

How Do We Know?

105Critical Thinking Questions

▶▶ In the mid-nineteenth century, a monk named Gregor Mendel discovered the principles of segre- gation, independent assortment, and dominance and recessiveness by doing experiments with pea plants. Although the field of genetics progressed exponentially during the twentieth century, the concepts first put forth by Mendel remain the basis of our current knowledge of how traits are inherited.

▶▶ Basic Mendelian principles are applied to the study of the various modes of inheritance we’re familiar with today. The most important factor in all the Mendelian modes of inheritance is the role of seg- regation of chromosomes and the alleles they carry during meiosis.

▶▶ Building on fundamental nineteenth-century con- tributions by Charles Darwin and the rediscov- ery of Mendel’s work in 1900, advances in genetics throughout the twentieth century contributed to contemporary evolutionary thought. In particular, the combination of natural selection with Mendel’s principles of inheritance and experimental evi- dence concerning the nature of mutation have all been synthesized into a modern understanding of evolutionary change. In this contemporary theory of evolution, evolutionary change is seen as a two- stage process. The first stage is the production and

redistribution of variation. The second stage is the process whereby natural selection acts on the accumulated genetic variation.

▶▶ Mutation is crucial to all evolutionary change because it’s the only source of completely new genetic material (that is, new alleles), which increases variation. In addition, recombination, genetic drift, and gene flow redistribute variation within individuals (recombination), within popu- lations (genetic drift), and between populations (gene flow).

▶▶ Natural selection is the central determining factor influencing the long-term direction of evolution- ary change. How natural selection works can best be explained as differential net reproductive suc- cess, or how successful individuals are compared to others, in leaving offspring to succeeding gen- erations. The detailed history of the evolutionary spread of the sickle-cell allele provides the best- documented example of natural selection among recent human populations. It must be remem- bered that evolution is an integrated process, and this chapter concluded with a discussion of how the various evolutionary factors can be integrated into a single comprehensive view of evolutionary change.

Summary of Main Topics

1. If two people with blood type A, both with the AO genotype, have children, what proportion of their children would be expected to have blood type O? Why? Can these two parents have a child with AB blood? Why or why not?

2. After having read this chapter, do you understand evolutionary processes more completely? What questions do you still have?

3. Sickle-cell anemia is frequently described as affecting only Africans or people of African

descent; it’s considered a “racial” disease that doesn’t affect other populations. How would you explain to someone that this view is wrong?

4. Give some examples of how selection, gene flow, genetic drift, and mutation have acted on popula- tions or species in the past. Try to think of at least one human and one nonhuman example. Why do you think genetic drift might be important to endangered species today?

Critical Thinking Questions

Connections

Humans are both vertebrates and mam-

mals, and we’ve shared evolutionary history for

millions of years.

Connections

Evolution results from DNA changes

and the action of other evolutionary factors.

Humans are primates and share

many biological characteristics with

other primates.

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After mastering the material in this chapter, you should be able to:

▶ �Compare microevolution and macroevolution and explain how they are similar and how they differ.

▶ �Describe the main animal classifications and explain how humans fit into such classifications as vertebrates and as mammals.

▶ �Compare and contrast the more traditional classification approach (evolutionary systematics) with that of cladistics.

▶ �Explain what a fossil is and describe how different kinds of fossils are formed.

▶ �Define the major characteristics of mammals, especially those of placental mammals.

▶ �Explain how species are defined by biologists and how they originate from prior species.

�

107

Many people think of paleon-tology as a pretty dreary sub-ject of interest only to overly serious academics. But have you ever been to a natural history museum—or perhaps to one of the larger, more elab- orate toy stores? If so, you may have seen a full-size mock-up of Tyranno- saurus rex, one that might even move its head and arms and scream threat- eningly. These displays are usually encircled by enthralled adults and flocks of noisy, excited children. These same onlookers, however, show almost no interest in the display cases contain- ing fossils of early marine organisms. Yet every trace of early life has a fasci- nating story to tell.

The study of the history of life on earth is full of mystery and adventure. The bits and pieces of fossils are the remains of once living, breathing ani- mals (some of them extremely large and dangerous). Searching for these fossils in remote corners of the globe— from the Gobi Desert in Mongolia, to the rocky outcrops of Madagascar, to the badlands of South Dakota—is not a task for the faint of heart. Piecing together the tiny clues and ultimately reconstructing what Tyrannosaurus rex or a small, 50-million-year-old pri- mate looked like and how it might have behaved is really much like detective work. Sure, it can be serious; but it’s also a lot of fun.

In this chapter, we review the evolu- tion of vertebrates—more specifically, mammals. It’s important to understand these more general aspects of evolu- tionary history so that we can place

5 Macroevolution: Processes of Vertebrate and Mammalian Evolution

our species in its proper biological con- text. Homo sapiens is only one of mil- lions of species that have evolved. More than that, people have been around for just an instant in the vast expanse of time that life has existed, and we want to know where we fit in this long and complex story of life on earth. To dis- cover how humans connect within this incredibly long story of life on earth, we also discuss some contemporary issues relating to evolutionary theory. In par- ticular, we emphasize concepts relating to large-scale evolutionary processes— that is, macroevolution (in contrast to the microevolutionary focus of Chapter 4). The fundamental perspec- tives reviewed here concern geologi- cal history, principles of classification, and the nature of evolutionary change. These perspectives will serve as a basis for topics covered throughout much of the remainder of this book.

Student Learning Objectives

chapter 5 Macroevolution: Processes of Vertebrate and Mammalian Evolution 108

How We Connect: Discovering the Human Place in the Organic World

There are millions of species liv-ing today; if we were to include microorganisms, the total would likely exceed tens of millions. And if we added in the multitudes of species that are now extinct, the total would be staggering—perhaps hundreds of mil- lions! Where do we fit in, and what types of evidence do scientists use to answer this question?

Biologists need methods to deal sci- entifically with all this diversity. One way to do this is to use a system of classification that organizes diversity into categories and at the same time indicates evolutionary relationships.

Multicellular organisms that move about and ingest food are called ani- mals (Fig. 5-1). Within the kingdom Animalia, there are more than 20 major groups called phyla (sing., phy- lum). Chordata is one of these phyla; it includes all animals with a nerve cord, gill slits (at some stage of devel- opment), and a supporting cord along the back. In turn, most chordates are vertebrates—so called because they have a vertebral column. Vertebrates also have a developed brain and paired sensory structures for sight, smell, and balance.

The vertebrates themselves are sub- divided into five classes: cartilaginous fishes, bony fishes, amphibians, rep- tiles/birds, and mammals. We’ll dis- cuss mammalian classification later in this chapter.

By putting organisms into increas- ingly narrow groupings, we organize diversity into categories and also make statements about evolutionary and genetic relationships between species and groups of species. Further divid- ing mammals into orders makes the statement that, for example, all car- nivores (Carnivora) are more closely

related to each other than they are to any species placed in another order. Consequently bears, dogs, and cats (Carnivora) are more closely related to each other than they are to cattle, pigs, or deer (Artiodactyla). At each suc- ceeding level (suborder, superfamily, family, subfamily, genus, and species), finer distinctions are made between categories until, at the species level, only those animals that can potentially interbreed and produce viable offspring are included.

Principles of Classification

Before we go any further, we must discuss the basis of animal clas- sification. The field that specializes in establishing the rules of classification is called taxonomy. Most traditionally, organisms are classified first according to their physical similarities. This was the basis of the first systematic classifi- cation devised by Linnaeus in the eigh- teenth century (see Chapter 2).

Today, basic physical similarities are still considered a good starting point. But for similarities to be useful, they must reflect evolutionary descent. For example, the bones of the forelimb of all air-breathing vertebrates initially adapted to terrestrial (land) environ- ments are so similar in number and form (Fig. 5-2) that the obvious expla- nation for the striking resemblance is that all four kinds of these “four- footed” (tetrapod) vertebrates ulti- mately derived their forelimb struc- ture from a common ancestor. What’s more, recent discoveries of remarkably well-preserved fossils from Canada have provided exciting new evidence of how the transition from aquatic to land living took place and what the earliest land vertebrates looked like (Daeschler et al., 2006; Shubin et al., 2006).

How could such seemingly major evolutionary modifications in struc- ture occur? They quite likely began

classification In biology, the order- ing of organisms into categories, such as orders, families, and genera, to show evolu- tionary relationships.

Chordata the phylum of the animal kingdom that includes vertebrates.

vertebrates animals with segmented, bony spinal columns; these include fishes, amphibians, reptiles (including birds), and mammals.

Dorine Essumang

Principles of Classification 109

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chapter 5 Macroevolution: Processes of Vertebrate and Mammalian Evolution 110

with only relatively minor genetic changes. For example, recent research shows that forelimb development in all vertebrates is directed by just a few regulatory genes, called Hox genes (see Chapter 3; Shubin et al., 1997; Riddle and Tabin, 1999). A few mutations in certain Hox genes in early vertebrates led to the basic limb plan seen in all subsequent vertebrates. With further small mutations in these genes or in the genes they regulate, the varied structures that make up the wing of a chicken, the flipper of a porpoise, or the upper limb of a human developed. You should recognize that basic genetic regulatory mechanisms are highly con- served in animals; that is, they’ve been maintained relatively unchanged for hundreds of millions of years. Like a musical score with a basic theme, small variations on the pattern can produce the various “tunes” that differenti- ate one organism from another. This is the essential genetic foundation for most macroevolutionary change; it is a crucial point, showing how we quite

easily connect biologically with other life-forms and how our and their evo- lutionary histories are part of the same grand story of life on earth (see “A Closer Look, Evo-Devo: The Evolution Revolution” on pages 82–83).

Structures that are shared by species on the basis of descent from a com- mon ancestor are called homologies. Homologies alone are reliable indica- tors of evolutionary relationship, but we have to be careful not to draw hasty conclusions from superficial similari- ties. For example, both birds and but- terflies have wings, but they shouldn’t be grouped together on the basis of this single characteristic; butterflies (as insects) differ dramatically from birds in several other, even more fundamen- tal ways. (For example, birds have an internal skeleton, central nervous sys- tem, and four limbs; insects don’t.)

Here’s what’s happened in evolution- ary history: From quite distant ances- tors, both butterflies and birds devel- oped wings independently. So their (superficial) similarities are a product of separate evolutionary responses to roughly similar functional demands. Such similarities, based on indepen- dent functional adaptation and not on shared evolutionary descent, are called analogies. The process that leads to the development of analogies (also called analogous structures) such as wings in birds and butterflies is termed homoplasy.

Making Connections: Constructing Classifications and Interpreting Evolutionary Relationships

Evolutionary biologists typically use two major approaches, or “schools,” when they interpret evo- lutionary relationships with the goal

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homologies Similarities between organisms based on descent from a com- mon ancestor.

analogies Similarities between organ- isms based strictly on common function, with no assumed common evolutionary descent.

homoplasy (homo, meaning “same,” and plasy, meaning “growth”) the separate evolutionary development of similar charac- teristics in different groups of organisms.

Making Connections: Constructing Classifications and Interpreting Evolutionary Relationships 111

of producing classifications. The first approach, called evolutionary systematics, is the more traditional. The second approach, called cladis- tics, has emerged primarily in the last three decades. Although aspects of both approaches are still used by most evolutionary biologists, in recent years cladistic methodologies have predomi- nated among anthropologists. Indeed, one noted primate evolutionist com- mented that “virtually all current stud- ies of primate phylogeny involve the methods and terminology” of cladistics (Fleagle, 1999, p. 1).

Comparing Evolutionary Systematics with Cladistics Before we begin drawing distinctions between these two approaches, it’s first helpful to note features shared by both evolutionary systematics and cladis- tics. First, both schools are interested in tracing evolutionary relationships and in constructing classifications that reflect these relationships. Second, both schools recognize that organisms must be compared using specific fea- tures (called characters) and that some of these characters are more informa- tive than others. And third (deriving directly from the previous two points), both approaches focus exclusively on homologies.

But these approaches also have some significant differences—in how charac- ters are chosen, which groups are com- pared, and how the results are inter- preted and eventually incorporated into evolutionary schemes and clas- sifications. The primary difference is that cladistics more explicitly and rig- orously defines the kinds of homolo- gies that yield the most useful informa- tion. For example, at a very basic level, all life (except for some viruses) shares DNA as the molecule underlying all organic processes. However, beyond inferring that all life most likely derives from a single origin, the mere pres- ence of DNA tells us nothing further regarding more specific relationships among different kinds of life-forms.

To draw further conclusions, we must look at particular characters that cer- tain groups share as the result of more recent ancestry.

This perspective emphasizes an important point: Some homologous characters are much more informative than others. We saw earlier that all ter- restrial vertebrates share homologies in the number and basic arrangement of bones in the forelimb. Even though these similarities are broadly useful in showing that these large evolution- ary groups (amphibians, reptiles, and mammals) are all related through a dis- tant ancestor, they don’t provide infor- mation we can use to distinguish one group from another (a reptile from a mammal, for example). These kinds of characters (also called traits) that are shared through such remote ancestry are said to be ancestral, or primitive. We prefer the term ancestral because it doesn’t reflect negatively on the evo- lutionary value of the character in question. In biological anthropology, the term primitive or ancestral sim- ply means that a character seen in two organisms is inherited in both of them from a distant ancestor.

In most cases, analyzing ances- tral characters doesn’t supply enough information to make accurate evo- lutionary interpretations of relation- ships between different groups. In fact, misinterpretation of ancestral charac- ters can easily lead to quite inaccurate evolutionary conclusions. Cladistics focuses on traits that distinguish par- ticular evolutionary lineages; such traits are far more informative than ancestral traits. Lineages that share a common ancestor are called a clade, giving the name cladistics to the field that seeks to identify and interpret these groups. It is perhaps the most fundamental point of cladistics that evolutionary groups (that is, clades) all share one common ancestor and are thus said to be monophyletic. If a pro- posed evolutionary grouping is found to have more than one ancestor (rather than a single one shared by all mem- bers), it is said to be polyphyletic, and

evolutionary systematics a tra- ditional approach to classification (and evo- lutionary interpretation) in which presumed ancestors and descendants are traced in time by analysis of homologous characters.

cladistics an approach to clas- sification that attempts to make rigorous evolutionary interpretations based solely on analysis of certain types of homologous characters (those considered to be derived characters).

ancestral referring to characters inherited by a group of organisms from a remote ancestor and thus not diagnostic of groups (lineages) that diverged after the character first appeared; also called primitive.

clade a group of organisms sharing a common ancestor. the group includes the common ancestor and all descendants.

monophyletic referring to an evolu- tionary group (clade) composed of descen- dants all sharing a common ancestor.

polyphyletic referring to an evolu- tionary group composed of descendants with more than one common ancestor (and thus not a true clade).

Dorine Essumang

112

Evo-Devo: The Evolution Revolution

In chapter 4, you learned how, in the 1930s, scientists came to a better understanding of evolution once they real- ized that Mendel’s principles and natural selection were both essential components of the process. this merger of ideas was a major step in evolutionary science, and with the discovery of the structure of DNa in 1953, the foundations of evolutionary biol- ogy were firmly established.

almost half a century after the structure of the DNa molecule was revealed, another merger of disciplines occurred (Goodman and coughlin, 2000). In 1999, the field of evolutionary developmental biology, or evo- devo, was created by uniting evolutionary biology with developmental biology. this combination resulted directly from research demonstrating that major evolutionary transformations involve changes in the very same regulatory genes that direct embryo- logical development. the main goals of evo-devo are to discover how animals are put together and how the genes that control their development can, over time, produce new species.

right now, there are millions of animal species (including insects and marine life), but they probably represent less than 1 percent of all the species that have ever existed on earth (carroll et al., 2001). In spite of how diverse these species are, they share many anatomical similarities. they’re all bilaterally symmetrical, meaning that one side is like the other except for certain aspects of internal organs. also, and this is important, they all have a modular body plan made up of repeated segments. arthropods (invertebrates with jointed feet, including all insects, spiders, and crustaceans) have segmented bodies and legs; and many have segmented wings, which are ultimately derived from leg-like appendages (Fig. 1).

Vertebrates also have segmented body parts, and this segmentation begins with the development of the head and vertebral column. although the number of vertebrae and the number of each type of vertebra vary among species, the spine is made of repeated segments (Fig. 2).

Individual body parts are also modular. In humans, upper arms and thighs have one bone; forearms and lower legs have two; wrists and ankles have eight and seven, respectively; and hands and feet have five digits (see Fig. 5-2 and appendix a). While snakes, whales, and dolphins don’t have legs and feet, they’re descended from animals that did. Moreover, some of these species, such as pythons and whales, have skeletal pelvic remnants.

We know that during embryonic development, bodies are formed accord- ing to a pattern that characterizes each species; and that pattern is dictated by a species’ genome. Because of advances in comparative genomics, we also now know that the coding sequences of even distantly related species are very similar. For example, around 99 percent of mouse genes have a human counterpart (Mouse Genome Sequencing consortium, 2002). So, what is it that makes us so different from mice?

Until about 25 years ago, biologists thought that changes in protein-coding genes were the key to evolutionary change,

but now it’s clear that changes in regulatory genes are the real answer to the ques- tion of how macroevolution occurs. DNa sequences of regulatory genes don’t differ greatly among species; however (and this is key), these genes do differ when it comes to when, where, and how long they func- tion. and these differences lead to major physical differences, because anatomical development depends on genes turning on and off at different times and in differ- ent places. there are many different kinds of regulatory genes, and they all instruct cells to make proteins (and different kinds of rNa) that in turn modulate the activity of yet other genes. regulatory genes can be thought of as switches that turn other genes on or off at specific times in specific parts of the body (carroll et al., 2008).

Many evolutionary biologists refer to the group of body-building regulatory genes as the genetic tool kit. It is highly conserved and is shared by all vertebrates and inver- tebrates. through the roughly 600 million years of animal evolution, many of the genes that make up the tool kit have been some- what changed by mutation and many have duplicated to produce families of genes. But given the amount of time and the huge array of descendant species, changes in the DNa sequences of tool kit genes have been extraordinarily minimal. consequently, the roughly 10 percent of your genome that consists of regulatory genes has almost

A Closer Look

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Making Connections: Constructing Classifications and Interpreting Evolutionary Relationships 113

113

exactly the same DNa sequences as the regulatory genes of mice. It goes without saying that the tool kit genes serve as the best example of biological continuity among all animals, living and extinct. You should now be able to appreciate these most basic connections that link all animals, including us, with one another.

the genetic tool kit is composed of genes that make two basic kinds of proteins: transcription factors and signal- ing molecules. here we’re focusing on transcription factors, protein molecules that bind to specific DNa segments called enhancers or promoters. By binding to enhancers, transcription factors switch genes on and off, and they also determine how long those genes produce proteins.

Many transcription factors are produced by homeobox genes. these genes contain a highly conserved region of 180 nucleotides called the homeobox, and this sequence codes for the proteins that bind to enhanc- ers. there are several families of genes that contain homeoboxes; the most familiar one is called Hox for short.

as we discussed in chapter 3, Hox genes direct the early stages of embryonic development. Initially, they establish the identity of regions of the body and the pat- tern of structures along the main body axis that runs lengthwise through the embryo. these structures are actually early precur- sors to the head and vertebral column. Later in development, these same genes establish where limb buds will form and also determine limb polarity (that is, front, back, and sides). Mutations in these genes cause the transformation of one body part to another; we’ve learned about the most famous of these transformations from experiments on fruit flies, in which induced mutations cause all sorts of bizarre phe- notypes (such as legs where antennae should be).

Most invertebrates have 10 Hox genes, fruit flies have 8, but vertebrates have more. Mammals, for example, have 39, located on four different chromosomes.

the reason vertebrates have more Hox genes than insects do is that, over time, the invertebrate versions have duplicated in vertebrates. From these observations, we can see that vertebrate Hox genes are descended from invertebrate Hox genes. Just to illustrate how conserved these genes are, many experiments have shown them to be interchangeable between species. For example, one study showed that fruit flies can function normally with Hox proteins derived from chick embryos (Lutz et al., 1996). this remarkable similarity indicates that these genes haven’t changed much since fruit flies and chickens last shared a common ancestor some 600 millions years ago (ayala and rzhetskydagger, 1998).

the science of evo-devo allows us, for the first time, to understand how morpho- logical change and macroevolution can occur through the action of the genes that make up the genetic tool kit. this under- standing has been made possible through the recently developed techniques of gene cloning and comparative genomics. By adding the evidence provided by evo- devo to comparative anatomy and fossil studies, scientists are on the threshold of demonstrating how evolution has worked

to produce the spectacular biological diversity we see today. the key to this great puzzle is to understand that it all derives from simple beginnings with a set of genes that have been shared by all ani- mals for hundreds of millions of years. as charles Darwin said in the last paragraph of Origin of Species, “there is grandeur in this view of life . . . from so simple a beginning endless forms most beautiful and most wonderful have been, and are being evolved.” this quotation has been a favorite of biologists and anthropolo- gists, not only for its eloquence, but also because we’ve long known that over many millions of years, life-forms have become more complex. For 150 years, we’ve explained this increased complexity in terms of natural selection, and we still do. But now we have the tools we need to reveal the very mechanism that allowed complexity to develop in the first place.

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chapter 5 Macroevolution: Processes of Vertebrate and Mammalian Evolution 114

it represents neither a well-defined clade nor an evolutionary group actu- ally separate from other ones. We’ll encounter problems of exactly this nature in Chapter 6, when we tackle the classification of a small primate called a tarsier as well as that of the great apes.

When we try to identify a clade, the characters of interest are said to be derived, or modified. Thus, while the general ancestral bony pattern of the forelimb in land vertebrates doesn’t allow us to distinguish among them, the further modification of this pattern in certain groups (as hooves, flippers, or wings, for instance) does.

An Example of Cladistic Analysis: The Evolutionary History of Cars and Trucks A simplified example might help clarify the basic principles used in cla- distic analysis. Figure 5-3a shows a hypothetical “lineage” of passenger vehicles. All of the “descendant” vehi- cles share a common ancestor, the pro- totype passenger vehicle. The first major division (I) differentiates pas- senger cars from trucks. The second split/diversification (II) is between lux- ury cars and sports cars (you could, of course, imagine many other subcate- gories). Derived characters that might distinguish trucks from cars could include type of frame, suspension, wheel size, and, in some forms, an open cargo bed. Derived characters that might distinguish sports cars from lux- ury cars could include engine size and type, wheel base size, and a decorative racing stripe.

Now let’s assume that you’re pre- sented with an “unknown” vehicle (that is, one as yet unclassified). How do you decide what kind of vehicle it is? You might note such features as four wheels, a steering wheel, and a seat for the driver, but these are ancestral char- acters (found in the common ances- tor) of all passenger vehicles. If, how- ever, you note that the vehicle lacks a cargo bed and raised suspension (so it’s

not a truck) but has a racing stripe, you might conclude that it’s a car, and more than that, a sports car (since it has a derived feature presumably of only that group).

All this seems fairly obvious, and you’ve probably noticed that this simple type of decision making characterizes much of human mental organization. Still, we frequently deal with compli- cations that aren’t so obvious. What if you’re presented with a sports util- ity vehicle (SUV) with a racing stripe (Fig. 5-3b)? SUVs are basically trucks; the presence of the racing stripe could be seen as a homoplasy with sports cars. The lesson here is that we need to be careful, look at several traits, decide which are ancestral and which are derived, and finally try to recognize the complexity (and confusion) introduced by homoplasy.

Our example of passenger vehicles is useful up to a point. Because it con- cerns human inventions, the groupings possess characters that humans can add and delete in almost any combina- tion. Naturally occurring organic sys- tems are more limited in this respect. Any species can possess only those characters that have been inherited from its ancestor or that have been subsequently modified (derived) from those shared with the ancestor. So any modification in any species is con- strained by that species’ evolutionary legacy—that is, what the species starts out with.

Using Cladistics to Interpret Real Organisms Another example, one drawn from paleontological (fossil) evidence of actual organisms, can help clarify these points. Most people know something about dinosaur evolution, and some of you may know about the recent contro- versies surrounding this topic. There are several intriguing issues concern- ing the evolutionary history of dino- saurs, and recent fossil discoveries have shed considerable light on them. Here we consider one of the more fascinat-

derived (modified) referring to characters that are modified from the ancestral condition and thus diagnostic of particular evolutionary lineages.

Making Connections: Constructing Classifications and Interpreting Evolutionary Relationships 115

ing questions: the relationship of dino- saurs to birds.

Traditionally, it was thought that birds were a quite distinct group from reptiles and not especially closely relat- ed to any of them (including extinct forms, such as the dinosaurs; Fig. 5-4a). Still, the early origins of birds were clouded in mystery and have been much debated for more than a century. In fact, the first fossil evidence of a very primitive bird (now known to be about 150 million years old) was discovered in 1861, just two years following Darwin’s publication of Origin of Species. Despite some initial and quite remarkably accu- rate interpretations linking these early birds to dinosaurs, most experts con- cluded that there was no close relation- ship. This view persisted through most of the twentieth century. But discover- ies made in the last two decades have supported the hypothesis that birds are closely related to some dinosaurs. Two developments in particular have influenced this change of opinion: the remarkable discoveries in the 1990s from China, Madagascar, and else- where and the application of cladistic methods to the interpretation of these and other fossils. (Here’s another exam- ple of how new discoveries as well as new approaches can become the basis for changing hypotheses.)

Recent finds from Madagascar of chicken-sized, primitive birds dated to

70–65 million years ago (mya) show an elongated second toe (similar, in fact, to that in the dinosaur Velociraptor, made infamous in the film Jurassic Park). Indeed, these primitive birds from Madagascar show many other similarities to Velociraptor and its close cousins, which together comprise a group of small- to medium-sized ground-living, carnivorous dinosaurs called theropods. Even more extraor- dinary finds have been unearthed recently in China, where the traces of what were once feathers have been found embossed in fossilized sedi- ments! For many researchers, these new finds have finally solved the mys- tery of bird origins (Fig. 5-4b), lead- ing them to conclude that “birds are not only descended from dinosaurs, they are dinosaurs (and reptiles)—just as humans are mammals, even though people are as different from other mammals as birds are from other rep- tiles” (Padian and Chiappe, 1998, p. 43).

There are some doubters who remain concerned that the presence of feathers in dinosaurs (145–125 mya) might simply be a homoplasy (that is, these creatures may have devel- oped the trait independently from its appearance in birds). Certainly, the possibility of homoplasy must always be considered, as it can add consider- ably to the complexity of what seems like a straightforward evolutionary

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Luxury cars

Sports cars

Trucks

SUVs

Cars

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theropods Small- to medium-sized ground-living dinosaurs, dated to approxi- mately 150 mya and thought to be related to birds.

chapter 5 Macroevolution: Processes of Vertebrate and Mammalian Evolution 116

interpretation. Indeed, strict cladis- tic analysis assumes that homoplasy is not a common occurrence; if it were, perhaps no evolutionary interpreta- tion could be very straightforward! In the case of the proposed relation- ship between some (theropod) dino- saurs and birds, the presence of feath- ers looks like an excellent example of a shared derived characteristic, which therefore does link the forms. What’s more, cladistic analysis emphasizes that several characteristics should be examined, since homoplasy might muddle an interpretation based on just one or two shared traits. In the bird/ dinosaur case, several other character-

istics further suggest their evolution- ary relationship.

One last point must be mentioned. Traditional evolutionary systematics illustrates the hypothesized evolution- ary relationships using a phylogeny, more properly called a phylogenetic tree. Strict cladistic analysis, how- ever, shows relationships in a clado- gram (Fig. 5-5). If you examine the charts in Figures 5-4 and 5-5, you’ll see some obvious differences. A phy- logenetic tree incorporates the dimen- sion of time, as shown in Figure 5-4 (you can find many other examples in this and upcoming chapters). A clado- gram doesn’t indicate time; all forms

▲�Figure 5-4 Evolutionary�rela- tionships�of�birds�and�dinosaurs.� (a) Traditional�view,�showing�no�close� relationship.�(b)�Revised�view,�show- ing�common�ancestry�of�birds�and� dinosaurs.

65 mya

150 mya

250 mya

Time (millions of years ago)

Common land vertebrate ancestor

Common land vertebrate (tetrapod)

ancestor

Mammals Mammals

Birds

Lizards, snakes

Reptiles

Turtles

Birds

Dinosaurs

Crocodiles

Amphibians Amphibians

Reptiles

▼�Figure 5-5 This�cladogram�shows� the�relationships�of�birds,�dinosaurs,� and�other�terrestrial�vertebrates.� Notice�that�there’s�no�time�scale,�and� both�living�and�fossil�forms�are�shown� along�the�same�dimension—that�is,� ancestor-descendant�relationships� aren’t�indicated.�The�chart�is�slightly� simplified,�as�there�are�other�branches� (not�shown)�within�the�reptiles�(with� birds�slightly�more�closely�related�to� crocodiles�than�to�other�reptiles,�such� as�snakes�and�lizards).

Mammals Birds Other reptiles

(crocodiles, snakes, etc.)Amphibians Other

dinosaurs Theropod dinosaurs

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shared derived relating to spe- cific character traits shared in common between two life-forms and considered the most useful for making evolutionary interpretations.

phylogenetic tree a chart showing evolutionary relationships as determined by evolutionary systematics. It contains a time component and implies ancestor- descendant relationships.

cladogram a chart showing evolution- ary relationships as determined by cladistic analysis. It’s based solely on interpretation of shared derived characters. It contains no time component and does not imply ancestor-descendant relationships.

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Definition of Species 117

(fossil and modern) are shown along one dimension. Phylogenetic trees usu- ally attempt to make some hypotheses regarding ancestor-descendant rela- tionships (for example, theropods are ancestral to modern birds). Cladistic analysis (through cladograms) makes no attempt whatsoever to discern ancestor-descendant relationships. In fact, strict cladists are quite skeptical that the evidence really permits such specific evolutionary hypotheses to be scientifically confirmed (because there are many more extinct species than liv- ing ones).

In practice, most physical anthro- pologists (and other evolutionary biolo- gists) utilize cladistic analysis to identi- fy and assess the utility of traits and to make testable hypotheses regarding the

relationships between groups of organ- isms. They also frequently extend this basic cladistic methodology to further hypothesize likely ancestor-descendant relationships shown relative to a time scale (that is, in a phylogenetic tree). In this way, aspects of both traditional evolutionary systematics and cladis- tic analysis are combined to produce a more complete picture of evolutionary history.

Definition of Species

Whether biologists are doing a cla-distic or more traditional phy- logenetic analysis, they’re comparing groups of organisms—that is, different species, genera (sing., genus), families,

Comparing Two Approaches to Interpretation of Evolutionary Relationships

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At a Glance

evolutionary biologists evolutionary biologists

classification using potentially all homologous characters

classification using only specifically chosen derived characters

Generalizations of evolutionary relationships

Development of phylogenetic chart showing relationships (i.e., hypothesized ancestor-

descendant links) through time

Development of cladogram; no ancestor- descendant relationships hypothesized; time

dimension not shown

Development of biodiversity

evolution of life Evolutionary Systematics Cladistics

Observation Observation

chapter 5 Macroevolution: Processes of Vertebrate and Mammalian Evolution 118

lation A will not mate with individu- als from B (Fig. 5-6). As time passes (perhaps hundreds or thousands of generations), genetic differences will accumulate in both populations. If population size is small, we can assume that genetic drift will also cause allele frequencies to change in both popula- tions. And because drift is random, we wouldn’t expect the effects to be the same. Consequently the two popula- tions will begin to diverge genetically.

As long as gene exchange is limited, the populations can only become more genetically different over time. What’s more, further difference can be expect- ed if the baboon groups are occupy- ing slightly different habitats. These additional genetic differences would be incorporated through the process of natural selection. Certain individuals in population A would be more repro- ductively fit in their own environment, but they would show less reproduc- tive success in the environment occu- pied by population B. So allele frequen- cies will shift further, resulting in even greater divergence between the two groups.

With the cumulative effects of genetic drift and natural selection act- ing over many generations, the result will be two populations that—even if they were to come back into geograph- ical contact—could no longer inter- breed. More than just geographical iso-

orders, and so forth. Fundamental to all these levels of classification is the most basic, the species. It’s appropri- ate, then, to ask how biologists define species. We addressed this issue briefly in Chapter 1, where we used the most common definition, one that empha- sizes interbreeding and reproductive isolation. While it’s not the only defi- nition of species (others are discussed shortly), this view, called the biologi- cal species concept (Mayr, 1970), is the one preferred by most zoologists.

To understand what species are, you might consider how they come about in the first place—what Darwin called the “origin of species.” This most fundamental of macroevolution- ary processes is called speciation. According to the biological species concept, the way new species are first produced involves some form of isola- tion. Picture a single species (baboons, for example) composed of several pop- ulations distributed over a wide geo- graphical area. Gene exchange between populations (gene flow) will be limited if a geographical barrier, such as an ocean or a large river, effectively sepa- rates these populations. This extremely important form of isolating mecha- nism is called geographical isolation.

If one baboon population (A) is sep- arated from another baboon popula- tion (B) by a river that has changed course, individual baboons of popu-

B A and B have not yet diverged.

A and B are just beginning to diverge.

A and B have diverged to a point where they’re no longer able to reproduce; speciation is complete.

Some isolation

More isolation

A B A

B A

Complete isolation

▲�Figure 5-6 This�speciation�model� illustrates�branching�evolution,�or� cladogenesis,�which�is�caused�by� increasing�reproductive�isolation.

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biological species concept a depiction of species as groups of individuals capable of fertile interbreeding but repro- ductively isolated from other such groups.

speciation the process by which a new species evolves from an earlier spe- cies. Speciation is the most basic process in macroevolution.

Interpreting Species and Other Groups in the Fossil Record 119

lation might now apply. There may, for instance, be behavioral differences that interfere with courtship—what we call behavioral isolation. Using our biologi- cal definition of species, we would now recognize two distinct species where initially only one existed.

Another related process that can contribute to the further differentia- tion of populations into incipient spe- cies concerns mate recognition. This is sometimes called the recognition species concept, though the cru- cial process, again, concerns reproduc- tion (that is, who’s mating with whom; Ridley, 1993).

Assume, in our baboon example, that some isolation has already occurred and that phenotypic (and genotypic) differences are beginning to be established between two popu- lations. In this situation, coloration patterns of faces or the size, location, coloration, or even smell of the female genital swelling might vary from group to group. If so, then a female from population A might not recognize a male from population B as an appro- priate mate (and vice versa, of course). Natural selection would quickly favor such discrimination if hybrids were less reproductively successful than within- population crosses. Indeed, once such “selective breeding” became estab- lished, speciation would be accelerated considerably.

Another definition of species focuses primarily on natural selection and emphasizes that speciation is the result of influences of varied habitats. In this view, called the ecological species concept, a species is defined as a group of organisms exploiting a single niche. Also called an ecologi- cal niche, this is the physical as well as biological position of an organism within the biological world (that is, within the full ecosystem).

For each population, the ecological niche will vary slightly, and different phenotypes will be slightly more advantageous in each. For example, one population might be more arboreal and another more terrestrial; but there

would not be an intermediate popula- tion equally successful on the ground and in the trees.

In recent years, the ecological spe- cies concept has attracted support from several evolutionary biologists, especially among physical anthropolo- gists. While the biological species con- cept emphasizes gene flow and repro- ductive isolation, the ecological species concept stresses the role of natural selection. Clearly, our approach in this text has been to focus on the evolution- ary contribution of natural selection; thus, the ecological species concept has much to offer here. Nevertheless, our understanding of species need not entail an either-or choice between the biological species concept and the eco- logical species concept. Some popula- tion isolation could indeed begin the process of speciation, and at this stage, the influence of genetic drift could be crucial. The process might then be fur- ther influenced by mate recognition as well as by natural selection as individ- uals in different populations adapt to varying environments.

Interpreting Species and Other Groups in the Fossil Record

Throughout much of this text, we’ll be using various taxonomic terms for fossil primates (including fossil hominins). You’ll be introduced to such terms as Proconsul, Sivapithecus, Aus- tralopithecus, and Homo. Of course, Homo is still a living primate. But it’s especially difficult to make these types of designations from remains of ani- mals that are long dead (and only par- tially preserved as skeletal remains). In these contexts, what do such names mean in evolutionary terms?

Our goal in applying species, genus, or other taxonomic labels to groups of organisms is to make meaningful biological statements about the varia- tion that’s represented. As we look at

recognition species concept a depiction of species in which the key aspect is the ability of individuals to identify members of their own species for purposes of mating (and to avoid mating with mem- bers of other species). In theory, this type of selective mating is a component of a species concept emphasizing mating and is therefore compatible with the biological species concept.

ecological species concept the concept that a species is a group of organisms exploiting a single niche. this view emphasizes the role of natural selec- tion in separating species from one another.

ecological niche the position of a species within its physical and biologi- cal environments. a species’ ecological niche is defined by such components as diet, terrain, vegetation, type of predators, relationships with other species, and activ- ity patterns, and each niche is unique to a given species. together, ecological niches make up an ecosystem.

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chapter 5 Macroevolution: Processes of Vertebrate and Mammalian Evolution 120

populations of living or long-extinct animals, we are certainly going to see variation; this happens in any sexually reproducing organism due to recom- bination (see Chapter 3). As a result of recombination, each individual organism is a unique combination of genetic material, and the uniqueness is often reflected to some extent in the phenotype.

Besides such individual variation, we see other kinds of systematic varia- tion in all biological populations. Age changes alter overall body size, as well as shape, in many mammals. One per- tinent example for fossil human and ape studies is the change in number, size, and shape of teeth from decidu- ous teeth, also known as baby or milk teeth (only 20 teeth are present) to the permanent dentition (32 are present). It would be an obvious error to dis- tinguish two fossil forms based solely on such age-dependent criteria. If one individual were represented just by milk teeth and another (seemingly very different) individual just by adult teeth, they could easily be different-aged individuals from the same population. Researchers dealing with fragmen- tary remains must be alert to varia- tion of this sort. Otherwise, one could make such a silly mistake as think- ing that pieces of a two-year-old were from a different species than his or her mother!

Variation due to sex also plays an important role. Differences in physi- cal characteristics between males and females of the same species, called sex- ual dimorphism, can result in marked variation in body size and proportions in adults of the same species (we’ll discuss this important topic in more detail in Chapter 6).

Recognition of Fossil Species Keeping in mind all the types of vari- ation present within interbreeding groups of organisms, the minimum biological category we’d like to define

in fossil primate samples is the species. As already defined (according to the biological species concept), a species is a group of interbreeding or poten- tially interbreeding organisms that is reproductively isolated from other such groups. In modern organisms, this concept is theoretically testable by observations of reproductive behavior. In animals long extinct, such obser- vations are obviously impossible. Our only way, then, of getting a handle on the variation we see in fossil groups is to refer to living animals.

In studying a fossil group, we may observe obvious variation, such as some individuals being larger and with bigger teeth than others. The ques- tion then becomes: What’s the bio- logical significance of this varia- tion? Two possibilities come to mind. Either the variation is accounted for by individual, age, and sex differences seen within every biological species (that is, it is intraspecific), or the vari- ation represents differences between reproductively isolated groups (that is, it is interspecific). To decide which answer is correct, we have to look at contemporary species.

If the amount of variation we observe in fossil samples is compara- ble to that seen today within species of closely related forms, then we shouldn’t “split” our sample into more than one species. We must, however, be care- ful in choosing modern analogues because rates of evolution vary among different groups of mammals. So, for example, in studying extinct fossil pri- mates, we must compare them with well-known modern primates. Even so, studies of living groups have shown that defining exactly where species boundaries begin and end is often dif- ficult. In dealing with extinct species, the uncertainties are even greater. In addition to the overlapping patterns of variation spatially (over space), varia- tion also occurs temporally (through time). In other words, even more vari- ation will be seen in paleospecies, since individuals may be separat-

sexual dimorphism Differences in physical characteristics between males and females of the same species. For example, humans are slightly sexually dimorphic for body size, with males being taller, on average, than females of the same population. Sexual dimorphism is very pro- nounced in many species, such as gorillas.

intraspecific Within species; refers to variation seen within the same species.

interspecific Between species; refers to variation beyond that seen within the same species to include additional aspects seen between two different species.

paleospecies Species defined from fossil evidence, often covering a long time span.

Dorine Essumang

Interpreting Species and Other Groups in the Fossil Record 121

ed by thousands or even millions of years. Applying a strict Linnaean tax- onomy to such a situation presents an unavoidable dilemma. Standard Linnaean classification, designed to take account of variation present at any given time, describes a static situa- tion. But when we deal with paleospe- cies, the time frame is expanded and the situation can be dynamic (that is, later forms might differ from earlier forms). In such a dynamic situation, taxonomic decisions (where to draw species boundaries) are ultimately going to be somewhat arbitrary.

Because the task of interpreting paleospecies is so difficult, paleoan- thropologists have sought various solutions. Most researchers today define species using clusters of derived traits (identified cladistically). But owing to the ambiguity of how many derived characters are required to identify a fully distinct species (as opposed to a subspecies), the frequent mixing of characters into novel combi- nations, and the always difficult prob- lem of homoplasy, there continues to be disagreement. A good deal of the dispute is driven by philosophical ori- entation. Exactly how much diver- sity should one expect among fos- sil primates, especially among fossil hominins?

Some researchers, called “split- ters,” claim that speciation occurred frequently during hominin evolu- tion, and they often identify numer- ous fossil hominin species in a sample being studied. As the nickname sug- gests, these scientists are inclined to split groups into many species. Others, called “lumpers,” assume that specia- tion was less common and see much variation as being intraspecific. These scientists lump groups together, so that fewer hominin species are identified, named, and eventually plugged into evolutionary schemes. As you’ll see in the following chapters, debates of this sort pervade paleoanthropology, per- haps more than in any other branch of evolutionary biology.

Recognition of Fossil Genera The next and broader level of taxo- nomic classification, the genus (pl., genera), presents another challenge for biologists. To have more than one genus, we obviously must have at least two species (reproductively isolated groups), and the species of one genus must differ in a basic way from the spe- cies of another genus. A genus is there- fore defined as a group of species com- posed of members more closely related to each other than they are to species from any other genus.

Grouping species into genera can be quite subjective and is often much debated by biologists. One possible test for contemporary animals is to check for results of hybridization between individuals of different species—rare in nature but quite common in captiv- ity. If members of two normally sepa- rate species interbreed and produce live (though not necessarily fertile) off- spring, the two parental species are probably not too different genetically and should therefore be grouped in the same genus. A well-known example of such a cross is horses with donkeys (Equus caballus × Equus asinus), which normally produces live but sterile off- spring (mules).

As previously mentioned, we can’t perform breeding experiments with extinct animals, which is why another definition of genus becomes highly rel- evant. Species that are members of the same genus share the same broad adap- tive zone. An adaptive zone represents a general ecological lifestyle more basic than the narrower ecological niches characteristic of individual species. This ecological definition of genus can be an immense aid in interpreting fos- sil primates. Teeth are the most fre- quently preserved parts, and they often can provide excellent general ecologi- cal inferences. Cladistic analysis also helps scientists to make judgments about evolutionary relationships. That is, members of the same genus should

genus (pl., genera) a group of closely related species.

chapter 5 Macroevolution: Processes of Vertebrate and Mammalian Evolution 122

all share derived characters not seen in members of other genera.

As a final comment, we should stress that classification by genus is not always a straightforward decision. For instance, in emphasizing the very close genetic similarities between humans (Homo sapiens) and chimpanzees (Pan troglodytes), some current research- ers (Wildman et al., 2003) place both in the same genus (Homo sapiens, Homo troglodytes). This philosophy has caused some to advocate for extension of basic human rights to great apes (as proposed by members of the Great Ape Project). Such thinking might startle you. Of course when it gets this close to home, it’s often difficult to remain objective!

What Are Fossils and How Do They Form?

Much of what we know about the history of life comes from study- ing fossils, which are traces of ancient organisms and can be formed in many ways. The oldest fossils found thus far date back more than 3 billion years; because they are the remains of micro- organisms, they are extremely small and are called microfossils.

These very early traces of life are fragile and very rare. Most of our evi- dence comes from later in time and usu- ally in the form of pieces of shells, bones, or teeth, all of which, even in a living animal, were already partly made of mineral, giving them a head start in the fossilization process. After the organism died, these “hard” tissues were further impregnated with other minerals, being eventually transformed into a stonelike composition in a process called miner- alization (Fig. 5-7).

There are, however, many other ways in which life-forms have left traces of their existence. Sometimes insects were trapped in tree sap, which later became hardened and chemically altered. Because there was little or no

oxygen inside the hardened amber, the insects have remained remarkably well preserved for millions of years, even with soft tissue and DNA still present (Fig. 5-8). This fascinating circum- stance led author Michael Crichton to conjure the events depicted in the novel (and motion picture) Jurassic Park.

Dinosaur footprints as well as much more recent hominin tracks, leaf imprints in hardened mud or similar impressions of small organ- isms, and even the traces of dino- saur feathers—all of these are fossils. Recently, beautifully preserved thero- pod dinosaur feathers have been dis- covered in northeastern China (dated to approximately 125 mya). These remains are so superbly preserved that even microscopic cell structures have been indentified. These tiny structures directly influenced feather color in ancient dinosaurs; what’s more, these same structures influence feather color in modern birds. Researchers are now able to deduce that some stripes in the feathers of one dinosaur were chestnut/ reddish brown in color (Zhang et al., 2010)!

A spectacular discovery of a 47- million-year-old early primate fos- sil was widely publicized in 2009. This fossil is remarkable, preserving more than 95 percent of the skeleton as well as outlines of soft tissue and even fos- silized remains of digestive tract con- tents (see Chapter 8) (Franzen et al., 2009). The amazing preservation of this small primate occurred because it died on the edge of a volcanic lake and was quickly covered with sediment. It reminds us that whether a dead animal will become fossilized and how much of it will be preserved depends partly on how it dies, but even more on where it dies.

Some ancient organisms have left vast amounts of fossil remains. Indeed, limestone deposits can be hundreds of feet thick and are largely made up of fossilized remains of marine shell- fish (see Chapter 2). However, fossils of land animals are not nearly so com-

fossils traces or remnants of organisms found in geological beds on the earth’s surface.

mineralization the process in which parts of animals (or some plants) become transformed into stonelike structures. Mineralization usually occurs very slowly, as water carrying minerals—such as silica or iron—seeps into the tiny spaces within a bone. In some cases, the original minerals within the bone or tooth can be completely replaced, molecule by molecule, with other minerals.

What Are Fossils and How Do They Form? 123

mon. After an animal dies—let’s say it’s an early hominin from 2 mya—it will probably be eaten; then its bones will be scattered and broken and even- tually decompose. After just a few weeks, there will be hardly anything left to fossilize. But suppose, by chance, this recently deceased hominin were quickly covered by sediment, perhaps by sand and mud in a streambed or

along a lakeshore or by volcanic ash from a nearby volcano. As a result, the long, slow process of mineralization might eventually turn at least some parts of the hominin into a fossil.

The study of how bones and other materials come to be buried in the earth and preserved as fossils is called taphonomy (from the Greek taphos,

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▲ Figure 5-7 Examples of mineralized fossils. (a) A mineralized snake caste from geological deposits in Wyoming (dated to about 50 mya). (b) A fossil dragonfly from Brazil, dated to more than 100 mya. (c) An early primate skull from Egypt, dated to about 30 mya. (d) A fossil fish (a relative of the piranha) from the same deposits as the snake above (also dated to approximately 50 mya). (e) A nautilus, a relative of living snails. (f) A fossilized skull of a hominin from East Africa, dated to 2.5 mya.

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taphonomy The study of how bones and other materials come to be buried in the earth and preserved as fossils.

chapter 5 Macroevolution: Processes of Vertebrate and Mammalian Evolution 124

meaning “study of the grave”). Such studies focus on everything that hap- pens to an organism once it has died, making it the life history of the dead, so to speak. Among the topics that tapho- nomists try to understand are process- es of sedimentation and burial, includ- ing the action of streams, preservation properties of bone, and carnivore dis- turbance factors.

Humans Are Vertebrates: Distant Connections

Biologists must contend with not only the staggering array of liv- ing and extinct life-forms but also the vast amount of time that life has been evolving on earth. Again, scientists have devised simplified schemes—but in this case to organize time, not bio- logical diversity.

Geologists have formulated the geological time scale (Fig. 5-9), in which very large time spans are orga- nized into eras that include one or more periods. Periods, in turn, can be broken down into epochs. For the time span encompassing vertebrate evolu- tion, there are three eras: the Paleozoic,

Mesozoic, and Cenozoic. The earli- est vertebrates are present in the fossil record dating to early in the Paleozoic at 500 mya, and their origins are prob- ably much older. It’s the vertebrates’ capacity to form bone that accounts for their more complete fossil record after 500 mya.

During the Paleozoic, several vari- eties of fishes (including the ances- tors of modern sharks and bony fishes), amphibians, and reptiles appeared. At the end of the Paleozoic, close to 250 mya, several varieties of mammal-like reptiles were also diversifying. It’s gen- erally thought that some of these forms ultimately gave rise to the mammals.

The evolutionary history of ver- tebrates and other organisms dur- ing the Paleozoic and Mesozoic was profoundly influenced by geographi- cal events. We know that the positions of the earth’s continents shifted dra- matically during the last several hun- dred million years. This process, called continental drift, is explained by the geological theory of plate tectonics, which states that the earth’s crust is a series of gigantic moving and colliding plates. Such massive geological move- ments can induce volcanic activity (as, for example, all around the Pacific Rim), mountain building (for exam- ple, the Himalayas), and earthquakes.

▶�Figure 5-8 A�spider�fossilized�in� amber.

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geological time scale the orga- nization of earth history into eras, periods, and epochs; commonly used by geologists and paleoanthropologists.

continental drift the movement of continents on sliding plates of the earth’s surface. as a result, the positions of large landmasses have shifted drastically during the earth’s history.

Dorine Essumang

Humans Are Vertebrates: Distant Connections 125

Living on the juncture of the Pacific and North American plates, residents of the Pacific coast of the United States are acutely aware of some of these con- sequences, as illustrated by the explo- sive volcanic eruption of Mt. St. Helens and the frequent earthquakes in Alaska and California.

While reconstructing the earth’s physical history, geologists have deter- mined the earlier, much altered posi- tions of major continental landmasses. During the late Paleozoic, the con- tinents came together to form a sin-

gle colossal landmass called Pangea. (In real- ity, the continents had been drifting on plates, coming together and separating, long before the end of the Paleozoic around 225 mya.) During the early Mesozoic, the southern continents (South America, Africa, Antarctica, Australia, and India) began to split off from Pangea, forming a large southern continent called Gondwanaland (Fig. 5-10a). Similarly, the northern continents (North America, Greenland, Europe,

570 mya 500 mya 430 mya 395 mya 345 mya 190 mya 136 mya 65 mya 0 mya225 mya280 mya

Cambrian 570

Ordovician 500

PALEOZOIC MESOZOIC

Silurian 430

Devonian 395

Carboniferous 345

Permian 280

Jurassic 190

Cretaceous 136

Triassic 225

Holocene 0.01

Pleistocene 1.8

Pliocene 5

Miocene 23

Oligocene 33

Eocene 56

Paleocene 65

Major extinction event

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ERA

▼ Figure 5-9 Geological time scale.

◀ Figure 5-10 Continental drift. (a) Positions of the continents during the Mesozoic (ca. 125 mya). Pangea is breaking up into a northern land- mass (Laurasia) and a southern land- mass (Gondwanaland). (b) Positions of the continents at the beginning of the Cenozoic (ca. 65 mya).

L A U R A S I A EURASIA

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INDIA

MADAGASCAR

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G O N D W A N A L A N D

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and Asia) were consolidated into a northern landmass called Laurasia. During the Mesozoic, Gondwanaland and Laurasia continued to drift apart and to break up into smaller segments. By the end of the Mesozoic (about 65 mya), the continents were begin- ning to assume their current positions (Fig. 5-10b).

The evolutionary ramifications of this long-term continental drift were profound. Groups of animals became effectively isolated from each other by oceans, significantly influenc- ing the distribution of mammals and

other land vertebrates. These conti- nental movements continued in the Cenozoic and indeed are still happen- ing, although without such dramatic results.

During most of the Mesozoic, rep- tiles were the dominant land verte- brates; they exhibited a broad expan- sion into a variety of ecological niches, which included aerial and marine hab- itats. The most famous of these highly successful Mesozoic reptiles were the dinosaurs, which themselves evolved into a wide array of sizes and species and adapted to a variety of lifestyles.

Deep Time

The vast expanse of time during which evolution has occurred on earth stag- gers the imagination. Indeed, this funda- mental notion of what John Mcphee has termed “deep time” is not really understood or, in fact, widely believed. Of course as we’ve emphasized beginning in chapter 1, belief, as such, is not part of science. But observation, theory building, and testing are. Still, in a world populated mostly by nonscientists, the concept of deep time, crucial as it is to geology and anthropology, is resisted by many people. this situation really isn’t surprising; the very notion of deep time is in many ways counterintui- tive. human beings tend to measure their existence in months, years, and the span of human lifetimes.

But what are these durations as measured against geological or galactic phenomena? In a real sense, these vast time expanses are beyond human com- prehension. We can reasonably fathom the reaches of human history stretching to about 5,000 years ago. In a leap of imagi- nation, we can perhaps even begin to grasp the stretch of time back to the cave painters of France and Spain, approximately 17,000

to 25,000 years ago. how do we relate, then, to a temporal span that’s 10 times this one, back to 250,000 years ago, about the time of the earliest Homo sapiens—or to 10 times this span to 2,500,000 years ago (about the time of the appear- ance of our genus, Homo)? and when we multiply this last duration another 1,000 times (to 2,500,000,000), we’re back to a time of fairly early life- forms. We’d have to reach still further into earth’s past, another 1.5 billion years, to approach the earliest documented life.

the dimensions of these intervals are humbling to say the least. the discovery in the nineteenth century of deep time (see chapter 2), what the late Stephen Jay Gould called “geology’s greatest contribu- tion to human thought,” plunged one more dagger into humanity’s long-cherished view of itself as something special. astronomers had previously established how puny our world was in the physical expanse of space, and then geologists showed that even on our own small planet we were but residues

dwarfed within a river of time “without a vestige of a beginning or prospect of an end” (from James hutton, a founder of modern geology and one of the discoverers of deep time). It’s no wonder that people resist the concept of deep time; it not only stupefies our reason but implies a sense of collective meaninglessness and reinforces our individual mortality. Geologists, astron- omers, and other scholars have struggled for over a century, with modest success, to

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A Closer Look

Humans Are Vertebrates: Distant Connections 127

translate the tales told in rocks and hurtling stars into terms that everyone could understand. Various analogies have been attempted—metaphors, really—drawn from common experience. among the most successful of these attempts is a “cosmic

calendar” devised by eminent astronomer carl Sagan in his book Dragons of Eden (1977). In this version of time’s immensity, Sagan likens the passage of geological time to that of one calendar year. the year begins on January 1 with the Big Bang, the

cosmic explosion marking the beginning of the universe and the beginning of time. In this version, the Big Bang is set at 15 billion years ago,* with some of the major events in the geological past as follows:

* recent evidence gathered by the hubble Space telescope has questioned the established date for the Big Bang. however, even the most recent data are somewhat contradictory, suggesting a date from as early as 16 billion years ago (indicated by the age of the oldest stars) to as recent as 8 billion years ago (indicated by the rate of expansion of the universe). here we’ll follow the conventional dating of 15 billion years; if you apply the most conservative approximation (8 billion years), the calibrations shift as follows: 1 day = 22,000,000 years; 1 hour = 913,000 years; 1 minute = 15,000 years. Using these calculations, for example, the first hominins appear on December 31 at 7:37 p.m., and modern humans (Homo sapiens) are on the scene at 11:42 p.m.

Time Unit Conversion Using the Cosmic Calendar

1 year = 15,000,000,000 years 1 hour = 1,740,000 years 1 month = 1,250,000,000 years 1 minute = 29,000 years 1 day = 41,000,000 years 1 second = 475 years

Big Bang January 1 Formation of the earth September 14 Origin of life on earth (approx.) September 25 Significant oxygen atmosphere begins to develop December 1 precambrian ends; paleozoic begins; December 17 invertebrates flourish paleozoic ends and Mesozoic begins December 25 cretaceous period: first flowers; December 28 dinosaurs become extinct Mesozoic ends; cenozoic begins; December 29 adaptive radiation of placental mammals

December 31 Events appearance of early hominoids 12:30 p.m. (apes and humans) First hominins 9:30 p.m. extensive cave painting in europe 11:59 p.m. Invention of agriculture 11:59:20 p.m. renaissance in europe; Ming 11:59:59 p.m. dynasty in china; emergence of scientific method Widespread development of NOW: the first science and technology; second of the emergence of a global culture; New Year first steps in space exploration; mass extinctions caused by humans

Dinosaur paleontology, never a boring field, has advanced several startling notions in recent years: that many dinosaurs were “warm-blooded”; that some varieties were quite social and probably also engaged in consider- able parental care; that many forms became extinct because of major cli- mate changes to the earth’s atmo- sphere from collisions with comets or asteroids; and, finally, that not all dinosaurs became entirely extinct and have many descendants still liv- ing today (that is, all modern birds). (See Fig. 5-11 for a summary of major

events in early vertebrate evolutionary history.)

The Cenozoic is divided into two periods, the Tertiary (about 63 mil- lion years in duration) and the Quaternary, from about 1.8 mya up to and including the present (see Fig. 5-9). Paleontologists often refer to the next, more precise level of subdivision within the Cenozoic as the epochs. There are seven epochs within the Cenozoic: the Paleocene, Eocene, Oligocene, Miocene, Pliocene, Pleistocene, and Holocene, the last often referred to as the Recent epoch.

epochs categories of the geological time scale; subdivisions of periods. In the cenozoic era, epochs include the paleocene, eocene, Oligocene, Miocene, and pliocene (from the tertiary period) and the pleistocene and holocene (from the Quaternary period).

chapter 5 Macroevolution: Processes of Vertebrate and Mammalian Evolution 128

Humans Are Also Mammals: Closer Connections

We can learn about mammalian evolution from fossils as well as from studying the DNA of living spe- cies (Bininda-Emonds et al., 2007). Studies using both of these approaches suggest that all the living groups of mammals (that is, all the orders) had diverged by 75 mya. Only later, several million years following the beginning of the Cenozoic, did the various cur- rent mammalian subgroups (that is, the particular families) begin to diversify.

Today there are over 4,000 species of mammals, and we could call the Cenozoic the Age of Mammals. It is during this era that, along with birds, mammals replaced earlier reptiles as the dominant land-living vertebrates.

How do we account for the rela- tively rapid success of the mammals during the late Mesozoic and early Cenozoic? Several characteristics relat- ing to learning and general flexibility of behavior are of prime importance. Mammals were selected for larger brains than those typically found in reptiles, making them better equipped to process information. In particu- lar, the cerebrum became generally enlarged, especially the outer covering, the neocortex, which controls higher brain functions (Fig. 5-12). In some mammals, the cerebrum expanded so much that it came to constitute most of the brain volume; the number of sur-

face convolutions also increased, cre- ating more surface area and thus pro- viding space for even more nerve cells (neurons). As we’ll see in Chapter 6, this trend is even further emphasized among the primates.

For such a large and complex organ as the mammalian brain to develop, a longer, more intense period of growth is required. Slower development can occur internally (in utero) as well as after birth. Internal fertilization and internal development aren’t unique to mammals, but the latter was a major innovation among terrestrial verte- brates. Other forms (most fishes and reptiles—including birds) lay eggs, and “prenatal” development occurs externally, outside the mother’s body. Mammals, with very few exceptions, give birth to live young. Even among mammals, however, there’s consider- able variation among the major groups in how mature the young are at birth; in placental mammals, including ourselves, in utero development goes farthest.

Another distinctive feature of mam- mals is the dentition. While many liv- ing reptiles (such as lizards and snakes) consistently have similarly shaped teeth (called a homodont dentition), mammals have differently shaped teeth (Fig. 5-13). This varied pattern, termed a heterodont dentition, is reflected in the ancestral (primitive) mammalian arrangement of teeth, which includes three incisors, one canine, four premo- lars, and three molars in each quarter of the mouth. So, with 11 teeth in each

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Cambrian

Trilobites abundant; also brachiopods, jellyfish, worms, and other invertebrates

Ordovician Silurian Devonian Carboniferous

First fishes; trilobites still abundant; graptolites and corals become plentiful; possible land plants

Jawed fishes appear; first air-breathing animals; definite land plants

Age of Fishes; first amphibians and first forests appear

First reptiles; radiation of amphibians; modern insects diversify

570 mya 500 mya 430 mya 395 mya 345 mya

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PALEOZOIC

neocortex the more recently evolved portions of the cortex of the brain that are involved with higher mental functions and composed of areas that integrate incoming information from different sensory organs.

placental a type (subclass) of mam- mal. During the cenozoic, placentals became the most widespread and numer- ous mammals and today are represented by upward of 20 orders, including the primates.

heterodont having different kinds of teeth; characteristic of mammals, whose teeth consist of incisors, canines, premo- lars, and molars.

Dorine Essumang

Humans Are Also Mammals: Closer Connections 129

quarter of the mouth, the ances- tral mammalian dental complement includes a total of 44 teeth. Such a heterodont arrangement allows mammals to process a wide variety of foods. Incisors are used for cut- ting, canines for grasping and pierc- ing, and premolars and molars for crushing and grinding.

A final point regarding teeth relates to their disproportionate rep- resentation in the fossil record. As the hardest, most durable portion of a vertebrate skeleton, teeth have the greatest likelihood of becoming fos- silized (that is, mineralized), because teeth are predominantly composed of mineral to begin with. As a result, the vast majority of available fos- sil data for most vertebrates, including primates, consists of teeth.

Another major adaptive complex that distinguishes contemporary mam- mals from reptiles (except birds) is the maintenance of a constant internal body temperature. Known colloquially (and incorrectly) as warm- bloodedness, this crucial physiological adaptation is also seen in contemporary birds and may have characterized many dino- saurs as well. Except for birds, reptiles maintain a constant internal body tem- perature through exposure to the sun; these reptiles are said to be ectother- mic. In mammals and birds, however, energy is generated internally through metabolic activity (by processing food or by muscle action); for this reason, mammals and birds are said to be endothermic.

Olfactory lobe

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Cerebrum Cerebellum

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Reptile radiation; mammal- like reptiles appear

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Great Age of Dinosaurs; flying and swimming dinosaurs appear; first toothed birds

Placental and marsupial mammals appear; first modern birds

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MESOZOIC

Major extinction

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Major extinction

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endothermic (endo, meaning “within” or “internal”) able to maintain internal body temperature by producing energy through metabolic processes within cells; characteristic of mammals, birds, and perhaps some dinosaurs.

Dorine Essumang

chapter 5 Macroevolution: Processes of Vertebrate and Mammalian Evolution 130

The Emergence of Major Mammalian Groups

There are three major subgroups of living mammals: the egg- laying mammals, or monotremes; the pouched mammals, or marsupials; and the placental mammals. The mono- tremes, of which the platypus is one example (Fig. 5-14), are extremely primitive and are considered more dis- tinct from marsupials or placentals

than these two subgroups are from each other. The recent sequencing

of the full genome of the platypus (Warren et al., 2008) has con- firmed the very ancient orgins of the monotremes and their distinctiveness from other mammals.

The most notable difference between marsupials and pla-

centals concerns fetal develop- ment. In marsupials, the young

are born extremely immature and must complete development in an

external pouch (Fig. 5-15). But pla- cental mammals develop over a longer

period of time in utero, made possible by the evolutionary development of a specialized tissue (the placenta) that provides for fetal nourishment.

With a longer gestation period, the central nervous system develops more completely in the placental fetus. What’s more, after birth, the “bond of milk” between mother and young allows more time for complex neu- ral structures to form. We should also emphasize that from a biosocial per- spective, this dependency period not only allows for adequate physiologi- cal development but also provides for a wider range of learning stimuli. That is, a vast amount of information is chan- neled to the young mammalian brain through observation of the mother’s behavior and play with age-mates. It’s not enough to have evolved a brain capable of learning. Collateral evo- lution of mammalian social systems has ensured that young mammallian brains are provided with ample learn- ing opportunities and are thus put to good use.

Processes of Macroevolution

As we noted earlier, evolution oper-ates at both micro- and macro- evolutionary levels. We discussed evolution primarily from a microevo- lutionary perspective in Chapter 4; in this chapter, our focus is on macroevo- lution. Macroevolutionary mechanisms operate more on the whole species than on individuals or populations, and they take much longer than microevolu- tionary processes to have a noticeable impact.

Adaptive Radiation As we mentioned in Chapter 2, the potential capacity of a group of organ- isms to multiply is practically unlim- ited, but its ability to increase its numbers is regulated largely by the availability of resources (food, water,

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Processes of Macroevolution 131

shelter, mates, and space). As popula- tion size increases, access to resources decreases, and the environment will ultimately prove inadequate. Depleted resources induce some members of a population to seek an environment in which competition is reduced and the opportunities for survival and repro- ductive success are increased. This evolutionary tendency to exploit unoc- cupied habitats can eventually produce an abundance of diverse species.

This story has been played out countless times during the history of life, and some groups have expanded extremely rapidly. Known as adaptive radiation, this evolutionary process can be seen in the divergence of the stem reptiles into the profusion of dif- ferent forms of the late Paleozoic and especially those of the Mesozoic. It’s a process that takes place when a life- form rapidly takes advantage, so to speak, of the many newly available eco- logical niches.

The principle of evolution illustrat- ed by adaptive radiation is fairly sim- ple, but important. It may be stated this way: A species or group of species will diverge into as many variations as two factors allow. These factors are (1) its adaptive potential and (2) the adaptive opportunities of the available niches.

In the case of reptiles, there was lit- tle divergence in the very early stages of evolution, when the ancestral form was little more than one among a variety of amphibian water dwellers. Later, a more efficient egg (one that could incu- bate out of water) developed in reptiles; this new egg, with a hard, watertight shell, had great adaptive potential, but initially there were few zones to invade. When reptiles became fully terres- trial, however, a wide array of ecologi- cal niches became accessible to them. Once freed from their attachment to water, reptiles were able to exploit landmasses with no serious compe- tition from any other animal. They moved into the many different ecologi- cal niches on land (and to some extent in the air and sea), and as they adapt- ed to these areas, they diversified into

a large number of species. This spec- tacular radiation burst forth with such evolutionary speed that it may well be termed an adaptive explosion.

Of course, the rapid expansion of placental mammals during the late Mesozoic and throughout the Cenozoic is another excellent exam- ple of adaptive radiation. The world- wide major extinction event at the end of the Mesozoic, as the dinosaurs dis- appeared, left thousands of econiches vacant. Small-bodied, mostly noctur- nal mammals had been around for at least 70 million years, and once they were no longer in competition with the dinosaurs, they were free to move into previously occupied habitats. Thus, over the course of several million years, there was a major adaptive radiation of mammals as they diversified to exploit previously unavailable habitats.

Generalized and Specialized Characteristics Another aspect of evolution closely related to adaptive radiation involves the transition from generalized char- acteristics to specialized characteris- tics. These two terms refer to the adap- tive potential of a particular trait. A trait that’s adapted for many functions is said to be generalized, whereas one that’s limited to a narrow set of func- tions is said to be specialized.

For example, a generalized mamma- lian limb has five fairly flexible digits adapted for many possible functions (grasping, weight support, and dig- ging). In this respect, human hands are still quite generalized. On the other hand (or foot), there have been many structural modifications in our feet to make them suited for the specialized function of stable weight support in an upright posture.

The terms generalized and special- ized are also sometimes used when speaking of the adaptive potential of whole organisms. Consider, for exam- ple, the aye-aye of Madagascar, an unusual primate species. The aye-aye adaptive radiation the relatively

rapid expansion and diversification of life- forms into new ecological niches.

chapter 5 Macroevolution: Processes of Vertebrate and Mammalian Evolution 132

is a highly specialized animal, structurally adapted to a nar-

row, rodent/woodpecker- like econiche—digging

holes with prominent incisors and removing insect larvae with an elongated bony finger (Fig. 5-16).

It’s important to note that only a gen-

eralized ancestor can provide the flexible evo-

lutionary basis for rapid diversification. Only a gener-

alized species with potential for adaptation to varied ecological niches can lead to all the later diversification and specialization of forms into partic- ular ecological niches.

An issue that we’ve already raised also bears on this discussion: the rela- tionship of ancestral and derived char- acters. It’s not always the case, but ancestral characters usually tend to be more generalized. And special- ized characteristics are nearly always derived as well.

Working Together: Microevolution and Macroevolution

For many years, evolutionary biolo-gists generally agreed that micro- evolutionary mechanisms could be translated directly into the larger-scale macroevolutionary changes, especially the most central of all macroevolution- ary processes, speciation. However, four decades ago, some leading evolu- tionary biologists challenged this tradi- tional view.

Over the last 40 years evolutionary biologists have debated whether there are fundamental differences between the processes of micro- as compared with macroevolution. This discus- sion continues, and divergent views,

framed as specific hypotheses, are fur- ther tested against new evidence. At present, the major difference seems to be one of scale. That is, both processes are driven by similar factors; however, macroevolution takes much longer than microevolution to occur.

For example, several species of very early hominins evolved over more than 4 million years, initially separat- ing from their common ancestor with chimpanzees, and some of these species eventually adapted to more ground- living niches. These changes clearly reflect macroevolutionary processes. Much more recently, some modern human populations adapted in just a couple of thousand years to living at high altitudes, which was made possible by changes in particular genes. This is a good example of microevolution.

We should note that rates of evo- lutionary change can speed up at cer- tain times and slow down during oth- ers. Most crucially, natural selection is influenced by how fast the environ- ment is changing (and how fast genetic changes appear and spread within a species). Both fossil and molecular evi- dence (Pagel et al., 2006) indicate that both gradual (slow) and rapid (also called “punctuated”) changes have occurred in the evolution of both plant and animal species.

In all lineages, the pace assuredly speeds up and slows down due to fac- tors that influence the size and rela- tive isolation of populations. As we’ve said, environmen tal changes that influ- ence the pace and direction of natu- ral selection must also be considered. So, in general accordance with the Modern Synthesis and as indicated by molecular evidence, microevolution and macro evolution needn’t be consid- ered separately, as some evolutionary biologists have suggested. Some groups of primates, for instance, simply have slower or faster durations of specia- tion, which is why Old World monkeys typically speciate more slowly than the great apes.

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133Critical Thinking Questions

We know about earlier life-forms directly from fos- sils, of which tens of trillions have formed over the vast time that life has existed on earth. We also know about “deep time” in earth’s geological history, and the age when fossils formed over the last 3 billion years, from studies made by geologists who use precise dat-

ing techniques (the latter to be discussed in Chapter 9). Connections among all these life forms and how humans fit in are interpreted from the analysis of spe- cific types of similarities called shared derived charac- teristics. From such data, hypotheses regarding evolu- tionary relationships are proposed and tested.

How Do We Know?

▶▶ Evolutionary systematics and cladistics are the two major types of classification. Evolutionary systematics uses homologous characteristics to make hypotheses regarding evolutionary rela- tionships as well as ancestor-descendant relation- ships and shows the latter through time as a phy- logenetic tree. Cladistics more rigorously uses only specific sorts of homologous characteris- tics (derived ones) and doesn’t attempt to draw ancestor-descendant conclusions or show evolu- tionary relationships through time; conclusions are shown in a cladogram.

▶▶ According to the biological species concept, spe- cies are groups of individuals capable of fertile interbreeding but are reproductively isolated from other such groups. There are also other definitions of species suggested by biologists, but this one is the most widely used.

▶▶ Vertebrates are animals with a segmented back- bone (vertebral column), a developed brain, and

paired sensory structures. Vertebrates include fishes, amphibians, reptiles (including birds), and mammals.

▶▶ Humans are placental mammals that (along with some other mammals) are characterized by devel- opment in utero (that is, live birth), differently shaped (heterodont) teeth, more complex brains, and maintenance of a constant internal body tem- perature (endothermic). Placental mammals in particular have even more complex brains (with a large neocortex), longer periods of development, and more complex social behavior.

▶▶ Macroevolution takes many hundreds or thou- sands of generations and can result in the appear- ance of new species (a process called speciation). Microevolution can occur within just a few gen- erations and results in small genetic differences between populations of a species.

Summary of Main Topics

1. Remains of a fossil mammal have been found on your campus. If you adopt a cladistic approach, how would you determine (a) that it’s a mammal rather than some other kind of vertebrate, (b) what kind of mammal it is, and (c) how it might be related to one or more living mammals?

2. For the same fossil find (and your interpretation) in question 2, draw an interpretive figure using cladistic analysis (that is, draw a cladogram). Next, using more traditional evolutionary systematics, construct a phylogenetic tree. Last, explain the dif- ferences between the cladogram and the phyloge-

netic tree (be sure to emphasize the fundamental ways in which the two schemes differ).

3. a. Humans are fairly generalized mammals. What do we mean by this, and what specific features (characters) would you select to illustrate this statement?

b. More precisely, humans are placental mam- mals. How do humans and all other placen- tal mammals differ from the other two major groups of mammals?

Critical Thinking Questions

Because humans are primates, we share many biological characteristics with other

primate species.

Connections

Humans are both verte- brates and mammals, and their evolutionary history

over many millions of years explains our early roots.

Partly because of common evolutionary history, many human behaviors are also

seen in other primates.

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After mastering the material in this chapter, you should be able to:

▶ �Discuss the major categories of nonhuman primates and how they differ from one another.

▶ �Describe the major characteristics of primates.

▶ �Explain why humans are considered primates.

▶ �Understand why it is important to study nonhuman primates.

▶ �List some of the many reasons why over half of all nonhuman primate species are threatened or highly endangered today.

135

Chimpanzees aren’t monkeys, and neither are gorillas or orangutans. They’re apes. And even though most people think that monkeys and apes are basically the same, they aren’t. Yet how many times have you seen a greeting card or maga- zine ad with a picture of a chimpanzee and a phrase that says something like, “Don’t monkey around” or “No more monkey business”? Or maybe you’ve seen people at zoos making fun of pri- mates. While these things may seem trivial, they really aren’t, because they demonstrate just how little most peo- ple know about our closest relatives. This is extremely unfortunate, because by better understanding these rela- tives, we can better understand our- selves. And just as important, we can also try to preserve the many nonhu- man primate species that are critically endangered today. Indeed, many will go extinct in the next 30 years or so if steps aren’t taken now to save them.

One way to understand any organ- ism is to compare its anatomy and behavior with that of other closely related species. This comparative approach helps explain how and why physiological and behavioral systems evolved as adaptive responses to vari- ous selective pressures throughout the course of evolution. This statement applies to humans just as it does to any other species. So if we want to identify the components that have shaped the evolution of our species, a good start- ing point is to compare ourselves with our closest living relatives, the nonhu-

6 Survey of the Living Primates

man primates (lemurs, lorises, tarsiers, monkeys, and apes).

Exactly how many nonhuman pri- mate species there are is not entirely clear because the taxonomic status of many groups has not been clari- fied. Furthermore, new species are still being discovered. Between 1990 and 2009, a total of 86 new primate spe- cies and subspecies were described (Mittermeier et al., 2009). While some authors believe that there may be as many as 300 nonhuman primate spe- cies, most feel more comfortable with an estimate of 230 to 270.

This chapter describes the physi- cal characteristics that define the order Primates, gives a brief overview of the major groups of living primates, and introduces some methods currently used to compare living primates genet- ically. (For a comparison of human and nonhuman skeletons, see Appendix A.) But before going any further, we again want to call attention to a few common misunderstandings about evolutionary processes.

Student Learning Objectives

primates Members of the mammalian order Primates (pronounced “pry-may´- tees”), which includes lemurs, lorises, tarsi- ers, monkeys, apes, and humans.

chaPter 6 Survey of the Living Primates 136

Evolution is not a goal- directed process. Therefore the fact that lemurs appeared earlier than anthropoids doesn’t mean that lemurs “progressed” or “advanced” to become anthro- poids. Living primates aren’t in any way “superior” to their evolution- ary predecessors or to one another. Consequently, in discussions of major groupings of contemporary nonhuman primates, there is no implied superior- ity or inferiority of any of these groups. Each lineage or species has come to possess unique qualities that make it better suited to a particular habitat and lifestyle than others. Given that all con- temporary organisms are “successful” results of the evolutionary process, it’s best to completely avoid such loaded terms as superior and inferior. Finally, you shouldn’t make the mistake of thinking that contemporary primates (including humans) necessarily rep- resent the final stage or apex of a lin- eage, because we all continue to evolve as lineages. Actually, the only species that represent final evolutionary stages of particular lineages are those that become extinct.

Primate Characteristics

As you learned in Chapter 5, all pri-mates share many characteristics with other placental mammals. Some of these basic mammalian traits are body hair; a relatively long gestation period followed by live birth; mamma- ry glands (thus the term mammal); dif- ferent types of teeth (incisors, canines, premolars, and molars); the ability to maintain a constant internal body temperature through physiological means, or endothermy (see Chapter 5); increased brain size; and a considerable capacity for learning and behavioral flexibility. So, to differentiate primates as a distinct group from other mam- mals, we must describe those charac- teristics that, taken together, set pri- mates apart.

It isn’t easy to identify single traits that define the primate order because, compared with most mammals, pri- mates have remained quite general- ized. This means that primates have retained several ancestral mammalian traits that many other mammals have lost over time. In response to particu- lar selective pressures, some mamma- lian groups have become increasingly specialized, or derived. For example, through the course of evolution, horses and cattle have undergone a reduc- tion in the number of digits (fingers and toes) from the ancestral pattern of five to one and two, respectively. These species have also developed hard, protective coverings over their feet in the form of hooves (Fig. 6-1a). This foot structure is beneficial in prey species, because their survival depends on speed and stability, but it restricts them to only one type of locomo- tion. Moreover, limb function is lim- ited to support and movement, and the ability to manipulate objects is lost completely.

Primates can’t be defined by one or even a few traits they share in com- mon because they aren’t as special- ized as many mammals. Therefore pri- matologists have drawn attention to a group of characteristics that more or less characterize the entire pri- mate order. Still, these are a set of gen- eral tendencies that are not equally expressed in all primates. In addition, while some of these traits are unique to primates, many others are retained ancestral mammalian characteristics shared with other mammals. The fol- lowing list is meant to give you a gen- eral anatomical and behavioral picture of the primates. Concentrating on cer- tain ancestral mammalian traits along with more specific, derived ones has been the traditional approach of pri- matologists, and it’s still used today. In their limbs and locomotion, teeth, diet, senses, brain, and behavior, primates reflect a common evolutionary history with adaptations to similar environ- mental challenges, primarily as highly social, arboreal animals.

anthropoids Members of the primate infraorder anthropoidea (pronounced “an-throw-poid´-ee-uh”), which includes monkeys, apes, and humans.

Dorine Essumang

Primate Characteristics 137

A. Limbs and Locomotion 1. A tendency toward an erect pos-

ture (especially in the upper body) (derived trait). All primates show this tendency to some degree; it’s variously associated with sitting, leaping, standing, and occasion- ally bipedal walking.

2. A flexible, generalized limb structure, which allows most pri- mates to practice numerous forms of locomotion (ancestral trait). Primates have retained some bones (such as the clav- icle, or collarbone) and cer- tain abilities (like rotation of the forearm) that have been lost in more specialized mammals such as horses (Fig. 6-1a). Various aspects of hip and shoulder morphology provide primates with a wide range of limb movement and function. Thus, by maintaining a general- ized locomotor anatomy, primates aren’t restricted to one form of movement, as are many other mammals. Primates also use their limbs for many activities besides locomotion.

3. Prehensile hands (and sometimes feet) (derived trait). Many animals can manipulate objects, but not as skillfully as primates (Fig. 6-1b). All primates use their hands and frequently their feet to grasp and manipu- late objects. This ability is variably expressed and is enhanced by sev- eral characteristics, including:

a. Retention of five digits on the hands and feet (ancestral trait). This trait varies somewhat throughout the order, with some species having reduced thumbs or second digits.

b. An opposable thumb and, in most species, a divergent and partially opposable big toe (derived trait). Most pri- mates are capable of moving the thumb so that it comes in contact with the second digit or with the palm of the hand (Fig. 6-1c–e).

▲�Figure 6-1 (a) A horse’s front foot, homologous with a human hand, has undergone reduction from five digits to one. (b) Although raccoons are capable of consid- erable manual dexterity and can easily pick up small objects with one hand, they have no opposable thumb. (c) Many monkeys are able to grasp objects with an oppos- able thumb, whereas others have very reduced thumbs. (d) Humans are capable of a “precision grip.” (e) Chimpanzees, with their reduced thumbs, are capable of a precision grip but frequently use a modified form.

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morphology the form (shape, size) of anatomical structures; can also refer to the entire organism.

chaPter 6 Survey of the Living Primates 138

c. Nails instead of claws (derived trait). This characteristic is seen in all primates except some New World monkeys. All lemurs and lorises also have a claw on one digit.

d. Tactile pads enriched with sen- sory nerve fibers at the ends of digits (derived trait). This char- acteristic enhances the sense of touch.

B. Diet and Teeth 1. Lack of dietary specialization

(ancestral trait). This trait is typi- cal of most primates, who tend to eat a wide assortment of foods. In general, primates are omnivorous.

2. A generalized dentition (ances- tral trait). Primate teeth aren’t specialized for processing only one type of food, a characteristic related to a general lack of dietary specialization.

▶�Figure 6-2 This simplified diagram shows the overlapping visual fields that permit bin- ocular vision in primates with eyes positioned at the front of the face. (The green-shaded area in front of the eyes represents the area of overlap.) Stereoscopic vision (three-dimensional vision) is provided in part by binocular vision and in part by the transmission of visual stimuli from each eye to both hemispheres of the brain. This is illus- trated by the blue and gold lines, represent- ing nerve fibers that transmit information from each eye to visual receiving areas at the rear of both sides of the brain. (In nonprimate mammals, most or all visual information crosses over to the hemisphere opposite the eye in which it was initially received.)

Area in primates where some fibers of optic nerve cross over to the opposite hemisphere

Primary receiving area for visual information

C. The Senses and the Brain. Primates (diurnal ones in par- ticular) rely heavily on vision and less on olfaction, especially when compared with other mammals. This emphasis is reflected in evo- lutionary changes in the skull, eyes, and brain (derived trait).

1. Color vision (derived trait). This is a characteristic of all Old World diurnal primates. Some New World species don’t have the full range of color vision, and noctur- nal primates lack color vision.

2. Depth perception (derived trait). Primates have stereoscopic vision, or the ability to perceive objects in three dimensions. This is made possible through a variety of mechanisms, including:

a. Eyes placed toward the front of the face (not to the sides). This position provides for overlap- ping visual fields, or binocular vision (Fig. 6-2).

b. Visual information from each eye transmitted to visual cen- ters in both hemispheres of the brain. In nonprimate mammals, most optic nerve fibers cross to the opposite hemisphere at the base of the brain. In primates, about 40 percent of the fibers remain on the same side, so that both hemispheres receive much of the same information.

c. Visual information organized into three-dimensional images by specialized structures in the brain itself. The capacity for stereoscopic vision depends on each hemisphere of the brain receiving visual information from both eyes and from over- lapping visual fields.

3. Decreased reliance on the sense of smell (olfaction) (derived trait). This trend is expressed as an over- all reduction in the size of olfac- tory structures in the brain. A cor- responding reduction of the entire olfactory apparatus has also result- ed in decreased size of the snout in most species. This is related to an increased dependence on vision.

omnivorous having a diet consisting of many food types, such as plant materi- als, meat, and insects.

diurnal active during the day.

olfaction the sense of smell.

nocturnal active during the night.

stereoscopic vision the condi- tion whereby visual images are, to varying degrees, superimposed. this provides for depth perception, or viewing the external environment in three dimensions. Stereoscopic vision is partly a function of structures in the brain.

binocular vision Vision character- ized by overlapping visual fields provided by forward-facing eyes. Binocular vision is essential to depth perception.

hemisphere One of the two halves of the cerebrum, which are connected by a dense mass of fibers. (the cerebrum is the large rounded outer portion of the brain.)

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Primate Adaptations 139

Some species, such as baboons, have large muzzles; however, this isn’t related to olfaction but rather to the necessity of accommodating large canine teeth (see “A Closer Look: Primate Cranial Anatomy”).

4. Expansion and increased com- plexity of the brain (derived trait). This is a general trend among pla- cental mammals, but it’s especially characteristic of primates. In pri- mates, this expansion is most evident in the visual and association areas of the neocortex (portions of the brain where information from different sensory modalities is combined). Expansion in regions involved with sensory and motor functions of the hand is seen in many primate spe- cies, particularly humans.

D. Maturation, Learning, and Behavior 1. A more efficient means of fetal

nourishment, longer periods of ges- tation, reduced numbers of off- spring (with single births the norm), delayed maturation, and extension of the entire life span (derived trait).

2. A greater dependence on flex- ible, learned behavior (derived trait). This trend is correlated with delayed maturation and subse- quently longer periods of infant and subadult dependency on at least one parent. Because of these trends, parental investment in each offspring is increased. Although fewer offspring are born, they receive more parental care.

3. The tendency to live in social groups and the permanent associa- tion of adult males with the group (derived trait). Except for some nocturnal species, primates tend to associate with other individuals. Also, the permanent association of adult males with the group is uncommon in most mammals but widespread in primates.

4. The tendency toward diurnal activity patterns (derived trait). This is seen in most primates: Lorises, tarsiers, one monkey spe- cies, and some lemurs are noctur- nal; all the rest (the other monkeys, apes, and humans) are diurnal.

Primate Adaptations

In this section, we consider how pri-mate anatomical traits evolved as adaptations to environmental circum- stances. It’s important to remember that when you see the phrase environ- mental circumstances, it refers to sev- eral interrelated variables, including climate, diet, habitat (woodland, grass- land, forest, and so on), and predation.

Evolutionary Factors Traditionally, the group of charac- teristics shared by primates has been explained as the result of an adapta- tion to arboreal living. While other mammals were adapting to various ground-dwelling lifestyles and even marine environ- ments, the primates found their adaptive niche in the trees. A number of other mammals were also adapting to arboreal living; but though many of them nested in the trees, they continued to for- age for food on the ground (Fig. 6-3). However, through- out the course of evolution, primates increasingly found food (leaves, seeds, fruits, nuts, insects, and small mam- mals) in the trees themselves. Over time, this dietary shift enhanced a general trend toward omnivory, and this trend in turn led to the reten- tion of the generalized dentition that’s characteristic of most primates.

Increased reliance on vision cou- pled with grasping hands and feet are also adaptations to an arboreal life- style. In a complex, three-dimensional environment with uncertain footholds, acute color vision with depth percep- tion is, for obvious reasons, extremely beneficial.

An alternative to this tradition- al arboreal hypothesis is based on the fact that animals such as squirrels are also arboreal, yet they haven’t evolved primate-like adaptations such as pre- hensile hands or forward-facing eyes.

neocortex the more recently evolved portions of the cortex (outer layer) of the brain that are involved with higher mental functions and composed of areas that inte- grate incoming information from different sensory organs.

sensory modalities Different forms of sensation (e.g., touch, pain, pres- sure, heat, cold, vision, taste, hearing, and smell).

arboreal tree living; adapted to life in the trees.

adaptive niche an organism’s entire way of life: where it lives, what it eats, how it gets food, how it avoids predators, and so on.

▼�Figure 6-3 Gray squirrels are extremely well adapted to life in the trees, where they nest, sleep, play, and frequently eat. However, unlike primates, they don’t have color vision or prehensile thumbs and big toes. They also have claws instead of nails.

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But visual predators, such as cats and owls, do have forward-facing eyes, and this fact may provide insight into an additional factor that could have shaped primate evolution.

Actually, forward-facing eyes (which facilitate binocular vision), grasping hands and feet, and the pres- ence of nails instead of claws may not have come about solely as adap- tive advantages in a purely arboreal setting. They may also have been the hallmarks of an arboreal visual pred- ator. So it’s possible that early pri- mates may first have adapted to shrub- by forest undergrowth and the lowest

tiers of the forest canopy, where they hunted insects and other small prey (Cartmill, 1972, 1992). In fact, many smaller primates occupy just such an econiche today.

Sussman (1991) suggested that the basic primate traits were developed in conjunction with another major evolutionary occurrence: the appear- ance of flowering plants, which began around 140 mya. Flowering plants pro- vide numerous resources for primates, including nectar, seeds, and fruits. Sussman argued that since visual pre- dation isn’t common among mod- ern primates, forward-facing eyes,

Primate Cranial Anatomy

Several anatomical features of the cra-nium distinguish primates from other mammals. The mammalian trend toward increased brain development has been fur- ther emphasized in primates, as shown by a relatively enlarged braincase. The primate emphasis on vision is further reflected in generally large eye sockets; the decreased dependence on olfaction is indicated by reduction of the snout and corresponding flattening of the face (Fig. 1).

Here are some of the specific anatomi- cal details seen in modern and most fossil primate crania:

1. The primate face is shortened and the size of the braincase relative to that of the face is enlarged compared with other mammals (see Fig. 1).

2. Unlike the eye sockets seen in other mammals, primate eye sockets are enclosed at the sides by a ring of bone called the postorbital bar (see Fig. 1). Also, in tarsiers, monkeys, apes, and humans, there is a plate of bone at the back of the eye orbit called the postorbital plate, a feature that isn’t

present in lemurs, lorises, and other mammals. The functional significance of these structures hasn’t been thoroughly explained, but it may be related to stresses on the eye orbits imposed by chewing (Fleagle, 1999).

3. The region of the skull that contains the structures of the middle ear is com- pletely encircled by a bony structure called the auditory bulla. In primates, the floor of the auditory bulla is derived from a segment of the temporal bone (Fig. 2). Of all the skeletal structures, most primate paleontologists consider

the postorbital bar and the derivation of the auditory bulla to be the two best diagnostic traits of the primate order.

4. The base of the skull in primates is somewhat flexed, so that the muzzle (mouth and nose) is positioned lower relative to the braincase (Fig. 3). This arrangement provides for the exertion of greater force during chewing, which is particularly needed for crushing and grinding tough vegetable fibers, seeds, and hard-shelled fruits.

A Closer Look

Braincase

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Eye socket No postorbital bar

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◀ Figure 1 The skull of a gibbon (left) com- pared with that of a red wolf (right). Note that the absolute size of the braincase in the gibbon is slightly larger than that of the wolf, even though the wolf (at about 80 to 100 pounds) is six times the size of the gibbon (about 15 pounds).

Primate Adaptations 141

grasping hands and feet, omnivory, and color vision may have arisen in response to the demand for fine visual and tactile discrimination. Certainly this type of discrimination is nec- essary when feeding on small food items such as fruits, berries, and seeds among branches and stems (Dominy and Lucas, 2001).

These hypotheses aren’t mutual- ly exclusive. The complex of primate characteristics might well have origi- nated in nonarboreal settings and cer- tainly could have been stimulated by the new econiches provided by evolv- ing flowering plants. But at some

point primates did take to the trees, and that’s where most of them still live today.

Geographical Distribution and Habitats With just a couple of exceptions, non- human primates are found in tropical or semitropical areas of the New and Old Worlds. In the New World, these areas include southern Mexico, Cen- tral America, and parts of South Amer- ica. Old World primates are found in Africa, India, Southeast Asia (including numerous islands), and Japan (Fig. 6-4).

▲ Figure 2 The base of an adolescent chimpanzee skull. (In an adult animal, the bones of the skull would be fused together and would not appear as separate elements, as shown here.)

▶ Figure 3 The skull of a male baboon (a) compared with that of a red wolf (b). The angle at the base of the baboon skull is due to flexion. The corresponding area of the wolf skull is relatively flat. Note the forward-facing position of the eye orbits above the snout in the baboon. Also note that in the baboon, the enlarged muzzle does not reflect a heavy reli- ance on the sense of smell. Rather, it serves to support very large canine teeth, the roots of which curve back through the bone for as much as 1½ inches. Photos not to scale.

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chaPter 6 Survey of the Living Primates 142

Howler species (Central and South America)

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Spider monkeys and muriquis (Central and South America)

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Primate Adaptations 143

Baboon species (throughout sub-Saharan Africa)

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Colobus species (throughout sub-Saharan Africa)

Tarsier species (southeast Asian islands)

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chaPter 6 Survey of the Living Primates 144

Even though most nonhuman primates are arboreal and live in forest or woodland habitats, some Old World monkeys (for exam- ple, baboons) spend much of the day on the ground. The same is true for the African apes (goril- las, chimpanzees, and bonobos). Nevertheless, all nonhuman pri- mates spend some time in the trees, especially when sleeping.

Diet and Teeth Omnivory is one example of the overall lack of specialization in pri- mates. Although all primates tend to emphasize some food items over others, most eat a combina- tion of fruits, nuts, seeds, leaves, other plant materials, and insects. Many also get animal protein from birds and amphibians. Some (capuchins, baboons, bonobos, and especially chimpanzees) occasion- ally kill and eat small mammals, including other primates. Others, such as African colobus monkeys and the leaf-eating monkeys (lan- gurs) of India and Southeast Asia, have become more specialized and mostly eat leaves.

This wide and varied menu is a good example of the advantages of having a generalized diet, espe- cially in less predictable environ- ments; if one food source fails (for example, during drought or because of human activities), other options may still be avail- able. The downside of being gen- eralized is that there may be com- petition for resources with other species that eat the same things. Specialization, where a species has a narrow ecological niche and eats only one or two things, can be advantageous in this regard because these species don’t have much competition from others; but it can be catastrophic if the food supply disappears.

Like nearly all other mam- mals, primates have four kinds of

teeth: incisors and canines for biting and cutting, and premolars and molars for chewing and grinding. Biologists use what’s called a dental formula to describe the number of each type of tooth that typifies a species. A dental formula indicates the number of each tooth type in each quadrant of the mouth (Fig. 6-5). For example, all Old World anthropoids (monkeys, apes, and humans) have two incisors, one canine, two premolars, and three molars on each side of the midline in both the upper and lower jaws, for a total of 32 teeth. This is represented by the fol- lowing dental formula:

2.1.2.3 (upper) 2.1.2.3 (lower)

The dental formula for a general- ized placental mammal is 3.1.4.3 (three incisors, one canine, four premolars, and three molars). Primates have fewer teeth than this ancestral pattern because of a general evolutionary trend toward fewer teeth in many mammal groups. Consequently the number of each type of tooth varies between lin- eages. For example, in most New World monkeys, the dental formula is 2.1.3.3 (two incisors, one canine, three premo- lars, and three molars).

The overall lack of dietary spe- cialization in primates is reflected in the lack of specialization in the size and shape of the teeth because tooth shape and size are directly related to diet. Carnivores typically have pre- molars and molars with high, pointed cusps adapted for tearing meat; but herbivores, such as cattle and horses, have premolars with broad, flat sur- faces suited to chewing tough grasses and other plant materials. Most pri- mates have premolars and molars with low, rounded cusps—a molar mor- phology that enables them to process most types of foods. So throughout their evolutionary history, the primates have developed a dentition adapted to a varied diet, and the capacity to exploit many foods has contributed to their overall success during the last 50 million years.

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▲�Figure 6-5 (a) The human maxilla illus- trates a dental formula characteristic of all Old World monkeys, apes, and humans. (b) The New World monkey (Cebus) maxilla shows the dental formula typical of most New World monkeys. (Not to scale; the monkey maxilla is actually much smaller than the human maxilla.)

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cusps the bumps on the chewing sur- face of premolars and molars.

Primate Adaptations 145

Locomotion Almost all primates are, at least to some degree, quadrupedal, meaning that they use all four limbs to support the body during locomotion. However, most primates use more than one form of locomotion, and they’re able to do this because of their generalized anatomy.

Vertical clinging and leaping, another form of locomotion, is char- acteristic of some lemurs and tarsiers. As the term implies, vertical clingers and leapers support themselves verti- cally by grasping onto trunks of trees or other large plants while their knees and ankles are tightly flexed (Fig. 6-6). By forcefully extending their long hind limbs, they can spring powerfully away either forward or backward.

Brachiation, or arm swinging, is a suspensory form of locomotion in which the body moves by being alter- natively supported by one forelimb and then the other. (You may have brachiated as a child on “monkey bars” in playgrounds.) Because of anatomi- cal modifications at the shoulder joint, apes and humans are capable of true brachiation. However, only the small gibbons and siamangs of Southeast Asia use this form of locomotion almost exclusively (Fig. 6-7).

Brachiation is seen in species char- acterized by arms longer than legs; a short, stable lower back; long curved fingers; and shortened thumbs. Because these are traits seen in all the apes, it’s believed that although none of the great apes (orangutans, goril- las, bonobos, and chimpanzees) habit- ually brachiates today, they probably inherited these characteristics from brachiating or climbing ancestors.

Some New World monkeys, such as spider monkeys and muriquis, are called semibrachiators because they practice a combination of leaping with some arm swinging. Also, some New World monkeys enhance arm swing- ing and other suspensory behaviors by using a prehensile tail, which serves as an effective grasping fifth hand. It’s

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▲ Figure 6-7 White-handed gibbon brachiating. Note the very long arms and long, curved fingers.

quadrupedal Using all four limbs to support the body during locomotion; the basic mammalian (and primate) form of locomotion.

brachiation Arm swinging, a form of locomotion used by some primates. Brachiation involves hanging from a branch and moving by alternately swinging from one arm to the other.

chapter 6 Survey of the Living Primates 146

important to men- tion here that pre- hensile tails are exclusively a New World phenome- non; they aren’t seen in any Old World primates.

Lastly, all the apes to varying degrees have arms that are longer than legs, and some (gorillas, bonobos, and chimpanzees) practice a special form of quadru- pedalism called knuckle walking. Because their arms are so long relative

to their legs, instead of walking with the palms of their hands flat on the ground as some monkeys do, they sup- port the weight of their upper body on the back surfaces of their bent fingers (Fig. 6-8).

Primate Classification The living primates are commonly categorized into their respective sub- groups, as shown in Figure 6-9. This taxonomy is based on the sys- tem originally established by Linnae- us (see Chapter 2). The primate order, which comprises approximately 230 species, belongs to a larger group, the class Mammalia (see Chapter 5).

In any taxonomic system, as you learned in Chapter 5, animals are organized into increasingly specific categories. For example, the order Primates includes all primates. But at the next level down, the suborder, pri- mates are divided into two smaller categories: Strepsirhini (lemurs and lorises) and Haplorhini (tarsiers, mon- keys, apes, and humans). Therefore the suborder distinction is narrower, or more specific. At the suborder level, the lemurs and lorises are distinct as a group from all the other primates. This classification makes the biologi-

cal and evolutionary statement that all the lemurs and lorises are more closely related to one another than they are to any of the other primates. Likewise, humans, apes, monkeys, and tarsiers are more closely related to one another than they are to the lorises and lemurs.

The taxonomy shown in Figure 6-9 is a modified version of a similar sys- tem that biologists and primatologists have used for decades. The traditional system was based on physical simi- larities between species and lineages. But that approach isn’t foolproof. For instance, some New and Old World monkeys resemble each other anatomi- cally; evolutionarily, however, they’re quite distinct, having diverged from a common ancestor perhaps as long as 40 mya. By considering only physi- cal characteristics, it’s possible to over- look the unknown effects of separate evolutionary history (see the discus- sion of homoplasy in Chapter 5). But thanks to the rapidly growing number of species whose genomes have been sequenced, geneticists can now make direct comparisons between the genes and indeed the entire genetic makeup of different species. This kind of analy- sis, called comparative genomics, gives us a much more accurate picture of evolutionary and biological relation- ships between species than was pos- sible even as recently as the late 1990s. So once again, we see how changing technologies influence the refining of older hypotheses and the development of new ones.

A complete draft sequence of the chimpanzee genome was completed in 2005 (Chimpanzee Sequencing and Analysis Consortium, 2005)— a major milestone in human com- parative genomics. Comparisons of the genomes of different species are extremely important because they reveal such differences in DNA as the number of nucleotide substitutions and/or deletions that have occurred since related species last shared a common ancestor. Geneticists esti- mate the rate at which genes change

▲ Figure 6-8 Chimpanzee knuckle walking. Note how the weight of the upper body is supported on the knuckles and not the palm of the hand.

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Strepsirhini (strep’-sir-in-ee) the primate suborder that includes lemurs and lorises. (colloquial form: strepsirhine.)

Haplorhini (hap’-lo-rin-ee) the primate suborder that includes tarsiers, monkeys, apes, and humans. (colloquial form: haplorhine.)

Primate Adaptations 147

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chaPter 6 Survey of the Living Primates 148

Lemurs and Lorises The suborder Strepsirhini includes the lemurs and lorises, the most non- derived or primitive living primates. Remember that by primitive we mean that lemurs and lorises are more simi- lar anatomically to their earlier mam- malian ancestors than are the other primates (tarsiers, monkeys, apes, and humans). For example, they retain cer- tain ancestral characteristics, such as a more pronounced reliance on olfac- tion. Their greater olfactory capabili- ties (compared with other primates) are reflected in the presence of a moist, fleshy pad, or rhinarium, at the end of the nose and a relatively long snout (Fig. 6-10).

Many other characteristics dis- tinguish lemurs and lorises from the other primates, including eyes placed more to the side of the face, differ- ences in reproductive physiology, and shorter gestation and maturation peri- ods. Lemurs and lorises also have a unique derived trait called a “dental comb” (Fig. 6-11), formed by forward- projecting lower incisors and canines. These modified teeth are used in both grooming and feeding. One other char- acteristic that sets lemurs and lorises apart is the retention of a claw (called a “grooming claw”) on the second toe.

Lemurs Lemurs are found only on the island of Madagascar and adja- cent islands off the east coast of Africa (Fig. 6-12). As the only nonhuman pri- mates on Madagascar, lemurs diversi- fied into many and varied ecological niches without competition from mon- keys and apes. Thus the 103 known lemur species on Madagascar today represent a kind of lost world, an evo- lutionary pattern that vanished else- where. It is a tragedy that, with 91 per- cent of lemur species now threatened with extinction, lemurs are possibly the most endangered group of vertebrates in the world (Mittermeier et al., 2012).

Lemurs range in size from the tiny Madame Berthe’s mouse lemur, with a body length (head and trunk) of only 3 inches, to the indri, with a body length

and then use this information, com- bined with the amount of change they observe, to estimate when related species diverged from their last com- mon ancestor.

Wildman and colleagues (2003) compared nearly 100 human genes with their chimpanzee, gorilla, and orangutan counterparts. Their results supported some earlier stud- ies, which had concluded that humans are most closely related to chimpan- zees and that the protein-coding DNA sequences of the two species are 98.4 to 99.4 percent identical. The results of the study also estimated that the chim- panzee and human lineages diverged between 6 and 7 mya. These results are consistent with the molecular find- ings of several other studies (Chen and Li, 2001; Clark et al., 2003; Steiper and Young, 2006). Other research has sub- stantiated these figures, but it has also revealed more variation in noncod- ing DNA segments and portions that have been inserted, deleted, or dupli- cated. So when the entire genome is considered, reported DNA differences between chimpanzees and humans range from 2.7 percent (Cheng et al., 2005) to 6.4 percent (Demuth et al., 2006). These aren’t substantial differ- ences, but perhaps the most impor- tant discovery of all is that humans have much more non-protein-coding DNA than do the other primates that have thus far been studied. Now that geneticists are beginning to under- stand some of the functions of non- protein-coding DNA, they hope to explain why humans have so much of it and how it makes us different from our closest relatives.

A Survey of the Living Primates

In this section, we discuss the major primate subgroups. Since it’s beyond the scope of this book to cover any spe- cies in great detail, we present a brief description of each major grouping, taking a closer look at the apes.

rhinarium (rine-air´-ee-um) the moist, hairless pad at the end of the nose seen in most mammalian species. the rhinarium enhances an animal’s ability to smell.

A Survey of the Living Primates 149

of 2 to 3 feet (Nowak, 1999). Typically the larger lemurs are diurnal and eat a wide variety of foods, such as leaves, fruits, buds, bark, and shoots, but the tiny mouse and dwarf lemurs are noc- turnal insectivores.

There is a great deal of behavioral variation among lemur species. Some are mostly arboreal, but others, such as ring-tailed lemurs, are more terrestrial. Some arboreal species are quadrupeds, and others (sifakas, ring-tails, and indris) are vertical clingers and leapers (Fig. 6-13). Several species (for exam- ple, ring-tailed lemurs and sifakas) live in groups of 10 to 25 animals com- prising males and females of all ages.

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▲�Figure 6-10 The moist surface of this cow’s nose enhances her sense of smell. Many mam- mals have rhinaria.

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Modern lemurs

A t l a n t i c O c e a n

I n d i a n O c e a n

AFRICA

MADAGASCAR

▲�Figure 6-11 Lemur dental comb, formed by forward-projecting incisors and canines.

Fr ed

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▼�Figure 6-13 Verreaux’s sifakas are another lemur species.

▲�Figure 6-12 Geographical distri- bution of modern lemurs.

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chapter 6 Survey of the Living Primates 150

However, indris are among the few primates that live in social units com- posed of mated pairs and dependent offspring. Additionally, several noctur- nal forms are mostly solitary.

Lorises Lorises (Fig. 6-14), which somewhat resemble lemurs, were able to survive in Africa and Asia by being nocturnal. In this way, they were (and are) able to avoid competition with more recently evolved primates, the diurnal monkeys.

There are at least eight loris species, all of which are found in tropical forest and woodland habitats of India, Sri Lanka, Southeast Asia, and Africa. Also included in the same general cat- egory are six to nine galago species, sometimes called bush babies (Bearder, 1987; Nowak, 1999), which are widely distributed throughout most of the for- ested and woodland savanna areas of sub-Saharan Africa (Fig. 6-15).

Locomotion in some lorises is a slow, cautious, climbing form of qua- drupedalism. All galagos, however, are highly agile vertical clingers and leapers. Some lorises and galagos are almost entirely insectivorous, while others also eat combinations of fruits, leaves, and other plant products. Lorises and galagos frequently forage alone, but feeding ranges can overlap, and two or more females may feed and

even nest together. Females also leave young infants behind in nests while they search for food. Leaving infants alone is extremely uncommon among primates. With these exceptions, all primate infants are always carried by a parent, usually the mother, from the time they’re born.

Lemurs and lorises represent the same general adaptive level. Both groups exhibit good grasping and climbing abilities and a well-developed visual apparatus; however, vision is not completely stereoscopic, and in diurnal species, color vision may not be as well developed as in anthropoids.

Tarsiers There are five recognized tarsier spe- cies (Nowak, 1999), all of which are restricted to islands of Southeast Asia (Malaysia, Borneo, Sumatra, and the Philippines), where they inhabit a wide range of habitats, from tropical forest to backyard gardens (Figs. 6-16 and 6-17). Tarsiers are nocturnal insec- tivores that use vertical clinging and leaping to surprise prey (which may also include small vertebrates) on lower branches and shrubs. They appear to form stable pair bonds, and the basic tarsier social unit is a mated pair and their young offspring (MacKinnon and MacKinnon, 1980).

DL IL

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tle r/

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▲ Figure 6-14 A slow loris in Malaysia. Note the large forward- facing eyes and rhinarium.

▶ Figure 6-15 Galago, or “bush baby.”

A Survey of the Living Primates 151

Tarsiers are highly specialized (derived) animals that have several unique characteristics. In the past, primatologists believed that tarsiers were more closely related to lemurs and lorises than to other primates because they share several traits with them. Consequently they were clas- sified in the same suborder as lemurs and lorises. However, tarsiers actually present a complex blend of characteris- tics not seen in any other primate. One of the most obvious is their enormous eyes, which dominate much of the face and are immobile within their sockets. To compensate for the inability to move their eyes, tarsiers, like owls, can rotate their heads 180 degrees.

In addition, tarsiers possess cer- tain anthropoid characteristics, and DNA studies have indicated that they are more closely related to monkeys, apes, and humans than to lemurs and lorises. Therefore, although there is still some debate as to the taxonomic status of tarsiers, they are now classi- fied in the suborder Haplorhini, along with the anthropoids (see Fig. 6-9 and Appendix A).

Anthropoids: Monkeys, Apes, and Humans Although there is much variation among anthropoids, they share cer- tain features that, taken together, dis- tinguish them as a group from lemurs and lorises. Here’s a partial list of these anthropoid traits:

1. A larger average body size 2. A larger brain in absolute terms

and relative to body weight 3. Reduced reliance on olfaction,

indicated by absence of a rhinarium and a reduction in the relative size of olfactory-related structures in the brain

4. Increased reliance on vision, with forward-facing eyes placed more to the front of the face

5. A greater degree of color vision 6. Back of eye socket protected by a

bony plate 7. Blood supply to the brain different

from that of lemurs and lorises 8. Fusion of the two sides of the man-

dible at the midline to form one bone (in lemurs and lorises, they’re

Tarsiers

ASIA

PHILIPPINES

BORNEOSUMATRA

◀ Figure 6-17 Geographical distribution of the various tar- sier species.

▼ Figure 6-16 Bornean tarsier.

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chaPter 6 Survey of the Living Primates 152

two distinct bones joined by carti- lage at the middle of the chin)

9. More generalized dentition, as seen in the absence of a dental comb and some other features

10. Differences in female internal reproductive anatomy

11. Longer gestation and maturation periods

12. Increased parental care 13. More mutual grooming

Approximately 85 percent of all pri- mates are monkeys and newly discov- ered species are still being described. Monkeys are divided into two groups separated by geographical area (New World and Old World) as well as at least 40 million years of separate evolu- tionary history.

New World Monkeys The approximately 70 New World monkey species can be found in a wide range of arboreal envi- ronments throughout most forested

areas in southern Mexico and Cen- tral and South America (Fig. 6-18). They exhibit a wide range of variation in size, diet, and ecological adaptation (Fig. 6-19). In size, they vary from the tiny marmosets and tamarins (about 12 ounces) to the 20-pound howler monkeys (Figs. 6-20 and 6-21). New World monkeys are almost exclusively arboreal, and some never come to the ground. Like the Old World monkeys, all except one species (the owl monkey) are diurnal.

One characteristic that distinguish- es New and Old World monkeys is the shape of the nose. New World monkeys have broad noses with outward-facing nostrils; Old World monkeys have nar- rower noses with downward-facing nostrils. To verify this, compare the white-faced capuchins in Figure 6-19 with the Sykes monkey in Figure 6-24 or with your own downward-facing nostrils. This difference in nose form has given rise to the terms platyrrhine

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▶�Figure 6-18 Geographical distri- bution of New World monkeys.

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A Survey of the Living Primates 153

▼�Figure 6-19 Some New World monkeys.

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chaPter 6 Survey of the Living Primates 154

(flat-nosed) and catarrhine (downward- facing nose) to refer to New and Old World anthropoids, respectively. The more formal terminology used in pri- mate classification is shown in Fig. 6-9 and will be discussed in more detail in Chapter 8.

In addition to being the smallest of all monkeys, marmosets and tamarins have several other distinguishing fea- tures. They have claws instead of nails, and unlike other primates, they usu- ally give birth to twins instead of a sin-

gle infant. They’re mostly insectivo- rous, although marmosets eat gums from trees and tamarins also eat fruits. Marmosets and tamarins are qua- drupedal, and they use their claws for climbing. These tiny monkeys live in social groups usually composed of a mated pair or a female and two adult males and their offspring. This type of mating pattern is rare among mam- mals. Indeed, marmosets and tamarins are among the few primate species in which males are extensively involved in infant care (a truly progressive society!).

Other New World species range in size from squirrel monkeys (weigh- ing only 1.5 to 2.5 pounds and having a body length of 12 inches) to the larger howlers (as much as 22 pounds in males and around 24 inches long).

New World monkeys rely on a combination of fruits and leaves sup- plemented to varying degrees with insects. Most are quadrupedal; but some, such as spider monkeys (Fig. 6-22), are semibrachiators. Howlers, muriquis, and spider monkeys also have prehensile tails that are used not only in locomotion but also for hanging from branches. Socially, most New World monkeys live in mixed-sex groups of all age categories. Some (such as titis) form monogamous pairs and live with their subadult offspring.

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▲�Figure 6-21 Male, female, and infant howler monkeys. Illustrating why they’re called “howlers.” The roaring sound they make is among the loudest of mammalian vocalizations.

▶�Figure 6-20 Golden lion tamarins.

A Survey of the Living Primates 155

Old World Monkeys Except for humans, Old World mon- keys are the most widely dis- tributed of all living primates. They’re found throughout sub-Saharan Africa and southern Asia, ranging from tropical jungle habitats to semiarid desert and even to seasonally snow- covered areas in northern Japan (Fig. 6-23).

All Old World monkeys are placed in one taxonomic family, Cercopithecidae. In turn, this family is divided into two subfami- lies: the cercopithecines and colobines. Most Old World monkeys are quadru- pedal and primarily arboreal, but some (such as baboons) spend a great deal of time on the ground and return to the trees at night.

The cercopithecines are more generalized than colo- bines. They’re more omnivo- rous and, as a group, will eat almost anything: fruits, seeds, leaves, grasses, tubers, roots, nuts, insects, birds’ eggs,

▲�Figure 6-22 Spider monkey. Note use of prehensile tail for suspension.

◀�Figure 6-23 Geographical distri- bution of living Old World monkeys.

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cercopithecines common name for members of the subfamily of Old World monkeys that includes baboons, macaques, and guenons.

colobines common name for mem- bers of the subfamily of Old World monkeys that includes the african colobus monkeys and asian langurs.

Old World monkeys

EUROPE

AFRICA

Atlantic Ocean

Indian Ocean

Pacific Ocean

ASIA

AUSTRALIA

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chaPter 6 Survey of the Living Primates 156

amphibians, small reptiles, and small mammals (the last seen in baboons).

The majority of cercopithecine spe- cies, such as the mostly arboreal gue- nons (Dutch for clown; Fig. 6-24) and the more terrestrial baboons (Fig. 6-25), are found in Africa. The many macaque species (including the well-known rhesus monkeys), however, are widely distributed in southern Asia and India.

Colobine species have a narrower range of food preferences and mainly

eat mature leaves, which is why they’re also called leaf-eating monkeys. The colobines are found mainly in Asia, but both the red colobus and black- and-white colobus are exclusively African (Fig. 6-26). Other colobines include several Asian langur species and the proboscis monkey of Borneo (Fig. 6-27).

Locomotion in Old World mon- keys includes arboreal quadrupedal- ism in guenons, macaques, and lan- gurs; terrestrial quadrupedalism in

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▶�Figure 6-24 Adult male Sykes monkey, one of several guenon species.

▶�Figure 6-25 Hamadryas baboons are found in Ethiopia. Note how much larger the male (at right) is than the female. The male also has much lon- ger hair around the head and shoul- ders, which produces a distinctive mane.

A Survey of the Living Primates 157

baboons and macaques; and semibra- chiation and acrobatic leaping in colo- bus monkeys.

Marked differences in body size or shape between the sexes, referred to as sexual dimorphism, are typical of some terrestrial species and are espe- cially pronounced in baboons. In these species, male body weight (up to 80 pounds in baboons) may be twice that of females.

Females of several species (espe- cially baboons and some macaques) have pronounced cyclical changes of the external genitalia. These changes, which include swelling and redness, are associated with estrus, a hormon- ally initiated period of sexual recep- tivity in female nonhuman mammals correlated with ovulation. They serve as visual cues to males that females are sexually receptive.

Old World monkeys live in a few dif- ferent kinds of social groups. Colobines tend to live in small groups, with only one or two adult males. Savanna baboons and most macaque species are found in large social units compris- ing several adults of both sexes and off- spring of all ages. Monogamous pairing isn’t common in Old World monkeys, but it’s seen in a few langur species and

possibly one or two guenon species.

Old and New World Monkeys: A Case of Homoplasy We’ve mentioned several differ- ences between New and Old World monkeys, but the fact remains that they’re all monkeys. That is, they’re all adapted to a similar (pri- marily arboreal) way of life. Except for South American owl monkeys, they’re all diurnal. All live in social groupings; all are omnivorous to varying degrees; and all are quadrupedal (though there are variations of this general locomo- tor pattern).

These similarities are even more striking when you consider that New and Old World monkeys have followed separate evolutionary paths for at least 40 million years. It was once believed that both lineages evolved indepen- dently from separate early primate ancestors; but today the consensus is that both New and Old World mon- keys arose in Africa from a common monkey ancestor. The animals that gave rise to today’s New World species reached South America by “rafting” over on chunks of land that had broken

N el

so n

Ti ng

◀ Figure 6-26 Black-and-white colobus monkeys.

▲ Figure 6-27 Male proboscis mon- key. The nose (which gives the species its common name) is much larger in males than in females.

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cr ui

ck sh

an k/

Al am

chaPter 6 Survey of the Living Primates 158

away from mainland areas (Hoffstetter, 1972; Ciochon and Chiarelli, 1980b). It is remarkable that the two forms haven’t become more different from one another. The arboreal adaptations we see in both New and Old World monkeys are examples of homoplasy resulting from adaptations in geo- graphically distinct populations that have responded to similar selective pressures. This phenomenon, which we’ll explain more fully in Chapter 8, probably happened many times over the course of several million years.

Hominoids: Apes and Humans Apes and humans are classified together in the same superfamily, the hominoids. Apes are found in Asia and Africa. The small-bodied gibbons and siamangs live in Southeast Asia, and the two orangutan subspecies live on the islands of Borneo and Sumatra (Fig. 6-28). In Africa, until the mid- to late twentieth century, gorillas, chim-

panzees, and bonobos occupied the forested areas of western, central, and eastern Africa, but their habitat is now extremely fragmented, and all are now threatened or highly endangered. Apes and humans differ from monkeys in numerous ways:

1. Generally larger body size (except for gibbons and siamangs)

2. No tail 3. Shorter and more stable lower back 4. Arms longer than legs (only in

apes) 5. Anatomical differences in the

shoulder joint, which facilitate sus- pensory feeding and locomotion

6. Generally more complex behavior 7. More complex brain and enhanced

cognitive abilities 8. Increased period of infant develop-

ment and dependency

Gibbons and Siamangs The eight gibbon species and the closely relat- ed siamangs are the smallest of the apes, with long, slender bodies that weigh approximately 13 pounds in gibbons (Fig. 6-29) and around 25 pounds in siamangs. Their most dis- tinctive anatomical features are adap- tations to feeding while hanging from tree branches, or brachiation, at which gibbons and siamangs excel. In fact, gibbons and siamangs are more dedi- cated to brachiation than any other pri- mate, a fact reflected in their extremely long arms, long, permanently curved fingers, short thumbs, and powerful shoulder muscles. (Their arms are so long that when they’re on the ground, they have to walk bipedally with their arms raised to the side.) Gibbons and siamangs mostly eat fruits, although they also consume a variety of leaves, flowers, and insects.

The basic social unit of gibbons and siamangs comprises an adult male and female with dependent offspring. Although they’ve been described as monogamous, in reality members of a pair do sometimes mate with other individuals. Like marmosets and tam- arins, male gibbons and siamangs are very much involved in rearing their

▲�Figure 6-28 Geographical distri- bution of living Asian apes.

hominoids Members of the primate superfamily (hominoidea), which includes apes and humans.

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Gibbons Orangutans

ASIA

PHILIPPINES

BORNEOSUMATRA

VIETNAM THAILAND

MYANMAR LAOS

CHINA

I N D O N E S I A

MALAYSIA MALAYSIA

BRUNEI

CAMBODIA

A Survey of the Living Primates 159

young. Both males and females are highly territorial and protect their ter- ritories with elaborate whoops and siren-like “songs,” lending them the name “the singing apes of Asia.”

Many gibbon species are critically endangered today. The eastern black- crested gibbon for example, is now represented by 18 known groups liv- ing in small areas along the border between Vietnam and China. The total number of animals living in these groups was estimated at approximately 110 individuals in 2007 (Dat et al. 2008). Much of the remaining habi- tat is threatened by for- est clearing for culti- vation and livestock.

Moreover, hunting is always a problem. With so few animals living in dispersed groups, the survival of this species is in doubt, but conservation efforts are under way.

Orangutans Orangutans (Pongo pyg- maeus) (Fig. 6-30) are represented by two subspecies found today only in heavily forested areas on the Indo- nesian islands of Borneo and Suma- tra. The name orangutan (which has no final g and should never be pro- nounced “o-rang-utang”) means “wise man of the forest” in the language of the local people. But despite this some- what affectionate-sounding label, orangutans are severely threatened with extinction in the wild because of poaching by humans and continuing habitat loss on both islands. Habi- tat loss is especially severe on Sumatra, where land is continuous- ly being cleared for coffee cul- tivation, wood pulp for paper products, and— most

▲�Figure 6-29 White-handed cream- colored gibbon. The combination of a much reduced thumb and extremely elongated fingers and shortened thumb enhances the ability to brachiate.

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▲�Figure 6-30 Bornean orangutans. (a) Female with infant. (b) Male.

territorial Pertaining to the protec- tion of all or a part of the area occupied by an animal or group of animals. territorial behaviors range from scent marking to out- right attacks on intruders.

chaPter 6 Survey of the Living Primates 160

important of all—palm oil production. Additionally, orangutans are shot as pests and infants find their way into the pet trade. Today an estimat- ed 6,600 Sumatran orangutans live in fragmented habitats in northern Suma- tra (Singleton et al, 2009). That may seem like a relatively high number, but Sumatra’s forests are currently being cleared at a rate of 300 football fields every hour, 24 hours a day. Indeed, half of the forest that existed in 1985 was destroyed by 2012,

Orangutans are slow, cautious climbers whose form of locomotion can best be described as four-handed, referring to their use of all four limbs for grasping and support. Although they’re almost completely arboreal, orangutans sometimes travel on the ground. They exhibit pronounced sex- ual dimorphism; males may weigh more than 200 pounds whereas females typically weigh less than 100 pounds. In the wild, orangutans lead largely sol-

itary lives, although adult females are usually accompanied by one or two dependent offspring. They’re primar- ily frugivorous but may also eat bark, leaves, insects, and (rarely) meat.

Gorillas The largest of all living pri- mates, gorillas (Gorilla gorilla) are found in forested areas of western and eastern equatorial Africa (Fig. 6-31). There are four generally recognized gorilla subspecies. Of these, Western lowland gorillas (Fig. 6-32) are the most numerous and are found in sev- eral countries of west-central Africa. In 1998, Doran and McNeilage esti- mated their population size at per- haps 110,000, but Walsh and colleagues (2003) suggested that their numbers were far lower. Staggeringly, in August 2008, the Wildlife Conservation Soci- ety reported the discovery of an esti- mated 125,000 western lowland gorillas in the northern region of the Demo- cratic Republic of the Congo (DRC, for- merly Zaire)! This is extremely encour- aging news, but it doesn’t mean that gorillas are out of danger. To put this figure into perspective, consider that a large football stadium can hold around 70,000 people. So next time you see a stadium packed with fans, think about the fact that you’re perhaps looking at a crowd that numbers around half of all the western lowland gorillas on earth. Unless the DRC government, acting with wildlife conservation groups, can set aside more land as national parks and protect the gorillas from hunt- ing and disease, it’s probable that west- ern lowland gorillas face extinction in the wild.

Cross River gorillas, a West African subspecies, were identified in the early 1900s but thought to be extinct until the 1980s, when primatologists became aware of a few small populations in areas along the border between Nigeria and Cameroon (Sarmiento and Oates, 2000). Primatologists believe that there may be only 250 to 300 of these animals; thus Cross River gorillas are among the most endangered of all primates. Currently the International Union for

frugivorous having a diet composed primarily of fruits.

en ga

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ea rn

in g Chimpanzees

Bonobos

Gorillas

AFRICA

PORTUGAL TURKEYGREECE

CYPRUS

KENYA

ETHIOPIA

ERITREA SUDAN

EGYPT

NIGER

MAURITANIA MALI

NIGERIA SOMALIA

NAMIBIA

LIBYA

CHAD

SOUTH AFRICA

TANZANIA

ANGOLA

ALGERIA

MADAGASCAR

MOZAMBIQUE

BOTSWANA

ZAMBIA

GABON

CENTRAL AFRICAN REPUBLIC

TUNISIAMOROCCO

UGANDA

SWAZILAND

LESOTHO

MALAWI

BURUNDI

RWANDA

TOGO

BENIN

GHANA

IVORY COAST

LIBERIA

SIERRA LEONE

GUINEA BURKINA

GAMBIA

CAMEROON

ZIMBABWE

CONGO

DEM.REP.

OF CONGO

EQUATORIAL GUINEA

WESTERN SAHARA

DJIBOUTI

SENEGAL

GUINEA BISSAU

JORDAN

ISRAEL LEBANON

KUWAIT

QATAR BAHRAIN

U. A. E.

YEMEN

SYRIA

IRAQ IRAN

SAUDI ARABIA

MALTA

▲�Figure 6-31 Geographical distri- bution of living African apes.

A Survey of the Living Primates 161

the Conservation of Nature and Natural Resources (IUCN) is developing plans to protect this vulnerable and little- known subspecies (Oates et al., 2007).

Eastern lowland gorillas, which haven’t been extensively studied, live near the eastern border of the DRC. At present, their numbers are unknown but suspected to be around 12,000. (You wouldn’t need a very large foot- ball stadium to hold this many peo- ple.) Owing to warfare in the region, researchers fear that many of these gorillas have been killed, but it’s impos- sible to know how many.

Mountain gorillas (Fig. 6-33), the most extensively studied of the four subspecies, are restricted to the moun- tainous areas of central Africa in Rwanda, the DRC, and Uganda. There have probably never been many moun- tain gorillas, and today they number only about 700 animals, making them one of the more endangered primate species.

Like all gorillas, Mountain gorillas exhibit marked sexual dimorphism, with males weighing up to 400 pounds and females around 150 to 200

pounds. Adult goril- las, especially males, are primarily terrestrial.

Mountain gorillas live in groups composed of one or sometimes two large silverback males, a vari- able number of adult females, and their subadult offspring. (The term silverback refers to the saddle of white hair across the backs of fully adult males that appears around the age of 12 or 13 years.) A silverback male may tolerate the presence of one or more young adult “blackback” males (prob- ably his sons) in his group. Typically but not always, both females and males leave their natal group as young adults. Females join other groups, and males, who appear to be less likely to emigrate, may live alone for a while or may join up with other males before eventually forming their own groups.

Systematic studies of free-ranging western lowland gorillas weren’t begun until the mid-1980s, so even though they’re the only gorillas you’ll see in zoos, we don’t know as much about them as we do about mountain gorillas.

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▲�Figure 6-32 Lowland gorillas. (a) Male. (b) Female with infant.

natal group the group in which ani- mals are born and raised. (Natal pertains to birth.)

chaPter 6 Survey of the Living Primates 162

The social structure of western low- land gorillas is similar to that of moun- tain gorillas, but groups are smaller and somewhat less cohesive.

All gorillas are almost exclusively vegetarian. Mountain and western lowland gorillas concentrate primar- ily on leaves, pith, and stalks, but west- ern lowland gorillas eat more fruit. Western lowland gorillas, unlike mountain gorillas (which avoid water), also frequently wade through swamps while foraging on aquatic plants (Doran and McNeilage, 1998).

Perhaps because of their large body size and enormous strength, goril- las have long been considered vicious;

but in reality, they’re usually shy and gentle. However, this doesn’t mean they’re never aggressive. In fact, among males, competition for females can be extremely violent. As might be expected, males will attack to defend their group from any perceived dan- ger, whether it’s another male gorilla or a human hunter. Still, the reputation of gorillas as murderous beasts is the result of uninformed myth making and little else.

Chimpanzees The three subspecies of common chimpanzee (Pan troglo- dytes) are probably the best known of all nonhuman primates, even though

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a▶�Figure 6-33 Mountain gorillas. (a) A male silverback mountain gorilla with his group in the background. (b) Female.

A Survey of the Living Primates 163

many people think they’re monkeys (Fig. 6-34). Chimpanzees are often misunderstood because of zoo exhib- its, circus acts, television shows, and movies; thus their true nature was unknown until years of fieldwork with wild chimpanzee groups provided a more accurate picture. Today chim- panzees are found in equatorial Africa, in a broad belt from the Atlantic Ocean in the west to Lake Tanganyika in the east (refer back to Fig. 6-31). But within this large geographical area, their range is very patchy, and it’s becoming even more so with continuous habitat destruction.

In many ways, chimpanzees are ana- tomically similar to gorillas, with corre- sponding limb proportions and upper- body shape. However, the ecological adaptations and behaviors of chimpan- zees and gorillas differ, with chimpan- zees spending more time in the trees. Chimpanzees are also frequently excit- able, active, and noisy, whereas gorillas tend to be placid and quiet.

Chimpanzees are smaller than orangutans and gorillas, and although they’re sexually dimorphic, sex differ- ences aren’t as pronounced as in goril- las and orangutans. A male chimpan-

zee may weigh 150 pounds, but females can weigh at least 100 pounds. In addi- tion to quadrupedal knuckle walking, chimpanzees (particularly youngsters) may brachiate. When on the ground, they frequently walk bipedally for short distances when they are carrying food or other objects.

Chimpanzees eat a huge variety of foods, including fruits, leaves, insects, nuts, birds’ eggs, berries, caterpillars, and small mammals. Moreover, both males and females occasionally take part in group hunting efforts to kill small mammals such as young bushpigs and antelope. Their prey also includes monkeys, especially red colobus. When hunts are successful, the members of the hunting party share the prey.

Chimpanzees live in large fluid communities ranging in size from 10 to as many as 100 individuals. A group of closely bonded males forms the core of chimpanzee communities in many locations, especially in East Africa (Goodall, 1986; Wrangham et al., 1992). But for some West African groups, females appear to be more cen- tral to the community (Boesch, 1996; Boesch and Boesch-Acherman, 2000; Vigilant et al., 2001). Relationships

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◀�Figure 6-34 Male, female, and infant chimpanzees. Chimpanzees do not live in “nuclear families,” as this photo might imply, and it’s quite possible that the male at left is not the father of the infant.

chaPter 6 Survey of the Living Primates 164

among closely bonded males aren’t always peaceful or stable, yet these males cooperatively defend their terri- tory and are highly intolerant of unfa- miliar chimpanzees, especially males.

Even though chimpanzees live in communities, it’s rare for all members to be together at the same time. Rather, they tend to come and go, thus they don’t encounter the same individuals on a daily basis. Adult females usually forage either alone or in the company of their offspring, a grouping that might include several animals, since females with infants sometimes accompany their own mothers and siblings. These associations have been reported for the chimpanzees at Gombe National Park, where about 40 percent of females remain in the group in which they were born (Williams, 1999). But in most other areas, females leave their natal group to join another community. This behavioral pattern reduces the risk of mating with close male relatives, because males apparently never leave the group in which they were born.

Chimpanzee social behavior is extremely complex, and individuals

form lifelong attachments with friends and relatives. If they continue to live in their natal group, the bond between mothers and infants can remain strong until one of them dies. This may be a considerable period of time, because many wild chimpanzees live well into their 40s and even longer.

Bonobos Bonobos (Pan paniscus) are found only in an area south of the Zaire River in the DRC (see Fig. 6-35). Not officially recognized by European sci- entists until the 1920s, they remain among the least studied of the great apes. Although ongoing field studies have produced much information (Sus- man, 1984; Kano, 1992), research has been hampered by civil war. There are currently no accurate counts of bono- bos, but their numbers are believed to be between 29,000 and 50,000 (IUCN, 2011). These few are highly threatened by human hunting, warfare, and habi- tat loss.

Because bonobos bear a strong resemblance to common chimpanzees but are slightly smaller, they’ve been called “pygmy chimpanzees.” Actually,

▶�Figure 6-35 Female bonobos with young.

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gma nso

A Survey of the Living Primates 165

the differences in body size aren’t great, but bonobos are less stocky. They also have longer legs relative to arms, a rel- atively smaller head, and a dark face from birth.

Bonobos are more arboreal than chimpanzees, and they’re less excit- able and aggressive. Although aggres- sion isn’t unknown, it appears that physical violence both within and between groups is uncommon. Like chimpanzees, bonobos live in geo- graphically based fluid communities, and they eat many of the same foods, including occasional meat derived from small mammals (Badrian and Malenky, 1984). But bonobo commu- nities aren’t centered around a group of males. Instead, male-female bond- ing is more important than in chim- panzees and most other nonhuman primates (Badrian and Badrian, 1984). This may be related to bonobo sexu- ality, which differs from that of other nonhuman primates in that copula- tion is frequent and occurs through- out a female’s estrous cycle. That is, among bonobos sex is not linked solely to reproduction. In fact, bonobos are famous for their sexual behavior, since they copulate frequently and use sex to defuse potentially tense situations. Sexual activity between members of the same sex is also common (Kano, 1992; de Waal and Lanting, 1997). Given this aspect of bonobo behavior, it’s perhaps not surprising that they’ve been called the “make love, not war” primate society.

Humans Humans (Homo sapiens) are the only living representatives of the habitually bipedal primates (hominin tribe). Our primate heritage is evident in our overall anatomy and genetic makeup and in many behavioral aspects. Except for reduced canine size, human teeth are typical primate (espe- cially ape) teeth. The human depen- dence on vision and decreased reliance on olfaction as well as flexible limbs and grasping hands are rooted in our primate, arboreal past (Fig. 6-36).

Humans in general are omnivorous, although all societies observe certain

culturally based dietary restrictions. Even so, as a species with a rather gen- eralized digestive system, we’re physi- ologically adapted to benefit from an extremely wide assortment of foods. Perhaps to our detriment, we also share with our relatives a fondness for sweets that originates from the importance of high-energy fruits eaten by many non- human primates.

But humans are obviously unique among primates and indeed among all animals. For example, no member of any other species has the ability to write or think about how it differs from other life-forms. This ability is rooted in the fact that during the last 800,000 years of human evolution, brain size has increased dramatically, and there have also been many other neurologi- cal changes.

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▲�Figure 6-36 Playground equip- ment frequently allows children to play in ways that reflect their arboreal heritage.

chaPter 6 Survey of the Living Primates 166

Humans are also completely depen- dent on culture. Without cultural innovation, it would never have been possible for us to leave the tropics. As it is, humans inhabit every corner of the planet except for Antarctica, and we’ve even established outposts there. And lest we forget, a fortunate few have even walked on the moon! None of the technologies (indeed, none of the other aspects of culture) that humans have developed over the last several thousand years would have been pos- sible without the highly developed cog- nitive abilities that we alone possess. Nevertheless, the neurological basis for intelligence is rooted in our evo- lutionary past, and it’s something that connects us to other primates. Indeed, research has demonstrated that sev- eral nonhuman primate species—most notably chimpanzees, bonobos, and gorillas—display a level of problem solving and insight that most people would have considered impossible 30 years ago (see Chapter 7).

Humans are uniquely predisposed to use spoken language, and some 5,000 years ago, we also developed writing. Our advanced capacity for lan- guage exists because during the course of human evolution, certain neurologi- cal and anatomical structures were modified in ways not seen in any other species. But although nonhuman pri- mates aren’t anatomically capable of producing speech, research has shown that, to varying degrees, the great apes are able to communicate by using sym- bols, which is a foundation for language that humans and the great apes (to a limited degree) have in common.

Aside from cognitive abilities, the one other trait that sets humans apart from other primates (and indeed other mammals) is our unique form of strid- ing, habitual bipedal locomotion. This particular trait appeared early in the evolution of our lineage and, over time, we’ve become more efficient at it because of related changes in the mus- culoskeletal anatomy of the pelvis, leg, and foot. Early hominins increasing- ly adopted bipedalism because it was advantageous to them. As primates

and especially as apelike primates, they were already behaviorally predisposed to, and anatomically capable of, at least short-term bipedal walking before they adopted it wholeheartedly. So although it’s certainly true that human beings are unique intellectually and in some ways anatomically, we’re still primates. As a matter of fact, humans are basi- cally exaggerated African apes.

Endangered Primates

In September 2000, scientists announced that a subspecies of red colobus, named Miss Waldron’s red colobus, indigenous to the West Afri- can countries of Ghana and the Ivory Coast, had officially been declared extinct. This announcement came after a 6-year search for this 20-pound monkey, which hadn’t been seen for 20 years (Oates et al., 2000). Since this announcement was published, there has been compelling evidence that at least a few of these monkeys may still survive, although there have been no confirmed sightings of live animals (Oates, et al., 2008). We can hope that the pronouncement of the extinction of Miss Waldron’s red colobus was pre- mature. But even if it was, the twenty- first century will see the extinction of many nonhuman primates. In fact, as of this writing, over half of all nonhu- man primate species are in jeopardy, and some face certain extinction in the wild (Table 6.1).

▶�Table 6-1 List of 16 of the 25 most highly endangered nonhuman primate species. Although estimated population sizes for some species (e.g.,Sumatran orangutan) are as high as 6,600, they are included here because they are in extreme danger of extinction owing to the rate at which their numbers are declining. These declining numbers result from the devastating pace of habitat destruction, usually combined with unprecedented hunting. Others, such as the northern sportive lemur, are threatened with immediate extinction because their popula- tion size is so reduced as to be nonviable. Moreover, for all practical purposes they are not protected, even in national parks.

intelligence Mental capacity; abil- ity to learn, reason, or comprehend and interpret information, facts, relationships, and meanings; the capacity to solve prob- lems, whether through the application of previously acquired knowledge or through insight.

Endangered Primates 167

Table 6.1 List of 16 of the Most Highly Endangered Nonhuman Primate Species

Species Region/ Country

Estimated Population Size Threats

AFRiCA

Cross River gorilla Cameroon, Nigeria

300 Restricted range: habitat loss due to agriculture and development. Hunting for bushmeat and the pet trade. Snares for trapping other animals.

Rondo dwarf galago

Tanzania No reliable estimates

Habitat loss (agriculture, logging and charcoal production). Fragmented range contributes to nonviable population size. Locally extinct in many former ranges. May be extinct in Ghana.

Roloway guenon West Africa (Côte d’Ivoire and Ghana)

No reliable estimates

Extensively hunted for bushmeat trade. Habitat loss (cultivation, including palm oil) and habitat fragmentation with resulting nonviable population size.

Kipunji Montane for- ests in south- ern Tanzania

1,117 Hunting and habitat loss. Groups mostly isolated from each other because of extreme fragmentation of forest. This species was already highly endangered when scientists discovered it in late 2003.

Niger Delta Red Colobus

Niger River Delta, Nigeria

No reliable estimates

Commercial bushmeat hunting. Habitat destruction due to logging and canal construction partly due to oil extraction.

MAdAgASCAR

Northern sportive lemur

Northern Madagascar

18 Deforestation for charcoal and hunting. Extreme habitat fragmenta- tion with resulting nonviable population size.

Greater bamboo lemur

Rainforests of southeastern Madagascar

100–160 Habitat loss due to mining, illegal logging, slash-and-burn agri- culture. Hunting. Reduced drinking water due to climate change. Bamboo cutting (this species relies heavily on bamboo).

Silky sifaka Northeastern Madagascar

100–1,000 Hunting. Habitat loss due to slash-and-burn agriculture and logging for fuel and precious woods for export (e.g., rosewood).

ASiA

Sumatran orangutan

Indonesia (Sumatra)

6,600 Habitat loss due to logging, forest clearing for agriculture, especially oil palm plantations and road construction. Killing for food, pet trade (infants), and as means of “pest” control.

Eastern black- crested gibbon

Vietnamese- Chinese border

110 Habitat loss (cultivation, firewood, charcoal) and small, isolated populations.

Tonkin snub- nosed monkey

Northeastern Vietnam

200 Hunting, habitat loss (charcoal production, cultivation), and small, isolated populations.

Cat Ba (golden- headed) langur

Cat Ba Island, Vietnam

60–70 Hunting for body parts used in traditional medicines.

Javan slow loris Java, Indonesia No reliable estimates

Habitat loss due to forest clearing. Capture for uncontrolled, exten- sive wildlife trade (traditional medicines and pets).

NEw woRld

Cottontop tamarin Northwestern Colombia

Fewer than 6,000 Habit loss and fragmentation (logging, oil palm plantations, agricul- ture, logging, and pet trade).

Brown (variegated) spider monkey

(2 subspecies)

Colombia and Venezuela

No reliable esti- mates

Habitat loss (agriculture, cattle ranching) and hunting for food and pet trade.

Peruvian yellow- tailed woolly monkey

Tropical Andean forests, Peru

No reliable estimates

Habitat loss and fragmentation (agriculture, roads, logging, influx of large numbers of humans) and hunting (food, skins, and pet trade).

Source: Mittermeier, R.A., et al. (eds.), 2009 Primates in Peril: The World’s 25 Most Endangered Primates 2008–2010. Arlington,VA: IUCN/SSC Primate Specialist Group, International Primatological Society, and Conservation International.

chaPter 6 Survey of the Living Primates 168

There are three basic reasons for the worldwide depletion of nonhuman primates: habitat destruction, human hunting, and live capture for export or local trade. Underlying these three causes is one major factor: unprece- dented human population growth, par- ticularly in developing countries, where most nonhuman primates live.

The developing nations of Africa, Asia, and Central and South America are home to over 90 percent of all nonhuman primate species. During the 1990s these countries—aided by Europe, China, and the United States—destroyed an average of 39 million acres of forest per year. The destruction declined between 2000 and 2010 to about 32 million acres per

year, largely because of restrictions in Brazil. Unfortunately, the Brazilian government has weakened some of these restrictions and is revisiting others (Tollefson, 2012). But whether these restrictions will hold remains to be seen.

The motivation behind deforesta- tion is, of course, economic: the short- term gains from clearing forests to cre- ate immediately available (but poor) farmland or ranchland; the use of trees for lumber, charcoal, and paper prod- ucts; and large-scale mining opera- tions (with their necessary roads)—all causing further habitat destruction. Regionally the loss of rain forest ranks as a national disaster for some coun- tries. For example, the West African

168

Aye-Ayes: Victims of Derived Traits and Superstition

The primate order is filled with a vari-ety of fascinating animals, although few seem as unusual as the aye-aye (Daubentonia madagascariensis), a type of lemur. this is because most primates aren’t as derived as the aye-aye. today, aye-ayes are the only members of their genus. a second species (a subfossil lemur) was exterminated by humans during the last few centuries, and the aye-aye was unknown (at least to Western science) until 1961. Like all lemurs, aye-ayes are found only on the island of Madagascar, where they occupy a niche similar to that of woodpeckers. Like woodpeckers, which aren’t found on Madagascar, aye-ayes feed on insects and grubs that live in tree bark. On the ground they also find these same foods in logs. But instead of using a long beak to drill for hidden prey, this nocturnal primate uses an extremely specialized, elongated bony mid- dle finger to tap, tap, tap along a tree trunk, listening for hollow spaces (Fig. 1). When

an aye-aye finds a hollow space where a grub might be hiding, it tears through the bark with its continuously growing incisor teeth (a rodent trait) and scoops out the unlucky larva with the long nail at the end of its peculiar middle finger.

aye-aye dentition is also quite derived and specialized for this particular dietary niche. the aye-aye dental formula of

1.0.1.3 1.0.0.3

isn’t unique only among primates; it’s unique among all mammals. as you can see, aye-ayes have no canine teeth and

no lower premolars, although there’s one upper premolar (hershkovitz, 1977).

this perhaps strange-looking primate, which seems to have a permanent “bad hair day,” is about the size of a small house cat and has little of the appeal of, say, a galago. Unfortunately, many Malagasy (the human inhabitants of Madagascar) find the aye- aye’s appearance less than endearing. In fact, many think aye-ayes are bad luck and don’t realize that they’re simply harmless primates making a living as best they can.

Sadly, human imagination may prove this primate’s undoing. aye-ayes are vari- ously thought to be heralds of evil or killers who creep into thatched huts and puncture their victim’s aorta with their frightening middle finger (Goodman and Schütz, 2000). and some Malagasy superstitiously believe that should an aye-aye point its long middle finger at you, you will die. So it seems that cruel fate and humans have pointed their own finger of condemnation at the aye-aye, for only about 2,500 live in the wild and only a dozen or so in captivity.

A Closer Look

◀�Figure 1 This nineteenth-century drawing of an aye-aye perfectly illustrates the elongated middle finger used for dig- ging insects and grubs from logs and tree bark.©

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Endangered Primates 169

nation of Sierra Leone had an estimat- ed 15,000 square miles of rain forest early in the twentieth century. Today, less than 530 square miles remain, and most of this destruction has occurred since World War II. People in many developing countries are also critically short of fuel; lacking electricity, they use whatever firewood they can get. In addition, the demand for tropical hardwoods (such as mahogany, teak, and rosewood) in the United States, Europe, and Japan continues unabated, creating an enormously profitable mar- ket for rain forest products.

The demand for wood has resulted in conflict with conservationists, especially in parts of South America and central Africa. For example, mountain gorillas are among the most endangered nonhuman primate spe- cies, and tourism has been the only real hope of salvation for these mag- nificent animals. For this reason, sev- eral gorilla groups have been habitu- ated to humans and are protected by park rangers. Nevertheless, poaching, civil war, and land clearing have con- tinued to take a toll on these small populations. Between January and late July 2007, for example, 10 moun- tain gorillas were shot in the Virunga Volcanoes Conservation Area shared by Uganda, Rwanda, and the DRC

(Fig. 6-37). The gorillas weren’t killed for meat or because they were raid- ing crops. They were shot because the presence and protection of moun- tain gorillas are obstacles to people who profit from the destruction of the forests. But gorillas are not the only primates to have been shot in the Virungas. In the past few years, more than 130 rangers have been killed while protecting wildlife.

The Bushmeat Trade Until the late 1990s, habitat loss was the single greatest threat to nonhuman primates. But in the past few years, human hunting has become an equally important factor in some parts of the world (Fig. 6-38). During the 1990s, primatologists and conservationists became aware of a rapidly develop- ing trade in bushmeat, meat from wild animals, especially in Africa. The cur- rent slaughter, which now accounts for an annual loss of tens of thousands of nonhuman primates and other ani- mals, has been compared to the near extinction of the American bison in the nineteenth century.

Wherever nonhuman primates live, people have always hunted them for food. But in the past subsistence hunt- ing wasn’t a serious threat to entire

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◀�Figure 6-37 Congolese villagers carrying the body of the silverback gorilla shot and killed in the July 2007 attack. His body was buried with the other members of his group who were also killed.

chaPter 6 Survey of the Living Primates 170

primate populations and certainly not to entire species. But now, hunters armed with automatic rifles can and do wipe out an entire group of monkeys or gorillas in minutes. In fact, it’s possible to buy bushmeat outside the country of ori- gin. In major cities throughout Europe and the United States, illegal bushmeat is readily available to immigrants who want traditional foods or to nonimmi- grants who think it’s trendy to eat meat from exotic and frequently endangered animals.

It’s impossible to know how many animals are killed each year, but the estimates are staggering. The Society for Conservation Biology estimates that about 6,000 kg (13,228 pounds) of bushmeat is taken through just seven western cities (New York, London, Toronto, Paris, Montreal, Chicago, and Brussels) every month. No one knows how much of this meat is from pri- mates, but this figure represents only a tiny fraction of all the animals being slaughtered, because much smuggled meat isn’t detected at ports of entry. Also, the international trade is thought to account for only about 1 percent of the total (Marris, 2006).

Quite clearly, slowly reproducing species such as primates, which num- ber only a few hundred or a few thou- sand animals, cannot and will not sur- vive this onslaught for more than a few years. In addition, hundreds of infants, orphaned by the bushmeat trade, are sold in markets as pets. Although a few of these traumatized orphans make it to sanctuaries, most die within days or weeks of capture (Fig. 6-39).

Logging has been a major factor in the development of the bushmeat trade. The construction of logging roads, mainly by French, German, and Belgian lumber companies, has opened up vast tracts of previously inaccessible forest to hunters. What has emerged is a multimillion-dollar trade in bush- meat, a trade in which logging com- pany employees and local government officials participate with hunters, vil- lagers, market vendors, and smugglers

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◀�Figure 6-38 (a) Red-eared guenons (with red tails) and Preuss’s guenons for sale in a bushmeat market, Malabo, Equatorial Guinea. (b) Body parts, mostly from various monkey spe- cies, for sale in a West African market.

Endangered Primates 171

to cater to local and overseas markets. In other words, the hunting of wild animals for food, particularly in Africa, has quickly shifted from a subsistence activity to a commercial enterprise of international scope.

Although the slaughter may be best known in Africa, it’s by no means limited to that continent. In South America, for example, the hunting of nonhuman primates for food is com- mon, although it has not become a commercial enterprise on the scale seen in Africa and parts of Asia. Nevertheless, one report documented that in less than 2 years, one family of Brazilian rubber tappers killed almost 500 members of various large- bodied species, including spider monkeys, woolly monkeys, and howlers (Peres, 1990). Moreover, live capture and ille- gal trade in endangered primate spe- cies continue unabated in China and Southeast Asia, where nonhuman pri- mates are not only eaten but also fun- neled into the exotic pet trade. Just as importantly, primate body parts also figure prominently in traditional med- icines. With increasing human popu- lation size, the enormous demand for these products (and products from other, nonprimate species, such as

tigers) has placed many species in extreme jeopardy (Table 6-1).

As a note of optimism, in November 2007, the DRC government and the Bonobo Conservation Initiative (in Washington, DC) created a bonobo reserve consisting of 30,500 km2. This amounts to about 10 percent of the land in the DRC, and the government has stated that its goal is to set aside an additional 5 percent for wildlife protec- tion (News in Brief, 2007). This was a huge step forward. But as of this writ- ing, warfare has once again begun in the DRC and, tragically, some of the fighting is happening in the gorilla sector.

Many conservation groups are working to protect nonhuman pri- mates. These include, among many others, Conservation International, the World Wildlife Fund, Wildlife Direct, the International Primate Protection League, the Great Ape Trust, the Jane Goodall Institute, and the Orangutan Conservancy. In 2000, the United Nations Environmental Program established the Great Ape Survival Project (GRASP). GRASP is an alli- ance of many of the world’s major great ape conservation and research orga- nizations. It goes without saying that

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◀�Figure 6-39 Orphaned bonobo infants being cared for at a bonobo sanctuary in the Democratic Republic of the Congo.

chaPter 6 Survey of the Living Primates 172

GRASP and other organizations must succeed if the great apes are to sur- vive in the wild for even a few more decades.

If you are in your 20s or 30s, you will certainly live to hear of the extinc- tion of some of our marvelous cous- ins. Many more will undoubtedly slip away unnoticed. Tragically, in most cases this will occur before we’ve even gotten to know them. Each species on earth is the current result of a unique set of evolutionary events that, over

millions of years, has produced a finely adapted component of a diverse eco- system. When it becomes extinct, that adaptation and that part of biodiver- sity is lost forever. What a tragedy it will be if, through our own misman- agement and greed, we awaken to a world without chimpanzees, mountain gorillas, lemurs, or the tiny, exquisite cotton-topped tamarin. When this day comes, we truly will have lost a part of ourselves, and we will certainly be the poorer for it.

Studies of nonhuman primates began in the 1920s but remained uncommon until the 1960s. Since that time primatologists have produced literally thousands of articles providing as much detail as possible about the lives of our closest relatives. Moreover, anatomical studies have produced hundreds of reports of various aspects of primate anatomy. These include between-

species comparisons of structure and function of teeth, muscles, and the skeleton. In the last 20 years genetic analysis (comparative genomics) has allowed more pre- cise understanding of biological and evolutionary rela- tionships within the primate order, and this has facili- tated some reorganization of primate taxonomy.

How Do We Know?

▶▶ The mammalian order Primates includes humans and approximately 230 – 270 nonhuman species: apes, monkeys, tarsiers, and lemurs. Most non- human primates live in tropical and subtropical regions of Africa, India, Asia, Mexico, and South America.

▶▶ The order Primates is divided into two suborders: Strepsirhini (lemurs and lorises) and Haplorhini (tarsiers, monkeys, apes, and humans).

▶▶ As a group, the primates are very generalized, meaning they’ve retained many anatomical char- acteristics that were present in early ancestral mammalian species. These traits include five dig- its on the hands and feet, different kinds of teeth, and a skeletal anatomy and limb structure that allow for different forms of locomotion (climbing, brachiation, quadrupedalism, and bipedalism).

▶▶ Primates have grasping hands, and most have an opposable thumb, which facilitates this ability. (Some species are more specialized in that their thumbs are reduced or even absent.) Many pri- mates, such as chimpanzees and bonobos, also have opposable big toes.

▶▶ Most primates are omnivorous, although certain species focus on only certain foods. For example, the colobines (colobus monkeys and langurs) pri- marily eat leaves.

▶▶ In general, primates have relatively larger, more complex brains than other mammals. Consequently they are comparatively more intel- ligent and exhibit more complex behaviors. This is especially true of monkeys, apes, and humans.

▶▶ Primates rely more on vision than olfaction, and diurnal primates (with some New World excep- tions) have full color vision. Correspondingly, the areas of the brain related to vision are larger and more complex than the areas related to olfaction.

▶▶ Almost all nonhuman primates are arboreal and spend at least part of their time in trees.

▶▶ Because of human hunting and habitat loss, the majority of nonhuman primates are endangered today, and many are on the verge of extinction. Without concerted efforts to preserve primate habitat and control hunting, many species, will probably be extinct by as soon as 2050.

Summary of Main Topics

173Critical Thinking Questions

1. What are some human characteristics that reflect a common ancestry between nonhuman primates and ourselves? Although we didn’t really discuss this topic in the chapter, can you think of some ways in which humans are more similar to chim- panzees than to monkeys?

2. How do you think continued advances in genetic research will influence how we look at our rela- tionship with nonhuman primates?

3. How does a classification scheme reflect biologi- cal and evolutionary changes in a lineage? Can you

give an example of suggested changes to how pri- mates are classified? What do you think most peo- ple’s reaction would be to hearing that scientists are placing the great apes into the same taxonomic family as humans?

4. What factors threaten the existence of nonhuman primates in the wild? Is this important to you? What can you do to help save nonhuman primates from extinction?

Critical Thinking Questions

Partly because of common evolutionary history, many human behaviors are also

seen in other primates.

Connections

Fossil evidence indicates our primate origins date

to at least 65 million years ago.

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Humans are primates and share many biological

characteristics with other primates.

After mastering the material in this chapter, you should be able to:

▶ �Explain why variables such as diet, body size, and ecological factors such as the distribution of resources and predators influence the evolution of behavior.

▶ �Discuss how dominance hierarchies function within primate societies.

▶ �Define communication and explain what kinds of behaviors primates use to communicate with one another. You should differentiate between autonomic responses and deliberate actions.

▶ �Explain why communication is so important to living in social groups.

▶ �Discuss the differences between male and female reproductive strategies.

▶ �Give some examples of nonhuman primate behaviors that humans also exhibit.

▶ �Define language and discuss how language studies have shown that many nonhuman primates have a capacity to communicate symbolically. You should also be able to provide examples of how wild nonhuman primates have been seen to communicate symbolically.

▶ �Explain the evidence for culture in many nonhuman species, including some that aren’t primates.

▶ �Provide examples of aggressive and affiliative behaviors in nonhuman primates, especially chimpanzees. You would want to include altruism and empathy in this discussion and to explain how these examples can help us understand the evolution of these capacities in our own species.

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Do you think cats are cruel when they play with mice? Or if you’ve ever fallen off a horse when it suddenly jumped sideways for no apparent reason, did you think it threw you deliberately? If you answered yes to either of these questions, you wouldn’t be alone. To most people, it does seem cruel for a cat to torment a mouse for no obvious reason; and more than one rider has blamed their horse for intentionally throwing them (it has been known to happen). But these commonly held views indicate how lit- tle most people really know about non- human animal behavior.

Behavior is extremely complex, especially in mammals and birds, because it’s been shaped over evolu- tionary time by interactions between genetic and environmental factors. Most people don’t give this much thought, and even those who do don’t necessarily accept this basic premise. For example, many social scientists object to the notion of genetic influ- ences on human behavior because of concerns that it implies that behav- iors are fixed and can’t be modified by experience (learning). This view could, in turn, be used to support racist and sexist ideologies. Nevertheless, there is a substantial body of scientific evi- dence that genes indeed have a consid- erable influence on individual behavior, human and otherwise.

7 Primate Behavior Student Learning Objectives

behavior Anything organisms do that involves action in response to internal or external stimuli. The response of an indi- vidual, group, or species to its environment. Such responses may or may not be deliber- ate and they aren’t necessarily the results of conscious decision making.

chApTer 7 Primate Behavior 176

Also, there’s the prevailing notion of a fundamental divide between humans and all other animals. Most people see themselves as uniquely set apart from all other species. At the same time, and in obvious contradiction, people some- times assign certain human attributes to other species in order to explain behaviors (for example, cats are cruel to play with mice). Of course this isn’t a valid thing to do for the simple rea- son that other animals aren’t human. Cats sometimes play with mice because that’s how, as kittens, they learn to hunt. Cruelty doesn’t enter into it because the cat has no concept of cru- elty and no idea of what it’s like to be the mouse.

Likewise, a horse usually doesn’t deliberately throw you off when it hears leaves rattling in a shrub. It jumps because its behavior has been shaped by thousands of generations of equine ancestors who leaped first and asked questions later. It’s important to under- stand that just as cats evolved as preda- tors, horses evolved as prey animals, and their evolutionary history is lit- tered with unfortunate animals that didn’t jump at a sound in a shrub. In many cases, those ancestral horses learned, too late, that the sound wasn’t caused by a breeze. This is a mistake that prey animals often fail to survive, and those that don’t leap first tend to leave fewer descendants than those who don’t wait to see why the leaves are shaking.

Obviously, this chapter isn’t about cats and horses. It’s about what we know and hypothesize about the indi- vidual and social behaviors of non- human primates. But we begin with the familiar examples of cats and horses because we want to point out that many basic behaviors have been shaped by the evolutionary history of particular species. So, if we want to discover the underlying principles of behavioral evolution, we must first identify the interactions between a number of environmental and physio- logical variables.

The Evolution of Behavior

Scientists study primates from an ecological and evolutionary per- spective, focusing on the relationship between behaviors (both individual and social), the natural environment, and various physiological traits. This approach, called behavioral ecology, is based on the assumption that all of the biological components of ecologi- cal systems (animals, plants, and even microorganisms) evolved together. Behaviors are thus adaptations to envi- ronmental circumstances that existed in the past and remain in the present.

Briefly, the cornerstone of this per- spective is that behaviors have evolved through the operation of natural selec- tion. The underlying assumption is that certain behaviors are influenced by genes and are therefore subject to natural selection in the same way that physical characteristics are. Therefore behavior constitutes a phenotype, and individuals whose behavioral pheno- types increase reproductive fitness will pass on their genes at a faster rate than others. But this doesn’t mean that pri- matologists think that genes code for specific behaviors, such as a gene for aggression, another for cooperation, and so on. The study of complex behav- iors from an evolutionary viewpoint does not imply a one gene–one behav- ior relationship, nor does it suggest that behaviors that are influenced by genes can’t be modified through learning.

In insects and other invertebrates, behavior is mostly under genetic con- trol. In other words, most behavioral patterns in these species aren’t learned; they’re innate. But in many vertebrates, especially birds and mammals, the pro- portion of behavior that’s due to learn- ing is substantially increased and the proportion under genetic control is reduced. This is especially true of pri- mates. And in humans, who are so much a product of culture, most behav- ior is learned.

ecological pertaining to the relation- ships between organisms and all aspects of their environment (temperature, preda- tors, nonpredators, vegetation, availability of food and water, types of food, disease organisms, parasites, etc.).

behavioral ecology The study of the evolution of behavior, emphasizing the role of ecological factors as agents of natural selection. Behaviors and behavioral patterns have been favored because they increase the reproductive fitness of indi- viduals (i.e., they are adaptive) in specific environmental contexts.

Dorine Essumang

The Evolution of Behavior 177

Behavioral genetics, the study of how genes affect behavior, is a rela- tively new field, and we don’t yet know the extent to which genes actually influence behavior in humans or other species. What we do know is that behavior must be viewed as the prod- uct of complex interactions between genetic and environmental factors. The limits and potentials for learn- ing, and for behavioral flexibility, vary considerably among species. In some species, such as primates, the poten- tials are extremely broad; in others, such as insects, they aren’t. Ultimately, those limits and potentials are set by genetic factors that have been sub- jected to natural selection throughout the evolutionary history of every spe- cies. That history, in turn, has been shaped by the ecological setting not only of living species but also of their ancestors.

One of the major goals of primatol- ogy is to discover how certain behav- iors influence reproductive fitness and how ecological factors have shaped the evolution of those behaviors. Although the actual mechanics of behavioral evolution aren’t yet fully understood, new methods and technologies are helping scientists answer many ques- tions. For example, genetic analysis has

recently been used to establish paterni- ty in a few primate groups, and this has helped support hypotheses about some behaviors in males. But in general, an evolutionary approach to the study of behavior doesn’t provide defini- tive answers to many research ques- tions. Rather, it offers primatologists a valuable framework within which they can analyze data and generate and test hypotheses concerning behavioral pat- terns. (Remember, the development and testing of new hypotheses is how scientific research is done.)

Because primates are among the most social of animals, social behav- ior is one of the major topics in pri- mate research (Fig. 7-1). This is a broad subject that includes all aspects of behaviors that occur in social group- ings, even some you may not think of as social behaviors, such as feeding or mating. To understand the function of one behavioral element, it’s neces- sary to determine how it’s influenced by numerous interrelated factors. As an example, we’ll consider some of the more important variables that influ- ence social structure. Bear in mind that social structure itself influences individual behavior, thus in many cases the distinctions between social and individual behaviors are blurred.

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social structure The composition, size, and sex ratio of a group of animals. The social structure of a species is, in part, the result of natural selection in a specific habitat, and it guides individual interactions and social relationships.

◀�Figure 7-1 These proboscis monkeys in Malaysia provide a good example of a small nonhuman primate group.

chapter 7 Primate Behavior 178

Some Factors That Influence Social Structure Body Size As a rule, larger animals require fewer calories per unit of weight than smaller animals because larger animals have less surface area relative to body mass than small- er animals. Since body heat is lost at the surface, larger animals can retain heat more efficiently, so they need less energy overall. It may seem strange, but two 10-pound monkeys require more food than one 22-pound monkey (Fleagle, 1999).

Basal Metabolic Rate (BMR) The BMR concerns metabolism, the rate at which the body uses energy to main- tain all bodily functions while in a

resting state. It’s closely corre- lated with body size. In general, therefore, small- er animals have a higher BMR than larger ones (Fig. 7-2). Con- sequently small- er primates—for instance, gala- gos and marmo- sets—require an energy-rich diet

high in protein (insects), fats (nuts and seeds), and carbohydrates (fruits and seeds). Some larger primates, which tend to have a lower BMR and reduced energy requirements relative to body size, can do well with less energy-rich foods, such as leaves.

Diet Because the nutritional require- ments of animals are related to body size and BMR, all three have evolved together. Therefore when primatolo- gists study the relationships between diet and behavior, they consider the benefits in terms of energy (calo- ries) derived from various food items against the costs (energy expended) of obtaining and digesting them. While small-bodied primates focus on high- energy foods, such as sugar-containing fruits or protein sources, larger ones don’t necessarily need to, at least not to the same degree. For instance, goril- las eat leaves, pith from bamboo stems, and other types of vegetation. These foods have less caloric value than fruits, nuts, and seeds, but they still serve these animals well because goril- las tend to spend much of the day eat- ing and they don’t expend a great deal of energy getting food (Fig. 7-3).

Some monkeys, especially colo- bines (colobus and langur species), are primarily leaf eaters. Compared with many other monkeys, they’re fair- ly large-bodied. They’ve also evolved elongated intestines and pouched stomachs that enable them, with the assistance of intestinal bacteria, to digest the tough fibers and cellulose in leaves. Moreover, in at least two langur species, there’s a duplicated gene that produces an enzyme that further helps

metabolism the chemical processes within cells that break down nutrients and release energy for the body to use. (When nutrients are broken down into their com- ponent parts, such as amino acids, energy is released and made available for the cells to use.)

▲ Figure 7-2 Dwarf mouse lemur.

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▶ Figure 7-3 This male mountain gorilla has only to reach out to find something to eat.

The Evolution of Behavior 179

with digestion. This gene duplication isn’t found in other primates that have been studied, so the duplication event probably occurred after colobines and cercopithecines last shared a common ancestor (Zhang et al., 2002). Having a second copy of the gene was advanta- geous to colobine ancestors, who were probably already eating some leaves, so natural selection favored it to the point that it was established in the lineage. (The discovery of this gene duplication is another example of how new tech- nologies help explain behavior, in this case, dietary differences.)

Distribution of Resources Various kinds of foods are distributed in dif- ferent ways. Leaves can be abundant and dense and will therefore support large groups of animals. Insects, on the other hand, may be widely scattered; therefore the animals that rely on them usually feed alone or with only one or two others.

Fruits, nuts, and berries occur in dispersed trees and shrubs. These are most efficiently exploited by small- er groups of animals, so large groups frequently break up into smaller sub- units while feeding. Such subunits may consist of one-male–multifemale groups (some baboons) or matrili- nes (macaques). Species that subsist

on abundantly distributed resources may also live in one-male groups, and because food is plentiful, these one- male units are able to join with others to form large, stable communities (for example, howlers and some baboons) (Fig. 7-4). To the casual observer, these communities can appear to be multimale-multifemale groups. (See “A Closer Look: Types of Nonhuman Primate Social Groups.”)

Some species that depend on foods distributed in small clumps are pro- tective of resources, especially if their feeding area is small enough to be defended. Some live in small groups composed of a mated pair (siamangs) or a female with one or two males (marmosets and tamarins) and their offspring. Last, foods such as fruits, nuts, and berries are only seasonal- ly available; therefore primates that rely on them must eat a wide variety of foods. This is another factor that tends to favor smaller feeding groups.

Predation Depending on their size, pri- mates are vulnerable to many types of predators, including snakes, birds of prey, leopards, wild dogs, and even other primates. Their responses to pre- dation depend on their body size, social structure, and the type of predator. Typically, where predation pressure is

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◀�Figure 7-4 Gelada baboons live in one male-multifemale groups that combine to form troops that can num- ber more than 300 animals.

matrilines Groups that consist of a female, her daughters, and their offspring. Matrilines are common among macaques.

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high and body size is small, large com- munities are advantageous. These may be multimale-multifemale groups or congregations of one male-multifemale groups.

Dispersal Dispersal is another factor that influences social structure and relationships within groups. As is true of most mammals (and indeed most vertebrates), members of one sex leave the group in which they were born (their natal group) about the time they become sexually mature. Male disper- sal is the more common pattern (ring- tailed lemurs, vervets, and macaques, to name a few). But female dispersal is seen in some colobus species, hama- dryas baboons, chimpanzees, and mountain gorillas. In species where the basic social structure is a mated pair, offspring of both sexes either leave or are driven away by their parents (gib- bons and siamangs).

Dispersal may have more than one outcome. When females leave, they join another group. Males may do like- wise, but in some species (for example, gorillas), they may live alone for a time, or they may temporarily join an all- male “bachelor” group until they’re able to establish a group of their own. But the common theme is that individuals who disperse usually find mates out- side their natal group. This has led pri- matologists to conclude that the most valid explanations for dispersal are related to two major factors: reduced competition between males for mates and, more importantly, the decreased likelihood of close inbreeding.

Life Histories Life history traits are characteristics or developmental stag- es that typify members of a given spe- cies and influence potential reproduc- tive rates. Examples of life history traits include length of gestation, length of

Types of Nonhuman Primate Social Groups

1. One-male–multifemale: a single adult male, several adult females, and their offspring. This is the most common primate mating structure, in which only one male actively breeds, and it’s typically formed by a male joining a kin group of females. Females usually form the permanent nucleus of the group. examples: guenons, gorillas, some spi- der monkeys, patas, some langurs, and some colobus monkeys. In many spe- cies, several one-male groups may form large congregations.

2. Multimale-multifemale: several adult males, several adult females, and their young. Many of the males reproduce. The presence of several males in the group may lead to tension and to the

formation of a dominance hierarchy. examples: some lemurs, macaques, mangabeys, savanna baboons, vervets, squirrel monkeys, some spider mon- keys, and chimpanzees. In some spe- cies (vervets, baboons, and macaques), females are members of matrilines, or groups composed of a female, her female offspring, and their offspring. These kin groups are ranked relative to one another in a hierarchy.

3. Monogamous pair: a mated pair and their young. The term monogamous is somewhat misleading because matings with individuals other than partners aren’t uncommon. Species that form pairs are usually arboreal, show minimal sexual dimorphism, and are frequently territorial. Adults don’t normally toler- ate other adults of the same sex. This grouping isn’t found among the great apes, and it’s the least common breed- ing structure among nonhuman pri- mates. examples: siamangs, gibbons, indris, titis, sakis, owl monkeys, and

pottos. Males may directly participate in infant care.

4. Polyandrous: one female and two males. This social group is seen only in some New World monkeys (marmosets and tamarins). Males participate in infant care.

5. Solitary: individual who forages for food alone. This is seen in nocturnal primates such as aye-ayes, lorises, and galagos. In some species, adult females may for- age in pairs or may be accompanied by offspring. Also seen in orangutans.

There are also other groupings, such as foraging groups, hunting groups, all-female or all-male groups, and so on. Like humans, nonhuman primates don’t always maintain one kind of group; one male–multifemale groups may sometimes form multimale- multifemale groups, and vice versa. hama- dryas and Gelada baboons, for example, are described as living in one-male groups, but they form large herds at night as they move to the safety of sleeping cliffs.

A Closer Look

life history traits characteristics and developmental stages that influence reproductive rates. examples include lon- gevity, age at sexual maturity, length of time between births, etc.

Why Be Social? 181

time between pregnancies (interbirth interval), period of infant dependency and age at weaning, age at sexual matu- rity, and life expectancy.

Life history traits have important consequences for many aspects of social life, and they can also be critical to species survival. In species that live in marginal or unpredictable habitats, shorter life spans can be advantageous. Members of these species mature early and have short interbirth intervals, so reproduction can occur at a relatively fast rate in a habitat that doesn’t favor longevity (Strier, 2003). Conversely, longer-lived species, such as gorillas, are better suited to stable environmen- tal conditions. The extended life spans of the great apes in particular, charac- terized by later sexual maturation and long interbirth intervals of 3 to 5 years, means that most females will raise only three or four offspring to maturity. Today, this slow rate of reproduction increases the threat of extinction for all the great apes, which are being hunted at a rate that far outpaces their replace- ment capacities.

Strategies Strategies are behaviors that increase individual reproductive success. They also influence the struc- ture and dynamics of primate social groups. We’re accustomed to using the word strategies to mean deliber- ate schemes or plans purposefully designed to achieve goals. But in the context of nonhuman behavioral ecol- ogy, strategies are seen as products of natural selection, and no conscious planning or motivation is implied (Strier, 2003). Several kinds of strate- gies are discussed in behavioral stud- ies, including life history strategies, feeding strategies, social strategies, reproductive strategies, and predator avoidance strategies.

Distribution and Types of Sleeping Sites Gorillas are the only nonhuman pri- mates that sleep on the ground. Pri- mate sleeping sites can be in trees or on cliff faces, and their spacing can be related to social structure and predator avoidance (Fig. 7-5).

Activity Patterns Most primates are diurnal, but galagos, lorises, aye-ayes, tarsiers, and New World owl monkeys are nocturnal. Nocturnal primates tend to forage for food alone or in groups of two or three, and many avoid predators by hiding.

Human Activities As you saw in Chap- ter 6, virtually all nonhuman pri- mate populations are now impacted by human hunting and forest clearing. These activities severely disrupt and isolate groups, reduce numbers, reduce resource availability, and eventually lead to extinction.

Why Be Social?

Group living exposes animals to competition with other group members for resources; so why don’t primates live alone? After all, com- petition can lead to injury or even death, and it’s costly in terms of ener- gy expenditure. One widely accepted answer to this question is that the costs of competition are offset by the ben- efits of predator defense. Multimale- multifemale groups are advantageous

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chApTer 7 Primate Behavior 182

in areas where predation pressure is high, particularly in mixed woodlands and on open savannas. Leopards are the most significant predator of ter- restrial primates (Fig. 7-6), and the chances of escaping a leopard attack are far greater for an animal that lives in a group than for a single individual.

Savanna baboons have long been used as an example of these principles. They live in semiarid grassland and broken woodland habitats throughout sub-Saharan Africa. To avoid noctur- nal predators, savanna baboons sleep in trees, but they spend much of the day on the ground foraging for food. If a predator appears, baboons flee back into the trees; but if they’re some dis- tance from safety, adult males (and sometimes females) may join forces to chase the intruder.

As effective as increased num- bers can be in preventing predation, there are other explanations for pri- mate sociality. One is that larger social groups can outcompete smaller groups of conspecifics foraging in the same area (Wrangham, 1980). Wrangham also suggests that large multimale- multifemale groups evolved because males were attracted to related females living together. And last, females may tolerate familiar males, since they can provide protection against other, potentially infanticidal males.

There is probably no single answer to the question of why primates live in groups. More than likely, predator avoidance is a major factor but not the only one. Group living evolved as an adaptive response to a number of eco- logical variables, and it has served pri- mates well for a very long time.

Primate Social Behavior

Because primates solve their major adaptive problems in a social con- text, we should expect them to behave in ways that reinforce the integrity of the group. The better known of these are described here. Remember, all these behaviors have evolved as adaptive responses during more than 50 million years of primate evolution.

Dominance Many primate societies are organized into dominance hierarchies, which impose a certain degree of order by establishing parameters of individual behavior. Although aggression is fre- quently used to increase an animal’s status within the group, dominance hierarchies usually reduce the amount of actual physical violence. Not only are lower-ranking animals unlike- ly to attack or even threaten a higher- ranking one, but dominant animals are also able to exert control simply by making a threatening gesture. Indi- vidual rank or status can be measured by access to resources, including food items and mating partners. Dominant animals (alpha males and females) are given priority by others, and they rarely give way in confrontations.

Many primatologists think that the primary benefit of dominance is the increased reproductive success of high- ranking animals. This is true in many cases, but there’s good evidence that lower-ranking males also mate success- fully. High-ranking females also have higher reproductive success because they have greater access to food than

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dominance hierarchies Systems of social organization wherein individuals within a group are ranked relative to one another. higher-ranking animals have greater access to preferred food items and mating partners than lower-ranking individuals. Dominance hierarchies are sometimes called “pecking orders.”

Primate Social Behavior 183

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subordinate females. Therefore they obtain more energy for the production and care of offspring (Fedigan, 1983).

Pusey and colleagues (1997) dem- onstrated that the offspring of high- ranking female chimpanzees at Gombe Stream National Park in Tanzania had significantly higher rates of infant survival than those of lower-ranking females. Moreover, their daughters matured faster, which meant they had shorter interbirth intervals and conse- quently produced more offspring.

An individual’s position in the hier- archy isn’t permanent. It changes throughout life and is influenced by many factors, including sex, age, level of aggression, amount of time spent in the group, intelligence, motivation, and sometimes the mother’s social position (particularly true of macaques).

In species organized into groups containing a number of females asso- ciated with one or several adult males, males are generally dominant to females. Within such groups, males and females have separate hierarchies,

although very high-ranking females can dominate the lowest-ranking males, particularly young ones. But there are exceptions to this pattern of male dominance. In many lemur spe- cies, females are the dominant sex. Moreover, in species that form bonded pairs (for example, indris and gibbons), males and females are codominant.

All primates learn their position in the hierarchy. From birth, an infant is carried by its mother, and it observes how she responds to every member of the group. Just as importantly, it sees how others react to her. Dominance and subordination are indicated by ges- tures and behaviors, some of which are universal throughout the primate order (including humans), and this gestural repertoire is part of every youngster’s learning experience.

Young primates also acquire social rank through play with age peers, and as they spend more time with play- groups, their social network wid- ens. Competition and rough-and- tumble play allow them to learn the

Primate Social Strategies

At a Glance

competition among individuals within group

protection from predators through multimale cooperation or increased

surveillance

Ability to compete for resources with other groups of the same

species

protection against infanticidal males

Group living and group foraging

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strengths and weaknesses of peers, and they carry this knowledge with them throughout their lives. Thus, through early contact with their moth- ers and subsequent exposure to peers, young primates learn to negotiate their way through the complex web of social interactions that makes up their daily lives.

Communication Communication is universal among animals; it includes scents and unin- tentional autonomic responses as well as behaviors that convey mean- ing. Such attributes as body posture provide information about an animal’s emotional state. For example, crouch- ing indicates submission, insecurity, or fear, and this is true of many nonpri- mate animals too (for example, dogs). At the same time, a purposeful strid- ing gait implies confidence. Moreover, autonomic responses to threatening or novel stimuli, such as raised body hair (most species) or enhanced body odor (gorillas), indicate excitement or fear.

Many intentional behaviors also serve as communication. In primates, these include a wide variety of ges-

tures, facial expressions, and vocaliza- tions, some of which we humans share. Among many primates an intense stare indicates a mild threat; indeed, we humans find prolonged eye con- tact with strangers very uncomfortable. (For this reason people should avoid eye contact with captive primates.) Other threat gestures include a quick yawn to expose canine teeth (baboons, macaques) (Fig. 7-7), crouching and bobbing back and forth (patas mon- keys), and branch shaking (many mon- key species). High-ranking baboons mount the hindquarters of subordi- nates to express dominance (Fig. 7-8). Mounting may also serve to defuse potentially tense situations by indicat- ing something like, “It’s okay, apology accepted.”

Primates also use a variety of behav- iors to indicate submission, reassur- ance, or amicable intentions. Most primates crouch to show submission, and baboons also present or turn their hindquarters toward an animal they want to appease. Reassurance takes the form of touching, patting, hugging, and holding hands (Fig. 7-9). Grooming also serves in a number of situations to indicate submission or reassurance.

communication Any act that conveys information to another individual. Frequently, the result of communication is a change in the behavior of the recipient. communication may not be deliberate but may instead be the result of involuntary processes or a secondary consequence of an intentional action.

autonomic pertaining to physiologi- cal responses not under voluntary control. An example in chimpanzees would be the erection of body hair during excitement. Blushing is a human example. Both convey information regarding emotional states, but neither is deliberate, and communication isn’t intended.

grooming picking through fur to remove dirt, parasites, and other materials that may be present. Social grooming is common among primates and reinforces social relationships.

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▲�Figure 7-7 A “yawn” that exposes long canine teeth is a common threat gesture in many primate species. Here an adult male baboon combines it with an “eyelid flash,” closing the eyes to expose light-colored eyelids that enhance the visual effect of the threat.

▲�Figure 7-8 One young male savanna baboon mounts another as an expression of dominance.

Primate Social Behavior 185

A wide variety of facial expressions indicating emotional state is seen in chimpanzees and especially in bono- bos (Fig. 7-10). These include the well- known play face (also seen in several other primate and nonprimate spe- cies) associated with play behavior and the fear grin indicating fear and submission.

Not surprisingly, vocalizations play a major role in primate commu- nication. Some, such as the bark of a baboon that has just spotted a leop- ard, are unintentional startled reac- tions. Others, such as the chimpanzee food grunt, are heard only in specific contexts, in this case in the presence of food. These vocalizations, whether deliberate or not, inform others of the possible presence of predators or food.

Primates (and other animals) also communicate through displays, which are more complicated, frequently elaborate combi- nations of behaviors. For example, the exaggerat- ed courtship dances of many male birds, often enhanced by colorful plumage, are displays. Chest slapping and tear- ing vegetation are com- mon gorilla threat dis- plays. Likewise an angry chimpanzee, with hair on end, may charge an opponent while screaming, waving its arms, and tearing vegetation (Fig. 7-11).

All nonhuman animals use vari- ous body postures, vocalizations, and

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▲�Figure 7-9 Adolescent savanna baboons holding hands.

▲�Figure 7-10 Chimpanzee facial expressions.

◀�Figure 7-11 Male chimpanzee display. Note how the hair on his arms and shoulders is raised to make him look larger.

displays Sequences of repetitious behaviors that serve to communicate emo- tional states. Nonhuman primate displays are most frequently associated with repro- ductive or agonistic behavior; examples include chest slapping in gorillas or, in male chimpanzees, dragging and waving branches while charging and threatening other animals.

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chApTer 7 Primate Behavior 186

ing partners or food. Instead of actual attacks or fighting, most aggression within a group occurs in the form of various signals and displays, frequently within the context of a dominance hierarchy. Most tense situations are resolved through various submissive and appeasement behaviors.

But conflicts aren’t always resolved peacefully; in fact, they can have seri- ous and even fatal consequences. For example, high-ranking female macaques frequently intimidate, harass, and even attack lower- ranking females to keep them away from food. Dominant females consistently chase subordinates away from food and have even been observed taking food from their mouths. In some cases, low- ranking females suffer weight loss and poor nutrition. They may also have lower reproductive success because they’re less able to rear offspring to maturity simply because they don’t get enough to eat (Silk et al., 2003).

Competition between males for mates frequently results in injury and even death (Fig. 7-12). In species that have a distinct breeding season, such as New World squirrel monkeys, conflict between males is most common during that time. In species not restricted to a mating season, such as baboons and chimpanzees, competition between males can be ongoing.

facial expressions to transmit infor- mation. But the array of communi- cative devices is much richer among nonhuman primates, even though they don’t use language the way humans do. Communication is impor- tant because it’s what makes social living possible. Through submis- sive gestures, aggression is reduced and physical violence is less likely. Likewise, friendly intentions and rela- tionships are reinforced through phys- ical contact and grooming. Indeed, we humans can see ourselves in other primates most clearly in their use of nonverbal communication, particu- larly because some of their gestures and facial expressions carry the same meaning as ours do.

Aggressive and Affiliative Behaviors within Groups

Aggression Within primate societies, there is an interplay between aggressive behaviors, which can lead to group disruption, and affiliative behaviors, which pro- mote group cohesion. Conflict within a group frequently develops out of com- petition for resources, including mat-

language A standardized system of arbitrary vocal sounds, written symbols, and gestures used in communication.

affiliative behaviors Amicable associations between individuals. Affiliative behaviors, such as grooming, reinforce social bonds and promote group cohesion.

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▲�Figure 7-12 (a) These finger bones are from a female chimpanzee named Gilka, a member of Jane Goodall’s study group in Tanzania. On more than one occasion, observers saw another female attack Gilka, and dur- ing one attack, Gilka was badly bitten on the hand. Afterward she suffered periodically from running sores on her hand. The cavities and deformation in these bones indicate severe infec- tion of the marrow cavity, probably resulting from the bite wound. (b) This male chimpanzee cranium from West Africa exhibits a healed bite wound beneath the nose (arrow) most likely inflicted by another chimpanzee. Also, the left margin of the nasal opening shows irregularities that may have been caused by an infection, perhaps related to the injury.

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Aggressive and Affiliative Behaviors within Groups 187

Affiliative Behaviors Even though conflict can be destruc- tive, a certain amount of aggression helps maintain order within groups and protects either individual or group resources. Fortunately, there are many affiliative behaviors that reinforce bonds between individuals, promote group cohesion, minimize actual vio- lence, and defuse potentially dangerous situations. Common affiliative behav- iors include reconciliation, consola- tion, and simple amicable interactions between friends and relatives. Most such behaviors involve various forms of physical contact such as touching, hand holding, hugging, and grooming (Fig. 7-13). In fact, physical contact is one of the most important factors in

primate development and is crucial in promoting peaceful relationships and reinforcing bonds in many primate social groups.

Grooming is one of the most impor- tant affiliative behaviors in many pri- mate species. Although it occurs in other animal species, social groom- ing is mostly a primate activity and plays an important role in day-to-day life. Because grooming involves using the fingers to pick through the fur of another individual (or one’s own) to remove insects, dirt, and other materi- als, it serves hygienic functions. But it’s also an immensely pleasurable activ- ity that members of some species, espe- cially chimpanzees, engage in for long periods of time.

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chApTer 7 Primate Behavior 188

Grooming occurs in a variety of contexts. Mothers groom infants; males groom sexually receptive females; subordinate animals groom dominant ones, sometimes to gain favor; and friends groom friends. In general, grooming is comforting. It restores peaceful relationships after conflict and provides reassurance dur- ing tense situations. In short, groom- ing reinforces social bonds and conse- quently helps strengthen and maintain a group’s structure.

Social relationships are crucial to nonhuman primates, and bonds between individuals can last a lifetime. These relationships serve many func- tions. Individuals of many species form alliances in which members support each other against outsiders. Alliances, or coalitions, as they’re also called, can be used to enhance the status of mem- bers. In fact, chimpanzees rely so heav- ily on coalitions and are so skillful politically that an entire book, appro- priately titled Chimpanzee Politics (de Waal, 2007), is devoted to the topic.

Reproduction and Reproductive Behaviors

In most primate species as in most mammals, sexual behavior is tied to the female’s reproductive cycle, with females being receptive to males only when they’re in estrus. Estrus is char- acterized by behavioral changes and, in Old World monkeys and apes that live in multimale groups, it is also accompanied by swelling and chang- es in color of the skin around the geni- tal area. These changes serve as visu- al cues of a female’s readiness to mate (Fig. 7-14).

Permanent bonding between males and females isn’t common among non- human primates. However, male and female savanna baboons sometimes form mating consortships. These tem- porary relationships last while the female is in estrus, and the two spend most of their time together, mating

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Reproduction and Reproductive Behaviors 189

frequently. Mating consortships are common among bonobos. In fact, male and female bonobos may spend sev- eral weeks primarily in each other’s company. During this time they mate often, even when the female is not in estrus.

Such a male-female bond may result in increased reproductive success for both sexes. For the male, there is the increased likelihood that he will be the father of any infant the female con- ceives. At the same time, the female potentially gains protection from pred- ators or other members of her group, and perhaps assistance in caring for offspring she may already have.

Reproductive Strategies Reproductive strategies, and espe- cially how they differ between the sexes, have been a primary focus of pri- mate research. The goal of these strat- egies is to produce and successfully rear to adulthood as many offspring as possible.

Primates are among the most K-selected of mammals. By this we mean that individuals produce only a few young, in whom they invest a tre- mendous amount of parental care. Contrast this pattern with r- selected species, where individuals produce large numbers of offspring but invest little or no energy in parental care. Good examples of r-selected spe- cies include insects, most fishes, and, among mammals, mice and rabbits.

Considering the degree of care required by young dependent pri- mate offspring, it’s clear that an enor- mous investment by at least one par- ent is necessary, and in most species the mother carries most of the bur- den. Primates are completely helpless at birth. They develop slowly and con- sequently are exposed to expanded learning opportunities within a social environment. Therefore what we see in ourselves and our close primate rel- atives (and presumably in our more recent ancestors as well) is a strategy in which at least one parent, usually the mother, makes an extraordinary

investment to produce a few “high- quality,” slowly maturing offspring.

Finding food and mates, avoid- ing predators, and caring for and pro- tecting dependent young are difficult challenges for nonhuman primates. In most species, males and females use different strategies to meet these challenges.

Female primates spend almost all their adult lives either pregnant, lactat- ing, and/or caring for offspring, and the resulting metabolic demands are enor- mous. A pregnant or lactating female, although perhaps only half the size of her male counterpart, may require about the same number of calories per day. Even if these demands are met, her physical resources may be drained. For example, analysis of chimpanzee skel- etons from Gombe showed significant loss of bone and bone mineral in older females (Sumner et al., 1989).

Given these physiological costs and the fact that her reproductive potential is limited by lengthy interbirth inter- vals births, a female’s best strategy is to maximize the amount of resourc- es available to her and her offspring. Indeed, as we discussed earlier, females of many primate species (marmo- sets, gibbons, and macaques, to name a few) are highly competitive with other females and aggressively protect resources. In other species (chimpan- zees, for example), females distance themselves from others to avoid com- petition. Males, however, face a dif- ferent set of challenges. Having little investment in the rearing of offspring and the continuous production of sperm, it’s to the male’s advantage to secure as many mates and produce as many offspring as possible.

Sexual Selection Sexual selection is one outcome of different mating strategies. It’s a type of natural selection that operates on only one sex, usually males. The selective agent is male competition for mates and, in some species, mate choice by females. The long-term effect of sexual selection is to increase the frequency of

reproductive strategies Behaviors or behavioral complexes that have been favored by natural selection to increase individual reproductive success. The behaviors need not be deliberate, and they often vary considerably between males and females.

K-selected pertaining to K-selection, an adaptive strategy whereby individuals produce relatively few offspring, in whom they invest increased parental care. Although only a few infants are born, chances of survival are increased for each one because of parental investments of time and energy. Birds, elephants, and canids (wolves, coyotes, and dogs) are examples of K-selected nonprimate species.

r-selected pertaining to r-selection, a reproductive strategy that emphasizes relatively large numbers of offspring and reduced parental care compared with K-selected species. K-selection and r-selection are relative terms; for example, mice are r-selected compared with pri- mates but K-selected compared with insects.

sexual selection A type of natural selection that operates on only one sex within a species. It’s the result of com- petition for mates, and it can lead to sexual dimorphism with regard to one or more traits.

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chApTer 7 Primate Behavior 190

those traits in males that lead to greater success in acquiring mates.

In the animal kingdom, numer- ous male attributes are the result of sexual selection. For example, female birds of many species are attracted to males with more vividly colored plumage. Selection has thus increased the frequency of alleles that influ- ence brighter coloration in males, and in these species (peacocks are a good example) males are more colorful than females.

Sexual selection in primates is most common in species in which mating is polygynous and there is consider- able male competition for females. In these species, sexual selection produc- es dimorphism with regard to a num- ber of traits, most noticeably body size (Fig. 7-15). As you have seen, the males of many primate species are considerably larger than females, and they also have larger canine teeth. Conversely, in species that live in pairs (such as gibbons) or where male com- petition is reduced, sexual dimor- phism in body size and canine teeth is either reduced or nonexistent. For this reason, the presence or absence of sexual dimorphism in a species can be a reasonably good indicator of mating structure.

Infanticide as a Reproductive Strategy? One way males may increase their chances of reproducing is to kill infants fathered by other males. This explana- tion was first offered in an early study of Hanuman langurs in India (Hrdy, 1977). Hanuman langurs (Fig. 7-16) typically live in groups composed of one adult male, several females, and their offspring. Males without mates form “bachelor” groups that frequent- ly forage within sight of one male– multifemale units. These peripheral males occasionally attack and defeat a reproductive male and drive him from his group. Sometimes, following such a takeover, the new male kills some or all of the group’s infants that were fathered by the previous male.

At first glance, infanticide would appear to be counterproductive, espe- cially for a species as a whole. However, individuals act to maximize their own reproductive success, no mat- ter what effect their actions may have on the group or species. Even though they aren’t really aware of it, by killing infants fathered by other animals, male langurs may in fact increase their own chances of fathering offspring. This is because a female doesn’t come into

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polygynous pertaining to polygyny. A mating system in which a male mates with more than one female. This is the most common mating pattern found in mam- mals, including most primates.

Reproduction and Reproductive Behaviors 191

estrus while she is producing milk and nursing an infant; therefore she isn’t sexually available. But when a female loses an infant, she resumes cycling and becomes sexually receptive. Thus, by killing a nursing infant, a new male avoids having to wait 2 to 3 years for it to be weaned before he can mate with its mother. This could be advantageous for him because chances are good that he won’t even be in the group for 2 or 3 years. Moreover, he also doesn’t expend energy and put himself at risk defend- ing infants who don’t carry his genes.

Hanuman langurs aren’t the only primates that practice infanticide. It has been observed or surmised among many primates, including red colobus, savanna baboons, orangutans, gorillas, chimpanzees (Struhsaker and Leyland, 1987), and humans. (We should also mention that infanticide occurs in numerous nonprimate species, includ- ing rodents, cats, and horses.)

In the majority of reported nonhu- man primate examples, infanticide coincides with the transfer of a new male into a group or, as among chim- panzees, an encounter with an unfa- miliar female and infant. Numerous objections to this explanation of infan- ticide have been raised. Alternative explanations have included compe- tition for resources (Rudran, 1973), aberrant behaviors related to human-

induced overcrowding (Curtin and Dohlinow, 1978), and inadvertent killing during conflict between ani- mals (Bartlett et al., 1993). But others (Struhsaker and Leyland, 1987; Hrdy, 1995) maintain that the incidence and patterning of infanticide by males are not only significant but also consistent with the assumptions established by theories of behavioral evolution.

In a study published in 2003, Henzi and Barrett reported that when chac- ma baboon males migrate into a new group, they “deliberately single out females with young infants and hunt them down” (Fig. 7-17). The impor- tance of these findings is the conclu- sion that, at least in chacma baboons, newly arrived males consistently try to kill infants, and their attacks are high- ly aggressive and purposeful. However, reports such as these don’t prove that infanticide increases a male’s repro- ductive fitness. In order to do this, pri- matologists must demonstrate two crucial facts:

1. Infanticidal males do not kill their own offspring.

2. Once a male has killed an infant, he subsequently fathers another infant with the victim’s mother.

These statements are hypothe- ses that can be tested; and to do this, Borries and coworkers (1999) collected

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chApTer 7 Primate Behavior 192

DNA samples from the feces of infanti- cidal males and their victims’ remains in several groups of free-ranging Hanuman langurs. This was done to determine if these males killed their own offspring. Their results showed that in all 16 cases where infant and male DNA was available, the males were not related to the infants they either attacked or killed. Moreover, DNA analysis also showed that in 4 out of 5 cases in which a victim’s mother subsequently gave birth, the new infant was fathered by the infanticidal male. The application of DNA technology to a long-unanswered question has pro- vided strong evidence suggesting that infanticide may indeed give males an increased chance of fathering offspring. Moreover, this study provides another example of how science works: hypoth- eses are refined and further tested as new discoveries are made or, as in this case, new technologies are developed.

Mothers, Fathers, and Infants

The basic social unit among all pri-mates is a female and her infants (Fig. 7-18). Except in those species in which monogamy or polyandry occurs, or in which the social group is a bonded pair, males usually don’t directly par- ticipate in the rearing of offspring.

The mother–infant bond begins at birth. Although the exact nature of the

bonding process isn’t fully understood, there appear to be predisposing, innate factors that strongly attract the female to her infant as long as she herself has had a sufficiently normal experience with her own mother. This doesn’t mean that primate mothers have innate knowledge of how to care for an infant. They don’t. Monkeys and apes raised in captivity without contact with their own mothers not only don’t know how to care for a newborn infant but may be afraid of it and attack or even kill it. Thus learning is essential to establishing a mother’s attraction to her infant.

The importance of a normal rela- tionship with the mother has been demonstrated by field and labora- tory studies. From birth, infant pri- mates are able to cling to their moth- er’s fur, and they’re in more or less constant physical contact with her for several months. During this criti- cal period, infants develop a closeness with their mothers that doesn’t always end with weaning. In some species it may be maintained until one or the other dies.

In some species, presumed fathers also participate in infant care (Fig. 7-19). Male siamangs actively care for their offspring, and marmo- set and tamarin males provide most of the direct infant care. In fact, marmo- set and tamarin offspring (frequently twins) are usually carried on the male’s back and transferred to their mother only for nursing.

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▲�Figure 7-17 An immigrant male chacma baboon chases a terrified female and her infant (clinging to her back). Resident males interceded to stop the chase.

polyandry A mating system wherein a female continuously associates with more than one male (usually two or three) with whom she mates. Among nonhuman pri- mates, polyandry is seen only in marmosets and tamarins. It also occurs in a few human societies.

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Even in species where males aren’t directly involved in infant care, they may take more than a casual interest in infants, and this is especially true of hama- dryas and savanna baboons. But to establish that baboons exhibit paternal care, it’s necessary to establish paternity. Buchan and colleagues (2003) did just that by analyzing the DNA of sub- adults and males. They showed that during disputes, males inter- vened on behalf of their off- spring significantly more often than they did for unrelated juve- niles. Because disputes can lead to severe injury, Buchan and colleagues considered the male intervention an example of true paternal care.

▲ Figure 7-18 Primate moth- ers with young. (a) Mongoose lemurs. (b) Chimpanzees. (c) Squirrel mon- keys. (d) Japanese macaques. (e) Sykes monkeys.

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Nonhuman Primate Models for the Evolution of Human Behavior

In Chapter 1 we said that primates, chimpanzees in particular, are often used as models for early hom- inin behavior. But once the human and chimpanzee lineages diverged from a common ancestor, they traveled down different evolutionary paths and con- tinued to evolve in response to differ- ent environmental pressures. Con- sequently no living species, not even

chimpanzees, can perfectly serve as representatives of early hominin adaptations.

Primatologists examine behavior- al patterns that have evolved as adap- tive responses in nonhuman primates, always keeping in mind the enormous degree of flexibility in primate behav- ior. Then they identify similar patterns in humans and try to draw conclu- sions about the ecological and genetic factors that may have produced simi- larities (and differences) between our closest relatives and ourselves. This approach places the study of human behavior firmly within an evolutionary context.

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Nonhuman Primate Models for the Evolution of Human Behavior 195

As a separate lineage, our own evo- lutionary story probably began with a behavioral shift to exploiting a mixed woodland habitat, an eco niche differ- ent from that of the great apes, and this new adaptation required spending more time on the ground and exploit- ing different types of resources. These factors, in turn, selected for additional behavioral and anatomical adaptations, at the same time that other hominoids were responding to different environ- mental pressures.

Brain and Body Size One predominant characteristic that clearly differentiates humans from other primates is relative brain size, by which we mean the proportion of some measure of body size, such as weight, that’s accounted for by the brain. Brain size and body size are closely corre- lated. Clearly an animal the size of a chimpanzee (about 100 to 150 pounds) has a larger brain than a 2 pound squir- rel monkey. But, the ratio between brain size and body weight is not the same in all species.

The predictable relationship between body and brain size has been called the “index of encephalization” (Jerison, 1973). The degree of encepha- lization is used to estimate the expect- ed brain size for any given body size. Most primates are close to predicted ratios for brain‒body size, but there’s one notable exception: ourselves. (New World capuchins and squirrel monkeys also show a degree of encephalization that considerably exceeds predictions.) Brain size in modern humans is well beyond what would be expected for a primate of similar body weight. It’s this degree of encephalization that must be explained as a unique and central com- ponent of relatively recent human evo- lution. Indeed, studies of fossil homi- nins have clearly demonstrated that early members of the genus Homo as well as even older less derived homi- nins (Australopithecus) weren’t nearly as encephalized as modern humans are.

Beyond simple comparisons of brain size between different species, it’s more

appropriate to emphasize the relative size of certain structures in the brain. Primitive (ancestral) brains, such as those of reptiles, are mostly composed of structures related to basic physi- ological functions, and there’s a small cortex that receives sensory (especial- ly olfactory) information. As discussed in Chapter 5, in mammals, the relative size of the most recently evolved layer of the cortex, called the neocortex, has increased. This increase permits a more detailed analysis and interpreta- tion of incoming sensory information and therefore more complex behav- ior. In primates, expansion of the neo- cortex has accounted for much of the increase in brain size (Fig. 7-20). The primate neocortex is partly composed of many complex association areas. It’s the part of the brain that, in humans, is associated with cognitive functions related to reasoning, complex prob- lem solving, forethought, and language. The neocortex accounts for about 80 percent of the total volume of the human brain (Dunbar, 1998).

Timing of brain growth is also important. In nonhuman primates, the most rapid period of brain growth occurs shortly before birth; but in humans, it occurs after birth. Human prenatal brain growth is restricted so that the infant can pass through the birth canal. As it is, the size of the head in human newborns makes childbirth more difficult in humans than in any other primate. Thus, in humans, the brain grows rapidly for at least the first 5 years after birth. Because brain tissue is the most costly of all body tissues in terms of energy consumed, the meta- bolic costs of such rapid and sustained neurological growth are enormous, requiring more than 50 percent of an infant’s metabolic output (Aiello, 1992).

In evolutionary terms, the meta- bolic costs of a large brain must be compensated for by benefits. That is, large brains would not have evolved if they didn’t offer some advantage (Dunbar, 1998). Various hypotheses have been proposed for the evolu- tion of large brains in primates, and many scientists in the past focused

encephalization The proportional size of the brain relative to some estimate of overall body size, such as weight. More pre- cisely, the term refers to increases in brain size beyond what would be expected given the body size of a particular species.

chApTer 7 Primate Behavior 196

▲�Figure 7-20 Comparisons of mammalian brains as seen in these left lateral views (front is to left). Expansion of the neocortex, the outer layers of the cerebral hemispheres, has been the most significant trend during the evolution of the mammalian brain. This is especially evident in the size of the neocortex relative to that of the olfactory bulb (ob) at the front of the brain. The olfactory bulb is the termination point of sensory fibers that send olfactory information from the nose to the brain. A relatively large olfactory bulb indicates a greater dependence on the sense of smell. Compare the size of this organ, relative to the neocortex, in these brains. In the mouse and cat, it’s particularly large, but it becomes smaller in primates. In humans, it’s barely visible. In fact, in chimpanzees and humans, the neocortex is all that’s visible from the top and sides except for the cerebellum. Also note the increasingly convoluted surface of the neocortex. This is due to cortical folding, which allows more neurons to be packed into a limited space. Increasing the number of neurons provides more interconnections between areas of the brain, allowing more information to be processed. The marmoset exhibits less cortical folding than the cat, but its temporal lobe (part of the neocortex) is better defined, and brain size relative to body size is greater. As you can see, cortical folding is most pronounced in humans. (Illustrations are shown approximately the same size and not to scale.) (Photos provided by the University of Wisconsin– Madison Comparative Mammalian Brain Collection: http://brainmuseum.org. Preparation of these images and specimens was funded by the National Science Foundation and the National Institutes of Health.)

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on problems related to getting food and the kinds of foods a species eats. For example, some monkeys (with a smaller relative brain size) primar- ily eat leaves, which, although plenti- ful, aren’t an energy-rich food source. Primates need a complex brain in order to be familiar with their home range; to be aware of when season- al foods are available; and to solve the problem of extracting foods from shells, hard peels, and even under- ground roots. But these are problems for all foraging species (squirrels and raccoons, for example), yet these ani- mals haven’t evolved such relatively large brains (Fig. 7-21).

Another explanation, the social brain hypothesis, proposes that pri- mate brains increased in relative size and complexity because primates live in social groups. The demands of social living are numerous, and primates must be able to negotiate a complex web of interactions, including compe- tition, alliance formation, forming and maintaining friendships, and avoiding certain individuals. Therefore Barton and Dunbar (1997) suggested that intelligence evolved not only to solve physical problems (such as finding food and avoiding predators) but also to analyze and use social information, such as which animals are dominant, who forms alliances with whom, and whom to avoid.

Language

The development of language was one of the most significant events in human evolution. We have already described several behaviors and auto- nomic responses that convey infor- mation in nonhuman primates. But although we emphasized the impor- tance of communication to primate social life, we also said that nonhuman primates don’t use language the way humans do.

The view traditionally held by most linguists and behavioral psychologists has been that nonhuman communi- cation consists of mostly involuntary vocalizations and actions that con- vey information solely about an ani- mal’s emotional state (anger, fear, and so on). Nonhuman animals haven’t been considered capable of communi- cating about external events, objects, or other animals, either in close prox- imity or removed in space or time. For example, when a startled baboon barks, other group members know only that it may have been surprised or fright- ened. But they don’t necessarily know why it barked until they look around to see what provoked it. In general, then, it’s been assumed that in nonhuman animals, including primates, vocaliza- tions, facial expressions, body postures, and so on don’t refer to specific exter- nal phenomena.

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◀�Figure 7-21 These young rac- coons are extremely intelligent and forage for a wide assortment of foods in a complex environment. However, they don’t spend their entire lives in social groups and their relative (and absolute) brain size is smaller than that of similarly sized primates.

chApTer 7 Primate Behavior 198

But these views have been chal- lenged for years (Steklis, 1985; King, 1994, 2004). For example, vervet mon- keys (Fig. 7-22) use specific vocal- izations to refer to particular catego- ries of predators, such as snakes, birds of prey, and leopards (Struhsaker, 1967; Seyfarth et al., 1980a,b). The fact that vervets use distinct vocaliza- tions to refer to specific components of the external environment demon- strates that their calls aren’t involun- tary and they don’t refer solely to the individual’s emotional state (alarm), although this information is certain- ly conveyed. While these findings dis- pel certain long-held misconceptions about nonhuman communication (at least for some species), they also indi- cate certain limitations. Vervet com- munication is restricted to the present; as far as we know, no vervet can refer to a predator it saw yesterday or one it might see in the future.

Other studies have demonstrated that numerous nonhuman primates produce distinct calls that have specific references. There is also compelling evidence that many birds and some nonprimate mammals use specific predator alarm calls.

Humans use language, a set of writ- ten and/or spoken symbols that refer to concepts, other people, objects, and so on. This set of symbols is said to be arbitrary because the symbol itself has no inherent relationship with whatever it stands for. For example, the English word flower, when written or spoken, neither looks, smells, nor feels like the thing it represents. Humans can also recombine their linguistic symbols in an infinite number of ways to cre- ate new meanings, and we can use lan- guage to refer to events, places, objects, and people far removed in both space and time. For these reasons, language is described as an open system of com- munication, based on the human abil- ity to think symbolically.

Language, as distinct from other forms of communication, has always been considered a uniquely human achievement, setting humans apart from the rest of the animal kingdom. But reports from psychologists, espe- cially those who work with chimpan- zees, leave little doubt that apes can learn to interpret visual signs and use them in communication. Other than humans, no mammal can speak. However, the fact that apes can’t speak

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has less to do with lack of intelligence than with differences in the anatomy of the vocal tract and language-related structures in the brain.

Beginning in the 1960s, after unsuc- cessful attempts by others to teach young chimpanzees to speak, psy- chologists Beatrice and Allen Gardner designed a study to test language capabilities in chimpanzees by teach- ing ASL (American Sign Language for the deaf) to an infant female named Washoe. The project began in 1966, and in 3 years, Washoe had acquired at least 132 signs. “She asked for goods and services, and she also asked ques- tions about the world of objects and events around her” (Gardner et al., 1989, p. 6).

Years later, an infant chimpan- zee named Loulis was placed in Washoe’s care, and she adopted him. Psychologist Roger Fouts and col- leagues wanted to know if Loulis would spontaneously acquire signing skills through contact with Washoe and other chimpanzees in the study group. Within just 8 days, Loulis began to imi- tate signs the other chimps were mak- ing. Also, Washoe deliberately taught Loulis how to make some signs. For example, when she wanted him to sit down, “Washoe placed a small plas- tic chair in front of Loulis, and then signed CHAIR/SIT to him sever- al times in succession, watching him closely throughout” (Fouts et al., 1989, p. 290).

There have been other chimpan- zee language experiments. A female named Sara was taught to recognize plastic chips as symbols for various objects. Importantly, the chips did not resemble the objects they represent- ed. For example, the chip that repre- sented an apple was neither round nor red. The fact that Sara was able to use the chips to communicate is significant because her ability to associate chips with concepts and objects to which they bore no similarity implies some degree of symbolic thought. And at the Yerkes Regional Primate Research Center in Atlanta, Georgia, two male

chimpanzees, Sherman and Austin, learned to communicate using a series of lexigrams, or geometric symbols, imprinted on a computer keyboard (Savage-Rumbaugh, 1986).

Other apes have also shown lan- guage abilities. The most famous of these is Koko, a female lowland goril- la who was taught to use ASL by Dr. Francine Patterson in the 1970s. Furthermore, Michael, an adult male gorilla who was also involved in the same study until his death in 2000, had a considerable vocabulary, and the two gorillas regularly communicated with each other using sign language.

In the late 1970s, a 2-year-old male orangutan named Chantek (also at Yerkes) acquired approximately 140 signs, which he sometimes used to refer to objects and people not pres- ent. Chantek also invented signs and recombined them in novel ways, and he appeared to understand that his signs were representations of items, actions, and people (Miles, 1990).

Several people have questioned this type of experimental work. Do the apes really understand the signs they learn or are they merely imitating their train- ers? Do they learn that a symbol refers to or represents an object, or do they only understand that making a symbol will produce that object?

Partly in an effort to address some of these questions, psychologist Sue Savage-Rumbaugh taught the two chimpanzees Sherman and Austin to use symbols for categories of objects, such as “food” or “tool.” This was done in recognition of the fact that in pre- vious studies, apes had been taught symbols for specific items, not catego- ries. Using a symbol as a label isn’t the same thing as understanding the repre- sentational value of the symbol. But if chimpanzees could classify things into groups, it would indicate that they can use symbols referentially.

Sherman and Austin were taught to recognize familiar food items, for which they routinely used symbols, as belonging to a broader catego- ry referred to by yet another symbol,

chApTer 7 Primate Behavior 200

“food.” They were then introduced to unfamiliar food items, for which they had no symbols, to see if they would place them in the food category. The fact that they both had perfect or near- ly perfect scores for this task was fur- ther evidence that they could indeed categorize unfamiliar objects. More importantly, it was clear that they could assign symbols to indicate an object’s membership in a broad group- ing. This ability strongly indicated that the chimpanzees understood that the symbols represented not only objects but also groups of objects (Savage- Rumbaugh and Lewin, 1994).

One criticism of the conclusions drawn from the ape language studies has been that young chimpanzees must be taught to use symbols, while human children spontaneously acquire lan- guage through exposure without being deliberately taught. Therefore it was significant when Savage-Rumbaugh and her colleagues reported that Kanzi, an infant male bonobo, was spontane- ously acquiring and using symbols at the age of 2½ years (Savage-Rumbaugh et al., 1986) (Fig. 7-23).

While Kanzi showed a remark- able degree of cognitive complexity, it remains clear that apes don’t acquire

and use language in the same way humans do. Nonetheless, we now have abundant evidence that humans aren’t the only species capable of some degree of symbolic thought and complex communication.

The Evolution of Language

From an evolutionary perspective, the ape language experiments may suggest clues to the origins of human language. It’s also highly significant that free-ranging great apes use some gestures for communication (King, 2004). In fact, it’s possible that the last common ancestor we share with the living great apes had communication capabilities similar to those we see in these species. Thus we need to identi- fy the factors that enhanced the adap- tive value of these abilities in our own lineage.

While increased brain size played a crucial role in human evolution, it was changes in preexisting neurologi- cal structures that permitted the devel- opment of language. Current evidence suggests that new structures and novel

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The Evolution of Language 201

connections haven’t generally been the basis for most of the neurologi- cal differences we see among species. Rather, reorganization, elaboration, and/or reduction of existing structures, as well as shifts in the proportions of existing connections, have been far more important (Deacon, 1992). It’s also important to understand that the neurological changes that enhanced language development in humans wouldn’t have occurred if early homi- nins hadn’t already acquired the behav- ioral and neurological foundations that made them possible. For reasons we don’t yet fully understand, communi- cation became increasingly important during the course of human evolution, and natural selection favored ana- tomical and neurological changes that enhanced our ancestors’ ability to use spoken language.

In most people, language function is located in the left hemisphere, meaning it’s lateralized. (The left hemisphere is the dominant hemisphere in most peo- ple, and since it controls motion on the right side of the body, most people are

right-handed.) Two regions in particu- lar, Broca’s area in the left frontal lobe and Wernicke’s area in the left tem- poral lobe, are directly involved in the production and perception, respective- ly, of spoken language (Fig. 7-24).

Broca’s area is located in the motor cortex immediately adjacent to a region that controls the movement of muscles in the face, lips, larynx, and tongue. When a person is speaking, informa- tion is sent to Broca’s area, where it’s organized specifically for communi- cation. Then it’s sent to the adjacent motor areas, which in turn activate the muscles involved in speech. We know that Broca’s area operates this way because when it’s damaged, speech production is impaired, even though there’s no muscle paralysis. Paralysis occurs only when nearby areas that control facial muscles are damaged, not when the damage is confined to Broca’s area.

Wernicke’s area is an association area that lies near structures involved in the reception of sound. A lesion in Wernicke’s area doesn’t impair hearing,

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but it severely affects language compre- hension. This, in turn, interferes with speech production because auditory information that is related specifical- ly to language is sent from Wernicke’s area to Broca’s area by way of a bun- dle of nerve fibers connecting the two regions.

But the perception and produc- tion of speech involve much more than these two areas, and the use of written language requires still other neurologi- cal structures. Eventually, information relating to all the senses (visual, olfac- tory, tactile, and auditory) is combined and relayed to Broca’s area, where it’s translated for speech production. This uniquely human ability depends on the interconnections between receiving areas for all sensory stimuli. While the brains of other species have such areas, they don’t have the ability to transform sensory information for the purpose of using language—or maybe they do at least to some degree.

Cantalupo and Hopkins (2001) report that magnetic resonance imag- ing of chimpanzee, bonobo, and goril- la brains demonstrates that in these species a region analogous to part of Broca’s area is larger on the left side than on the right. These authors fur- ther report that in captive great ape studies, gestures are preferentially made by the right hand (controlled by the left hemisphere), especially when gestures are combined with vocaliza- tions. This study suggests, therefore, that perhaps the anatomical basis for the development of left-hemisphere dominance in speech production in humans was present, at least to an incipient degree, in the last common ancestor of humans and the African great apes.

Specialization of auditory centers of the left hemisphere for language may have preceded the evolutionary diver- gence of humans and apes. A team of neuroscientists has shown that, to a degree, rhesus macaques also have this type of lateralization (Poremba et al., 2004). In these monkeys, evidence suggests that the left temporal lobe is specialized for processing the vocal-

izations of other rhesus macaques in particular.

The identification of a regulato- ry gene involved in speech may pro- vide another piece to the puzzle of the evolution of human language. This gene, called FOXP2, produces a pro- tein that influences the expression of other genes. In turn, those genes con- trol the embryological development of brain circuits that relate to language in humans. People who inherit a particu- lar FOXP2 mutation have developmen- tal disorders in the brain that cause severe speech and language impair- ment (Lai et al., 2001).

The FOXP2 gene isn’t unique to humans. In fact, it’s present in mice, indicating that all mammals probably have it. But while FOXP2 is important to neurological development in non- human mammals, it has nothing to do with language in these species. When researchers compared the human form of the FOXP2 protein with that of chimpanzees and gorillas, they found that the human protein differed from the two ape versions by two amino acid substitutions. This means that since humans last shared a common ances- tor with chimpanzees and gorillas, the gene has undergone two point muta- tions during the course of human evo- lution. But in chimpanzees and goril- las, it hasn’t changed.

The FOXP2 gene is the first gene demonstrated to influence language development. It varies between our- selves and closely related species, indi- cating not only that natural selec- tion has acted on it in our lineage but also that the FOXP2 protein may have played a role in the development of lan- guage capacities in humans.

Primate Cultural Behavior One important trait that makes pri- mates, and especially chimpanzees, attractive as models for early hominin behavior may be called cultural behav- ior. Although many cultural anthropol- ogists and others prefer to use the term culture specifically to human activities, most biological anthropologists con-

The Evolution of Language 203

sider it appropriate to apply the term to many nonhuman primate behaviors, too (McGrew, 1992, 1998; de Waal, 1999; Whiten et al., 1999).

Cultural behavior is learned, not genetically determined, although the capacity to learn is greatly influenced by genes. Whereas humans deliberately teach their young, free-ranging nonhu- man primates (with the exception of a few reports) don’t appear to do so. But at the same time, like young nonhuman primates, human children also acquire a tremendous amount of knowl- edge through observation rather than instruction (Fig. 7-25). By watching their mothers and other members of their group, nonhuman primate infants learn about food items, appropriate behaviors, and how to use and modify objects to achieve certain ends. In turn, their own offspring will observe their activities. What emerges is a cultural tradition that may eventually come to typify an entire group or even a species.

The earliest reported exam- ple of cultural behavior concerned a study group of Japanese macaques on Koshima Island, Japan. In 1952, Japanese researchers began feeding the

macaques sweet potatoes. The follow- ing year, a young female started wash- ing her potatoes before eating them. Within 3 years, several other monkeys were also washing their potatoes. The researchers pointed out that dietary habits and food preferences are learned and that potato washing is an exam- ple of nonhuman culture. Because the practice arose as an innovative solution to a problem (removing dirt) and grad- ually spread through the troop until it became a tradition, it was seen as con- taining elements of human culture.

A study of orangutans listed 19 behaviors that showed sufficient regional variation to be classed as “very likely cultural variants” (van Schaik et al., 2003). Four of these were differ- ences in how nests were used or built. Other behaviors that varied included the use of branches to swat insects and pressing leaves or hands to the mouth to amplify sounds.

The use of tools or objects to accomplish tasks has always been con- sidered one of the hallmarks of being human. In fact, tool use and lan- guage have traditionally been said to set humans apart from other animals.

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▲�Figure 7-25 (a) This little girl is learning basic computer skills by watching her older sister. (b) A chimpanzee learns the art of termiting through intense observation.

However, we now know that humans are not the only animals that use tools. A few nonhuman primates also use tools, with chimpanzees being the most notable example. What’s more, tool use isn’t even restricted to pri- mates. New Caledonian crows modify and use leaf stems to probe for insect larvae, and in captivity, they’ve bent

wire to make “hooks” to obtain food (Hunt, 1996; Weir et al., 2008); and sea otters use rocks to crack open abalone shells (Fig. 7-26). Nevertheless, tool use is most elaborate among primates and, needless to say, no other species even comes close to developing tools to the degree that humans have. But human technology had to begin some- where, so we briefly discuss some of the many examples of tool use in non- human primates.

Reports of tool use by gorillas aren’t common, but recently Breuer et al. (2005) reported seeing two female low- land gorillas in the DRC using branch- es as tools. In one case, a gorilla used a branch to test the depth of a pool of water. Then, as she waded bipedally through the pool, she used the branch again, this time as a walking stick (Fig. 7-27).

Chimpanzees exhibit more com- plex forms of tool use than any other nonhuman primate. They routinely insert twigs and grass blades into ter- mite mounds in a practice primatolo- gists call “termite fishing” (refer back to Fig. 7-25). The termites seize the twig in an attempt to protect their nest; but unfortunately for them, they become

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The Evolution of Language 205

a light snack once the chimpan- zee pulls the twig out of the mound. Importantly, chimpanzees frequently modify some of their stems and twigs by stripping the leaves—in effect, mak- ing a tool. For example, chimpanzees often choose a particular piece of vine, twig, or palm frond, remove leaves or other extraneous material, and then break off portions until it’s the proper length. Chimpanzees have also been seen making these tools even before the termite mound is in sight.

The modification of natural objects for use as tools has several implica- tions for nonhuman primate intel- ligence. First, the chimpanzees are involved in an activity that prepares them for a future task at a somewhat distant location, and this implies plan- ning and forethought. Second, atten- tion to the shape and size of the raw material indicates that chimpanzees have a preconceived idea of what the finished product needs to be in order to be useful. To produce a tool, even a simple one, based on a concept is an extremely complex behavior that, as we now know, is not the exclusive domain of humans.

Primatologists have been aware of termite fishing and similar behaviors since the 1960s, but they were sur- prised by the discovery that chimpan- zees also use tools to catch small prey. Preutz and Bertolani (2007) reported that savanna chimpanzees in Senegal, West Africa, sharpen small branches to use as thrusting spears for captur- ing galagos. This is the first report of a nonhuman primate hunting with what is basically a manufactured weapon.

On 22 occasions, 10 different ani- mals jabbed sharpened sticks into cavi- ties in branches and trunks to extract galagos from their sleeping nests. In much the same way they modify ter- miting sticks, these chimpanzees had stripped off side twigs and leaves. But they’d also chewed the ends to sharpen them, in effect producing small thrust- ing “spears”.

After several thrusts, the chim- panzee would reach into the open- ing to see if there was anything to be

had. Observers only saw one gala- go being retrieved and eaten, and although it wasn’t moving or vocal- izing, it was unclear if it had actually been killed by the “spear” (Preutz and Bertolani, 2007).

In several West African study groups, chimpanzees use unmodi- fied stones as hammers and anvils (Fig. 7-28) to crack nuts and hard- shelled fruits (Boesch et al., 1994). Interestingly, stone hammers and platforms are used only in West African groups and not in East Africa. Likewise, termite fishing is seen in Central and East Africa, but apparent- ly it’s not done in West African groups (McGrew, 1992).

The fact that chimpanzees show regional variation in the types of tools they use is significant because these variations are cultural differences. Chimpanzees also exhibit region- al dietary preferences (Nishida et al., 1983; McGrew, 1992, 1998). For exam- ple, oil palm fruits and nuts are eaten at many locations, including Gombe. But even though oil palms also grow in the Mahale Mountains (only about 90 miles from Gombe), the chimpan- zees there seem to ignore them. Such regional patterns in tool use and food preferences are very similar to the

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chApTer 7 Primate Behavior 206

cultural differences typi- cal of humans. Therefore it’s possible that this kind of variation existed in early hominins too.

So far we’ve focused on tool use and cul- ture in great apes, but they aren’t the only nonhuman primates that consistently use tools and exhibit ele- ments of cultural behav- ior. Primatologists have been studying tool use in capuchin or cebus mon- keys for over 30 years. Capuchins are found in South America in Colombia, Venezuela, Brazil, and Northern Argentina. They are the most encephalized of all monkeys and, while forest-dwelling capu- chin species are arbo- real, other species live in

a more savanna-like habitat, and these spend a fair amount of time on the ground. It’s these more terrestrial mon- keys that have been studied because of their tool use.

Many of the capuchin tool-using behaviors parallel those we’ve dis- cussed for chimpanzees. Capuchins use leaves to extract water from cav- ities in trees (Phillips, 1998), and they use small, modified branches to probe holes in logs for invertebrates (Westergaard and Fragaszy, 1987). But what they’ve really become known for is using stones to obtain food. They use stones to smash foods into smaller pieces, crack palm nuts, break open hollow tree branches and logs, and dig for tubers and insects. Capuchins are the only monkeys known to use stones as tools and the only nonhuman pri- mates to dig with stones (Moura and Lee, 2004; Visalberghi, 1990; Moura and Lee, 2004; Ottoni and Izar, 2008).

The importance of palm nuts as a food source is revealed by the enor- mous effort required to obtain them. Adult female and male capuchins weigh

around 6 to 8 pounds, respectively, yet they walk bipedally carrying stones that weigh as much as 2 pounds (25 to 40 percent of their own body weight) (Fragaszy, et al., 2004; Visalberghi, et al., 2007). Because the stones are heavy, it’s difficult for capuchins to sit while cracking nuts, so they frequently stand bipedally, raise the hammer stone with both hands, and then pound the nut using their entire body (Fig. 7-29).

Capuchins who use stones to crack nuts and dig for roots have one extremely important thing in com- mon with chimpanzees who dig with sticks and hunt galagos with sharpened branches: They all live in seasonally dry, open woodland environments and not in forests. In general, this is similar to the habitat occupied by early homi- nins. Of course capuchins and chim- panzees aren’t hominins, but those populations that live in more margin- al environmental settings face many of the same challenges encountered by early hominins. Moreover, chim- panzees and capuchins are among the most encephalized nonhuman pri- mates and have manipulative abili- ties similar to those of early hominins. By further studying these behaviors, researchers hope to better understand how dry, relatively open habitats, where resources are more scarce and unpre- dictable (compared with forest envi- ronments), may have been the con- text that stimulated the use of tools as a means of obtaining otherwise inac- cessible foods. Culture has become the environment in which modern humans live. Quite clearly, the use of sticks in termite fishing and hammer stones to crack nuts is hardly compa- rable to modern human technology. However, modern human technology is rooted in behaviors such as these. This doesn’t mean that nonhuman primates are “on their way” to becoming human. Remember, evolution isn’t goal direct- ed, and even if it were, there’s nothing to dictate that modern humans neces- sarily constitute an evolutionary goal. Such a conclusion is a purely anthro- pocentric view and has no validity in discussions of evolutionary processes.

▲�Figure 7-28 Chimpanzees in Bossou, Guinea, West Africa, use a pair of stones as a hammer and anvil to crack oil palm nuts. Although the youngster isn’t being deliberately taught to use stone tools, it’s learning about them through observation.

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Conflict between Groups 207

Conflict between Groups

For many primate species, especially those whose ranges are small, con- tact with one or more other groups of conspecifics is a daily occurrence, and the nature of these encounters can vary from one species to another. Primate groups are associated with a home range, where they remain permanently. (Although individuals may leave their home range and join another commu- nity, the group itself remains in a par- ticular area.) Within the home range is a portion called the core area. This area contains the highest concentra- tion of predictable resources, and it’s where the group is most likely to be found. Although portions of the home range may overlap with that of one or more other groups, core areas of adja- cent groups don’t overlap. The core area can also be said to be a group’s territory; it’s the portion of the home range defended against intrusion. In some species, however, other areas of the home range may also be defended.

Not all primates are territorial. In general, territoriality is associated with species whose ranges are suffi- ciently small to permit patrolling and

protecting (such as gibbons and ver- vets). But male chimpanzees are highly intolerant of unfamiliar chimpanzees, especially other males, and fiercely defend their territories and resources. Therefore interactions between groups of chimpanzees almost always include aggressive displays, chasing, and some- times fighting.

In recent years, a good deal of atten- tion has been focused on lethal attacks by male coalitions on other chimpan- zees. Such attacks occur when a num- ber of individuals attack and some- times kill one or two others who may or may not be members of the same group. Lethal aggression is relatively common between groups of chimpan- zees. It has also been reported for a few monkey species, including capuchins (Gros-Louis et al., 2003).

Groups of male chimpanzees, sometimes accompanied by one or two females, patrol the boundar- ies of their home range and some- times enter another group’s territory (Wrangham, 1999; Wilson et al., 2004). While they’re patrolling, chimpan- zees travel silently in compact group- ings (Fig. 7-30). They stop frequent- ly to sniff, look around, or climb tall trees, where they may sit for an hour or more surveying the region. During

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core area The portion of a home range containing the highest concentration and most reliable supplies of food and water. The core area is defended.

territories portions of an individual’s or group’s home range that are actively defended against intrusion, especially by members of the same species.

chApTer 7 Primate Behavior 208

such times, they appear to be tense, and a sudden sound, such as a snapping twig, causes them to touch or embrace each other for reassurance (Goodall, 1986). It’s apparent from their nervous behavior and uncharacteristic silence that they know they’re venturing into a potentially dangerous situation.

Before they enter peripheral areas, chimpanzees usually hoot and display to determine if other animals are pres- ent. If members of another community appear, some form of aggression occurs until one group retreats. But if the intruders encounter a female with an infant or a lone male, they will almost certainly attack, and chances are good that an infant or a single male will be killed. (Mothers of killed infants are frequently allowed to escape.)

Beginning in 1974, Jane Goodall and her colleagues witnessed at least five unprovoked and extremely bru- tal attacks by groups of chimpanzees (usually but not always males) upon lone individuals. To explain these attacks, we must point out that by 1973, the original Gombe communi- ty had split into two distinct groups, one in the north and the other in the south of what was once the origi- nal group’s home range. In effect, the southern splinter group had denied the others access to part of their former home range.

By 1977, all seven males and one female of the splinter group were either known or suspected to have been killed. All observed incidents involved several animals, usually adult males, who brutally attacked lone indi- viduals (Fig. 7-31). It’s impossible to know exactly what motivated the attacks, but it was clear that the attack- ers intended to incapacitate their vic- tims (Goodall, 1986). Whether chim- panzees actually intend to kill their victims is difficult to ascertain since we don’t know to what degree they have a concept of death.

The violence at Gombe has con- tinued over the years, although the actual number of observed attacks is low. Wilson and colleagues (2004) described four cases of aggression between groups at Gombe between 1993 and 2002. In these incidents, two infants were killed and eaten and two young adult males were severe- ly injured and presumed dead, as they were never seen again. In all these attacks, the victims were either lone males or mothers with dependent young. And there were always at least four attackers; thus the risk of injury to the attackers was reduced.

A situation similar to the one at Gombe was also reported for a group of chimpanzees in the Mahale Mountains south of Gombe. Over a 17-year peri-

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▶�Figure 7-30 A chimpanzee border patrol. Note the bristling hair of the animal in front. This is an indication of excitement.

Conflict between Groups 209

od, all the males of a small commu- nity disappeared. Although no attacks were actually observed, there was cir- cumstantial evidence that most of these males met the same fate as the Gombe attack victims (Nishida et al., 1985, 1990).

Mitani and colleagues (2010) doc- ument a third such situation in a large chimpanzee community at Ngogo, Kibale National Park, Uganda. Between 1999 and 2009, members of this group were observed killing or fatally wounding 18 individuals from other groups, and all but one of the observed attacks were made by coali- tions of males on patrol. There was also convincing evidence of three additional lethal attacks. The entire Ngogo community now regularly uses the area where they frequently con- ducted border patrols and where 13 of the attacks occurred; meanwhile the former residents have not been seen. In effect, these chimpanzees have increased their territory by 2.5 square miles, or 22 percent. Given this fact, the researchers attribute the attacks on a neighboring group to territo- rial expansion, which increases the chimpanzees’ resource base and in turn may lead to greater reproductive success.

Even though chimpanzees clear- ly engage in lethal attacks, the actual number of observed incidents is low. In the period between 1966 and 1999 at Mahale, aggression accounted for 16 percent of known deaths. In all, 18 individuals are known to have been killed by adult males, and all but one were infants. Actually the major cause of death among the Mahale chimpan- zees was disease (Nishida et al., 2003); this is probably typical of most chim- panzee populations and perhaps early hominin populations as well. Certainly among preindustrial modern humans, infant childhood and adolescent mortality was at least 50 percent for most groups.

Efforts to identify the social and ecological factors that predispose males of some species to engage in lethal attacks have led to hypothe-

ses that attempt to explain the func- tion and adaptive value of these activi- ties (Manson and Wrangham, 1991; Nishida, 1991). In this context, the ben- efits and costs of extreme aggression must be identified. The principal ben- efits to aggressors are protection and acquisition of territory (thus reduced competition for resources), and per- haps the acquisition of mating part- ners, especially in cases of infanticide. Costs include risk of injury or death and loss of energy expended in per- forming aggressive acts, but these risks are greatly reduced, since attacks occur only when the attackers considerably outnumber their victim.

Although we may never have a pre- cise explanation for lethal raiding, it appears that protection and acquisi- tion of resources are of major impor- tance (Goodall, 1986; Nishida et al., 1990; Manson and Wrangham, 1991; Nishida, 1991; Aureli et al., 2006; Mitani et al., 2010). Early hominins and chimpanzees may have inherited from a common ancestor the predis- positions that have resulted in shared patterns of strife between popula- tions. It’s difficult to draw direct com- parisons between nonhuman primate conflict and human warfare, partly because of elaborations of human cul- ture including symbols (such as flags), religion, and language. But it’s impor- tant to speculate on the fundamental issues that may have led to the devel- opment of similar patterns in different species, and the acquisition and pro- tection of resources was undoubtedly crucial. In fact, even though nations go to war for many stated reasons, such as religion or retaliation, the underlying, most basic causes almost always have to do with increased access to resources, be they water, ter- ritory, or oil.

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▲ Figure 7-31 The right ulna (the long bone on the little finger side of the forearm) of a female Gombe chimpan- zee called Madam Bee. Madam Bee was one of the 1970s attack victims. The enlarged area of the shaft is the site of a healing fracture near the wrist. Apparently the bone was broken in one attack and had partially healed. (The enlarged area is a result of the healing process). Then the bone was rebroken in a subsequent episode. (As her left arm had been paralyzed by polio, she had only her right arm to defend herself.) Madam Bee died within a few days of the last attack. Her adult daughter frequently sat next to her before her death.

chapter 7 Primate Behavior 210

prosocial behaviors actions that benefit other individuals and/or a society as a whole. Loosely speaking, the term “prosocial” is the opposite of “antisocial.”

altruism actions that benefit another individual but at some potential risk or cost to oneself.

Prosocial Behaviors: Affiliation, Altruism, and Cooperation

Earlier, we discussed affiliative behaviors and the role they play in maintaining nonhuman primate group cohesion by reinforcing bonds between individuals. There are also prosocial behaviors that indicate just how important social bonds are; these include assistance, sharing, caregiving, and perhaps even compassion. Humans are by far the most prosocial of spe- cies. It’s not uncommon for people to risk their lives to save the lives of oth- ers, even strangers. On a simpler level, we pick things up for each other; we help strangers who’ve fallen down; we contribute to charities that help peo- ple we’ve never met; and we especially come to the assistance of children and the elderly (Fig. 7-32). Why we have a propensity to do this isn’t well under- stood, but studying these behaviors in other primates can help clarify this important issue.

Laboratory studies have been instrumental in testing food-sharing tendencies in nonhuman primates. These studies have shown that bono- bos and some monkeys, in particular, engage in sharing behaviors similar to those seen in humans. When given the option to perform tasks to obtain food

solely for themselves or for themselves and another animal, both capuchins and bonobos most frequently chose the latter option (Lakshminarayan and Santos, 2008; Hare and Kwetuenda, 2010). Indeed, bonobos showed a clear preference for eating with anoth- er unrelated individual even when it meant sharing highly desirable food items.

Altruism Altruism is behavior that bene- fits another individual while involv- ing some risk or sacrifice to the per- former. Cooperation, assistance, and

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Prosocial Behaviors: Affiliation, Altruism, and Cooperation 211

altruism are fairly common in many primate species, and altruistic acts sometimes contain elements of com- passion. It’s somewhat risky to use the term compassion because in humans, compassion is motivated by empa- thy for another individual. We don’t know whether nonhuman primates can empathize with another’s situation, but many researchers believe they do. Cer- tainly there are many examples, most- ly from chimpanzee studies, of actions that resemble compassionate behav- ior in humans. Examples include pro- tecting victims during attacks, helping younger siblings, and remaining near ill or dying relatives or friends.

Some other examples involve chim- panzees attempting to rescue others who have fallen into water. Because chimpanzees can’t swim, jumping into water is a life-threatening action. Nevertheless, there are several reports of chimpanzees doing just that, espe- cially in zoos where water-filled moats sometimes surround portions of chim- panzee exhibits. In one case, an adult male actually drowned while trying to save an infant that had fallen into the water (de Waal, 2007).

The most fundamental of altruis- tic behaviors, protecting dependent offspring, is ubiquitous among mam- mals and birds; in most species, altru- istic acts are confined to this context. Among primates, however, recipients of altruistic acts may include indi- viduals who aren’t offspring and who may not even be closely related to the performer.

Chimpanzees routinely come to the aid of relatives and friends, female hanuman langurs join forces to pro- tect infants from infanticidal males, and male baboons protect infants and cooperate to chase predators. In fact, the primate literature abounds with examples of altruistic acts—individu- als placing themselves at risk to protect others from attack.

One very intriguing report con- cerns the attempted rescue of a young adult male baboon who, at some dis- tance from his group, was being chased by a hyena. Suddenly, observers saw an

adult female racing toward the hyena in what turned out to be a vain attempt to rescue the male (Stelzner and Strier, 1981; Strier, 2003). The female wasn’t the victim’s mother, and a female baboon is no match for a hyena. So why would she place herself in serious dan- ger to help an animal to whom, as far as was known, she wasn’t closely related? We don’t know, but this was clearly an altruistic albeit unsuccessful act.

Adopting orphans is a form of altru- ism that has been reported for capu- chins, macaques, baboons, and espe- cially chimpanzees. When chimpanzee youngsters are orphaned, they’re rou- tinely adopted, usually by older sib- lings, who are solicitous and highly protective. Adoption is crucial to the survival of orphans, who certainly wouldn’t survive on their own.

Evolutionary explanations of altru- ism are based on the premise that indi- viduals are more likely to perform risky or self-sacrificing behaviors for the benefit of a relative who shares genes with the performer. According to this hypothesis, known as kin selection, an individual may enhance his or her reproductive success by saving the life of a relative. Even if the performer’s life is lost because of the act, the relative may survive to reproduce and pass on genes that both individuals shared.

There’s also the hypothesis of recip- rocal altruism, where the recipient of an altruistic act (that is, the one who benefits) may later return the favor. Coalitions, or alliances between two or more individuals, are an often cited example of reciprocal altruism, and they’re common among baboons and chimpanzees. As we mentioned ear- lier, members of alliances support and defend one another in conflicts with others and may use the alliance to increase their status within the group hierarchy. Even though reciprocal altruism may occur, it’s a hypothesis that needs further testing.

Group selection is a third hypoth- esis that some primatologists have supported. According to this model, an individual may act altruistically to benefit other group members because

empathy The ability to identify with the feelings and thoughts of another individual.

chApTer 7 Primate Behavior 212

ultimately it’s to the performer’s ben- efit that the group be maintained. If the altruist dies, genes he or she shares with other group members may still be passed on (as in kin selection). But there’s a problem with group selection theory: According to natural selection theory, individual reproductive success is enhanced by acting selfishly, and the individual is the object of natural selection.

Although the group selection issue hasn’t been resolved, we do know that for many reasons primates, includ- ing humans, have a better chance of surviving and reproducing if they live in groups. Given this important fact, any behavioral mechanism that reinforces the integrity and cohe- sion of social groupings works to the advantage of individual group mem- bers. These mechanisms include altruism, perhaps a form of compas- sion, and a certain degree of empathy (de Waal, 2005).

Primatologist Frans de Waal has published extensively on empathy and altruism in chimpanzees. He points out that theories of kin selection, recip- rocal altruism, and group selection ultimately explain altruism and coop- eration in terms of selfishness. But this is the explanation of how the behaviors evolved, not the motivation of the ani- mal performing the altruistic act, and de Waal views the immediate moti- vation as a function of “sensitivity to the needs of others,” or empathy. He states, “In humans, the most common- ly assumed motivation behind altruism is empathy. We identify with anoth- er in need, pain, or distress, which induces emotional arousal that may translate into sympathy and helping. Inasmuch as there are signs of empathy in other animals, from rodents to pri- mates, the same hypothesis may apply” (de Waal, 2007).

The issue of empathy is much dis- cussed, and not all primatologists agree that nonhuman primates pos- sess a true capacity for it. Nonetheless, many behaviors certainly support the hypothesis that empathy is a behav- ioral trait that other species have at

least to some degree. Further studies no doubt will clarify the issue and pro- vide yet another example of behavioral continuity between other primates and ourselves.

The Primate Continuum

It’s an unfortunate fact that humans generally view themselves as sepa- rate from the rest of the animal king- dom. This perspective is partly due to a prevailing lack of knowledge of the behavior and abilities of other spe- cies. Moreover, these notions are con- tinuously reinforced through exposure to advertising, movies, and television (Fig. 7-33).

For decades, behavioral psychology taught that animal behavior represents nothing more than a series of condi- tioned responses to specific stimuli. (This perspective is very convenient for those who exploit nonhuman ani- mals, for whatever purposes, and want to remain guilt-free.) Fortunately this attitude has begun to change in recent years to reflect a growing awareness that humans, although in many ways unquestionably unique, are neverthe- less part of a biological continuum as well as a behavioral continuum. We are connected not only to our closest rela- tives, the other primates, but also to all life on earth.

Where do humans fit in this con- tinuum? The answer depends on the criteria used. Certainly we’re the most intelligent species if we define intelli- gence in terms of problem-solving abil- ities and abstract thought. However, if we look more closely, we recognize that the differences between ourselves and our primate relatives, especially chim- panzees and bonobos, are primarily quantitative and not qualitative.

Although the human brain is abso- lutely and relatively larger, neurologi- cal processes are functionally the same. The necessity of close bonding with at least one parent and the need for physi- cal contact are essentially the same.

biological continuum refers to the fact that organisms are related through common ancestry and that behaviors and traits seen in one species are also seen in others to varying degrees. (When expressions of a phenomenon continu- ously grade into one another so that there are no discrete categories, they are said to exist on a continuum. color is one such phenomenon.)

213How Do We Know?

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Developmental stages and dependence on learning are similar. Indeed, even in the capacity for cruelty and aggres- sion combined with compassion, ten- derness, and altruism, as exhibited by chimpanzees, we see a close par- allel to the dichotomy between “evil” and “good” so long recognized in our- selves. The main difference between how chimpanzees and humans express these qualities (and therefore the dichotomy) is one of degree. Humans are much more adept at cruelty and compassion, and we can reflect on our behavior in ways that chimpanzees cannot. Like the cat that plays with a mouse, chimpanzees don’t seem to understand the suffering they inflict on others. But humans do. Likewise, while an adult chimpanzee may sit next to a dying relative, it doesn’t seem to feel the intense grief a human normally does in the same situation.

To arrive at any understanding of what it is to be human, it’s impor- tant to recognize that many of our behav- iors are elaborate extensions of those of our hominin ances- tors and close primate relatives. The fact that so many of us prefer to bask in the sun on a beach with hun- dreds or thousands of others reflects our heritage as social animals adapt- ed to life in the tropics. And the sweet tooth that afflicts so many of us is a result of our earlier primate ancestors’ predilection for the high-energy sugar contained in ripe fruit. Thus it’s impor- tant to recognize our primate heritage as we explore how humans came to be and how we continue to adapt.

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◀ Figure 7-33 Stereotypes and miscon- ceptions many people have of our closest relatives are illustrated by (a) this unfortunate advertising display and (b) a well-meaning but ill-informed poster.

What we know about nonhuman primate behavior has been obtained by literally tens of thousands of hours spent by primatologists collecting data while observ- ing nonhuman primates in the wild. Frequently such observations are made under uncomfortable and sometimes dangerous circumstances. These observa- tions have produced studies in which hypotheses about primate behavior and the evolution of human behav-

ior have been tested, refined, and retested. The devel- opment of various kinds of DNA testing procedures has been immensely helpful in the testing of several hypotheses. As primate research continues, we will one day be able to answer many of the questions we still have about our closest relatives and how certain aspects of human behavior came to be.

How Do We Know?

chapter 7 Primate Behavior 214

▶▶ The fundamental principle of behavioral evolution is that aspects of behavior (including social behav- ior) are influenced by genetic factors. Because some behavioral elements are influenced by genes, natural selection can act on them in the same way it acts on anatomical characteristics.

▶▶ Behavioral ecology is the discipline that examines behavior from the perspective of complex ecologi- cal relationships and the role of natural selection as it favors behaviors that increase reproductive fitness. This approach generates many models of behavioral evolution that can be applied to all spe- cies, including humans.

▶▶ Members of each species inherit a genome that is species-specific, and some part of that genome influences behaviors. But in more complex ani- mals, the genome allows a greater degree of behav- ioral flexibility and learning. In humans, who rely on cultural adaptations for survival, most behavior is learned.

▶▶ Life history traits or strategies (developmental stages that characterize a species) are important to the reproductive success of individuals. These traits include length of gestation, number of off- spring per birth, interbirth interval, age of sexual maturity, and longevity. Although these charac- teristics are strongly influenced by the genome of any species, they’re also influenced by environ- mental and social factors, such as nutrition and social status. In turn, nutritional requirements are affected by body size, diet, and basal metabolic rate (BMR).

▶▶ There are several types of primate social groups: one male–multifemale groups, multimale- multifemale groups, bonded pairs consisting of one male and one female and subadult offspring, polyandrous groups consisting of one female and usually 2 males, and more or less solitary individuals.

▶▶ Primatologists have provided various explanations for why primates live in social groups (for example, predator avoidance and competition for resources with other groups).

▶▶ Primates are among the most social of animals, but within social groups there is competition for resources and conflict. Dominance hierarchies help to reduce the amount of physical aggression. Also, there are numerous amicable behaviors, such as grooming, that maintain peaceful relationships between individuals.

▶▶ Males of many primate and nonprimate species attack and kill infants. The reason for this has been debated among anthropologists for years, but one recurring explanation is that infanti- cide increases the male’s reproductive success. While this remains to be proved, there have now been some DNA studies that have supported this hypothesis.

▶▶ The relationship between mothers and infants is the most important interaction among primates, and there is increasing evidence that males provide more parental care than was previously thought.

▶▶ Affiliative behaviors such as grooming, hugging, and helping others (altruism) also promote group cohesion.

▶▶ Communication makes it possible to live in social groups. It occurs in many forms, including vocal- izations and gestures. Some primate species are able to communicate about certain aspects of the external environment, indicating some ability to think symbolically.

▶▶ Long-term language studies with the great apes have shown that these species have the ability to communicate using different kinds of symbols, including sign language. Many of those involved in language studies also understand spoken language.

▶▶ Several nonhuman primates exhibit aspects of cul- ture, including tool use and regional variation in dietary preferences. These variations represent cultural traditions that were perhaps present in early hominins.

▶▶ Biological and behavioral continuity within the primate order reveals how humans are connected to our closest relatives and allows us to explain some aspects of human behavior.

Summary of Main Topics

215Critical Thinking Questions

1. Apply some of the topics presented in this chap- ter to some nonprimate species with which you are familiar. Can you develop some hypotheses to explain the behavior of some domestic species? You might want to speculate on how behavior in domestic animals may differ from that of their wild ancestors. (Chapter 2 might help you here.)

2. We used birds as an example of sexual dimor- phism resulting from sexual selection. But there are some bird species in which males, not females, sit on the nest to warm and protect the eggs. These males are less colorful than the females. How would you explain this? (Hint: Sexual selec- tion may not be the only factor involved in sexual dimorphism in bird coloration.)

3. Speculate on how the behavioral ecology of non- human primates may be helpful in explaining some human behaviors.

4. How might infanticide be seen as a reproductive strategy for males? What would you say if you saw a newspaper article that applied this concept (not the act itself) to human males? Do you think some people would object? Why or why not?

5. Do you think that knowing about aggression between groups of chimpanzees is useful in under- standing conflicts between human societies? Why or why not?

6. Why are the language capabilities of nonhuman primates important to our understanding of how our own species may have acquired language?

Critical Thinking Questions

Fossil evidence indicates our primate origins date to at least 65 million years ago.

Connections

Partly because of common evolutionary history, many human

behaviors are also seen in other primates.

Paleoanthropology, which includes physical anthro- pology, archaeology, and geology, provides the sci- entific basis to understand

hominin evolution.

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After mastering the material in this chapter, you should be able to:

▶ �Describe the major anatomical and dental features that characterized the earliest primates and explain how they compare with the most primitive of the living primates (the lemurs and lorises).

▶ �Describe the major geographical areas and general dating of the key early fossil evidence of the primate order.

▶ �Define homoplasy and convergent evolution and give at least one example from primate evolution. Explain why this occurs.

▶ �Describe the evolution and subsequent dispersal of the superfamily Hominoidea (apes and humans) during the Miocene. Explain the significance of Afropithecus and Griphopithecus.

▶ �Discuss how the massive extinct ape Gigantopithecus fits into the primate family tree.

217

When gazing into the eyes of a great ape, we see in them something unique that we feel inside ourselves. Often, however, when looking into the eyes of a gala- go (“bush baby”), we see nothing but a cuddly animal that we might like to take home as a pet (see Fig. 6-14 in Chapter 6). When most of us think back to the origins of our own spe- cies, we generally stop once we’ve evoked the idea of an upright-walking ape ancestor. But have you ever con- sidered extending your family tree to the baboons you may see in a wildlife park or to the lemurs or bush babies you see in the zoo? You might think, “How can a creature so small and, well, animal-like have anything to do with us or our evolutionary background?” In this chapter, we focus on bridging the gap between these creatures and our- selves—between strepsirhines and haplorhines—to help us better under- stand our own evolutionary history.

As we’ve seen in Chapters 6 and 7, some of our primate cousins share many of the traits we generally think of as uniquely human. Many of these similarities can be traced to shared origins in highly social groups liv- ing in the trees. We see these origins in the structure of our body and in the retention of many primitive fea- tures, such as pentadactyly (five fin- gers and toes) and unfused lower arm bones, but also in more “derived” skel- etal traits that came later. Among the most important of these derived pri- mate traits are evolutionary trends toward a more orthograde (upright)

8 Overview of the Fossil Primates

body position and more forward- facing eyes. Distinguishing these uniquely primate features in the fossil record as being different from those traits found in more distantly related mam- malian cousins is the first step in rec- ognizing our own beginnings. As we move in time through the Cenozoic era (see Chapter 5), we see in rough form the recapitulation of our own (pri- mate) order from “primitive” to highly derived. We’ll also trace the develop- ment of mammals that resemble us more and more over time until we con- clude this chapter in the Miocene, 23 to 5 million years ago (mya), with the emergence of the first hominoids (apes) and then the first possible homi- nins (humans). As you’ll see, our abil- ity to recognize primate families in the fossil record not only uses the same skills that allow us to discover our later

Student Learning Objectives

strepsirhines (strep-sir´-rines) Members of the primate suborder Strepsirhini, which includes lemurs and lorises.

haplorhines (hap-lore´-ines) Members of the primate suborder Haplorhini, which includes tarsiers, monkeys, apes, and humans.

derived Being or having a feature that is not present in the ancestral form.

orthograde Referring to an upright body position. This term relates to the posi- tion of the head and torso during sitting, climbing, etc., and doesn’t necessarily mean that an animal is bipedal.

cHapTeR 8 Overview of the Fossil Primates 218

human origins but also enables us to organize these creatures into meaning- ful groups.

This organization means that you’ll face a multitude of taxonomic desig- nations. These names aren’t meant to scare you, but they should impress upon you how successful past lineages of primates have been—in fact, much more so than they are now. As you’ll see, learning about the earliest begin- nings and recent past of our primate order can lend powerful perspective and meaning to our own origins, even though most of the fossil groups dis- cussed in this chapter never led to any extant (currently living) forms, and even fewer are related to our own hom- inin ancestors.

Background to Primate Evolution: Late Mesozoic

The exact origins of the earliest pri-mates aren’t well understood; in fact, they’re shrouded in some degree of mystery. We do know that follow- ing the extinction of the dinosaurs at the end of the Mesozoic, the reign of the giant reptiles was over and the Age of Mammals had begun. Primates were just one of the many groups of small mammals that were left to diversify and explore the many niches left vacant with the passing of the dinosaurs.

Primates began to diverge from closely related mammalian lin- eages during the Cretaceous, right around the mass extinction of dino- saurs. Some scientists place these closely related (“sister”) lineages into a superorder that includes tree shrews, flying lemurs (also known as the colugos, which don’t fly and aren’t lemurs), and primates (Fig. 8-1). Sister groups are the related new clades that result from the splitting of a single common lineage. It’s interest- ing to note that the closest relatives of this superorder are rabbits, rodents, and their relatives.

This diversification of early mam- mals took place in a global tropical cli- mate that accompanied the emergence of modern plants—although neither the exact region where primates first evolved nor the precise pressures that molded their adaptations are known. These uncertainties continue to intrigue scientists even today.

Primate Origins

The Cenozoic era is the broad time period during which most of pri- mate evolution has unfolded (and con- tinues to unfold). This time period is divided into seven epochs, the oldest of which is called the Paleocene (begin- ning 65 mya). For each of these broad epochs, we can roughly attribute a particular phase of primate evolution and development. However, evolution knows no temporal bounds, so the time line for these phases will always be imperfectly defined (more precise dates and particular fossil primate groups are discussed later in this chapter):

• Paleocene (65 to 55.8 mya): first archaic primates, plesiadapiforms

• Eocene (55.8 to 33 mya): first eupri- mates, early strepsirhines and haplorhines

• Oligocene (33 to 23 mya): early catarrhines, precursors to monkeys and apes

• Miocene (23 to 5.3 mya): monkeys and apes; first humanlike creatures

• Pliocene (5.3 to 1.8 mya): early hom- inin diversification

• Pleistocene (1.8 to 0.01 mya): early Homo

• Holocene (0.01 mya to present): modern humans

Paleontological evidence indi- cates that the first indisputable pri- mates emerged just before the Eocene epoch (56 mya). Given that this is their first occurrence in the fossil record, it has led many primate biologists to hypothesize that the initial radiation of archaic primates must have occurred long before this, perhaps during the

superorder a taxonomic group rank- ing above an order and below a class or subclass.

sister groups The relationship of new clades that result from the splitting of a single common lineage.

Primate Origins 219

late Cretaceous to early Paleocene time period (71 to 62 mya) (Miller et al., 2005; Bloch et al., 2007). Still, our search for the key time of evolutionary divergence—that is, the time when the last common ancestor of primates and their closest relatives lived—remains tricky. The last common ancestor (LCA) is the hypothetical species that was the last to exist before it speci- ated into the myriad of sister orders related to primates. This critical spe- cies is often difficult to pinpoint mor- phologically since it doesn’t yet have the shared derived traits found in the crown group (Fig. 8-2). This means that researchers can’t confidently asso- ciate it with any given fossil. A crown group is easier to identify because it includes all of the taxa that come after a major speciation event. All extant (currently living) groups and fossils sharing their specific derived traits are crown. Despite its lack of the clade’s derived traits, the LCA also belongs to the crown group. On the other hand, the stem group includes all of the taxa in a clade before a major speciation event. For this reason, like the LCA, stem group taxa are often difficult to recognize in the fossil record. In spite of this, many scientists feel more com- fortable classifying uncertain taxa as stem rather than committing them to the crown group (see Chapter 5 for a

more complete discussion of phyloge- netic concepts).

Thus the time when we can first confidently identify an archaic primate is almost assuredly an under estimate of the actual time of divergence (the assumed date when the last common ancestor lived). Molecular data, on the other hand, have often provided us with overestimates of this time (Steiper and Young, 2008; Wilkinson et al., 2011). What is important to realize, however,

Order Scandentia (tree shrews)

Order Primates (living primates + extinct relatives)

Order Dermoptera (flying lemurs)

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▲�Figure 8-1 The superorder which includes the sister orders of tree shrews, flying lemurs, and primates.

last common ancestor (LCA) The final evolutionary link between two related groups.

crown group all of the taxa that come after a major speciation event. crown groups are easier to identify than stem groups because the members possess the clade’s shared derived traits.

taxa (sing. taxon) a taxonomic group of any rank (e.g., species, family, or class).

stem group all of the taxa in a clade before a major speciation event. Stem groups are often difficult to recognize in the fossil record since they don’t often have the shared derived traits found in the crown group.

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▼�Figure 8-2 Visual representa- tion of crown group, stem group, and last common ancestor concepts. In this example both the stem group and crown group have last common ancestors.

220

Building Family Trees from Genes

Molecular anthropology uses genetics to investigate the biology and evolu- tion of humans and our closest relatives, the nonhuman primates. Before we can test specific hypotheses about primate evolution and adaptation, we must understand how primate species are related to each other. Molecular anthropologists use proteins, genes, and even genomes to test hypoth- eses regarding the relationships within the primate order. The use of molecular methods in this manner has revolutionized our knowledge of primate systematics and revealed evolutionary relationships that have otherwise been difficult to resolve.

This primate tree (Fig. 1) is compiled from recent research performed by two teams of molecular anthropologists (perelman et al., 2011; Jameson et al., 2011).

Molecular anthropologists can use DNa sequences to make inferences as to how long ago primate species last shared a common ancestor. Since mutations in DNa occur at a relatively constant rate, the dif- ferences between two samples are propor- tional to the time since they last shared a common ancestor. This is often referred to as the “molecular clock.” The fossil record can calibrate this “clock” with information about when species on a tree diverged from one another and thus how long it takes for mutations to accumulate. as with the construction of gene trees, molecular diver- gence dates are best inferred from multiple parts of the genome in order to ensure

that divergences calculated from different regions are generally consistent. In many cases, primate divergence times inferred from molecular data are much older than expected, which leaves the exciting pos- sibility that we are missing even more of the primate fossil record than previously thought.

advances in genome sequencing technology now allow for the collection of unprecedented amounts of molecular data so rapidly that new analytical meth- ods must be developed to analyze this data deluge. In this new age of genomics, molecular anthropologists are now using genome-scale data to further examine the evolutionary relationships of extant primate species as well as to identify the genotypes that underlie distinctly modern human characteristics.

A Closer Look

12 8

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▲�Figure 1 Molecular primate family tree based on the works of two research teams (see text). Dates of divergence are noted in the gold-colored nodes.

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Made to Order: Archaic Primates 221

is that (1) since molecular estimates of divergence dates (see “Building Family Trees from Genes,” left) are calibrated using known fossil dates, the two approaches are inextricably linked, and (2) determining the appropriate rate of mutation, which joins these two together, can be tricky. Together, these two approaches (morphological and molecular) now place the origins of indisputable primates at some time during the Paleocene about 65 mya (Steiper and Seiffert, 2012).

Made to Order: Archaic Primates

Fossil evidence indicates that during the earliest Paleocene, between 65 and 52 mya, a major radiation of archaic primates known as the plesiadapiforms occurred. Plesiadapiforms are members of an extinct group that occupies a con- troversial position in primate phylog- eny. When first discovered, these crea- tures were considered early members of the primate order, but in the 1960s this conclusion was reversed and they were treated as their own order, Plesi-

adapiformes. In recent years, however, the careful analysis of an amazing array of more newly discovered fossils has once again placed plesiadapiforms back within Primates (Bloch and Silcox, 2001; Silcox, 2001; Bloch and Boyer, 2002; Bloch et al., 2007). They are now gaining acceptance as a semiorder within Primates that is separate from the later euprimates (Silcox, 2007).

Plesiadapiforms are best known from a large number of fossil finds from the American West (especially Montana and Wyoming). Some of the more recent finds of these Paleocene mammals, particularly those from Clarks Fork Basin, Wyoming, have yielded a variety of nearly complete skeletons. Some members of this group exhibit a striking continuity of traits with some of the earliest strepsirhines from the later Eocene epoch. Although as many as six families are commonly recognized within this group, we’ll concentrate on the three families that are most pertinent for this discussion.

The first family, Purgatoriidae, counts among their numbers the oldest recognized archaic primate, Purgatorius (Clemens, 1974) (Fig. 8-3). Members of this extinct genus

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semiorder The taxonomic category above suborder and below order.

euprimates “True primates.” This term was coined by elwyn Simons in 1972.

◀�Figure 8-3 Artist’s representations of Purgatorius. (a) Rendering of the best-preserved jaw of Purgatorius with the front portion reconstructed. The dime is present to indicate the small scale of the specimen. (b) An artist’s depiction of Purgatorius based on our current knowledge of the groups to which it belongs. Note in particular the feet as they tread over the Paleocene sycamore and hackberry leaf litter.

cHapTeR 8 Overview of the Fossil Primates 222

are believed to have been about the size of modern rats, and at least two (and perhaps as many as four) species lived in the American Northwest dur- ing the earliest Paleocene about 65 mya (Lofgren, 1995; Clemens, 2004; Bloch et al., 2007). Evidence of a radiation of this kind, however, most likely indicates an origin in the late Cretaceous, 71 to 65 mya (see “A Closer Look: Building Family Trees from Genes” on p. 220). Based on Purgatorius’ placement at the base of their sister lineages (think “stem group”), it is important to note that postcranial material from Garbani Channel in northeastern Montana (dated to ~ 65 mya) reveals arboreal adaptation within the feet. This sup- ports the hypothesis that arboreal adaptation has been a prime mover in primate evolution since the very begin- ning of the order (see Chapter 6). This adaptation to life in the trees has differ- entiated primates from other similar- sized mammals as far back as the earli- est Paleocene (Chester et al., 2012).

Another family, Plesiadapidae, was among the more successful plesiadapi- form groups. They were chipmunk- to groundhog-sized mammals with large incisors similar to those of a rodent. However, unlike rodents, plesi- adapid incisors weren’t continuously growing and didn’t self-sharpen, sug- gesting that they used their incisors for a purpose other than gnawing. Some have suggested that this fam- ily subsisted on a vegetative diet of leaves supplemented with fruits. The best-known of this family is the genus Plesiadapis, which probably originated in North America but went on to col- onize Europe via a land bridge across Greenland before eventually dying out during the early Eocene.

The last family we’ll look at, Carpolestidae (whose name means “fruit stealer”), was quite common dur- ing the Paleocene in North America and Asia, although its members were never as successful as the plesiadapids. These creatures were much smaller, generally mouse- to rat-sized, though they exhibit the typically enlarged inci- sors seen in these early groups. They

also have additional specialized dental traits that allowed them to efficiently process fibrous vegetation as well as nuts and insects. For a long time, car- polestids were known only from fossil teeth and jaws, but our knowledge of them changed when a nearly complete skeleton of Carpolestes (Fig. 8-4) was discovered in the Clarks Fork Basin, in Wyoming (Bloch and Boyer, 2002). The Clarks Fork specimen is estimat- ed at about 3.5 ounces, the size of the average hamster, and its postcranial anatomy reveals many traits adapted to a highly arboreal environment (par- ticularly since it had opposable grasp- ing big toes with nails instead of claws). But unlike later euprimates that were fully adapted to living in the trees, Carpolestes displays no adaptations for leaping, though it was almost certainly a terminal branch feeder (Sargis et al., 2007).

Eocene Euprimates

During the Eocene epoch (55.8 to 33 mya) we see the gradual extinction of the plesiadapiforms and their replacement by the euprimates (Fig. 8-5). These mammals, unlike the plesiadapiforms, have definite recog- nizable and modern derived primate traits, such as forward-facing eyes, greater encephalization, a postorbital bar, nails instead of claws at the ends of their fingers and toes, and an oppos- able big toe (see Chapter 6). These and other basic primate features suggest an adaptation to environmental condi- tions that were fundamentally different from those experienced by the plesi- adapiforms, as this was a warmer cli- mate with year-round rainfall and lush, broad-leaved evergreen forests.

At the beginning of the Eocene epoch, North America and Europe were connected; they didn’t split apart until the middle Eocene. Meanwhile, during the middle to late Eocene, North America was sporadically con- nected to Asia via the Bering land bridge. These early connections between these three continents meant

postcranial Referring to all or part of the skeleton not including the skull. The term originates from the fact that in quadru- peds the body is posterior to the head; the term literally means “behind the head.”

Eocene Euprimates 223

that they shared many species in com- mon. In contrast, the continents of Africa, Antarctica, Australia, and South America remained isolated by large bodies of water. These connec- tions and isolations led to the evolution of a variety of animals of very different characters. In fact, following the end of the reign of dinosaurs, the Eocene was a time of rapid diversification for all mammals, not just the primates. As a result, the variety of animals known from this time period is much greater than that known from the earlier Paleocene.

Euprimates were part of this wave of diversification and adaptive radia- tion (see Chapter 5). They came on the scene around 56 mya—nearly simulta- neously, it seems—in North America, Europe, and Asia. There are two main branches of euprimates grouped into different superfamilies (Adapoidea and Omomyoidea). These two super- families include primitive primates described as being either more lemur- like (adapoid) or tarsier- or galago- like (omomyoid). Both groups have been well known from cranial, den- tal, and postcranial remains from North America and Europe, as well as now from more fossil finds in Asia and Africa.

Lemur Connections? The Adapoids The adapoids are the best known of the Eocene stem strepsirhines and include more than 35 genera that we know of; their actual biodioversity during the Eocene was surely far greater. These are the most primitive of the eupri- mates, as recognized by their dental anatomy. Their primitive dental for- mula (2.1.4.3; see Chapter 6) provided a generalized ancestral baseline from which many later, more derived vari- eties of dental specializations could evolve. The adapoids are divided into five families, based mostly on biogeo- graphical distinctions. The most prom- inent are the notharctids of North America (predominantly) and the adapids of Europe.

The first of the two major adapoid families, the notharctids, includes the genus Cantius. This was the earli- est notharctid and one of the earliest of any of the adapoids. This small- to medium-sized animal is known pri- marily from North America, with just two species from Europe. Cranial and skeletal remains indicate that it was a diurnal creature, foraging during the day. It also probably traveled very rapidly through the trees, leaping

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cHapTeR 8 Overview of the Fossil Primates 224

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quadrupedally. Traits of its mandi- ble and its primitive dental formula of 2.1.4.3 indicate that it was prob- ably a fruit eater. Another promi- nent notharctid was unveiled in 2009 to great fanfare. This 47-million- year-old creature, Darwinius (nick- named, “Ida”), does not appear to have had a dental comb or a groom- ing claw, which its scientific propo- nents argued was evidence that the adapoids are much more than mere lemur relatives (Fig. 8-6). In fact, these researchers went on to sen- sationally assert that Ida and other adapoids were basal haplorhines, a position not supported by the pre- ponderance of scientific evidence (Franzen et al., 2009). Ironically, just months later, a new adapid from Egypt solidified the adapoid posi- tion as a stem strepsirhine group and helped bolster the hypothesis that apparent similarities to higher pri- mates are indicative of convergent evolution (Seiffert et al., 2009).

This informative fossil, dating to about 37 mya, represents Afradapis, a previously unknown large-bodied adapiform genus. Afradapis belongs to the third major family of adapoids, appropriately called the adapids, which abruptly appeared in Europe near the end of the Eocene and just as quickly became extinct. For this reason, phylo- genetic relations for this group are not well understood, although the adapids probably emigrated from another con- tinent, most likely Asia.

Remember that in Chapter 5 we introduced the terms homology (simi- lar traits based on descent) and homo plasy (similar traits that evolve inde- pendently in different groups) and talked about the example of theropod dinosaurs and birds sharing derived traits. The teeth of Afradapis indi- cate that it may have exploited anthro- poidlike feeding niches in Africa, eat- ing leaves like a monkey (Seiffert et al., 2010). This example of convergent evolution due to shared dietary pat- terns (very common in early primate

evolution) means that adapoids might have been the first primates to exploit anthropoid- like feeding niches in Africa. If true, this could have some important implications with regard to the role that potential ecological competition might have played in the early evolution of stem strepsirhine and haplo- rhine groups, explain- ing some of these early apparent convergences (Seiffert et al., 2009).

Perhaps the best- known fossil of this group is called Adapis. It was not only the first nonhuman fossil pri- mate named but was also first described by the well-known nineteenth-century nat- uralist Georges Cuvier. As you may remember from Chapter 2, Cuvier didn’t believe in evolving lineages, even going so far as to state, in 1812, “ l’homme fossile n’existe pas” (“fossil man does not exist”). By this he also meant fossil primates. So it’s ironic that in 1822, it was Cuvier who described and named the first fossil primate. Unfortunately for him, he confused the remains for that of an ungulate (a hoofed mammal); how- ever, shortly after his death in 1837, the fossil was correctly identified as a primate. Adapis’ dental formula remains primitive (2.1.4.3), and some have argued that an incipient dental comb (a lemur feature) could be rec- ognized in this fossil genus. (You may recall from Chapter 6 that a dental comb is a specialization of the front teeth in the lower jaw; the teeth are elongated and project forward like a small comb.) A slow arboreal quad- ruped, Adapis most likely spent its time foraging for leaves during the daytime hours.

▲�Figure 8-6 Skeleton of Darwinius, nicknamed “Ida.”

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cHapTeR 8 Overview of the Fossil Primates 226

Closer Connections to Living Primates: The Evolution of True Lemurs and Lorises As we’ve mentioned, the adapoids were fairly lemurlike in their overall pattern, and they show distinctive primate ten- dencies. Although the ancient adapoids do resemble lemurs in overall anatomi- cal body plan, this is mostly because modern lemurs retain some ances- tral traits. The adapoid fossils don’t show the same specializations seen in crown members of lemurs, galagos, and lorises, such as development of the den- tal comb. For this reason we may say that modern-day lemurs, galagos, and lorises have retained many “primitive” aspects of anatomy, though there’s no clear evolutionary relationship between the Eocene adapoids and these latter- day creatures (but see Kay et al., 2004; Ross et al., 2004).

It’s important to note that the evo- lution of lemurs and other strepsi-

rhines is of great interest to research- ers because of their basal position as the sister group to all other primate lineages (Horvath and Willard, 2007; Horvath et al., 2008). Accordingly, information related to their initial emergence and dispersal can be used to better calibrate subsequent primate divergence dates.

Lorisoids (lorises and galagos) are the earliest examples of strepsi- rhine primates in the fossil record. These small primitive creatures have been found in late Eocene deposits of the Fayum Depression in Egypt, an area that we’ll discuss in more detail shortly. A late Eocene (circa 34 mya) fossil find from Egypt appears to have had a dental comb (Stevens and Heesy, 2006). This and other features have led to the conclusion that it’s a stem galagid. Together with molecular evi- dence (Seiffert et al., 2003), it can be inferred that lorises and galagos (also known as “bush babies”) likely diverged by the close of the middle Eocene.

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Key Early Primate Names

Genus Name Epoch Sites/Regions The Big Picture

Purgatorius paleocene american Southwest, Bug creek anthills (Montana)

plesiadapiform; first known archaic primate.

Darwinius early eocene Messel, Germany adapoid genus named to commemorate the bicentenary of the birth of charles Darwin; known from one astonishingly complete and well-preserved fossil.

Teilhardina early eocene North america, europe, asia

Omomyoid genus whose lineage demonstrates that all euprimates likely engaged in a rapid westward dispersal from asia to europe and finally, North america.

Archaeolemur Holocene (modern epoch)

Madagascar Subfossil lemur with fused mandible and bilophodont molars; converged upon monkey anatomy in a monkey- less environment.

At a Glance

Eocene Euprimates 227

The existence of an early African bush baby in Egypt during this time indicates that stem strepsirhines ini- tially evolved on the African main- land. These primates likely colonized Madagascar to give rise to crown lem- uriforms, which would mean that lemurs have never existed outside of this tiny island (Seiffert et al., 2005a). The colonization itself most likely occurred when these animals crossed the Mozambique Channel, perhaps by unintentionally rafting over on drift- ing debris (Yoder et al., 1996, 2003; Kappeler, 2000; Ali and Huber, 2010), a phenomenon that most likely had its heyday during the early Cenozoic, before a change to modern ocean cur- rents between Madagascar and the mainland (Samonds et al., 2012). Additionally, other biogeographical mechanisms, such as “island hopping,” have been suggested (McCall, 1997; Arnason et al., 2000), though, as you will see, these may have had a bigger hand in the original monkey coloniza- tion of South America.

There are few if any truly fossil- ized lemur remains in Madagascar; but there are numerous subfossil lemurs. These unfossilized skeletal remains are too recent to have become completely mineralized into fossils. Many of these extinct subfossil lemurs were colossal

compared with the lemurs of today— indeed, some of them were up to five times as big! Despite their large size, they were mostly tree dwelling and likely diurnal. Most interesting of all, many filled unusual ecological niches not shared by any living lemurs. Many of these peculiar adaptations provide examples of convergence with higher primate niches found elsewhere in the Old World. For instance, the extinct Archaeolemur (Fig. 8-7), with its fused mandible and bilophodont molars, in many ways more closely resembled a monkey than the 37-pound lemur that it was (Fleagle, 1999). What’s more, the sulcal (grooved) pattern of Archaeolemur’s brain was similar to that seen in higher primates (Martin, 1990). Based on this evidence, we can see this group as converging on a mon- keylike role on a monkeyless island.

The best known of the giant lemurs, however, is the 170-pound Megaladapis, it was built like a koala on steroids. It’s koalalike similarities are due to a convergence of dietary pat- terns, since these slow-climbing over- sized lemurs cropped leaves with their front incisors much like modern koa- las (Tattersall, 1982). Unfortunately this specialized forest dweller became extinct with the appearance of humans on the island, when the trees

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▲�Figure 8-7 Comparison of the skull of Archaeolemur (left) and a macaque monkey. Note how the lemur resembles the monkey in the shape of the jaw, teeth, and overall cranial form. This is an excellent example of conver- gent evolution.

subfossil Bone not old enough to have become completely mineralized as a fossil.

bilophodont Referring to molars that have four cusps oriented in two parallel rows, resembling ridges, or “lophs.” This trait is characteristic of Old World monkeys.

cHapTeR 8 Overview of the Fossil Primates 228

ing point. In fact, analysis of related species of Teilhardina has shown that the oldest and most primitive mem- bers were from Asia while the youngest were from North America. This evi- dence would tend to support a west- ward migration of euprimates from Asia, through Europe, and eventually to North America (Smith et al., 2006) (Fig. 8-9). A more recently discovered species of Teilhardina from the state of Mississippi, however, has challenged this view. Biostratigraphic or faunal correlation (see Chapter 9) of fossils of this coastal dweller appears to indi- cate that it predates those in Europe, though by how much is not certain. Still, this would mean that the genus actually moved east to west from Asia to North America before finally mov- ing into western Europe, most likely by traveling over land bridges as sea levels fell (Beard, 2008). It is impor- tant to recognize, however, that stan- dard carbon isotope evidence has been notably omitted from the pub- lished study (Gingerich et al., 2008). Without this evidence, it’s difficult to accept the early date of the Mississippi Teilhardina at face value.

Other Eocene fossils of the family Omomyidae from North America (Shoshonius) and Europe (Necrolemur) are also thought to be closely related to the tarsier. Like modern tarsiers, these animals apparently possessed large convergent eye orbits as well as details of the ear region that unite them to the tarsier group. In addition, there is some evidence that Necrolemur may have had a fused tibia and fibula as well as an elongated calcaneus, a lever- like construction (much like that seen in a jackrabbit) that gives modern tarsiers their fantastic leaping abili- ties. However, many researchers con- clude that these similarities are super- ficial ones, not necessarily indicating any unique (that is, shared derived) relationship. Even so, at least one fea- ture, the position of the olfactory por- tion of the brain that processes scent, links these Eocene forms with later tarsiers though not with anthropoids (Fleagle, 1999).

were cleared for farmland. Sadly, the Megaladapis story isn’t unusual; most of the 16 subfossil species discovered went extinct within the last 2,000 years—at the same time that humans began colonizing the island. Because these large-bodied lemurs (over 22 pounds) had low reproductive rates, the predation and deforestation carried out by these early peoples rapidly caused the extinction of these massive animals (Catlett et al., 2010). Unfortunately the remaining lemurs of Madagascar will meet the same fate unless the con- tinued destruction of their habitat by humans ceases.

Tarsier Connections? The Omomyoids The tarsier-like omomyoids, the earli- est haplorhine group, are more taxo- nomically diverse than the adapoids. They’re often called tarsierlike because the European specimens of this group more closely resemble the tarsier, though no specific phylogenetic con- nection has been made. They have a similar dental formula to living tar- siers (1.1.3.3) as well as large orbits and small snouts. Earlier members of this group are somewhat more gen- eralized than later ones, and some researchers hypothesize that they rep- resent the stock for all later haplo- rhines—that is, tarsiers, New World monkeys, Old World monkeys, apes, and humans (Ross, 2000). Paleopri- matologists have traced this success- ful radiation from primarily the Eocene and early Oligocene of North America and Europe, with a small number also known from Asia.

Members of the genus Teilhardina (Fig. 8-8) are found on three conti- nents (although a new analysis dis- putes whether all the attributed mate- rial belongs in the same genus; see Tornow, 2008). The fossil record appears to show that the earliest eupri- mates (including all adapoids and omomyoids) engaged in a rapid west- ward dispersal, with evidence point- ing to Asia as the euprimates’ start-

paleoprimatologists anthropologists specializing in the study of the nonhuman primate fossil record.

biostratigraphic/faunal correlation a method of dating strata that relates the fossil content of an unknown stratum to a like one that has been securely chronometrically dated.

Eocene Euprimates 229

Evolution of True Tarsiers For many years, “the ‘living fossil’ [had] no fossil record!” (Schwartz, 1984, p. 47). However, the situation has recently improved. Fragmen- tary remains of fossil tarsiers (a sin- gle jaw and isolated teeth) are now known from Egypt, China, Myanmar and Thailand. In 2006, the first cra- nial remains of an early tarsier were described. Amazingly enough, these remains are “virtually identical to the corresponding anatomy in living tarsi- ers” (Rossie et al., 2006, p. 4381). Since that time another fossil tarsier has been described, this one from the mid- dle Miocene of Thailand. This new- est discovery is of a bug-eyed tarsier so extreme in its orbital size that it falls outside the range of variation for extant members of the genus (Chaima- nee et al., 2011). From these fossils it’s been generally concluded that modern tarsiers have retained essentially the same body plan that they had in the Eocene, though their current restric- tion to the islands of Southeast Asia is a relatively new condition. Molec- ular evidence has shown that the five extant (currently existing) spe- cies of tarsiers diverged in the Mio- cene (Wright et al., 2003); and as you learned in Chapter 6, all living tarsi- ers are now limited to a few islands in Southeast Asia.

Toward the end of the Eocene, there was a shift from tropical to drier and

more seasonal climates. This change led to more diverse land- scapes, opening many niches for the highly adaptable primates to exploit. This backdrop sets the stage for our next saga in primate origins—that of our own infraorder, Anthropoidea. Of course tarsiers and strepsi- rhine primates have continued to evolve since the Eocene, but we’ll now focus on those pri- mates most directly related to our own evolution as humans. For a comparison of strepsi- rhines and anthropoids, see Figure 8-10.

Eocene and Oligocene Early Anthropoids It’s important to realize that when we’re trying to interpret the past, things aren’t as straightfor- ward as they may at first seem. In addi- tion to the debate about the earliest emergence of strepsirhines and tarsi- ers (and therefore the most “primitive” members of Primates), we’re equally unsure about the origins of anthropoid primates—the ones that eventually led to apes and monkeys as well as to our own lineage.

In recent years, new discoveries have led scientists to dispute an adapoid or even omomyoid origin of anthropoids, with some advocating that crown

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▲�Figure 8-8 Teilhardina. (a) View of the skull of Teilhardina from the top. (b) An artist’s reconstruction of Teilhardina, with areas in gray repre- senting missing fragments.

◀�Figure 8-9 The rapid westward dispersal of euprimates of the genus Teilhardina. Analysis of related species of Teilhardina shows that the oldest and most primitive members were from Asia, while the youngest were from North America.

cHapTeR 8 Overview of the Fossil Primates 230

▲�Figure 8-10 Anatomical comparisons of strepsirhine and anthro- poid primates. (Adapted in part from Fleagle, 1999, p. 134.)

Lemuriforms Anthropoids

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Oligocene Primates 231

haplorhines (tarsiers and anthropoids) are a sister group to omomyoids as a whole (Bajpai et al., 2008; Williams et al., 2010).

The Fayum Depression in Egypt (see “Primate Diversity in the Fayum,” below), an arid region today, provides most of our early anthropoid record for the Eocene and Oligocene. Over the last five decades, paleoprimatolo- gist Elwyn Simons and colleagues have excavated this rich area and found a remarkable array of fossil primates. One of these discoveries, Biretia, is precisely dated to 37 mya and repre- sents the most complete remains of an early African anthropoid. This small primate, weighing just under a pound, exhibits dental morphology typical of that expected for a basal (most primi- tive) anthropoid. Surprisingly though, the structure of the upper molar tooth roots points to large orbits, implying that Biretia was nocturnal (Seiffert et al., 2005b). This is interesting because, as discussed in Chapter 6, the general trend for Anthropoidea is toward a diurnal activity pattern. Simons has placed these fossils, based on their dental characters, into the extinct superfamily Parapithecoidea. This superfamily is significant as the most primitive anthropoid group and there- fore the possible root stock from which

the entire New World anthropoid evo- lutionary group (that is, clade) evolved.

The later Oligocene evolution of these very early anthropoids (Seiffert et al., 2005b) is discussed in the next section. Somewhat more recent (dating to around 35 mya) are the Fayum primate genera from the family Oligopithecidae, including Catopithecus (Fig. 8-11), which clearly possessed anthropoid features (such as complete postorbital closure) and some derived catarrhine features (such as a 2.1.2.3 dental formula). These Fayum discoveries help fill the gap between later (more derived) anthropoids and the middle Eocene primates of Algeria. Most scientists, though there are exceptions (notably, Chaimanee et al., 2012), agree that the earliest fossil anthropoids appear to have been from Africa. Current molecular and bio- geographical data apparently confirm that anthropoids had an African ori- gin, much like the African origin of our own genus, Homo (Miller et al., 2005).

Oligocene Primates

The vast majority of Old World primate fossils of the Oligocene epoch (33 to 23 mya) come from just one region, the Fayum Depression in

catarrhine Member of catarrhini, a parvorder of primates, one of the three major divisions of the suborder Haplorhini. It contains the Old World monkeys, apes, and humans.

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◀�Figure 8-11 Three specimens of Catopithecus, the earliest anthropoid genus to preserve a skull. These ele- ments give us our first view of early catarrhine cranial anatomy, including fully enclosed orbits.

232

Primate Diversity in the Fayum

Today el-Fayuom, or the Fayum, is an egyptian province about 40 miles southwest of cairo. In the eocene and Oligocene epochs, it was a swampy forest playground for primates. Now all that’s left of that primate eden is chunks of petrified wood, flotsam adrift in the vast desert of the Sahara. The name Fayum probably comes from the ancient egyptian word Baym, meaning “lake or sea” and refer- ring to the area’s proximity to a large lake near the Nile. Nowadays, though, the last thing anyone would associate with this arid region is a body of water.

In 1906, the first primate ever discov- ered in egypt was unearthed and later identified as Apidium. Many considered this discovery, hailed as a “dawn ape,” to be the earliest relative of apes and monkeys. Though several primate fossils were discovered in the early 1900s, it wasn’t until 1961 that the dogged persistence of elwyn Simons led to the unearthing of the Fayum’s true fossil primate abundance. Fifty years later, Simons still coaxes dry bones from the sand of the Fayum. Through the efforts of Simons and colleagues (Fig. 1), the Fayum primates are the best-studied fossils in the region and far and away the most abundant late eocene and Oligocene finds from anywhere in the world, and they shape many of our views regarding the diversification of strepsirhines, tarsi- ers, monkeys, and apes. These fossils are often referred to as the “lower-sequence primates” and “upper-sequence primates,” according to their placement in the strati- graphic section. From these eocene (low- er) and Oligocene (upper) sediments, over 17 genera are known, presenting us with a wide variety of dietary niches. What’s most surprising, however, is that both the strepsirhines and some anthropoids

exploited a frugivorous (fruit-eating) lifestyle, challenging the idea that ecological changes might account for the emergence of the latter group (Kirk and Simons, 2001). So for the time being, anthropoid origins remain as enig- matic as the Sphinx.

A Closer Look

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Figure 1 Elwyn Simons and col- leagues toil in the harsh heat of the Fayum in Egypt while collect- ing fossils of the earliest anthro- poids. These fossils are so small that workers must excavate with their faces close to the ground.

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Oligocene Primates 233

Egypt—the same area that has yield- ed abundant late Eocene remains. All together, well over 1,000 specimens have been retrieved from the Fayum, representing a remarkable paleonto- logical record of what was once an extremely rich primate ecosystem.

True Anthropoids The early primates of the Oligocene are generally placed into three families: the oligopithecids, parapithecids, and pro- pliopithecids. Members of the oligo- pithecid family are among the earliest catarrhine (Old World) anthropoid pri- mates, with some also known from the late Eocene of the Fayum in Egypt. One of these early taxa, Catopithecus (men- tioned earlier), is represented by several crushed crania. Analyses of these frag- mentary remains, with their complete postorbital closure and derived 2.1.2.3 dental formula, have led paleoprimatol- ogists to conclude that Catopithecus is the earliest catarrhine.

The most abundant of the Oligocene fossils from the Fayum are from the parapithecid family, and they belong to the genus Apidium. About the size of a squirrel, Apidium had several anthropoidlike features, but it also possessed some unusual dental fea- tures. Apidium fossils exhibit a den- tal formula of 2.1.3.3, indicating that Apidium probably appeared before the Old and New World anthropoids diverged. As noted, this makes the early relatives of Apidium possible can- didates as ancestors of New World anthropoids (that is, platyrrhines; Fig. 8-12). The teeth also suggest a diet composed of fruits and probably some seeds. Another interesting fea- ture suggests something about this animal’s social behavior: an unusually large degree of sexual dimorphism in canine size may indicate that Apidium lived in polygynous social groups of a single male and multiple females and offspring. Limb remains show that this creature was a small arboreal quad- ruped, adept at leaping and springing. We now know much more about the

cranial anatomy of the parapithecids thanks to the discovery of a complete skull of the genus Parapithecus (Fig. 8-13), a close relative of Apidium.

Members of the third major fam- ily are called the propliopithecids. They include possibly the most sig- nificant fossil genus from the Fayum, Aegyptopithecus (Fig. 8-14). This genus has been proposed as the ances- tor of both later Old World monkeys and hominoids. Aegyptopithecus is known from several well-preserved crania, numerous jaw fragments, and a fair number of limb bones. The largest of the Fayum anthropoids, Aegyptopithecus was roughly the size of a modern howler monkey at 13 to 18 pounds, with considerable sexual dimorphism. With a dental formula of 2.1.2.3, Aegyptopithecus shares the derived catarrhine dental formula. The skull is small and resembles a modern monkey skull in certain details, while the brain size appears to have been at best strepsirhinelike; some even consider it so primitive as to be non- primatelike. In fact, a reappraisal of intracranial size has determined that given the small brain size of this genus, greater encephalization must have evolved independently within the two anthropoid parvorders, Platyrrhini and Catarrhini (Simons et al., 2007).

platyrrhines Members of platyrrhini, a parvorder of primates, one of the three major divisions of the suborder Haplorhini. These include only the New World monkeys.

parvorder a taxonomic group below infraorder.

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Platyrrhines

▲�Figure 8-12 Diagram of the phyletic relationships (cladogram) of Fayum early anthropoids and liv- ing catarrhines (monkeys, apes, and humans). (Adapted from Fig. 13-18 in Fleagle, 1999, p. 418.)

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▲�Figure 8-13 Parapithecus belongs to the group of Fayum anthropoids most closely related to the ancestry of New World monkeys.

cHapTeR 8 Overview of the Fossil Primates 234

Postcranial evidence reveals that Aegyptopithecus was likely a

short-limbed, heavily mus- cled, slow- moving arboreal

quadruped. Aegyptopithecus was

long viewed as the best candidate from the Fayum to have given rise to Old World monkeys, apes, and humans. Aside from

isolated teeth, there was little other fossil mate-

rial discovered subse- quent to Aegyptopithecus.

However, a recent discovery from the Afro-Arabian region, this

time from Saudi Arabia, might shed important light on the timing of the cercopithecoid-hominoid split (but see Pozzi et al., 2011). This new anthro- poid find, assigned to the new genus Saadanius, defies current attribution to any existing catarrhine family or superfamily (Fig. 8-15). What’s more, its date of 29 to 28 mya is within a criti- cal period in the evolution of our lin- eage. This time period is so crucial because it bridges evidence of the earli- est stem catarrhines (related to extant catarrhines but not actually from with- in the lineage) that we’ve just summa- rized with the Miocene fossils we’ll discuss later that definitively indicate that the major split between Old World monkeys and hominoids had already occurred. Until the discovery of this surprising fossil, scientists faced a puz-

zling gap of many millions of years, with very few fossils available

between 30 and 23 mya to pro- vide insight. Saadanius dates to within this gap, and lacking derived features of either cerco- pithecoids or hominoids, sug-

gests that the split between these lines had not yet occurred. Saadanius’ most significant features in this respect include a projecting midface, a tube- like middle ear, and large broad molars. The tubelike middle ear is especially important, as it is a characteristic that it shares with crown catarrhines (mon- keys, apes, and humans) to the exclu-

sion of the propliopithecids. This would make Saadanius an advanced stem cat- arrhine, though perhaps intermediate between Aegyptopithecus and Miocene apes (Zalmout et al., 2010).

Early Platyrrhines: New World Anthropoids The earliest primates yet found in the New World date to around 27 mya, about 10 million years after fossil evi- dence for the first anthropoids appears in the Fayum of Egypt. However, they probably evolved from ancestors simi- lar to those seen within the parapithe- cids of the Fayum primate radiation. The earliest platyrrhine (New World anthropoid) fossils are found in the late Oligocene of Bolivia and have been placed in the genus Branisella. Mem- bers of this genus appear to have been small monkeys (about 2 pounds), with diets composed primarily of fruits. The evolutionary relationships of these first fossil platyrrhines are still greatly debated. Branisella is thought to be so primitive that it’s not placed in any liv- ing platyrrhine lineage; it perhaps rep- resents a remnant of the first platyr- rhine radiation. Molecular evidence supports this view, as living platyr- rhines converge on a shared ancestor that is only 25 million years old (Perel- man et al., 2011). Branisella represents a side branch from the clade of living New World monkeys that includes the last common ancestor of extant plat- yrrhines (Fig. 8-16). But this doesn’t mean that it has nothing to tell us about modern platyrrhines. As a rem- nant of the stem New World radiation, this fossil opens a window through which we can begin to view the first primate colonizers of South America.

Based on the presence of the first platyrrhines in South America at 27 mya, it’s likely that the very first anthropoids arrived in the New World somewhat earlier, probably during the late Eocene (45 to 35 mya). In fact, recent molecular data indi- cate that the platyrrhine-catarrhine (New World–Old World anthro- poid) lineages diverged approximately

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Oligocene Primates 235

between 50 and 35 mya, with a conser- vative estimate of 43 mya (Steiper and Young, 2006). This estimate is further bolstered by fossil and molecular evi- dence concerning the arrival and diver- sification of caviomorph rodents (for example, guinea pigs, chinchillas, New World porcupines, and their relatives). “Cavies” also originate from African stock and were the only other group of terrestrial mammals to colonize South America at the same time as platyr- rhines (Poux et al., 2006). The early transatlantic migration of both groups would have involved the crossing of some sort of oceanic barrier, since South America was an island continent until 5 to 3 mya. We know that these two groups overcame this boundary, but how platyrrhines arrived in the New World in general and in South America in particular remains one of the most fascinating questions in pri- mate evolution (Fig. 8-17 on p. 237).

Several competing theories have been proposed in an attempt to explain the mysterious arrival of platyrrhines in South America: North American migration, Antarctic migration, and South Atlantic “island hopping.”

The scenario for a North American migration route argues that one of the North American tarsierlike omo- myoids journeyed down to South America, giving rise to the later plat- yrrhines. An alternative scenario con- tends that migration could have been accomplished by passing through the Antarctic—first crossing by water from Africa south to Antarctica and then crossing a land bridge that linked Antarctica to South America. The most likely scenario for the arrival of platyrrhines in South America, how- ever, involves their floating between closely spaced islands across the Atlantic Ocean from Africa to South America on rafts made of naturally

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Basal Platyrrhine Radiation

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▲�Figure 8-16 Cladogram of extant groups of New World monkeys based on molecular evidence, with dates of divergence noted in the gold nodes (Perelman et al., 2011). Branisella has been plotted relative to its position with respect to living groups and is representative of the basal adaptive radiation of the stem group of New World monkeys, unrelated to the crown group species living today.

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island hopping Traveling from one island to the next.

236

Island Hopping and Primate Evolution

Despite the peculiar images this state-ment might conjure, island hopping and the associated phenomenon of rafting are actually well-recognized methods of animal migration for some vertebrates. In fact, there’s documented evidence of a natural raft carrying a crocodile 685 miles from Java to the cocos Islands in 1930 (ciochon and chiarelli, 1980a). admittedly such instances of natural rafting are rare; but given the geological span of time, even unlikely events (such as you winning the lot- tery or monkeys floating to South america) become likely. This idea is known as the sweepstakes model, and it was popularized by evolutionist G. G. Simpson (contribu- tor to the Modern Synthesis, discussed in chapter 4).

as better information regarding the rare availability of land bridges has been absorbed, scientists are relying more and more on sweepstakes models such as rafting to explain events that are otherwise impossible to explain. Such is the case for the lemur population of Madagascar and the New World monkeys. In both circum- stances, we have the relatively sudden appearance of primates in areas where no ancestor is present and for which migra- tion could only have been predominantly over a large body of water. The existence of islands that are now submerged as inter- mediates accompanied by short instances of natural rafting could have accommodated such an otherwise unlikely route of travel. coincidentally, africa is the apparent source of both the lemur and platyrrhine root stock.

The scenario goes like this: a female primate and her mate live on the edge of a river. During one particularly nasty storm, their home is disconnected from the mainland, becoming a natural houseboat of sorts. The storm rages, and the entire raft is carried out to sea. Days later, the bedraggled primates wash ashore at their new home (Fig. 1). The rest is history. Or is it?

Recently scientists reevaluated this sweepstakes model, exposing some seri- ous flaws. To be a lucky ticket holder, the primates would have to actually survive the voyage or the whole model is useless. In 1976, Simons calculated that it would take only 4 to 6 days for most small primates to succumb to the combined effects of lacking food and water and experiencing salt imbal- ance and exposure (Simons, 1976). The shortest distance today from the african mainland to Madagascar is 249 miles. even with a stiff continuous wind, it would take 10 days to make the journey, so the migrant lemurs would be comatose days before. The first platyrrhines would have had to cross 870 miles—that’s an intolerably lengthy journey for a thirsty primate.

Despite these shortcomings, rafting is still viewed by many as the best explanation that we have for these dispersals—short of some even more obscure method of trans- portation. additionally, rafting is presumed to have been the method of the primate colonization of Madagascar (Samonds et al., 2012). combined with the prob- able existence of islands intermediate to Madagascar and the New World during the times of these voyages, it’s quite possible that the primates were first washed up on one of these isles and only later rafted to their current residences. This would mean that they would not have to cross the entire span in one daunting voyage but would instead engage in island hopping. In addi- tion, alain Houle (1998) has researched the idea of “floating islands” as a mode of distant dispersal of small- to medium-sized vertebrates. These vegetation rafts could have supported microhabitats that would have permitted small vertebrates, such as primates, to cross ocean barriers and reach far distant islands. additional random dis- persals on vegetation rafts from these dis- tant islands would ultimately have allowed primates to colonize the New World.

A Closer Look

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▶�Figure 1 An artist’s rendering of the South Atlantic populating scenario called island hopping, which would allow primates to take their time in moving from one island to another before finally reaching South America.

Miocene Primates 237

formed mats of vegetation (see “Island Hopping and Primate Evolution,” left). The rafting scenario is support- ed by the fact that during the Eocene, South America and Africa were clos- er to each other than they are today. An additional drop in sea level would have further decreased the distance between Africa and South America and may have exposed mid-Atlantic islands, allowing early platyrrhines to “raft” their way to South America (Ciochon and Chiarelli, 1980b; Houle, 1999; Poux and Douzery, 2004). Paleo- oceanographic modeling has indi- cated that paleocurrent directions at this time may have favored this meth- od of dispersal (Ali and Huber, 2010). Though it sounds fanciful, this meth- od of accidental colonization has actu- ally been used very recently to explain early hominin colonization of islands in Southeast Asia without the use of swimming or seafaring technology (Ruxton and Wilkinson, 2012).

Miocene Primates

Throughout the Miocene we see diversification of the anthro- poids into the groups we’re familiar with today. The cercopithecoid mon- keys and the hominoids competed for the dominant position on the primate landscape in the Old World, with the former finally emerging victorious. Today the number of ape groups is very limited compared with the diversity they enjoyed in the Miocene, while cer- copithecoids remain relatively varied.

Monkeying Around Following the emergence of Afro- Arabian stem catarrhines like Aegyp topithecus and Saadanius, we have evidence of further diversification of later catarrhines—namely, the Old World monkeys and the homi- noids. The cercopithecoids, as the Old World monkeys are known, fall into two families—one extinct (called the victoriapithecids) and the other the liv- ing cercopithecids. The late Miocene

was a highly successful time for the radiation of monkeys in the Old World. Their more immediate descendants, which evolved during the Pliocene and the Pleistocene, were much more varied in size, locomo- tion, and diet than their coun- terparts today. For a compari- son of New World monkeys and Old World monkeys, see Figure 8-19 on page 238.

The extinct family Victoriapi the cidae repre- sents the earliest members of the lineage leading to present- day Old World monkeys. The victoriapithecids were found throughout northern and east- ern Africa as early as 24 mya (Gutiérrez, 2011), predating the split between the two extant subfami- lies of Old World monkeys—the colo- bines (leaf-eating monkeys) and the cercopithecines (cheek-pouch mon- keys)—which occurred around 18 mya (Perelman et al., 2011). If accurate, this would conform well to a molecu- lar clock date of about 30 mya for the cercopithecoid-hominoid split. Since they’re more “primitive” in many fea- tures than either colobines or cerco- pithecines, the victoriapithecids may represent a basal cercopithecoid and therefore the last common ancestors of crown Old World monkeys, but it’s also possible that they represent an extinct sister group (Jablonksi and Frost, 2010; Gutierrez, 2011). The best known of the victoriapithe- cids is Victoriapithecus (Fig. 8-18), a small mon- key whose cranium exhibits a mosaic of later colobine and cercopith- ecine features that place it close to the root of both subfamilies. The molars of Victoriapithecus, like those of all living Old World mon- keys, exhibit bilophodonty, indi- cating a diet of hard fruits and seeds. Meanwhile postcranial skeletal fea- tures demonstrate similarities to

▲�Figure 8-17 Here are the conti- nental relationships during the late Eocene. Several competing theories have been proposed in an attempt to explain the arrival of platyrrhines in South America: North American migration, Antarctic migration, and South Atlantic migration (by way of island hopping). The broken white line and surrounding shades of blue in the ocean represent seafloor spread- ing, which caused the continents to drift apart.

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cHapTeR 8 Overview of the Fossil Primates 238

▲�Figure 8-19 Anatomical comparison of New World monkeys and Old World monkeys. (Adapted in part from Fleagle, 1999, p. 137.)

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Miocene Primates 239

living terrestrial monkeys (Benefit and McCrossin, 1997; Miller et al., 2009).

By 12 mya, the victoriapithecids had been replaced by monkeys whose direct descendants are still alive today—that is, cercopithecines and colobines (see Chapter 6). Fossils of the first true colobine are found in African deposits dating to approximately 9 mya. These monkeys were smaller than most liv- ing forms, though—at 8 to 9 pounds— they weren’t lightweights. Following their first appearance in Africa, the colobines quickly radiated into Europe and Asia. As you’ll see, this was when Eurasian ape groups also began reentering Africa.

You may not know it, but you’re probably already familiar with mem- bers of Cercopithecinae, a subfamily of the family Cercopithecidae. This subfamily includes monkeys such as today’s macaques (for example, the rhesus monkeys used in labs) and baboons. Most fossil macaques appear remarkably similar to each other and to living forms, indicating that ances- tral macaque morphology has been retained for more than 5 million years. This is bolstered by molecular evi- dence indicating that Macaca diverged

from Papio (the modern baboon) about 8 mya (Perelman et al., 2011).

In East Africa, the baboon-like Theropithecus was the dominant cercopithecine genus of the Plio- Pleistocene (Fig. 8-20). Adaptations of the hands and teeth indicate that all species of Theropithecus exploited a dietary niche consisting almost exclu- sively of grasses—a unique diet among primates that feed on small objects. This group contains some notable fos- sil specimens, among them the larg- est monkey, weighing 225 pounds, that ever lived. Theropithecus was an incredibly successful genus through- out much of the Pliocene and Early Pleistocene; but at some time dur- ing the Middle Pleistocene, most of its members went extinct, leaving a single remaining species—the gela- da (Theropithecus gelada). While we don’t completely understand exactly what caused these extinctions, many researchers hypothesize that compe- tition with the closely related Papio baboons of today was a major factor. Today, the living gelada is confined to the high wet grasslands of the Amhara Plateau, in Ethiopia, an ecological zone where no Papio baboons are found.

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Key Early Anthropoid Names

Genus Name Epoch Sites/Regions The Big Picture

Biretia Late eocene The Fayum (egypt); North africa

The most complete remains of an early african anthropoid; may have been nocturnal.

Saadanius Oligocene Saudi arabia; afro-arabia

First stem catarrhine; has ear tube.

Branisella Late Oligocene Bolivia; South america First known fossil platyrrhine; remnant of the first New World monkey adaptive radiation but unrelated to extant forms.

Victoriapithecus Middle Miocene Kenya and Uganda; east africa

Has bilophodont molar pattern; ancestor of all Old World monkeys.

At a Glance

cHapTeR 8 Overview of the Fossil Primates 240

Aping Monkeys By the end of the Oligocene, the world’s major continents were located about where they are today. During the Miocene (23 to 5.3 mya), however, the drifting of South America and Austra- lia away from Antarctica significantly altered ocean currents. At the same time, the South Asian Plate continued to ram into Asia, producing the Hima- layan Plateau. Together, these major paleogeographical modifications sig- nificantly affected the climate, causing the early Miocene to be considerably warmer and wetter than the Oligo- cene. As a result, subtropical dense woodlands became the dominant envi- ronments of Africa during the early Miocene. It was in this forested envi- ronment of Africa that the first apelike primates evolved.

The Apelike Proconsuloids Molecular evidence suggests that the evolution-

ary lineages leading to monkeys and apes diverged approximately 32 mya (Perelman et al., 2011) (Fig. 8-21), which is consistent with the fossil evi- dence following the recent discovery of Saadanius, the Oligocene advanced stem catarrhine (Zalmout et al., 2010). Not surprisingly, the first apelike fos- sils share many postcranial character- istics with monkeys. In fact, in many of these early forms of the superfamily Proconsuloidea, the only apelike fea- ture is the presence of the Y-5 molar pattern. As shown in Figure 8-22, the ape molars have five cusps separated by a “Y” groove, as opposed to the mon- key’s typical four bilophodont cusps. Consequently proconsuloids were once commonly called dental apes, reflect- ing their apelike teeth but monkeylike postcranial skeleton. Today, procon- suloids are widely viewed as gener- al precursors to all later hominoids (Harrison, 2010; but see Zalmout et al., 2010).

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▲�Figure 8-20 Skull of Theropithe cus brumpti, the most bizarre fossil monkey (inset). An artist’s rendering of Theropithecus on the landscape in the Omo Basin of Ethiopia about 3 mya.

▶�Figure 8-21 (opposite page) Family tree of early catarrhines and their relationships to modern Old World monkeys and apes. Red is for living apes and their immediate ances- tors (Hominoidea), green is for the Old World monkeys and their immedi- ate ancestors (Cercopithecoidea), orange is for precursors to apes (Proconsuloidea), purple is for the primitive catarrhines (Pliopithecoidea), and blue represents the Fayum early anthropoid radiation.

Y-5 molar Molar that has five cusps with grooves running between them, form- ing a Y shape. This is characteristic of hominoids.

Miocene Primates 241

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cHapTeR 8 Overview of the Fossil Primates 242

Nearly all of the proconsuloid fossils come from East Africa, although some fossils have been recovered as far south and west as Namibia, on the southern coast of Africa. The fossil record shows that these early apelike creatures were a highly diverse group, vary- ing greatly in both size and loco- motor patterns (Gebo et al., 1997; Fleagle, 1999). The best known of the proconsuloids is the genus Proconsul, which lived in Africa 20 to 17 mya. The first example of Proconsul, a skull, was discov- ered on Rusinga Island, Kenya, in 1948 by esteemed fossil hunter Mary Leakey. This fruit-eating apelike creature roamed a wide range of environments from rain-

forest to open woodlands. Though gen- erally considered small-bodied, various Proconsul species actually ranged in size from 10 to 150 pounds (Harrison, 2002). Proconsul exhibits a general- ized cranium (Fig. 8-23) and an ape- like Y-5 dental pattern, but postcranial remains show that Proconsul’s limbs and long torso retained adaptations for

quadrupedal locomotion similar to that of monkeys. Scientists are

increasingly accepting that Proconsul may not have had

a tail, which could indi- cate that this particu- lar hominoid charac- teristic had a relatively ancient origin (Begun, 2003; Nakatsukasa et al., 2004; Ward, 2005). However, the procon-

suloids’ uncertain posi- tion has caused many

researchers to place them outside of Hominoidea (in

Proconsuloidea), just prior to the divergence of hominoids and

cercopithecoids (Harrison, 2010; but see McCollum et al., 2010, and Zalmout et al., 2010). For a comparison of Old World Monkey and Apes, see Figure 8-25.

Afropithecus, a more derived mem- ber of this superfamily, had a long snout with procumbent incisors that protrud- ed horizontally from its face (Fig. 8-24). Its relatively thickly enameled teeth indicate that Afropithecus enjoyed a diet of hard fruits, while the sexual dimorphism of its molars and premo- lars exceeds that of even of living goril- las (Andrews and Martin, 1987; Leakey et al., 1988; Rose, 1993). The few known limb and hand bones point toward a quadrupedal arboreal lifestyle. Known from both Kenya and Saudi Arabia between 16 and 18 mya, Afropithecus provides compelling evidence of trans- continental migration and may have provided the basal stock in Europe from which the later true ape radiations across that continent and into Asia came. Researchers now conclude that Afropithecus was likely the first apelike primate to leave Africa about 17.5 mya (Begun et al., 2012).

Members of the superfamily Pliopithecoidea, like the proconsuloids, are also generally known from the early Miocene, though they’re more primi- tive in their features than all other cat- arrhines. Most evidence indicates that the pliopithecoids were an early small- bodied (6 to 44 pounds) group of stem catarrhines that branched off prior to the cercopithecoid-hominoid split. A highly successful group once thought

▲�Figure 8-22 Comparison of (a) bilophodont molars, as found in cercopithecoids, and (b) Y-5 molars, as seen in hominoids. (a) Notice that the four cusps are positioned in two parallel rows or lobes. (b) See how the five cusps are arranged so that a Y-shaped valley runs between them.

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▲�Figure 8-23 Skull of Proconsul, the best known of the early Miocene precursors to apes.

▶�Figure 8-24 Skull of Afropithecus, the first apelike primate to leave Africa. ©

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▲�Figure 8-25 Anatomical comparison of Old World monkeys and apes. (Adapted in part from Fleagle, 1999, p. 187.)

Old World Monkeys

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Key Fossil Ape Names

Genus Name Epoch Sites/Regions The Big Picture

Afropithecus Miocene Kenya; africa The first apelike primate to leave africa; may have given rise to the european apes; thick-enameled teeth and Y-5 pattern molars.

Griphopithecus Miocene Germany, Slovakia, Turkey; eastern europe/ Western asia

The first true ape; may have given rise to both the later radiations of european and asian apes; no tail.

Ouranopithecus Late Miocene Greece; europe Fossil great ape; believed by many to have returned to africa to give rise to the living great apes and humans.

Lufengpithecus Late Miocene- early pliocene

china; asia part of the asian fossil great ape radiation; stem orangutan.

Gigantopithecus Miocene- pleistocene

china, Vietnam, India, Myanmar; asia

The largest ape that ever lived; only great ape to go extinct in the pleistocene.

At a Glance

to be related to extant hylobatids, they underwent a rapid adaptive radiation in the Miocene (Begun, 2002; Alba et al., 2010).

Toward the end of the early Miocene, around 19 mya, the Arabian Plate moved to its current location, forming a land bridge between Africa and Eurasia. Major animal migrations could then take place between the two previously separated land masses. It’s thought that African pliopithecoids were among the first transcontinen- tal primate migrants and, impor- tantly, represent the first anthropoids to colonize both Asia and Europe. Researchers thus commonly agree that the pliopithecoids were the first stem catarrhines to leave Africa. For many years, however, this migration was only assumed, since pliopithe- coid fossil remains were known only from Eurasia. But in 2006, a new genus of pliopithecoid, Lomorupithecus, was described from Uganda. Dating to the early Miocene (nearly 20 mya), Lomorupithecus could be the earliest member of this group, and—as pre-

dicted—it’s from Africa (Rossie and MacLatchy, 2006)! Though still more recent in age than Saadanius, the pli- opithecoids’ more primitive features indicate that they actually diverged earlier, possibly giving rise to the early primitive catarrhine group to which Saadanius belongs, among others (Begun, 2002; Alba et al., 2010). This find could provide the proof that plio- pithecoids had their roots in Africa, bringing this idea from the realm of conjecture into reality. The pliopithe- coids enjoyed an intense and prolific radiation early on, but it appears that later, during the Pliocene, their success ended. All forms went extinct, with no known living descendants.

True Apes The first true apes, those belonging to the superfamily Hominoidea, appear during the early to middle Miocene, 17 mya, first in Europe, presum- ably coming from an African procon- suloid ancestor (Begun et al., 2012) (Fig. 8-26). These earliest hominoids

Miocene Primates 245

▲ Figure 8-26 Model providing geographical context for the evolution and dispersal of the Miocene apes. (a) Map of present-day Africa, Europe, and Asia showing ape and proto-ape fossil localities. Maps (b–e) are paleogeographic maps showing the loca- tions of inland seas at various time intervals in the Miocene: (b) 17 to 16.5 mya, first dispersal of apelike Afropithecus out of Africa into Europe; (c) 16.5 to 14 mya, Griphopithecus evolves and expands its range throughout Europe and into western Asia; (d) 13.5 to 12 mya, Dryopithecus evolves and disperses in Europe and Sivapithecus evolves and disperses in southern Asia; (e) 10 to 6 mya, Ouranopithecus disperses from southern Europe back into Africa to give rise to the African great apes and humans, in Asia the ances- tors of Pongo disperses into southern China and Southeast Asia. Maps modified after Begun (2003) and Begun et al. (2012).

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are united by their thick enamel on their molars, which appears to have been a trait that was important in their ability to adapt to a variety of new non- African paleoenvironments (Böhme et al., 2011). What this tells us is that hard-object feeding (such as tough, fibrous fruits and nuts) was a key fea- ture of these new environments (Alba et al., 2010).

West Side Story: True Apes in Europe Miocene Europe was a much differ- ent continent from that which we know today. The climate was warm and humid, with a landscape dominat- ed by lush subtropical forests. It was these swampy forests that attracted a diverse group of animals, of which stem hominoids were part. It was at some time during the early-middle part of this epoch that Afropithecus ven- tured out of Africa via land bridges, crossing parts of the modern Middle East to give rise to the first true apes in Europe. Although this initial hominoid (true ape) radiation to which it gave rise

was widespread geographically, so far we’ve found only scant evidence

of it from scattered localities in France, Spain, Italy, Greece,

Austria, Germany, Slovakia, and Hungary.

Dated to roughly 17 mya, the earliest of these true apes, Griphopithecus, is known first from south- ern Germany and later from Slovakia and Turkey. Similar

to what we saw with the ear- lier proconsuloids, the earliest

apelike features are in the den- tition, with the retention of more

monkeylike postcrania. However, very unlike proconsuloids, Griphopithecus and later true apes all lack a tail, one of the distinguishing traits of hominoids (see Chapter 6). Their limb propor- tions were roughly similar and there is no evidence of the more suspen- sory adaptations we see in later apes, but their hands do indicate a greater grip than that of your average mon- key. Additionally, Griphopithecus’ thickly enameled and more general-

ized teeth made it possible for this ape to exploit a variety of different envi- ronments, which was perhaps key in allowing it to migrate from Turkey and into the Asian continent at about 15 mya. In fact, David Begun of the University of Toronto has gone so far as to propose that Griphopithecus repre- sents a Eurasian linchpin in hominoid evolution, providing the stock from which both European and Asian apes later derived (Begun, 2010; Begun et al., 2012).

The best-known European homi- noid of the middle Miocene (circa 12 to 10 mya) is Dryopithecus, from southern France and northern Spain (Fig. 8-27). Unlike Griphopithecus, Dryopithecus resembles modern hominoids in many cranial and postcranial features, includ- ing long arms, large hands, and long fingers—all signifying an ability to bra- chiate. The relatively thinly enameled teeth of Dryopithecus imply an unusual diet of both fruits and leaves (Begun, 1994). Also, these skeletal and dental remains suggest that unlike most other great apes, Dryopithecus was a highly arboreal species, rarely descending from its high-canopy forested habitat.

As the Miocene progressed, the formerly subtropical environment of Europe began to cool and the swampy parts began to dry. These changes led to the extinction of many forest- adapted animals, though others met this more open, grassy environment with increased body size and/or more complex dentition (Begun et al., 2012). One of these “new apes” was the late Miocene (9.6 to 8.7 mya) European fos- sil hominoid Ouranopithecus, whose face shares many features with the living African great apes, including large browridges and a wide distance between the eye orbits (Fig. 8-28). Ouranopithecus’ powerful jaws, with small canines and extremely thick molar enamel, led some researchers to postulate that these hominoids sub- sisted on a diet consisting of relatively hard foods, such as nuts (Ungar and Kay, 1995). The variation in both body and canine size indicates a range of sexual dimorphism comparable to that

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▲�Figure 8-27 Skull of Dryopithecus, one of the earliest European apes. The left side is reconstructed as a mirror image of the complete right side.

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▲�Figure 8-28 Ouranopithecus, possible extinct relative of the African apes. Notice that the face shares many features with living African great apes, including large browridges and a wide distance between the eye orbits. The upper left side is recon- structed as a mirror image of the com- plete right side.

Miocene Primates 247

of the modern gorilla, which these ani- mals resemble in size. Ouranopithecus, is a taxon to watch, as it will come up later in our discussion of the emer- gence of the African apes. For the time being, the most likely position of Ouranopithecus appears to be as a separate sister clade to the extant African apes and to humans (Begun et al., 2012).

East Side Story: Asian Radiation Hominoids do not appear to have colo- nized Asia until about 15 mya (Heiz- mann and Begun, 2001). This initial incursion is first recorded at the site of Paşalar in southwestern Turkey and is marked by the expansion of Gripho pithecus, a European genus, into west- ern Asia (Begun et al., 2012). The hom- inoids of the middle and late Miocene of Asia represent one of the most var- ied Miocene fossil ape assemblages. These Asian fossil apes are geographi- cally dispersed from Turkey in the west to China in the east.

Sivapithecus dates to the middle and late Miocene and has been recovered from southern Asia, in the Siwalik Hills of India and Pakistan. Included in this large collection are a multitude of man- dibles, many postcranial remains, and a partial cranium, including most of the face. Sivapithecus was a large homi- noid, ranging from 70 to 150 pounds; it probably inhabited a mostly arboreal niche. The most characteristic anatom- ical aspects of Sivapithecus are seen in the face, which exhibits a concave pro-

file (dished face), broad zygomatics (cheekbones), and a procumbent (pro- jecting) maxilla and incisors remark- ably resembling the face of the modern orangutan (Pilbeam, 1982) (Fig. 8-29). It’s important to note that the body of Sivapithecus is distinctly unlike that of living orangutans or any other known hominoid for that matter. For example, the forelimb exhibits a unique mix- ture of traits, probably indicating some mode of arboreal quadrupedalism with no ability for brachiation (Pilbeam et al., 1990).

One of Sivapithecus’ descendants from the late Miocene through the Pleistocene, Gigantopithecus (“Giganto”), was discovered in a rather unconventional way. For thou- sands of years, Chinese pharma- cists have used fossils as ingredients in potions intended to cure ailments ranging from backache to sexual impotence. In 1935, Dutch paleoan- thropologist Ralph von Koenigswald came across a large fossil primate molar in a Hong Kong apothecary shop. He named the fossil tooth Gigantopithecus, meaning “gigantic ape,” and the species blacki, in honor of his late friend and colleague Davidson Black (the discoverer of “Peking Man”). Subsequent researchers were able to source the teeth to China’s southernmost Guangxi Province, a karstic (eroded limestone) region of great rock towers riddled with caves.

While four lower jaws and 1,500 iso- lated teeth of the extinct ape have been

Chimpanzee Sivapithecus Orangutan

▲�Figure 8-29 Comparison of a modern chimpanzee (left), Sivapithecus (middle), and a modern orangutan (right). Notice that both Sivapithecus and the orangutan exhibit a dished face, broad cheek- bones, and projecting maxilla and incisors.

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cHapTeR 8 Overview of the Fossil Primates 248

found, no other bones have turned up (Fig. 8-30). Based only on the jaws and teeth, however, researchers can attempt to reconstruct both the ani- mal and its way of life. Estimates based on the massive mandibles indicate that the Chinese species of Giganto likely weighed more than 800 pounds and was possibly 9 feet tall standing erect on its hind legs (though it was most likely a terrestrial fist walker). This makes Gigantopithecus the larg- est primate that ever lived. But Giganto wasn’t always the king of apes that it became in later years. Evidence shows that this great ape increased in size as the genus evolved, which follows a trend seen in other large Pleistocene mammals, such as the mammoth. The earlier Indian and Pakistani Gigantopithecus giganteus (8.5 mya), despite its specific name, was about half the size of the later Chinese and Southeast Asian Gigantopithecus blacki (around 1.8 mya).

The comparatively small incisors and canines, very thick enamel on the cheek teeth, and massive, robust jaws led to the inevitable conclusion that the animal was adapted to the consump- tion of tough, fibrous foods by cutting, crushing, and grinding them. Some researchers have argued that Giganto’s huge mandible and dentition were an adaptation for a diet consisting primar- ily of bamboo, much like that of the

giant panda. More current research has supported this claim and also con- cludes that its diet may have included the durian, a tropical fruit with a tough outer skin (Ciochon et al., 1990) (Fig. 8-31).

Sadly, at some time near the end of the Middle Pleistocene, around 200,000 years ago (ya), Giganto went extinct. The animal had flourished for more than 8.5 million years, but cli- matic or other environmental change may have proved too much for the veg- etarian giant.

A final ape from Asia, Lufengpi thecus, has been recovered from locali- ties in southern China and dated to the late Miocene/early Pliocene (9 to 5 mya). This medium-sized ape, with an estimated adult body weight of about 110 pounds, is known from one of the most complete fossil ape assemblages: 5 crania, 41 mandibles, over 650 iso- lated teeth, and, most recently, post- crania including finger bones and a femur (Xu and Lu, 2007). With its nar- row interorbital distance, ovoid orbits, and procumbent incisors (Fig. 8-32), some researchers have argued that Lufengpithecus is related to the mod- ern orangutan, while others believe that it is related to the European Dryopithecus. If not for its location in southern China, Lufengpithecus would be just another of the many apes that faced extinction at the end of the

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▶�Figure 8-30 Comparison of the mandibles and teeth of Gigantopithecus and Homo sapiens. Notice that Giganto’s jaw is almost three times the size of the human’s, as are the teeth.

Miocene Primates 249

Miocene. However, this, in conjunc- tion with its more recently described curved phalanges, has catapulted this genus to prominence. It now appears that Lufengpithecus is most properly considered a stem orangutan (Harrison et al., 2008; Harrison, 2010).

Lufengpithecus is also noted for its existence within a protected area created by the uplift of the Tibetan Plateau—the result of Himalayan mountain building (Harrison et al., 2002). Within this refuge, a sort of “lost world,” Lufengpithecus survived until at least 5 mya—or at least that’s what scientists used to believe. In recent years, however, Pleistocene cave sites in southern China that have long yield- ed teeth belonging to Gigantopithecus have now also produced more diminu- tive teeth initially identified as belong- ing to an early human. These same teeth, following more rigorous analy- sis, are now thought to be those of a previously unknown, medium-sized Pleistocene “mystery” ape. The teeth are too small to be those of either Giganto or the orangutan Pongo. Could these mystery ape teeth be a descen- dant of Lufengpithecus (Ciochon, 2009)? In fact, the strongest evidence points to the existence of three dis- tinct great ape lineages in Asia: the massive Gigantopithecus, the large-

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▲�Figure 8-31 An artist’s rendering of Gigantopithecus enjoying a meal of the tasty but tough tropical fruit known as durian.

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◀�Figure 8-32 Skull of a Lufengpi thecus juvenile from the late Miocene of Yunnan Province, China. Note the orangutanlike oval eye orbits and nar- row distance between the eyes.

cHapTeR 8 Overview of the Fossil Primates 250

bodied Pongo, and the medium-sized Lufengpithecus descendant. As you’ve seen in Chapter 6, this Asian homi- noid diversity has dwindled in modern times, just as it has in Africa and else- where in the world.

Evolution of Extant Hominoids Hylobatids: The Lesser Apes Molecu- lar evidence indicates that the gib- bon–great ape split occurred 20 mya (Perelman et al. 2011). This would place their divergence around the time that migration into Eurasia from Africa would have first become geo- graphically possible (Pilbeam, 1996; Thinh et al., 2010). The molecular evi- dence also shows that extant hyloba- tids (lesser apes, such as gibbons) only diverged from one another between 9 to 6 mya (Perelman et al., 2011), with 9-million-year-old Yuanmoupithecus supporting that date (Harrison et al., 2008). For many years, researchers had considered pliopithecoids as pos- sible gibbon ancestors owing to simi- larities in the shape of the face. But pliopithecoids and Oligocene catar- rhines actually share numerous primi- tive features, including the lack of a tubelike middle ear, the presence of a small tail, and an elbow joint that’s strikingly similar to those of various Fayum primates. These features, as well as their monkeylike limb propor- tions, clearly remove pliopithecoids from consideration as the ancestors of modern gibbons. From molecular evi- dence and from fossil remains of the small-bodied Chinese stem hyloba- tid Yuanmoupithecus (Harrison et al., 2008), however, we can determine that the gibbon radiation most likely began in mainland Asia, perhaps in China, before dispersing southward to Malay- sia and Sumatra via tropical forests connected by the land bridges of the Miocene. Once in Sumatra, gibbons differentiated into two taxa, including the modern Hylobates, which eventu- ally made their way into Borneo and Java via the same route, though multi- ple migrations via these land bridges is

possible (Chatterjee, 2006; Harrison et al., 2008; Thinh et al., 2010).

The African Great Apes Recent molec- ular studies suggest that gorillas diverged from humans and chimpan- zees about 8 mya, with the divergence between humans and chimpanzees occurring at 6 mya (Perelman et al., 2011). If these estimates are right, then the late Miocene (11 to 5 mya) becomes a crucial period for understanding African great apes and human origins. Strangely, hominoids disappear from the African fossil record about 13 mya, not to appear again until the late Mio- cene about 10 mya. This African “ape gap” (Hill, 2007) has led researchers to hypothesize that the appearance of hominoids in Africa during the late Miocene was the result of Eurasian fos- sil apes migrating into Africa at the same time the colobine monkeys were leaving.

European Ouranopithecus (9.6 to 8.7 mya), a large-bodied hominoid from Greece, is considered the best candi- date for a stem African ape/human ancestor. This argument is based pri- marily on the facial similarities dis- cussed earlier. This out-of-Europe ape line later migrated into Africa at some time during the late Miocene, producing the ape-human line (see Chapter 10).

The 9.9- to 9.8-million-year-old Nakalipithecus from Kenya may be close to the last common ancestor of the African great apes and humans. Nakalipithecus is reconstructed as hav- ing been comparable in size to a female gorilla, with dental features that indi- cate a hard-object diet, both sugges- tive of a terrestrial lifestyle (substan- tial ground living) (Kunimatsu et al., 2007; Nakatsukasa and Kunimatsu, 2009). Size and dental similarities between Nakalipithecus and the slightly younger Ouranopithecus (the two are separated by only 200 to 300 thousand years) may be due to the two having lived in similar environments, an ancestor-descendent relationship, or even, as some scientists argue, that they actually are members of the same

terrestrial Living and locomoting pri- marily on the ground.

Miocene Primates 251

taxon. Despite its still ambiguous phy- logenetic affiliation, it is clear that the Samburu Hills of northern Kenya, where Nakalipithecus was found, were a hotbed of hominoid diversity, with at least two other genera known from this region during the Miocene (Nakatsukasa and Kunimatsu, 2009) (Fig. 8-33).

In 2005, researchers discovered sev- eral teeth of a fossil chimpanzee at a site near Lake Baringo, in Kenya. This discovery adds some fossil time depth to at least the Pan lineage. These fos- sil chimpanzee teeth date to approxi- mately 500,000 ya and represent the first and only fossils belonging to the genus Pan (such fossils are rare because tropical forest environments aren’t conducive to preserving organ- ic remains). Also note that these fos- sils are quite late, several million years after the chimpanzee lineage diverged from hominins. Although currently not assigned to a particular chimpan- zee species, the fossil teeth exhibit greater similarities to the common

chimpanzee (Pan troglodytes) than to bonobos (Pan paniscus) (McBrearty and Jablonski, 2005).

Another reason why African ape and chimpanzee fossils in particu- lar may seem so rare is the difficulty in identifying them as such and not as early hominins. As we will see in Chapter 10, the controversial and now iconic rebranding of Ardipithecus, a previously described genus, reveals a complex and unexpected mix of primitive and derived traits, meaning that the last common ancestor of the African apes and humans may not have looked like either group as we know them now (Lovejoy, 2009; Shreeve, 2009). In fact, a number of research- ers believe that this genus, once open to inspection, will be revealed not as a hominin but rather as a descendant of a late Miocene African ape. However, given the shortage of African hominoid fossils, why can’t that be good enough? Still, if these aren’t our distant relatives, where do we come from? In Chapter 10, we’ll seek answers to this question.

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▲�Figure 8-33 Cladogram of Homininae showing the relation- ships of gorillas, chimpanzees, and humans with their fossil ape relatives. Griphopithecus is the sister group of the Homininae.

cHapTeR 8 Overview of the Fossil Primates 252

Asia’s Lone Great Ape Of all the living apes, the orangutan’s ancestry is prob- ably the best documented. Recall that the European Griphopithecus expand- ed its range into western Asia (Paşalar, Turkey) beginning approximately 15 mya, so it may be viewed as the progen- itor of later Asian apes (Begun et al., 2012). Current evidence indicates that

Sivapithecus gave rise to Gigantopithe cus (some time before 9 mya) as well as to Lufengpithecus and then finally to the orangutans (Pongo), possibly in the Pliocene. Since the earliest Sivapithecus fossils date to more than 12 mya, it’s clear that the branching event separat- ing orangutans and the lineage leading to the African great apes and humans must have occurred before then. In fact, molecular evidence indicates that this divergence took place approxi- mately 17 mya (Perelman et al., 2011). The relationship between Sivapithecus and Pongo is based primarily on cra- nial similarities, though their vastly differing postcranial anatomies raise questions regarding their evolution- ary proximity to each another. As men- tioned earlier, the face of Lufengpithe cus is also very similar to that of the modern orangutan. However, it’s the postcrania of Lufengpithecus (particu- larly its curved phalanges) that indicate its closer relationship to Pongo than to Sivapithecus (Harrison et al., 2008). Several other Asian hominoids have been suggested as more recent orang- utan ancestors, but there’s as yet little evidence to support these assertions (Fig. 8-34).

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We know a great deal about the earliest primates and their ancestors based mostly on fossil finds. Molecular (DNA and mtDNA) data from living pri- mates, when paired with these fossils, allows scien- tists to determine when primate lineages diverged in time. Unfortunately the number of fossils (especially complete ones) that have been discovered from the Paleocene through the Miocene is still relatively small compared with later taxa, but the teeth in particu- lar are very informative regarding dietary habits and

paleoenvironments. By taking careful measurements and differentiating between primitive and derived fea- tures, scientists can cluster these fossils into groups that represent extinct taxa. By comparing and con- trasting these quantitative data with the same data collected for living primates, we can further distin- guish how these extinct taxa relate to one another and to extant forms in terms of locomotor, dietary, and social behaviors as well as where they fit in the pri- mate family tree.

How Do We Know?

▲�Figure 8-34 Cladogram of Ponginae showing the relationship of the orangutan with its fossil ape relatives. Griphopithecus is the sister- group of the Ponginae.

253Critical Thinking Questions

▶ Beginning in the Paleocene, the earliest primate ancestors were probably little more than arbore- ally adapted insectivores, much like modern tree shrews.

▶ In the Eocene, we see an abundant diversification of readily identifiable euprimates, with the lemur- like adapoids and the tarsierlike omomyoids begin- ning their evolutionary radiations.

▶ As demonstrated by recent evidence from the Fayum and other locations in Africa, early anthro- poid origins also date to a time in the middle Eocene.

▶ Old and New World anthropoids apparently shared their last common ancestry in the Eocene or early Oligocene and have gone their separate evolutionary ways ever since. In the Old World, the Oligocene reveals numerous possible early anthropoid ancestors, again mostly at the Fayum, but none of the modern lineages (Old World mon- keys, gibbons, large-bodied apes) can definitely be traced to this time.

▶ The Miocene reveals the first Old World mon- keys and a highly complex array of ape forms;

many large-bodied varieties are represented from remains discovered in Africa, Asia, and Europe. Some early forms from Kenya and Uganda (the proconsuloids) are more primitive than all of the hominoids from Eurasia. It is likely that one of these (Afropithecus) migrated into Europe to give rise to the later true apes.

▶ The first true ape, Griphopithecus, is known from the early-middle Miocene of Europe, which is where apes had their initial origin and adaptive radiation. Later they made their way into Asia and finally back into Africa.

▶ Though there’s little firm evidence tying Miocene fossil forms to living apes or humans, morpho- logical evidence suggests that Yuanmoupithecus may be related to the gibbon, and Lufengpithecus is probably closely related to the orangutan. Ouranopithecus or a related form may have migrated back into Africa, where the more recently discovered Nakalipithecus might be an ancestor of the African apes.

Summary of Main Topics

1. In the dating of fossil lineages, how do molecular and direct estimates differ? How can they be used to give us a more complete view of the past?

2. Why is it difficult to distinguish the earliest mem- bers of the primate order from other placental mammals? If you found a nearly complete skel- eton of an early Paleocene mammal, what struc- tural traits might lead you to determine that it was a euprimate?

3. Compare and contrast the adapoids and omomy- oids with living members of the primate order.

Why do we call them lemur- or tarsierlike and not lemurs and tarsiers?

4. Where is the Fayum, and why is it significant in primate evolution? Are there any other sites where so many fossil primates have been found? Why or why not?

5. Where do the first true apes arise and from where do they migrate? How are the earliest forms differ- ent from extant groups and to whom are they most closely related?

Critical Thinking Questions

Paleoanthropology, which includes physical anthropology,

archaeology, and geology, provides the scientific basis to understand hominin evolution.

Connections

Fossil evidence indicates our primate origins

date to at least 65 million years ago.

The first more human- like animals (hominins)

appeared in Africa around 6 mya ago and evolved

into a variety of different species.

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After mastering the material in this chapter, you should be able to:

▶ �Describe why paleoanthropology is necessarily a multidisciplinary science and discuss the major subdisciplines that contribute to it.

▶ �Explain what is meant by biocultural evolution and provide examples of how it might have influenced the development of the earliest cultural behavior in hominins and also simultaneously influenced biological/anatomical changes in them.

▶ �Discuss why precise dating is essential to understanding human evolution and describe some of the major techniques used.

▶ �Discuss what the earliest tools thus far discovered looked like and explain how they may have been made.

▶ �Describe the different hypotheses that try to account for the evolution of bipedal locomotion and discuss the strengths and weaknesses of each.

255

A portion of a pig’s tusk, a small sample of volcanic sediment, a battered rock, a primate’s molar: What do these seemingly unre- markable remains have in common, and more to the point, why are they of interest to paleoanthropologists? First of all, if they’re all discovered at sites in Africa or Eurasia, they may be quite ancient—indeed, perhaps millions of years old. Further, some of these mate- rials actually inform scientists directly of quite precise dating of the finds. Last and most exciting, some of these finds may have been modified, used, and dis- carded by bipedal creatures who looked and behaved in some ways like our- selves but were in other respects very different. And what of that molar? Is it a fossilized remnant of an ancient hominin? These are the kinds of ques- tions asked by paleoanthropologists, and to answer them, these research- ers travel to remote locales across the Old World.

How do we distinguish possible hominins from other types of ani- mals (most notably from other pri- mates), especially when all we have are fragmentary fossil remains from just a small portion of a skeleton? How do humans and our most distant ances- tors compare with other animals? In the last three chapters, we’ve seen how humans are classified as primates, both structurally and behaviorally, and how our evolutionary history coincides with that of other mammals and specifi-

9 Paleoanthropology: Reconstructing Early Hominin Behavior and Ecology

cally other primates. Even so, we’re a unique kind of primate, and our ances- tors have been adapted to a particular lifestyle for several million years. Some late Miocene fossil apes prob- ably began this process close to 7 mya, though better-preserved fossil discov- eries reveal more definitive evidence of hominins shortly after 5 mya.

We’re able to determine the hom- inin nature of these remains by more than the structure of teeth and bones; we know that these animals were hom- inins also because of the way they behaved—emphasizing once again the biocultural nature of human evolution. In this chapter, we’ll discuss the meth- ods scientists use to explore the secrets of early hominin behavior and ecology.

Student Learning Objectives

chapter 9 Paleoanthropology: Reconstructing Early Hominin Behavior and Ecology 256

Understanding Our Direct Evolutionary Connections: What’s a Hominin?

The earliest evidence of hominins that has been found dates to the end of the Miocene and mainly includes dental and cranial pieces. But dental features alone don’t describe the special features of hominins, and they certainly aren’t distinctive of the later stages of human evolution. Modern humans, as well as our most immediate hom- inin ancestors, are distinguished from the great apes by more obvious features than tooth and jaw dimensions. For example, various scientists have pointed to such distinctive hominin character- istics as bipedal locomotion, large brain size, and toolmaking behavior as being significant (at some stage) in defining what makes a hominin a hominin.

It’s important to recognize that all these characteristics did not develop simultaneously or at the same pace. In fact, over the last several million years of hominin evolution, a very different pattern has been evident, in which the various components (dentition, loco- motion, brain size, and toolmaking) have developed at quite different rates. This pattern, in which physiological and behavioral systems evolve at dif- ferent rates, is called mosaic evolu- tion. As we first pointed out in Chapter 1 and will emphasize in this and the next chapter, the single most impor- tant defining characteristic of the full course of hominin evolution is biped- al locomotion. In the earliest stages of hominin emergence, skeletal evi- dence indicating bipedal locomotion is the only truly reliable indicator that these fossils were indeed hominins. But in later stages of hominin evolution, other features, especially those relat- ing to brain development and behavior, become highly significant (Fig. 9-1).

These behavioral aspects of hom- inin emergence—particularly toolmak- ing—are what we’d like to emphasize

in this chapter. Important structural attributes of the hominin brain, teeth, and especially locomotor apparatus are discussed in the next chapter, where we investigate early hominin anatomical adaptations in greater detail.

What’s in a Name? Throughout this book, we refer to members of the human family as hom- inins (the technical name for mem- bers of the tribe Hominini). Most pro- fessional paleoanthropologists now prefer this terminology, since it more accurately reflects evolutionary rela- tionships. As we mentioned briefly in Chapter 6, the more traditional classi- fication of hominoids is not as accurate and actually misrepresents key evolu- tionary relationships.

Over the last several years detailed molecular evidence has clearly shown that the great apes (tradition- ally classified as pongids and includ- ing orangutans, gorillas, chimpan- zees, and bonobos) do not make up a coherent evolutionary group sharing a s ingle common ancestor and thus are not a monophyletic group. Indeed, the molecular data indicate that the African great apes (gorillas, chimpan- zees, and bonobos) are significantly more closely related to humans than is the orangutan. What’s more, at an even closer evolutionary level, we now know that chimpanzees and bonobos are yet more closely linked to humans than is the gorilla. Hominoid classification has been significantly revised to show these more complete relationships, and two further taxonomic levels (subfam- ily and tribe) have been added.

We should mention a couple of important ramifications of this new classification. First, it further empha- sizes the very close evolutionary rela- tionship of humans with African apes and most especially with chimpanzees and bonobos. Second, the term homi- nid, which has been used for decades to refer to our specific evolutionary lin- eage, has a quite different meaning in the revised classification; now it refers to all great apes and humans together.

mosaic evolution a pattern of evo- lution in which the rate of evolution in one functional system varies from that in other systems. For example, in hominin evolution, the dental system, locomotor system, and neurological system (especially the brain) all evolved at markedly different rates.

Biocultural Evolution: The Human Capacity for Culture 257

Biocultural Evolution: The Human Capacity for Culture

One of the most distinctive behav-ioral features of humans is our extraordinary elaboration of and dependence on culture. Certainly other primates, and many other ani- mals for that matter, modify their envi- ronments. As we saw in Chapter 7, chimpanzees especially are known for such behaviors as using termite sticks,

and some chimpanzees as well as capu- chin monkeys even carry rocks to use for crushing nuts. Because of such observations, we’re on shaky ground when it comes to drawing sharp lines between early hominin toolmaking behavior and that exhibited by other animals.

Another point to remember is that human culture, at least as it’s defined in contemporary contexts, involves much more than toolmaking capacity. For humans, culture integrates an entire adaptive strategy involving cognitive,

(Miocene, generalized hominoid) (Early hominin) (Modern Homo sapiens)

TOOLMAKING BEHAVIOR

DENTITION

BRAIN

LOCOMOTION

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▲�Figure 9-1 Mosaic evolution of hominin characteristics: a postulated time line.

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culture Behavioral aspects of human adaptation, including technology, tradi- tions, language, religion, marriage pat- terns, and social roles. culture is a set of learned behaviors transmitted from one generation to the next by nonbiological (i.e., nongenetic) means.

chapter 9 Paleoanthropology: Reconstructing Early Hominin Behavior and Ecology 258

political, social, and economic compo- nents. Material culture—or the tools humans use—is but a small portion of this cultural complex.

Still, when we examine the archae- ological record of earlier hominins, what’s available for study is almost exclusively limited to material cul- ture, especially the bits and pieces of broken stone left over from tool man- ufacture. This is why it’s extremely difficult to learn anything about the earliest stages of hominin cultural development before the regular manu- facture of stone tools. As you’ll see, this most crucial cultural development has been traced to approximately 2.6 mya (Semaw et al., 2003). Yet because of our contemporary primate models, we can assume that hominins were undoubt- edly using other kinds of tools (made of perishable materials) and displaying a whole array of other cultural behaviors long before then. But with no “hard” evidence preserved in the archaeologi- cal record, our understanding of the early development of these nonmaterial cultural components remains elusive.

The fundamental basis for human cultural success relates directly to our cognitive abilities. Again, we’re not dealing with an absolute distinction but a relative one. As you’ve already learned, other primates, as documented in the great apes, have some of the language capabilities exhibited by humans. Even so, modern humans display these abili- ties in a complexity several orders of magnitude beyond that of any other animal. And only humans are so com- pletely dependent on symbolic commu- nication and its cultural by-products that contemporary Homo sapiens could not survive without them.

At this point you may be wonder- ing when the unique combination of cognitive, social, and material cultur- al adaptations became prominent in human evolution. In answering that question we must be careful to recog- nize the manifold nature of culture; we can’t expect it to always contain the same elements across species (as when comparing ourselves with nonhuman

primates) or through time (when try- ing to reconstruct ancient hominin behavior). Richard Potts (1993) has critiqued such overly simplistic per- spectives and suggests instead a more dynamic approach, one that incorpo- rates many subcomponents (includ- ing aspects of behavior, cognition, and social interaction).

We know that the earliest hominins almost certainly didn’t regularly man- ufacture stone tools (at least none that have been found and identified as such). These earliest members of the hominin lineage, dating back to approximately 6 to 5 mya, may have carried objects such as naturally sharp stones or stone flakes, parts of carcasses, and pieces of wood around their home ranges. At the very least, we would expect them to have displayed these behaviors to at least the same degree as exhibited by living chimpanzees.

Also, as you’ll see in the next chap- ter, by around 6 mya, hominins had developed one crucial advantage: They were bipedal and so could more easily carry all kinds of objects from place to place. Ultimately, the efficient exploi- tation of resources widely distributed in time and space would most likely have led to using “central” spots where key components—especially stone objects—were cached, or collected (Potts, 1991; see “A Closer Look, What Were Early Hominins Doing, and How Do We Know?” on pages 260–261).

What we know for sure is that over a period of several million years, during the formative stages of hominin emer- gence, many components interacted, but not all of them developed simul- taneously. As cognitive abilities devel- oped, more efficient means of commu- nication and learning resulted. Largely because of consequent neurological reorganization, more elaborate tools and social relationships also emerged. These, in turn, selected for greater intelligence, which in turn selected for further neural elaboration. Quite clearly these mutual dynamic interac- tions are at the very heart of what we call hominin biocultural evolution.

Discovering Human Evolution: The Science of Paleoanthropology 259

Discovering Human Evolution: The Science of Paleoanthropology

To adequately understand human evolution, we obviously need a broad base of information. It’s the paleoanthropologist’s task to recover and interpret all the clues left by early hominins. Paleoanthropology is defined as “the study of ancient humans.” As such, it’s a diverse multi- disciplinary pursuit seeking to recon struct every possible bit of informa tion concerning the dating, anatomy, behavior, and ecology of our hominin ancestors. Over the past few decades, the study of early humans has mar shaled the specialized skills of many different kinds of scientists. This grow ing and exciting adventure includes but is not limited to geologists, verte brate paleontologists, archaeologists, physical anthropologists, and paleo ecologists (Table 9.1).

Geologists, usually working with other paleoanthropologists, do the ini tial surveys to locate potential early hominin sites. Many sophisticated techniques aid in this search, including aerial and satellite imagery (Fig. 9-2), though the most common way to find these sites is simply to trip over fos sil remains. Vertebrate paleontologists are usually involved in this early sur vey work, helping to find fossil beds containing faunal (animal) remains,

because where conditions are favorable for the preservation of bone from such species as pigs and elephants, hom inin remains may also be preserved. Paleontologists also can (through com parison with known faunal sequences) give quick and dirty approximate age estimates of fossil sites in the field without having to wait for the results of more time consuming (though more accurate) analyses that will later be performed in a lab (Fig. 9-3 on page 262).

Once identified, fossil beds likely to contain hominin finds are subjected to extensive field surveying. For some sites, generally those postdating 2.6 mya (roughly the age of the oldest identified human artifacts), archaeolo gists take over in the search for hom inin material traces. We don’t neces sarily have to find remains of early hominins themselves to know that

Table 9.1 Subdisciplines of Paleoanthropology Physical Sciences Biological Sciences Social Sciences

Geology

Stratigraphy

Petrology

(rocks, minerals)

Pedology (soils)

Geomorphology

Geophysics

Chemistry

Taphonomy

Physical anthropology

Paleoecology

Paleontology

(fossil animals)

Palynology

(fossil pollen)

Primatology

Archaeology

Ethnoarchaeology

Cultural anthropology

Ethnography

Psychology

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▲ Figure 9-2 Satellite photo of geological exposures in northern Tanzania, near Olduvai Gorge. The mountainous regions are part of the Rift Valley. The lake has formed inside a volcanic crater.

multidisciplinary Pertaining to research involving mutual contributions and the cooperation of experts from various scientific fields, or disciplines.

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they consistently occupied a particular area. Such material clues as artifacts inform us directly about early hominin activities. Modifying rocks according to a consistent plan or simply carrying them around from one place to another over fairly long distances and distrib- uting them in a manner not explicable by natural means—like movement due to streams or glaciers—is characteris- tic of no other animal but a hominin.

So when we see such material evidence at a site, we know without a doubt that hominins were once present there.

We’ve suspected for a while that hominins likely used stone and other materials for a long time before they began modifying rock to a consis- tent (and recognizable) pattern. After all, chimpanzees carry rocks short distances and bash nuts with them (see Chapter 8). New evidence from

What Were Early Hominins Doing, and How Do We Know?

Many years ago, the popular interpre-tation of the bone refuse and stone tools discovered at Olduvai Gorge and other sites suggested that most or all of these materials resulted from hominin activities. however, a later and more comprehen- sive reanalysis of the bone remains from Olduvai localities has challenged this view (Binford, 1981, 1983). Olduvai is so impor- tant because it has the most complete and best studied paleoanthropological record of any early hominin site in the world. archaeologist Lewis Binford criticizes those who are drawn too quickly to concluding that these bone scatters are the remnants of hominin behavior patterns while simul- taneously ignoring the possibility of other explanations.

From information concerning the kinds of animals present, which body parts were found, and the differences in preservation among these skeletal elements, Binford has concluded that much of what’s pre- served can be explained by carnivore activ- ity. this conclusion has been reinforced by certain details observed by Binford himself in alaska—details on animal kills, scavenging, the transportation of elements, and preservation that are the result of wolf and dog behaviors. Binford describes his approach:

I took as “known,” then, the struc- ture of bone assemblages pro- duced in various settings by animal predators and scavengers; and as “unknown” the bone deposits excavated by the Leakeys at Olduvai Gorge. Using mathematical and statistical techniques I considered to what degree the finds from Oldu- vai Gorge could be accounted for in terms of the results of predator behavior and how much was “left over.” (Binford, 1983, pp. 56–57)

Binford isn’t arguing that all of the remains found at Olduvai resulted from nonhominin activity. In fact, he recognizes that “residual material” was consistently found on surfaces with high tool concen- tration “which could not be explained by what we know about african animals” (Binford, 1983).

Support for the idea that early homi- nins utilized at least some of the bone refuse has come from a totally different perspective. researchers have analyzed (both macroscopically and microscopically) the cut marks left on fossilized bones. By experimenting with modern materials, they’ve been able to delineate more clearly the differences between marks left by stone tools and those left by animal teeth or other factors (Bunn, 1981; potts and Shipman, 1981). analyses of bones from several early localities at Olduvai have shown unambigu- ously that hominins used these specimens and left telltale cut marks from their stone tools. the sites investigated so far reveal

a somewhat haphazard cutting and chop- ping, apparently unrelated to deliberate disarticulation. So the conclusion is that hominins scavenged carcasses, probably of carnivore kills, and did not hunt large animals themselves (Shipman, 1983). as we’ll see in a moment, new evidence of possible cut marks as well as indications of pounding to get at the marrow has been found at a site in ethiopia dating as far back as 3.4 mya.

Following and expanding on the experi- mental approaches pioneered by Binford, Bunn, and others, robert Blumenschine, of rutgers University, has more recently conducted a more detailed analysis of the Olduvai material. Like his predecessors, Blumenschine has also concluded that the cut marks on animal bones are the result of hominin processing (Blumenschine, 1995). Blumenschine and colleagues further surmise that most meat acquisition (virtu- ally all from large animals) was the result of scavenging (from remains of carnivore kills or from animals that died from natural causes). In fact, these researchers suggest that scavenging was a crucial adaptive strategy for early hominins and considerably influenced their habitat usage, diet, and utilization of stone tools (Blumenschine and cavallo, 1992; Blumenschine and peters, 1998). What’s more, Blumenschine and colleagues have developed a model detail- ing how scavenging and other early hominin adaptive strategies integrate into patterns of land use (that is, differential utilization of various niches in and around Olduvai). From this model, they formulated specific hypoth-

A Closer Look

artifacts Objects or materials made or modified for use by hominins. the earliest artifacts are usually tools made of stone or occasionally bone.

Discovering Human Evolution: The Science of Paleoanthropology 261

the Dikika site in Ethiopia might indi- cate that hominins were using stone in an even more sophisticated way as far back as 3.4 mya (McPherron et al., 2010). No stone tools were found, but two animal bones show cut marks (see “A Closer Look,” above) as well as other marks suggesting that the bones were pounded with unmodi- fied rocks (ostensibly to slice away meat and retrieve marrow). While it’s

true that this evidence doesn’t mean that hominins were yet modifying rocks consistently to make tools, it potentially shows advanced behavior, including scavenging, meat eating, and marrow extraction that have not pre- viously been considered possible for very early hominins. These finds are extremely important and have been very carefully investigated. However, just the two bones by themselves (and

eses concerning the predicted distribution of artifacts and animal remains in different areas at Olduvai. Subsequent excavations at Olduvai were aimed specifically at testing these hypotheses.

If early hominins (close to 2 mya) weren’t hunting consistently, what did they obtain from scavenging the kills of other animals? One obvious answer is whatever meat was left behind. however, the posi- tion of the cut marks suggests that early hominins were often hacking at non- meat-bearing portions of the skeletons. perhaps they were after bone marrow and brain, substances not fully exploited by other predators and scavengers (Binford, 1981; Blumenschine and cavallo, 1992).

exciting discover- ies from the Bouri peninsula of the Middle

awash of ethiopia pro-

vide the best evidence yet for

meat and mar- row exploitation by

early hominins. Dated to 2.5 mya (that is, as old as the

oldest known artifacts), antelope and horse fossils from Bouri show telltale inci- sions and breaks, indicating that bones were not only smashed to extract marrow but also cut, ostensibly to retrieve meat (de heinzelin et al., 1999). the research- ers who analyzed these materials have suggested that the greater dietary reliance on animal products may have been impor- tant in stimulating brain enlargement in the lineage leading to genus Homo.

another recent research twist relating to the reconstruction of early hominin diets has come from the biochemical analysis of some hominin teeth from South africa (dating to about the same time range as hominins from Olduvai—or perhaps slightly earlier). In an innovative application of stable carbon isotope analysis, Matt Sponheimer and Julia Lee-thorp found that these early hominin teeth revealed telltale chemical signatures relat- ing to diet (Sponheimer and Lee-thorp, 1999). In particular, the proportions of

stable carbon isotopes indicated that these early hominins ate either grass products (such as seeds) or meat/marrow from animals that in turn had eaten grass products (that is, the hominins might well have derived a significant portion of their diet from meat or other animal products). What’s more, newly collected stable car- bon isotope data from another South afri- can early hominin show a quite different diet from that of other South african finds and, indeed almost all other early homi- nins (henry et al., 2012) (see chapter 10). this evidence comes from an exciting new perspective that provides a more direct indicator of early hominin diets. While it’s not clear how much meat these early hom- inins consumed, these new data do sug- gest that they were consistently exploiting more open regions of their environment. Moreover, a new laser technology makes it possible to detect, from a single tooth, what sorts of foods were eaten from year to year and even seasonally within the same year. Sponheimer, thorp, and colleagues have used this new approach to show that some early hominins were able to flexibly move between different environments and exploit seasonally avail- able foods (Sponheimer et al., 2006). to demonstrate that stable isotope data are accurate, researchers need to evaluate the influence of chemical changes (diagenesis) to bones and teeth that occurred during fossilization. Stable isotope methods will continue to play a prominent role in the reconstruction of hominin diets and paleoenvironments.

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▲�Figure 1 Hyenas scavenging a buffalo carcass in East Africa. Early hominins also scavenged animals that had been killed by predators. In so doing, they almost certainly competed with hyenas and other scavengers.

stable carbon isotopes Isotopes of carbon that are produced in plants in differing proportions, depending on envi- ronmental conditions. By analyzing the pro- portions of the isotopes contained in fossil remains of animals (who ate the plants), it’s possible to reconstruct aspects of ancient diet and environments (particularly tem- perature and aridity).

chapter 9 Paleoanthropology: Reconstructing Early Hominin Behavior and Ecology 262

no stone tools) are not enough evi- dence for many paleoanthropologists to be entirely convinced that the eat- ing of meat and marrow were yet typi- cal behaviors of such ancient hominins (Domínguez-Rodrigo et al., 2010).

Once an area has clearly been dem- onstrated to be a hominin site, much more concentrated research begins (Fig. 9-4). We should point out that a more mundane but significant aspect of paleoanthropology not reflected in Table 9-1 is the financial one. Just the initial survey work in usually remote areas costs many thousands of dollars, and mounting a concentrated research project costs several hundred thou- sand dollars more. This is why many projects are undertaken in areas where promising surface finds have already been made. Massive financial support is required from government agen- cies and private donations; therefore, it’s unrealistic just to dig at random. A great deal of a paleoanthropologist’s effort and time is necessarily devoted to writing grant proposals or speak- ing on the lecture circuit to raise the required funds for this work.

Once the financial hurdle has been cleared, a coordinated research proj- ect can begin. Usually headed by an archaeologist or physical anthropolo- gist, the field crew continues to survey

and map the target area in great detail. In addition, field crew members begin searching carefully for bones and arti- facts eroding out of the soil, taking pol- len and soil samples for ecological anal- ysis, and carefully collecting rock and other samples for use in various dat- ing techniques. If, at this early stage of exploration, members of the field crew find fossil hominin remains, they will feel very lucky indeed. The internation- al press usually considers human fossils the most exciting kind of discovery—a fortunate circumstance that produces wide publicity and often ensures future financial support. More likely, the crew will accumulate much information on geological setting, ecological data (par- ticularly faunal remains), and, with some luck, artifacts and other archaeo- logical traces.

Although paleoanthropological fieldwork is typically a long and ardu- ous process, the detailed analyses of collected samples and other data back in the laboratory are even more time- consuming. Archaeologists must clean, sort, label, and identify all artifacts, and vertebrate paleontologists must do the same for all faunal remains. Knowing the kinds of animals represented— whether forest browsers, woodland spe- cies, or open-country forms—greatly helps in reconstructing the local paleo- ecological settings in which early homi- nins lived. Analysis of the fossil pollen collected from hominin sites by a sci- entist called a palynologist further aids in developing a detailed environmental reconstruction. All these paleoecologi- cal analyses can assist in reconstruct- ing the diet of early humans. Also, the taphonomy of the site must be worked out to understand its depositional his- tory—that is, how the site formed over time and if its present state is in a pri- mary or secondary context.

In the concluding stages of interpre- tation, the paleoanthropologist draws together these essentials:

1. Dating: geological, paleontological, geophysical

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▲ Figure 9-3 A geologist is shown making entries on a detailed map as he surveys a large area of exposures in the Hadar region of northeastern Ethiopia.

taphonomy (taphos, meaning “tomb”) the study of how bones and other materials came to be buried in the earth and pre- served as fossils. taphonomists study the processes of sedimentation, the action of streams, preservation properties of bone, and carnivore disturbance factors.

context the environmental setting where an archaeological trace is found. primary context is the setting in which the archaeological trace was originally depos- ited. a secondary context is one to which it has been moved (such as by the action of a stream).

Discovering Human Evolution: The Science of Paleoanthropology 263

2. Paleoecology: paleontology, palynology, geomorphology, taphonomy

3. Archaeological traces of behavior 4. Anatomical evidence from hominin

remains

By analyzing all this information, scientists try to “flesh out” the kind of creature that may have been our direct ancestor (or at least a very close relative). Primatologists may assist here by show- ing the detailed relationships between the anatomical structure and behavior of humans and that of contemporary nonhuman primates. Cultural anthro- pologists and ethno archaeologists (who study the “archaeology” of living groups

by examining their material remains) may contribute ethnographic infor- mation concerning the varied nature of modern human behavior, particu- larly ecological adaptations of those contemporary hunter-gatherer groups exploiting roughly similar environmen- tal settings as those reconstructed for a hominin site.

The end result of years of research by dozens of scientists will (we hope) produce a more complete and accurate understanding of human evolution— how we came to be the way we are. Both biological and cultural aspects of our ancestors contribute to this inves- tigation, each process developing in relation to the other.

▲�Figure 9-4 Location of sites where early evidence of stone tools has been discovered. The dates shown for each site represent the earliest dated tools found at that location.

*Interpretation of the Dikika evidence is controversial. It includes bones with presumed cut marks. However, no stone tools have been found.

K E N Y A

E T H I O P I A

ERITREA

S U D A N

E G Y P T

N I G E R

M A L I

N I G E R I A

S O M A L I A

C H A D

T A N Z A N I A

A N G O L A

MOZAMBIQUE

Z A M B I A

GABON

CENTRAL AFRICAN REPUBLIC

UGANDA

MALAWI

BURUNDI

RWANDA

TOGO

BENIN

GHANA

BURKINA

CAMEROON

CONGO D E M . R E P .

O F C O N G O

EQUATORIAL GUINEA

DJIBOUTI

Y E M E N

S A U D I A R A B I A

Dikika (3.4 my)*/ Hadar (2.3 my)

Bouri (2.6 my)

Gona (2.6 my)

Koobi Fora (East Turkana) (1.8 my)

Olduvai (1.8 my)

West Turkana (2.3 my)

Omo (2.3 my)

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chapter 9 Paleoanthropology: Reconstructing Early Hominin Behavior and Ecology 264

Connecting the Dots through Time: Paleoanthropological Dating Methods

An essential objective of paleoan-thropology is to place sites and fos- sils into a time frame. In other words, we want to know how old they are. How, then, do we date sites—or more precisely, the geological strata, or lay- ers, in which sites are found? The ques- tion is both reasonable and important, so let’s examine the dating techniques used by paleontologists, archaeologists, and other scientists involved in paleo- anthropological research.

Scientists use two kinds of dating for this purpose: relative dating and chronometric dating (also known as absolute dating). Relative dating meth- ods tell us that something is older or younger than something else but not by how much. If, for example, a cranium is found at a depth of 50 feet and another cranium at 70 feet at the same site, we usually assume that the specimen dis- covered at 70 feet is older. We may not know the date (in years) of either one, but we’d know that one is older (or younger) than the other. Although this may not satisfy our curiosity about the actual number of years involved, it would give us some idea of the evolu- tionary changes in cranial morphology (structure), especially if we found sev- eral crania at different levels and com- pared them.

This method of relative dating is based on stratigraphy and was one of the first techniques to be used by sci- entists working with the vast period of geological time. Stratigraphy, in turn, is based on the principle of superposi- tion, which states that a lower stratum (layer) is older than a higher stratum. Because much of the earth’s crust has been laid down by layer after layer of sedimentary rock, much like the layers of a cake, stratigraphy has been a valu- able aid in reconstructing the history of the earth and the life upon it.

Stratigraphic dating does, how- ever, have some problems. Earth disturbances, such as volcanic activ- ity, river activity, and mountain build- ing, may shift strata and the objects within them; in such cases the chronol- ogy of the material may be difficult or even impossible to reconstruct. What’s more, it’s impossible to accurately determine the time period of a particu- lar stratum—that is, how long it took to accumulate (Fig. 9-5).

Another method of relative dat- ing is fluorine analysis, which applies only to bones (Oakley, 1963). Bones in the earth are exposed to the seep- age of groundwater, which usually con- tains fluorine. The longer a bone lies in the earth, the more fluorine it will incorporate during the fossilization process. Bones deposited at the same time in the same location thus should contain the same amount of fluorine. Professor Kenneth Oakley, of the British Museum, used this technique in the early 1950s to expose the Piltdown (England) hoax by demonstrating that a human skull was considerably older than the jaw (ostensibly also human) found with it (Weiner, 1955). When a discrepancy in the fluorine content led Oakley and others to examine the bones more closely, they found that the jaw was not that of a hominin at all but of a young adult orangutan!

Unfortunately, fluorine analysis is useful only with bones found at the same location. Because the amount of fluorine in groundwater is based on local conditions, it varies from place to place. Also, some groundwater may not contain any fluorine. For these reasons it’s impossible to use fluorine analysis when comparing bones from different localities.

In both stratigraphy and fluorine analysis, it’s impossible to calculate the actual age of a geological stratum and the objects within it. To determine the age in years, scientists have devel- oped various chronometric techniques based on the phenomenon of radioac- tive decay. Actually, the theory is pretty simple: Certain radioactive isotopes of

chronometric dating (chrono, meaning “time,” and metric, meaning “measure”) a dating technique that gives an estimate in actual numbers of years; also known as absolute dating.

stratigraphy Study of the sequential layering of deposits.

principle of superposition In a stratigraphic sequence, the lower layers were deposited before the upper layers. Or, simply put, the stuff on top of a heap was put there last.

Connecting the Dots through Time: Paleoanthropological Dating Methods 265

elements are unstable, causing them to decay and form an isotopic varia- tion of another element. Since the rate of decay follows a definite mathemati- cal pattern, the radioactive material forms an accurate geological time clock of sorts. By measuring the amount of decay in a particular sample, scientists can calculate the number of years it took for that amount of decay to accu- mulate. Chronometric techniques have been used for dating the immense age of the earth as well as artifacts less than 1,000 years old. Several techniques have been employed for a number of years and are now quite well known.

The most important chronometric technique used to date early hominins involves potassium-40 (40K), which has a half-life of 1.25 billion years and pro- duces argon-40 (40Ar). Known as the K/ Ar or potassium-argon method, this procedure has been extensively used by paleoanthropologists in dating mate- rials in the 1- to 5-million-year range, especially in East Africa, where past volcanic activity makes this dating technique possible. A variant of this technique, the 40Ar/39Ar method, has also been used to date several hominin localities. The 40Ar/39Ar method per- mits the analysis of smaller samples (even single crystals), reduces experi-

mental error, and is more precise than standard K/Ar dating. Consequently, it can be used to date a wide chrono- logical range—indeed, the entire hom- inin record, even up to modern times. Recent applications have provided excellent dates for several early hom- inin sites in East Africa (discussed in Chapter 10) as well as somewhat later sites in Java (discussed in Chapter 11). In fact, the technique was used to date the famous Mt. Vesuvius eruption of a.d. 79, which destroyed the city of Pompeii, as documented by ancient historians. Remarkably, the midrange date obtained by the 40Ar/39Ar tech- nique was a.d. 73, just six years from the known date (Renne et al., 1997)! And still another radiometric dating method, this one measuring the decay of uranium into lead (the U/Pb method, with a half-life of 4.47 million years), has been used recently in South Africa to date hominin sites (De Ruiter et al., 2009; Dirks et al., 2010). Organic mate- rial, such as bone, can’t be directe- ly dated by these techniques; but the rock matrix in which the bone is found can be. Scientists used K/Ar dating to obtain a minimum date for the deposit containing the Zinjanthropus cranium discovered at Olduvai by dating a vol- canic layer above the fossil (Fig 9-6).

◀�Figure 9-5 View of the main gorge at Olduvai Gorge in Tanzania. Note the clear sequence of geological beds. The discontinuity in the stratigraphic layers (to the right of the red arrow) is a major fault line. The stratigraphy at Olduvai is exceptionally well pre- served, although even here you can see that it can be complicated.

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half-life the time period in which one- half the amount of a radioactive isotope is converted chemically to a daughter prod- uct. For example, after 1.25 billion years, half the potassium-40 (40K) remains; after 2.5 billion years, one-fourth remains.

chapter 9 Paleoanthropology: Reconstructing Early Hominin Behavior and Ecology 266

building up electrons at a steady rate. To determine the age of an archaeolog- ical sample, the researcher must heat the sample to 500°C and measure its thermoluminescence, from which the date can be calculated. Used especially by archaeologists to date ceramic pots from recent sites, TL can also be used to date burned flint tools from earlier hominin sites.

Like TL, two other techniques used to date sites from the latter phases of hominin evolution (where neither K/ Ar nor radiocarbon dating is possible) are uranium series dating and electron spin resonance (ESR) dating. Uranium series dating relies on the radioac- tive decay of short-lived uranium iso- topes, and ESR is similar to TL because it’s based on measuring trapped elec- trons. However, while TL is used on heated materials such as clay or stone tools, ESR is used on the dental enamel of animals. All three of these dating methods have been used to provide key dating controls for hominin sites dis- cussed in Chapters 11 through 13.

You should realize that none of these methods is precise. Each one has problems that must be carefully con- sidered during laboratory measure- ment and in collecting material to be analyzed. Because the methods aren’t perfectly accurate, approximate dates are given as probability statements with an error range. For example, a date given as 1.75 ± 0.2 mya should be read as having a 67 percent chance that the actual date lies somewhere between 1.55 and 1.95 mya (see “A Closer Look, Chronometric Dating Estimates”).

An important means of cross- checking dates is called paleomag- netism. This technique is based on the constantly shifting nature of the earth’s magnetic pole. Of course, the earth’s magnetic pole is now oriented in a northerly direction, but this hasn’t always been so. In fact, the orientation and intensity of the geomagnetic field have undergone numerous document- ed changes in the last few million years. From our current viewpoint, we call a

Rocks that provide the best sam- ples for K/Ar and 40Ar/39Ar dating are

those that have been heated to an extremely high temperature,

such as that generated by vol- canic activity. When the

rock is in a molten state, argon, a gas, is driven off. As the rock cools and solidifies, 40K continues to break down to argon; but now the gas is physi-

cally trapped in the cooled rock. To obtain the date

of the rock, scientists reheat it and measure the escaping

gas. Because the rock must in the past have been exposed to extreme heat, this limits these techniques to areas where sediments have been superheated, such as regions of past volcanic activity or meteorite falls.

Another well-known radiometric method popular with archaeologists makes use of carbon-14 (14C), with a half-life of 5,730 years. It has been used to measure the age of organic mate- rials (such as wood, bone, cloth, and plant remains) dating from less than 1,000 years to more than 75,000 years ago, although accuracy is reduced for materials more than 40,000 years old. Since this technique is used to study the latter stages of hominin evolution, its applications relate to material dis- cussed in Chapters 12 and 13.

Some inorganic artifacts can be directly dated through the use of ther- moluminescence (TL). This method, too, relies on the principle of radio- metric decay. Stone material used in manufacturing tools invariably con- tains trace amounts of radioactive ele- ments, such as uranium or thorium. As the rock gets heated (perhaps by accidentally falling into a campfire or deliberately being heated to help in its production), the rapid heating releases displaced beta particles trapped within the rock. As the particles escape, they emit a dull glow known as thermolumi- nescence. After that, radioactive decay resumes within the fired stone, again

▲�Figure 9-6 Zinjanthropus cranium, discovered at Olduvai Gorge and dated to 1.75 mya. This dating (using the potassium/argon method) was extraordinarily important, because previously most paleoanthropologists didn’t think hominins appeared until around a million years ago.

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thermoluminescence (TL) (ther- mo-loo-min-ess´-ence) a technique for dat- ing certain archaeological materials (such as stone tools) that were heated in the past and that, upon reheating, release the stored energy of radioactive decay as light.

paleomagnetism Dating method based on the earth’s shifting magnetic pole.

Connecting the Dots through Time: Paleoanthropological Dating Methods 267

northern orientation “normal” and a southern one “reversed.” Paleomagnetic dating is accomplished by carefully taking samples of sediments that con- tain magnetically charged particles. Since these particles maintain the mag- netic orientation they had when they were consolidated into rock (millions of years ago), we have a kind of “fossil compass” (Fig. 9-7). Then the paleo- magnetic sequence is compared against the K/Ar dates to see if they agree. Some complications may arise, but once these oscillations in the geomag- netic pole are worked out, the sequence of paleomagnetic orientations can pro- vide a valuable cross-check for K/Ar age determinations. Paleomagnetic dating has also been used recently in South Africa to confirm the U/Pb dates from a newly discovered hominin site (Dirks et al., 2010).

A final dating technique used at sev- eral African sites is based on the regu- lar evolutionary changes in well-known groups of mammals. This technique, called faunal correlation, or biostra- tigraphy, provides yet another means of cross-checking the other meth- ods. This technique employs some of the same methods used in relative stratigraphic dating, but it incorpo- rates information on sequences of fau- nal remains from different sites. For

instance, the pres- ence of particular fossil pigs, elephants, antelopes, rodents, and carnivores in areas where dates are known (by K/Ar, for example) can be used to extrapolate an approximate age for other, more hard- to-date sites by not- ing which genera and species are present at those sites.

All these meth- ods—K/Ar dating, paleomagnetism, and biostratigra- phy—have been used in dating early hom- inin sites. So many different dating tech- niques are necessary because no single method is perfectly reliable by itself. Sampling error, contamination, and experimental error can all introduce ambiguities into our so-called absolute dates. Because the sources of error are different for each technique, however, cross-checking among several indepen- dent methods is the most reliable way of authenticating the chronology for early hominin sites.

Chronometric Dating Estimates

Chronometric dates are usually deter-mined after testing several geological samples. the dates that result from such testing are combined and expressed sta- tistically. For example, say that five differ- ent samples are used to give the K/ar

date 1.75 ± 0.2 mya for a particular geo- logical bed. the individual results from all five samples are totaled together to give an average date (here, 1.75 mya), and the standard deviation is calculated (here, 0.2 million years; that is, 200,000 years). the dating estimate is then reported as the mean plus or minus (±) 1 standard deviation. those of you who have taken statistics will realize that (assuming a nor- mal distribution) 67 percent of a distribu- tion of dates is included within 1 standard

deviation (±) of the mean. thus, the chro- nometric result, as shown in the reported range, is simply a probability statement that 67 percent of the dates from all the samples tested fell within the range of dates from 1.55 to 1.95 mya. You should carefully read chronometric dates and study the reported ranges. It’s likely that the smaller the range, the more samples were analyzed. Smaller ranges mean more precise estimates; better laboratory controls will also increase precision.

A Closer Look

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▲�Figure 9-7 A geologist carefully takes a sample of sediment contain- ing magnetically charged particles for paleomagnetic dating. He must very precisely record the exact compass orientation so that it can be corre- lated with the sequence of magnetic orientations.

biostratigraphy a relative dating technique based on the regular changes seen in evolving groups of animals as well as the presence or absence of particular species.

chapter 9 Paleoanthropology: Reconstructing Early Hominin Behavior and Ecology 268

Experimental Archaeology

Simply classifying artifacts into cat-egories and types is not enough. We can learn considerably more about our ancestors by understanding how they made and used their tools. It is, after all, the artifactual traces of pre- historic tools of stone (and, to a lesser degree, bone) that provide much of our information concerning early human behavior. Tons of stone debris litter archaeological sites worldwide. A casu- al walk along the bottom of Olduvai Gorge could well be interrupted every few seconds by tripping over prehistor- ic tools!

Clearly, archaeologists are presented with a wealth of information r evealing at least one part of human material culture. What do these artifacts tell us about our ancestors? How were these tools made, and how were they used? To answer these questions, contempo- rary archaeologists have tried to recon- struct prehistoric techniques of stone toolmaking, butchering, and so forth. In this way, experimental archaeolo- gists are, in a sense, trying to re-create the past.

Stone Tool (Lithic) Technology Stone is by far the most common resi- due of prehistoric cultural behavior. For this reason, archaeologists have long been keenly interested in this material.

When struck properly, certain types of stone will fracture in a controlled way; these nodules are called blanks. The smaller piece that comes off is called a flake, while the larger remain- ing chunk is called a core (Fig. 9-8). Both core and flake have sharp edges that are useful for cutting, sawing, or scraping. The earliest hominin cul- tural inventions probably used non- durable materials that didn’t survive archaeologically (such as digging sticks

or ostrich eggshells used as watertight containers). Still, a basic human inven- tion was the recognition that stone can be fractured to produce sharp edges.

For many years, it’s been assumed that in the earliest known stone tool industry (that is, the Oldowan), both core and flake tools were deliberately manufactured as final, desired prod- ucts. Such core implements as “chop- pers” were thought to be central arti- factual components of these early lithic assemblages (in fact, the Oldowan is often depicted as a “chopping tool industry”). However, detailed reevalua- tion of these artifacts has thrown these traditional assumptions into doubt. By carefully analyzing the attributes of Oldowan artifacts from Olduvai, Potts (1991, 1993) concluded that the so-called core tools really weren’t tools after all. He suggests instead that early hominins were deliberately produc- ing flake tools, and the various stone choppers were simply “incidental stop- ping points in the process of removing flakes from cores” (Potts, 1993, p. 60). As Potts concludes, “The flaked stones of the Oldowan thus cannot be dem- onstrated to constitute discrete target designs, but can be shown to represent simple by-products of the repetitive act of producing sharp flakes” (Potts, 1993, pp. 60–61).

Breaking rocks by bashing them together is one thing. Producing con- sistent results, even apparently simple flakes, is quite another. You might want to give it a try, just to appreciate how difficult making a stone tool can be. It takes years of practice before modern stone knappers learn the intricacies— the type of rock to choose, the kind of hammer to employ, the angle and velocity with which to strike, and so on. Such experience allows us to appreciate how skilled in stoneworking our ances- tors truly were.

Flakes can be removed from cores in various ways. The object in making a tool, however, is to produce a usable cutting surface. By reproducing results similar to those of earlier stoneworkers, experimental archaeologists can infer

▲�Figure 9-8 Flake and core.

flake core

blanks In archaeology, stones suitably sized and shaped to be further worked into tools.

flake a thin-edged fragment removed from a core.

core a stone reduced by flake removal. a core may or may not itself be used as a tool.

lithic (lith, meaning “stone”) referring to stone tools.

knappers people (frequently archae- ologists) who make stone tools.

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Experimental Archaeology 269

which kinds of techniques might have been employed.

For example, the nodules (now thought to be blanks) found in sites in Bed I at Olduvai (circa 1.85 to 1.2 mya) are flaked on one side only (that is, uni- facially). It’s possible, but by no means easy, to produce such implements by hitting one stone—the hammer- stone—against another—the core—in a method called direct percussion (Fig. 9-9).

However, in later sites, particularly well studied at Olduvai (circa 400,000 ya*), most of the tools are flaked on both sides (that is, bifacially) and have long rippled edges. Such a result can’t be reproduced by direct percus- sion with just a hammerstone. The edges must have been straightened (“retouched”) with a “soft” hammer, such as bone or antler.

Reproducing implements similar to those found in later stages of human cultural development calls for even more sophisticated techniques. Tools such as the delicate microliths found in the uppermost beds at Olduvai (circa 17,000 ya), the superb Solutrean blades from Europe (circa 20,000 ya), and the expertly crafted Folsom projec- tile points from the New World (circa 10,000 ya) all require a mastery of stone matched by few knappers today.

To reproduce implements like those just mentioned, the knapper must remove extremely thin flakes. This can be done only through pressure flaking—for example, using a pointed piece of bone, antler, or hard wood and pressing firmly against the stone (Fig. 9-10).

Once the tools were manufactured, our ancestors used them in ways that we can infer through further experi- mentation. For example, archaeologists from the Smithsonian Institution suc- cessfully butchered an entire elephant (which had died in a zoo) using stone tools they had made for that purpose (Park, 1978). Other archaeologists have

* y.a. = years ago

cut down (small) trees using stone axes they had made.

Ancient tools themselves may carry telltale signs of how they were used. Lawrence Keeley performed a series of experiments in which he manufac- tured flint tools and then used them in diverse ways—whittling wood, cutting bone, cutting meat, and scraping skins. Viewing these implements under a microscope at fairly high magnification revealed patterns of polishes, striations, and other kinds of microwear. What’s most intriguing is that these patterns varied depending on how the tool was used and which material was worked. For example, Keeley was able to distin- guish among tools used on bone, ant- ler, meat, plant materials, and hides. In the last case, he was even able to deter- mine if the hides were fresh or dried! Orientations of microwear mark- ings also give some indication of how the tool was used (such as for cutting or scraping). Because these experi- ments into stone tool manufacture and use reveal valuable information about variations in microwear mor- phology, researchers are able to use the experimentally produced data to make inferences about specific stone tool usage in the past. For example, the 9,000-year-old Paleo-Indian flake from Nebraska shown in Figure 9-11 shows microwear polish from cutting antler or bone. Evidence of microwear polish has been examined on even the extremely early hominin stone tools from Koobi Fora (East Lake Turkana), in Kenya (Keeley and Toth, 1981).

Advances in tool use studies include the application of scanning electron microscopy (SEM). Working at 10,000× magnification, researchers have found that the edges of stone implements sometimes retain plant fibers and amino acids as well as nonorganic resi- dues, including phytoliths. Because phytoliths produced by different plant species are distinctive, there is good potential for identifying the botanical materials that came in contact with the tool during its use (Rovner, 1983). Such work is most exciting; for the first time,

▲�Figure 9-9 Direct percussion.

▲�Figure 9-10 Pressure flaking.

direct percussion Striking a core or flake with a hammerstone.

microliths (micro, meaning “small,” and lith, meaning “stone”) Small stone tools usually produced from narrow blades punched from a core; found especially in africa during the latter part of the pleistocene.

pressure flaking a method of removing flakes from a core by pressing a pointed implement (e.g., bone or antler) against the stone.

microwear polishes, striations, and other diagnostic microscopic changes on the edges of stone tools.

phytoliths (phyto, meaning “hidden,” and lith, meaning “stone”) Microscopic silica structures formed in the cells of many plants, particularly grasses.

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chapter 9 Paleoanthropology: Reconstructing Early Hominin Behavior and Ecology 270

we may be able to make definite state- ments concerning the uses of ancient tools. In addition, phytoliths have also been found in the dental calculus (i.e., plaque) on some Neandertal teeth as well as recently on 2-million-year-old hominins from South Africa (Henry et al., 2012). The findings for the early African hominins provided quite a sur- prise (see Chapter 10).

Analysis of Bone Experimental archaeologists are also interested in the ways in which bone is altered by human and natural forces. Other scientists are vitally concerned with this process as well; in fact, it has produced an entire new branch of paleoecology—taphonomy. Taphono- mists have carried out comprehensive research on how natural factors influ- ence bone deposition and preserva- tion. In South Africa, C. K. Brain col- lected data on contemporary African butchering practices, carnivore (dog) disturbances of carcasses, and so forth and then correlated these factors with the kinds and numbers of elements usually found in bone accumulations (Brain, 1981). In this way, he was able to account for the accumulation of most of the bones in South African cave sites. Likewise, in East African game parks, observations have been made on decaying animals to measure the effects of weathering, predator chew- ing, and trampling (Behrensmeyer et al., 1979; Perkins, 2003).

Further insight into the many ways bone is altered by natural factors has come from experimental work in the laboratory (Boaz and Behrensmeyer, 1976). In an experiment conducted at the University of California, Berkeley, human bones were put into a running- water trough. Researchers observed how far the water carried different pieces and recorded how much and what kind of damage was done. Such information is extremely useful in interpreting early hominin sites. For example, the distribution of hominin

fossils at Olduvai suggests that active water transport was less prevalent there than in the Omo River Valley in southern Ethiopia.

Detailed examination of bones may also provide evidence of butcher- ing and bone breakage by hominins, including cut and percussion marks left by stone tools. Great care must be taken to distinguish marks left on bone by carnivore or rodent gnawing, weathering processes, hoof marks, or even normal growth. High magnifica- tion of a cut made by a stone tool may reveal a minutely striated and rough- ened groove scored into the bone’s sur- face. Many such finds have been recog- nized at early hominin sites, including Olduvai Gorge (Bunn, 1981; Potts and Shipman, 1981). (See “A Closer Look,” pp. 260–261.)

Reconstruction of Early Hominin Environments and Behavior

Now that we’ve reviewed the many methods used by paleoanthro- pologists to collect their varied data, we can look at the intriguing ways in which this information is interpreted. Be aware that much of this interpreta- tion is quite speculative and less ame- nable to scientific verification than more concrete sources of data (for example, that relating to dating, geol- ogy, or hominin anatomy). (In Chap- ter 1, we discussed how hypotheses are developed and tested by scientists, noting the requirement that scientific explanations be falsifiable.)

Paleoanthropologists are keenly interested not just in how early hom- inins evolved but also in why the process occurred the way it did. Accordingly, they frequently use the data available as a basis for broad, spec- ulative scenarios that try to explain both early hominin adaptations to a

▲�Figure 9-11 Photomicrograph (200x) showing polish resulting from bone modification on a 9,000-year-old stone tool excavated from the O. V. Clary site in Nebraska by Dr. M.G. Hill, of Iowa State University.

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Reconstruction of Early Hominin Environments and Behavior 271

changing environment and the new behaviors that these hominins adopted. Such scenarios are fascinating, and paleoanthropologists enjoy construct- ing them (and certainly many in the general public enjoy reading them). Without doubt, for scientists and lay- persons alike, our curiosity inevitably leads to intriguing and sweeping gener- alizations. Still, in the following discus- sion, we’ll focus on what is known from the paleoanthropological record itself and separate that from the more spec- ulative conclusions. You, too, should evaluate these explanations with a crit- ical eye and try to identify the empiri- cal basis for each type of reconstruc- tion. It’s important not to accept a scenario merely because it’s appeal- ing (often because it’s simple) or just because it seems plausible. We must always ask ourselves what kinds of evi- dence support a particular contention, how generally the explanation fits the evidence (that is, how consistent it is with different types of data from var- ied sources), and what types of new evidence might either help to verify or potentially falsify the interpretation.

Why Did Hominins Become Bipedal? As we’ve noted several times, the adap- tation of hominins to bipedal locomo- tion was the most fundamental adap- tive shift among the early members of our lineage. But what were the fac- tors that initiated this crucial change? Ecological theories have long been thought to be central to the develop- ment of bipedalism. Clearly, howev- er, environmental influences would have to have occured before evidence of well-adapted bipedal behavior could appear. In other words, the major shift would have been at the end of the Mio- cene. Although the evidence indicates that no sudden wide ecological change took place at that time, locally forests probably did become patchier as rain- fall became more seasonal. Given the changing environmental conditions,

did hominins come to the ground to seize the opportunities offered in these more open habitats? Did bipedalism quickly ensue, stimulated somehow by this new way of life? At a very general level, the answer to these questions is yes. Obviously, hominins did at some point become bipedal, and this adap- tation took place on the ground. Like- wise, hominins are more adapted to mixed and open-country habitats than are our closest modern ape cousins. Successful terrestrial bipedalism prob- ably made possible the further adapta- tion to more arid, open-country ter- rain. Still, this rendition simply tells us where hominins found their niche, not why.

As always, it’s wise to be cautious in speculating about causation in evo- lution. It is all too easy to draw super- ficial conclusions. For example, sci- entists often surmise that the mere availability of ground niches (and per- haps that there were no direct competi- tors for them) inevitably led the earli- est hominins to terrestrial bipedalism. But consider this: Plenty of mamma- lian species, including some nonhu- man primates, also live mostly on the ground in open country—and they aren’t bipedal. Clearly, beyond such simplistic environmental generaliza- tions, some more complex explanation for hominin bipedalism is required. There must have been something more than just an environmental opportu- nity to explain this adaptation to such a unique lifestyle.

Another issue sometimes over- looked in the discussion of early hom- inin bipedal adaptation is that these creatures did not suddenly become completely terrestrial; but they also didn’t slouch about, as illustrations of a linear progression of human evo- lution would suggest. We know, for example, that all terrestrial species of nonhuman primates (including savan- na baboons, hamadryas baboons, and patas monkeys; see Chapter 7) regu- larly seek out safe sleeping sites off the ground. These safe havens help

chapter 9 Paleoanthropology: Reconstructing Early Hominin Behavior and Ecology 272

protect against predation and are usually found in trees or on cliff faces. Likewise, early hominins almost cer- tainly sought safety at night in the trees, even after they became well adapted to terrestrial bipedalism dur- ing daytime foraging. What’s more, the continued opportunities for feed- ing in the trees would most likely have remained significant to early homi- nins well after they were also utilizing ground-based resources.

Various hypotheses explaining why hominins initially became bipedal have been suggested and are summarized in Table 9.2. The primary influences claimed to have stimulated the shift to bipedalism include acquiring the abil- ity to carry objects (and offspring), hunting on the ground, gathering of seeds and nuts, feeding from bushes, improved thermoregulation (that is, keeping cooler on the open savanna), having a better view of open country (to spot predators), walking long dis- tances, and provisioning by males of females with dependent offspring.

These are all creative scenarios, but once again they’re not very conducive to rigorous testing and verification. Still, two of the more ambitious sce- narios proposed by Clifford Jolly (1970) and Owen Lovejoy (1981) deserve fur- ther mention. Both of these views sought to link several aspects of early hominin ecology, feeding, and social behavior and both utilized models derived from studies of contemporary nonhuman primates.

Jolly’s seed-eating hypothesis used the feeding behavior and ecology of gelada baboons as an analogy for very early hominins. Seed eating is an activ- ity that requires keen hand-eye coor- dination, with presumed bipedal shuffling potentially improving the efficiency of foraging. In this view, early hominins are hypothesized to have adapted to open country and bipedal- ism as a result of their primary adap- tation to eating seeds and nuts (found on the ground). The key assumption is that early hominins were eating seeds acquired in similar ecological condi-

tions to those of contemporary gelada baboons.

Lovejoy, meanwhile, has combined presumed aspects of early hominin ecology, feeding, pair bonding, infant care, and food sharing to devise his creative scenario. This view hinges on these assumptions: (1) that the earli- est hominins had offspring at least as K-selected (see Chapter 7) as other large-bodied hominoids; (2) that hom- inin males ranged widely and provi- sioned females and their young, who remained more tied to a “home base”; and (3) that males were paired monog- amously with females.

As we’ve noted, while not strictly testable, such scenarios do make cer- tain predictions that can be potentially falsified or upheld. Accordingly, aspects of each scenario can be evaluated in light of more specific data (obtained from the paleoanthropological record). Regarding the seed-eating hypoth- esis, predictions relating to the size of the back teeth in most early homi- nins are met, but the proportions of the front teeth in many forms aren’t what we’d expect to see in a committed seed eater. Besides, the analogy with gelada baboons is not as informative as once thought; these animals actually don’t eat that many seeds and certainly aren’t habitual bipeds. Finally, many of the characteristics that Jolly suggested were restricted to hominins (and geladas) are also found in several late Miocene hom- inoids (who weren’t hominins—nor obviously bipeds). Thus, regarding the seed-eating hypothesis, the proposed dental and dietary adaptations don’t appear to be linked specifically to hom- inin origins or bipedalism.

Further detailed analyses of data have also questioned crucial ele- ments of Lovejoy’s male-provisioning scenario. The evidence that appears to most contradict this view is that all early hominins were quite sexu- ally dimorphic (McHenry, 1992). According to Lovejoy’s model (and analogies with contemporary monoga- mous nonhuman primates such as gib- bons), there shouldn’t be such dramatic

Reconstruction of Early Hominin Environments and Behavior 273

Table 9.2 Possible Factors Influencing the Initial Evolution of Bipedal Locomotion in Hominins

Factor Speculated Influence Comments

Upright posture freed the arms to carry various objects (including offspring).

Bipedalism allowed carrying of weap- ons, more accurate throwing of certain weapons, and improved long-distance walking.

Feeding on seeds and nuts occurred while standing upright.

Upright posture provided access to seeds, berries, etc., in lower branches; analogous to adaptation seen in some specialized antelope.

Vertical posture exposes less of the body to direct sun; increased distance from ground facilitates cooling by increased exposure to breezes.

Standing up provided better view of surrounding countryside (view of poten- tial predators as well as other group members).

Covering long distances was more effi- cient for a biped than for a quadruped (during hunting or foraging); mechani- cal reconstructions show that bipedal walking is less energetically costly than quadrupedalism (this is not the case for bipedal running).

Males carried back resources to dependent females and young.

Charles Darwin emphasized this view, particularly relating to tools and weapons; how ever, evidence of stone tools is found much later in the record than first evidence of bipedalism.

Systematic hunting is now thought not to have been practiced until after the origin of bipedal hominins.

Model initially drawn from analogy with gelada baboons (see text).

Climbing adaptation already existed as prior ancestral trait in earliest hominins (i.e., bush and tree feeding already was established prior to bipedal adaptation).

Works best for animals active midday on savanna; moreover, adaptation to bipedalism may have initially occurred in woodlands, not on savanna.

Behavior seen occasionally in terres- trial primates (e.g., baboons); probably a contributing factor, but unlikely as “prime mover.”

Same difficulties as with hunting explanation; long-distance foraging on ground also appears unlikely adapta- tion in earliest hominins.

Monogamous bond suggested; however, most skeletal data appear to falsify this part of the hypothesis (see text).

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Carrying (objects, tools, weapons, infants)

Hunting

Seed and nut gathering

Feeding from bushes

Thermoregulation (cooling)

Visual surveillance

Long-distance walking

Male provisioning

chapter 9 Paleoanthropology: Reconstructing Early Hominin Behavior and Ecology 274

differences in body size between males and females. Recent studies (Reno et al., 2003, 2005) have questioned this conclusion regarding sexual dimor- phism, suggesting, at least for one spe- cies (Australopithecus afarensis), that it was only very moderate. Further evalu- ation of another, even earlier hominin (Ardipithecus) has led Lovejoy to con- tinue to forcefully argue for his male- provisioning model (Lovejoy, 2009). From a wider perspective, these con- clusions appear at odds with most of the evidence regarding early homi- nins. What’s more, the notions of food sharing (presumably including con- siderable meat), home bases, and long- distance provisioning are questioned by more controlled interpretations of the archaeological record.

Another imaginative view is also rel- evant to this discussion of early hom- inin evolution, since it relates the adap- tation to bipedalism (which was first) to increased brain expansion (which came later). This interpretation, pro- posed by Dean Falk, suggests that an upright posture put severe constraints on brain size (since blood circulation and drainage would have been altered and cooling would consequently have been more limited than in quadru- peds). Falk thus hypothesizes that new brain-cooling mechanisms must have coevolved with bipedalism; this view is articulated in what she calls the “radia- tor theory” (Falk, 1990). Falk further surmises that the requirement for bet- ter brain cooling would have been par- ticularly marked as hominins adapted to open-country ground living on the hot African savanna. Another inter- esting pattern observed by Falk con- cerns two varying cooling adaptations found in different early hominin spe- cies. She thus suggests that the type of “radiator” adapted in the genus Homo was particularly significant in reduc- ing constraints on brain size—which

presumably limited some other early hominins. The radiator theory works well, since it helps to explain not only the relationship of bipedalism to later brain expansion but also why only some hominins became dramatically encephalized.

The radiator theory, too, has been criticized by some paleoanthropolo- gists. Most notably, the presumed spe- cies distinction concerning varying cooling mechanisms is not as obvi- ous as suggested by the hypothesis. Both types of venous drainage systems can be found in contemporary Homo sapiens as well as within various early hominin species (that is, the varia- tion is intraspecific, not just interspe- cific). Indeed, in some early hominin specimens, both systems can be found in the same individual (expressed on either side of the skull). Besides, as Falk herself has noted, the radiator itself didn’t lead to larger brains; it simply helped reduce constraints on increased encephalization among hominins. It thus requires some further mechanism (prime mover) to explain why, in some hominin species, brain size increased the way it did.

As with any such ambitious effort, it’s all too easy to find holes. Falk aptly reminds us that “the search for such ‘prime movers’ is highly spec- ulative, and these theories do not lend themselves to hypothesis test- ing” (Falk, 1990, p. 334). Even so, the attempt to interrelate various lines of evidence, the use of contemporary primate models, and predictions con- cerning further evidence obtained from paleoanthropological contexts all conform to sound scientific meth- odology. All the views discussed here have contributed to this venture— one not just aimed at understanding our early ancestors but also seeking to refine its methodologies and scientific foundation.

275Media Resources

This entire chapter is all about how we can learn about the age, behavior, and environments of our early hom- inin relatives. Briefly, we know the ages of most impor- tant sites by using an array of precise dating tech- niques. Artifacts, fossil animals, and early hominins themselves are recovered and recorded using con- trolled archaeological methods. How tools were made and used is discovered through experimentation in

stone tool manufacture as well as the chemical study of plant residues left on tools, and early hominin diets can be revealed through chemical analysis of fossil teeth. Finally, the key hominin adaptation to bipedal loco- motion can be explained by a variety of hypotheses. These are less secure and show how science continu- ally refines its approach and tests ideas to make con- clusions more rigorous.

How Do We Know?

▶▶ The most important subfields of paleoanthropol- ogy are geology, paleontology, archaeology, and physical anthropology.

▶▶ The two types of dating techniques are relative dating and chronometric dating. Stratigraphy and paleomagnetism are the two most impor- tant examples of relative dating; potassium-argon dating and radiocarbon (14C) dating are the most important examples of chronometric dating.

▶▶ The first stone tools thus far discovered date to about 2.6 mya. These tools include mostly simple flake implements and the discarded cores from which they were struck.

▶▶ Bipedal locomotion is thought to have been signif- icantly influenced by one or more of the following: carrying objects, seed gathering or feeding from bushes, visual spotting of predators, and long- distance walking (the latter coming more recently in human evolution).

Summary of Main Topics

1. You are leading a paleoanthropological expedition aimed at discovering an early hominin site dating to the Pliocene. In what part of the world will you pick your site, and why? After selecting a particu- lar region, how will you identify which area(s) to survey on foot?

2. Why is it important to have accurate dates for paleoanthropological localities? Why is it nec- essary to use more than one kind of dating technique?

3. What do we mean when we say that early homi- nins displayed cultural behavior? What types of behavior do you think this would have included?

(Imagine that you’ve been transported back in time by a time machine, and you’re sitting in a tree watching a group of hominins at Olduvai Gorge 1.5 mya.)

4. Now put yourself in the same place, this time lead- ing an archaeological excavation. What would be left for you to detect of the cultural behavior you observed in question 3? What happened to the remainder of this behavioral repertoire?

5. What do we mean when we say that human evolu- tion is biocultural? How do paleoanthropologists investigate early hominins using such a biocultural perspective?

Critical Thinking Questions

Video See the video “Olduvai Gorge, Tanzania”

to learn more about topics covered in this chapter. Login to your Anthropology CourseMate at www.cengagebrain.com to access videos.

Media Resources

The first more human-like animals (hominins) appeared in Africa around 6 mya ago

and evolved into a variety of different species.

Connections

Paleoanthropology, which includes physical anthropology, archaeol- ogy, and geology, pro-

vides the scientific basis to understand hominin

evolution.

Hominins began to dis- perse out of Africa around 2 million years ago, and during the next 1 million years inhabited much of

Eurasia.

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After mastering the material in this chapter, you should be able to:

▶ �Discuss why Africa is so central to the study of the earliest hominins and describe which portions of the continent have yielded hominin fossil remains.

▶ �Explain why evidence of bipedal locomotion is so important in the study of fossil hominins and describe the basic mechanics of bipedal locomotion.

▶ �Discuss what specific features indicate adaptation to bipedal locomotion and which fossil hominins display these features.

▶ �Describe the three major groups of early hominins discussed in this chapter.

▶ �Specifically, compare and contrast the earliest (possible) hominins (i.e., Sahelanthropus, Orrorin, and Ardipithecus). Also, explain why (or why not) you think they are hominins.

▶ �Explain why we say that australopiths are diverse and some are more derived than others.

▶ �Describe what is considered the earliest evidence of the genus Homo, where and when these hominins lived, and what all this tells us about human evolution.

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Our species today dominates earth because we use our brains and cultural inventions to invade every corner of the planet. Yet, around 5 million years ago, our ancestors were little more than bipedal apes, confined to a few regions in Africa. What were these creatures like? When and how did they begin their evolutionary journey?

In Chapter 9, we discussed the tech- niques paleoanthropologists use to locate and excavate sites, as well as the multidisciplinary approaches used to interpret discoveries. In this chapter, we turn to the physical evidence of the hominin fossils themselves. The earliest fossils identifiable as hominins are all from Africa. They date from as early as 6+ mya; after 4 mya, varieties of these early hominins become more plentiful and widely distributed in Africa. It’s fas- cinating to think about all these quite primitive early members of our fam- ily tree living side by side for millions of years, especially when we also try to figure out how they managed to coexist with their different adaptations. Most of these species became extinct. Why? And were some of these apelike animals possibly our direct ancestors?

Hominins, of course, evolved from earlier primates (dating from the Eocene to late Miocene), and in Chapter 8 we discussed the fossil evi- dence of prehominin primates. These fossils provide us with a context within which to understand the subsequent evolution of the human lineage. In recent years, paleoanthropologists

10 Hominin Origins in Africa

from several countries have been exca- vating sites in Africa, and many excit- ing new finds have been uncovered. However, because many such disover- ies are so recent, detailed evaluations are still in progress, and conclusions must remain tentative.

One thing is certain, however. The earliest members of the human lineage were confined to Africa. Only much later did their descendants disperse from the African continent to other areas of the Old World. (This “out of Africa” saga will be the topic of the next chapter.)

Student Learning Objectives

chapter 10 Hominin Origins in Africa 278

Walking the Walk: The Bipedal Adaptation

In our overview in Chapter 9 of behavioral reconstructions of early hominins, we highlighted several hypotheses that attempt to explain why bipedal locomotion first evolved in the hominins. Here we turn to the spe- cific anatomical (that is, morphologi- cal) evidence showing us when, where, and how hominin bipedal locomotion evolved. From a broader perspective, we’ve noted a tendency in all primates for erect body posture and some biped- alism. Of all living primates, how- ever, efficient bipedalism as the pri- mary (habitual) form of locomotion is seen only in hominins. Function- ally, the human mode of locomotion is most clearly shown in our striding gait, where weight is alternately placed on a single fully extended hind limb. This specialized form of locomotion has developed to a point where energy levels are used to near peak efficiency. Our manner of bipedal locomotion is a far cry from what we see in nonhuman primates, who move bipedally with hips and knees bent and maintain bal- ance clumsily and inefficiently, totter- ing along rather than striding.

From a survey of our close primate relatives, it’s apparent that while still in the trees, our ancestors were adapted to a fair amount of upper-body erect- ness. Prosimians, monkeys, and apes all spend considerable time sitting erect while feeding, grooming, or sleeping. Presumably, our early ancestors dis- played similar behavior. What caused these forms to come to the ground and embark on the unique way of life that would eventually lead to humans is still a mystery. Perhaps natural selec- tion favored some Miocene hominoids coming occasionally to the ground to forage for food on the forest floor and forest fringe. In any case, once they were on the ground and away from the immediate safety offered by trees, bipedal locomotion could become a tremendous advantage. (For a discus-

sion of some specific hypotheses that have tried to explain the early evolution of bipedal locomotion, see Chapter 9.)

The Mechanics of Walking on Two Legs Our mode of locomotion is indeed extraordinary, involving, as it does, a unique kind of activity in which “the body, step by step, teeters on the edge of catastrophe” (Napier, 1967, p. 56). In this way, the act of human walking is the act of almost falling repeatedly! The problem is to maintain balance on the “stance” leg while the “swing” leg is off the ground. In fact, during normal walking, both feet are simultaneously on the ground only about 25 percent of the time, and this figure becomes even less as we walk (or run) faster.

Maintaining a stable center of bal- ance in this complex form of locomo- tion calls for many drastic structural/ anatomical alterations in the basic pri- mate quadrupedal pattern. The most dramatic changes are seen in the pel- vis. The pelvis is composed of three elements: two hip bones, or ossa coxae (sing., os coxae), joined at the back to the sacrum (Fig. 10-1). In a quadru- ped, the ossa coxae are vertically elon- gated bones positioned along each side of the lower portion of the spine and oriented more or less parallel to it. In hominins, the pelvis is comparatively much shorter and broader and extends around to the side (Fig. 10-2). This configuration helps to stabilize the line of weight transmission in a bipedal posture from the lower back to the hip joint (Fig. 10-3).

Several consequences resulted from the remodeling of the pelvis during early hominin evolution. Broadening the two sides and extending them around to the side and front of the body produced a basin-shaped struc- ture that helps support the abdominal organs (pelvis means “basin” in Latin). These alterations also repositioned the attachments of several key muscles that act on the hip and leg, changing their mechanical function. Probably morphological pertaining to the

form and structure of organisms.

Left os coxae

Sacrum

Right os coxae

▲�Figure 10-1 The human pelvis: various elements shown on a modern skeleton.

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Walking the Walk: The Bipedal Adaptation 279

the most important of these altered relationships is that involving the glu- teus maximus, the largest muscle in the body, which in humans forms the bulk of the buttocks. In quadrupeds, the gluteus maximus is positioned to the side of the hip and functions to pull the thigh to the side and away from the body. In humans, this muscle is posi- tioned behind the hip; this arrange- ment allows it, along with the ham- strings, to extend the thigh, pulling it to the rear during walking and running (Fig. 10-4). The gluteus maximus is a truly powerful extensor of the thigh and provides additional force, particu- larly during running and climbing.

Modifications also occurred in other parts of the skeleton because of the shift to bipedalism. The most significant of these, summarized in “A Closer Look: Major Features of Bipedal Locomotion,” (pp. 280–281) include (1) repositioning of the foramen magnum, the opening at the base of the skull through which the spinal cord emerges; (2) the addition of spinal curves which help to trans- mit the weight of the upper body to the hips in an upright posture; (3) shorten- ing and broadening of the pelvis and the stabilization of weight transmis- sion (discussed earlier); (4) lengthen- ing of the hind limb, thus increasing stride length; (5) angling of the femur (thighbone) inward to bring the knees and feet closer together under the

body; and (6) several structural chang- es in the foot, including the develop- ment of a longitudinal arch and realign- ment of the big toe in parallel with the other toes (that is, making it no longer divergent).

As you can appreciate, the evolu- tion of hominin bipedalism required complex anatomical reorganization. For natural selection to produce ana- tomical change of the magnitude seen in hominins, the benefits of bipedal locomotion must have been significant indeed! We mentioned in Chapter 9 several possible adaptive advantages

Ilium

Pubis Ischium

▲�Figure 10-2 The human os coxae, com- posed of three bones (right side shown).

▼�Figure 10-3 Ossa coxae. (a) Homo sapiens. (b) Early hominin (australopith) from South Africa. (c) Great ape. Note especially the length and breadth of the iliac blade (boxed) and the line of weight transmission (shown in red).

(b) Chimpanzee

Ilium

Gluteus maximus

Hip joint

(a) Human

Knee

Hamstrings

a b

▼�Figure 10-4 Comparisons of important muscles that act to extend the hip. Note that the attachment surface (origin, shown in black) of the gluteus maximus in humans (a) is farther in back of the hip joint than in a chimpanzee standing bipedally (b). Conversely, in chimpanzees, the ham- strings are farther in back of the knee.

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that bipedal locomotion may have con- ferred upon early hominins. But these all remain hypotheses (since they can’t be tested, they could more accurately be called scenarios), and we have inad- equate data for testing the various pro- posed models.

Still, given the anatomical altera- tions required for efficient bipedalism, some major behavioral stimuli must have influenced its development. When

they interpret evolutionary history, biologists are fond of saying that form follows function. In other words, dur- ing evolution, organisms don’t undergo significant reorganization in struc- ture unless these changes—over many generations—assist individuals in some functional capacity (and in so doing increase their reproductive success). Such changes didn’t necessarily occur all at once, but probably evolved over a

Major Features of Bipedal Locomotion

A Closer Look

During hominin evolution, several major structural features through- out the body have been reorganized (from those seen in other pri- mates), facilitating efficient bipedal locomotion. These are illustrated here, beginning with the head and progressing to the foot: (a) The foramen magnum (shown in blue) is repositioned farther underneath

the skull, so that the head is more or less balanced on the spine (and thus requiring less robust neck muscles to hold the head upright). (b) The spine has two distinctive curves—a backward (thoracic) one and a forward (lumbar) one—that keep the trunk (and weight) centered above the pelvis. (c) The pelvis is shaped more in the

Human Great ape

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Walking the Walk: The Bipedal Adaptation 281

fairly long period of time. Even so, once behavioral influences initiated certain structural modifications, the process gained momentum and proceeded irreversibly.

We say that hominin bipedalism is both habitual and obligate. By habitual bipedalism, we mean that hominins, unlike any other primate, move bipedally as their standard and most efficient mode of locomotion. By

obligate bipedalism, we mean that hominins are committed to bipedal- ism and cannot locomote efficiently in any other way. For example, the loss of grasping ability in the foot makes climbing much more difficult for humans (although by no means impos- sible). The central task, then, in try- ing to understand the earliest members of the hominin lineage is to identify anatomical features that indicate

form of a basin to support internal organs; the ossa coxae (specifi- cally, the iliac blades) are also shorter and broader, thus stabilizing weight transmission. (d) The lower limbs are elongated, as shown by the proportional lengths of various body segments (for example, in humans the thigh comprises 20 percent of body height, while in

gorillas it comprises only 11 percent). (e) The femur is angled inward, keeping the legs more directly under the body; modified knee anat- omy also permits full extension of this joint. (f) The big toe is enlarged and brought in line with the other toes; a distinctive longitudinal arch also forms, helping to absorb shock and adding propulsive spring.

Human

Great ape

Human Great ape

9.4% 58.6%

20%

9.2%

2.8% 2.6%

15.5% 4.4%

11%

66.5%

habitual bipedalism Bipedal loco- motion as the form of locomotion shown by hominins most of the time.

obligate bipedalism Bipedalism as the only form of hominin terrestrial locomo- tion. Since major anatomical changes in the spine, pelvis, and lower limb are required for bipedal locomotion, once hominins adopted this mode of locomotion, other forms of locomotion on the ground became impossible.

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chapter 10 Hominin Origins in Africa 282

bipedalism and to interpret to what degree these organisms were commit- ted to this form of locomotion (that is, was it habitual and was it obligate?).

What structural patterns are observ- able in early hominins, and what do they imply regarding locomotor func- tion? By at least 4 mya, all the major structural changes required for biped- alism are seen in early hominins from Africa (at least as far as the evidence permits conclusions to be drawn). In particular, the pelvis, as clearly docu- mented by several excellently preserved specimens, was dramatically remodeled

to support weight in a bipedal stance (see Fig. 10-3b).

Other structural changes shown after 4 mya in the

earliest relatively com- plete hominin postcra-

nial remains further confirm the pattern seen in the pelvis. For example, the vertebral column (as known from speci- mens in East and

South Africa) shows the same curves as in

modern hominins. The lower limbs are also elon-

gated, and they seem to be proportionately about as long

as in modern humans (although the arms are longer in these early hom- inins). Further, the angle of weight sup- port from the hip to the knee is very similar to that seen in Homo sapiens.

Fossil evidence of early hominin foot structure has come from two sites in South Africa; especially important are some fossils from Sterkfontein (Clarke and Tobias, 1995). These speci- mens, consisting of four articulating elements from the ankle and big toe, indicate that the heel and longitudi- nal arch were both well adapted for a bipedal gait. But the paleoanthropolo- gists (Ron Clarke and Phillip Tobias) who analyzed these remains also sug- gest that the large toe was divergent, unlike the hominin pattern shown in “A Closer Look: Major Features of Bipedal Locomotion.” If the large toe

really did possess this anatomical posi- tion (and this is disputed), it most likely would have aided the foot in grasp- ing. In turn, this grasping ability (as in other primates) would have enabled early hominins to more effectively exploit arboreal habitats. Finally, since anatomical remodeling is always con- strained by a set of complex functional compromises, a foot highly capable of grasping and climbing is less useful as a stable platform during bipedal loco- motion. Some researchers therefore see early hominins as perhaps not quite as fully committed to bipedal locomotion as were later hominins.

Further evidence for evolutionary changes in the foot comes from two sites in East Africa where numerous fossilized elements have been recov- ered (Fig. 10-5). As in the remains from South Africa, the East African fossils suggest a well-adapted bipedal gait. The arches are developed, but some differences in the ankle also imply that considerable flexibility was possible (again, probably indi- cating some continued adaptation to climbing). From this evidence some researchers have concluded that many forms of early hominins probably spent considerable time in the trees. What’s more, they may not have been quite as efficient bipedally as has previously been suggested. Nevertheless, most researchers maintain that early homi- nins from Africa displayed both habit- ual and obligate bipedalism (despite the new evidence from South Africa and the earliest traces from central and East Africa, all of which will require further study).

Digging for Connections: Early Hominins from Africa

As you are now well aware, a variety of early hominins lived in Africa, and we’ll cover their comings and goings over a 5-million-year period, from at least 6 to 1 mya. It’s also impor-Sterkfontein (sterk´-fawn-tane)

▲ Figure 10-5 A nearly complete hominin foot (OH 8) from Olduvai Gorge, Tanzania. (See Appendix C on the Anthropology CourseMate at Cengagebrain.com for an explanation of how specimen numbers such as OH 8 are assigned.)

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Pre-Australopiths (6.0+ to 4.4 mya) 283

tant to keep in mind that these homi- nins were geographically widely dis- tributed, with fossil discoveries coming from central, East, and South Africa (Fig. 10-8 on p. 284). Paleoanthropolo- gists generally agree that there were at least six different genera among these early African fossils, which in turn comprised upward of 13 different spe- cies. At no time, in no other place were hominins ever as diverse as these very ancient members of our family tree. As you’ll see in a minute, some of the ear- liest fossils thought by many research- ers to be hominins are primitive in some ways and unusually derived in others. In fact, some paleoanthropolo- gists remain unconvinced that they are really hominins.

As you’ve already guessed, there are quite a few different fossils from many sites; their formal naming can be dif- ficult to pronounce and not easy to remember. So we’ll try to discuss these fossil groups in a way that’s easy to understand. Our primary focus will be to organize them by time and by major evolutionary trends. In so doing, we recognize three major groups:

• Pre-australopiths—the earliest and most primitive (possible) hominins (6.0+ to 4.4 mya)

• Australopiths—diverse forms, some more primitive, others highly derived (4.2 to 1.2 mya)

• Early Homo—the first members of our genus (2.0+ to 1.4 mya)

Pre-Australopiths (6.0+ to 4.4 mya)

The oldest and most surprising of these earliest hominins is rep- resented by a cranium discovered at a central African site called Toros- Menalla in the modern nation of Chad (Brunet et al., 2002) (Fig. 10-6). Pro- visional dating using faunal correla- tion (biostratigraphy) suggests a date of between 7 and 6 mya (Vignaud et al., 2002). Closer examination of the evidence used in obtaining this bio- stratigraphic date now has led many

paleoanthropologists to suggest that the later date (6 mya) is more likely.

The morphology of the fossil is unusual, with a combination of characteristics unlike that found in other early hominins. The brain- case is small, estimated at no larger than a modern chimpanzee’s (prelimi- nary estimate in the range of 320 to 380 cm³), but it is massively built, with huge brow ridges in front, a crest on top, and large muscle attachments in the rear. Yet, combined with these apelike features is a smallish vertical face containing front teeth very unlike an ape’s. In fact, the lower face, being more tucked in under the brain vault (and not protruding, as in most other early hominins), is more of a derived feature more commonly expressed in much later hominins (especially mem- bers of genus Homo). What’s more, unlike the dentition seen in apes (and some early hominins), the upper canine is reduced and is worn down from the tip (rather than shearing along its side against the first lower premolar). The lack of such a shearing canine/premolar arrangement (called a honing complex) (Fig. 10-7) is viewed by many researchers as an important derived characteristic of early homi- nins (White et al., 2010). Other experts are not entirely convinced and suggest that it could just as easily have evolved in both hominins and other hominoids because of homoplasy (Wood and Harrison, 2011).

In recognition of this unique com- bination of characteristics, paleoan- thropologists have placed the Toros- Menalla remains into a new genus and species of hominin, Sahelanthropus tchadensis (Sahel being the region of the southern Sahara in North Africa). These new finds from Chad have forced an immediate and significant reassessment of early hominin evo- lution. Two cautionary comments,

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▲�Figure 10-7 Canine/lower first premolar honing complex, typical of most Old World anthropoids, but lack- ing in most hominins (shown here in a male patas monkey). Note how the large upper canine shears against the elongated surface of the lower first premolar.

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honing complex the shearing of a large upper canine with the first lower premolar, with the wear leading to honing of the surfaces of both teeth. this anatomical pattern is typical of most Old World anthro- poids but is mostly absent in hominins.

chapter 10 Hominin Origins in Africa 284

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Pre-Australopiths (6.0+ to 4.4 mya) 285

however, are in order. First, as we noted, the dating is only approximate, since it is based on biostratigraphic correlation with sites in Kenya (1,500 miles to the east). Second, and per- haps more serious, is the hominin sta- tus of the Chad fossil. Given the facial structure and dentition, it’s difficult to see how Sahelanthropus could be anything but a hominin. However, the position of its foramen magnum is intermediate between that of a qua- drupedal ape and that of a bipedal hominin (Fig. 10-9); for this and other reasons, some researchers (Wolpoff et al., 2002) suggest that at this time, “ape” may be a better classification for Sahelanthropus. As we have previ- ously said, the best-defining anatomi- cal characteristics of hominins relate to bipedal locomotion. Unfortunately, no postcranial elements have been recovered from Chad—at least not yet. Consequently, we do not yet know the locomotor behavior of Sahelanthropus, and this raises even more fundamental questions: What if further finds show this form not to be bipedal? Should we still consider it a hominin? What, then, are the defining characteris- tics of our lineage? For all these rea- sons, several paleoanthropologists have recently grown more skeptical regard- ing the hominin status of all the pre- australopith finds, and Bernard Wood (2010) prefers to call them “possible hominins.”

Probably living at about the same time as Sahelanthropus, two other very early (possible) hominin genera have been found at sites in central Kenya in the Tugen Hills and from the Middle Awash area of northeastern Ethiopia. The earlier of these finds (dated by radiometric methods to around 6 mya) comes from the Tugen Hills and includes mostly dental remains, but also some quite complete lower limb bones. These fossils have been placed in a separate early hominin genus called Orrorin. The postcranial remains are especially important, since they seem to indicate bipedal locomo- tion (Pickford and Senut, 2001; Senut et al., 2001; Galik et al., 2004; Richmond

and Jungers, 2008). As a result of these further analyses, Orrorin is the pre- australopith generally recognized as having the best evidence to estab- lish it as a hominin (compared to less clear evidence for Sahelanthropus and Ardipithecus).

The last group of possible hominins dating to the late Miocene (that is, ear- lier than 5 mya) comes from the Middle Awash in the Afar Triangle of Ethiopia. Radiometric dating places the age of these fossils in the very late Miocene, 5.8 to 5.2 mya. The fossil remains themselves are very fragmentary. Some of the dental remains resemble some later fossils from the Middle Awash (discussed shortly), and Yohannes Haile-Selassie, the researcher who first found and described these earlier materials, has provisionally assigned them to the genus Ardipithecus (Haile- Selassie et al., 2004). (See “At a Glance: Pre-Australopith Discoveries” on p. 290.) In addition, some postcra- nial elements have been preserved— most informatively a toe bone, a pha- lanx from the middle of the foot (see Appendix A, Fig. A-8). From clues in this bone, Haile-Selassie concludes that this primate was a well-adapted biped (once again, the best-supporting evi- dence of hominin status).

From another million years or so later in the geological record in Ethiopia’s Middle Awash region, a very large and significant assemblage of fos- sil hominins has been discovered at a site called Aramis. Radiometric dat- ing firmly places these remains at about 4.4 mya. The site, represent- ed by a 6-foot-thick bed of bones, has yielded more than 6,000 fossils. These abundant finds include both large and small vertebrates—birds and other reptiles and even very small mam- mals. Additionally, fossil wood and pollen samples have been recovered. All this information is important for understanding the environments in which these ancient hominins lived (Fig. 10-10).

Hominin fossil remains from Aramis include several individuals, the most noteworthy being a partial

▲�Figure 10-9 Position of the fora- men magnum in (a) a human and (b) a chimpanzee. Note the more forward position in the human cranium.

Aramis (air-ah-miss)

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skeleton. From this important site a total of at least 36 other hominins are represented by isolated teeth, cranial bones, and a few limb bones. All the bones were extremely fragile and frag- mentary and required many years of incredibly painstaking effort to clean and reconstruct. Indeed, it took 15 years before the partial skeleton was in good enough condition to be intensively studied. But the wait was well worth it, and in 2009, Tim White and colleagues published their truly remarkable finds. By far the most informative fossil is the partial skeleton. Even though it was found crushed and fragmented, the years of work and computer imag- ing have now allowed researchers to interpret this 4.4- million-year-old individual. Nicknamed “Ardi,” this individual has more than 50 percent of its skeleton represented; however, since it was found in such poor condi- tion, any reconstruction must be seen as provisional and open to varying interpretations. Ardi has been sexed as female and contains several key por- tions, including a skull, a pelvis, and almost complete hands and feet (White et al., 2009; Fig. 10-11).

Ardi’s brain size, estimated between 300 and 350 cm³, is quite small, being no larger than a chimpanzee’s. However, it is much like that seen in Sahelanthropus, and overall the skulls of the two hominins also appear to be

similar. The preservation of much of the postcranial skeleton is potentially crucial, because key body elements, such as the pelvis and the foot, are only very rarely discovered. This is the earliest hominin for which we have so many different parts of the body rep- resented, and it permits researchers to hypothesize more confidently about body size and proportions and, per- haps most crucially of all, the mode of locomotion.

Height is estimated at close to 4 feet, with a body weight of around 110 pounds. Compared to other early hom- inins, such a body size would be similar to that of a male and well above aver- age for a female (Table 10.1). The pel- vis and foot are preserved well enough to allow good-quality computer recon- structions. According to White and colleagues, both areas of the body show key anatomical changes indicating that Ardipithecus was a competent biped. For example, the ilium is short and broad (see Figs. 10-2 and 10-3), and the foot has been modified to act as a prop for propulsion during walking.

However, Ardi also presents some big surprises. While the shape of the ilium seems to show bipedal ability, other parts of the pelvis show more ancestral (“primitive”) hominoid char- acteristics. In fact, the paleoanthro- pologists who analyzed the skeleton concluded that Ardi likely walked

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▶�Figure 10-10 Tim White and Yohannes Hailie-Selassie search the Aramis site, looking for even the tiniest of fossil fragments of Ardipithecus.

Pre-Australopiths (6.0+ to 4.4 mya) 287

quite adequately but might well have had difficulty running (Lovejoy et al., 2009a, b). The foot is also an odd mix of features, showing a big toe that is highly divergent and capable of consid- erable grasping. Some researchers are not convinced that Ardi was bipedal, and considering all her other primi- tive characteristics, some have ques- tioned whether Ardipithecus was really a hominin at all (Sarmiento, 2010). The extreme degree of reconstruction that was required (for the skull and pelvis especially) adds further uncertainty to understanding this crucial discov- ery. One thing that everyone agrees on is that Ardi was an able climber who likely was well adapted to walking on all fours along the tops of branches. It seems clear that she spent a lot of time in the trees.

Accepting for the moment that Ardipithecus was a hominin, it was a very primitive one, displaying an array of characteristics quite distinct from all later members of our lineage. In fact, its combination of characteristics is very odd and unique among our lineage. The new evidence that Ardi provides has not convinced all paleoanthro- pologists that Ardipithecus or any of the other very early pre- australopiths are hominins; indeed, Ardi’s very odd anatomy has caused doubts to increase. One thing is for sure: It would take a considerable adaptive shift in the next 200,000 years to produce the more derived hominins we’ll discuss in a moment. All of these considerations

have not only intrigued professional anthropolo- gists but also captured the imagination of the general public. When did the earli- est member of our lineage first appear? The search goes on, and professional repu- tations are made and lost in this quest.

Another intriguing aspect of all these late Miocene/ early Pliocene locales (that is, Toros-Menalla, Tugen Hills, early Middle Awash sites, and Aramis) relates to the ancient environments associ- ated with these earliest hom- inins. Rather than the more open grassland savanna habitats so characteristic of most later hominin sites, the environment at all these early locales is more heavily forested. Perhaps at Aramis and these other ancient sites we are seeing the very begin- nings of hominin divergence, not long after the division from the African apes.

▶�Figure 10-11 A mostly com- plete (but fragmented) skeleton of Ardipithecus. Dating to about 4.4 mya, this is the earliest hom- inin skeleton yet found contain- ing so many different portions of the body. Da

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Table 10.1 Estimated Body Weights and Stature in Plio-Pleistocene Hominins Body Weight Stature

Male Female Male Female

A. afarensis 45 kg (99 lb) 29 kg (64 lb) 151 cm (59 in.) 105 cm (41 in.)

A. africanus 41 kg (90 lb) 30 kg (65 lb) 138 cm (54 in.) 115 cm (45 in.)

A. robustus 40 kg (88 lb) 32 kg (70 lb) 132 cm (52 in.) 110 cm (43 in.)

A. boisei 49 kg (108 lb) 34 kg (75 lb) 137 cm (54 in.) 124 cm (49 in.)

H. habilis 52 kg (114 lb) 32 kg (70 lb) 157 cm (62 in.) 125 cm (49 in.)

Source: After McHenry, 1992. Note: Reno et al. (2003) conclude that sexual dimorphism in A. afarensis was considerably less than shown here.

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later one that is much more derived. These earlier australopiths, dated 4.2 to 3.0 mya, show several more primi- tive (ancestral) hominin characteris- tics than the later australopith group, whose members are more derived, some extremely so. These more derived hominins lived after 2.5 mya and are composed of two different genera, together represented by at least five different species. (See Appendix C on the Anthropology CourseMate at Cengagebrain.com for a complete list- ing and more information about early hominin fossil finds.)

Given the 3-million-year time range as well as quite varied ecological niches, there are numerous intriguing adaptive differences among these var- ied australopith species. We’ll discuss the major adaptations of the different species in a moment. But first let’s emphasize the major features that all australopiths share:

1. They are all clearly bipedal (although not necessarily identical to Homo in this regard).

2. They all have relatively small brains (at least compared to Homo).

Australopiths (4.2 to 1.2 mya)

The best-known, most widely dis-tributed, and most diverse of the early African hominins are colloqui- ally called australopiths. In fact, this varied and highly successful group of hominins is made up of two closely related genera, Australopithecus and Paranthropus. These hominins have an established time range of over 3 mil- lion years, stretching back as early as 4.2 mya and not becoming extinct until apparently close to 1 mya— making them the longest-enduring hominins yet documented. In addition, these hominins have been found in all the major geographical areas of Africa that have, to date, produced early hominin finds, namely, South Africa, central Africa (Chad), and East Africa. From all these areas combined, there appears to have been considerable complexity in terms of evolutionary diversity, with numerous species now recognized by most paleoanthropologists.

There are two major subgroups of australopiths: an earlier one that is more anatomically primitive and a

australopiths a colloquial name referring to a diverse group of plio- pleistocene african hominins. australopiths are the most abundant and widely distrib- uted of all early hominins and are also the most completely studied.

Key Pre-Australopith Discoveries

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Date Region Hominin Site Evolutionary Significance

4.4 mya east africa Ardipithecus ramidus

aramis Large collection of fossils, including partial skeletons; bipedal, but derived.

5.8–5.2 mya Ardipithecus Middle awash Fragmentary, but possibly bipedal.

~6.0 mya Orrorin tugenensis

tugen hills First hominin with post-cranial remains; possibly bipedal.

~7.0– 6.0 mya

central africa Sahelanthropus tchadensis

toros-Menalla Oldest potential hominin; well- preserved cranium; very small-brained; bipedal?

At a Glance

Australopiths (4.2 to 1.2 mya) 289

3. They all have large teeth, particu- larly the back teeth, with thick to very thick enamel on the molars.

In short, then, all these australopith species are relatively small-brained, big-toothed bipeds.

The earliest australopiths, dating to 4.2 to 3.0 mya, come from East Africa from a couple of sites in northern Kenya as well as two other sites in the Middle Awash region of Ethiopia (in the same area where Ardipithecus was discovered). Among the fossil finds of those earliest australopiths so far dis- covered, a few postcranial pieces clearly indicate that locomotion was bipedal. There are, however, a few primitive fea- tures in the dentition, including a large canine and a sectorial lower first pre- molar (see Fig. 10-8).

Since these particular fossils have initially been interpreted as more primitive than all the later mem- bers of the genus Australopithecus, paleoanthropologists have provision- ally assigned them to a separate spe- cies. This important fossil species is now called Australopithecus anamen- sis, and some researchers suggest that it is a potential ancestor for many later australopiths as well as perhaps early members of the genus Homo (White et al., 2006) (see Fig. 10-12).

Australopithecus afarensis Slightly later and much more com- plete remains of Australopithecus have come primarily from the sites of Hadar (in Ethiopia) and Laetoli (in Tanzania). Much of this material has been known for over three decades, and the fossils have been very well studied; indeed, in certain instances, they are quite famous. For example, the Lucy skeleton was discovered at Hadar in 1974, and the Laetoli footprints were first found in 1978. These hominins are classified as members of the species Australo- pithecus afarensis.

Literally thousands of footprints have been found at Laetoli, represent- ing more than 20 different kinds of

animals (Pliocene elephants, horses, pigs, giraffes, antelopes, hyenas, and an abundance of hares). Several hom- inin footprints have also been found, including a trail more than 75 feet long made by at least two—and perhaps three—individuals (Leakey and Hay, 1979) (Fig. 10-13). Such discoveries of well-preserved hominin footprints are extremely important in furthering our understanding of human evolution. For the first time, we can make definite statements regarding the locomotor pattern and stature of early hominins.

Studies of these impression pat- terns clearly show that the mode of locomotion of these hominins was bipedal (Day and Wickens, 1980). Some researchers, however, have conclud- ed that A. afarensis was not bipedal in quite the same way that modern humans are. From detailed compari- sons with modern humans, estimates

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▲�Figure 10-12 Fossil remains of Australopithecus ana mensis from the Middle Awash region of Ethiopia. In addition to teeth and jaw fragments, several postcranial pieces were also found (hand and foot bones, pieces of vertebrae, and part of a thigh bone—that is, a femur).

sectorial adapted for cutting or shear- ing; among primates, this term refers to the compressed (side-to-side) first lower premolar, which functions as a shearing surface with the upper canine.

chapter 10 Hominin Origins in Africa 290

of stride length, cadence, and speed of walking have been ascertained, indi- cating that the Laetoli hominins moved in a slower (“strolling”) fashion with a rather short stride.

One extraordinary discovery at Hadar is the Lucy skeleton (Fig. 10-14), found eroding out of a hillside by Don Johanson. This fossil is scientifically designated as Afar Locality (AL) 288-1 but is usually just called Lucy (after the Beatles song “Lucy in the Sky with Diamonds”). Representing almost 40 percent of a skeleton, this is one of the most complete individuals from any- where in the world for the entire period before about 100,000 years ago.

Because the Laetoli area was cov- ered periodically by ashfalls from near- by volcanic eruptions, accurate dat- ing is possible and has provided dates of 3.7 to 3.5 mya. Dating from the Hadar region hasn’t proved as straight- forward; however, more complete dat- ing calibration using a variety of tech- niques has determined a range of 3.9 to 3.0 mya for the hominin discoveries from this area.

Several hundred A. afarensis speci- mens, representing a minimum of 60 individuals (and perhaps as many as 100), have been removed from Laetoli and Hadar. At present, these materials represent the largest well-studied col- lection of early hominins and as such

are among the most significant of the hominins discussed in this chapter.

Without question, A. afarensis is more primitive than any of the other later australopith fossils from South or East Africa (discussed shortly). By primitive we mean that A. afarensis is less evolved in any particular direc- tion than are later-occurring hominin species. That is, A. afarensis shares more primitive features with some late Miocene apes and with living great apes than do later hominins, who display more derived characteristics.

For example, the teeth of A. afaren- sis are quite primitive. The canines are often large pointed teeth. Moreover, the lower first premolar is semisecto- rial (that is, it provides a shearing sur- face for the upper canine), and the tooth rows are parallel, even converg- ing somewhat toward the back of the mouth (Fig. 10-15).

The cranial portions that are pre- served also display several primitive hominoid characteristics, including a crest in the back as well as several primitive features of the cranial base. Cranial capacity estimates for A. afar- ensis show a mixed pattern compared to later hominins. A provisional esti- mate for the one partially complete cranium—apparently a large indi- vidual—gives a figure of 500 cm³, but another even more fragmentary cra-

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▶�Figure 10-13 Hominin footprint from Laetoli, Tanzania. Note the deep impression of the heel and the large toe (arrow) in line (adducted) with the other toes.

Australopiths (4.2 to 1.2 mya) 291

nium is apparently quite a bit smaller and has been estimated at about 375 cm³ (Holloway, 1983). Thus for some individuals (males?), A. afarensis is well within the range of other aus- tralopith species (see “A Closer Look: Cranial Capacity” on p. 293); but oth- ers (females?) may have a significant- ly smaller cranial capacity. However, a detailed depiction of cranial size for A. afarensis is not possible at this time; this part of the skeleton is unfortunate- ly too poorly represented. One thing is clear: A. afarensis had a small brain, probably averaging for the whole spe- cies not much over 420 cm³.

On the other hand, a large assort- ment of postcranial pieces represent- ing almost all portions of the body of A. afarensis has been found. Initial impressions suggest that relative to lower limbs, the upper limbs are longer than in modern humans (also a primitive Miocene ape condition). (This statement does not mean that the arms of A. afarensis were longer than the legs.) In addi- tion, the wrist, hand, and foot bones show several differ- ences from modern humans (Susman et al., 1985). From such excellent postcranial evi- dence, stature can be confi- dently estimated: A. afaren- sis was a short hominin. From her partial skeleton, Lucy is estimated to have been only 3 to 4 feet tall. However, Lucy—as demonstrated by her pelvis—was probably a female, and there is evidence of larger individuals as well. The most economical hypoth- esis explaining this variation is that A. afarensis was quite sexually dimorphic: The larger individuals are male, and the smaller ones, such as Lucy, are female. Estimates of male stat- ure can be approximated from the larger footprints at Laetoli, inferring a height of not quite 5 feet. If we accept this inter- pretation, A. afarensis was a

very sexually dimorphic form indeed. In fact, for overall body size, this spe- cies may have been as dimorphic as any living primate (that is, as much as gorillas, orangutans, or baboons).

Significant further discoveries of A. afarensis have come from Ethiopia in the last few years, including two further partial skeletons. The first of these is a mostly complete skele- ton of an A. afarensis juvenile discov- ered at the Dikika locale in northeast- ern Ethiopia, very near the Hadar sites mentioned earlier (Fig. 10-16). What’s more, the juvenile skeleton comes from the same geological horizon as Hadar, with very similar dating: 3.3 to 3.2 mya (Alemseged et al., 2006).

This find of a 3-year-old hominin is remarkable because it’s the first exam- ple of a very well-preserved immature

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chapter 10 Hominin Origins in Africa 292

hominin prior to about 100,000 years ago. From the individual’s extremely

well-preserved teeth, scientists hypothesize that she was female.

A comprehensive study of her developmental biology has

already begun, and many more revelations are surely in store as the Dikika fossil is more completely cleaned and studied. Initial results, accounting for her imma- ture age, show a skeletal

pattern quite similar to what we’d expect in an A. afar-

ensis adult. What’s more, the limb proportions, anatomy of

the hands and feet, and shape of the scapula (shoulder blade) reveal a simi- lar “mixed” pattern of locomotion. The foot and lower limb indicate that this young hominin would have been a ter- restrial biped. Further analysis of her shoulder confirms that she was also capable of climbing about quite ably in the trees (Green and Alemseged, 2012).

The second recently discovered A. afarensis partial skeleton comes from the Woranso-Mille research area in the central Afar, only about 30 miles north of Hadar (Haile-Selassie et al., 2010). The dating places the find at close to 3.6 mya (almost 400,000 years earlier than Lucy). Moreover, this individual was considerably larger than Lucy and likely was male. Analysis of bones preserved in this new find reinforces what was previously known about A. afarensis as well as adding some further insights.

The large degree of sexual dimorphism and well-adapted bipedal locomotion agree with prior evidence.

What makes A. afarensis a hominin? The answer is revealed by its manner of locomotion. From the abundant limb bones recovered from Hadar and other locales, as well as those beautiful foot- prints from Laetoli, we know unequiv- ocally that A. afarensis walked biped- ally when on the ground. (At present, we do not have nearly such good evi- dence concerning locomotion for any of the earlier hominin finds.) Whether Lucy and her contemporaries still spent considerable time in the trees and just how efficiently they walked have become topics of some contro- versy. Most researchers, however, agree that A. afarensis was an efficient habit- ual biped while on the ground. These hominins were also clearly obligate bipeds, which would have hampered their climbing abilities but would not necessarily have precluded arboreal behavior altogether.

Australopithecus afarensis is a cru- cial hominin group. Since it comes after the earliest, poorly known group of pre-australopith hominins, but prior to all later australopiths as well as Homo, it is an evolutionary bridge, linking together much of what we assume are the major patterns of early hominin evolution. The fact that there are many well- preserved fossils and that they have been so well studied also adds to the paleoanthropological significance of A. afarensis. The consensus among

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a b▶�Figure 10-15 Jaws of Australo pithecus afarensis. (a) Maxilla, AL 200-1a, from Hadar, Ethiopia. (Note the parallel tooth rows and large canines.) (b) Mandible, LH 4, from Laetoli, Tanzania. This fossil is the type specimen for the species Australopithecus afarensis.

▲�Figure 10-16 Complete skull with attached vertebral column of the juvenile skeleton from Dikika, Ethiopia (dated to about 3.3 mya).

Australopiths (4.2 to 1.2 mya) 293

most experts over the last several years has been that A. afarensis is a poten- tially strong candidate as the ances- tor of all later hominins. Some ongoing analysis has recently challenged this hypothesis (Rak et al., 2007), but at least for the moment, this new interpreta- tion has not been widely accepted. Still, it reminds us that science is an intel- lectual pursuit that constantly reevalu- ates older views and seeks to provide more systematic explanations about the world around us. When it comes to understanding human evolution, we should always be aware that things might change. So stay tuned.

A Contemporaneous and Very Different Kind of Hominin From Woranso-Mille, the same site in the central Afar where researchers recently discovered a partial A. afaren-

sis skeleton, they have also uncovered a partial foot dated to about 3.4 mya (Haile-Selassie et al, 2012). However, the partial foot remains, which include several nicely preserved toe bones, are very different from those of A. afaren- sis and other obligate bipeds.

The new find shows a divergent opposable big toe and other ape-like features that strongly suggesting that this animal was a good climber. At the same time there are some other char- acteristics suggesting that it probably could walk bipedally on the ground, although not in a manner like A. afar- ensis or any later hominin. This odd mix of characteristics looks most like that of Ardipithecus, which lived a full million years earlier. Without more complete fossil remains, it’s impos- sible, for now, to assign this new find to a particular species. One thing is for sure: It isn’t A. afarensis! So, there were two different lineages living side by side, each with very different foot

Cranial Capacity

Cranial capacity, usually reported in cubic centimeters, is a measure of brain size, or volume. the brain itself, of course, doesn’t fossilize. however, the space once occupied by brain tissue (the inside of the cranial vault) is sometimes preserved, at least in those cases where fairly complete crania are recovered.

For purposes of comparison, it’s easy to obtain cranial capacity estimates for contemporary species (including humans) from analy- ses of skeletonized specimens in museum collections. From studies of this nature, estimated cranial capacities for modern hominoids have been determined as follows (tobias, 1971, 1983):

Range (cm³) Aveage (cm³)

human 1,150–1,750* 1,325 chimpanzee 285–500 395 Gorilla 340–752 506 Orangutan 276–540 411 Bonobo — 350

these data for living hominoids can then be compared with those obtained for early hominins:

Average (cm³)

Sahelanthropus ~350 Orrorin Not currently known Ardipithecus ~420 Australopithecus anamensis Not currently known Australopithecus afarensis 438 Later australopiths 410–530 early members of genus Homo 631

as the tabulations indicate, cranial capacity estimates for aus- tralopiths fall within the range of most modern great apes, and gorillas actually average slightly greater cranial capacity than that seen in most early hominins. It’s important to remember, however, that gorillas are very large animals, whereas most early hominins probably weighed on the order of 100 pounds (see table 10-1). Since brain size is partially correlated with body size, comparing such different-sized animals can’t be justified. compared to living chimpanzees (most of which are slightly larger than early hominins) and bonobos (which are somewhat smaller), australopiths had pro- portionately about 10 percent bigger brains; so we would say that these early hominins were more encephalized.

A Closer Look

*the range of cranial capacity for modern humans is very large—in fact, even greater than that shown (which approximates cranial capacity for the majority of contemporary H. sapiens populations).

chapter 10 Hominin Origins in Africa 294

anatomy and varied forms of locomo- tion. The researchers who have studied these new foot fossils as well as some other experts (Lieberman, 2012) think it was a hominin that was at least par- tially bipedal. On both counts, we’ll have to wait and see.

Later More Derived Australopiths (3.0 to 1.2 mya) Following 3.0 mya, hominins became more diverse in Africa. As they adapted to varied niches, australopiths became considerably more derived. In other words, they show physical changes making them quite distinct from their immediate ancestors.

In fact, there were at least three sep- arate lineages of hominins living (in some cases side by side) between 2.0 and 1.2 mya. One of these is a later form of Australopithecus; another is represented by the highly derived three species that belong to the genus Paranthropus; and the last consists of early members of the genus Homo. Here we’ll discuss Paranthropus and Australopithecus. Homo will be dis- cussed in the next section.

The most derived australopiths are the various members of Paranthropus. While all australopiths are big-toothed, Paranthropus has the biggest teeth of all, especially as seen in its huge premo- lars and molars. Along with these mas- sive back teeth, these hominins show a variety of other specializations related to powerful chewing (Fig. 10-17). For example, they all have large deep lower jaws and large attachments for muscles associated with chewing. In fact, these chewing muscles are so prominent that major anatomical alterations evolved in the architecture of their face and skull vault. In particular, the Paranthropus face is flatter than that of any other australopith; the broad cheekbones (to which the masseter muscle attaches) flare out; and a ridge develops on top of the skull (this is called a sagittal crest, and it’s where the temporal muscle attaches).

All these morphological features indicating strong chewing suggest that

Paranthropus likely was adapted for a diet emphasizing rough vegetable foods. However, this does not mean that these very big-toothed hominins did not also eat a variety of other foods, perhaps including some meat. In fact, sophisticated recent chemical analy- ses of Paranthropus teeth suggest that their diet may have been quite varied (Sponheimer et al., 2006).

The first member of the Paranthropus evolutionary group (clade) comes from a site in north- ern Kenya on the west side of Lake Turkana. This key find is that of a nearly complete skull, called the “Black Skull” (owing to the chemical stain- ing from manganese-rich soil during fossilization), dating to approximately 2.5 mya (Fig. 10-18). This skull, with a cranial capacity of only 410 cm³, is among the smallest for any hom- inin known, and it has other primi- tive traits reminiscent of A. afarensis. For example, there’s a compound crest in the back of the skull, the upper face pro jects considerably, and the upper dental row converges in back (Kimbel et al., 1988).

But here’s what makes the Black Skull so fascinating: Mixed into this array of distinctively primitive traits are a host of derived ones that link it to other, later Paranthropus species (including a broad face, a very large palate, and a large area for the back teeth). This mosaic of features seems to place this individual between ear- lier A. afarensis on the one hand and the later Paranthropus species on the other. Because of its unique position in hominin evolution, the Black Skull (and the population it represents) has been placed in a new species, Paranthropus aethiopicus.

Around 2 mya, different varieties of even more derived members of the Paranthropus lineage were on the scene in East Africa. As well documented by finds dated after 2 mya from Olduvai and East Turkana, Paranthropus con- tinued to have a relatively small cra- nial capacity (ranging from 510 to 530 cm³) and a very large, broad face with massive back teeth and lower jaws.

sagittal crest a ridge of bone that runs down the middle of the cranium like a short Mohawk. this serves as the attach- ment for the large temporal muscles, indi- cating strong chewing.

Australopiths (4.2 to 1.2 mya) 295

The larger (probably male) individu- als also show the characteristic raised ridge (sagittal crest) along the mid- line of the cranium. Females are not as large or as robust as the males, indi-

cating a fair degree of sexual dimor- phism. In any case, the East African Paranthropus individuals are all extremely robust in terms of their teeth and jaws—although in overall body

Postorbital constriction

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Note: The size and proportions of this specimen differ from ER 406 and OH 5

(above), and this individual has been

suggested as a female Paranthropus.

Broad cheekbones (zygomatics)

ER 406 (Koobi Fora) Superior view

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chapter 10 Hominin Origins in Africa 296

size they are much like other australo- piths. Since these somewhat later

East African Paranthropus* fossils are so robust, they

are usually placed in their own separate species,

Paranthropus boisei. Paranthropus fossils

have also been found at several sites in South Africa. The geologi- cal context in South Africa usually does not

allow as precise chrono- metric dating as is possi-

ble in East Africa. Based on less precise dating methods,

Paranthropus in South Africa existed about 2.0 to 1.2 mya.

Paranthropus in South Africa is very similar to its close cousin in East Africa, but it’s not quite as dentally robust. As a result, paleoanthropolo- gists prefer to regard South African Paranthropus as a distinct species— one called Paranthropus robustus.

What became of Paranthropus? After 1 mya, these hominins seem to have vanished without descen- dants. Nevertheless, we should be careful not to think of them as “failures.” After all, they last- ed for 1.5 million years, during which time they expanded over a considerable area of sub-Saha- ran Africa. Moreover, while their extreme dental/chewing adapta- tions may seem peculiar to us, they represent a fascinating “evo- lutionary experiment” in hominin evolution. And it was an innova- tion that worked for a long time. Still, these big-toothed cousins of

ours did eventually die out. It remains to us, the descendants of another hom- inin lineage, to find their fossils, study them, and ponder what these creatures were like.

No fossil finds of genus Australopithecus more recent than

*Note that these later East African Paranthropus finds are at least 500,000 years later than the earlier species (P. aethiopicus, exemplified by the Black Skull).

3 mya have yet been found in East Africa. As you know, their close Paranthropus kin were doing quite well during this time. Whether Australopithecus actually did become extinct in East Africa following 3 mya or whether we just haven’t yet found their fossils is impossible to say.

South Africa, however, is another story. A very well-known Australopithecus species has been found at four sites in southernmost Africa, in a couple of cases in limestone caves very close to where Paranthropus fossils have also been found.

In fact, the very first early hominin discovery from Africa (indeed, from anywhere) came from the Taung site and was discovered back in 1924. The story of the discovery of the beautifully preserved child’s skull from Taung is a fascinating tale (Fig. 10-19). When first published in 1925 by a young anatomist named Raymond Dart (Fig. 10-20), most experts were unimpressed by the small-brained specimen of a 3- to 4-year-old child. They believed that our earliest ancestors would be easily identi- fiable by their larger brains and thought of Africa as an unlikely place for the origins of hominins. These skeptics, who for a long time had been focused on European and Asian hominin finds, were initially unprepared to acknowl- edge Africa’s central place in human evolution. Only years later, following many more African discoveries from other sites, did professional opinion shift. With this admittedly slow scien- tific awareness came the eventual con- sensus that the Taung specimen (which Dart classified as Australopithecus afri- canus) was indeed an ancient member of the hominin family tree.

Like other australopiths, the “Taung child” (the type specimen) and other A. africanus individuals (Fig. 10-21) were small-brained, with an adult cra- nial capacity of about 440 cm³. In fact, the Taung child is quite remarkable for its preservation of a natural endo- cast. It was this fossilized mold of the external morphology of the right side of the child’s brain that led Dart to rec- ognize it as hominin and not an ape.

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▲�Figure 10-18 The “Black Skull,” discovered at West Lake Turkana. This specimen is usually assigned to Paranthropus aethiopicus. It’s called the Black Skull because of its dark color due to the fossilization (mineral- ization) process.

▲�Figure 10-19 The Taung child’s skull, discovered in 1924. There is a fossilized endocast of the brain in back, with the face and lower jaw in front.

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endocast a solid impression of the inside of the skull vault, often preserving details relating to the size and surface fea- tures of the brain.

Australopiths (4.2 to 1.2 mya) 297

As a recent reassessment of this brain mold has shown, A. africanus already had a pattern of brain development more in line with that of later homi- nins (Falk et al., 2012). A africanus was also big-toothed relative to later homi- nins, although not as extremely so as Paranthropus. Moreover, from very well-preserved postcranial remains from Sterkfontein, we know that these individuals were also were well- adapted bipeds. The ongoing excava- tion of the remarkably complete skel- eton at Sterkfontein should tell us a lot about A. africanus’ locomotion, body size and proportions, and much more (Fig. 10-22).

The precise dating of A. africanus, as with most other South African hom- inins, has been disputed. Over the last several years, it’s been assumed that this species existed as far back as 3.3 mya. However, the most recent analysis suggests that A. africanus lived approx- imately between 3 and 2 mya (Walker et al., 2006; Wood, 2010) (Fig. 10-23).

New Connections: A Transitional Australopith? As we’ll see in the next section, almost all the evidence for the earliest appear- ance of our genus, Homo, has come

from East Africa. So it’s no surprise that most researchers have assumed that Homo probably first evolved in this region of Africa.

However, new and remarkably well- preserved fossil dis- coveries from South Africa may challenge this view. In 2008, paleoan- thropologists discovered two partial skeletons at the Malapa Cave, located just a few miles from Sterkfontein and Swartkrans (see Fig. 10-6). Actually, the first find was made

◀�Figure 10-20 Raymond Dart, shown working in his laboratory.

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▲�Figure 10-21 Adult cranium of Australopithecus africanus from Sterkfontein.

◀�Figure 10-22 Paleoanthropologist Ronald Clarke carefully excavates a 2-million-year-old skeleton from the limestone matrix at Sterkfontein Cave. Clearly seen are the cranium (with articulated mandible) and the upper arm bone.

chapter 10 Hominin Origins in Africa 298

by the lead researcher’s 9-year-old son, Matthew, while out walking the fam- ily dog. His father (Lee Berger, from the University of Witwatersrand) and col- leagues have been further investigating inside the cave, where several skeletons may be buried; they announced and described these finds in 2010 (Berger et al., 2010).

Using paleomagnetic dating as well as more precise radiometric

techniques than have been used before in South

Africa (Dirks et al., 2010; Pickering et al.,

2011) (see Chapter 9), the fossils are dated to just a lit- tle less than 2 mya and show a fas- cinating mix of australopith char- acteristics along

with some features more suggestive of

Homo. Because of this unique anatomical com-

bination, these fossils have been assigned to a new spe-

cies, Australopithecus sediba (sediba means “wellspring” or “fountain” in the local language). Australopith-like char- acteristics seen in A. sediba include a small brain (estimated at 420 cm³), the australopith shoulder joint, long arms

with curved fingers, and several primi- tive traits in the feet. In these respects A. sediba most resembles A. africanus, its potential immediate South African predecessor.

On the other hand, some other aspects of A. sediba more resemble Homo. Among these characteristics are short fingers and possible indi- cations of brain reorganization (see Fig. 10-24). All this is very new and quite complex. Indeed, initial paleo- anthropological interpretations are highly varied (Balter, 2010; Pickering et al., 2011; Gibbons, 2011). It will take some time for experts to figure it out.

What’s more, new dental evidence shows that A. sediba had a surpising diet, at least one that is unusual for a hominin. Using an array of methods— including stable carbon isotopes, phy- tolith residues in dental calculus, and dental microwear (see Chapter 9 for discussion of all three methods)— Amanda Henry and colleagues have analyzed teeth from both skeletons thus far excavated at Malapa (Henry et al., 2012). Their results indicate that A. sediba primarily ate leaves, fruit, wood, and bark, along with a few grasses. Unlike that seen in most other early hominins, there is no evidence of a dietary focus on grass resources or meat, which are more typically found in more open savanna habitats. Indeed,

5 mya 4 mya6 mya7 mya 3 mya 2 mya 1 mya

Early Homo

Paranthropus robustus

Australopithecus sediba

Paranthropus boisei

Paranthropus aethiopicus

Australopithecus africanus

Australopithecus afarensis

Australopithecus anamensis

Orrorin tugenensis

Ardipithecus ramidus*

Sahelanthropus tchadensis

*The earlier Ardipithecus specimens (5.8–5.2 mya) are placed in a separate species.

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▲�Figure 10-23 Time line of early African hominins. Note that most dates are approximations. Question marks indicate those estimates that are most tentative.

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▲�Figure 10-24 A. sediba skull, found at Malapa Cave, South Africa.

Closer Connections: Early Homo (2.0 to 1.4 mya) 299

A. sediba’s diet appears to more closely resemble that of chimpanzees rather than that of most other hominins. The closest early hominin similarity is with Ardipithecus. These findings indi- cate that in anatomy as well as behav- ior, early hominins were an extremely varied group.

Remember, too, that there are more fossils still to be unearthed at Malapa. The initial consensus among paleoan- thropologists is that A. sediba is quite different from other australopiths and shows a surprising and unique mix of primitive and derived characteristics. How it fits in with the origins of Homo remains to be determined. Certainly, more detailed studies of the A. sediba fossils, including further comparisons with other early hominins will help to further our understanding where

A. sediba fits in (Fig. 10-25). For the moment, most paleoanthropologists still think that the best evidence for the origins of our genus comes from East Africa.

Closer Connections: Early Homo (2.0 to 1.4 mya)

In addition to the australopith remains, there’s another largely con- temporaneous hominin that is quite distinctive and thought to be more closely related to us. In fact, as best documented by fossil discoveries from Olduvai and East Turkana, these mate- rials have been assigned to the genus Homo—and thus are different from all species assigned to either Australo- pithecus or Paranthropus.

The earliest appearance of genus Homo in East Africa may date prior to 2 mya (and thus considerably before A. sediba). A discovery in the 1990s from the Hadar area of Ethiopia sug- gested to many paleoanthropologists that early Homo was present in East Africa by 2.3 mya; however, we must be cautious, since the find is quite incom- plete (including only one upper jaw) (Kimbel et al., 1996).

Better-preserved evidence of a Plio- Pleistocene hominin with a signifi- cantly larger brain than seen in aus- tralopiths was first suggested by Louis Leakey in the early 1960s on the basis of fragmentary remains found at Olduvai Gorge. Leakey and his col- leagues gave a new species designation to these fossil remains, naming them Homo habilis (see Fig. 10-26). There may, in fact, have been more than one species of Homo living in Africa during the Plio-Pleistocene. Therefore, more generally, we’ll refer to them all as “early Homo.” The species Homo habi- lis comprises particularly those early Homo fossils from Olduvai and the Turkana Basin.

The Homo habilis material at Olduvai dates to about 1.8 mya, but

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▲�Figure 10-25 One of the two partial A. sediba skeletons so far discovered at Malapa Cave, showing those elements that were preserved.

Plio-Pleistocene pertaining to the pliocene and first half of the pleistocene, a time range of 5 to 1 mya. For this time period, numerous fossil hominins have been found in africa.

chapter 10 Hominin Origins in Africa 300

owing to the fragmentary nature of the fossil remains, evolutionary inter- pretations have been difficult. The most immediately obvious feature distinguishing the H. habilis mate- rial from the australopiths is crani- al size. For all the measurable early Homo skulls, the estimated aver- age cranial capacity is 631 cm³, com- pared to 520 cm³ for all measurable Paranthropus specimens and 442 cm³ for Australopithecus crania (McHenry, 1988), including A. sediba (see “A Closer Look: Cranial Capacity,” p. 295). Early Homo, therefore, shows an increase in cranial size of about 20 per- cent over the larger of the australopiths and an even greater increase over some of the smaller-brained forms. In their

initial description of H. habilis, Leakey and his associates also pointed to dif- ferences from australopiths in cranial shape and in tooth proportions.

The naming of this fossil material as Homo habilis (“handy man”) was mean- ingful from two perspectives. First of all, Leakey argued that members of this group were the early Olduvai tool- makers. Second, and most significant- ly, by calling this group Homo, Leakey was arguing for at least two separate branches of hominin evolution in the Plio-Pleistocene. Clearly, only one could be on the main branch eventu- ally leading to Homo sapiens. By label- ing this new group Homo rather than Australopithecus, Leakey was guessing that he had found our ancestors.

Because the initial evidence was so fragmentary, most paleoanthropolo- gists were reluctant to accept H. habilis as a valid species distinct from all aus- tralopiths. Later discoveries, especially from Lake Turkana, of better- preserved fossils have shed further light on early Homo in the Plio-Pleistocene. The most important of this additional material is a nearly complete cranium (Fig. 10-27). With a cranial capacity of 775 cm³, this individual is well outside the known range for australopiths and actually overlaps the lower boundary for later species of Homo (that is, H. erectus, dis- cussed in the next chapter). In addi- tion, the shape of the skull vault is in many respects unlike that of australo- piths. However, the face is still quite robust (Walker, 1976), and the frag- ments of tooth crowns that are pre- served indicate that the back teeth in this individual were quite large.* The East Turkana early Homo material is generally contemporaneous with the Olduvai remains. The oldest date back to about 1.8 mya, but another speci- men found a few years ago dates to as recently as 1.44 mya, making it by far

*In fact, some researchers have suggested that all these “early Homo” fossils are better classified as Australopithecus (Wood and Collard, 1999a).

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▲�Figure 10-26 Artist’s reconstruc- tion of a female Homo habilis based on a cranium from East Lake Turkana. (Skull 1813; see photo of this speci- men in Figure 10-28.)

Interpretations: What Does It All Mean? 301

the latest surviving early Homo fossil yet found (Spoor et al., 2007). In fact, this discovery indicates that a species of early Homo co existed in East Africa for several hundred thousand years with H. erectus, with both species liv- ing in the exact same area on the east- ern side of Lake Turkana. This new evidence raises numerous fascinating questions regarding how two closely related species existed for so long in the same region.

As in East Africa, early members of the genus Homo have also been found in South Africa, and these fossils are considered more distinctive of Homo than is the transitional australopith, A. sediba. At both Sterkfontein and Swartkrans, fragmentary remains have been recognized as most likely belong- ing to Homo (Fig. 10-28 on p. 302).

On the basis of evidence from Olduvai, East Turkana, and Hadar, we can reasonably postulate that at least one species (and possibly two) of early Homo was present in East Africa per- haps before 2 mya, developing in paral- lel with an australopith species. These hominin lines lived contemporane- ously for at least 1 million years, after which the australopiths apparently dis- appeared forever. One lineage of early Homo likely evolved into H. erectus about 1.8 mya. Any other species of early Homo became extinct sometime after 1.4 mya.

Interpretations: What Does It All Mean?

By this time, you may think that anthropologists are obsessed with finding small scraps buried in the ground and then giving them con- fusing numbers and taxonomic labels impossible to remember. But it’s impor- tant to realize that the collection of all the basic fossil data is the foundation of human evolutionary research. With- out fossils, our speculations would be largely hollow—and most certainly not scientifically testable. Several large, ongoing paleoanthropological projects are now collecting additional data in an attempt to answer some of the more perplexing questions about our evolu- tionary history.

The numbering of specimens, which may at times seem some- what confusing, is an effort to keep the designations neutral and to make reference to each individual fossil as clear as possible. The formal nam- ing of finds as Australopithecus, Paranthropus, or Homo habilis should come much later, since it involves a lengthy series of complex interpreta- tions. Assigning generic and specific names to fossil finds is more than just a convenience; when we attach a par- ticular label, such as A. afarensis, to a particular fossil, we should be fully

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◀�Figure 10-27 A nearly complete early Homo cranium from East Lake Turkana (ER 1470), one of the most important single fossil hominin discov- eries from East Africa. (a) Lateral view. (b) Frontal view.

chapter 10 Hominin Origins in Africa 302

S O US OS O US O UO U T HU T HSS S U DS U DUU DD AD A ND A ND

A F R I C A

ITALY

S P A I N

P O R T U G A L

T U R K E YGREECE

CYPRUS

K E N Y A

E T H I O P I A

ERITREA S U D A N

E G Y P T

N I G E RM A U R I T A N I A M A L I

N I G E R I A

S O M A L I A

N A M I B I A

L I B Y A

C H A D

SOUTH AFRICA

T A N Z A N I A

A N G O L A

A L G E R I A

MADAGASCAR

MOZAMBIQUE

B O T S W A N A

Z A M B I A

GABON

CENTRAL AFRICAN REPUBLIC

TUNISIAM O R O C C O

UGANDA

SWAZILAND

LESOTHO

MALAWI

BURUNDI

RWANDA

TOGO

BENIN

GHANA

CÔTE D’IVOIRE

LIBERIASIERRA LEONE

GUINEA

BURKINA FASO

THE GAMBIA

CAMEROON

Z I M B A B W E

EQUATORIAL GUINEA

WESTERN SAHARA

DJIBOUTI

SENEGAL

GUINEA-BISSAU

JORDAN

ISRAEL

LEBANON

KUWAIT

QATAR

BAHRAIN

U. A. E.

Y E M E N

SYRIA

I R A Q

I R A N

S A U D I A R A B I A

MALTA

D E M O C R A T I C

R E P U B L I C

O F T H E C O N G O

REP. OF THE

CONGO

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East Turkana

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▲�Figure 10-28 Early Homo fossil finds.

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Interpretations: What Does It All Mean? 303

aware of the biological implications of such an interpretation.

From the time that fossil sites are first located until the eventual inter- pretation of hominin evolutionary pat- terns, several steps take place. Ideally, they should follow a logical order, for if interpretations are made too hastily, they confuse important issues for many years. Here’s a reasonable sequence:

1. Selecting and surveying sites 2. Excavating sites and recovering

fossil hominins 3. Designating individual finds

with specimen numbers for clear reference

4. Cleaning, preparing, studying, and describing fossils

5. Comparing with other fossil material—in a chronological framework if possible

6. Comparing fossil variation with known ranges of variation in closely related groups of living pri- mates and analyzing ancestral and derived characteristics

7. Assigning taxonomic names to fossil material

But the task of interpretation still isn’t complete, for what we really want to know in the long run is what hap-

pened to the populations represent- ed by the fossil remains. In looking at the fossil hominin record, we’re actu- ally looking for our ancestors. In the process of eventually determining those populations that are our most likely antecedents, we may conclude that some hominins are on evolutionary side branches. If this conclusion is accurate, those hominins necessarily must have become extinct. It’s both interesting and relevant to us as hominins to try to find out what influenced some earlier members of our family tree to continue evolving while others died out.

Although a clear evolutionary pic- ture is not yet possible for organiz- ing all the early hominins discussed in this chapter, there are some gen- eral patterns that for now make good sense (Fig. 10-29). New finds may of course require serious alterations to this scheme. Science can be exciting, but it can also be frustrating to many in the general public looking for sim- ple answers to complex questions. For well-informed students of human evo- lution, it’s most important to grasp the basic principles of paleoanthropology, how interpretations are made, and why they must sometimes be revised. This way you’ll be prepared for whatever shows up tomorrow.

0 mya

1 mya

2 mya

3 mya

4 mya

5 mya

6 mya

7 mya

8 mya

Orrorin

Australopithecus anamensis

A. afarensis

Ardipithecus

Sahelanthropus

H. erectus

Homo habilis A. sediba

A. africanus Paranthropus

? ??

◀�Figure 10-29 A tentative early hominin phylogeny. Note the numer- ous question marks, indicating continuing uncertainty regarding evolutionary relationships.

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chapter 10 Hominin Origins in Africa 304

Seeing the Big Picture: Adaptive Patterns of Early African Hominins

As you are aware by now, there are several different African hominin genera and certainly lots of species. This in itself is interesting. Speciation was occurring quite frequently among the various lineages of early homi- nins—more frequently, in fact, than among later hominins. What explains this pattern?

Evidence has been accumulating at a furious pace in the last decade, but it’s still far from complete. What’s clear is that we’ll never have anything approaching a complete record of early hominin evolution, so some significant gaps will remain. After all, we’re able to discover hominins only in those special environmental contexts where fossil- ization was likely. All the other poten- tial habitats they might have exploited are now invisible to us.

Still, patterns are emerging from the fascinating data we do have. First, it appears that early hominin species (pre-australopiths, Australopithecus, Paranthropus, and early Homo) all had restricted ranges. It’s therefore likely that each hominin species exploited a rela- tively small area with specific niches and could easily have become separated from other populations of its own species. So genetic drift (and to some extent natural selection) could have led to rapid genetic divergence and eventual speciation.

Second, most of these species appear to have been at least partially tied to arboreal habitats, although there’s disagreement on this point regarding early Homo (see Wood and Collard, 1999b; Foley 2002). Also, Paranthropus was probably some- what less arboreal than Ardipithecus or Australopithecus. These very large- toothed hominins apparently con- centrated on a diet of coarse, fibrous plant foods, such as roots. Exploiting such resources may have routinely taken these hominins farther away from the trees than their dentally

more gracile—and perhaps more omnivorous—cousins.

Third, except for some early Homo individuals, there’s very little in the way of an evolutionary trend of increased body size or of markedly greater encephalization. Beginning with Sahelanthropus, brain size was no more than that in chimpanzees—although when accounting for body size, this earliest of all known hominins may have had a proportionately larger brain than any living ape. Close to 5 million years later (that is, the time of the last surviving australopith species), relative brain size increased by no more than 10 to 15 percent. Perhaps tied to this relative stasis in brain capacity, there’s no absolute association of any of these hominins with patterned stone tool manufacture (see Chapter 9).

Although conclusions are becom- ing increasingly controversial, for the moment early Homo appears to be a partial exception. This group shows both increased encephalization and numerous occurrences of likely associ- ation with stone tools (though at many of the sites, australopith fossils were also found).

Last, all of these early African homi- nins show an accelerated developmental pattern (similar to that seen in African apes)—one quite different from the delayed developmental pattern char- acteristic of Homo sapiens (and our immediate precursors). This apelike development is also seen in some early Homo individuals (Wood and Collard, 1999a). Rates of development can be accurately reconstructed by examining dental growth markers (Bromage and Dean, 1985), and these data may provide a crucial window into understanding this early stage of hominin evolution.

These African hominin predeces- sors were rather small, able bipeds, but still closely tied to arboreal and/or climbing niches. They had fairly small brains and, compared to later Homo, matured rapidly. It would take a major evolutionary jump to push one of their descendants in a more human direc- tion. For the next chapter in this more human saga, read on.

305Media Resources

▶▶ The earliest possible members of our lineage date back to about 6 mya, and for the next 4 mil- lion years, they stayed geographically restricted to Africa, where they diversified into many different forms.

▶▶ During this several-million-year span, at least six different hominin genera and upward of 13 spe- cies have been identified from the available fossil record.

▶▶ These early African hominins fit into three major groupings:

• Pre-australopiths (6.0+ to 4.4 mya), including three genera of very early, and still primitive, possible hominins (Sahelanthropus, Orrorin, and Ardipithecus)

• Australopiths (4.2 to 1.2 mya): Early, more primitive australopith species (4.2 to 3.0 mya), including Australopithecus ana- mensis and Australopithecus afarensis. These are the earliest definite hominins. Later, more derived australopith species (2.5 to 1.2 mya) include two genera (Paranthropus and later species of Australopithecus). A recently dis- covered species (A. sediba), shows a combination of features that some researchers hypothesize as transitional between Australopithecus and early Homo (but this view remains controversial).

• Early Homo (2.0+? to 1.4 mya), including the first members of our genus, who around 2 mya likely diverged into more than one species

Summary of Main Topics

1. In what ways are the remains of Sahelanthropus and Ardipithecus considered primitive? How do we know that these forms are hominins? How sure are we?

2. Assume that you are in the laboratory analyz- ing the “Lucy” A. afarensis skeleton. You also have complete skeletons from a chimpanzee and a mod- ern human. (a) Which parts of the Lucy skeleton are more similar to the chimpanzee? Which are more similar to the human? (b) Which parts of

the Lucy skeleton are most informative regarding hominin status?

3. Discuss two current disputes regarding taxonomic issues concerning early hominins. Try to give sup- port for alternative positions.

4. What is a phylogeny? Construct one for early hom- inins (6.0 to 1.0 mya). Make sure you can describe the conclusions to which your scheme leads. Also, try to defend it.

Critical Thinking Questions

We know a great deal about early hominin evolution (during the time span from 6 to 1 mya), most specifi- cally from a large number of fossils, which include thousands of individual elements—representing more than 500 individuals. What’s more, some of these finds are quite complete, including some remarkable partial skeletons discovered recently in South and East Africa. By comparing these finds with contemporary primates (modern humans and great apes, especially), we can interpret the anatomy and likely function

of these early hominins (for example, determining whether they were bipedal). We can also date these finds quite precisely using an array of dating tech- niques. Last, new research techniques (e.g., advanced computed tomography scans) allow paleoanthropolo- gists to obtain remarkably accurate images of hom- inin fossils, even permitting them to actually “see inside the brain” of these ancient animals. Other new advances use very small samples of fossil teeth or even dental plaque to provide chemical evidence of diet.

How Do We Know?

Videos See the videos “Biomechanics” and “Tool Time”

to learn more about topics covered in this chapter.

Media Resources

Hominins began to disperse out of Africa around 2 million

years ago, and during the next 1 million years inhabited much

of Eurasia.

Connections

The first more human- like animals (hominins)

appeared in Africa around 6 mya ago and evolved

into a variety of different species.

The immediate predecessors of modern humans, includ- ing the Neandertals, were

much like us, but had some anatomical and behavioral

differences.

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After mastering the material in this chapter, you should be able to:

▶ �Discuss the geographic range of Homo erectus and compare it to that of earlier hominins.

▶ �Discuss why it isn’t yet fully established where the earliest H. erectus first evolved and describe which data you think provide the best evidence.

▶ �Compare and contrast the morphology of H. erectus with that of early Homo as well as with H. sapiens.

▶ �Compare and contrast the Dmanisi discoveries with H. erectus from Africa and Europe and discuss how the Dmanisi hominins complicate earlier hypotheses regarding hominin dispersal.

▶ �Discuss what sorts of tools are associated with H. erectus and what they tell us about the hominins’ cultural adaptations.

307

It’s estimated that more than 1 mil-lion people now cross national bor-ders every day. Some travel for busi- ness, some for pleasure, and others may be seeking refuge from persecu- tion in their own countries. Regard- less, it seems that modern humans have wanderlust—a desire to see dis- tant places. Our most distant hominin ancestors were essentially homebod- ies, staying in fairly restricted areas, exploiting the local resources, and try- ing to stay out of harm’s way. In this respect, they were much like other pri- mate species.

One thing is certain: All these early hominins were restricted to Africa. When did hominins first leave Africa? What were they like, and why did they leave their ancient homeland? In what ways did they differ physically from their australopith and early Homo fore- bears, and did they have new behav- ioral and cultural capabilities that helped them successfully exploit new environments?

It would be a romantic misconcep- tion to think of these first hominin transcontinental emigrants as “brave pioneers, boldly going where no one had gone before.” They weren’t delib- erately striking out to go someplace in particular. It’s not as though they had a map! Still, for what they did, deliberate or not, we owe them a lot.

Sometime close to 2 mya, something decisive occurred in human evolution. As the title of this chapter suggests, for the first time, hominins expanded widely out of Africa into other areas of the Old World. Because all the early

11The First Dispersal of the Genus Homo: Homo erectus and Contemporaries

fossils have been found only in Africa, it seems that hominins were restricted to that continent for perhaps as long as 5 million years. The later, more widely dispersed hominins were quite differ- ent both anatomically and behavior- ally from their African ancestors. They were much larger in body size, more committed to a completely terrestrial habitat, used more elaborate stone tools, and probably supplemented their diets with meat.

There is some variation among the different geographical groups of these highly successful hominins, and anthropologists still debate how to classify them. In particular, discover- ies from eastern Europe over the last couple of decades have forced a major reevaluation of exactly which hominin species were the first to leave Africa (Fig. 11-1).

Student Learning Objectives

308 chapter 11 The First Dispersal of the Genus Homo: Homo erectus and Contemporaries

A F R I C A

ITALY S P A I N

P O R T U G A L T U R K E Y

GREECE

K E N Y A

E T H I O P I A

ERITREA

S U D A N

E G Y P T

N I G E R

M A U R I T A N I A M A L I

N I G E R I A

S O M A L I A

N A M I B I A

L I B Y A

C H A D

SOUTH AFRICA

T A N Z A N I A

A N G O L A

A L G E R I A

MADAGASCARMOZAMBIQUE

B O T S W A N A

Z A M B I A

G A B O N

CENTRAL AFRICAN REPUBLIC

TUNISIA

M O R O C C O

UGANDA

SWAZILAND

LESOTHO

MALAWI

BURUNDI

TOGO

BENIN

GHANA

IVORY COAST

LIBERIASIERRA LEONE

GUINEA

BURKINAGAMBIA

CAMEROON

Z I M B A B W E

EQUATORIAL GUINEA

WESTERN SAHARA

DJIBOUTI

SENEGAL

GUINEA BISSAU

JORDAN

ISRAEL

LEBANON

KUWAIT

U. A. E.

OMAN

Y E M E N

SYRIA I R A Q I R A N

S A U D I A R A B I A

MALTA

RWANDA

D E M O C R A T I C

R E P U B L I C

O F T H E C O N G O

REP. OF THE

CONGO

Sima del Elefante/ Gran Dolina Dmanisi

East Turkana

West Turkana

Olduvai

Swartkrans

Nariokotome

Daka

Ceprano

D2700

WT 15000

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▲�Figure 11-1 Major Homo erectus sites and localities of other contemporaneous hominins.

309

M A L A Y S I A

I N D O N E S I A

P H I L I P P I N E S

SUMATRA BORNEO

BRUNEI

I N D I A

A U S T R A L I A

C H I N A

M O N G O L I A

TAIWAN

VIETNAM

CAMBODIA

THAILAND

LAOS

BURMA

BANGLADESH

K A Z A K H S T A N

KYRGYZSTAN

SOUTH KOREA

NORTH KOREA

JAPAN

Hexian (Lontandong Cave)

Zhoukoudian

Lantian (Chenjiawo)

Sangiran Trinil

Ngandong

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310 chapter 11 The First Dispersal of the Genus Homo: Homo erectus and Contemporaries

Nevertheless, after 2 mya, there’s less diversity among African homi- nins than is apparent in their pre- australopith and australopith prede- cessors. Consequently there is nearly universal agreement that the hominins found outside of Africa are all mem- bers of genus Homo. Thus taxonomic debates focus solely on how many spe- cies are represented. The early Homo species for which we have the most evi- dence, both physically and culturally, is called Homo erectus. Furthermore, this is the one group of early humans that most paleoanthropologists have rec- ognized for decades and still agree on. Thus, in this chapter we’ll focus our discussion on Homo erectus. We will, however, also discuss alternative inter- pretations that “split” the fossil sample into more species.

A New Kind of Hominin

The discovery of fossils now referred to as Homo erectus began in the nineteenth century. Later in this chap- ter, we’ll discuss the historical back- ground of these earliest discoveries in Java and the somewhat later discover- ies in China. For these fossils, as well as several from Europe and North Africa, a variety of taxonomic names have been suggested.

It’s important to realize that such taxonomic splitting was quite common during the late nineteenth century, in the early years of paleoanthropology. More systematic biological think- ing came to the fore only after World War II, with the incorporation of the Modern Synthesis into paleontology. Most of the fossils that were given these varied names are now placed in the species Homo erectus—or at the very least have been lumped into one genus (Homo).

In the last few decades, discoveries from East Africa of firmly dated fos- sils have established the clear presence of Homo erectus by 1.7 mya and even a little earlier in southeastern Europe

(Ferring et al., 2011). Some research- ers see several anatomical differences between these African representatives of an erectus-like hominin and their Asian cousins (hominins that almost everybody refers to as Homo erectus). Thus they place the African fossils into a separate species, one they call Homo ergaster (Andrews, 1984; Wood, 1991).

Though, as we will discuss, there are some anatomical differences between the African specimens and those from Asia, they are all clearly closely related and quite possibly represent geographi- cal varieties of a single species. We’ll thus refer to them collectively as Homo erectus.

Most analyses show that H. erec- tus represents a quite different kind of hominin than its more ancient African predecessors. An increase in body size and robusticity, changes in limb pro- portions, and greater encephalization all indicate that these hominins were more like modern humans in their adaptive pattern than their African ancestors were. It’s clear from most of the fossils usually classified as Homo erectus that a major adaptive shift had taken place—one setting hominin evolution in a distinctly more human direction.

We mentioned that there is con- siderable variation among different regional populations defined as Homo erectus. More recent discoveries show even more dramatic variation, suggest- ing that some of these hominins may not fit closely with this general adaptive pattern (more on this presently). For the moment, however, let’s review what most of these fossils look like.

The Morphology of Homo erectus

Homo erectus populations lived in very different environments over much of the Old World. They all, how- ever, shared several common physical traits.

311The First Homo erectus: Homo erectus from Africa

Body Size Anthropologists estimate that some H. erectus adults weighed well over 100 pounds, with an average adult height of about 5 feet 6 inches (McHenry, 1992; Ruff and Walker, 1993; Walker and Leakey, 1993). Another point to keep in mind is that H. erectus was quite sex- ually dimorphic—at least as indicated by the East African specimens.

Increased height and weight in H. erectus are also associated with a dramatic increase in robusticity. In fact, a heavily built body was to domi- nate hominin evolution not just during H. erectus times but through the long transitional era of premodern forms as well. Only with the appearance of anatomically modern H. sapiens did a more gracile skeletal structure emerge, one that still characterizes most mod- ern populations.

Brain Size Although Homo erectus differs in sev- eral respects from both early Homo and Homo sapiens, the most obvious feature is cranial size—which is closely related to brain size. Early Homo had cranial capacities ranging from as small as 500 cm³ to as large as 800 cm³. H. erectus, on the other hand, shows considerable brain enlarge- ment, with a cranial capacity of about 700* to 1,250 cm³ (and a mean of approximately 900 cm³).

As we’ve discussed, brain size is closely linked to overall body size. So it’s important to note that along with an increase in brain size, H. erectus was also considerably larger than ear- lier members of the genus Homo. In fact, when we compare H. erectus with the larger-bodied early Homo individu- als, relative brain size is about the same

*Even smaller cranial capacities are seen in recently discovered fossils from the Caucasus region of southeastern Europe at a site called Dmanisi. We’ll discuss these fossils In a moment.

(Walker, 1991). What’s more, when we compare the relative brain size of H. erectus with that of H. sapiens, we see that H. erectus was considerably less encephalized than later members of the genus Homo.

Cranial Shape Homo erectus crania display a highly distinctive shape, partly because of increased brain size but probably more correlated with increased body size. The ramifications of this heavily built cranium are reflected in thick cranial bone (in most specimens), large brow- ridges (supraorbital tori) above the eyes, and a projecting nuchal torus at the back of the skull (Fig.11-2).

The braincase is long and low, receding from the large browridges with little forehead development. Also, the cranium is wider at the base com- pared with earlier and later species of genus Homo. The maximum cranial breadth is below the ear opening, giv- ing the cranium a pentagonal shape (when viewed from behind). In con- trast, the skulls of early Homo and H. sapiens have more vertical sides, and the maximum width is above the ear openings.

Most specimens also have a sagit- tal keel running along the midline of the skull. Very different from a sagit- tal crest, the keel is a small ridge that runs front to back along the sagittal suture. The sagittal keel, browridges, and nuchal torus don’t seem to have served an obvious function, but most likely reflect bone buttressing in a very robust skull.

The First Homo erectus: Homo erectus from Africa

Where did Homo erectus first appear? The answer seems fairly simple: Most likely, this species nuchal torus (nuke´-ul) (nucha,

meaning “neck”) a projection of bone in the back of the cranium where neck muscles attach. these muscles hold up the head.

312 chapter 11 The First Dispersal of the Genus Homo: Homo erectus and Contemporaries

Low forehead

Zhoukoudian

O.H. 9

ER 3733

Zhoukoudian

Ngandong 5

Thick cranial bone

Supraorbital torus (browridge)

Nuchal torus

Sagittal ridge

(Lateral view)

Fairly large posterior teeth

Broad at base

(Rear view)

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▲�Figure 11-2 Morphology and variation in Homo erectus.

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313The First Homo erectus: Homo erectus from Africa

initially evolved in Africa. Two impor- tant pieces of evidence help to confirm this hypothesis. First, all of the earlier hominins prior to the appearance of H. erectus come from Africa. What’s more, by 1.7 mya, there are well-dated fossils of this species at East Turkana, Kenya, and not long after that at other sites in East Africa.

But there’s a small wrinkle in this neat view. We now know that at about 1.8 mya, similar populations were already living far away in southeastern Europe, and by 1.6 mya, in Indonesia. So, adding these pieces to our puzzle, it seems likely that H. erectus first arose in East Africa and then very quickly migrated to other continents; never- theless, as we’ll see shortly, the dating of sites from Africa and elsewhere does not yet clearly confirm this hypothesis. Let’s first review the African H. erectus specimens dated at 1.7 to 1 mya, and then we’ll discuss those populations that emigrated to Europe and Asia.

The earliest of the East African H. erectus fossils come from East Turkana, from the same area where earlier australopith and early Homo fossils have been found (see Chapter 10). Indeed, it seems likely that in East Africa around 2.0 to 1.8 mya, some form of early Homo evolved into H. erectus.

The most significant H. erectus fossil from East Turkana is a nearly complete skull (ER 3733; Fig. 11-3). Recently redated at 1.7 mya, this fos- sil is about the same age (or even just a little younger) than some other fos- sils outside of Africa; nevertheless, for now, it certainly is the oldest known member of this species from Africa (Lepre and Kent, 2010). The cranial capacity is estimated at 848 cm³, in the lower range for H. erectus (700 to 1,250 cm³), which isn’t surprising con- sidering its early date. A second very significant find from East Turkana is notable because it has the smallest cra- nium of any H. erectus specimen from anywhere in Africa. Dated to around 1.5 mya, the skull has a cranial capac- ity of only 691 cm³. As we’ll see shortly, there are a couple of crania from south-

eastern Europe that are even smaller. The small skull from East Turkana also shows more gracile features (such as smaller browridges) than do other East African H. erectus individuals, but it preserves the overall H. erectus vault shape. It’s been proposed that perhaps this individual is a female and that the variation indicates a very high degree of sexual dimorphism in this species (Spoor et al., 2007).

Another remarkable discov- ery was made in 1984 by Kamoya Kimeu, a member of Richard Leakey’s team known widely as an outstand- ing fossil hunter. Kimeu discovered a small piece of skull on the west side of Lake Turkana at a site known as Nariokotome. Excavations produced the most complete H. erectus skeleton ever found (Fig. 11-4). Known prop- erly as WT 15000, the almost complete skeleton includes facial bones, a pelvis, and most of the limb bones, ribs, and vertebrae; it is chronometrically dated to about 1.6 mya.

Such well-preserved postcranial ele- ments make for a very unusual and highly useful discovery, because these elements are scarce at other H. erectus sites. The skeleton is that of an adoles- cent about 8 years of age with an esti- mated height of about 5 feet 3 inches (Walker and Leakey, 1993; Dean and Smith, 2009).

◀�Figure 11-3 Nearly complete skull of Homo erectus from East Lake Turkana, Kenya, dated to approximately 1.7 mya.

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▲�Figure 11-4 WT 15000 from Nariokotome, Kenya: The “Nariokotome boy” is the most com- plete H. erectus specimen yet found.

Nariokotome (nar´-ee-oh-koh´-tow-may)

314 chapter 11 The First Dispersal of the Genus Homo: Homo erectus and Contemporaries

Some estimates have hypothesized that the adult height of this individual could have been about 6 feet. However, this conclusion is contentious, since it assumed that the growth pattern of this species was similar to that of mod- ern humans. But more recent and more detailed analyses find the developmen- tal pattern in this and other H. erec- tus individuals to actually be more like that of an ape (Dean and Smith, 2009). What’s more, it now seems unlikely that this individual would have expe- rienced the typical adolescent growth spurt seen in modern humans (see Chapter 16). Indeed, the most recent estimates suggest that had he lived, the Nariokotome youth would have grown to a full adult stature of perhaps only about 64 inches (Graves et al., 2010). This may be a minimum estimate; other paleoanthropologists think that the adult stature may have been closer to 69 inches.

Nevertheless, the postcranial bones look very similar, though not quite identical, to those of modern humans. And the recent publication describing additional vertebral and rib fragments indicates that the modern human spine and rib cage shape were already present (Haeusler, Schiess, and Boeni, 2011). The cranial capacity of WT 15000 is estimated at 880 cm³. Brain growth was nearly complete, and the adult cranial capacity would have been approxi- mately 909 cm³, or twice that of the australopith mean (Begun and Walker, 1993; Falk, 2012).

Other important H. erectus finds have come from Olduvai Gorge, in Tanzania; they include a very robust skull discovered there by Louis Leakey in 1960. The skull is dated at 1.4 mya and has a well-preserved cranial vault with just a small part of the upper face. Estimated at 1,067 cm³, its cranial capacity is the largest of all the African H. erectus specimens. The browridge is huge, the largest known for any hom- inin, but the walls of the braincase are relatively thin. This last characteristic is seen in most East African H. erectus specimens; in this respect, they differ

from Asian H. erectus, in which cranial bones are thick.

Three other sites from Ethiopia have yielded H. erectus fossils, the most noteworthy coming from the Gona area and the Daka locale, both in the Awash River region of eastern Africa (Gilbert and Asfaw, 2008). As you’ve seen, numerous remains of ear- lier hominins have come from this area (see Chapter 10 and Appendix C on the Anthropology CourseMate at Cengagebrain.com).

A recently discovered nearly com- plete female H. erectus pelvis comes from the Gona area in Ethiopia and is dated to approximately 1.3 mya (Simpson et al., 2008). It is a particu- larly interesting find because H. erec- tus postcranial remains are so rare, and this is the first H. erectus female pelvis yet found. The Gona pelvis is very different from the Nariokotome pelvis and is unusual for its consider- able width, along with a short stature. It’s possible that this may reflect con- siderable sexual dimorphism. This fossil also reveals some tantalizing glimpses of likely H. erectus growth and development. The pelvis has a very wide birth canal, indicating that quite large-brained infants could have devel- oped in utero (before birth); in fact, it’s possible that a newborn H. erec- tus could have had a brain that was as large as what’s typical for modern human babies (DeSilva, 2011). These factors indicate a modern compro- mise between the demands of obligate bipedalism and that of birthing large- brained infants.

This evidence has led research- ers to suggest that H. erectus prena- tal brain growth was more like that of later humans and quite different from that found in apes or in australopiths such as Lucy. However, it’s also evi- dent that H. erectus brain growth after birth was more rapid than it is in mod- ern humans. The Gona female was in some ways quite primitive, especially her unusually small body size (approxi- mately 81 pounds, as estimated by the size of her hip joint). Some anthro-

Who Were the Earliest African Emigrants? 315

pologists conclude from this evidence that the Gona pelvis may actually have come from an australoptith rather than from H. erectus (or any other species of Homo) (Ruff, 2010).

Another recent discovery from the Middle Awash of Ethiopia of a mostly complete cranium from Daka is also important because this individual (dated at approximately 1 mya) is more like Asian H. erectus than are most of the earlier East African remains we’ve discussed (Asfaw et al., 2002). Consequently, the suggestion by sev- eral researchers that East African fossils are a different species from (Asian) H. erectus isn’t supported by the morphology of the Daka cranium (Fig. 11-5).

Who Were the Earliest African Emigrants?

The fossils from East Africa imply that a new adaptive pattern in human evolution appeared in Africa not long after 2 mya. Until recently, H. erectus sites outside Africa all have shown dates later than the earliest finds of this species in Africa, lead-

ing paleoanthropologists to assume that the hominins who migrated to Asia and Europe descended from ear- lier African ancestors. Also, these travelers look like Homo, with longer limbs and bigger brains. Because H. erectus originated in East Africa, they were close to land links to Eur- asia (through the Middle East) and thus were prob- ably the first to leave the continent. We can’t be sure why these hominins left— were they following ani- mal migrations, or was it simply population growth and expansion?

What we do know is that we’re see- ing a greater range of physical varia- tion in the specimens outside of Africa and that the emigration out of Africa happened earlier than we had previ- ously thought. Current evidence shows H. erectus in East Africa about 1.7 mya, while similar hominins were living in the Caucasus region of southeast- ern Europe even a little earlier, about

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▲�Figure 11-5 Daka cranium from the Middle Awash region of Ethiopia, dated to 1.0 mya. This specimen shows many similarities with Homo erectus finds from Indonesia and China as well as Europe.

Key Homo erectus Discoveries from Africa

Date Site Evolutionary Significance

1.4 mya Olduvai Large individual, very robust (male?) H. erectus

1.6 mya Nariokotome, W. turkana

Nearly complete skeleton; young male

1.7 mya e. turkana Oldest well-dated H. erectus in africa; great amount of variation seen among individuals, possibly due to sexual dimorphism

At a Glance

316 chapter 11 The First Dispersal of the Genus Homo: Homo erectus and Contemporaries

1.8 mya.** Eventually hominins made it all the way to the island of Java, Indonesia, by 1.6 mya! It took H. erectus less than 200,000 years to travel from East Africa to Southeast Asia. Let’s look at this fascinating evidence.

The site of Dmanisi, in the Republic of Georgia, has produced several indi- viduals, giving us a unique look at these first possible travelers. The age of this crucial site has recently been radiomet- rically redated to 1.81 mya (Garcia et al., 2010). The Dmanisi crania are similar to those of H. erectus (for example, the long, low braincase, wide base, and sag- ittal keeling; see especially Fig. 11-6b, and compare with Fig. 11-2). However, other characteristics of the Dmanisi individuals are different from other hominins outside Africa. In particu- lar, the most complete fossil (specimen 2700; see Fig. 11-6c) has a less robust and thinner browridge, a projecting lower face, and a relatively large upper canine. At least when viewed from the front, this skull is more reminiscent of the smaller early Homo specimens from East Africa than it is of H. erectus. Also, specimen 2700’s cranial capacity is very small—estimated at only 600 cm³, well within the range of early Homo. In fact, all four Dmanisi crania so far described have relatively small cranial capaci- ties—the other three being estimated at 630, 650, and 780 cm³.

Probably the most remarkable find from Dmanisi is the most recently dis-

* Note that these dates are based solely on what has been discovered so far.

covered skull. This nearly complete cranium is of an older adult male; and surprisingly for such an ancient find, he died with only one tooth remaining in his jaws (Lordkipanidze et al., 2006). Because his jawbones show advanced bone loss (which occurs after tooth loss), it seems that he lived for several years without being able to chew his food efficiently (Fig. 11-7). As a result, it probably would have been difficult for him to maintain an adequate diet.

Researchers have also recovered some stone tools at Dmanisi. The tools are similar to the Oldowan industry from Africa, as would be expected for a site dated earlier than the beginning of the Acheulian industry; this later and very important tool industry is first found associated with African H. erec- tus about 1.6 mya.

The most recent evidence from Dmanisi includes several postcranial bones coming from at least four indi- viduals (Lordkipanidze et al., 2007). This evidence is especially important because it allows us to make compari- sons with what is known of H. erectus from other areas. The Dmanisi fos- sils have an unusual combination of traits. They weren’t especially tall, hav- ing an estimated height ranging from about 4 feet 9 inches to 5 feet 5 inches. Certainly, based on this evidence, they seem smaller than the full H. erec- tus specimens from East Africa or Asia. Yet, although very short in stature, they still show body proportions (such as leg length) like that of H. erectus (and H. sapiens) and quite different from that seen in earlier hominins.

Dmanisi (dim´-an-eese´-ee)

Acheulian (ash´-oo-lay-en) pertaining to a stone tool industry from the early and Middle pleistocene; characterized by a large proportion of bifacial tools (flaked on both sides). acheulian tool kits are common in africa, Southwest asia, and western europe, but they’re thought to be less com- mon elsewhere. also spelled acheulean.

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▲�Figure 11-6 Dmanisi crania discovered in 1999 and 2001 and dated to 1.8 to 1.7 mya. (a) Specimen 2282. (b) Specimen 2280. (c) Specimen 2700.

317Homo erectus from Indonesia

Based on the evidence from Dmanisi, we can assume that Homo erectus was the first hominin to leave Africa. Although the Dmanisi speci- mens are small in both stature and cranial capacity, they have specific characteristics that identify them as H. erectus (for example, a sagittal keel and low braincase). So for now, the Dmanisi hominins are thought to be H. erectus, although an early and quite different variety from that found almost anywhere else.

The recent evidence raises impor- tant and exciting possibilities. The Dmanisi findings suggest that the first hominins to leave Africa were quite possibly a small-bodied very early form of H. erectus, possessing smaller brains than later H. erectus and carrying with them a typical African Oldowan stone tool culture.

Also, the Dmanisi hominins had none of the adaptations hypothesized to be essential to hominin migration— that is, being tall and having relatively large brains. Another explanation may be that there were two migrations out of Africa at this time: one consisting of the small-brained, short- statured Dmanisi hominins and an almost immediate second migration that founded the well-recognized H. erec- tus populations of Java and China. The scientific community has only just recently reached a point where it is able to absorb these data, though it’s still too soon to predict what further revi- sions may be required.

Homo erectus from Indonesia

After the publication of On the Origin of Species, debates about evolution were prevalent throughout Europe. While many theorists sim- ply stayed home and debated the mer- its of natural selection and the likely course of human evolution, one young Dutch anatomist decided to go find evidence of it. Eugene Dubois (1858– 1940) enlisted in the Dutch East Indian

Army and was shipped to the island of Suma- tra, Indonesia, to look for what he called “the missing link.”

In October 1891, after moving his search to the neighboring island of Java, Dubois’ field crew unearthed a skullcap along the Solo River near the town of Trinil—a fossil that was to become interna- tionally famous as the first recognized human ancestor (Fig. 11-8). The following year, a human femur was recovered about 15 yards upstream in what Dubois claimed was the same level as the skullcap, and he assumed that the skullcap (with a cra- nial capacity of slightly over 900 cm³) and the femur belonged to the same individual.

Counting the initial find plus later discoveries, so far, all the Javanese H. erectus fossil remains have come from six sites located in the east- ern part of the island. The dating of these fossils has been hampered by the complex nature of Javanese geology, but it’s generally accepted that most of the fossils belong to the Early to Middle Pleistocene and are between 1.6 and 1 million years old. The island of Java con- tinues to yield new hominin fos- sils, with the discovery in 2001 of a H. erectus upper jaw at the fossil- rich Sangiran Dome (see “A Closer Look,” pp. 318–319). Very well- controlled 40Ar/39Ar dating places this fossil very close to an age of 1.5 mya. Comparisons of this newly described jaw with Chinese and Western Homo erectus (from Georgia and Africa), as well as with Homo habilis reveal some interesting differences. These differ- ences seem to indicate that there were two separate population sources for the earlier Sangiran H. erectus and later Zhoukoudian H. erectus, which

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▲�Figure 11-7 The most recently dis- covered cranium from Dmanisi, almost totally lacking in teeth (with both upper and lower jaws showing advanced bone resorption).

Pleistocene the epoch of the cenozoic from 1.8 mya until 10,000 ya. Frequently referred to as the Ice age, this epoch is associated with continental glacia- tions in northern latitudes.

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▲�Figure 11-8 The famous Trinil skullcap discovered by Eugene Dubois near the Solo River in Java. Discovered in 1891, this was the first fossil human found outside of Europe or Africa.

318

you will be introduced to in a moment (Zaim et al., 2011).

What’s more, there was also a very late-surviving H. erectus group in Java that apparently managed to sur- vive there until less than 100,000 years ago. These fossils from the Ngandong site are by far the most recent group of H. erectus fossils from Java or any- where else. At Ngandong, an excava- tion along an ancient river terrace pro- duced 11 mostly complete hominin skulls. Some estimates of the age of the Ngandong H. erectus fossils sug- gested an age of only 50,000 to 25,000 years ago (ya). These dates are quite controversial, but further evidence is establishing more strongly a very late survival of H. erectus in Java (approxi-

mately 70,000 to 40,000 ya) (Yokoyama et al., 2008). So these individuals would be contemporary with H. sapiens— which, by this time, had expanded widely throughout the Old World and into Australia around 60,000 to 40,000 ya. Recent work on the old excavation site of Ngandong (first excavated in the early 1930s) has led to a rediscovery of the fossil bed where all the H. erectus individuals had been found (Ciochon et al., 2009). New dating techniques and fossil identification will be undertaken to better understand site formation and taphonomy. As we’ll see in Chapter 13, even later—and very unusual—hom- inins have been found not far away, apparently evolving in isolation on another Indonesian island.

In Search of Ancient Human Ancestors— and a Little Shade

“W hoops!” Upon hearing this excla-mation, my colleagues halt their progress along the narrow earthen walk- ways that outline the flooded rice paddies and make an emerald patchwork quilt on the Java landscape. They turn around and see that I’ve slipped. Again. Each misstep comes with some good-hearted ribbing as my comrades heave me back onto dry land. Each day we traverse the paddies by way of the thin dikes en route to our research site in central Java. Around us rise great cliffs of ancient soil, striated like an intricately layered cake. Rich green jewel tones dazzle the eye as we pass by peasants laboring in the fields under the hot sun. We, too, are in Java to work, but we toil for a different kind of produce—we seek answers about our early ancestor, homo erectus. As we tread across the paddies to a dusty oxcart path, our eyes comb the adjacent outcrops

for darkened silhouettes of fossils—care- fully, we note their locations. By the time we reach our destination, our backpacks are filled with curious remains—this one a tooth of a fossil deer, that one a piece of ancient crocodile bone—but no humans. All the fossils are stained crimson or black by the very soils in which they have lain for nearly a million years. As we begin to exam- ine the exposed sediments, we resume our search for more fossils, our sweat-soaked shirts sticking to our skin. It’s 9 a.m. and were already tired and hot, but we quickly brush these distractions away. Our search has just begun.

For the past 12 years, my colleagues and I have been conducting fieldwork in the rice paddies of central Java. You might think it unusual to conduct scientific research in a rice paddy, but you have to “follow the fossils.” ancient sediments in our field area, the Sangiran Dome, were forced to the surface by the pressure of subterranean mud volcanoes about 120,000 years ago. What attracts us to the Sangiran Dome? It’s the 1- to 2-million- year-old fossils and sediments that have been unearthed by erosion and other natu- ral processes. this special series of events

means that the Sangiran Dome is prime for both discovering the fossils of early humans in their original environmental context and for radiometrically dating them using volca- nic sediments—a common occurrence in Java, an island formed by volcanoes.

If the cradle of human origins is africa, then asia was one of the playgrounds where our species grew and matured. around 2 mya, Homo erectus, our first widely traveled ancestor, left the african savanna homeland to expand its horizons in the larger world. the first stop on this species’ journey was in what is now the republic of Georgia in southeastern europe, where four skulls and a partial skeleton have been found. From here, we know that Homo erectus ventured onward to east asia and eventually Java. We know little about the features that attracted these hominins to the Javanese landscape or when the first migration to this island occurred. We do know that over time, the descendants of original Homo erectus immigrants evolved, giving us both full-sized primitive peoples with thick skulls and projecting browridges and later the diminutive “hobbits” on the island of Flores (you’ll meet them in chapter 13).

A Closer Look

319Homo erectus from Indonesia

Homo erectus from China The story of the first discoveries of Chinese H. erectus is another saga filled with excitement, hard work, luck, and misfortune. Europeans had known for a long time that “dragon bones,” used by the Chinese as medi- cine and aphrodisiacs, were actually ancient mammal bones. Scientists eventually located one of the sources of these bones near Beijing at a site called Zhoukoudian. Serious excavations were begun there in the 1920s, and in 1929, a fossil skull was discovered. The skull turned out to be a juvenile’s, and although it was thick, low, and rela-

tively small, there was no doubt that it belonged to an early hominin.

Zhoukoudian Homo erectus The fossil remains of H. erectus dis- covered in the 1920s and 1930s, as well as some more recent excavations at Zhoukoudian (Fig. 11-9), are by far the largest collection of H. erectus material found anywhere. This excellent sample includes 14 skullcaps (Fig. 11-10), other cranial pieces, and more than 100 iso- lated teeth, but only a scattering of post- cranial elements (Jia and Huang, 1990). Various interpretations to account for this unusual pattern of preservation have been offered, ranging from ritu- alistic treatment or cannibalism to the

every good realtor will tell you that it’s “location, location, location!” What was it about this asian setting—particularly the island of Java—that drew these ancient immigrants to colonize, as evidenced by the nearly 100 fossils of Homo erectus that have been unearthed there over the past century? Was it, perhaps, the rich volcanic soils and the vegetation they fostered that

attracted our distant relatives to the San- giran Dome, or did Homo erectus simply follow land-loving animals to the newly emergent environment of central Java? Our research centers on this very issue, using visual and geochemical clues from soils and plant and animal fossils to reconstruct the landscape of Java when Homo erectus first arrived millions of years ago.

As the sun dips low on the horizon, the valley of the Sangiran Dome dims. At the end of the day, our team reas- sembles for the trek back to our van, joking and chatting about the day’s finds. Our packs are heavy with samples of ancient soils, fossil shells and teeth, and rocks from ancient volcanic eruptions, all

being hauled back for analysis. We watch our shadowy likenesses in the murky water of the paddies as we trudge out of the mists of time. In an hour we’ll return to the hustle and bustle of Solo and wash away the dirt of ages. But before reentering civilization, we cast one last look into the past and wonder—“What was this place like during the time of our very ancient ancestors?” Was the landscape dominated by palms, mahogany, and cashew-bearing trees, as it is today, or was the countryside completely foreign? The full answers are just beyond our grasp. Perhaps today we carry in our backpacks the answers to these questions. Someday soon we’ll be able to look at this landscape as our ancestors did, linking our common histories with modern technology.

—Russell L. Ciochon

◀�Figure 1 The Sangiran Dome team, com- posed of researchers from the University of Iowa and the Bandung Institute of Technology, shown here doing a paleoecological analysis of the ancient strata of the dome.

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Zhoukoudian (Zhoh´-koh-dee´-en)

320 chapter 11 The First Dispersal of the Genus Homo: Homo erectus and Contemporaries

more mundane suggestion that the H. erectus remains are simply the left- overs of the meals of giant hyenas. The hominin remains were studied and casts were made immediately, which proved invaluable, because the original specimens were lost during the evacu- ation of Americans from China at the start of World War II.

The hominin remains from China belong to upward of 40 adults and chil- dren and together provide a good over- all picture of Chinese H. erectus. Like the materials from Java, they have typi- cal H. erectus features, including a large browridge and nuchal torus. Also, the skull has thick bones, a sagittal keel, and a protruding face and is broadest near the bottom. This site, along with others in China, has been difficult to date accurately. Although Zhoukoudian was previously dated to about 500,000 ya, a relatively new radiometric dat- ing technique that measures isotopes of aluminum and beryllium shows that Zhoukoudian is actually considerably older, with a dating estimate of approx- imately 780,000 ya (Ciochon and Bettis, 2009; Shen et al., 2009).

Cultural Remains from Zhoukoudian More than 100,000 artifacts have been

recovered from this vast site, which was occupied intermittently

for many thousands of years. The earliest

tools are generally crude and shape-

less, but they become more refined over time. Com- mon tools at the site are cores, perhaps used as “chop- pers,” but,

more impor- tantly, retouched

flakes were fash- ioned into scrapers,

points, burins, and awls (Fig. 11-11).

The way of life at Zhoukoudian has traditionally been described as that of hunter-gatherers who killed deer, horses, and other animals. Fragments of charred ostrich eggshells and abun- dant deposits of hackberry seeds unearthed in the cave seemed to sug- gest that these hominins supplemented their diet of meat by gathering herbs, wild fruits, tubers, and eggs. Layers of what appeared to be ash in the cave (over 18 feet deep at one point) were interpreted as indicating the use of fire by H. erectus.

However, with the rise of more modern techniques and the infusion of Western scientists, this idyllic pic- ture of Zhoukoudian life was shat- tered. Lewis Binford and colleagues (Binford and Ho, 1985; Binford and Stone, 1986a,b) reject the description of H. erectus as hunters and argue that the evidence clearly points more accurately to scavenging. Using advanced archae- ological analyses, Noel Boaz and col- leagues have even questioned whether the H. erectus remains at Zhoukoudian represent evidence of hominin habi- tation of the cave. By comparing the types of bones, as well as the damage to the bones, with that seen in contempo- rary carnivore dens, Boaz and Ciochon (2001) have suggested that much of the material in the cave likely accumulated through the activities of extinct giant hyenas. In fact, they hypothesize that most of the H. erectus remains, too, are the leftovers of hyena meals. Boaz and his colleagues do recognize that the tools in the cave, and possibly the cut marks on some of the animal bones, provide evidence of hominin activities at Zhoukoudian.

Probably the most intriguing archae- ological aspect of the presumed hom- inin behavior at Zhoukoudian has been the long-held assumption that H. erec- tus deliberately used fire inside the cave. Controlling fire was one of the major cultural breakthroughs of all pre- history. By providing warmth, a means of cooking, light to further modify tools, and protection, controlled fire would have been a giant technologi- cal innovation. However, in the course

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▼�Figure 11-10 Composite cranium of Zhoukoudian Homo erectus, recon- structed by Ian Tattersall and Gary Sawyer of the American Museum of Natural History in New York.

321Homo erectus from China

of further excavations at Zhoukoudian during the 1990s, researchers care- fully collected and analyzed soil sam- ples for distinctive chemical signatures that would show whether fire had been present in the cave (Weiner et al., 1998). They determined that burnt bone was only rarely found in association with tools. And in most cases, the burning appeared to have taken place after fos- silization—that is, the bones weren’t cooked. In fact, it turns out that the “ash” layers aren’t actually ash but nat- urally accumulated organic sediment. This last conclusion was derived from chemical testing that showed absolutely no sign of wood having been burnt inside the cave. Finally, the “hearths” that have figured so prominently in archaeological reconstructions of presumed fire control at this site apparently aren’t hearths at all. They are simply round depressions formed in the past by water.

Despite this debunking of some long-held beliefs, some potential early African sites have yielded evidence suggesting hominin control of fire, though many of these finds are con- troversial. However, a newly discov- ered cave site in South Africa, dated to 1 mya, has shown the best evidence yet of likely fire use based on archaeologi- cal finds of ash and burnt bone asso- ciated with Acheulian tools. Not only that, but it suggests that our ancestors controlled fire much earlier than we had thought (Berna et al., 2012). (See A Closer Look on pp. 322–323.)

Another provisional interpretation of Zhoukoudian’s cave geology suggests

that the cave wasn’t open to the out- side, as a habitation site would be, but was accessed only through a vertical shaft. This theory has led archaeologist Alison Brooks to remark, “It wouldn’t have been a shelter, it would have been a trap” (quoted in Wuethrich, 1998). These serious doubts about control of fire, coupled with the suggestive evi- dence of bone accumulation by carni- vores, have led anthropologists Boaz and Ciochon to conclude that the “Zhoukoudian cave was neither hearth nor home” (Boaz and Ciochon, 2001).

Other Chinese Sites More work has been done at Zhoukoudian than at any other Chinese site. Even so, there are other paleoanthropological sites worth men- tioning. Three of the more important regions outside of Zhoukoudian are Lantian County (including two sites, often simply referred to as Lantian), Yunxian County, and several discover- ies in Hexian County (usually referred to as the Hexian finds).

Dated to 1.15 mya, Lantian is older than Zhoukoudian (Zhu et al., 2003). The cranial remains of two adult H. erectus females have been found at the Lantian sites (Woo, 1966; Fig. 11-12a on p. 324). One of the specimens, an almost complete mandible contain- ing several teeth, is quite similar to those from Zhoukoudian.

Two badly distorted crania were discovered in Yunxian County, Hubei Province, in 1989 and 1990 (Li and Etler, 1992). A combination

Quartzite chopperFlint pointFlint awlGraver, or burin

▲�Figure 11-11 Chinese tools from Middle Pleistocene sites. (Adapted from Wu and Olsen, 1985.)

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322

of ESR and paleomagnetism dating methods (see Chapter 9) gives us an average dating estimate of 800,000 to 580,000 ya. If the dates are correct, this would place Yunxian at a simi- lar age to Zhoukoudian in the Chinese sequence. Due to extensive distor- tion of the crania from ground pres- sure, it was very difficult to compare these crania with other H. erectus fos- sils; more recently, however, French paleoanthropologist Amélie Vialet has restored the crania using sophisticated imaging techniques (Vialet et al., 2005). And from a recent analysis of the fauna

and paleoenvironment at Yunxian, the H. erectus inhabitants are thought to have had limited hunting capabilities, since they appear to have been restrict- ed to the most vulnerable prey, namely, the young and old animals.

In 1980 and 1981, the remains of several individuals, all bearing some resemblance to similar fos- sils from Zhoukoudian, were recov- ered from Hexian County, in south- ern China (Wu and Poirier, 1995; see Fig. 11-12b). A close relationship has been postulated between the H. erec- tus specimens from the Hexian finds

Dragon Bone Hill: Cave Home or Hyena Den?

About 30 miles southwest of Beijing, near Zhoukoudian, is the locality known as Dragon Bone hill. In the 1920s and 1930s, this cave site yielded the first (and still the largest) cache of fossils of Homo erectus, historically known as peking Man. the remains of about 45 individuals, along with thousands of stone tools, debris from tool manufacture, and thousands

of animal bones, were contained within the 100-foot-thick deposits that once completely filled the original cave. Some evidence unearthed at the site suggests to many researchers that these creatures, who lived from about 800,000 to 400,000 ya, had mastered the use of fire and practiced cannibalism. Still, despite years of excava- tion and analysis, little is certain about what occurred here long ago.

to most of the early excavators, the likely scenario was that these particular early humans lived in the cave where their bones and stone tools were found. the animal bones were likely the remains of meals—proof of their hunting expertise. a more sensational view, first advanced

in 1929, was that the cave contained evidence of cannibalism. Skulls were con- spicuous among the remains, suggesting to chinese paleoanthropologist Jia Lanpo that these might be the trophies of headhunters.

But another chinese paleoanthropolo- gist—pei Wenzhong, who codirected the early Zhoukoudian excavations—believed that hyenas , not human killers, were responsible for the presence and condition of the skulls and other accompanying dam- age. In 1939, his views were bolstered by the emerging science of taphonomy, which is the study of how, after death, animal and plant remains become modified, moved, buried, and fossilized (see chapter 9). pub- lished observations on the way hyenas at

A Closer Look

▲�Figure 1 These illustrations demonstrate the two interpreta- tions of the remains from Dragon Bone Hill: (a) the more traditional

cave home model and (b) the newer, and probably more accu- rate, hyena den model.

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323Asian and African Homo erectus: A Comparison

and from Zhoukoudian (Wu and Dong, 1985). Dating of the Hexian remains is unclear, but they appear to be later than Zhoukoudian, perhaps by several hundred thousand years.

The Asian crania from Java and China share many similar features, which could be explained by H. erec- tus migration from Java to China per- haps around 1 mya. Asia has a much longer H. erectus habitation than Africa (1.8 mya to 40,000 or 70,000 ya versus 1.7 to 1 mya), and it’s important to understand the variation seen in this geographically dispersed species.

Asian and African Homo erectus: A Comparison

The Homo erectus remains from East Africa show several differ- ences from the Javanese and Chinese fossils. Some African cranial speci- mens—particularly ER 3733, presum- ably a female, and WT 15000, pre- sumably a male—aren’t as strongly buttressed at the browridge and nuchal torus, and their cranial bones aren’t as

the Vienna zoo fed on cow bones led later scientists to reject the idea of cannibalism, although they continued to look upon the cave as a shelter used by early humans equipped with stone tools and fire (as reflected in the title of The Cave Home of Peking Man, published in 1975).

In the mid- to late 1970s, however, Western scientists began to better appreci- ate and develop the field of taphonomy. One assumption of taphonomy is that the most common species at a fossil site and/or the best-preserved animal remains at the site are most likely the ones to have inhabited the area in life. Of all the mammal fossils from the cave, very few belonged to H. erec- tus—perhaps only 0.5 percent, suggesting that most of the time, this species did not live in the cave. What’s more, none of the H. erectus skeletons are complete. there’s a lack of limb bones—especially of forearms, hands, lower leg bones, and feet—indicat- ing that these individuals died somewhere else and that their partial remains were later carried to the cave. But how?

the answer is suggested by the remains of the most common and complete animal skeletons in the cave deposit—those of the giant hyena, Pachycrocuta brevirostris. had H. erectus, instead of being the mighty hunter of anthropological lore, simply met the same unhappy fate as the deer and other prey species in the cave? to test the

giant hyena hypothesis, scientists reex- amined the fossil casts and a few actual fossils of H. erectus from Zhoukoudian for evidence of carnivore damage. Surprisingly, two thirds of the H. erectus fossils displayed puncture marks from a carnivore’s large, pointed front teeth, most likely the canines of a hyena. What’s more, there were long, scraping bite marks, typified by U-shaped grooves along the bone, and fracture pat- terns comparable to those modern hyenas make when they chew bone. One of the H. erectus bones, part of a femur, even reveals telltale surface etchings from stomach acid, indicating it was swallowed and then regurgitated.

cut marks (made by stone tools) observed on several mammal bones from the cave suggest that early humans did sometimes make use of Zhoukoudian, even if they weren’t responsible for accumulating most of the bones. Stone tools left near the cave entrance also attest to their presence. Given its long history, the cave may have served a variety of occupants or at times have been configured as several separate, smaller shelters. another possibility is that, in a form of time sharing, early humans ventured part way into the cave during the day to scavenge on what the hyenas had not eaten and to find temporary shelter. they might not have realized that the ani- mals, which roamed at twilight and at night, were sleeping in the dark recesses a couple of hundred feet away.

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◀�Figure 2 A composite image of the skulls of Pachycrocuta and Homo erectus that shows how the giant hyena may have attacked the face. Recent studies have shown that many of the Homo erectus remains from Zhoukoudian show hyena damage.

324 chapter 11 The First Dispersal of the Genus Homo: Homo erectus and Contemporaries

thick. Indeed, some researchers are so impressed by these differences, as well as others in the post- cranial skeleton, that they’re arguing for a

separate species status for the Afri- can material, to distinguish it from the Asian samples. Bernard Wood, the leading proponent of this view, has suggested that the name Homo ergas- ter be used for the African remains and that H. erectus be reserved solely

for the Asian material (Wood, 1991). In addition, the very early dates now pos- tulated for the dispersal of H. erectus into Asia (Java) would argue that the Asian and African populations were separate (distinct) for more than 1 mil- lion years.

As a result of the discovery of the Daka cranium in Ethiopia and contin- ued comparison of these specimens, this species division has not been fully accepted; the current consensus (and the one we prefer) is to continue refer- ring to all these hominins as Homo

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b▶�Figure 11-12 (a) Reconstructed cranium of Homo erectus from Lantian, China, dated to approximately 1.15 mya. (b) Hexian cranium.

Key Homo erectus Discoveries from Asia

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Date Site Evolutionary Significance

70,000– 40,000 ya

Ngandong (Java)

Very late survival of H. erectus in Java

780,000 ya Zhoukoudian (china)

Large sample; most famous H. erectus site; shows some H. erectus populations well adapted to temperate (cold) environments

1.6 mya Sangiran (Java)

First discovery of H. erectus from anywhere; shows dispersal out of africa into southeast asia by 1.6 mya

At a Glance

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325Later Homo erectus from Europe

erectus (Kramer, 1993; Conroy, 1997; Rightmire, 1998; Asfaw et al., 2002). Therefore, as with some earlier homi- nins, our interpretation of H. erectus requires us to recognize a considerable degree of variation within this species. This high degree of variability is likely related to the vast differences in cli- matic and environmental conditions encountered by ancient humans in the West and in the East. Additionally, the vast distances and island dynam- ics encountered by Homo erectus in the East increased genetic drift, perhaps in some cases producing large enough biological differences to cause specia- tion (Larick and Ciochon, in press). We will explore this topic further in later chapters.

Later Homo erectus from Europe

We’ve talked about H. erectus in Africa, the Caucasus region, and Asia, but there are European speci- mens as well, found in Spain and Italy. Though not as old as the Dmanisi material, fossils from the Atapuerca region in northern Spain are signifi- cantly extending the antiquity of homi- nins in western Europe. There are sev- eral caves in the Atapuerca region, two of which (Sima del Elefante and Gran Dolina) have yielded hominin fossils contemporaneous with H. erectus.

The earliest find from Atapuerca (from Sima del Elefante) was discov- ered recently and dates to 1.2 mya, making it clearly the oldest hominin specimen yet found in western Europe (Carbonell et al., 2008). So far, just one specimen has been found here, a partial jaw with a few teeth. Very provisional analysis suggests that it most closely resembles the Dmanisi fossils. There are also tools and animal bones from the site. As at the Dmanisi site, the implements are simple flake tools simi- lar to those of the Oldowan. Some of the animal bones also bear the scars of hominin activity, with cut marks indi- cating butchering.

Gran Dolina is a later site, and based on specialized techniques discussed in Chapter 9, it’s dated to approxi- mately 850,000 to 780,000 ya (Parés and Pérez-González, 1995; Falguères et al., 1999). Because all the remains so far identified from both these caves at Atapuerca are fragmentary, assigning these fossils to particular species poses something of a prob- lem. Spanish paleoanthropologists who study the Atapuerca hominins have placed them into another (sepa- rate) species, which may represent a link between early Homo and the later hominins (Bermúdez de Castro et al., 1997; Arsuaga et al., 1999; Bermúdez de Castro et al., 2011). And though they may exhibit some modern fea- tures, there is speculation that the hominins of Gran Dolina engaged in a most startling behavior: cannibal- ism. What’s most unsettling about this practice is that the evidence suggests that this was not for ritual purpos- es or as a last resort. Cut and percus- sion marks on the hominin bones in question indicate that the bodies were processed much in the same way as any other animal (Carbonell et al., 2010).

Finally, the southern European discovery of a well-preserved cra- nium from the Ceprano site in cen- tral Italy may be the best evidence yet of H. erectus in Europe (Ascenzi et al., 1996). Provisional dating sug- gested a date between 900,000 and 800,000 ya (Fig. 11-13), but a recent

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▼�Figure 11-13 The Ceprano Homo erectus cranium from central Italy, recently dated to 450,000 ya. This is the best evidence for Homo erectus in Europe.

326 chapter 11 The First Dispersal of the Genus Homo: Homo erectus and Contemporaries

40Ar/39Ar study has indicated that it more likely dates only as far back as 353,000 ya (Nomade et al., 2011). Philip Rightmire (1998) has concluded that cranial morphology places this speci- men quite close to H. erectus. Italian researchers have proposed a differ- ent interpretation, which classifies the Ceprano hominin as a species sepa- rate from H. erectus. For the moment, the exact relationship of the Ceprano find to H. erectus remains to be fully determined.

After about 400,000 ya, the European fossil hominin record becomes increasingly abundant. More

fossils mean more variation, so it’s not surprising that interpretations regard- ing the proper taxonomic assessment of many of these remains have been debated, in some cases for decades. In recent years, several of these somewhat later “premodern” specimens have been regarded either as early representatives of H. sapiens or as a separate species, one immediately preceding H. sapiens. These enigmatic premodern humans are discussed in Chapter 12. A time line for the H. erectus discoveries dis- cussed in this chapter as well as other finds of more uncertain status is shown in Figure 11-14.

Gran Dolina (Atapuerca)

Dmanisi

Ceprano

Sima del Elefante (Atapuerca)

Hexian

Zhoukoudian

Yunxian

Lantian

Sangiran

Ngandong

Daka

Olduvai

Nariokotome

East Turkana

2.0 mya 1.8 mya 1.6 mya 1.4 mya 1.2 mya 1.0 mya 0.8 mya 0.6 mya 0.4 mya 0.2 mya

EAST AFRICA

JAVA

CHINA

EUROPE

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▲�Figure 11-14 Time line for Homo erectus discoveries and other con- temporary hominins. (Note: Most dates are only imprecise estimates. However, the dates from East African sites are chronometrically determined and are thus much more secure. The early dates from Java are also radiometric and are gaining wide acceptance.)

Key Homo erectus and Contemporaneous Discoveries from Europe

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??900,000– 350,000 ya

ceprano (Italy)

Well-preserved cranium; best evidence of full H. erectus morphology from any site in europe

1.2 mya Sima del elefante (atapuerca, Spain)

Oldest evidence of hominins in western europe, possibly not H. erectus

1.80 mya Dmanisi (republic of Georgia)

Oldest well-dated hominins outside of africa; not like full H. erectus morphology, but are small-bodied and small-brained

At a Glance

327Technological Trends During Homo erectus Times

Technological Trends During Homo erectus Times

The temporal span of H. erectus includes two different stone tool industries, one of which was probably first developed by H. erectus. Earlier finds indicate that H. erectus started out using Oldowan tools, which the H. erectus emigrants took with them to Dmanisi, Java, and Spain. The newer industry was invented (about 1.6 mya) after these early African emigrants left their original homeland for other parts of the Old World. This new tool kit is called the Acheulian. The impor- tant change in this kit was a core worked on both sides, called a biface (known widely as a hand axe or cleav- er; Fig. 11-15). The biface had a flat- ter shape than seen in the rounder earlier Oldowan cores (which were worked to make quick and easy flakes and were soon discarded). Beginning with the Acheulian culture, we find the first evidence that raw materials were being transported more consis- tently and for longer distances. When Acheulian tool users found a suitable piece of stone, they would often take it with them as they traveled from one place to another. This behavior sug- gests foresight: They likely knew that they might need to use a stone tool in the future and that this chunk of rock could later prove useful. This is a major change from the Oldowan, where all stone tools are found very close to their raw-material sources. With the biface as a kind of “Acheulian Swiss army knife,” these tools served to cut, scrape, pound, and dig. This most use- ful tool has been found in Africa, parts of Asia, and later in Europe. Take note as well that Acheulian tool kits also include several types of small tools (Fig. 11-16).

For many years, scientists thought that a cultural “divide” separated the Old World, with Acheulian technol- ogy found only in Africa, the Middle East, and parts of Europe (elsewhere, the Acheulian was presumed to be

absent). But more recently reported excavations from many sites in south- ern China have forced reevaluation of this hypothesis (Hou et al., 2000). The archaeological assemblages from southern China are securely dated at about 800,000 ya and contain numerous bifaces, very similar to contemporaneous Acheulian bifaces from Africa (see Fig. 11-15). New evidence from India dates the Acheulian in south- ern Asia to at least 1 mya (Pappu et al., 2011). It now appears likely that cultural traditions relating to stone tool technology were largely equivalent over the full geograph- ical range of H. erectus and its contemporaries.

Evidence of butchering is wide- spread at H. erectus sites; in the past, such evidence has been cited in arguments for consistent hunt- ing (researchers formerly inter- preted any association of bones and tools as evidence of hunting). But some studies now suggest that cut marks on bones from the H. erectus time period often overlie carnivore tooth marks. This would mean that hominins weren’t necessarily hunt- ing large animals but were scaveng- ing meat from animals killed by car- nivores. It’s also crucial to mention

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◀�Figure 11-15 Acheulian biface (“hand axe”), a basic tool of the Acheulian tradition.

▲�Figure 11-16 Small tools of the Acheulian industry. (a) Side scraper. (b) Point. (c) End scraper. (d) Burin.

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328 chapter 11 The First Dispersal of the Genus Homo: Homo erectus and Contemporaries

that they obtained a large amount of their daily calories from gathering wild plants, tubers, and fruits. Like hunter- gatherers of modern times, H. erectus individuals were most likely consum- ing most of their daily calories from plant materials.

Seeing the Connections: Interpretations of Homo erectus

Several aspects of the geographi-cal, physical, and behavioral pat- terns shown by Homo erectus seem clear. But new discoveries and more in-depth analyses are helping us to reevaluate our prior ideas. The fas- cinating Dmanisi hominins are per- haps the most challenging piece of this puzzle.

Early scenarios suggested that H. erectus was able to emigrate from Africa owing to more advanced tools and a more modern anatomy (longer legs, larger brains) compared to earlier African predecessors. Yet, now we see that what really happened was not this straightforward. Much like the Taung child changed our perspectives on early hominin evolution, the Dmanisi homi- nins surprisingly reveal that these very early Europeans still had small brains; moreover, in Dmanisi, Java, and Spain, these hominins were also still using Oldowan-style tools.

What becomes clear is that at least some of the earliest emigrants from Africa didn’t yet show the entire suite of H. erectus physical and behavioral traits. Additionally, the Dmanisi homi- nins exhibit a very wide range of vari- ability, making it tempting to conclude that more than one type of hominin is represented; but this is not likely, because all the fossils were found in the same geological context. This degree of apparent intraspecific variation is bio- logically noteworthy, and it’s influenc-

ing how paleoanthropologists interpret all of these fossil samples.

This growing awareness of the broad intraspecific variation among some hominins brings us to our second con- sideration: Is Homo ergaster in Africa a separate species from Homo erectus, as strictly defined in Asia? Although this interpretation was popular in the last decade, it’s now losing support. The finds from Dmanisi raise fundamen- tal issues of interpretation. For exam- ple, among four crania from one local- ity (see Fig. 11-6), we see more variation than between the African and Asian forms, which many researchers have interpreted as different species. Also, the discovery from Daka (Ethiopia) of a young African specimen with Asian traits further weakens the separate- species interpretation of H. ergaster.

The separate-species status of the early European fossils from Spain (Sima del Elefante and Gran Dolina) is also not yet clearly established. Recall also that no other western European hominin fossils are known until at least 500,000 years later. Nevertheless, it’s quite apparent that later in the Pleistocene, well-established hominin populations were widely dispersed in both Africa and Europe. These later premodern humans are the topic of the next chapter.

In looking back at the evolution of H. erectus, we realize how significant this early human was. H. erectus had greater limb length and thus more effi- cient bipedalism; was the first spe- cies with a cranial capacity approach- ing the range of H. sapiens; became a more efficient scavenger and exploited a wider range of nutrients, includ- ing meat; and ranged across the Old World, from Spain to Indonesia. In short, it was H. erectus that trans- formed hominin evolution to human evolution. As Richard Foley states, “The appearance and expansion of H. erectus represented a major change in adaptive strategy that influenced the subsequent process and pattern of human evolution” (1991, p. 425).

329Critical Thinking Questions

▶▶ Homo erectus remains have been found in Africa, Europe, and Asia dating from about 1.8 mya to at least 100,000 ya and probably even later; thus this species spanned a period of more than 1.5 million years.

▶▶ Homo erectus likely first appeared in East Africa and later migrated to other areas. This widespread and highly successful hominin displays a new and more modern pattern of human evolution.

▶▶ Homo erectus differs from early Homo, with a larger brain, taller stature, robust build, and changes in facial structure and cranial buttressing.

▶▶ Homo erectus and contemporaries introduced more sophisticated tools (as part of the Acheulian industry) and probably ate novel foods processed in new ways. By using these new tools—and at later sites possibly fire as well—they were also able to move into different environments and success- fully adapt to new conditions.

Summary of Main Topics

1. Why is the nearly complete skeleton from Nariokotome so important? What kinds of evi- dence does it provide?

2. Assume that you’re in the laboratory and have the Nariokotome skeleton as well as a skeleton of a modern human. First, given a choice, what age and sex would you choose for the comparative human skeleton, and why? Second, what similarities and differences do the two skeletons show?

3. What fundamental questions of interpretation do the fossil hominins from Dmanisi raise? Does this evidence completely overturn the earlier views (hypotheses) concerning H. erectus dispersal from Africa? Explain why or why not.

4. How has the interpretation of H. erectus behav- ior at Zhoukoudian been revised in recent years? What kinds of new evidence from this site have been used in this reevaluation, and what does that tell you about modern archaeological techniques and approaches?

Critical Thinking Questions

We know about the dispersal of early hominins out of Africa from a large number of fossils found in Africa, Asia, and Europe. Fairly recently, more discoveries have been made in East Africa, Asia (Indonesia), and Europe (Republic of Georgia and Spain). Accurate radiometric dating techniques have been used in Africa, Indonesia, and Georgia, and new methods have

recently established more accurate dating for early Chinese fossils. Archaeological as well paleoecological studies have shown the variety of stone tools used by H. erectus as well as aspects of their behavioral adapta- tions (e.g., were they mostly hunters or scavengers? It seems they were mostly the latter).

How Do We Know?

The immediate predecessors of modern humans, including the

Neandertals, were much like us, but had some anatomical and

behavioral differences.

Connections

Hominins began to dis- perse out of Africa around 2 million years ago, and during the next 1 million years inhabited much of

Eurasia.

Modern humans first evolved in Africa and later spread to other areas of the world, where they

occasionally interbred with Neandertals and other pre-

modern humans.

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After mastering the material in this chapter, you should be able to:

▶ �Describe the general time frame when earlier premodern humans (mostly classified as Homo heidelbergensis) lived and in what areas of the world they have been found.

▶ �Compare and contrast the physical characteristics of H. heidelbergensis with H. erectus.

▶ �Describe the time frame during which Neandertals lived and where their remains have been found.

▶ �Compare and contrast the physical characteristics of Neandertals with those of modern humans.

▶ �Explain what the information from the whole genome sequencing of Neandertals tells us and why this is important.

▶ �Discuss some of the major cultural innovations displayed by Neandertals and how these compare with those of earlier hominins.

331

What do you think of when you hear the term Nean-dertal? Most people think of imbecilic hunched-over brutes. Yet Neandertals had brains at least as large as ours, and they showed many sophisticated cultural capabilities. What’s more, they definitely weren’t hunched over but stood fully erect (as hominins had for millions of years). In fact, Neandertals and their imme- diate predecessors could easily be called human.

That brings us to possibly the most basic of all questions: What does it mean to be human? The meaning of this term is highly varied, encompass- ing religious, philosophical, and bio- logical considerations. As you know, physical anthropologists primarily concentrate on the biological aspects of the human organism. All living peo- ple today are members of one species, sharing a common anatomical pat- tern and similar behavioral potentials. We call hominins like us “modern” Homo sapiens, and in the next chap- ter, we’ll discuss the origin of forms that were essentially identical to people living today.

When in our evolutionary past can we say that our predecessors were obvi- ously human? Certainly, the further back we go in time, the less hominins look like modern Homo sapiens. This is, of course, exactly what we’d expect in an evolutionary sequence.

12 Premodern Humans

We saw in Chapter 11 that Homo erectus took crucial steps in the human direction and defined a new adaptive level in human evolution. In this chap- ter, we’ll discuss the hominins who con- tinued this journey. Both physically and behaviorally, they’re much like modern Homo sapiens, though they still show several significant differences. So while most paleoanthropologists are com- fortable referring to these hominins as “human,” we must qualify this recog- nition a bit to set them apart from fully modern people. Thus, in this text, we’ll refer to these fascinating immediate predecessors as “premodern humans.”

Student Learning Objectives

chapter 12 Premodern Humans 332

When, Where, and What

Most of the hominins discussed in this chapter lived during the Middle Pleistocene, a period begin- ning 780,000 ya and ending 125,000 ya. In addition, some of the later premod- ern humans, especially the Neander- tals, lived well into the Late Pleisto- cene (125,000 to 10,000 ya).

The Pleistocene The Pleistocene has been called the Ice Age because, as had occurred before in geological history, it was marked by periodic advances and retreats of mas- sive continental glaciations. During glacial periods, when temperatures dropped dramatically, ice accumulated because more snow fell each year than melted, causing the advance of mas- sive glaciers. As the climate fluctu- ated, it sometimes became much warmer. During these interglacials, the ice that had built up during the glacial periods melted and the glaciers retreated back toward the earth’s polar regions. The Pleistocene was char- acterized by numerous advances and retreats of ice, with at least 15 major and 50 minor glacial advances docu-

mented in Europe alone (Delson et al., 2000).

These glaciations, which envel- oped huge swaths of Europe, Asia, and North America as well as Antarctica, were mostly confined to northern lati- tudes. Hominins living at this time— all still restricted to the Old World— were severely affected as the climate, flora, and animal life shifted during these Pleistocene oscillations. The most dramatic of these effects were felt in Europe and northern Asia—less so in southern Asia and Africa.

Still, the climate also fluctuated in the south. In Africa, the main effects were changing rainfall patterns. During glacial periods, the climate in Africa became more arid, while during inter- glacials, rainfall increased. The chang- ing availability of food resources affect- ed not only the hominins permanently residing in Africa; but probably even more importantly, also their migration routes, which swung back and forth. For example, during glacial periods (Fig. 12-1), the Sahara Desert expanded, blocking migration in and out of sub- Saharan Africa (Lahr and Foley, 1998).

In Eurasia, glacial advances also greatly affected migration routes. As the ice sheets expanded, sea lev- els dropped, making more north- ern regions uninhabitable, and some

Middle Pleistocene the portion of the pleistocene epoch beginning 780,000 ya and ending 125,000 ya.

Late Pleistocene the portion of the pleistocene epoch beginning 125,000 ya and ending approximately 10,000 ya.

glaciations climatic intervals when continental ice sheets cover much of the northern continents. Glaciations are associ- ated with colder temperatures in northern latitudes and more arid conditions in south- ern latitudes, most notably in africa.

interglacials climatic intervals when continental ice sheets are retreating, eventually becoming much reduced in size. Interglacials in northern latitudes are asso- ciated with warmer temperatures, while in southern latitudes the climate becomes wetter.

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▲�Figure 12-1 Changing Pleistocene environments in Africa.

AFRICA

Interglacial period (increased rainfall)

Glacial period (reduced rainfall, increased aridity,

expansion of deserts)

Savannas Forests

Sahara at maximum extent

INDIAN OCEAN

ATLANTIC OCEAN

INDIAN OCEAN

ATLANTIC OCEAN

When, Where, and What 333

key passages between areas became blocked by glaciers. For example, dur- ing glacial peaks, much of western Europe would have been cut off from the rest of Eurasia (Fig. 12-2).

During the warmer—and in the south wetter—interglacials, the ice sheets shrank, sea levels rose, and cer- tain migration routes reopened (for example, from central Europe into western Europe). Clearly, to under- stand Middle Pleistocene hominins, it’s crucial to view them within their shifting Pleistocene world. As we will see, this had important implications for gene flow, causing some popula- tions to become isolated, leading to genetic drift.

Dispersal of Middle Pleistocene Hominins Like their Homo erectus predecessors, later hominins were widely distrib- uted in the Old World. Discoveries of their presence have come from three continents—Africa, Asia, and Europe. For the first time, Europe became more permanently and densely occu- pied, with evidence of Middle Pleisto- cene hominins from England, France, Spain, Germany, Italy, Hungary, and Greece. Africa, as well, probably con- tinued as a central area of hominin occupation, and finds have come from northern, eastern, and southern Africa. Finally, Asia has yielded several impor- tant finds, especially from China. We should point out, though, that these

Middle Pleistocene premodern humans didn’t vastly extend the geographi- cal range of Homo erectus, but rather largely replaced the earlier hominins in previously exploited habitats. One exception appears to be the more suc- cessful occupation of Europe, a region where earlier hominins have only spo- radically been found.

Middle Pleistocene Hominins: Terminology The premodern humans of the Middle Pleistocene (that is, after 780,000 ya) generally succeeded H. erectus. Still, in some areas—especially in South- east Asia—there apparently was a long period of coexistence, lasting 300,000 years or longer; you’ll recall the very late dates for the Javanese Ngandong H. erectus (see Chapter 11).

The earliest premodern humans exhibit several H. erectus character- istics: The face is large, the brows are projected, the forehead is low, and in some cases the cranial vault is still thick. Even so, some of their other fea- tures show that they had some derived traits more closely approximating the modern condition than their H. erec- tus predecessors. Compared with H. erectus, these premodern humans possessed an increased brain size, a more rounded braincase (that is, the maximum breadth is higher up on the sides), a more vertical nose, and a less angled back of the skull (occipi- tal). We should note that the time span

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◀�Figure 12-2 Changing Pleistocene environments in Eurasia. Orange areas show regions of likely hominin occupation. White areas are major glaciers. Arrows indicate likely migra- tion routes.

chapter 12 Premodern Humans 334

encompassed by Middle Pleistocene premodern humans is at least 500,000 years, so it’s no surprise that over time we can observe certain trends. Later Middle Pleistocene hominins, for example, show even more brain expan- sion and an even less angled occipital than do earlier forms.

We know that premodern humans were a diverse group dispersed over three continents. Deciding how to classify them has been disputed for decades, and anthropologists still have disagreements. However, a growing consensus has recently emerged. Beginning perhaps as early as 850,000 ya and extending to about 200,000 ya, the fossils from Africa and Europe are placed within Homo heidel- bergensis, named after a fossil found in Germany in 1907. What’s more, some Asian specimens possibly represent a regional variant of H. heidelbergensis.

Until recently, many researchers regarded these fossils as early but more primitive members of Homo sapiens. In recognition of this somewhat tran- sitional status, the fossils were called “archaic Homo sapiens,” with all later humans also belonging to the spe-

cies Homo sapiens. However, most paleoanthropologists

now find this terminol- ogy unsatisfactory.

For example, Phillip Rightmire con-

cludes that “sim- ply lumping diverse ancient groups with living popula- tions obscures their differ- ences” (1998, p.

226). In our own discussion, we

recognize H. hei- delbergensis as a

transitional species between H. erectus and

later hominins (that is, pri- marily H. sapiens). Keep in mind,

however, that this species was probably an ancestor of both modern humans and Neandertals. It’s debatable whether

H. heidelbergensis actually represents a fully separate species in the biological sense, that is, following the biological species concept (see Chapter 5). Still, it’s useful to give this group of premod- ern humans a separate name to make this important stage of human evo- lution more easily identifiable. (We’ll return to this issue later in the chapter when we discuss the theoretical impli- cations in more detail.)

Premodern Humans of the Middle Pleistocene

Africa In Africa, premodern fossils have been found at several sites. One of the best known is Kabwe (Broken Hill). At this site in Zambia, fieldworkers discov- ered a complete cranium (Fig. 12-3) together with other cranial and post- cranial elements belonging to several individuals. In this and other African premodern specimens, we can see a mixture of primitive and more derived traits. The skull’s massive browridge (one of the largest of any hominin), low vault, and prominent occipital torus recall those of H. erectus. On the other hand, the occipital region is less angu- lated, the cranial vault bones are thin- ner, and the cranial base is essential- ly modern. Dating estimates of Kabwe and most of the other premodern fos- sils from Africa have ranged through- out the Middle and Late Pleistocene, but recent estimates have given dates for most of the sites in the range of 600,000 to 125,000 ya.

Bodo is another significant African premodern fossil (Fig. 12-4). A nearly complete cranium, Bodo has been dated to relatively early in the Middle Pleistocene (estimated at 600,000 ya), making it one of the oldest specimens of H. heidelbergensis from the African continent. The Bodo cranium is par- ticularly interesting because it shows a distinctive pattern of cut marks, sim- ilar to modifications seen on butch- ered animal bones. Researchers have

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▲�Figure 12-3 The Kabwe (Broken Hill) Homo heidelbergensis skull from Zambia. Note the very robust browridges.

Premodern Humans of the Middle Pleistocene 335

thus hypothesized that the Bodo indi- vidual was defleshed by other homi- nins, but for what purpose is not clear. The defleshing may have been related to cannibalism, though it also may have been for some other purpose, such as ritual. In any case, this is the earliest evidence of deliberate bone processing of hominins by hominins (White, 1986).

A number of other crania from South and East Africa also show a combination of retained ancestral with more derived (modern) characteris- tics, and they’re all mentioned in the literature as being similar to Kabwe. The most important of these African finds come from the sites of Florisbad and Elandsfontein (in South Africa) and Laetoli (in Tanzania).

The general similarities among all these African premodern fossils indi- cate a close relationship between them, almost certainly representing a single species (most commonly referred to as H. heidelbergensis). These African pre- modern humans are also quite similar to those found in Europe.

Europe More fossil hominins of Middle Pleis- tocene age have been found in Europe than in any other region—maybe because more archaeologists have been

searching longer in Europe than any- where else. In any case, during the Middle Pleistocene, Europe was more widely and consistently occupied than it was earlier in human evolution.

The time range of European pre- modern humans extends the full length of the Middle Pleistocene and beyond. At the earlier end, the Gran Dolina finds from northern Spain (dis- cussed in Chapter 11) are definitely not Homo erectus. The Gran Dolina remains may, as proposed by Spanish researchers, be members of a new

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▲�Figure 12-4 Bodo cranium, the earliest evidence of Homo heidelber- gensis in Africa.

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Key Premodern Human (H. heidelbergensis) Fossils from Africa

Date Site Evolutionary Significance

130,000 ya Kabwe (Broken hill, Zambia)

Nearly complete skull; mosaic of features (browridge very robust, but braincase expanded)

600,000 ya Bodo (ethiopia)

earliest example of african H. heidelbergensis; likely evidence of butchering

At a Glance

chapter 12 Premodern Humans 336

hominin species. However, Rightmire (1998) has suggested that the Gran Dolina hominins may simply repre- sent the earliest well-dated occurrence of H. heidelbergensis, possibly dating as early as 850,000 ya.

More recent and more complete- ly studied H. heidelbergensis fossils have been found throughout much of Europe. Examples of these finds come from Steinheim (Germany), Petralona (Greece), Swanscombe (England), Arago (France), and another cave site

at Atapuerca (Spain), known as Sima de los Huesos. Like their African coun- terparts, these European premoderns have retained certain H. erectus traits, but they’re mixed with more derived ones—for example, increased cranial capacity, less angled occiput, parietal expansion, and reduced tooth size (Figs. 12-5 and 12-7 on pp. 338–339).

The hominins from the Atapuerca site of Sima de los Huesos are espe- cially interesting. These finds come from another cave in the same area as the Gran Dolina discoveries, but are slightly younger, likely dating to between 500,000 and 400,000 ya. Using a different dating method, a date as early as 600,000 ya has been pro- posed (Bischoff et al., 2007), but most researchers prefer the more conser- vative later dating (Green et al., 2010; Wood, 2010). A total of at least 28 indi- viduals have been recovered from Sima de los Huesos, which literally means “pit of bones.” In fact, with more than 4,000 fossil fragments recovered, Sima de los Huesos contains more than 80 percent of all Middle Pleistocene hom- inin remains in the world (Bermúdez de Castro et al., 2004). Excavations continue at this remarkable site, where bones have somehow accumulated within a deep chamber inside a cave. From initial descriptions, paleoanthro- pologists interpret the hominin mor- phology as showing several indications

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▶�Figure 12-5 Steinheim cranium, a representative of Homo heidel- bergensis from Germany.

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Key Premodern Human (H. heidelbergensis) Fossils from Europe

Date Site Evolutionary Significance

300,000?– 259,000? ya

Swanscombe (england)

partial skull, but shows considerable brain expansion

?600,000– 400,000 ya

Sima de los huesos (atapuerca, northern Spain)

Large sample; very early evidence of Neandertal ancestry (>500,000 ya); earliest evidence of deliberate body disposal of the dead anywhere

At a Glance

Premodern Humans of the Middle Pleistocene 337

of an early Neandertal-like pattern, with arching browridges, a projecting midface, and other Neandertal features (Rightmire, 1998).

Asia Like their contemporaries in Europe and Africa, Asian premodern speci- mens discovered in China also display both earlier and later characteristics. Chinese paleoanthropologists suggest that the more ancestral traits, such as a sagittal ridge and flattened nasal bones, are shared with H. erectus fossils from Zhoukoudian. They also point out that some of these features can be found in modern H. sapiens in China today, indicating substantial genetic continu- ity. That is, some Chinese researchers have argued that, anatomically, modern Chinese didn’t evolve from H. sapiens in either Europe or Africa; instead, they evolved locally in China from a separate H. erectus lin- eage. Whether such regional evo- lution occurred or whether ana- tomically modern migrants from Africa displaced local populations is the subject of a major ongoing debate in paleoanthropology. This important controversy will be a central focus of the next chapter.

Dali, the most complete skull of the later Middle or early Late Pleistocene fossils in China, dis- plays H. erectus and H. sapiens traits, with a cranial capacity of 1,120 cm³ (Fig. 12-6). Like

Dali, several other Chinese speci- mens combine both earlier and later traits. In addition, a partial skele- ton from Jinniushan, in northeast China, has been given a provisional date of 200,000 ya (Tiemel et al., 1994). The cranial capacity is fairly large (approximately 1,260 cm³), and the walls of the braincase are thin. These are both modern features, and they’re somewhat unexpected in an individual this ancient—if the dat- ing estimate is indeed correct. Just how to classify these Chinese Middle Pleistocene hominins has been a sub- ject of debate and controversy. More recently, though, a leading paleoan- thropologist has concluded that they’re regional variants of H. heidelbergensis (Rightmire, 2004).

Key Premodern Human (H. heidelbergensis) Fossils from Asia

Date Site Evolutionary Significance

230,000– 180,000 ya

Dali (china)

Nearly complete skull; best evidence of H. heidelbergensis in asia

200,000 ya Jinniushan (china)

partial skeleton with cranium showing relatively large brain size; some chinese scholars suggest it as possible ancestor of early chinese H. sapiens

At a Glance ©

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▲�Figure 12-6 (a) Dali skull and (b) Jinniushan skull, both from China. These two crania are considered by some to be Asian representatives of Homo heidelbergensis.

chapter 12 Premodern Humans 338

A F R I C A

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Premodern Humans of the Middle Pleistocene 339

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A Review of Middle Pleistocene Evolution

Premodern human fossils from Africa and Europe resemble each other more than they do the hominin fossils from Asia. The mix of some ancestral characteristics—retained from Homo erectus ancestors—with more derived features gives the African and European fossils a distinctive look; thus Middle Pleistocene hominins from these two continents are usually referred to as H. heidelbergensis.

The situation in Asia isn’t so tidy. To some researchers, the remains, especially those from Jinniushan, seem more modern than do contemporary fossils from either Europe or Africa. This observation explains why Chinese paleoanthropologists and some American colleagues conclude that the Jinniushan remains are early mem- bers of H. sapiens. Other researchers (for example, Rightmire, 1998, 2004) suggest that they represent a regional branch of H. heidelbergensis.

The Pleistocene world forced many small populations into geographical isolation; most of these regional popu- lations no doubt died out. Some, how- ever, did evolve, and their descendants are likely a major part of the later hom- inin fossil record. In Africa, H. hei- delbergensis is hypothesized to have evolved into modern H. sapiens. In Europe, H. heidelbergensis evolved into

Neandertals. Meanwhile, the Chinese premodern populations may all have met with extinction. Right now, though, there’s no consensus on the status or the likely fate of these enig- matic Asian Middle Pleistocene homi- nins (Fig. 12-8).

Middle Pleistocene Culture

The Acheulian technology of H. erectus carried over into the Middle Pleistocene with relatively little change until near the end of the period, when it became slightly more sophisti- cated. Bone, a high-quality tool mate- rial, remained practically unused dur- ing this time. Stone flake tools similar to those of the earlier era persisted, possibly in greater variety. Some of the later premodern humans in Africa and Europe invented a method— the Levallois technique (Fig. 12-9)— for controlling flake size and shape, resulting in a “turtle back” profile. The Levallois technique required several complex and coordinated steps, sug- gesting increased cognitive abilities in later premodern populations.

Premodern human populations con- tinued to live in both caves and open- air sites, but they may have increased their use of caves. Did these homi- nins control fire? Klein (1999), in inter- preting archaeological evidence from

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▼�Figure 12-8 Time line of Middle Pleistocene hominins. Note that most dates are approximations. Question marks indicate those estimates that are most tentative.

Neandertals: Premodern Humans of the Late Pleistocene 341

France, Germany, and Hungary, sug- gests that they did. What’s more, Chinese archaeologists insist that many Middle Pleistocene sites in China contain evidence of human-controlled fire. However, the best (and earliest) documented evidence has recently been found in South Africa (Berna et al., 2012). (This new discovery was dis- cussed in Chapter 11.)

We know that Middle Pleistocene hominins built temporary structures, because researchers have found con- centrations of bones, stones, and arti- facts at several sites. We also have evidence that they exploited many dif- ferent food sources—fruits, vegeta- bles, seeds, nuts, and bird eggs, each in its own season. Importantly, they also exploited marine life, a new innovation in human biocultural evolution.

The hunting capabilities of premod- ern humans, as for earlier hominins, are still greatly disputed. Most research- ers have found little evidence support- ing widely practiced advanced hunting. Some more recent finds, however, are beginning to change this view—espe- cially the discovery in 1995 of remark- able wood spears from the Schöningen site in Germany (Thieme, 1997). These large, extremely well-preserved weap- ons (provisionally dated to about 400,000 to 300,000 ya) were most likely used as throwing spears, presumably to hunt large animals. Also interesting in this context, the bones of numerous horses were recovered at Schöningen.

As documented by the fossil remains as well as artifactual evi- dence from archaeological sites, the long period of transitional hominins in Europe continued well into the Late Pleistocene (after 125,000 ya). But with

the appearance and expansion of the Neandertals, the evolution of premod- ern humans took a unique turn.

Neandertals: Premodern Humans of the Late Pleistocene

Since their discovery more than a century ago, the Neandertals have haunted the minds and foiled the best-laid theories of paleoanthropolo- gists. They fit into the general scheme of human evolution, and yet they’re misfits. Classified variously either as H. sapiens or as belonging to a separate species, they are like us and yet differ- ent. It’s not easy to put them in their place. Many anthropologists classify Neandertals within H. sapiens, but as a distinctive subspecies, Homo sapi- ens neanderthalensis,* with modern H. sapiens designated as Homo sapiens sapiens. However, not all experts agree with this interpretation. The most recent genetic evidence of interbreed- ing between Neandertals and early modern humans (Green et al., 2010) suggests that complete speciation was never attained. This argues against a clear designation of Neandertals as a species separate from H. sapiens. We’ll discuss this important evidence in more detail in a moment.

* Thal, meaning “valley,” is the old spelling; due to rules of taxonomic naming, this spelling is retained in the formal species designation Homo neanderthalensis (although the h was never pronounced). The modern spelling, tal, is used today in Germany; we follow contemporary usage in the text with the spelling of the colloquial Neandertal.

A final blow struck at one end removes a large flake. The flake on the right is the goal of the whole process and is the completed tool.

Nodule The nodule is chipped on the perimeter.

on the perimeter.

Flakes are radially removed from top surface.

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▲�Figure 12-9 The Levallois technique.

chapter 12 Premodern Humans 342

Neandertal fossil remains have been found at dates approaching 130,000 ya; but in the following discussion of Neandertals, we’ll focus on those populations that lived especially dur- ing the last major glaciation, which began about 75,000 ya and ended about 10,000 ya (Fig. 12-10). We should also note that the evolutionary roots of Neandertals apparently reach quite far back in western Europe, as evidenced by the 400,000+-year-old remains from Sima de los Huesos. Some research- ers conclude that these hominins are derived enough to be considered members of the Neandertal clade (Stringer, 2012).

The majority of fossils have been found in Europe, where they’ve been most studied. Our description of Neandertals is based primarily on those specimens, usually called clas- sic Neandertals, from western Europe. Not all Neandertals—including others from eastern Europe and western Asia and those from the interglacial period just before the last glacial one—exactly fit our description of the classic mor- phology. They tend to be less robust, possibly because the climate in which

they lived was not as cold as in western Europe during the last glaciation.

One striking feature of Neandertals is brain size, which was actually larger than that of H. sapiens today. The aver- age for contemporary H. sapiens is between 1,300 and 1,400 cm³, while for Neandertals it was 1,520 cm³. The larger size may be associated with the metabolic efficiency of a larger brain in cold weather. The Inuit (Eskimo), also living in very cold areas, have a larger average brain size than most other modern human populations. We should also point out that the larger brain size in both premodern and contemporary human populations adapted to cold cli- mates is partially correlated with larg- er body size, which has also evolved among these groups (see Chapter 15).

The classic Neandertal cranium is large, long, low, and bulging at the sides. Viewed from the side, the occipi- tal bone is somewhat bun-shaped, but the marked occipital angle typical of many H. erectus crania is absent. The forehead rises more vertically than that of H. erectus, and the browridges arch over the orbits instead of forming a straight bar (see Fig. 12-11).

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▼�Figure 12-10 Correlation of Pleistocene subdivisions with archaeological industries and homi- nins. Note that the geological divi- sions are separate and different from the archaeological stages (e.g., Late Pleistocene is not synonymous with Upper Paleolithic).

Neandertals: Premodern Humans of the Late Pleistocene 343

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chapter 12 Premodern Humans 344

Compared with anatomically mod- ern humans, the Neandertal face stands out. It projects almost as if it were pulled forward. Postcranially, Neandertals were very robust, barrel-chested, and powerfully mus- cled. This robust skeletal structure, in fact, dominates hominin evolution from H. erectus through all premod- ern forms. Still, the Neandertals appear particularly robust, with shorter limbs than seen in most modern H. sapiens populations. Both the facial anatomy

and the robust postcranial structure of Neandertals have been interpreted by Erik Trinkaus, of Washington University in St. Louis, as adaptations to rigorous living in a cold climate.

For about 100,000 years, Neandertals lived in Europe and west- ern Asia (see Fig. 12-12), and their coming and going have raised more questions and controversies than for any other hominin group. As we’ve noted, Neandertal forebears were transitional forms dating to the

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Neandertals: Premodern Humans of the Late Pleistocene 345

later Middle Pleistocene. However, it’s not until the Late Pleistocene that Neandertals become fully recognizable.

Western Europe One of the most important Neander- tal discoveries was made in 1908 at La Chapelle-aux-Saints, in southwest- ern France. A nearly complete skeleton was found buried in a shallow grave in a flexed position (Fig. 12-13). Several fragments of nonhuman long bones had been placed over the head, and over them, a bison leg. Around the body were flint tools and broken animal bones.

The skeleton was turned over for study to Marcellin Boule, a well-known French paleontologist, who subse- quently depicted the La Chapelle Neandertal as a brutish, bent-kneed, not fully erect biped. Because of this exaggerated interpretation, some scholars, and certainly the general pub- lic, concluded that all Neandertals were highly primitive creatures.

Why did Boule draw these con- clusions from the La Chapelle skele- ton? Today, we think he misjudged the Neandertal posture because this adult male skeleton had arthritis of the spine. Also, and probably more importantly, Boule and his contemporaries found it difficult to accept an individual who appeared in any way to depart from the modern pattern as a human ancestor.

The skull of this male, who was pos- sibly at least 40 years of age when he died, is very large, with a cranial capac- ity of 1,620 cm³. Typical of western European classic forms of Neandertal, the vault is low and long; the brow- ridges are immense, with the typical Neandertal arched shape; the forehead is low and retreating; and the face is long and projecting. The back of the skull is protuberant and bun-shaped (see Figs. 12-11 and 12-14).

The La Chapelle skeleton actu- ally isn’t a typical Neandertal but an unusually robust male who “evi- dently represents an extreme in the Neandertal range of variation” (Brace et al., 1979, p. 117). Unfortunately, this

skeleton, which Boule claimed didn’t even walk complete- ly erect, was widely accepted as “Mr. Neandertal.” But few other Neandertal individuals possess such an exaggerated expression of Neandertal traits as the “Old Man of La Chapelle-aux-Saints.”

Dramatic new evidence of Neandertal behavior comes from the El Sidrón site in northern Spain. Dated to about 49,000 ya, fragmented remains of 12 indi- viduals show bone changes indi- cating that they were smashed, butchered, and likely canni- balized—presumably by other Neandertals (Lalueza-Fox et al., 2011).

Because the remains of all 12 individuals were found togeth- er in a cave where their remains had accidentally fallen, they all probably died (were killed) at about the same time. Lying there undis- turbed for almost 50,000 years, these individuals reveal several secrets about Neandertals. First, they are hypothesized to all have belonged to the same social group, rep- resenting a band of hunter-gatherers. Their ages and sex support this interpretation: three adult males, three adult females, five children/ adolescents, and one infant.

What’s more, genetic evidence shows that the adult males were all closely related, but the females weren’t. It seems that Neandertals practiced a patrilocal form of mating, in which related males stay together and mate with females from other groups (see Fig. 12-15).

Some of the most recent of the west- ern European Neandertals come from St. Césaire, in southwestern France, and are dated at about 35,000 ya

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▲�Figure 12-13 Artist’s reconstruc- tion of an adult male Neandertal based on skeletal remains from La Chapelle, France.

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▲�Figure 12-14 Specimen from La Chapelle-aux-Saints. Note the occipi- tal bun, projecting face, and low vault.

chapter 12 Premodern Humans 346

▲�Figure 12-15 “Clean” excavations at the El Sidrón cave in Spain, where special precautions are used to pre- vent contamination and allow more controlled later DNA analyses. From this site recent evidence from mtDNA analyses suggests that males likely practiced a patrilocal mating pattern.

(Fig. 12-16). At St. Césaire, Neandertal remains were recovered from an archaeological level that also included discarded chipped blades, hand axes, and other stone tools of an Upper Paleolithic tool industry associated with Neandertals.

Central Europe There are quite a few other European classic Neandertals, including sig- nificant finds from central Europe (see Fig. 12-12). At Krapina, Croatia, researchers have recovered an abun- dance of bones—1,000 fragments repre- senting up to 70 individuals—and 1,000 stone tools or flakes (Trinkaus and Shipman, 1992). Krapina is an old site, possibly the earliest showing the full suite of classic Neandertal morphology (Fig. 12-17) dating back to the begin- ning of the Late Pleistocene ( estimated at 130,000 to 110,000 ya). Krapina is also important as an intentional burial site—one of the oldest on record.

About 30 miles from Krapina, Neandertal fossils have also been dis- covered at Vindija. This site is an excellent source of faunal, cultural, and hominin materials stratified in sequence throughout much of the Late Pleistocene. Neandertal fossils from Vindija consist of some 35 specimens dated to between 42,000 and 32,000 ya, making them some of the most recent Neandertals ever discovered (Higham et al., 2006). Given these dates, it seems that the most recent Neandertal remains yet recovered come from Vindija.

As we’ve seen, the Neandertals from St. Césaire are only slightly older than those from Vindija, making these two sites important for several rea- sons. Anatomically modern humans were living in both western and cen- tral Europe by about 35,000 ya or a bit earlier. So it’s possible that Neandertals and modern H. sapiens were living quite close to each other for several thousand years (Fig. 12-18). How did these two groups interact? Evidence from a number of French sites indicates that Neandertals may have borrowed

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Upper Paleolithic a cultural period usually associated with modern humans but also found with some Neandertals and distinguished by technological innovation in various stone tool industries. Best known from western europe, similar industries are also known from central and eastern europe and africa.

▲�Figure 12-16 Specimen from St. Césaire, among the “last” Neandertals.

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Neandertals: Premodern Humans of the Late Pleistocene 347

technological methods and tools (such as blades) from the anatomically mod- ern populations and thereby modified their own tools, creating a new indus- try, the Chatelperronian. It’s also possible, of course, that early modern H. sapiens borrowed cultural innova- tions from the Neandertals (who, as we’ll soon see, were in many ways also quite sophisticated). What’s more, we now know that they very likely were interbreeding with each other!

Western Asia Israel Many important Neander- tal discoveries have also been made in southwest Asia. Neandertal spec- imens from Israel are less robustly

built than the classic Neandertals of Europe, though again the overall pat- tern is clearly Neandertal. One of the best known of these discoveries is from Tabun (Fig. 12-19). Tabun, excavated in the early 1930s, yielded a female skeleton dated by thermoluminescence (TL) at about 120,000 to 110,000 ya. (TL dating is discussed in Chapter 9.) If this dating is accurate, Neandertals at Tabun were generally contemporary with early modern H. sapiens found in nearby caves.

A more recent Neandertal burial of a large male comes from Kebara, a neighboring cave at Mt. Carmel. A par- tial skeleton, dated to 60,000 ya, it con- tains the most complete Neandertal thorax and pelvis yet found. Also

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▲�Figure 12-18 Time line for Neandertal fossil discoveries.

◀�Figure 12-17 Krapina cra- nium. (a) Lateral view showing characteristic Neandertal traits. (b) Three-quarters view.

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Chatelperronian pertaining to an Upper paleolithic industry found in France and Spain, containing blade tools and asso- ciated with Neandertals.

chapter 12 Premodern Humans 348

recovered at Kebara is a hyoid—a small bone located in the throat, and the first ever found from a Neandertal; this bone is especially important because of its usefulness in reconstructing lan- guage capabilities.*

Iraq A most remarkable site is Shani- dar Cave, in the Zagros Mountains of northeastern Iraq, where fieldworkers found partial skeletons of nine indi- viduals, four of them deliberately bur- ied. One of the more interesting skel- etons recovered from Shanidar is that of a male (Shanidar 1) who lived to be approximately 30 to 45 years old, a con- siderable age for a prehistoric human (Fig. 12-20). He is estimated to have stood 5 feet 7 inches tall, with a cra- nial capacity of 1,600 cm³. The skeletal remains of Shanidar 1 also exhibit sev- eral other fascinating features.

There had been a crushing blow to the left side of the head, fracturing the eye socket, displacing the left eye, and probably causing blindness on that side. He also sustained a mas- sive blow to the right side of the body

*The Kebara hyoid is identical to that of modern humans, suggesting that Neandertals did not differ from modern H. sapiens in this key element.

that so badly damaged the right arm that it became withered and useless; the bones of the shoulder blade, col- lar bone, and upper arm are much smaller and thinner than those on the left. The right lower arm and hand are missing, probably not because of poor preservation . . . but

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▶�Figure 12-19 Excavation of the Tabun Cave, Mt. Carmel, Israel.

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▲�Figure 12-20 Shanidar 1. Does he represent Neandertal compassion for the disabled?

Neandertals: Premodern Humans of the Late Pleistocene 349

because they either atrophied and dropped off or because they were amputated. (Trinkaus and Shipman, 1992, p. 340)

Besides these injuries, the man had further trauma to both legs, and he probably limped. It’s hard to imagine how he could have performed day-to- day activities without assistance. This is why Erik Trinkaus, who has stud- ied the Shanidar remains, suggests that to survive, Shanidar 1 must have been helped by others: “A one-armed, par- tially blind, crippled man could have made no pretense of hunting or gather- ing his own food. That he survived for years after his trauma was a testament to Neandertal compassion and human- ity” (Trinkaus and Shipman, 1992, p. 341).

Central Asia Neandertals extended their range even farther to the east, far into central Asia. A discovery made in the 1930s at the site of Teshik-Tash, in Uzbekistan, of a Neandertal child associated with tools of the Mousterian industry suggested that this species had dispersed a long way into Asia. However, owing to poor archaeological control during excava- tion and the young age of the individ- ual, the find was not considered by all paleoanthropologists as clearly that of a Neandertal. New finds and molec- ular evaluation have provided crucial evidence that Neandertals did in fact extend their geographical range far into central Asia and perhaps even far- ther east.

DNA analysis of the Teshik-Tash remains shows that they are clearly Neandertal. What’s more, other frag- ments from southern Siberia also show a distinctively Neandertal genetic pat- tern (Krause et al., 2007a). As we’ll see shortly, researchers have recently been able to identify and analyze DNA from several Neandertal specimens. It’s been shown that Neandertals and modern humans differ in both their mitochondrial DNA (mtDNA) and nuclear DNA; these results are extremely significant in determin-

ing the evolutionary status of the Neandertal lineage. Moreover, in the case of the fragmentary remains from southern Siberia (dating to 44,000 to 37,000 ya), it was the DNA find- ings that provided the key evidence in determining whether the hominin is even a Neandertal. In a sense, this is analogous to doing forensic analysis on our ancient hominin predecessors.

Surprising Connections: Another Con- temporary Hominin? In 2000, 2008, and 2010 researchers found more fragmen- tary hominin remains in another cave (Denisova Cave) in the Altai Moun- tains of southern Siberia. Only a fin- ger bone and two teeth were found, and these are dated to as old as 80,000– 60,000 ya (Meyer et al., 2012). From such incomplete skeletal remains, accu- rate anatomical species identification is impossible. In prior years, this seem- ingly meager find would have been stashed away in a cabinet in a museum or a university laboratory and mostly forgotten. But in the twenty-first cen- tury, we have new ways to study bits and pieces of ancient hominins. So the finger bone was sent to the Max-Planck Institute for Evolutionary Biology in Germany to see if DNA analysis could determine to which species it belongs.

Initially, mitochondrial DNA analy- sis was performed and provided a big surprise: The mtDNA from the hom- inin at Denisnova Cave did not match that of either a modern H. sapiens or a Neandertal!

Lying in a cool, dry, stable environ- ment inside the cave, the Denisnova remains stood a good chance of pre- serving even more complete ancient DNA. So, the Max Planck team, along with many colleagues from around the world, decided to attempt to sequence the nuclear genome derived from DNA in the finger bone (in which DNA pres- ervation was exceptionally good).

Within less than 2 years they suc- cessfully sequenced the entire genome from this one small bone, in other words, more than three billion base pairs—a truly amazing scientific accomplishment (Reich et al., 2010). In

chapter 12 Premodern Humans 350

2012 they went even further doing a far more precise sequencing (up to 30× more accurate than the one two years earlier) of the entire genome from the same finger bone. (Meyer et al., 2012). These far more complete data con- firmed the earlier findings, most nota- bly that the “Denisovans” were a sepa- rate branch of hominins living side by side in central Asia with two other lin- eages of hominins (Neandertals and modern humans).

The most recent whole genome analysis has also been able to identify the sex of the individual (as female) and reveal that her skin was dark along with brown hair and brown eyes. What’s more it was possible to sequence sepa- rately the two DNA strands and thus to tell which genes were inherited from the girl’s mother and which ones from her father. Lastly, up to 34 genes that are known to cause disease were found to be different in the Denisovans as compared to modern humans (Meyer et al., 2012). The complete genome also provided another big surprise regard- ing how these ancient Denisovans are genetically connected to some living human populations (see “Molecular Connections” below).

Culture of Neandertals

Anthropologists almost always asso-ciate Neandertals, who lived in the cultural period known as the Mid- dle Paleolithic, with the Mousterian industry—although they don’t always associate the Mousterian industry with just Neandertals (since it is sometimes also found with modern humans). Early in the last glacial period, Mous- terian culture extended across Europe and North Africa into the former Soviet Union, Israel, Iran, and as far east as central Asia and possibly even China. Also, in sub-Saharan Africa, the contemporaneous Middle Stone Age industry is broadly similar to the Mousterian.

Technology Neandertals extended and diversi- fied traditional methods of mak- ing tools, and there’s some indica- tion that they developed specialized tools for skinning and preparing meat, hunting, woodworking, and hafting (Fig. 12-21).

Even so, in strong contrast to the following cultural period, the Upper

Key Neandertal Fossil Discoveries

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Vindija (croatia)

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50,000 ya La chapelle (France)

Most famous Neandertal site; historically provided early, but distorted, interpretation of Neandertals

70,000– 60,000 ya

Shanidar (Iraq)

Several well-preserved skeletons; good example of Neandertals from southwestern asia; one individual with multiple injuries

110,000 ya; date uncertain

tabun (Israel)

Well-preserved and very well-studied fossils showing early evidence of Neandertals in southwestern asia

At a Glance

Mousterian pertaining to the stone tool industry associated with Neandertals and some modern H. sapiens groups; also called Middle paleolithic. this industry is characterized by a larger proportion of flake tools than is found in acheulian tool kits.

Culture of Neandertals 351

Paleolithic, there’s almost no evi- dence that they used bone tools. Still, Neandertals advanced their technol- ogy well beyond that of earlier homi- nins. It’s possible that their technologi- cal advances helped provide part of the basis for the remarkable changes of the Upper Paleolithic, which we’ll dis- cuss in the next chapter. What’s more, Neandertals also were quite advanced in exploiting new food resources as well as fashioning personal adornments.

Subsistence We know, from the abundant remains of animal bones at their sites, that Neandertals were successful hunters. But though it’s clear that Neandertals could hunt large mammals, they may not have been as efficient at this task as Upper Paleolithic modern humans. For example, it wasn’t until the beginning of the Upper Paleolithic that the spear- thrower, or atlatl, came into use (see Chapter 13). Soon after that, in Upper Paleolithic groups, the bow and arrow greatly increased efficiency (and safety) in hunting large mammals by put- ting distance between the hunters and the hunted. Because Neandertals had no long-distance weaponry and were mostly limited to thrusting spears, they may have been more prone to seri- ous injury—a hypothesis supported by paleoanthropologists Thomas Berger

and Erik Trinkaus. Berger and Trinkaus (1995) analyzed the pattern of trauma, particularly fractures, in Neandertals and compared it with that seen in con- temporary human samples. Interest- ingly, the pattern in Neandertals, espe- cially the relatively high proportion of head and neck injuries, was most similar to that seen in contemporary rodeo performers. Berger and Trinkaus concluded that “the similarity to the rodeo distribution suggests frequent close encounters with large ungu- lates unkindly disposed to the humans involved” (Berger and Trinkaus, 1995, p. 841).

Recent archaeological discover- ies have shown that Neandertals also expanded their range of available foods to include marine resources—a sub- sistence strategy previously thought to have been developed later by modern humans during the Upper Paleolithic. From the island of Gibraltar, new evidence has shown that some Neandertals gathered shellfish and hunted seals and dolphins, displaying no difference in their hunting behav- ior from modern humans of the same region (Stringer et al., 2008).

Speech and Symbolic Behavior There are a variety of hypotheses con- cerning the speech capacities of Nean- dertals, and many of these views

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are contradictory. Although some researchers argue that Neandertals were incapable of human speech, the prevailing consensus has been that they were capable of articulate speech and possibly capable of producing the same range of sounds as modern humans.

Recent genetic evidence likely will help us to determine when fully human language first emerged (Enard et al., 2002; Fisher and Scharff, 2009). In humans today, mutations in a particu- lar gene (locus) are known to produce serious language impairments. From an evolutionary perspective, what is perhaps most significant is the greater variability seen in the alleles at this locus in modern humans as compared with other primates. One explanation for this increased variation is intensi-

fied selection acting on human popu- lations. And, as we’ll see shortly, DNA evidence from Neandertal fossils shows that these hominins had already made this transformation.

Many researchers are convinced that Upper Paleolithic H. sapiens had some significant behavioral advan- tages over Neandertals and other pre- modern humans. Was it some kind of new and expanded ability to sym- bolize, communicate, organize social activities, elaborate technology, obtain a wider range of food resources, or care for the sick or injured? Or was it some other factor? Compared with modern H. sapiens, were the Neandertals limited by neurological differences that may have contributed to their demise?

The Evolution of Language

One of the most distinctive behavioral attributes of all modern humans is our advanced ability to use highly sophisti- cated symbolic language. Indeed, it would be impossible to imagine human social relationships or human culture without language.

When did language evolve? First, we should define what we mean by full human language. as we discussed in chapter 7, nonhuman primates have shown some elements of language. For example, some chimpanzees, gorillas, and bonobos display the ability to manipulate symbols and a rudimentary understanding of grammar. Still, the full complement of skills dis- played by humans includes the extensive use of arbitrary symbols; sophisticated grammar; and a complex, open system of communication.

Most scholars are comfortable attribut- ing such equivalent skills to early members of H. sapiens, as early as 200,000 to

100,000 ya. In fact, some researchers have hypothesized that the elaborate technology and artistic achievements, as well as the rapid dispersal, of modern humans were a direct result of behavioral advantages— particularly full language capabilities. More recently, we have come to appreciate that Neandertal cultural abilities were also quite advanced and that the transition to the more elaborate Upper paleolithic associated with modern humans was not instantaneous.

clearly, earlier hominins had some form of complex communication; almost everyone agrees that even the earliest hominins did communicate (and the form was at least as complex as that seen in living apes). What’s not generally agreed upon is just when the full complement of human language capacity first emerged. Indeed, the controversy relating to this process will continue to ferment, since there’s no clear answer to the question. at present, there’s not enough evidence available to fully establish the language capabilities of any fossil hominin. We said in chapter 7 that there are neurological foundations for language and that these features relate more to brain reorganization

than to simple increase in brain size. also, as far as spoken language is concerned, alterations within several anatomical struc- tures—including the brain, tongue and vocal tract—must have occurred at some time during hominin evolution.

Yet, because it’s soft tissue, we have no complete record of fossil hominin brains or their vocal tracts. We do have endocasts, which preserve a few external features of the brain. For example, there are several preserved endocasts of aus- tralopiths from South africa. however, the information is incomplete and thus subject to varying interpretations. (For example, did these hominins possess language? If not, what form of communication did they display?) evidence from the vocal tract has been even more elusive, although recent finds are helping to fill in at least some of the gaps.

In such an atmosphere of fragmentary data, a variety of conflicting hypotheses have been proposed. Some paleoanthropol- ogists argue that early australopiths (3 mya) had language. Others think that such capabilities were first displayed by early Homo (perhaps 2 mya). Still others sug- gest that language didn’t emerge fully until

A Closer Look

Culture of Neandertals 353

The direct anatomical evidence derived from Neandertal fossils isn’t much help in answering these ques- tions. Ralph Holloway (1985) has main- tained that Neandertal brains—at least as far as the fossil evidence suggests (from endocasts—both natural and artificial)—aren’t significantly differ- ent from those of modern H. sapiens. What’s more, the positioning of the Neandertal vocal tract (determined by the shape of the hyoid bone), as well as other morphological features, doesn’t appear to have seriously limited them.

Most of the reservations about advanced cognitive abilities in Neandertals have been based on archaeological data. However, as more archaeological data have been collect- ed and better dating controls applied

to a large number of sites bridging the Mousterian–Upper Paleolithic transi- tion, many of the proposed behavioral differences between Neandertals and early modern humans have blurred. For example, it is now known that, like early H. sapiens, Neandertals some- times used pigment (probably as body ornamentation) and wore jew- elry. The most significant recent finds come from two sites in Spain dating to 50,000 to 37,000 ya, and both have a Mousterian stone tool industry. Since these sites were occupied before mod- ern H. sapiens reached this part of Europe, the most likely conclusion is that the objects found were made by Neandertals (Zilhão et al., 2010). The finds include perforated shells, osten- sibly drilled to be used as jewelry, as

the time of Homo erectus (2 to 1 mya), or perhaps it was premodern humans (such as the Neandertals) who first displayed such skills. and finally, some researchers assert that language first developed only with the appearance of fully modern H. sapiens.

Because the question of language evo- lution is so fundamental to understanding human evolution (indeed, what it means to be human), a variety of creative techniques have been applied to assess the (limited) evidence that’s available. We’ve already mentioned the analysis of endocasts.

to reconstruct speech capabilities in fossil hominins, the physiology of the vocal tract can also provide some crucial hints, especially the position of the voice box (larynx) within the throat. In adult modern humans, the larynx is placed low in the throat, where it can better act as a resonat- ing chamber. Unfortunately, since all the crucial structures within the vocal tract are soft tissue, they decompose after death, leaving paleoanthropologists to their own imaginations to speculate about the rela- tive positions of the larynx in life. One way to determine the position of the larynx in long-dead hominins is to look at the degree of flexion at the base of the cranium. this

flexion can be directly linked to the place- ment of the larynx in life, since “it shapes the roof of the voice box” (Klein, 1999). In comparisons of fossil hominin crania, it’s been determined that full cranial base flex- ion similar to that found in modern sapiens is not found before Homo heidelbergensis.

the tongue is, of course, another crucial structure influencing speech. Because it’s a site of attachment for one of the muscles of the tongue, the shape and position of the hyoid bone (Fig. 1) can tell us a lot about speech capabilities in earlier homi- nins. a hyoid located higher up and farther back in the throat allows modern humans to control their tongues much more efficiently and precisely. In the Australopithecus afarensis child’s skeleton (from Dikika, ethiopia; see chapter 10), the hyoid is shaped more like that in a chimpanzee than in a modern human. So it seems most likely that these early hominins weren’t able to fully articulate human speech. the only other hyoid found in a fossil hominin comes from the Neandertal skeleton found at Kebara (Israel); quite unlike the australopith condition, it resembles

modern hyoids in all respects. We thus have some basis for concluding that the tongue musculature of Neandertals may have been much like our own.

also potentially informative are possible genetic differences between humans and apes in regard to language. as the human genome is fully mapped (especially identify- ing functional regions and their specific actions) and compared with ape DNa (the chimpanzee genome is now also completely

sequenced at a structural level), we might at long

last begin to find a key to solving this great mystery.

◀�Figure 1 The position of the hyoid bone in the throat, shown in a modern human skeleton.

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well as natural pigments that were deliberately brought to the site

and applied to the shells and some animal bones (see

Fig. 12-22). Neandertals and

modern humans coexisted in some parts of Europe for up to 15,000 years, so Neandertals didn’t vanish suddenly. Nevertheless, shortly

after 30,000 ya, they disappear from the fos-

sil and archaeological record. At some point, as a

recognizable human group, Neandertals became an evolu-

tionary dead end. Right now, we can’t say exactly what caused their disap- pearance and ultimate replacement by anatomically modern Upper Paleolithic peoples. Indeed, Neandertals didn’t really disappear altogether, since a few of their genes can still be found today in many human groups.

Burials Anthropologists have known for some time that Neandertals deliberately bur- ied their dead. Undeniably, the spectac- ular discoveries at La Chapelle, Shan- idar, and elsewhere were the direct results of ancient burial, which per- mits preservation that’s much more complete. Such deliberate burial treat- ment goes back at least 90,000 years at Tabun. From a much older site, some form of consistent “disposal” of the dead—not necessarily below-ground burial—is evidenced. As previously discussed, at the site of Sima de los Huesos in Spain, archaeologists found thousands of fossilized bone frag- ments in a cave at the end of a deep vertical shaft. From the nature of the site and the accumulation of hominin remains, Spanish researchers are con- vinced that the site demonstrates some form of human activity involving delib- erate disposal of the dead (Arsuaga et al., 1997).

The recent dating of Sima de los Huesos to more than 400,000 ya sug- gests that Neandertal precursors were already handling their dead in special ways during the Middle Pleistocene. Such behavior was previously thought to have emerged only much later, in the Late Pleistocene. As far as current data indicate, this practice is seen in west- ern European contexts well before it appears in Africa or eastern Asia. For example, in the premodern sites at Kabwe and Florisbad (discussed ear- lier), deliberate disposal of the dead is not documented, nor is it seen in African early modern sites—for exam- ple, the Klasies River Mouth, dated at 120,000 to 100,000 ya (see Chapter 13).

Yet, in later contexts (after 35,000 ya), where modern H. sapiens remains are found in clear burial contexts, their treatment is considerably more com- plex than in Neandertal burials. In these later (Upper Paleolithic) sites, grave goods, including bone and stone tools as well as animal bones, are found more consistently and in greater con- centrations. Because many Neandertal sites were excavated in the nineteenth or early twentieth century, before more rigorous archaeological methods were developed, many of these supposed burials are now in question. Still, the evidence seems quite clear that delib- erate burial was practiced not only at La Chapelle, La Ferrassie (eight graves), Tabun, Amud, Kebara, Shanidar, and Teshik-Tash, but also at several other localities, especially in France. In many cases, the body’s position was delib- erately modified, having been placed in the grave in a flexed posture. This flexed position has been found in 16 of the 20 best-documented Neandertal burial contexts (Klein, 1999).

Molecular Connections: The Genetic Evidence

With the revolutionary advances in molecular biology (discussed in Chapter 3), fascinating new ave-

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▲�Figure 12-22 Upper portion of a bivalve shell that has been perforated and stained with pigment, from the Antón rock-shelter site in Spain (dated around 44,000 to 37,000 ya). The red- dish inner surface (left) is natural, but the yellow colorant on the outer whit- ish surface (right) was the result of an added pigment.

Molecular Connections: The Genetic Evidence 355

nues of research have become pos- sible in the study of earlier hominins. It’s becoming fairly commonplace to extract, amplify, and sequence ancient DNA from contexts spanning the last 10,000 years or so. For example, researchers have analyzed the entire nuclear genome from a 4,000-year-old Inuit (Eskimo) from Greenland (Ras- mussen et al., 2010) and recently the 5,000-year-old “Iceman” found in the Italian Alps. The last of these analyses has provided us with surprisingly com- plete information about the Iceman. For example, he most likely had brown eyes and was blood-type O; it was even determined that he couldn’t digest lac- tose (Keller et al., 2012).

It’s much harder to find usable DNA in even more ancient remains because the organic components, often including the DNA, have been destroyed during the mineraliza- tion process. Nevertheless, in the past few years exciting results have been announced about DNA found in more than a dozen different Neandertal fos- sils dated between 50,000 and 32,000 ya. These fossils come from sites in France (including La Chapelle), Germany (from the original Neander Valley locality), Belgium, Italy, Spain, Croatia, and Russia (Krings et al., 1997, 2000; Ovchinnikov et al., 2000; Schmitz et al., 2002; Serre et al., 2004; Green et al., 2006). As we previously mentioned, recently ascertained ancient DNA evidence strongly sug- gests that other fossils from cen- tral Asia (Uzbekistan and two caves in southern Siberia), dated at 48,000 to 30,000 ya, are also Neandertals (Krause et al., 2007b) or even an entirely different species (Krause et al., 2010; Reich et al., 2010).

The technique most often used in studying most Neandertal fos- sils involves extracting mitochondrial DNA (mtDNA), amplifying it through polymerase chain reaction (PCR; see Chapter 3), and sequencing nucleo- tides in parts of the molecule. Initial results from the Neandertal specimens show that these individuals are geneti-

cally more different from contempo- rary Homo sapiens populations than modern human populations are from each other—in fact, about three times as much.

Major advances in molecular biol- ogy have allowed much more of the Neandertal genetic pattern to be determined, with the ability to now sequence the entire mtDNA sequence in several individuals (Briggs et al., 2009) as well as big chunks of the nuclear DNA (which, as you may recall, contains more than 99 per- cent of the human genome). In fact, the most exciting breakthrough yet in ancient DNA studies was achieved in 2010 with the completion of the entire nuclear genome of European Neandertals (Green et al., 2010). Just a handful of years ago, this sort of achievement would have seemed like science fiction.

This new information has already allowed for crucial (as well as quite surprising) revisions in our under- standing of Neandertal and early modern human evolution. First of all, Neandertal DNA is remarkably simi- lar to modern human DNA, with 99.84 percent of it being identical. However, to detect those few (but possibly infor- mative) genes that do differ, the team sequenced the entire genome of five modern individuals (two from Africa and one each from China, France, and New Guinea). To the surprise of almost everyone, the research- ers found that many people today still have Neandertal genes! What’s more, these Neandertal genes are found only in non-Africans, strongly sug- gesting that interbreeding occurred between Neandertals and modern H. sapiens after the latter had emi- grated out of Africa. In fact, the three modern non-African individuals used for comparison in this study all had the same amount of Neandertal DNA. What makes this finding even more startling is the fact that the modern non-African humans evaluated come from widely scattered regions (west- ern Europe, China, and the far South

356

Pacific). Further evidence, includ- ing complete genomes from another seven modern people from even more dispersed populations, has further confirmed these findings (Reich et al., 2010).

The best (and simplest) hypothesis for this genetic pattern is that shortly after modern H. sapiens migrants left Africa, a few of them interbred with Neandertals before these people and their descendants dispersed to other areas of the world. The best guess is that this intermixing between the two groups occurred in the Middle East, likely sometime between 80,000 and 50,000 ya. DNA data from more individ- uals, both within and outside of Africa, will help to substantiate this hypothe- sis. For the moment, the degree of inter-

breeding appears to be small but still significant—about 1 to 4 percent of the total genome for living non-Africans.

More astonishing molecular find- ings also came in 2010 and 2012 dur- ing the analysis of the Denisovan DNA from Siberia (see above). These ancient hominins, called “Denisovans,” from central Asia quite possibly represent a different branch of recent human evo- lution (Reich et al., 2010). They are also more closely related to just some pop- ulations of modern humans, sharing about 4% to 5% of genes with contem- porary people from Melanesia (a region of islands in the south Pacific, includ- ing New Guinea, located north and east of Australia). We will focus much more on the ancestral connections of modern humans in the next chapter. As you’ll

Are They Human?

At the beginning of this chapter, we posed the question “What does it mean to be human?” applying the term human to our extinct hominin predecessors is somewhat tricky. Various prior hominin species share with contemporary Homo sapiens a mosaic of physical features. For example, they’re all bipedal, most (but not all) have fairly small canine teeth, some are completely terrestrial, and some are mod- erately encephalized (while others are much more so). thus, the physical characteristics that define humanity appear at different times during hominin evolution.

even more tenuous are the behavioral characteristics frequently identified as sig- nifying human status. the most significant of these proposed behavioral traits include major dependence on culture, innovation, cooperation in acquiring food, full language, and elaboration of symbolic representations in art and body adornment. Once again, these characteristics become apparent at different stages of hominin evolution. But distinguishing when and how these behav-

ioral characteristics became established in our ancestors is even more problematic than analyzing anatomical traits. While the archaeological record provides considerable information regarding stone tool technology, it’s mostly silent on other aspects of mate- rial culture. the social organization and language capabilities of earlier hominins are as yet almost completely invisible.

From the available evidence, we can conclude that H. erectus took significant steps in the human direction—well beyond that of earlier hominins. H. erectus vastly expanded hominin geographical ranges, achieved the full body size and limb pro- portions of later hominins, had increased encephalization, and became considerably more dependent on culture for their sur- vival, unlike previous forms, which relied more upon physical adaptations.

H. heidelbergensis (in the Middle pleis- tocene) and, to an even greater degree, Neandertals (in the Late pleistocene) maintained several of these characteris- tics—such as body size and proportions— while also showing further evolution in the human direction. Most particularly, relative brain size increased further, expanding on average about 22 percent beyond that of

H. erectus (Fig. 1). Notice, however, that the largest jump in proportional brain size occurs very late in hominin evolution— only with the appearance of fully modern humans.

In addition to brain enlargement, cranial shape also was remodeled in H. heidelber- gensis and Neandertals, producing a more globular shape of the vault as well as sug- gesting further neurological reorganization. Stone tool technology also became more sophisticated during the Middle pleistocene, with the manufacture of tools requiring a more complicated series of steps. also, for the first time, fire was definitely controlled and widely used; caves were routinely occupied; hominin ranges were success- fully expanded throughout much of europe as well as into northern asia (that is, colder habitats were more fully exploited); structures were built; the dead were delib- erately buried; and more systematic hunting took place.

Some premoderns also were like modern humans in another significant way. analysis of teeth from a Neandertal shows that these hominins had the same delayed maturation found in modern H. sapiens (Dean et al., 2001). We don’t yet have similar data for

A Closer Look

Seeing Close Human Connections: Understanding Premodern Humans 357

see, all of us derive mostly from fairly recent African ancestors. But when these African migrants came into con- tact with premodern humans living in Eurasia, some interbreeding occurred with at least two of these premodern groups. We can tell this by distinctive genetic “signatures” that can still be found in living people.

What’s more, we’ve already had tantalizing clues of how we differ from Neandertals as well as from Denisovans in terms of specific genes. As the data are further analyzed and expanded, we will surely learn more about the evolutionary development of human anatomy and human behavior. In so doing, we’ll be able to answer far more precisely the age-old question of “What does it mean to be human?”

Seeing Close Human Connections: Understanding Premodern Humans

As you can see, the Middle Pleisto-cene hominins are a very diverse group, broadly dispersed through time and space. There is considerable varia- tion among them, and it’s not easy to get a clear evolutionary picture. We know that regional populations were small and frequently isolated. As envi- ronmental conditions changed, hom- inin populations were likely pushed into smaller and smaller habitable areas, often referred to by biologists as “refugia” (Stewart and Stringer, 2012).

earlier H. heidelbergensis individuals, but it’s possible that they, too, showed this distinc- tively human pattern of development.

Did these Middle and Late pleistocene hominins have the full language capabili-

ties and other symbolic and social skills of living peoples? It’s impossible to answer this question completely, given the types of fossil and archaeological evidence available. Yet, it does seem quite possible that neither

H. heidelbergensis nor the Neandertals had the entire array of fully human attri- butes. that’s why we call them premodern humans.

So, to rephrase our initial question: “Were these hominins human?” We can answer conditionally: they were human— at least mostly so.

▲�Figure 1 Relative brain size in hominins. The scale shows brain size as cm³ per 50 kg of body weight. Premodern humans have a more than 20 percent increase in relative brain size compared to H. erectus, but modern humans show another 30 percent expan- sion beyond that seen in premodern humans.

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*There are no direct current data for body size in Sahelanthropus. Body size is estimated from tooth size in comparison with A. afarensis. Data abstracted from McHenry (1992), Wood and Collard (1999), Brunet (2002), and Carroll (2003).

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chapter 12 Premodern Humans 358

As conditions became harsher, these refugia supported fewer people, leading to a dramatic decrease in population size. In turn, such circumstances accel- erated the effects of genetic drift as well as intensifying natural selection. Biologist John Stewart and anthropolo- gist Chris Stringer (2012) have recently developed a comprehensive model employing environmental ( specifically glacial/interglacial cycles), genetic, and fossil data to explain how in Ice Age Eurasia the development and fate of refuge populations of both premod- ern and modern humans help explain species distributions, extinctions, and potential opportunities for interbreed- ing (e.g., Neandertals or Denisovans with modern humans).

We must remember, though, that it’s virtually certain that many pre- modern human populations died out, leaving no descendants. So it’s a mis- take to see an “ancestor” in every fos- sil find. Still, as a group, these Middle Pleistocene premoderns do reveal some general trends. In many ways, for exam- ple, it seems that they were transitional between the hominins that came before them (H. erectus) and the ones that fol- lowed them (modern H. sapiens). It’s not a stretch to say that all the Middle Pleistocene premoderns derived from H. erectus forebears and that some of them, in turn, were probably ancestors of the earliest fully modern humans.

Paleoanthropologists are certainly concerned with such broad generalities as these, but they also want to focus on meaningful anatomical, environmen- tal, and behavioral details as well as the underlying processes. So they consider the regional variability displayed by particular fossil samples as significant— but just how significant is debatable. In addition, increasingly sophisticated the- oretical and technological approaches are being used to better understand the processes that shaped the evolution of later Homo at both macroevolutionary and microevolutionary levels.

Scientists, like all humans, assign names or labels to phenomena—a point we addressed in discussing classifica- tion in Chapter 5. Paleoanthropologists

are certainly no exception. Yet, work- ing from a common evolutionary foun- dation, paleoanthropologists still come to different conclusions about the most appropriate way to interpret the Middle/Late Pleistocene hominins. Consequently, a variety of species names have been proposed in recent years.

Paleoanthropologists who advo- cate an extreme lumping approach recognize only one species for all the premodern humans discussed in this chapter. These premoderns are clas- sified as Homo sapiens and are thus lumped together with modern humans, although they’re partly distinguished by such terminology as “archaic H. sapiens.” As we’ve noted, this degree of lumping is no longer supported by most researchers. Alternatively, a sec- ond, less extreme view postulates mod- est species diversity and labels the ear- lier premoderns as H. heidelbergensis (Fig. 12-23a).

At the other end of the spectrum, more enthusiastic paleontological split- ters have identified at least two (or more) species distinct from H. sapiens. The most important of these, H. hei- delbergensis and H. neanderthalensis, have been discussed earlier. This more complex evolutionary interpretation is shown in Figure 12-23b.

We addressed similar differences of interpretation in Chapters 10 and 11, and we know that disparities such as these can be frustrating to students who are new to paleoanthropology. The proliferation of new names is con- fusing, and it might seem that experts in the field are endlessly arguing about what to call the fossils.

Fortunately, it’s not quite that bad. There’s actually more agreement than you might think. No one doubts that all these hominins are closely relat- ed to each other as well as to modern humans. And everyone agrees that only some of the fossil samples repre- sent populations that left descendants. Where paleoanthropologists disagree is when they start discussing which hominins are the most likely to be closely related to later hominins. The grouping of hominins into evolution-

Seeing Close Human Connections: Understanding Premodern Humans 359

ary clusters (clades) and assignment of different names to them is a reflection of differing interpretations—and, more fundamentally, of somewhat differing philosophies.

But we shouldn’t emphasize these naming and classification debates too much. Most paleoanthropologists rec- ognize that a great many of these dis- agreements result from simple, prac- tical considerations. Even the most enthusiastic splitters acknowledge that the fossil “species” are not true species as defined by the biological spe- cies concept (see Chapter 5) (Holliday, 2003). As prominent paleoanthropolo- gist Robert Foley puts it, “It is unlikely they are all biological species. . . . These are probably a mixture of real biologi-

cal species and evolving lineages of subspecies. In other words, they could potentially have interbred, but owing to allopatry [that is, geographical sep- aration] were unlikely to have had the opportunity” (Foley, 2002, p. 33).

Even so, Foley, along with an increasing number of other profession- als, distinguishes these different fossil samples with species names to high- light their distinct position in hom- inin evolution. That is, these hominin groups are more loosely defined as a type of paleospecies (see Chapter 5) rather than as fully biological species. Giving distinct hominin samples a sep- arate (species) name makes them more easily identifiable to other researchers and makes various cladistic hypotheses

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▲�Figure 12-23 (a) Phylogeny of the genus Homo. Only very modest spe- cies diversity is implied. (b) Phylogeny of genus Homo showing considerable species diversity (after Foley, 2002).

chapter 12 Premodern Humans 360

more explicit and, equally important, more directly testable.

The hominins that best illus- trate these issues are the Neandertals. Fortunately they’re also the best known, represented by dozens of well- preserved individuals and also a com- plete genome. With all this evidence, researchers can systematically test and evaluate many of the differing hypotheses.

Are Neandertals very closely related to modern H. sapiens? Certainly. Are they physically and behaviorally some- what distinct from both ancient and fully modern humans? Yes. Does this mean that Neandertals are a fully sep- arate biological species from modern humans and therefore theoretically incapable of fertilely interbreeding with modern people? Almost certainly not. Finally, then, should Neandertals really be placed in a separate species from H. sapiens? For most purposes, it doesn’t matter, since the distinction at some point is arbitrary, like looking at a spectrum of colors that grade from red to orange to yellow. Where does one color definitely begin and end? Is

that reddish-orange or is it orangey- red? Speciation is, after all, a dynamic process and fossil groups such as the Neandertals represent just one point in this process (see Chapter 5), which continues even today.

We can view Neandertals as a dis- tinctive side branch of later hom- inin evolution. It is not unreasonable to say that Neandertals were likely an incipient species. The much less well- known “Denisovans” from Siberia also likely represent another partially dis- tinct incipient species, separate from both Neandertals and early mod- ern humans. Given enough time and enough isolation, Neandertals and Denisovans likely would have sepa- rated completely from their modern human contemporaries. The new DNA evidence suggests that they were part- ly on their way but had not yet reached full speciation from Homo sapiens. Their fate, in a sense, was decided for them as more successful competitors expanded into their habitats. These highly successful hominins were fully modern humans, and in the next chap- ter we’ll focus on their story.

We know a great deal about premodern humans, based both on fossil finds as well as new and highly informa- tive DNA data. Not only have a large number of fossils been discovered but, for the first time, many are quite complete (as a result of deliberate burial). In addition, more complete archaeological remains make it possi- ble to test much more specific hypotheses about their behavior than is possible for any earlier group of homi-

nins. Last, the detailed DNA data, obtained from skel- etal remains dated from as early as 60,000 years ago, allow far-reaching scientific study and rigorous con- clusions regarding exactly how similar these homi- nins were to us. Indeed, new studies have shown that they interbred with early modern humans, and we can still see traces of this gene exchange in living human populations.

How Do We Know?

361Critical Thinking Questions

▶▶ Premodern humans from the Middle Pleistocene show similarities both with their predecessors (H. erectus) and with their successors (H. sapiens). They’ve also been found in many areas of the Old World—in Africa, Asia, and Europe.

▶▶ Most paleoanthropologists call the majority of Middle Pleistocene fossils H. heidelbergensis. Similarities between the African and European Middle Pleistocene hominin samples suggest that they can all reasonably be seen as part of this same species, but contemporaneous Asian fossils don’t fit as neatly into this model.

▶▶ Some of the later H. heidelbergensis populations in Europe likely evolved into Neandertals, and abun-

dant Neandertal fossil and archaeological evidence has been collected from the Late Pleistocene time span of Neandertal existence, about 130,000 to 30,000 ya.

▶▶ Neandertals are more geographically restricted than earlier premoderns and are found in Europe, southwest Asia, and central Asia.

▶▶ Neandertals have been considered quite distinct from modern H. sapiens, but recent genetic evi- dence confirms that some interbreeding took place between these hominins (likely 80,000 to 50,000 ya).

Summary of Main Topics

1. Why are the Middle Pleistocene hominins called premodern humans? In what ways are they human?

2. What is the general popular conception of Neandertals? Based on what you have just learned, would you agree with this view? (Cite both ana- tomical and archaeological evidence to support your conclusion.)

3. What evidence suggests that Neandertals deliber- ately buried their dead? Do you think the fact that

they buried their dead is important? Why? How would you interpret this behavior (remembering that Neandertals were not identical to us)?

4. How are species defined, both for living animals and for extinct ones? Use the Neandertals to illus- trate the problems encountered in distinguishing species among extinct hominins. Contrast specifi- cally the interpretation of Neandertals as a distinct species with the interpretation of Neandertals as a subspecies of H. sapiens.

Critical Thinking Questions

Modern humans first evolved in Africa and later spread

to other areas of the world, where they occasionally inter-

bred with Neandertals and other pre-modern humans.

Connections

The immediate predeces- sors of modern humans,

including the Neandertals, were much like us, but

had some anatomical and behavioral differences.

Modern human variation is best understood by examining similarities and differences in DNA

among populations.

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After mastering the material in this chapter, you should be able to:

▶ �Compare and contrast the two major models that seek to explain modern human origins.

▶ �Explain the evidence that supports each model and critically evaluate why recent molecular evidence has largely solved this issue.

▶ �Describe the major geographical areas and general dating of the key early fossil evidence of modern humans.

▶ �Describe the major physical features of Homo floresiensis and explain why the discovery of this hominin was such a surprise.

▶ �Discuss the cultural developments that characterize the Upper Paleolithic as well as contemporaneous cultures in other parts of the world (e.g., Africa) and contrast these with cultural/ technological practices of earlier periods.

363

Today, our species numbers more than 7 billion individu-als spread all over the globe, and there are no other living homi- nins but us. Our last hominin cousin disappeared several thousand years ago. Perhaps about 80,000 ya, modern peoples in the Middle East encoun- tered beings that walked on two legs, hunted large animals, made fire, lived in caves, and fashioned complex tools. These beings were the Neandertals, and imagine what it would have been like to be among a band of modern people following game into what is now Israel and coming across these other humans, so like yourself in some ways, yet so different in others. It’s almost certain that such encounters took place, perhaps many times. How strange would it have been to look into the face of a being sharing so much with you, yet being a total stranger both culturally and, to some degree, biologically? What would you think seeing a Neandertal for the first time? What do you imagine a Neandertal would think seeing you? If a similar encounter had occurred in southern Siberia, modern people would quite likely have been staring into the eyes of a Denisovan. What would that have been like?

At some time, probably close to 200,000 ya, the first modern Homo sapiens populations appeared in Africa. Within 150,000 years or so, their descendants had spread across most of the Old World, even expanding as far as Australia (and somewhat later to the Americas).

13The Origin and Dispersal of Modern Humans

Who were they, and why were these early modern people so successful? What was the fate of the other homi- nins, such as the Neandertals, who were already long established in areas outside Africa? Did they continue to evolve as well, leaving descendants among some living human popula- tions? Or did they go extinct, com- pletely swept aside and replaced by African emigrants?

In this chapter, we’ll discuss the ori- gin and dispersal of modern H. sapi- ens sapiens. All contemporary popu- lations are placed within this species and subspecies. Most paleoanthropol- ogists agree that several fossil forms of Homo sapiens, dating back as far as 100,000 ya, should also be included in the same fully modern group as our- selves. In addition, some recently dis- covered fossils from Africa are also

Student Learning Objectives

chapter 13 The Origin and Dispersal of Modern Humans 364

clearly H. sapiens, though they show some (minor) differences from living people and could thus be more accu- rately described as near-modern. Still, we can think of these early African humans as well as their somewhat later relatives as “us.”

These first modern humans, who had evolved by 195,000 ya, were probably descendants of some of the premodern humans we discussed in Chapter 12. In particular, African populations of H. heidelbergensis are the most likely ancestors of the ear- liest modern H. sapiens. The evo- lutionary events that took place as modern humans made the transi- tion from more ancient premodern forms and then dispersed throughout most of the Old World were relatively rapid, and they raise several basic questions:

1. When (approximately) did modern humans first appear?

2. Where did the transition take place? Did it occur in just one region or in several?

3. What was the pace of evolutionary change? How quickly did the tran- sition occur and was it uniform across regions?

4. How did the dispersal of modern humans to other areas of the Old World (outside their area of origin) take place?

These questions concerning the origins and early dispersal of modern Homo sapiens continue to fuel much controversy among paleoanthropolo- gists. And it’s no wonder, for at least some early H. sapiens populations are the direct ancestors of all contempo- rary humans. They were much like us skeletally, genetically, and (most likely) behaviorally. In fact, it’s the various hypotheses regarding the behaviors and abilities of our most immediate predecessors that have most fired the imaginations of scientists and laypeo- ple alike. In every major respect, these are the first hominins that we can con- fidently refer to as fully human.

In this chapter, we’ll also discuss archaeological evidence coming from the Upper Paleolithic cultures. This evidence will give us a better under- standing of the technological and social developments during the period when modern humans arose and quickly came to dominate the planet.

The evolutionary story of Homo sapiens is really the biological autobi- ography of all of us. It’s a story that still has many unanswered questions, but some general theories can help us orga- nize the many lines of evidence that are now available.

Approaches to Understanding Modern Human Origins

In attempting to organize and explain modern human origins, paleoanthro- pologists have proposed a few major hypotheses that can be summarized into two contrasting views: the multi- regional continuity model and various versions of replacement models. These two views are quite distinct, and in some ways they’re completely opposed to each other. Since so much of our contemporary view of modern human origins is influenced by the debates linked to these differing models, we’ll start by briefly reviewing them. Then we’ll turn to the fossil evidence and emerging genetic analyses to see what morphology and molecules can con- tribute to answering the four questions we’ve posed.

The Regional Continuity Model: Multiregional Evolution The multiregional continuity model is most closely associated with paleo- anthropologist Milford Wolpoff of the University of Michigan and his associ- ates (Wolpoff et al., 1994, 2001). They

Approaches to Understanding Modern Human Origins 365

suggest that local populations—not all, of course—in Europe, Asia, and Africa continued their indigenous evolution- ary development from premodern Mid- dle Pleistocene forms to anatomically modern humans. But if that’s true, we have to ask how so many different local populations around the globe happened to evolve with such simi- lar morphology. In other words, how could anatomically modern humans arise separately in different conti- nents and end up so much alike, both physically and genetically? The multi- regional model answers this question by (1) denying that the earliest mod- ern H. sapiens populations originated exclusively in Africa and (2) assert- ing that significant levels of gene flow (migration and interbreeding) between various geographically dispersed pre- modern populations were extremely likely throughout the Pleistocene.

Through gene flow and natural selection, according to the multi- regional hypothesis, local populations would not have evolved totally inde- pendently from one another, and such mixing would have “prevented spe- ciation between the regional lineages and thus maintained human beings as a single, although obviously polytyp- ic [see Chapter 14], species through- out the Pleistocene” (Smith et al., 1989). Thus, under a multiregional model, there are no taxonomic distinctions between modern and premodern hom- inins. That is, all hominins following Homo erectus are classified as a single species: Homo sapiens.

In light of emerging evidence over the last few years, advocates of the mul- tiregional model tend not to be dog- matic about the degree of regional con- tinuity. They recognize that a strong influence from modern humans evolv- ing first in Africa has left an imprint on populations throughout the world that is still genetically detectable today. Nevertheless, the most recent data sug- gest that multiregional models no lon- ger tell us much that is useful about the origins of modern humans, nor do they seem to provide much informa-

tion regarding the dispersal of modern H. sapiens.

Replacement Models Replacement models all emphasize that modern humans first evolved in Africa and only later dispersed to other parts of the world, where they replaced those hominins already living in these other regions. In recent years, two versions of such replacement models have been proposed, the first emphasizing complete replacement. The complete replacement model pro- poses that anatomically modern popu- lations arose in Africa within the last 200,000 years and then migrated from Africa, completely replacing popu- lations in Europe and Asia (Stringer and Andrews, 1988). It’s important to note that this model doesn’t account for a transition from premodern forms to modern H. sapiens anywhere in the world except Africa. Stringer and Andrews’ original hypothesis argued that anatomically modern humans appeared as the result of a biologi- cal speciation event. So in this view, migrating African modern H. sapiens could not have successfully interbred with local non-African populations producing fertile offspring because the African modern humans were a bio- logically different species. Under this model, all of the premodern popula- tions outside Africa would be taxo- nomically classified as belonging to different species of Homo. For exam- ple, the Neandertals would be clas- sified as H. neanderthalensis. This explanation of nonhybridizing specia- tion would fit nicely with, and, in fact, help explain complete replacement; but Stringer has more recently stated that he isn’t insistent on this issue. He does suggest that even though there may have been potential for interbreed- ing, apparently very little actually took place (Stewart and Stringer, 2012).

Interpretations of the latter phases of human evolution have recently been greatly extended and aided by newly available genetic techniques

chapter 13 The Origin and Dispersal of Modern Humans 366

that have been applied to the question of modern human origins. Drawing genetic data from numerous geograph- ically diverse contemporary human populations, geneticists have precisely determined and compared a wide variety of DNA sequences in order to gain a better understanding of cur- rent human variation. The theoretical basis of this approach assumes that at least some of the genetic patterning seen today can act as a kind of window into the past. In particular, the genetic patterns observed today between geo- graphically widely dispersed humans are thought to partly reflect migra- tions occurring in the Late Pleistocene. This hypothesis can be further tested as contemporary and archaic popula- tion genetic patterning becomes better documented.

As these new data have accumu- lated and are being assimilated, reli- able relationships are emerging, espe- cially those showing that indigenous African populations have far greater diversity than do populations from elsewhere in the world. The consis- tency of the results is highly signifi- cant because it strongly supports an African origin for modern humans and some subsequent mode of replace- ment across other regions. What’s more, as we will discuss in Chapter 14, new, even more complete nuclear genomic data on contemporary pop- ulation patterning further confirm these observations.

Certainly, most molecular data come from contemporary individuals, since ancient DNA is not usually pre- served. Even so, exceptions do occur; for example, the Ice Man and two very recently sequenced 7,000-year-old Iberian hunter-gatherers (Sánchez- Quinto et al., 2012). These cases open another genetic window—one that can directly illuminate the past. As discussed in Chapter 12, mtDNA has been recovered from more than a dozen Neandertal fossils.

In addition, researchers have recent- ly sequenced the mtDNA of nine ancient fully modern H. sapiens skel-

etons from sites in Italy, France, the Czech Republic, and Russia (Caramelli et al., 2003; Kulikov et al., 2004; Serre et al., 2004). MtDNA data, however, are somewhat limited because mtDNA is a fairly small segment of DNA, and since it is transmitted between gen- erations without recombination with male DNA, it only provides informa- tion regarding the maternal lineage. Indeed, in just the last few years, com- parisons of Neandertal and early mod- ern mtDNA have led to some signifi- cant misinterpretations. It should be no surprise, though, that data from the vastly larger nuclear genome are far more informative.

As we discussed in Chapter 12, a giant leap forward occurred in 2010 when sequencing of the entire Neandertal nuclear genome was com- pleted. Researchers immediately compared the Neandertal genome with that of people living today and discovered that some populations still retain some Neandertal genes (Green et al., 2010; Reich et al., 2011). Without doubt, we can now conclude that some interbreeding took place between Neandertals and modern humans, arguing against complete replacement and supporting some form of partial replacement.

Partial Replacement Models For a num- ber of years, several paleoanthropol- ogists, such as Günter Bräuer, of the University of Hamburg, suggested that very little interbreeding occurred—a view supported more recently by John Relethford (2001) in what he described as “mostly out of Africa.” The DNA analysis done in 2010 by Green and colleagues confirms that the degree of interbreeding was modest, ranging from 1 to 4 percent in modern popula- tions outside Africa, while also reveal- ing that contemporary Africans have no trace of Neandertal genes, suggest- ing that the interbreeding occurred after modern humans migrated out of Africa. Another fascinating discov- ery is that among the modern peo- ple so far sampled for these compari-

Approaches to Understanding Modern Human Origins 367

sons (five individuals: two African, one European, one Asian and one Pacific Islander), the three non-Africans all have some Neandertal DNA. The ten- tative conclusion from these prelimi- nary findings suggests that the inter- breeding occurred soon after modern humans emigrated out of Africa. The most likely scenario suggests that the intermixing occurred around 80,000 to 50,000 ya, quite possibly in the Mid- dle East and only later in Europe and then Asia.

These results are very new and are partly based on very limited sam- ples of living people. Technological innovations in DNA sequencing are occurring at an amazing pace, mak- ing it faster and cheaper. But it is still a challenge to sequence all the 3 bil- lion nucleotides each of us has in our nuclear genome. When we have full genomes from more individuals living in many more geographical areas, the patterns of modern human dispersal should become clearer. Did the mod- ern human- Neandertal interbreeding occur primarily in one area, or did it happen in several regions? Moreover, did some modern human populations several thousand years ago interbreed with their Neandertal cousins more than others did?

We can ask yet another question, which is perhaps even most interest- ing: Were there still other premodern human groups still around when mod- ern humans emigrated from Africa— and did they interbreed with mod- ern humans too? As we discussed in Chapter 12, the answer is yes! Detailed DNA evidence from the fragmen- tary remains from Denisova Cave in southern Siberia show that these hom- inins had also interbred with mod- ern humans. What’s more, these Denisovans may have been quite wide- spread, since we can today still see a few of their genes in Southeast Asian, Pacific islands, and Australian popula- tions (Reich et al., 2011; Rasmussen et al., 2011).

This recent research has helped to support what appears to have been (at

least) a two-stage migration of mod- ern humans into Asia (after an earlier initial migration of modern humans out of Africa). The earlier of these migrations took place through parts of Southeast Asia and eventually reached the South Pacific (including New Guinea and Australia). In fact, the recent whole genome sequenc- ing using the hair from an Australian Aboriginal man who lived 100 years ago shows that he had Denisovan genes and that Aboriginal populations diverged from other groups 75,000 to 62,000 ya. The second migration occurred considerably later (38,000 to 25,000 ya), and it led to the peo- pling of eastern Asia (Rasmussen et al., 2011).

From his study of fossil remains, Fred Smith of Illinois State University has proposed an “assimilation” model hypothesizing that more interbreeding did take place, at least in some regions (Smith, 2002). To test these hypoth- eses and answer all the fascinating questions associated with them, we will also need more whole-genome DNA from ancient remains, particu- larly from early modern human skel- etons. New technology applied just in the last year allows far faster DNA sequencing; so at least some of our questions may soon be answered. However, we also need to be aware that DNA thousands of years old can be obtained from hominin remains found in environments that have been persistently cold (or at least cool). In tropical areas, DNA degrades rapidly, so it seems a long shot that any usable DNA can be obtained from homi- nins that lived in many extremely large and significant regions (for example, Africa and Southeast Asia). Nevertheless, another alternative and very useful approach to partly answer these questions uses the genetic pat- terning still visible in contemporary humans. From such studies we know that there was more interbreeding and eventual gene flow of Denisovan genes in Asia (and the Pacific) than there was in Europe.

chapter 13 The Origin and Dispersal of Modern Humans 368

The Earliest Discoveries of Modern Humans

Africa In Africa, several early (around 200,000 to 100,000 ya) fossils have been inter- preted as fully anatomically modern forms (Fig. 13-2). The earliest of these specimens comes from Omo Kibish, in southernmost Ethiopia. Using radio- metric techniques, the redating of a fragmentary skull (Omo 1) demon- strated that this is the earliest mod- ern human—originating 195,000 ya— yet found in Africa or, for that matter, anywhere (McDougall et al., 2005). An interesting aspect of fossils from this site concerns the variation shown between the two individuals. Omo 1 (Fig. 13-1) is essentially modern in most respects (note the presence of a chin; see Fig. 13-3, where a variety of mod- ern human cranial characteristics are shown). But another ostensibly contem- porary cranium (Omo 2) is much more robust and less modern in morphology.

Somewhat later modern human fos- sils come from the Klasies River Mouth on the south coast of Africa and from

Border Cave, just slightly to the north. Using relatively new

techniques, paleoan- thropologists have

dated both sites to about 120,000

to 80,000 ya. The origi- nal geologi- cal context at Border Cave is uncertain, and the fos- sils may be younger

than those at Klasies

River Mouth. Although a

recent reevalua- tion of the Omo site

has provided much more dependable dating, there

are still questions about some of the other early African modern fossils. Nevertheless, it now seems very likely that early modern humans appeared in East Africa by shortly after 200,000 ya and had migrated to southern Africa by approximately 100,000 ya. More recently discovered fossils are helping to confirm this view.

Herto The announcement in 2003 of well-preserved and well-dated H. sapi- ens fossils from Ethiopia has gone a long way toward filling gaps in the African fossil record. As a result, these fossils are helping to resolve key issues regard- ing modern human origins. Tim White of the University of California, Berkeley, and his colleagues have been working for three decades in the Middle Awash area of Ethiopia. They’ve discovered a remarkable array of early fossil homi- nins (Ardipithecus and Australopithe- cus) as well as somewhat later forms (H. erectus). From this same area in the Middle Awash, further highly signifi- cant discoveries came to light in 1997. For simplicity, these new hominins are referred to as the Herto remains.

These Herto fossils include a most- ly complete adult cranium, an incom- plete adult cranium, a fairly complete (but heavily reconstructed) child’s cra- nium, and a few other cranial frag- ments. Following lengthy reconstruc- tion and detailed comparative studies, White and colleagues were prepared to announce their findings in 2003.

What they said caused quite a sensa- tion among paleoanthropologists, and it was reported in the popular press as well. First, well-controlled radiomet- ric dating (40Ar/39Ar) securely places the remains at between 160,000 and 154,000 ya, making these the best- dated hominin fossils from this time period from anywhere in the world. Note that this date is clearly older than for any other equally modern H. sapiens from anywhere else in the world. Moreover, the preservation and morphology of the remains leave little doubt about their relationship to modern humans. The mostly complete adult cranium (Fig. 13-4) is very large, with an extremely ©

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▼�Figure 13-1 Reconstructed skull of Omo 1, an early modern human from Ethiopia, dated to 195,000 ya. Note the clear presence of a chin.

The Earliest Discoveries of Modern Humans 369

A F R I C A

ITALY

S P A I N

P O R T U G A L T U R K E Y

GREECE

K E N Y A

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E G Y P T

N I G E R M A U R I T A N I A

M A L I

N I G E R I A

S O M A L I A

N A M I B I A

L I B Y A

C H A D

SOUTH AFRICA

T A N Z A N I A

A N G O L A

A L G E R I A

MADAGASCAR

MOZAMBIQUE

B O T S W A N A

Z A M B I A

GABON

CENTRAL AFRICAN REPUBLIC

TUNISIA M O R O C C O

UGANDA

SWAZILAND

LESOTHO

MALAWI

BURUNDI

TOGO

BENIN

GHANA

LIBERIA

SIERRA LEONE

GUINEA

BURKINA FASO

THE GAMBIA

CAMEROON

Z I M B A B W E

EQUATORIAL GUINEA

WESTERN SAHARA

DJIBOUTI

SENEGAL

GUINEA-BISSAU

JORDANISRAEL

LEBANON

KUWAIT

U. A. E.

Y E M E N

O M A N

SYRIA I R A Q I R A N

S A U D I A R A B I A

MALTA

RWANDA

CÔTE D’IVOIRE

REP. OF THE

CONGO D E M O C R A T I C

R E P U B L I C

O F T H E C O N G O

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Klasies River Mouth

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▲�Figure 13-2 Modern humans from Africa and the Near East.

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chapter 13 The Origin and Dispersal of Modern Humans 370

Relatively small browridges

Canine fossa

Jebel Qafzeh 6

Cro-Magnon I

Pyramidal mastoid process

Definite chin

Vertical forehead

Border Cave 1

Skhul 5–

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▲�Figure 13-3 Morphology and variation in early specimens of modern Homo sapiens.

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The Earliest Discoveries of Modern Humans 371

long cranial vault. The cranial capac- ity is 1,450 cm³, well within the range of contemporary H. sapiens populations. The skull is also in some respects heav- ily built, with a large, arching browridge in front and a large, projecting occipital protuberance in back. The face does not project, in stark contrast to Eurasian Neandertals.

The overall impression is that this individual is clearly Homo sapiens— as are the other fossils from the site. Following comprehensive statisti- cal studies, Tim White and colleagues concluded that, though not identical to modern people, the Herto fossils are near-modern. That is, these fos- sils “sample a population that is on the verge of anatomical modernity but not yet fully modern” (White et al., 2003, p. 745). To distinguish these individuals from fully modern humans (H. sapiens sapiens), the researchers have placed them in a newly defined subspecies: Homo sapiens idaltu. The word idaltu, from the Afar language, means “elder.”

What, then, can we conclude? First, we can say that these new finds strong- ly support an African origin of modern humans. The Herto fossils are the right age, and they come from the right place. Besides that, they look much like what we might have predicted. Considering all these facts, they’re the most con- clusive fossil evidence yet indicating

an African origin of modern humans. What’s more, this fossil evidence is compatible with a great deal of strong genetic data indicating some form of replacement model for human origins.

The Near East In Israel, in the Skhūl Cave at Mt. Car- mel, researchers found early modern H. sapiens fossils, including the remains of at least 10 individuals (Figs. 13-5 and

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▲�Figure 13-4 Herto cranium from Ethiopia, dated 160,000 to 154,000 ya. This is the best-preserved early modern H. sapiens cranium yet found.

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◀�Figure 13-5 Mt. Carmel, studded with caves, was home to H. sapiens sapiens at Skhū l (and to Neandertals at Tabun and Kebara).

chapter 13 The Origin and Dispersal of Modern Humans 372

13-6a). Also from Israel, the Qafzeh Cave has yielded the remains of at least 20 individuals (Fig. 13-6b). Although their overall configuration is definitely modern, some specimens show certain premodern features. Skhūl has been dated to between 130,000 and 100,000 ya (Grün et al., 2005), while Qafzeh has been dated to around 120,000 to 92,000 ya (Grün and Stringer, 1991). The time line for these fossil discover- ies is shown in Figure 13-7.

Such early dates for modern speci- mens pose some problems for those advocating the influence of local evolu- tion as proposed by the multiregional

model. How far back do the premodern populations—that is, Neandertals— appear in the Near East? A chronomet- ric calibration for the Tabun Cave sug- gests a date as early as 120,000 ya. This dating for these sites, all located very close to each other, suggests that there’s considerable chronological overlap in the occupation of the Near East by Neandertals and modern humans. This chronological overlap in such a small area (as well as in close proximity to Africa) has led anthropologists to sug- gest this region as a likely place where Neandertals and modern humans might well have interbred.

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a b▶�Figure 13-6 (a) Skhū l 5. (b) Qafzeh 6. These specimens from Israel are thought to be representatives of early modern Homo sapiens. The vault height, forehead, and lack of progna- thism are modern traits.

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200,000 ya 160,000 ya 120,000 ya 100,000 ya 80,000 ya 60,000 ya 40,000 ya 20,000 ya

Kow Swamp

140,000 ya180,000 ya 190,000 ya 150,000 ya 110,000 ya 90,000 ya 70,000 ya 50,000 ya 30,000 ya 10,000 ya130,000 ya170,000 ya

Lake Mungo

Mladec

Cro-Magnon

Lagar Velho

Niah Cave

Tianyuan

Ordos Zhoukoudian (Upper Cave)

Jebel Qafzeh

Klasies River Mouth

Omo Kibish

Border Cave

Herto

Skhul

? ?

Oase

EUROPE

AUSTRALIA

SOUTHEAST ASIA

CHINA

NEAR EAST

AFRICA

▼�Figure 13-7 Time line of modern Homo sapiens discoveries. Note that most dates are approximations. Question marks indicate those esti- mates that are most tentative.

The Earliest Discoveries of Modern Humans 373

Asia There are seven early anatomically modern human localities in China, the most significant of which are Upper Cave at Zhoukoudian, Tianyuan Cave (very near Zhoukoudian), and Ordos, in Mongolia (Fig. 13-8). The fossils from these Chinese sites are all fully modern, and all are considered to be from the Late Pleistocene, with dates probably later than 40,000 ya. Many of these dates are controversial and not very precise; for example, Upper Cave at Zhoukoudian has been dated vari- ously to between 10,000 and 29,000 ya (Cunningham and Wescott, 2002).

In addition, some researchers (e.g., Tiemel et al., 1994) have suggested that the Jinniushan skeleton discussed in Chapter 12 hints at modern features in China as early as 200,000 ya. If this date—as early as that proposed for direct antecedents of modern H. sapi- ens in Africa—should prove accurate, it would cast doubt on replacement mod- els. This position, however, is a minor- ity view and is not supported by more recent and more detailed analyses.

Just about four miles down the road from the famous Zhoukoudian Cave

is another cave called Tianyuan, the source of an important find in 2003. Consisting of a fragmentary skull, a few teeth, and several postcranial bones, this fossil is accurately dated by radio- carbon at close to 40,000 ya (Shang et al., 2007). The skeleton shows mostly modern features but has a few archa- ic characteristics as well. The Chinese and American team that analyzed the remains from Tianyuan proposes that they indicate an African origin of mod- ern humans, but there is also evidence of at least some interbreeding in China with resident archaic (that is, premod- ern) populations. More complete anal- ysis and (with some luck) further finds at this new site will help to provide a better picture of early modern H. sapi- ens in China. For the moment, this is the best-dated early modern H. sapiens from China and one of the two earliest from anywhere in Asia.

The other early fossil is a partial skull from Niah Cave on the north coast of the Indonesian island of Borneo (see Fig. 13-8). This is actu- ally not a new find and was, in fact, first excavated more than 50 years ago. However, until recent, more extensive

Key Early Modern Homo sapiens Discoveries from Africa and the Near East

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Date Site Hominin Evolutionary Significance

110,000 ya Qafzeh (Israel)

H. sapiens sapiens

Large sample (at least 20 individuals); definitely modern, but some individuals fairly robust; early date (>100,000 ya)

115,000 ya Skhūl (Israel)

H. sapiens sapiens

Minimum of 10 individuals; like Qafzeh modern morphology, but slightly earlier date (and earliest modern humans known outside of africa)

160,000– 154,000 ya

herto (ethiopia)

H. sapiens idaltu Very well-preserved cranium; date >150,000 ya, the best- preserved early modern human found anywhere

195,000 ya Omo (ethiopia)

H. sapiens Dated almost 200,000 ya and the oldest modern human found anywhere; two crania found, one more modern looking than the other

At a Glance

chapter 13 The Origin and Dispersal of Modern Humans 374

A U S T R A L I A

M A L A Y S I A

C H I N A

M O N G O L I A

I N D O N E S I A

PAPUA NEW GUINEA

BRUNEI

JAPAN

TAIWAN

VIETNAM

CAMBODIA

THAILAND

SOUTH KOREA

NORTH KOREA

BURMA

LAOS

P H I L I P P I N E S

SUMATRA

JAVA

SOLOMON ISLANDS

I N D I A BANGLADESH

BHUTAN

NEPAL

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Zhoukoudian/Tianyuan (Upper Cave)

Kow Swamp

Lake Mungo

Niah Cave

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▲�Figure 13-8 Anatomically modern Homo sapiens in Asia and Australia.

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The Earliest Discoveries of Modern Humans 375

analysis, it had been relegated to the paleoanthropological back shelf owing to uncertainties regarding its archae- ological context and dating. Now all this has changed with a better under- standing of the geology of the site and new dates strongly supporting an age of more than 35,000 ya—most likely even 45,000 to 40,000 ya, making it per- haps older than Tianyuan (Barker et al., 2007). Like its Chinese counterparts, the Niah skull is modern in morphol- ogy. It’s hypothesized that some pop- ulation contemporaneous with Niah or somewhat earlier inhabitants of Indonesia was perhaps the first group to colonize Australia.

Australia During glacial times, the Indonesian islands were joined to the Asian main- land, but Australia wasn’t. It’s likely that by 50,000 ya, modern humans inhabited Sahul—the area includ- ing New Guinea and Australia. Bam- boo rafts may have been used to cross the ocean between islands, though this would certainly have been danger- ous and difficult. It’s not known just where the ancestral Australians came from, but as noted, Indonesia has been suggested.

Human occupation of Australia occurred quite early, as indicated by several types of evidence. Some archae- ological sites have been dated 55,000 ya. There’s some controversy about the dating of the earliest Australian human remains, which are all modern H. sapi- ens. The earliest finds so far discov- ered have come from Lake Mungo, in southeastern Australia (see Fig. 13-8). In agreement with archaeological con- text and radiocarbon dates, the homi- nins from this site have been dated at approximately 30,000 to 25,000 ya.

Fossils from a site called Kow Swamp suggest that the people who lived there between about 14,000 and 9,000 ya were different from the more gracile early Australian forms from Lake Mungo (see Fig. 13-8). The Kow Swamp fossils display certain archaic cranial traits—such as reced-

ing foreheads, heavy supraorbital tori, and thick bones—that are difficult to explain, since these features con- trast with the postcranial anatomy, which matches that of living indige- nous Australians. Regardless of the different morphology of these later Australians, recent genetic evidence indicates that all native Australians are descendants of a single migra- tion dating back to at least 50,000 ya (Hudjashou et al., 2007). Even newer research using the whole genome anal- ysis of an Aboriginal Australian male (mentioned earlier) suggests that the divergence of native Australian popu- lations occurred sometime between 75,000 and 62,000 ya.

Central Europe Central Europe has been a source of many fossil finds, including the earli- est anatomically modern H. sapiens yet discovered anywhere in Europe. Dated to approximately 40,000 ya, these early H. sapiens fossils come from dis- coveries at the Oase Cave in Roma- nia (Fig. 13-9). Here cranial remains of three individuals were recovered, including a complete mandible and a partial skull. While quite robust, they are similar to later modern specimens, as seen in the clear presence of both a chin and a canine fossa (see Fig. 13-3) (Trinkaus et al., 2003; Crevecoeur et al., 2009).

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▼�Figure 13-9 Excavators at work within the spectacular cave at Oase, in Romania. The floor is littered with the remains of fossil animals, including the earliest dated cranial remains of Homo sapiens in Europe.

chapter 13 The Origin and Dispersal of Modern Humans 376

S P A I N I T A L Y

S W I T Z . A U S T R I A H U N G A R Y

F R A N C E

G E R M A N Y

P O L A N D

R O M A N I A

B U L G A R I A

U K R A I N E

M O L D O V A

T U R K E Y

G R E E C E

M A C E D O N I A

B E L A R U S

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CROATIA

C Z E C H . R E P .

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Combe Capelle Cro-Magnon

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▲�Figure 13-10 Anatomically modern humans in Europe.

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The Earliest Discoveries of Modern Humans 377

Another early modern human site in central Europe is Mladeč in the Czech Republic (Fig. 13-10). Several individuals have been excavated here and are dated to approximately 31,000 ya. Although there’s some variation among the crania, includ- ing some with big browridges, Fred Smith (1984) is confident that they’re all best classified as modern H. sapiens (Fig. 13-11). It’s clear that by 28,000 ya, modern humans were widely dis- persed in central and western Europe (Trinkaus, 2005).

Western Europe For several reasons, western Europe (and its fossils) has received more attention than other regions. Over the last 150 years, many of the scholars doing this research happened to live in western Europe, and the southern region of France turned out to be a fos- sil treasure trove.

As a result of this scholarly inter- est, a great deal of data accumulated beginning back in the nineteenth cen- tury, with little reliable comparative information available from elsewhere in the world. Consequently, theories of human evolution were based almost exclusively on the western European material. It’s only been in more recent years, with growing evidence from other areas of the world and the appli- cation of new dating techniques, that recent human evolutionary dynamics are being seriously considered from a worldwide perspective.

Western Europe has yielded many anatomically modern human fossils, but by far the best-known sample of western European H. sapiens is from the Cro-Magnon site, a rock shelter in southern France. At this site, the remains of eight individuals were dis- covered in 1868.

The Cro-Magnon materials are associated with an Aurignacian tool assemblage, an Upper Paleolithic industry. Dated at about 28,000 ya, these individuals represent the ear-

liest of France’s anatomically mod- ern humans. The so-called Old Man (Cro-Magnon 1) became the original model for what was once termed the Cro-Magnon, or Upper Paleolithic, “race” of Europe (Fig. 13-12). Actually, of course, there’s no such valid bio- logical category, and Cro-Magnon 1 is not typical of Upper Paleolithic west- ern Europeans—and not even all that similar to the other two male skulls found at the site.

Most of the genetic evidence, as well as the newest fossil evidence from Africa, argues against continu- ous local evolution producing mod- ern groups directly from any Eurasian premodern population (in Europe, these would be Neandertals). Still, for some researchers, the issue isn’t com- pletely settled. With all the latest evi- dence, there’s no longer much debate that a large genetic contribution from migrating early modern Africans influenced other groups throughout the Old World. What’s being debated is just how much admixture might have occurred between these migrat- ing Africans and the resident premod- ern groups. For those paleoanthropol- ogists (for example, Trinkaus, 2005) who hypothesize that significant admixture (assimilation) occurred in western Europe as well as else- where, a recently discovered child’s skeleton from Portugal provides some of the best skeletal evidence of possible interbreeding between Neandertals and anatomically mod- ern H. sapiens. This important discov- ery from the Abrigo do Lagar Velho site was excavated in late 1998 and is dated to 24,500 ya—that’s at least 5,000 years more recent than the last clearly identifiable Neandertal fossil. Associated with an Upper Paleolithic industry and buried with red ocher and pierced shell is a fairly complete skeleton of a 4-year-old child (Duarte et al., 1999). In studying the remains, Cidália Duarte, Erik Trinkaus, and their colleagues found a highly mixed set of anatomical features. From this

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▲�Figure 13-11 The Mladec̆ cranium from the Czech Republic represents a good example of early modern Homo sapiens in central Europe. Along with Oase, in Romania, the evidence for early modern Homo sapiens appears first in central Europe before the later finds in western Europe.

Cro-Magnon (crow-man´-yon)

Aurignacian pertaining to an Upper paleolithic stone tool industry in europe beginning at about 40,000 ya.

chapter 13 The Origin and Dispersal of Modern Humans 378

evidence they concluded that the young child was the result of inter- breeding between Neandertals and modern humans and thus sup- ports a partial replacement model of human origins. It’s still debatable from this fossil evidence whether interbreeding with Neandertals took place in Portugal this late in time. Nevertheless, the genetic evidence is unequivocal: Neandertals and modern humans did interbreed at some point, though the extent and frequency are presently unknown.

Something New and Different: The “Little People”

As we’ve seen, by 25,000 years ago, modern humans had dispersed to all major areas of the Old World, and they would soon journey to the New World as well. But at about the same time, remnant populations of earlier hominins still survived in a few remote and isolated corners. We mentioned in

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a b▶�Figure 13-12 Cro-Magnon 1 (France). In this specimen, modern traits are quite clear. (a) Lateral view. (b) Frontal view.

Key Early Modern Homo sapiens Discoveries from Europe and Asia

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Date Site Hominin Evolutionary Significance

24,500 ya abrigo do Lagar Velho (portugal)

H. sapiens sapiens

child’s skeleton; some suggestion of possible hybrid between Neandertal and modern human—but is controversial

30,000 ya cro-Magnon (France)

H. sapiens sapiens

Most famous early modern human find in world; earliest evidence of modern humans in France

40,000 ya tianyuan cave (china)

H. sapiens sapiens

partial skull and a few postcranial bones; oldest modern human find from china

45,000– 40,000 ya

Niah cave (Borneo, Indonesia)

H. sapiens sapiens

partial skull recently redated more accurately; oldest modern human find from asia

At a Glance

Something New and Different: The “Little People” 379

Chapter 11 that populations of Homo erectus in Java managed to survive on that island long after their cousins had disappeared from other areas (for example, China and East Africa). What’s more, even though they persist- ed well into the Late Pleistocene, these Javanese hominins were still physically similar to other H. erectus individuals.

Even more surprising, it seems that other populations possibly branched off from some of these early inhabit- ants of Indonesia and either intention- ally or accidentally found their way to other, smaller islands to the east. There, under even more extreme iso- lation pressures, they evolved in an astonishing direction. In late 2004, the world awoke to the startling announcement that an extremely small- bodied, small-brained hom- inin had been discovered in Liang Bua Cave on the island of Flores, east of Java (Fig. 13-13). Dubbed the “Little Lady of Flores” or simply “Flo,” the remains consist of an incomplete skel- eton of an adult female (LB1) as well as additional pieces from approximately 13 other individuals, which the press has collectively nicknamed “hobbits.” The female skeleton is remarkable in several ways (Fig. 13-14), though in some aspects similar to the Dmanisi hominins. First, she was barely 3 feet tall—as short as the smallest aus- tralopith—and her brain, estimated at a mere 417 cm³ (Falk et al., 2005), was no larger than that of a chimpan- zee (Brown et al., 2004). Possibly most startling of all, these extraordinary hominins were still living on Flores just 13,000 ya (Morwood et al., 2004, 2005; Wong, 2009)!

Where did they come from? As we said, their predecessors were per- haps H. erectus populations like those found on Java. How they got to Flores— some 400 miles away, partly over open ocean—is a mystery. There are sever- al connecting islands, and to get from one to another these hominins may have drifted across on rafts; but there’s no way to be sure of this. What’s more, these little hominins were apparent- ly living on Flores for a very long time;

recently discovered stone tools have been radiometrically dated to at least 1 mya (Brumm et al., 2010). Such an ancient date, as well as the overall simi- larities to the Dmanisi hominins, sug- gests to some researchers that Homo floresiensis may derive from an early migration of early Homo to Southeast Asia (Jungers et al., 2009; Wong, 2009). In other words, this highly unusu- al hominin might have evolved from ances- tors who left Africa even before H. erectus did.

How did they get to be so physically differ- ent from all other known hominins? Here we’re a lit- tle more certain of the answer. Isolated island populations can quite rapidly diverge from their rel- atives elsewhere. Among such iso- lated animals, natural selection fre- quently favors reduced body size. For example, remains of dwarfed ele- phants have been found on islands in the Mediterranean as well as on some channel islands off the coast of south- ern California. And perhaps most interesting of all, dwarf elephants also

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▲�Figure 13-13 Location of the Flores site in Indonesia.

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▲�Figure 13-14 Cranium of an adult female Homo floresiensis from Flores, Indonesia, dated 18,000 ya.

chapter 13 The Origin and Dispersal of Modern Humans 380

evolved on Flores; they were found in the same geological beds with the little hominins. The evolutionary mechanism (called “insular dwarf- ing”) thought to explain such extreme body size reduction in both the ele- phants and the hominins is an adapta- tion to reduced resources, with natu- ral selection favoring smaller body size (Schauber and Falk, 2008).

Other than short stature, what did the Flores hominins look like? In their cranial shape, thickness of cranial bone, and dentition, they most resemble H. erectus. Still, they have some derived features that also set them apart from all other hominins. For that reason, many researchers have placed them in a separate species, Homo floresiensis.

Immediately following the first pub- lication of the Flores remains, intense controversy arose regarding their inter- pretation (Jacob et al., 2006; Martin et al., 2006). Some researchers have argued that the small-brained hominin (LB1) is actually a pathological modern H. sapiens afflicted with a severe dis- order (microcephaly, and others have been proposed). The researchers who did most of the initial work reject this conclusion and provide some further details to support their original inter- pretation (for example, Dean Falk and colleagues’ further analysis of microce- phalic endocasts; Falk et al., 2009).

The conclusion that among this already small-bodied island population the one individual found with a pre- served cranium happened to be afflicted with a severe (and rare) growth defect is highly unlikely. Yet, it must also be rec- ognized that long-term, extreme isola-

tion of hominins on Flores, leading to a new species showing dramatic dwarf- ing and even more dramatic brain size reduction, is quite unusual.

So where does this leave us? Because a particular interpretation is unlikely, it’s not necessarily incorrect. We do know, for example, that such “insular dwarfing” has occurred in other mam- mals. For the moment, most analyses strongly indicate that this hominin spe- cies (H. floresiensis) did, in fact, evolve on Flores (Nevell et al., 2007; Tocheri et al., 2007; Falk et al., 2008; Schauber and Falk, 2008; Jungers et al., 2009). The more detailed studies of hand and foot anatomy suggest that in several respects the morphology is like that of H. erec- tus (Nevell et al., 2007; Tocheri et al., 2007) or even early Homo (Jungers et al., 2009). The most comprehensive recent analysis reviews all the available data relating to the well-preserved cra- nium of LB1 (Kaifu et al., 2011). In most respects the cranium most resembles early Homo erectus from Java—which, after all, is very close to Flores. In any case, the morphology of the Flores hominins is different in several key respects from that of H. sapiens, includ- ing even those rare individuals who show pathological conditions.

Technology and Art in the Upper Paleolithic

Europe The cultural period known as the Upper Paleolithic began in western

Europe approximately 40,000 ya (Fig. 13-15). Upper Paleolith- ic cultures are usually divided into five different industries based on stone tool technolo- gies: Chatelperronian, Aurigna- cian, Gravettian, Solutrean, and Magdalenian. Major environ- mental shifts were also appar- ent during this period. During the last glacial period, about 30,000 ya, a warming trend last- ing several thousand years par-

40,000 ya 35,000 ya 30,000 ya 25,000 ya 20,000 ya 15,000 ya 10,000 ya

Aurignacian

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▼�Figure 13-15 Cultural periods of the European Upper Paleolithic and their approximate beginning dates.

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Technology and Art in the Upper Paleolithic 381

tially melted the glacial ice. The result was that much of Eurasia was covered by tundra and steppe, a vast area of treeless country dotted with lakes and marshes. In many areas in the north, permafrost prevented the growth of trees but permitted the growth, in the short summers, of flowering plants, mosses, and other kinds of vegetation. This vegetation served as an enormous pasture for herbivorous animals large and small, and carnivorous animals fed off the herbivores. It was a hunter’s paradise, with millions of animals dis- persed across expanses of tundra and grassland from Spain through Europe and into the Russian steppes.

Large herds of reindeer roamed the tundra and steppes, along with mammoths, bison, horses, and a host of smaller animals that served as a bountiful source of food. In addition, humans exploited fish and fowl sys- tematically, apparently for the first time. It was a time of relative abun- dance, and ultimately Upper Paleolithic people spread out over Eurasia, living in caves and open-air camps and build- ing large shelters. We should recall that many of the cultural innovations seen in the Upper Paleolithic had begun with Neandertals (see Chapter 12). Nevertheless, in looking at the entire Upper Paleolithic, there are notable differences. For example, far more elaborate burials are found, most spec- tacularly at the 24,000-year-old Sungir site near Moscow (Fig. 13-16), where grave goods included a bed of red ocher, thousands of ivory beads, long spears made of straightened mam- moth tusks, ivory engravings, and jew- elry (Formicola and Buzhilova, 2004). During this period, either western Europe or perhaps portions of Africa achieved the highest population densi- ty in human history up to that time.

Humans and other animals in most of Eurasia had to cope with shifts in climate conditions, some of them quite rapid. For example, at 20,000 ya, another climatic “pulse” caused the weather to become noticeably colder in Europe and Asia as the continental gla- ciations reached their maximum extent

for this entire glacial period, which is called the Würm in Eurasia.

As a variety of organisms attempted to adapt to these changing conditions, Homo sapiens had a major advantage: the elaboration of increasingly sophis- ticated technology and probably other components of culture as well. In fact, one of the greatest challenges facing numerous Late Pleistocene mam- mals was the ever more dangerously equipped humans—a trend that con- tinues today.

The Upper Paleolithic was an age of innovation that can be compared to the past few hundred years in our recent history of amazing techno- logical change. Anatomically mod- ern humans of the Upper Paleolithic not only invented new and specialized tools (Fig. 13-17) but, as we’ve seen, also experimented with and greatly increased the use of new materials such as bone, ivory, and antler.

Solutrean tools are good examples of Upper Paleolithic skill and likely aesthetic appreciation as well (see Fig. 13-17b). In this lithic (stone) tradition, skill in modifying rock (called “knap- ping”) developed to the finest degree ever known. Using specialized flaking techniques, the artist/technicians made beautiful parallel-flaked lance heads, expertly flaked on both surfaces. The lance points are so delicate that they can be considered works of art that quite possibly never served, nor were intended to serve, a utilitarian purpose.

The last stage of the Upper Paleo- lithic, known as the Magdalenian, saw even more advances in technol- ogy. The spear-thrower, or atlatl, was a hooked rod made of bone or wood that extended the hunter’s arm, enhancing the force and distance of a spear throw (Fig. 13-18). For catching salmon and other fish, the barbed harpoon is a good example of skillful craftsman- ship. There’s also evidence that bows and arrows may have been used for the first time during this period. The intro- duction of much more efficient manu- facturing methods, such as the punch blade technique (Fig. 13-19), provided an abundance of standardized stone

▲�Figure 13-16 Skeletons of two teenagers, a male and a female, from Sungir, Russia. Dated 24,000 ya, this is the richest find of any Upper Paleolithic grave.

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Magdalenian pertaining to the final phase of the Upper paleolithic stone tool industry in europe.

chapter 13 The Origin and Dispersal of Modern Humans 382

blades. These could be fashioned into burins (see Fig. 13-17a) for working wood, bone, and antler; borers for drill- ing holes in skins, bones, and shells; and knives with serrated or notched edges for scraping wooden shafts into a variety of tools.

By producing many more special- ized tools, Upper Paleolithic peoples probably had more resources available to them; moreover, these more effec- tive tools may also have had an impact on the biology of these populations. Emphasizing a biocultural interpreta- tion, C. Loring Brace of the University of Michigan has suggested that with more effective tools as well as the use of fire, allowing for more efficient food processing, modern H. sapiens wouldn’t have required the large teeth and facial skeletons seen in earlier populations.

In addition to their reputation as hunters, western Europeans of the Upper Paleolithic are even better known for their symbolic representa- tion (what we today recognize as art). There’s an extremely wide geographi- cal distribution of symbolic images, best known from many parts of Europe but now also well documented from Siberia, North Africa, South Africa, and Australia. Given a 25,000-year time depth of what we call Paleolithic art, along with its nearly worldwide distribution, we must appreciate that it showed a remarkable range of expression.

Besides cave art, there are many examples of small sculptures exca- vated from sites in western, central, and eastern Europe. Perhaps the most famous of these are the female figu- rines, popularly known as “Venuses,” found at such sites as Brassempouy in France and Grimaldi in Italy. Some of these figures were realistically carved, and the faces appear to be modeled after actual women. Other figurines may seem grotesque, with sexual char- acteristics exaggerated, perhaps to promote fertility or serve some other ritual purpose.

Beyond these quite well-known figu- rines, there are numerous other exam-

ples of what’s frequently called portable art, including elaborate engravings on tools and tool handles (see Fig. 13-18). Such symbolism can be found in many parts of Europe and was already well established early in the Aurignacian, by perhaps as early as 40,000 ya. Recently improved carbon dating used at Geissenklösterle Cave in southwest Germany shows what are thought to be the earliest musical instruments found anywhere (eight flutes made of bone). In addition, sophisticated carved fig- ures were also found, all dating to at least 40,000 ya (Higham et al., 2012). Improved dating methods also show early painted representations in sev- eral caves in Spain. From the famous cave site at Altamira (dating to 35 kya*) as well as at El Castillo (dating to about 41 kya) come the earliest examples of cave painting from anywhere yet discovered. These new, surprisingly early dates derive from advancements in a radiometric technique called uranium-series dating (see Chapter 9). By using tiny samples of accumu- lated calcite deposits that form on top of painted or engraved images, archae- ologists now have much more accurate ideas of when these images were made (Pike et al., 2012). Remember too that the dates are minimum ones: The cal- cite formed after (perhaps long after) the images were completed.

Innovations in symbolic repre- sentations also benefited from and probably further stimulated tech- nological advances. New methods of mixing pigments and applying them were important in rendering painted or drawn images. Engraving and carving on bone and ivory were made easier with the use of special stone tools (see Fig. 13-17). At two sites in the Czech Republic, Dolní Věstonice and Předmostí (both dated at approximately 27,000 to 26,000 ya), small animal figures were fash- ioned from fired clay. This is the first documented use of ceramic technol- ogy anywhere; in fact, it precedes the

*kya = thousand years ago

a b

▲�Figure 13-17 (a) A burin, a very common Upper Paleolithic tool. (b) A Solutrean blade. This is the best- known work of the Solutrean tradition. Solutrean stonework is considered the most highly developed of any Upper Paleolithic industry.

burins Small, chisel-like tools with a pointed end; thought to have been used to engrave bone, antler, ivory, or wood.

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Technology and Art in the Upper Paleolithic 383

later invention of pottery by more than 15,000 years.

But it wasn’t until the final phases of the Upper Paleolithic, particularly dur- ing the Magdalenian, that European prehistoric art reached its climax. Cave art is now known from more than 150 separate sites, the vast majority from southwestern France and north- ern Spain. Apparently in other areas the rendering of such images did not take place in deep caves. People in cen- tral Europe, China, Africa, and else- where certainly may have painted or carved representations on rock faces in the open, but these images long since would have disappeared. So we’re for- tunate that the people of at least one of the many sophisticated cultures of the Upper Paleolithic chose to jour- ney below ground to create their art- work, preserving it not just for their immediate descendants but for us as well. The most spectacular and famous of the cave art sites are Lascaux and Grotte Chauvet in France and Altamira in Spain.

In Lascaux Cave, for example, immense wild bulls dominate what’s

called the Great Hall of Bulls; also horses, deer, and other animals drawn with remarkable skill adorn the walls in black, red, and yellow. Equally impressive, the walls and ceiling of an immense cave at Altamira are filled with superb portrayals of bison in red and black. The artist even took advantage of bulges in the walls to create a sense of relief (that is, three- dimensionality) in the paintings.

Inside the cave called Grotte Chauvet, preserved unseen for thou- sands of years, are a multitude of images including dots, stenciled human handprints, and, most dramati- cally, hundreds of animal representa- tions. Radiocarbon dating has placed the paintings during the Aurignacian,

▲�Figure 13-18 Spear-thrower (atlatl). Note the carving.

(a) A large core is selected and the top portion removed by use of a hammerstone.

(b) The objective is to create a flat surface called a striking platform.

(c) Next, the core is struck by use of a hammer and punch (made of bone or antler) to remove the long narrow flakes (called blades).

(d) Or the blades can be removed by pressure flaking.

(e) The result is the production of highly consistent sharp blades, which can be used, as is, as knives; or they can be further modified (retouched) to make a variety of other tools (such as burins, scrapers, and awls).

Striking platform

b c d

▼�Figure 13-19 The punch blade technique.

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likely more than 35,000 ya, making Grotte Chauvet considerably earlier than the Magdalenian sites of Lascaux and most of the images at Altamira (Balter, 2006). However, as we men- tioned above, Altamira and a couple of other Spanish caves contain some images that are now dated even earlier.

Africa Early accomplishments in rock art, possibly as early as in Europe, are seen in southern Africa (Namibia) at

the Apollo 11 rock shelter site, where painted slabs have been identified as dating to between 28,000 and 26,000 ya (Freundlich et al., 1980; Vogelsang, 1998). At Blombos Cave, farther to the south, remarkable bone tools, beads, and decorated ocher fragments are all dated to 73,000 ya (Henshilwood et al., 2004; Jacobs et al., 2006). The most recent and highly notable dis- covery from South Africa comes from another cave located at Pinnacle Point, not far from Blombos. At Pinnacle Point, ocher has been found (per-

Maybe You Can Take It with You

The practice of deliberately burying the dead is an important and distinctive aspect of later human biocultural evolution. We saw in chapter 12 that Neandertals buried their dead at a number of sites; but we also noted that the assortment of grave goods found in Neandertal burials was pretty sparse.

Something remarkable happened with the appearance and dispersal of modern humans. Suddenly—at least in archaeo- logical terms—graves became much more elaborate. and it wasn’t just that many more items were placed with the deceased; it was also the kinds of objects. Neandertal graves sometimes contain a few stone tools and some unmodified animal bones, such as cave bear. But fully modern humans seem to have had more specialized and far more intensive cultural capacities. For example, from 40,000 ya at twilight cave, in Kenya, researchers have found 600 frag- ments of carefully drilled ostrich eggshell beads (Klein and edgar, 2002). these beads aren’t directly associated with a human burial, but they do show an intensi- fication of craft specialization and possibly a greater interest in personal adornment (although Neandertals in Spain at about the same time were doing similar things, but to a somewhat lesser extent; see chapter 12)

a locale where such elaborate grave goods (including beads) have been found in association with Upper paleolithic modern human burials is the famous cro-Magnon site in southwestern France. Likewise, numerous elaborate grave goods were found with human burials at Grimaldi, in Italy.

No doubt the richest Upper paleolithic burial sites are those at Sungir, in russia. parts of several individuals have been recovered there, dating to about 24,000 ya. Most dramatically, three individuals were found in direct association with thousands of ivory beads and other elaborate grave goods. two of the individuals, a girl about 9 or 10 years of age and a boy about 12 or 13 years of age, were buried together head to head in a spectacular grave (see Fig. 13-16). the more than 10,000 beads excavated here were probably woven into clothing, a task that would have been extraordinarily time-consuming. the two individuals were placed directly on a bed of red ocher, and with them were two mag- nificent spears made of straightened mam- moth tusks—one of them more than 6 feet (240 cm) long! What’s more, there were hundreds of drilled fox canine teeth, pierced antlers, and ivory carvings of animals as well as ivory pins and pendants (Formicola and Buzhilova, 2004).

the production of all of these items, which were so carefully placed with these two young individuals, took thousands of hours of labor. Indeed, one estimate sug-

gests that it took 10,000 hours just to make the beads (Klein and edgar, 2002). What were the Magdalenian people who went to all this trouble thinking? the double burial is certainly the most extrava- gant of any from the Upper paleolithic, but another at Sungir is almost as remarkable. here, the body of an adult male—perhaps about 40 years old when he died—was also found with thousands of beads, and he, too, was carefully laid out on a bed of red ocher.

Sungir is likely a somewhat extraor- dinary exception; still, far more elaborate graves are often found associated with early modern humans than was ever the case in earlier cultures. at Sungir, and to a lesser extent at other sites, it took hundreds or even thousands of hours to produce the varied and intricate objects.

the individuals who were buried with these valuable goods must have been seen as special. Did they have unique talents? Were they leaders or the children of lead- ers? Or did they have some special religious or ritual standing? to be sure, this evidence is the earliest we have from human his- tory revealing highly defined social status. thousands of years later, the graves of the egyptian pharaohs express the same thing—as do the elaborate monuments seen in most contemporary cemeteries. the Magdalenians and other Upper paleolithic cultures were indeed much like us. they, too, may have tried to defy death and “take it with them”!

A Closer Look

Summary of Upper Paleolithic Culture 385

haps used for personal adornment) as well as clear evidence of system- atic exploitation of shellfish and the use of very small stone blades (micro- liths). What is both important and surprising is that the site is dated to approximately 165,000 ya, providing the earliest evidence from anywhere of these behaviors, which are thought by many to be characteristic of mod- ern humans (Marean et al., 2007). The microliths also show evidence that the stone had been carefully heated, mak- ing it easier to modify into such small tools (Brown et al., 2009; Marean, 2010). Other recent finds from Sibu- du, another cave site in South Africa dated to around 70,000 ya, show what archaeologist Lyn Wadley and col- leagues have identified as traces of compound adhesives made from red ocher and plant gum, which were then used to haft stone tools to handles (Wadley et al., 2009). Wadley and col- leagues conclude that such traces of behavior show evidence of what she terms “complex cognition,” since they appear to indicate an understanding of basic chemical reactions.

In central Africa there was also considerable use of bone and ant- ler, some of it possibly quite early. Excavations in the Katanda area of the eastern portion of the Democratic Republic of the Congo (Fig. 13-20) have shown remarkable development of bone craftwork. Dating of the site is quite early, with initial ESR and TL dating results indicating an age of 80,000 ya (Feathers and Migliorini, 2001). Preliminary reports have dem- onstrated that these technological achievements rival those of the more renowned European Upper Paleolithic (Yellen et al., 1995).

Summary of Upper Paleolithic Culture

In looking back at the Upper Paleo-lithic, we can see it as the culmina- tion of 2 million years of cultural devel- opment. Change proceeded incredibly

slowly for most of the Pleistocene; but as cultural traditions and materials accumulated, and the brain—as well as, we assume, intelligence— expanded and reorganized, the rate of change quickened.

Cultural evolution continued with the appearance of early pre- modern humans and moved a bit faster with later premodern humans. Neandertals in Eurasia and their contemporaries elsewhere added deliberate burials, body ornamenta- tion, technological innovations, and much more.

Building on existing cultures, Late Pleistocene populations attained sophisticated cultural and material heights in a seemingly short (by previ- ous standards) burst of exciting activ- ity. In Europe and southern and cen- tral Africa, particularly, there seem to have been dramatic cultural inno- vations, among them big game hunt- ing with new weapons, such as har- poons, spear-throwers, and eventually bows and arrows. Other innovations included needles, “tailored” cloth- ing, hafting of tools, and burials with elaborate grave goods—a practice that may indicate some sort of status hierarchy.

This dynamic age was doomed, or so it seems, by the climate changes of about 10,000 ya. As the temperature slowly rose and the glaciers retreat- ed, animal and plant species were seriously affected, and these chang- es, in turn, affected humans. As tra- ditional prey animals were depleted or disappeared altogether, humans had to seek other means of obtain- ing food.

The grinding of hard seeds or roots became important, and as humans grew more familiar with propagating plants, they began to domesticate both plants and animals. Human depen- dence on domestication became criti- cal, and with it came permanent set- tlements, new technology, and more complex social organization. This continuing story of human biocul- tural evolution will be the topic of the remainder of this text.

chapter 13 The Origin and Dispersal of Modern Humans 386

A F R I C A

ITALYS P A I N

F R A N C E

G E R M A N Y

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B E L G I U M

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▲�Figure 13-20 Symbolic artifacts from the Middle Stone Age of Africa and the Upper Paleolithic in Europe. It is notable that evidence of symbolism is found in Blombos Cave (77,000 ya) and Katanda (80,000 ya), both in Africa, about 45,000 years before any comparable evidence is known from Europe.

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387Critical Thinking Questions

▶▶ Two main hypotheses have been used to explain the origin and dispersal of modern humans:

— The regional continuity model suggests that dif- ferent groups of modern people evolved from local populations of premodern humans.

— Various replacement models, especially those emphasizing partial replacement, suggest that modern humans originated in Africa and migrated to other parts of the world. However, when they came into contact with premodern human groups, they did not completely replace them, but interbred with them to some extent.

▶▶ New DNA evidence from ancient Neandertals as well as from modern people demonstrates that some modest interbreeding did take place, prob- ably between 80,000 and 50,000 ya. These findings clearly support a partial replacement model.

▶▶ Archaeological finds and some fossil evidence (although the latter is not as well established)

also support the view that intermixing occurred between modern H. sapiens and Neandertals.

▶▶ The earliest finds of modern H. sapiens come from East Africa (Ethiopia), with the oldest dat- ing to about 200,000 ya. Another find from Herto is very well dated (160,000 ya) and is the best evi- dence of an early modern human from anywhere at this time.

▶▶ Modern humans are found in South Africa begin- ning around 100,000 ya, and the first anatomical modern H. sapiens are found in the Middle East, dating to perhaps more than 100,000 ya.

▶▶ The Upper Paleolithic is a cultural period showing many innovations in technology, development of more sophisticated (cave) art, and, in many cases, very elaborate burials rich in grave goods. Similar cultural developments occurred in both Eurasia and Africa.

Summary of Main Topics

1. What anatomical characteristics define modern as compared with premodern humans? Assume that you’re analyzing an incomplete skeleton that may be early modern H. sapiens. Which portions of the skeleton would be most informative, and why?

2. What recent evidence supports a partial replace- ment model for an African origin and later disper- sal of modern humans? Do you find this evidence convincing? Why or why not? Can you propose an alternative that has better data to support it?

3. Why are the fossils discovered from Herto so important? How does this evidence influence your conclusions in question 2?

4. What archaeological evidence shows that modern human behavior during the Upper Paleolithic was significantly different from that of earlier homi- nins? Do you think that early modern H. sapi- ens populations were behaviorally superior to the Neandertals? Be careful to define what you mean by superior.

5. Why do you think some Upper Paleolithic people painted in caves? Why don’t we find such evidence of cave painting from a wider geographical area?

Critical Thinking Questions

As with the previous discussions of early hominins, our main basis of information comes from a well- dated and quite complete fossil record (including doz- ens of skeletons) from Africa, Europe, and Asia as well as the first finds from Australia. In addition, new ancient DNA data, especially the sequencing of the full

Neandertal and Denisovan genomes, has shed crucial new light on the age, location, and aspects of gene flow, all relating to the dispersal of modern human popu- lations. Last, abundant archaeological discoveries of tools as well as symbolic representations tell us a great deal about the behavior of early modern human beings.

How Do We Know?

Modern human variation is best understood by examining simi- larities and differences in DNA

among populations.

Connections

Modern humans first evolved in Africa and later spread to other

areas of the world, where they occasionally inter- bred with Neandertals and other pre-modern

humans.

Through natural selec- tion, humans have and

continue to adapt to environmental factors

including solar radiation, cold, altitude, and, most importantly, infectious

disease.

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After mastering the material in this chapter, you should be able to:

▶ �Compare and contrast the traditional view of race with the contemporary one based on genetic information.

▶ �Explain how the concept of “race” developed in Europe and the United States, emphasizing its early limitations and why these views are no longer considered scientifically valid.

▶ �Describe what is meant by the term polymorphism, emphasizing particularly those traits that are determined directly from DNA.

▶ �Explain how population genetics studies provide information regarding modern human diversity as well as telling us about microevolution.

▶ �Discuss, using at least two examples, how a biocultural approach provides useful information about the development of human diversity.

389

At some time or other, you’ve probably been asked to speci-fy your “race” or “ethnicity” on an application or census form. Did that bother you, and if so, why? Usually, you can choose from a few racial/eth- nic categories. Was it easy to pick one? Where would your parents and grand- parents fit in?

Notions about human diversity have played an extremely important role in human relations for at least a few thou- sand years, and they still influence political and social perceptions. While we’d like to believe that informed views have become almost universal, the gruesome tally of genocidal/eth- nic cleansing atrocities in recent years tells us that tragically, worldwide, we have a long way to go before tolerance becomes the norm.

Unfortunately there are probably hundreds (if not thousands) of popu- lar misconceptions regarding human diversity, and to make matters worse, many people seem unwilling to accept what science has to say on the subject. Many misconceptions, especially those regarding how race is defined and cat- egorized, are rooted in cultural history over the last few centuries.

In Chapters 3 and 4, we saw how physical characteristics are influenced by the DNA in our cells. We discussed how people inherit genes from their parents and how variations in those genes (alleles) can produce different expressions of traits. We also focused on how the basic principles of inheritance are related to evolutionary change.

14Modern Human Biology: Patterns of Variation

In this chapter, we’ll continue to deal with topics that directly relate to genetics—namely, biological diversity in humans and how biocultural evo- lution influences the ways in which humans adapt to environmental chal- lenges. After discussing historical attempts to explain human phenotypic variation and racial classification, we’ll examine contemporary methods of interpreting diversity. In recent years, several new techniques have emerged that permit direct examination of the DNA molecule, revealing differences among people even at the level of single nucleotides. But as discoveries of dif- ferent levels of diversity emerge, geneti- cists have also shown that our species is remarkably uniform genetically, par- ticularly when compared with other species.

Student Learning Objectives

chapter 14 Modern Human Biology: Patterns of Variation390

Historical Views of Human Variation

The first step toward understanding diversity in nature is to organize it into categories that can then be named, discussed, and perhaps studied. Histor- ically, when different groups of people came into contact with each other, they tried to account for the physical differ- ences they saw. Because skin color was so noticeable, it was one of the more frequently explained characteristics, and most systems of racial classifica- tion were based on it.

As early as 1350 b.c.e., the ancient Egyptians had classified humans based on their skin color: red for Egyptian, yellow for people to the east, white for those to the north, and black for sub- Saharan Africans (Gossett, 1963). In the sixteenth century, after the dis- covery of the New World, several European countries embarked on a period of intense exploration and col- onization in both the New and Old Worlds. One result of this contact was an increased awareness of human diversity.

Throughout the eighteenth and nineteenth centuries, European and American scientists concentrated on describing and classifying biological variation in humans and also in non- human species. The first scientific attempt to describe the newly discov- ered variation among human popula- tions was Linnaeus’s taxonomic classi- fication (see Chapter 2), which placed humans into four separate categories (Linnaeus, 1758). Linnaeus assigned behavioral and intellectual qualities to each group, with the least complimen- tary descriptions going to sub-Saha- ran Africans. This ranking system was typical of the period and reflect- ed the almost universal European view that Europeans were superior to everyone else.

Johann Friedrich Blumenbach (1752–1840), a German anatomist, classified humans into five races. Although Blumenbach’s categories

came to be described simply as white, yellow, red, black, and brown, he also used criteria other than skin color. What’s more, he emphasized that racial categories based on skin color were arbitrary and that many traits, includ- ing skin color, weren’t discrete phe- nomena. Blumenbach pointed out that classifying all humans using such a system would completely omit every- one who didn’t fall into a specific cat- egory. Blumenbach and others also recognized that traits such as skin color showed overlapping expression between groups.

Most Europeans ignored these com- plexities, so that by the mid-nineteenth century populations were ranked on a scale based primarily on skin color (along with size and shape of the head), again with sub-Saharan Africans at the bottom. The Europeans themselves were also ranked, with northern, light- skinned populations considered superi- or to their southern, somewhat darker- skinned neighbors in Italy and Greece.

To many Europeans, the fact that non-Europeans weren’t Christian sug- gested that they were “uncivilized” and implied an even more basic inferior- ity of character and intellect. This view was rooted in a concept called biologi- cal determinism, which in part holds that there is an association between physical characteristics and such attri- butes as intelligence, morals, values, abilities, and even social and econom- ic condition. In other words, cultural variations were thought to be inherited in the same way that biological varia- tions are. It followed, then, that there are inherent behavioral and cognitive differences between groups and that some groups are by nature superior to others. Unfortunately, many people still hold these views, and following this logic, it’s a simple matter to justify the persecution and even enslavement of other peoples simply because their outward appearance differs from what is familiar.

After 1850, biological determin- ism was a constant theme underlying common thinking as well as scientif-

biological determinism the concept that phenomena, including vari- ous aspects of behavior (e.g., intelligence, values, morals) are governed by biological (genetic) factors; the inaccurate association of various behavioral attributes with certain biological traits, such as skin color.

The Concept of Race 391

ic research in Europe and the United States. Most people—including such notables as Thomas Jefferson, Georges Cuvier, Benjamin Franklin, Charles Lyell, Abraham Lincoln, Charles Darwin, and Supreme Court Justice Oliver Wendell Holmes—held deter- ministic (and what today we’d call rac- ist) views. Commenting on this usu- ally deemphasized characteristic of more respected historical figures, the late evolutionary biologist Stephen J. Gould (1981, p. 32) remarked that “all American culture heroes embraced racial attitudes that would embarrass public-school mythmakers.”

Francis Galton (1822–1911), Charles Darwin’s cousin, shared a growing fear among nineteenth-century Europeans that “civilized society” was being weak- ened by the failure of natural selection to completely eliminate unfit and infe- rior members (Greene, 1981, p. 107). Galton wrote and lectured on the necessity of “race improvement” and suggested government regulation of marriage and family size, an approach he called eugenics. Although eugen- ics had its share of critics, its popular- ity flourished throughout the 1930s. Nowhere was it more attractive than in Germany, where the viewpoint took a horrifying turn. The false idea of pure races was increasingly extolled as a means of reestablishing a strong and prosperous state. Eugenics was seen as scientific justification for purg- ing Germany of its “unfit,” and many of Germany’s scientists continued to support the policies of racial purity and eugenics during the Nazi period (Proctor, 1988, p. 143), when these pol- icies served as justification for con- demning millions of people to death.

But at the same time, many scien- tists were turning away from racial typologies and classification in favor of a more evolutionary approach. No doubt for some, this shift in direction was motivated by their growing con- cerns over the goals of the eugenics movement. Probably more important, however, was the synthesis of genetics and Darwin’s theories of natural selec-

tion during the 1930s. As discussed in Chapter 4, this breakthrough influ- enced all the biological sciences, and some physical anthropologists soon began applying evolutionary principles to the study of human variation.

The Concept of Race

All contemporary humans are mem-bers of the same polytypic spe- cies, Homo sapiens. A polytypic species is composed of local populations that differ in the expression of one or more traits. It’s crucial to emphasize that even within local populations, there’s a great deal of genotypic and phenotypic variation among individuals.

Nevertheless, in discussions of human variation, most people typically have emphasized and grouped togeth- er various characteristics, such as skin color, face shape, nose shape, hair color, hair form (curly or straight), and eye color. Those individuals who have par- ticular combinations of these and other traits have been placed together in cat- egories associated with specific geo- graphical localities. Traditionally, such categories have been called races.

We all think we know what we mean by the word race, but in real- ity the term has had various meanings since the 1500s, when it first appeared in the English language. Race has been used synonymously with species, as in “the human race.” Since the 1600s, race has also referred to various cul- turally defined groups, and this mean- ing is still common. For example, you’ll hear people say, “the English race” or “the Japanese race,” when they actu- ally mean nationality. Another phrase you’ve probably heard is “the Jewish race,” when the speaker is really talking about a particular ethnic and religious identity.

So, even though race is usually a term with biological connotations, it also has enormous social significance. And there’s still a widespread percep- tion that certain physical traits (skin color in particular) are associated with

eugenics the philosophy of “race improvement” through the forced steril- ization of members of some groups and increased reproduction among others; an overly simplified, often racist view that’s now discredited.

polytypic referring to species com- posed of populations that differ in the expression of one or more traits.

392

Racial Purity: A False and Dangerous Ideology

During the late nineteenth and early twentieth centuries, a growing sense of nationalism swept europe and the United States. at the same time, an increased emphasis on racial purity was coupled with the more dangerous aspects of what’s known as biological determinism. the concept of pure races is based in part on the notion that in the past, races were com- posed of people who conformed to idealized types and were similar in appearance and intellect. according to this concept, over time some variation was introduced into these pure races through interbreeding with other groups. Increasingly, this type of “contamination” was seen as a threat to be avoided.

In today’s terminology, pure races would be said to be genetically homogenous, or to possess little genetic variation. therefore everyone would have the same alleles at most of their loci. actually, we do see this situation in “pure breeds” of domesticated animals and plants, developed deliberately by humans through selective breeding. We also see many of the detrimental conse- quences of such genetic uniformity in vari- ous congenital abnormalities, such as hip dysplasia in some breeds of dogs.

With our current understanding of genetic principles, we’re able to appreciate the potentially negative outcomes of mat-

ings between genetically similar individu- als. For example, we know that inbreeding increases the likelihood of offspring who are homozygous for certain deleterious reces- sive alleles. We also know that decreased genetic variation in a species diminishes the potential for natural selection to act, thus compromising that species’ ability to adapt to certain environmental fluctuations. What’s more, in genetically uniform popula- tions, individual fertility can be seriously reduced, potentially with disastrous con- sequences for the entire species. So, even if pure human races did exist at one time (and they didn’t), it would not have been a genetically desirable condition, and these groups most certainly would have been at an evolutionary disadvantage.

In northern europe, particularly Ger- many, and in the United States, racial superiority was increasingly embodied in

the so-called aryan race. Aryan is a term that’s still widely used, albeit erroneously, with biological connotations. actually, Aryan doesn’t refer to a biological population, as most people who use the term intend it. rather, it’s a linguistic term that refers to an ancient language group that was ancestral to the Indo-european family of languages, and it’s the word from which the name Iran is derived.

By the early twentieth century, the “ary- ans” had been transformed into a mythical superrace of people whose noble traits were embodied in an extremely idealized “Nordic type.” the true aryan was held to be tall, blond, blue-eyed, strong, industri- ous, and “pure in spirit.” Nordics were extolled as the developers of all ancient “high” civilizations and as the founders of modern industrialized nations. (It would appear that the ancient cultures of the

numerous cultural attributes (such as occupational preferences or even morality). As a result, in many cultur- al contexts, a person’s social identity is strongly influenced by the way he or she expresses those physical traits traditionally used to define “racial groups.” Characteristics such as skin color are highly visible, and they make it easy to immediately and superficially

place people into socially defined cat- egories. However, so-called racial traits aren’t the only phenotypic expressions that contribute to social identity. Sex and age are also critically important. But aside from these two variables, an individual’s biological and/or ethnic background is still inevitably a factor that influences how he or she is initial- ly perceived and judged by others.

A Closer Look

▼�Figure 1 Victims of genocide in Rwanda

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The Concept of Race 393

References to national origin (for example, African, Asian) as substitutes for racial labels have become more common in recent years, both with- in and outside anthropology. Within anthropology, the term ethnicity was proposed in the early 1950s to avoid the more emotionally charged term race. Strictly speaking, ethnicity refers to cultural factors, but the fact that the

words ethnicity and race are used inter- changeably reflects the social impor- tance of phenotypic expression and demonstrates once again how pheno- type is mistakenly associated with cul- turally defined variables.

In its most common biological usage, the term race refers to geo- graphically patterned phenotypic variation within a species. By the

Indus Valley, china, arabia, Mexico, Zimba- bwe, Greece, and rome were unknown.) In europe, there was growing emphasis on the superiority of northwestern europeans as the modern representatives of “true Nordic stock,” while southern and eastern europe- ans were viewed as inferior.

In the United States, there prevailed the strongly held opinion that america was “originally” settled by christian Nordics. One wonders how Native americans could have been so conveniently forgotten. Before about 1890, most recent newcom- ers to the United States had come from Germany, Scandinavia, Great Britain, and Ireland. But by the 1890s, the pattern of immigration had changed. the arrival of increasing numbers of Italians, turks, Greeks, and eastern european Jews among the thousands of newcomers raised fears that society was being contami- nated by immigration from southern and eastern europe.

also in the United States, there were concerns about the large population of for- mer slaves and their descendants. as afri- can americans left the South to work in the factories of the North, many unskilled white workers felt economically threatened by this competition. It was no coincidence that the Ku Klux Klan, which had been inactive for some years, was revived in 1915 and by the 1920s was preaching vehement opposition to african americans, Jews, and catholics in support of the supremacy of the white, protestant “Nordic race.” these sentiments were widespread in the general popula- tion, although they didn’t always take the extreme form advocated by the Klan. One result of these views was the Immigration

restriction act, passed by congress in 1924, which was aimed at curtail- ing the immigration of non-Nordics, including Italians, Jews, and east- ern europeans, in order to pre- serve “america’s Nordic heritage.”

to avoid the further “decline of the superior race,” many states practiced policies of racial segregation until the mid-1950s. particularly in the South, segregation laws resulted in an almost total separation of whites and blacks except where blacks were employed as servants or laborers. there were also laws against marriage between whites and blacks in over half the states, and unions between whites and asians were frequently illegal. In several states, marriage between whites and blacks was punishable as either a misdemeanor or a felony, and astonish- ingly, some of these laws weren’t repealed until the late 1950s or early 1960s. Like- wise, in Germany, by 1935, the newly insti- tuted Nuremberg Laws forbade marriage or sexual intercourse between so-called aryan Germans and Jews.

the fact that belief in racial purity and superiority led ultimately to the Nazi death camps in World War II is undisputed (except for continuing efforts by certain white supremacist and neo-Nazi organiza- tions). It’s one of the great tragedies of the twentieth century that some of history’s

most glaring examples of discrimination and brutality were perpetrated by people who believed their actions to be based in scientific principles. In reality, there’s abso- lutely no evidence to suggest that “pure” human races ever existed. Indeed, such an idea flies in the face of everything we know about natural selection, recombination, and gene flow. the degree of genetic uni- formity throughout our species (compared with some other species), as evidenced by mounting data from mitochondrial and nuclear DNa analysis, argues strongly that there has always been gene flow between human populations and that genetically homogenous races are nothing more than fabrications.

▲�Figure 2 Emaciated survivors of one of the largest Nazi concentration camps, at Ebensee, Austria, liberated by U.S. Army troops in May 1945.

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chapter 14 Modern Human Biology: Patterns of Variation394

seventeenthcentury,naturalistswere beginningtodescriberacesinplants andnonhumananimals.Theyhad recognizedthatwhenpopulationsof aspeciesoccupieddifferentregions, theysometimesdifferedfromone anotherintheexpressionofoneor moretraits.Buteventoday,thereare noestablishedcriteriaforassessing racesofplantsandanimals,includ- inghumans.Asaresult,biologistsnow almostneverreferto“races”ofother speciesbutmoretypicallytalkabout populationsor,formajorsubdivisions, subspecies.

BeforeWorldWarII,moststudies ofhumanvariationfocusedonvisible phenotypicvariationbetweenlarge, geographicallydefinedpopulations, andthesestudieswerelargelydescrip- tive.Butinthelast60yearsorso,the emphasishasshiftedtoexaminingthe differencesinallelefrequencies(and, morebasically,DNAdifferences)with- inandbetweenpopulations,aswellas consideringtheadaptivesignificance ofphenotypicandgenotypicvaria- tion.Thisshiftinfocusoccurredpart- lybecauseoftheModernSynthesisin biology.Butnow,armedwithgenome datasetsforpopulations,biologists haveanunprecedentedopportunityto studyandexplainhumanvariationand therolethatevolutionaryfactorshave playedinproducingit(Pritchard,2010).

Inthetwenty-firstcentury,the applicationofevolutionaryprinci- plestothestudyofmodernhuman variationhasreplacedthesuperfi- cialnineteenth-centuryviewofrace based solely on observed phenotype. Additionally,thegeneticemphasishas dispelledpreviouslyheldmisconcep- tionsthatracesarefixedbiological entitiesthatdon’tchangeovertimeand arecomposedofindividualswhoall conformtoaparticulartype.

Clearly,therearevisiblephenotyp- icdifferencesbetweenhumans,and someoftheseroughlycorrespondto particulargeographicallocations.But weneedtoaskifthere’sanyadaptive significanceattachedtothesediffer- ences.Isgeneticdriftafactor?Whatis thedegreeofunderlyinggeneticvaria-

tionthatinfluencesphenotypicvaria- tion?Whatinfluencehasculturehad inthepast?Thesequestionsplacecon- siderationsofhumanvariationwithina contemporaryevolutionary,biocultur- alframework.

Although,asadiscipline,physical anthropologyisrootedinattemptsto explainhumandiversity,nocontempo- raryscholarsubscribestopre–Modern Synthesisconceptsofraces(human ornonhuman)asfixedbiologicalenti- ties.Also,anthropologistsrecognize thatsuchoutdatedconceptsofraceare nolongervalid,becausetheamount ofgeneticvariationaccountedforby differencesbetweengroupsisvastly exceededbythevariationthatexists withingroups.Manyphysicalanthro- pologistsalsoarguethatraceisanout- datedcreationofthehumanmindthat attemptstosimplifybiologicalcom- plexitybyorganizingitintocatego- ries.So,humanracesareaproductof thehumantendencytoimposeorder oncomplexnaturalphenomena.In thisview,simplisticclassificationmay havebeenanacceptableapproach100 yearsago,butgiventhecurrentstate ofgeneticandevolutionaryscience,it’s meaningless.

However,eventhoughracialcat- egoriesbasedonoutwardlyexpressed variationsareinvalid,manybiologi- calanthropologistscontinuetostudy differencesinsuchtraitsasskinoreye colorbecausethesecharacteristics, andthegenesthatinfluencethem,can yieldinformationaboutpopulation adaptation,geneticdrift,mutation,and geneflow.Forensicanthropologists,in particular,findthephenotypiccriteria associatedwithrace(especiallyinthe skeleton)tohavepracticalapplications. Lawenforcementagenciesfrequent- lycallonthesescientiststohelpiden- tifyhumanskeletalremains.Because unidentifiedhumanremainsareoften thoseofcrimevictims,identification mustbeasaccurateaspossible.The mostimportantvariablesinsuchiden- tificationaretheindividual’ssex,age, stature,andancestry(“racial”andeth- nicbackground).Usingmetricand nonmetriccriteria,forensicanthropol-

The Concept of Race 395

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ogists employ various techniques for establishing broad population affinity (that is, a likely relationship) for a par- ticular individual, and for most appli- cations their findings are accurate about 80 percent of the time (Owsley et al., 2009).

Another major limitation of tradi- tional classification schemes derives from their inherently typological nature, meaning that categories are distinct and based on stereotypes or ideals that comprise a specific set of traits. So in general, typologies are inherently misleading because any grouping always includes many indi- viduals who don’t conform to all aspects of a particular type. In any

so-called racial group, there are indi- viduals who fall into the normal range of variation for another group based on one or several characteristics. For example, two people of different ances- try might differ in skin color, but they could share any number of other traits, including height, shape of head, hair color, eye color, and ABO blood type. In fact, they could easily share more similarities with each other than they do with many members of their own populations (Fig. 14-1).

To blur this picture further, the characteristics that have traditionally been used to define races are polygenic; that is, they’re influenced by more than one gene and therefore exhibit a

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chapter 14 Modern Human Biology: Patterns of Variation396

continuous range of expression. So it’s difficult, if not impossible, to draw dis- tinct boundaries between populations with regard to many traits. This limi- tation becomes clear if you ask your- self: At what point is hair color no lon- ger dark brown but medium brown, or no longer light brown but dark blond? (Look back at Figure 4-16 for an illustration showing variability in eye color.)

The scientific controversy over race will fade as we enhance our under- standing of the genetic diversity (and uniformity) of our species. Given the rapid changes in genome studies, and because very few genes actually con- tribute to outward expressions of phe- notype, dividing the human species into racial categories isn’t a biologi- cally meaningful way to look at human variation. But among the general pub- lic, variations on the theme of race will undoubtedly continue to be the most common view of human biologi- cal and cultural variation. Keeping all this in mind, it’s up to anthropolo- gists to continue exploring the issue so that, to the best of our abilities, accu- rate information about human varia- tion will be available to anyone who seeks informed explanations of com- plex phenomena.

Contemporary Interpretations of Human Variation

Because the physical characteristics (such as skin color and hair form) that are used to define race are poly- genic, precisely measuring the genetic influence on them hasn’t been possible (although geneticists are getting closer) (Gibbons, 2010). Physical anthropolo- gists and other biologists who study modern human variation have largely abandoned the traditional perspective of describing superficial phenotypic characteristics in favor of examining differences in the frequencies of genes.

Beginning in the 1950s, studies of modern human variation focused on the various components of blood as well as other aspects of body chemis- try. Such traits as the ABO blood types are phenotypes, but they’re also direct products of the genotype. (Recall that protein-coding genes direct cells to make proteins, and the antigens on blood cells and many constituents of blood serum are partly composed of proteins; Fig.14-2.) During the twen- tieth century, this perspective met with a great deal of success, as even- tually dozens of loci were identified and the frequencies of many specif- ic alleles were obtained from numer- ous human populations. Even so, in all these cases, it was the phenotype that was observed, and information about the underlying genotype remained

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Contemporary Interpretations of Human Variation 397

largely unobtainable. But begin- ning in the 1990s, with the advent of genomic studies, new techniques were developed. Now that we can directly sequence DNA, we can actually iden- tify entire genes and even larger DNA segments and make comparisons between individuals and populations. A decade ago, only a small portion of the human genome was accessible to physical anthropologists, but now we have the capacity to obtain DNA pro- files for virtually every human popula- tion on earth. And we can expect that in the next decade, our understanding and knowledge of human biological variation and adaptation will dramati- cally increase.

Human Polymorphisms Traits (or the DNA sequences that code for them) that differ in expression between populations and individuals are called polymorphisms, and they’re the main focus of human variation studies. A genetic trait is polymorphic if the locus that governs it has two or more alleles. (See Chapter 4 for a dis- cussion of the ABO blood group sys- tem, which is governed by three alleles at one locus.) A locus can consist of hundreds of nucleotides or just one nucleotide.

Understanding polymorphisms requires evolutionary explanations, and geneticists use polymorphisms as a principal tool to understand evolu- tionary processes in modern popula- tions. By using these polymorphisms to compare gene frequencies between different populations, we can begin to reconstruct the evolutionary events that link human populations with one another.

The ABO system is interesting from an anthropological perspective because the frequencies of the A, B, and O alleles vary tremendously among humans. In most groups, A and B are rarely found in frequencies greater than 50 percent, and usually their fre- quencies are much lower. Still, most human groups are polymorphic for all three alleles, but there are excep-

tions. For example, in native South American Indians, frequencies of the O allele reach 100 percent. Exceptionally high frequencies of O are also found in northern Australia, and some islands off the Australian coast show frequen- cies exceeding 90 percent. In these populations, the high frequencies of the O allele are probably due to genet- ic drift (founder effect), although the influence of natural selection can’t be entirely ruled out.

Besides ABO, there are many other red blood cell phenotypes, each under the control of a different genetic locus. These include the well-known Rh blood group as well as the less famil- iar Duffy and MN blood groups. Some antigens on white blood cells are also polymorphic. Called human leuko- cyte antigens (HLAs) in humans, these are crucial to the immune response because they allow the body to rec- ognize and resist potentially danger- ous infections. But unlike simple poly- morphisms, such as ABO (one locus with three alleles) or MN (one locus with only two alleles), the HLA sys- tem is governed by perhaps hundreds of alleles at six different loci. Therefore, the HLA system is by far the most polymorphic genetic system known in humans.

Because there are so many HLA alleles, they’re useful in showing pat- terns of human population diversity. For example, Lapps, Sardinians, and Basques differ in HLA allele frequen- cies from other European populations, and these data coincide with allele fre- quency distributions for ABO, MN, and Rh (Fig. 14-3). Founder effect is the most likely explanation for the dis- tinctive genetic patterning in these smaller, traditionally more isolated groups. Likewise, some of the atypical frequencies of HLA alleles characteris- tic of certain populations in Australia and New Guinea probably result from founder effect. Natural selection has also influenced the evolution of HLA alleles in humans, especially as related to infectious disease. For example, cer- tain HLA antigens appear to be asso- ciated with resistance to malaria and

polymorphisms Loci with more than one allele. polymorphisms can be expressed in the phenotype as the result of gene action (as in aBO), or they can exist solely at the DNa level within noncoding regions.

chapter 14 Modern Human Biology: Patterns of Variation398

hepatitis B and perhaps to HIV as well. And finally, one physiological and evo- lutionary influence of HLA concerns male fertility. Data suggest that some HLA antigens are found in higher fre- quencies in infertile males, suggesting that there may be some influence of two or more HLA loci on sperm pro- duction and function (van der Ven et al., 2000).

Another well-studied polymor- phism is the ability to taste an artifi- cial substance called phenylthiocar- bamide (PTC). While many people perceive PTC as extremely bitter, oth- ers don’t taste it at all. The mode of inheritance follows a Mendelian pat- tern, with two alleles (T and t). The ability to taste PTC is a dominant trait, while the inability to taste it is reces- sive. So, “nontasters” are homozygous (tt) for the recessive allele. The fre- quency of PTC tasting varies consid- erably in human populations, and the evolutionary explanation for the pat- terns of variation isn’t clear. But it’s possible that perceiving substances as bitter could be advantageous, espe- cially in children, because poisonous plants are often bitter. Thus height- ened sensitivity to bitter substances increases the likelihood that toxic sub- stances will be avoided.

Polymorphisms at the DNA Level

As a result of the Human Genome Project, we’ve gained remarkable insights into human variation at the DNA level, and molecular biologists have recently discovered many varia- tions in the human genome. For exam- ple, there are thousands of DNA seg- ments called copy number variants (CNVs), where DNA segments are repeated, in some cases just a few times and in other cases hundreds of times. These segments vary tremendous- ly from person to person and, in fact, every person has a unique arrange- ment that defines his or her distinctive “DNA fingerprint.”

Researchers are expanding their approach to map patterns of varia- tion for individual nucleotides. As you know, point mutations have been rec- ognized for some time. But what’s only recently been appreciated is that single-nucleotide changes also fre- quently occur in non–protein-coding portions of DNA. These point muta- tions, together with those in cod- ing regions of DNA, are all referred to as single-nucleotide polymorphisms (SNPs). From years of detailed analyses, about 15 million SNPs have been rec- ognized. These are dispersed through- out the human genome (the majority found in noncoding DNA), and they’re extraordinarily variable (Durbin et al., 2010). SNPs are only one of several recent genetic discoveries and indeed, geneticists have gained access to a vast biological “library” that documents the genetic history of our species.

The field of population genetics is taking advantage of these new dis- coveries. While traditional polymor- phic traits, such as ABO, are still being studied, researchers are directing more and more attention to the remarkably variable DNA polymorphisms. These molecular applications are now being widely used to evaluate human varia- tion at a microevolutionary level, and this information provides far more accurate measures of within- and

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population genetics the study of the frequency of alleles, genotypes, and phenotypes in populations from a micro- evolutionary perspective.

▲�Figure 14-3 People in Sardinia, a large island off the west coast of Italy, differ from other European popula- tions in allele frequencies at some loci.

Contemporary Interpretations of Human Variation 399

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between-group variation than was pre- viously possible. Besides that, we can now use the vast amount of new data to more fully understand very recent events in human population history, including the many roles of natural selection, genetic drift, gene flow, and mutation. As an example of how far the study of human variation has moved toward a molecularly based approach, more than 95 percent of papers deal- ing with population variation present- ed at a recent anthropology confer- ence made use of DNA polymorphisms obtained from populations from all over the world.

The most recent and most com- prehensive population data regarding worldwide patterns of variation come from scans of extremely large portions of DNA, called “whole-genome” analy- sis. Three recent studies have evaluat- ed molecular information for the entire genome in more than 1,000 individu- als. The first two studies each identi- fied and traced the patterning of more

than 500,000 SNPs as expressed in a few dozen populations worldwide (Jakobsson et al., 2008; Li et al., 2008). The most recent study, called the 1000 Genomes Project, is a massive col- laboration of more than 400 scientists worldwide; its preliminary findings reported on close to 15 million SNPs (as well as other DNA variants such and insertions and deletions); indeed, with more detailed sequencing meth- ods and more sophisticated analyses, the researchers concluded they already had discovered the molecular basis for 95 percent of all fairly common pat- terns of human variation (Durbin et al., 2010). They have also identified between 50 and 100 gene variants asso- ciated with disease. Rather than rely- ing on scans of DNA segments (which locate SNPs), this study also made use of the latest sequencing tech- niques of human genomes and could thus quite accurately reconstruct the entire genome for 179 individuals (with an ultimate goal of completing whole

Genetic Polymorphisms Used to Study Human Variation

At a Glance

examples:

red blood cell antigens (aBO, MN, etc.

White blood cell antigens (hLa)

ptc

examples:

Microsatellites (multiple repeats along a chromosomal region)

Alus (single repeats that can jump between chromosomes

Single nucleotide polymorphisms (SNps) (change in single nucleotide within coding or noncoding DNa)

Note: Most of these traits are subject to natural selection.

Note: Most of these characteristics are neutral and therefore not influenced by natural selection.

DNa basedphenotypically ascertained

400

genome sequences for 2,500 people from all around the world). These more complete data, particularly as they are enhanced further, will provide the basis for the next generation of human population genetics studies.

So far, the results of these new stud- ies are highly significant because they confirm earlier findings from more restricted molecular data and they pro- vide new insights. The higher degree of genetic variation seen in African populations as compared with any other geographical group was once again clearly seen. All human pop- ulations outside Africa have much less genetic variation than is seen in Africa. These findings further verify the earlier genetic studies (as well as fossil discoveries) that suggest a fair- ly recent African origin of all modern

humans (as discussed in Chapter 13). Moreover, these new data shed light on the genetic relationships between pop- ulations worldwide and the nature of human migrations out of Africa (see “A Closer Look: What DNA Tells Us about Ancient Human Migrations”). They also provide evidence of the role of genetic drift (founder effect) in recent human evolution as successive- ly smaller populations split off from larger ones. Finally, preliminary results suggest that the patterning of human variation at the global level may help scientists identify genetic risk factors that influence how susceptible differ- ent populations are to various diseases. Specifically, the relative genetic uni- formity in non-African populations (for example, European Americans) as compared with those of more recent

What DNA Tells Us about Ancient Human Migrations

Recent investigations using whole genome sequencing have greatly expanded our knowledge of the origins and migration patterns of modern popula- tions. two recent studies have focused on ancestry in african populations. In the first study (Schuster et al., 2010) two South african individuals had their full genomes sequenced and analyzed, one a San, and the other a descendant of Bantu-speaking ancestors. Interestingly, the South african of Bantu descent is quite a well-known individual, archbishop Desmond tutu (Fig.1). In addition, another three San indi- viduals were evaluated for partial genomes (focusing on protein-coding regions). the most recent investigation (Lachance et al., 2012) expanded the sample to hunter-gatherers from other regions of africa (including two populations from

tanzania in eastern africa and a pygmy group from cameroon in western africa). Whole genome sequences were obtained from five individuals from each group, and the results reinforced earlier work as well as providing a few surprises. First, the variation found in all these african hunter-gatherer populations far exceeds that in other groups in africa or anywhere else in the world. Second, initial evidence suggests some interbreeding with archaic hominins occurred perhaps as early as has been more fully documented in eurasia (i.e., interbreeding with Neandertals and Denisovans around 50,000 ya).

the results emphasize how genetically diverse are african hunter-gatherer popula- tions. In fact, two San individuals are as genetically distinct from each other as, for example, is a european from an asian indi- vidual. the degree of uniqueness (‘private alleles”) found among the San and other hunter-gatherers is much further supported by information from the whole genome sequencing used in this research. Strikingly, the researchers found in their small sample of five South african men 1.3 million novel DNa differences not reported previously in

other populations. this is quite astounding as it expands the range of known genetic variants for Homo sapiens by more than 10% from what has been reported previ- ously for the whole world.

Based on the best current evidence, major migration(s) of modern humans out of africa took place 50,000 to 60,000 ya. One hypothesis proposed two major migra- tion routes. One of these was a “northern” route, up through the Nile Valley in North africa, directly into the Middle east. a sec- ond route suggests a migration from east africa across the mouth of the red Sea, into arabia, then along south asia (notably southern India), and eventually all the way to australia, reaching there as early as 50,000 ya (Kayser, 2010).

this dual out-of-africa migration hypothesis has mostly been based on mtDNa and Y chromosome data. More complete nuclear DNa evidence better supports a single (southern) route deriving from east africa (campbell and tishkoff, 2010), with some descendants traveling north and a larger migration following the southern tier (Majumder, 2010; Stoneking and Deflin, 2010).

A Closer Look

Contemporary Interpretations of Human Variation 401

African descent (for example, African Americans) exposes the former to a greater risk of developing disease (Lohmueller et al., 2008). How such information might be put to use, how- ever, is controversial.

All these genetic data, including the more traditional polymorphisms (such as blood groups) and the vast new DNA-based evidence, point in the same direction: Genetically, humans differ individually within popula- tions far more than large geographical groups (“races”) differ from each other. Does this mean, as eminent geneticist Richard Lewontin concluded 40 years ago, that there’s no biological value in the further study of geographical pop- ulations (Lewontin, 1972)? Even with all our new information, the answer isn’t entirely clear. Some of the recent

genetic evidence from patterns of two different types of CNVs (Rosenberg et al., 2002; Bamshad et al., 2003) has pointed to broad genetic correlations that consistently indicate an individ- ual’s geographical ancestry. We must consider some important points here, however. These geographically pat- terned genetic clusters aren’t “races” as traditionally defined, and so they aren’t closely linked to simple patterns of phenotypic variation (such as skin color). What’s more, the correlations are broad, so not all individuals can be easily classified. In fact, many people would probably be misclassified, even when the best information for dozens of genetic loci is used.

This debate isn’t entirely academic, and it really never has been. Just con- sider the destructive social impact

Once they had dispersed out of africa, human populations fairly quickly spread throughout the Old World. as mentioned in chapter 13, there appear to have been two separate major migrations in asia. One of these occurred earlier (perhaps as

far back as 75,000 years ago) and fol- lowed along South- east asia, through pacific Island chains, and eventually all the way to australia. the

second asian dispersal occurred sometime after

40,000 years ago and led to the first modern human

occupation of east asia; it included the ancestors of han

chinese populations (rasmussen et al., 2011). these ancient travels are

revealed to us through the analysis of DNa patterns in contemporary popula- tions as well as some remarkable dis- coveries from ancient DNa. For example, the population history of Southeast asia/ pacific Island/australia populations was influenced by early interbreeding of mod- ern humans with Denisovans. as we men- tioned in chapter 13, we can still see the traces of this ancient gene flow from the whole genome sequencing of hair from an aboriginal australian who died 100 years ago!

european modern human popula- tion history can be traced back to about 45,000 ya, and further genetic data sug- gest at least four subsequent significant migration episodes, culminating in histori- cal times, about 5,000 years ago (Soares et al., 2010). the origins of New World populations posed perhaps the biggest enigma regarding the worldwide history of major population expansions. Unques- tionably, all the genetic data confirm that Native americans have asian origins. however, the most comprehensive recent data based on comparative analysis of more than 350,000 SNps from both the americas and Siberia suggest there were at least three separate migrations from asia (reich et al., 2012). the earliest of these, called the “First americans,” left traces throughout the New World, while the latter two migrations included, respectively, ancestors of both aleut and Inuit populations and members of the Na-Dene–speaking language group found in canada (and perhaps the United States, although no DNa samples were made available by any Native american groups other than in alaska).

Trin ity

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y ▲�Figure 1 Archbishop Desmond Tutu, who recently had his entire genome sequenced. This information was com- pared with that of other South African indi- viduals of different ancestries.

chapter 14 Modern Human Biology: Patterns of Variation402

that the misuse of the race concept has caused over the last few centu- ries. A contemporary continuation of the debate concerns the relationship of ancestry and disease. It’s long been recognized that some disease- causing genes are more common in certain populations than in others (such as the allele that causes sickle-cell ane- mia). The much more complete data on human DNA patterns have further expanded our knowledge, showing, for example, that some people are more resistant than others to HIV infection (see Chapter 15 for further discussion). Does this mean that a person’s ances- try provides valuable medical informa- tion in screening or even treating cer- tain diseases?

Some experts argue that such infor- mation is medically helpful (e.g., Rosenberg et al., 2002; Bamshad and Olson, 2003; Burchard et al., 2003). What’s more, official federal guidelines recently issued by the U.S. Food and Drug Administration recommend the collection of ancestry data (“race/eth- nic identity”) in all clinical trials test- ing new drugs. Other researchers dis- agree and argue that such information is at best tenuous (King and Motulsky, 2002) or that it has no obvious medical use (e.g., Cooper et al., 2003). A major difficulty fueling this controversy has been poor communication between biomedical researchers and anthro- pologists and other evolutionary biol- ogists. To allow for a more balanced and useful approach, anthropologist Clarence Gravlee has argued for adop- tion of a “more complex biocultural view of human biology” (2009, p. 54).

Even the general public has weighed in on this issue, defeating a 2003 California ballot measure that would have restricted the collection of “racial” (ethnic) information on medi- cal records. There are no easy answers to the questions we’ve raised, and this is an even stronger argument for an informed public. The subject of race has been contentious, and anthropol- ogy and other disciplines have strug- gled to come to grips with it. Our new genetic tools have allowed us to expand

our knowledge at a rate far beyond any- thing seen previously. But increased information alone doesn’t permit us to fully address all human concerns. How we address diversity, both individu- ally and collectively, must balance the potential scientific benefits against a history of social costs.

Population Genetics

As we defined it in Chapter 4, a pop-ulation is a group of interbreed- ing individuals. More precisely, a pop- ulation is the group within which an individual is most likely to find a mate. As such, a population is marked by a degree of genetic relatedness and shares a common gene pool.

In theory, this is a straightforward concept. In every generation, the genes (alleles) are mixed by recombination and rejoined through mating. What emerges in the next generation is a direct product of the genes going into the pool, which in turn is a product of who is mating with whom.

In practice, however, describing human populations is difficult. The largest human population that can be described is our entire species. All members of a species are potentially capable of interbreeding but are inca- pable of producing fertile offspring with members of other species. Our species, like any other, is thus a geneti- cally closed system. The problem arises not in describing who can potentially mate with whom but in determining the exact pattern of those individuals who are doing so.

Factors that determine mate choice are geographical, ecological, and social. If individuals are isolated on a remote island in the middle of the Pacific Ocean, there isn’t much chance that they’ll find mates outside the immedi- ate vicinity. Such breeding isolates are fairly easily defined and are a favor- ite focus of microevolutionary stud- ies. Geography plays a dominant role in producing these isolates by severely limiting the range of available mates. But even within these limits, cultur-

gene pool the total complement of genes shared by the reproductive members of a population.

breeding isolates populations that are clearly isolated geographically and/or socially from other breeding groups.

Population Genetics 403

al rules can easily play a deciding role by stipulating who is most appropri- ate among those who are potentially available.

Human population segments are defined as groups with relative degrees of endogamy (marrying/mating with- in the group). But these aren’t totally closed systems. Gene flow often occurs between groups, and individuals may choose mates from distant locations. With the advent of modern transpor- tation, the rate of exogamy (marrying/ mating outside the group) has dramati- cally increased.

Today, most humans aren’t clear- ly defined as members of particular populations because they don’t belong to a breeding isolate. Inhabitants of large cities may appear to be members of a single population; but within the city, there’s a complex system of social, ethnic, and religious boundaries that are crosscut to form smaller popula- tion segments. Besides being members of these highly open local population groupings, we’re simultaneously mem- bers of overlapping gradations of larg- er populations—the immediate geo- graphical region (a metropolitan area or perhaps an entire state), a section of the country, the entire nation, and ulti- mately the whole species.

After identifying specific human populations, the next step is to find out what evolutionary forces, if any, are operating on them. To determine whether evolution is taking place at a given genetic locus, we measure allele frequencies for specific traits. We then compare these observed frequencies with those predicted by a mathemati- cal model called the Hardy-Weinberg theory of genetic equilibrium. This model gives us a baseline set of evo- lutionary expectations under known conditions.

The Hardy-Weinberg theory estab- lishes a set of conditions in a hypo- thetical population where no evolution occurs. In other words, no evolution- ary forces are acting and all genes have an equal chance of recombining in each generation (that is, there’s random mating of individuals). More precise-

ly, the conditions that such a popula- tion would be assumed to meet are as follows:

1. The population is infinitely large; this eliminates the possibility of random genetic drift—that is, changes in allele frequencies due to chance.

2. There’s no mutation; thus, no new alleles are being added by changes in genes.

3. There’s no gene flow; thus there’s no exchange of genes with other populations that could alter allele frequencies.

4. Natural selection isn’t operating; thus specific alleles offer no advan- tage over others that might influ- ence reproductive success.

5. Mating is random; therefore, there’s nothing to influence who mates with whom; all females are assumed to have an equal chance of mating with any male, and vice versa.

If all these conditions are met, allele frequencies won’t change from one generation to the next (that is, no evo- lution will take place), and as long as these conditions prevail, the popula- tion maintains a permanent equilibri- um. This equilibrium model provides population geneticists with a standard against which they can compare actu- al circumstances. Notice that the con- ditions defining the Hardy-Weinberg equilibrium constitute an idealized, hypothetical state. In the real world, no actual population would fully meet any of these conditions. But don’t be con- fused by this distinction. By explicit- ly defining the allele frequencies that would be expected if no evolutionary change were occurring (that is, in equi- librium), we establish a baseline with which to compare the allele frequen- cies we actually observe in real human populations.

If the observed frequencies dif- fer from those of the expected model, we can then say that evolution is tak- ing place at the locus in question. The alternative, of course, is that the

endogamy Mating with individuals from the same group.

exogamy Mating pattern whereby individuals obtain mates from groups other than their own.

Hardy-Weinberg theory of genetic equilibrium the math- ematical relationship expressing—under conditions in which no evolution is occur- ring—the predicted distribution of alleles in populations; the central theorem of popula- tion genetics.

chapter 14 Modern Human Biology: Patterns of Variation404

observed and expected frequencies don’t differ enough that we can confi- dently say that evolution is occurring at a particular locus in a population. In fact, this is often what happens; in such cases, population geneticists aren’t able to clearly define evolutionary change at the particular locus under study.

The simplest way to do a microevo- lutionary study is to observe a genetic trait that follows a simple Mendelian pattern and has only two alleles (A and a). Remember that there are only three possible genotypes: AA, Aa, and aa. Proportions of these genotypes (AA:Aa:aa) are a function of the allele frequencies themselves (percentage of A and percentage of a). To provide uni- formity for all genetic loci, a standard notation is employed to refer to these frequencies:

Frequency of dominant allele (A) = p

Frequency of recessive allele (a) = q

Since in this case there are only two alleles, their combined total frequency must represent all possibilities. In other words, the sum of their separate fre- quencies must be 1:

p + q (Frequency of (Frequency of = A alleles) a alleles)

1 (100% of alleles at the locus in question)

To determine the expected pro- portions of genotypes, we compute the chances of the alleles combining with one another in all possible com- binations. Remember, they all have an equal chance of combining and no new alleles are being added. These proba- bilities are a direct function of the fre- quency of the two alleles. The chances of all possible combinations occurring randomly can be simply shown as

p + q × p + q

pq + q² p² + pq

p² + 2pq + q²

Mathematically, this is known as a binomial expansion and can also be shown as:

(p + q)(p + q) = p² + 2pq + q²

What we have just calculated is simply:

Expected Allele Genotype Proportion in Combination Produced Population

Chances of AA p × p = p² A combining with A

Chances of Aa p × q = A combining with a; 2pq

a combining aA p × q = with A

Chances of aa q × q = q² a combining with a

Thus, p² is the frequency of the AA genotype, 2pq is the frequency of the Aa genotype, and q² is the frequency of the aa genotype, where p is the fre- quency of the dominant allele and q is the frequency of the recessive allele in a population.

Calculating Allele Frequencies We can best demonstrate how geneti- cists use the Hardy-Weinberg formu- la by giving an example. Let’s assume that a population contains 200 indi- viduals, and we’ll use the MN blood group locus as the gene to be mea- sured. The two alleles of the MN locus produce two antigens (M and N) that are similar to the ABO anti- gens and are also located on red blood cells. Because the M and N alleles are codominant, we can ascertain every- one’s phenotype by taking blood sam- ples and testing them in a process very similar to that for ABO (see Fig. 14-2). From the phenotypes, we can then directly calculate the observed allele frequencies. So let’s see what we can determine.

All 200 individuals are tested, and the observed data for the three pheno- types are as follows:

Population Genetics 405

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Number of Alleles

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MM 80 40 160 0

MN 80 40 80 80

NN 40 20 0 80

Totals 200 100 240 + 160 = 400

Proportion 0.6 + 0.4 = 1

From these observed results, we can count the number of M and N alleles

and thus calculate the observed allele frequencies:

p = frequency of M = 0.6 q = frequency of N = 0.4

The total frequency of the two alleles combined should always equal 1. As you can see, they do.

Next, we need to calculate the expected genotypic proportions. This calculation comes directly from the Hardy-Weinberg equilibrium formula: p² + 2 pq + q² = 1.

p² = (.6) (.6) = .36

2 pq = 2(.6) (.4) = 2(.24) = .48

q² = (.4)(.4) = .16

Total 1.00

*Each individual has two alleles, so a person who’s MM contributes two M alleles to the total gene pool, a person who’s MN contributes one M and one N, and a person who’s NN contributes two N alleles. For the MN locus, then, 200 individuals contribute 400 alleles.

Population Genetics Research

At a Glance

Selection of population (frequently an isolate)

collection of samples (blood samples or swabs from inside mouth)

calculation of allele frequencies in population

Determination of evolutionary status using hardy-Weinberg equilibrium formula

analysis of specific gene patterns; loci and alleles determined from expressed phenotype (as in aBO) or directly at DNa level (as in microsatellites)

Null hypothesis; population in equilibrium at loci tested;

no evolution

population not in equilibrium; population is

evolving

evolutionary process explained by natural selection, genetic, drift,

gene flow, and/or mutation

406

There are only three possible geno- types: MM, MN, and NN. The total of the relative proportions should equal 1. Again, as you can see, they do.

Finally, we need to compare the two sets of data—that is, the observed fre- quencies (what we actually found in the population) with the expected fre- quencies (those predicted by Hardy- Weinberg under conditions of genetic equilibrium). How do these two sets of data compare?

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MM .36 72 .40 80

MN .48 96 .40 80

NN .16 32 .20 40

We can see that although the match between observed and expected fre- quencies isn’t perfect, it’s close enough statistically to satisfy equilibrium con- ditions. Since our population isn’t a large one, sampling may easily account for the small degree of observed dif- ferences. Our population is therefore probably in equilibrium (that is, it’s not evolving at this locus).

Of course, the observed allele fre- quencies do sometimes vary enough from equilibrium predictions to sug- gest that the population isn’t in equilib- rium—that is, it’s evolving. For exam- ple, consider the locus influencing PTC tasting. What makes PTC tasting such a useful characteristic is how easy it is to identify. Unlike blood antigens such as ABO or MN, PTC tasting can be tested by simply having subjects place a thin paper strip on their tongues. This paper contains concentrated PTC, and people either taste it or they don’t.

Calculating Allele Frequencies: PTC Tasting in a Hypothetical Population

For the ptc tasting trait, it’s assumed that there are two alleles, T and t. also, while dominance is displayed, it’s incomplete. So it’s theoretically possible to ascertain the phenotypes of heterozy- gotes. to simplify calculations for this example, we assume that all heterozygotes can be ascertained.

In our population of 500 individuals, we find the following observed phenotypic frequencies: Number Number of of Alleles Genotype Individuals Percent T t

TT 125 25 250 0 Tt 325 65 325 325 tt 50 10 0 100 totals 500 100 575 425

thus, the observed allele frequencies are

T(p) = .575 t(q) = .425

the expected genotypic proportions are

p² = (.575)(.575) = .33

2 pq = 2(.575)(.425) = .49

q² = (.425)(.425) = .18

Now we compare the observed and expected genotypic frequencies: Actual Number of Expected Individuals Expected Number of Observed with Each Frequency Individuals Frequency Genotype

TT .33 165 .25 125 Tt .49 245 .65 325 tt .18 90 .10 50

these results show considerable departures of the observed genotypic proportions from those predicted under equilibrium con- ditions. Both types of homozygotes (TT and tt ) are less commonly observed than expected, while the heterozygote (Tt ) is more com- mon than expected. a statistical test (called a chi-square) can be performed to test the statistical significance of this difference. the results of this test are shown in appendix c on the anthropology courseMate at cengagebrain.com.

A Closer Look

Evolution in Action: Modern Human Populations 407

So testing is quick, inexpensive, and doesn’t involve a blood test. With such an efficient means of screening sub- jects, we now consider a sample popu- lation of 500 individuals. The results from observing the phenotypes and calculations of expected genotypic pro- portions are shown in “A Closer Look: Calculating Allele Frequencies: PTC Tasting in a Hypothetical Population.” You’ll find additional examples of population genetics calculations in Appendix D, which is available on the Anthropology CourseMate at Cengagebrain.com.

Evolution in Action: Modern Human Populations

Once a population has been defined, it’s possible to determine wheth- er allele frequencies are stable (that is, in genetic equilibrium) or changing. As we’ve seen, the Hardy-Weinberg formula provides the tool to establish whether allele frequencies are indeed changing. But what factors cause changes in allele frequencies? There are a number of factors, including:

1. Production of new variation (that is, mutation)

2. Redistribution of variation through gene flow or genetic drift

3. Selection of “advantageous” allele combinations that promote repro- ductive success (that is, natural selection)

Notice that factors 1 and 2 consti- tute the first stage of the evolution- ary process, as first emphasized by the Modern Synthesis, while factor 3 is the second stage (see Chapter 4). There’s also another factor, as implied by the condition of genetic equilib- rium that under idealized condi- tions all matings are random. Thus, an evolutionary alteration (that is, deviation from equilibrium) is called nonrandom mating.

Nonrandom Mating Although sexual recombination doesn’t itself alter allele frequencies, any consis- tent bias in mating patterns can change the genotypic proportions. By affecting genotype frequencies, nonrandom mat- ing causes deviations from Hardy-Wein- berg expectations of the proportions p², 2pq, and q². It therefore sets the stage for the action of other evolutionary factors, particularly natural selection.

A form of nonrandom mating, called assortative mating, occurs when individuals of either similar pheno- types (positive assortative mating) or dissimilar phenotypes (negative assortative mating) mate more often than expected by Hardy-Weinberg predictions. However, in the vast majority of human populations, neither factor appears to have much influence.

Inbreeding is a second type of non- random mating, and it can have impor- tant medical and evolutionary con- sequences. Inbreeding occurs when relatives mate more often than expect- ed. Such matings will increase homo- zygosity, since relatives who share close ancestors will probably also share more alleles than two unrelated people would. When relatives mate, their offspring have an increased probability of inher- iting two copies of potentially harmful recessive alleles from a relative (perhaps a grandparent) they share in common. Many potentially deleterious genes that are normally “masked” in heterozygous carriers may be expressed in homozy- gous offspring of inbred matings and therefore “exposed” to the action of nat- ural selection. Among offspring of first- cousin matings in the United States, the risk of congenital disorders is 2.3 times greater than it is for the overall popula- tion. Matings between especially close relatives (incest) often lead to multiple genetic defects.

All societies have incest taboos that ban matings between close relatives, such as between parent and child or brother and sister. Thus these mat- ings usually occur less frequently than predicted under random mating con- ditions. Whether biological factors

nonrandom mating pattern of mating in which individuals choose mates preferentially, with mate choice based on criteria such as social status, ethnicity, or biological relationship. In nonrandom mat- ing, an individual doesn’t have an equal chance of mating with all other individuals in the group.

inbreeding a type of nonrandom mat- ing in which relatives mate more often than predicted under random mating conditions.

chapter 14 Modern Human Biology: Patterns of Variation408

also interact to inhibit such behavior has long been a topic of debate among anthropologists. For many social, eco- nomic, and ecological reasons, exog- amy is an advantageous strategy for hunting and gathering bands. Selective pressures may also play a part, since highly inbred offspring have a great- er chance of expressing a recessive genetic disorder and thereby lower- ing their reproductive fitness. What’s more, inbreeding reduces genetic vari- ability among offspring, potentially reducing reproductive success (Murray, 1980). In this regard, it’s interesting to note that incest avoidance is wide-

spread among vertebrates. Detailed studies of free- ranging chimpanzees indi- cate that they usually avoid incestuous matings with- in their family groups, although exceptions do occur (Constable et al., 2001). In fact, in most pri- mate species, adults of one sex consistently find mates from groups other than the one in which they were reared (see Chapter 7). As we’ve seen, recognition of close kin apparently is an ability displayed by sever- al (perhaps all) primates.

Primatologists are currently investi- gating this aspect of our primate cous- ins. Apparently both biological factors (in common with other primates) and uniquely human cultural factors have interacted during hominin evolution to produce this universal behavioral pat- tern among contemporary societies.

Human Biocultural Evolution

We’ve defined culture as the human strategy of adaptation. Human beings live in cultural environments that are continually modified by human activity; thus evolutionary process- es are understandable only within this cultural context. We’ve discussed at

length how natural selection operates within specific environmental settings. For humans and many of our hominin ancestors, this means an environment dominated by culture. For example, the sickle-cell allele hasn’t always been an important genetic factor in human populations. Before the development of agriculture, humans rarely, if ever, lived close to mosquito-breeding areas. With the spread in Africa of slash-and-burn agriculture, perhaps in just the last 2,000 years, penetration and clearing of tropical rain forests occurred. This deforestation created open, stagnant pools that provided prime mosquito- breeding areas in close proximity to human settlements. DNA analyses have further confirmed such a recent ori- gin and spread of the sickle-cell allele in West Africa. A recent study of a popu- lation from Senegal has estimated the origin of the HbS mutation in this group at between 2,100 and 1,250 ya (Currat et al., 2002).

So quite recently, and for the first time, malaria struck human popula- tions with its full impact; and it became a powerful selective force. No doubt, humans attempted to adjust culturally to these circumstances, and many bio- logical adaptations also probably came into play. The sickle-cell trait is one of these biological adaptations. But there’s a definite cost involved with such an adaptation. Carriers have increased resistance to malaria and presumably higher reproductive success, though some of their offspring may be lost to the genetic disease sickle-cell anemia. So there’s a counterbalancing of selec- tive forces with an advantage for car- riers only in malarial environments. (The genetic patterns of recessive traits such as sickle-cell anemia are dis- cussed in Chapter 4.)

Following World War II, extensive DDT spraying by the World Health Organization began systematic control of mosquito-breeding areas in the trop- ics. Forty years of DDT spraying killed millions of mosquitoes; but at the same time, natural selection acted to produce several strains of DDT-resistant mos- quitoes (Fig. 14-4). Accordingly, espe-

incest avoidance In animals, the tendency not to mate with close relatives. this tendency may be due to various social and ecological factors that keep the indi- viduals apart. there may also be innate fac- tors that lead to incest avoidance, but these aren’t well understood.

slash-and-burn agriculture a traditional land-clearing practice involv- ing the cutting and burning of trees and vegetation. In many areas, fields are aban- doned after a few years and clearing occurs elsewhere.

Agricultural practices

Spread of sickle-cell mutation

Human malaria

Mosquitoes spread

Adaptation: DDT-resistant strains

DDT spraying

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▲�Figure 14-4 Evolutionary interactions affecting the frequency of the sickle-cell allele.

Human Biocultural Evolution 409

cially in the tropics, malaria is again on the rise, with up to 500 million new cases reported annually and more than 1 million people dying each year.

A genetic characteristic (such as sickle-cell trait) that provides a repro- ductive advantage to heterozygotes in certain environments is a clear exam- ple of natural selection in action among human populations. The precise evo- lutionary mechanism in the sickle-cell example is called a balanced poly- morphism. A polymorphism, as we’ve defined it, is a trait with more than one allele at a locus in a population. But when a harmful allele (such as the sickle- cell allele) has a higher frequency than can be accounted for by mutation alone, a more detailed evolutionary explana- tion is required. In this case, the addi- tional mechanism is natural selection.

This brings us to the second part of the term. By balanced we mean the interaction of selective pressures oper- ating on specific alleles in a particu- lar environment (in this case, the sick- le-cell alleles in malarial areas). Some individuals (mainly homozygous nor- mals) will die of the infectious disease malaria. Others (homozygous reces- sives) will die of the inherited disease sickle-cell anemia. Thus, the individu- als with the highest reproductive suc- cess are the heterozygotes who have sickle-cell trait. These heterozygotes pass both the normal allele (HbA) and the sickle-cell allele (HbS) to offspring, thus maintaining both alleles at fairly high frequencies. Since one allele in this population won’t significantly increase in frequency over the other allele, this situation will become “balanced” and will persist as long as malaria continues to be a selective factor.

Lactose intolerance, which involves an individual’s ability to digest milk, is another example of human biocultur- al evolution. In all human populations, infants and young children are able to digest milk, an obvious necessity for any young mammal. One ingredient of milk is lactose, a sugar that’s broken down by the enzyme lactase. In most mammals, including many humans, the gene that codes for lactase production “switches

off” in adolescence. Once this happens, if a person drinks fresh milk, the lactose ferments in the large intestine, leading to diar- rhea and severe gastrointestinal upset. So, as you might expect, adults stop drinking fresh milk. Among many African and Asian populations (a majority of humankind today), most adults are lactose-intolerant (Table 14.1). But in other populations, including some Africans and Europeans, adults continue to produce lactase and are able to digest fresh milk. This continued production of lactase is called lactase persistence.

Evidence has suggested a simple dominant mode of inher- itance for lactase persistence in adults. The environment also plays a role in expression of the trait—that is, whether a per- son will be lactose-intolerant— since intestinal bacteria can somewhat buffer the adverse effects of drinking fresh milk. Because these bac- teria increase with previous exposure, some tolerance can be acquired, even in individuals who genetically are not lactase-persistent.

Throughout most of hominin evolu- tion, milk was unavailable after wean- ing; therefore, there may be a selective advantage to switching off the gene that codes for lactase production. So why can some adults (the majority in some populations) tolerate milk? The distribution of lactose-tolerant popu- lations may provide an answer to this question, and it suggests a powerful cultural influence on this trait.

Europeans, who are generally lactose-tolerant, are partly descended from Middle Eastern populations. Often economically dependent on pas- toralism, these groups raised cows and/or goats and probably drank con- siderable quantities of milk. In such a cultural environment, strong selec- tion pressures apparently favored lac- tose tolerance, a trait that has been retained in modern Europeans. Genetic evidence from north-central Europe

balanced polymorphism the maintenance of two or more alleles in a population due to the selective advantage of the heterozygote.

lactase persistence In adults, the continued production of lactase, the enzyme that breaks down lactose (milk sugar). this allows adults in some human populations to digest fresh milk products. the discontinued production of lactase in adults leads to lactose intolerance and the inability to digest fresh milk.

Table 14.1 Frequencies of Lactase Persistence

Population Group Percent

U.S. whites 81–98

Swedes and Danes >90

Swiss 88

U.S. blacks 23–30

Ibos 1

Bantu 10

Fulani 50

Chinese 1

Thais 1

Asian Americans <5

Native Americans 85

Source: Lerner and Libby, 1976, Tishkoff et al., 2007.

chapter 14 Modern Human Biology: Patterns of Variation410

supports this interpretation. DNA analysis of both cattle and humans sug- gests that these species have, to some extent, influenced each other geneti- cally. The interaction between humans and cattle resulted in cattle that pro- duce high-quality milk and humans with the ability to digest it (Beja-Pereira et al., 2003). In other words, more than 5,000 ya, populations of north- central Europe were selectively breeding cat- tle for higher milk yields. And as these populations were increasing their dependence on fresh milk, they were inadvertently selecting for the gene that produces lactase persistence.

But perhaps even more informative is the distribution of lactose tolerance in Africa, where the majority of people are lactose-intolerant. Groups such as the Fulani and Tutsi have been pasto-

ralists for perhaps thousands of years and have much higher rates of lactase persistence than nonpastoralists (Fig. 14-5). Presumably, like their European counterparts, they’ve retained the abil- ity to produce lactase because of their continued consumption of fresh milk (Powell and Tishkoff, 2003).

Recent molecular evidence has supported this hypothesis, show- ing a similar coevolution of humans and cattle in East Africa (Tishkoff et al., 2007). The pattern of DNA muta- tions (SNPs) in Africa is different from that seen in Europe, strongly suggest- ing that lactase persistence has evolved independently in the two regions. In fact, the data show that lactase persis- tence has evolved several times just in East Africa. The importance of cattle domestication in providing milk for human groups was clearly a cultural and dietary shift of major importance. As humans selectively bred cattle to produce more and higher-quality milk, they promoted fairly rapid evolution in these animals. At the same time, humans in different areas coevolved through natural selection as allele fre- quencies shifted to produce higher fre- quencies of lactase persistence.

As we’ve seen, the geographical dis- tribution of lactase persistence is relat- ed to a history of cultural dependence on fresh milk products. There are, however, some populations that rely on dairying but don’t have high rates of lactase persistence (Fig. 14-6). It’s been suggested that such groups have tra- ditionally consumed their milk in the form of cheese and yogurt, in which the lactose has been broken down by bacterial action.

The interaction of human cultur- al environments and changes in lac- tose tolerance in human populations is another example of biocultural evo- lution. In the last few thousand years, cultural factors have initiated spe- cific evolutionary changes in human groups. Such cultural factors have probably influenced the course of human evolution for at least 3 million years, and today they are of paramount importance.

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▲�Figure 14-5 Fulani cattle herder with his cattle.

▼�Figure 14-6 Natives of Mongolia rely heavily on milk products from goats and sheep but consume these foods mostly in the form of cheese and yogurt.

411Media Resources

▶ Physically visible traits, traditionally used in attempts to classify humans into clearly defined groups (“races”), have emphasized such features as skin color, hair color, hair form, head shape, and nose shape.

▶ However, all of these physical characteristics are not only influenced by several genetic loci but are also modified by the environment. As a result, these traditional markers of race aren’t reliable indicators of genetic relationships, and they’re not biologically useful in depicting patterns of human diversity.

▶ Since the middle of the twentieth century, more precise techniques have allowed a far better under- standing of actual patterns of human variation, beginning with information obtained from the phenotypic expression of Mendelian traits such as blood groups. Population genetics analyses of sev- eral of these genetic polymorphisms proved useful in showing broad patterns, such as the high degree

of within-population variation and the relatively minor amount of between-population variation.

▶ Since the 1990s, the development and rapid appli- cation of comparative genomics have drastically expanded genetic data. These powerful new tools allow evaluation of human population variation using thousands (or hundreds of thousands) of precisely defined DNA sequences. Such population studies are aimed at reconstructing the microevo- lutionary population history of our species and understanding the varied roles of natural selection, genetic drift, gene flow, and mutation.

▶ For humans, of course, culture also plays a cru- cial evolutionary role. Interacting with biological influences, these factors define the distinctive bio- cultural nature of human evolution. Two excellent examples of recent human biocultural evolution relate to resistance to malaria (involving the sickle- cell allele) and lactase persistence.

Summary of Main Topics

1. Imagine you’re with a group of friends discuss- ing human diversity and the number of races. One friend says there are three clearly defined races, a second says five, while the third isn’t sure. Would you agree with any of them? Why or why not?

2. For the same group of friends mentioned in ques- tion 1 (none of whom have had a course in biologi- cal anthropology), how would you explain how scientific knowledge fits (or doesn’t fit) with their preconceived notions about human races?

3. Explain how the concept of race has developed in the Western world. What are the limitations of this approach? How have current genetic studies changed this view?

4. Explain how modern genetic studies can contrib- ute to our understanding of biological variation in humans. Be as specific as possible.

Critical Thinking Questions

Evidence of modern human diversity comes from genetics, either indirectly from phenotypes (e.g., ABO or MN blood groups) or more directly from DNA sequencing. The most complete and powerful tool uses whole genome sequencing. In just the last few years, this type of analysis has contributed greatly to

increased understanding of the origins and dispersal of human populations—that is, how long ago they first appeared, where they came from, how they are related to each other, and what migration routes they followed in the peopling of the world.

How Do We Know?

Video See the video “Race as a Cultural Construct”

to learn more about topics covered in this chapter.

Media Resources

Through natural selection, humans have and continue to adapt to environmental factors including solar radiation, cold, altitude, and, most importantly,

infectious disease.

Connections

Modern human varia- tion is best under- stood by examining

similarities and differ- ences in DNA among

populations.

Human development and adaptation is best understood

from an evolutionary perspective.

N AS

After mastering the material in this chapter, you should be able to:

▶ �Describe how patterns of adaptation in humans can be linked to natural selection.

▶ �Explain how solar radiation has played a major role in human variation in skin color. You should include two vitamins in your explanation.

▶ �Discuss why reduced pigmentation is advantageous for populations living in northern latitudes.

▶ �Explain why the study of SNPs is important to understanding human biological adaptation.

▶ �Discuss human adaptive responses to heat and cold.

▶ �Describe a mutation present in most highland Tibetan populations that allows them to live at high altitude while producing the same amount of hemoglobin as do people living at sea level. Why is this advantageous?

▶ �Explain how infectious disease became a selective force in human evolution. You should be able to give examples.

▶ �Discuss in general what pathological conditions skeletal biologists have studied in archaeologically derived human skeletons.

413

In previous chapters, we explored the genetic bases for biological vari-ation within and between human populations. We discussed how, as a species, humans are remarkably genet- ically uniform compared with our clos- est primate relatives. We’ve also placed these discussions within an evolution- ary framework, emphasizing the roles of natural selection and genetic drift in human evolution. With this founda- tion, we can turn our attention to some of the many challenges we have faced through our evolutionary journey and consider some of the ways we’ve met these challenges as a species, as popu- lations, and as individuals.

Early humans migrated out of Africa some 200,000 to 100,000 ya, and we now permanently inhabit the entire planet except for the oceans, the high- est mountain peaks, and Antarctica. But as human populations spread over the earth, they had to cope with varia- tions in ultraviolet (UV) radiation, alti- tude, temperature, humidity, diet, and infectious diseases. All of these fac- tors, plus the fact that populations were separated from one another by enor- mous distances, have combined to pro- duce many forms of adaptation in our species.

15Modern Human Biology: Patterns of Adaptation

The Adaptive Significance of Human Variation

A s you know, when biological anthropologists study human variation, they consider all evolu- tionary factors. But natural selection favoring adaptive traits was the most important mechanism that produced the variation we see today. We must also bear in mind that to accommo- date differences in climate, terrain,

Student Learning Objectives

chapter 15 Modern Human Biology: Patterns of Adaptation414

and available resources, humans had to adopt lifestyles that differed with regard to technology and diet. As time passed, and especially after the domes- tication of plants and animals begin- ning around 14,000 ya, cultural chang- es, including dietary practices, exerted an even greater degree of selective pressure. Thus, as populational differ- ences in lactose tolerance demonstrate, the interaction between culture and biology became ever more important to human adaptive responses, and this interaction was responsible for chang- es in the frequencies of many alleles. Since the sequencing of the human genome in 2003, geneticists, armed with an array of new technologies, have been looking at the genes that govern adaptive traits in many populations. Specifically, they’ve been focusing on single nucleotide polymorphisms, or SNPs, studying how differences in sin- gle DNA bases alter gene action and how their frequencies vary between populations. Within the next few years, our understanding of many aspects of human adaptation will increase dra- matically, owing to advances in genetic research that will allow the testing not only of long-held hypotheses but also of new ones.

To survive, all organisms need to maintain the normal functions of internal organs, tissues, and cells. What’s more, they must accomplish this task in the context of an ever- changing environment. Even dur- ing the course of a single, seemingly uneventful day, there are numerous fluctuations in temperature, wind, solar radiation, humidity, and so on. Physical activity also places stress on physiological mechanisms. The body must accommodate all these changes in order to maintain internal constan- cy, or homeostasis, and all life forms have evolved physiological mechanisms that, within limits, achieve this goal.

Physiological responses to environ- mental change are influenced by genet- ic factors. We’ve already defined adap- tation as a response to environmental conditions in populations and indi-

viduals. In a broader sense, adaptation refers to long-term evolutionary (that is, genetic) changes that characterize all individuals within a population or species.

Examples of long-term adapta- tions in humans include physiological responses to heat (sweating) or exces- sive levels of UV light (deeply pig- mented skin near the equator). These characteristics are the results of evolu- tionary change in our species and they don’t vary because of short-term envi- ronmental change. For example, the ability to sweat isn’t lost in people who spend their lives in predominantly cool areas. Likewise, individuals born with dark skin won’t become pale, even if they’re never exposed to sunlight.

Acclimatization is another kind of physiological response to changing environmental conditions in individu- als. Most forms of acclimatization are temporary and last only until environ- mental conditions return to their for- mer state. The physiological responses to environmental stressors are at least partially influenced by genetic factors, but some can also be affected by the duration and severity of the exposure, technological buffers (such as shelter or clothing), individual behavior, weight, and overall body size.

The simplest form of acclimatiza- tion is a temporary and rapid adjust- ment to an environmental change (for example, tanning). Another example is one you may not know about although you’ve probably experienced it. This is the rapid increase in hemoglobin pro- duction that occurs in low-altitude residents who travel to higher eleva- tions. (It’s happened in your own body if you’ve spent a few days in the moun- tains.) In both these examples, the physiological changes are temporary. Tans fade when exposure to sunlight is reduced, and hemoglobin production drops to original levels after returning to lower elevations.

Another type of acclimatization, called developmental acclimatiza- tion, results from exposure to an envi- ronmental challenge during growth

stress In a physiological context, any factor that acts to disrupt homeostasis; more precisely, the body’s response to any factor that threatens its ability to maintain homeostasis.

homeostasis a condition of balance, or stability, within a biological system, maintained by the interaction of physi- ological mechanisms that compensate for changes (both external and internal).

acclimatization physiological responses to changes in the environment that occur during an individual’s lifetime. Such responses may be temporary or permanent, depending on the duration of the environmental change and when in the individual’s life it occurs. the capac- ity for acclimatization may typify an entire population or species, and because it’s under genetic influence, it’s subject to evo- lutionary factors such as natural selection and genetic drift.

The Adaptive Significance of Human Variation 415

and development. Because this kind of acclimatization is incorporated into an individual’s physiology, it isn’t revers- ible. Certain physiological responses seen in lifelong residents of high alti- tude are examples of developmental acclimatization.

In this section, we present some of the many examples of how humans respond to environmental challenges. Some of these examples describe adap- tations that characterize our entire species; others are shared by most or all members of only certain populations.

Solar Radiation and Skin Color For many years, skin color has been cited as an example of adaptation through natural selection in humans. In general, pigmentation in indigenous populations prior to European con- tact (beginning around 1500) followed a particular geographical distribution, especially in the Old World. This pat- tern pretty much holds true today. As Figure 15-1 shows, populations with the most pigmentation are found in the

tropics, while lighter skin color is asso- ciated with more northern latitudes, especially among the long-term inhab- itants of northwestern Europe.

Three substances influence skin color: hemoglobin, the protein caro- tene, and, most important, the pig- ment melanin. Melanin is a granu- lar substance produced by cells called melanocytes, located in the outer layer of the skin (Fig. 15-2). Melanin is extremely important because it acts as a built-in sunscreen by absorb- ing potentially dangerous ultraviolet (UV) rays that are present but not vis- ible in sunlight. So melanin protects us from overexposure to UV radia- tion, which frequently causes genetic mutations in skin cells. These muta- tions can lead to skin cancer, which, if left untreated, can eventually spread to other organs and even cause death (see “A Closer Look: Skin Cancer and UV Radiation”).

As mentioned earlier, exposure to sunlight triggers a protective mecha- nism in the form of tanning, the result of a temporary increase in melanin production (acclimatization). This

▲�Figure 15-1 Geographical distribution of skin color in indigenous human populations. (After Biasutti, 1959.)

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Biasutti‘s skin color map

Note: Higher numbers represent darker skin color. From data collected by R. Biasutti prior to 1940. While imprecise, these data are the best that are available.

1–12

12–14

15–17

21–23

24–26

27–29

18–20 Over 30

PA C I F I C O C E A N

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I N D I A N O C E A N

PA C I F I C O C E A N

NORTH AMERICA

SOUTH AMERICA

ASIA

AUSTRALIA

AFRICA

EUROPE

chapter 15 Modern Human Biology: Patterns of Adaptation416

UVA UVB

Artery Vein

Epidermis

Squamous cells

Basal cells

Dermis

Fat layer

Blood vessels

Hair follicle Sweat

gland

Damaged DNA

Melanin granules

Melanocyte

response occurs in all humans except albinos, who carry a genetic mutation that prevents their melanocytes from producing melanin. But even people who do produce melanin differ in their ability to tan. For instance, in all popu- lations, women tend not to tan as deep- ly as men. More importantly, however, people of northern European descent tend to have very fair skin, blue eyes, and light hair. Their cells produce only small amounts of melanin and, when exposed to sunlight, they have almost no ability to increase production. But in areas closest to the equator (the tropics), where the sun’s rays are most direct and where exposure to UV light is most intense and constant, natural selection has favored deeply pigmented skin. In considering the cancer-causing effects of UV radiation from an evolu- tionary perspective, keep in mind these three points:

1. Early hominins lived in the trop- ics, where solar radiation is more intense than in temperate areas to the north and south.

2. Unlike most modern city dwellers, early hominins spent their days outdoors.

3. Early hominins didn’t wear protec- tive clothing.

Under these conditions, UV radia- tion was a powerful agent selecting for maximum levels of melanin production as a means of protection from UV radi- ation. Physical anthropologists have long considered this protection to be very important, because UV radiation is the most common cause of skin can- cer. There’s an important objection to this hypothesis, however. As we men- tioned in Chapter 4, natural selection can act only on traits that affect repro- duction. Because cancers tend to occur

▲ Figure 15-2 Ultraviolet rays penetrate the skin and can eventually damage DNA within skin cells. The three major types of cells that can be affected are squamous cells, basal cells, and melanocytes.

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The Adaptive Significance of Human Variation 417

later in life, after people have had their children, it should theoretically be dif- ficult for selection to act effectively against a factor that might facilitate the development of cancer. This is prob- ably true in general, but in one African study it was shown that all albinos in dark-skinned populations of Nigeria and Tanzania had either precancerous lesions or skin cancer by the age of 20 (Robins, 1991). This evidence suggests that in early hominins of reproductive age, less pigmented skin could poten- tially have reduced individual repro- ductive fitness in regions of intense sunlight.

However, Jablonski (1992) and Jablonski and Chaplin (2000, 2010) dis- agree that skin cancer was the most important factor; they have provided convincing evidence for another, prob- ably more important explanation for heavily pigmented skin in the tropics. This explanation concerns the degra- dation of folate by UV radiation. Folate is a B vitamin that is not stored in the body and must be replenished through dietary sources such as leafy green veg- etables and certain fruits. Adequate levels of folate are required for cell divi- sion, and this is especially important during embryonic and fetal develop- ment, when cell division is rapid and ongoing. In pregnant women, insuffi- cient levels of folate are associated with numerous fetal developmental disor- ders, including neural tube defects such as spina bifida (Fig. 15-3). The consequences of severe neural tube defects can include pain, infection, paralysis, and even failure of the brain to develop. Given the importance of folate to many processes related to reproduction, it’s clear that maintain- ing adequate levels of this vitamin con- tributes to individual reproductive fitness.

Studies have shown that UV radia- tion rapidly depletes serum folate levels in both laboratory animals and light- skinned people. These findings have implications for pregnant women, chil- dren, and the evolution of dark skin in early hominins. Jablonski (1992) has proposed that the earliest hominins

may have had light skin covered with dark hair, as seen in chimpanzees and goril- las (who have darker skin on exposed body parts, such as the face and hands). But as loss of body hair occurred in hominins, dark skin evolved rather rapidly as a protective response to the damaging effects of UV radiation on folate.

The maintenance of sufficient lev- els of folate and, perhaps to a lesser degree, the occurrence of skin cancer have no doubt been selective agents that have favored dark skin in popula- tions living where UV radiation is most intense. Therefore we have good expla- nations for darker skin in the tropics. But what about less pigmented skin? Why do indigenous populations in higher latitudes, farther from the equa- tor, have lighter skin? There are several closely related hypotheses, and recent studies have added strength to these arguments.

As hominins migrated out of Africa and into Asia and Europe, they faced new selective pressures. In particular, those populations that eventually occu- pied northern Europe encountered cold temperatures and cloudy skies, frequently during summer as well as winter. Winter also meant many fewer hours of daylight, and with the sun well to the south, solar radiation was very indirect. What’s more, people in these areas wore animal skins and other types of clothing, which blocked the sun’s rays. For some time, research- ers proposed that because of reduced exposure to sunlight, the advantages of deeply pigmented skin in the tropics no longer applied, and selection for mela- nin production may have been relaxed.

However, relaxed selection for dark skin doesn’t adequately explain the very depigmented skin seen in some north- ern Europeans. In fact, natural selec- tion appears to have acted very rapidly against darker skin as humans moved to northern latitudes. This is because

Vertebrae

Spinal Cord

Spinal Fluid

▲�Figure 15-3 Spina bifida occurs when the back of the vertebral column (spine) fails to close during embryonic development. It ranges from mild to lethal. In this illustration the last two lumbar vertebrae failed to fuse and the spinal cord has protruded through the opening.

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neural tube In early embryonic development, the anatomical structure that develops to form the brain and spinal cord.

spina bifida a condition in which one or more of the vertebral arches fail to fuse and form a protective barrier around the spinal cord.

chapter 15 Modern Human Biology: Patterns of Adaptation418

the need for a physiological UV filter was outweighed by another extremely important biological necessity, the pro- duction of vitamin D. The theory con- cerning the role of vitamin D is called the vitamin D hypothesis.

Since the early twentieth century, scientists have known that vitamin D is essential for the mineralization and normal growth of bones during infan- cy and childhood because it enables the body to absorb calcium (the major source of bone mineral) from dietary sources. Vitamin D is also required for the continued mineralization of bones in adults. Many foods, including fish oils, egg yolk, butter, cream, and liver, are good sources of vitamin D. But the body’s primary source of vita- min D is its own ability to synthesize it through the interaction of UV radia- tion and a form of cholesterol found in skin cells. Therefore adequate exposure to sunlight is essential to normal bone growth.

Insufficient amounts of vitamin D during childhood result in rickets, a condition that leads to skeletal defor- mities, especially in the weight-bearing bones of the legs and pelvis. Thus, peo- ple with rickets frequently have bowed legs and pelvic deformities (Fig. 15-4). Pelvic deformities are of particular concern for pregnant women because they can lead to a narrowing of the birth canal. Without surgical interven- tion, both the mother and her infant can die during childbirth, thus allow- ing natural selection to act powerful- ly in favor of any mechanism that pro- vides proper bone mineralization.

In addition to its role in bone min- eralization, vitamin D has many other critical functions. In the body, vitamin D is converted to a different molecule called 1,25D, which can attach direct- ly to DNA, and act to regulate more than 1,000 different genes (Tavera- Mendoza and White, 2007). Some of these genes are involved in cell replica- tion, and because 1,25D influences this activity, it appears to provide some pro- tection against certain cancers, espe- cially prostate and colon cancer (Lin and White, 2004). (Cancer is caused

by uncontrolled cell replication.) Moreover, 1,25D reduces inflammation and may eventually be used as a basis for treating certain diseases, includ- ing multiple sclerosis (Tavera-Mendoza and White, 2007).

Other genes influenced by 1,25D produce proteins that act as natural antibiotics to kill certain bacteria and viruses, one of which is Mycobacterium tuberculosis (M. tuberculosis), the bac- terium that causes tuberculosis (TB). Liu et al. (2006) demonstrated how 1,25D is involved in the destruction of M. tuberculosis in infected cells. The fact that exposure to UV radia- tion is necessary for vitamin D synthe- sis probably explains why, in the early twentieth century, TB patients often improved after being sent to sanitari- ums in sunny locations.

The influence of latitude and skin pigmentation on levels of 1,25D in the body has been demonstrated by epide- miological studies of modern popula- tions. For example, one study revealed that 92 percent of more than 400 girls in several northern European coun- tries were severely deficient in 1,25D during the winter months. Also, the fact that African Americans appear to have about half the amount of 1,25D seen in European Americans illustrates the role of increased pigmentation in reducing vitamin D levels in more northern latitudes (Tavera-Mendoza and White, 2007). This fact is signifi- cant because African Americans have a higher incidence of TB than European Americans (Liu et al., 2006).

As you can see, vitamin D is an immensely important factor in the body’s response to a number of condi- tions, many of which influence repro- ductive success. This evidence sub- stantially supports the vitamin D hypothesis and argues for strong and rapid positive selection for lighter skin in northern latitudes. Furthermore, the vitamin D evidence is strongly sup- ported by recent genetic studies.

At least 100 genes are thought to be involved in pigmentation in ver- tebrates. One of the more important of these genes is called MC1R, which

▲ Figure 15-4 A child with rickets.

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The Adaptive Significance of Human Variation 419

affects coloration in all mammals. The human version of this gene has at least 30 alleles, some of which are associ- ated with red hair combined with fair skin and a tendency to freckle (Lin and Fisher, 2007). As we mentioned in Chapter 13, research on Neandertal DNA has revealed that some Neandertals probably had red hair and fair skin. This research revealed the presence of an MC1R allele that reduc- es the amount of pigment in skin and hair, but it’s not an allele that occurs in modern humans. Therefore less pig- mented skin developed in two hom- inin species but through different mutations in the same gene. This fact strongly reinforces the hypothesis that there is a significant selective advan- tage to having lighter skin in higher latitudes.

Lastly, evidence for the importance of vitamin D is provided by the recent discovery of yet another gene, called SCL24A5, which we’ll refer to sim- ply as SCL (Lamason et al., 2005). This gene and its effects on pigmentation were first discovered in zebrafish, and just to emphasize (yet again) the con- cept of biological continuity or connec- tions between species, we’ll point out that approximately 68 percent of the sequences of DNA bases in the human and zebrafish SCL genes are the same (Balter, 2007).

Like MC1R, the SCL gene is involved in melanin production. This gene has two primary alleles that differ by one single base substitution; that is, one allele arose as a point mutation. The original form (allele) of the gene is pres- ent in 93 to 100 percent of Africans, Native Americans, and East Asians. However, and most importantly, vir- tually 100 percent of Europeans and European Americans have the more recent (mutated) allele that inhibits melanin production. These frequen- cies provide yet more compelling evi- dence of very strong selection for light- er skin in northern latitudes. In fact, it appears that natural selection favored the mutated allele to the point that it became the only SCL allele in northern European populations.

But there’s a question that has yet to be answered. (Actually, there are several questions, but we’ll mention only one.) In East Asians, the frequen- cy of the original melanin-producing allele is the same as in sub-Saharan Africans, yet on average, skin color in East Asians is fairly light. Lamason and colleagues (2005) argue that this means that in East Asian populations, there are other, as yet unidentified genes that interact with the SCL locus to reduce skin pigmentation. Certainly, sever- al other genes that contribute to skin pigmentation have been identified, but none has yet been shown to have the same degree of variation between populations.

Jablonski and Chaplin (2000) have looked at the potential for vitamin D synthesis in people of different skin color based on the yearly average UV radiation at various latitudes (Fig. 15-5). Their conclusions support the vitamin D hypothesis to the point of stating that the requirement of vitamin D synthesis in northern latitudes was as important to natural selection as the need for protection from UV radiation in tropical regions.

Except for a person’s sex, more social importance has been attached to skin color than to any other single human biological trait. But there’s absolute- ly no valid reason for this. Aside from its adaptive significance relative to UV radiation, skin color is no more impor- tant physiologically than many other biological characteristics. But from an evolutionary perspective, skin color provides an outstanding example of how the forces of natural selection have produced geographically patterned variation as the result of two conflict- ing selective forces: the need for pro- tection from overexposure to UV radi- ation on the one hand and the need for adequate UV exposure for vitamin D synthesis on the other.

The Thermal Environment Mammals and birds have evolved complex mechanisms to maintain a constant internal body temperature.

chapter 15 Modern Human Biology: Patterns of Adaptation420

While reptiles must rely on expo- sure to external heat sources to raise body temperature and energy levels, mammals and birds have physiologi- cal mechanisms that, within certain limits, increase or reduce the loss of body heat. The optimum body tem- perature for normal cellular functions is species-specific, and for humans, it’s approximately 98.6°F.

People are found in a wide vari- ety of habitats, with thermal environ- ments ranging from exceedingly hot (in excess of 120°F) to bitter cold (less than −60°F). In such extremes, particularly cold, human life would not be possible without cultural innovations. But even accounting for the artificial environ- ments we live in, such external condi- tions expose the human body to enor- mous stress.

Response to Heat All available evi- dence suggests that the earliest homi- nins evolved in the warm-to-hot wood- lands and savannas of East Africa. The fact that humans cope better with heat, especially dry heat, than they do with cold is testimony to the long-term

adaptations to heat that evolved in our ancestors.

In humans as well as some other species such as horses, sweat glands are distributed throughout the skin. This wide distribution of sweat glands makes it possible to lose heat at the body’s surface through evaporative cooling, a mechanism that has evolved to the greatest degree in humans. In fact, perspiration is the most important factor in heat dissipation in humans.

The capacity to dissipate heat by sweating is seen in all human popula- tions to an almost equal degree, with the average number of sweat glands per individual (approximately 1.6 million) being fairly constant. However, there is some variation, since people who are not generally exposed to hot condi- tions do experience a period of accli- matization that initially involves sig- nificantly increased perspiration rates (Frisancho, 1993). An additional fac- tor that enhances the cooling effects of sweating is increased exposure of the skin through reduced amounts of body hair. We don’t know when in our evo- lutionary history the loss of body hair

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evaporative cooling a physi- ological mechanism that helps prevent the body from overheating. It occurs when perspiration is produced from sweat glands and then evaporates from the surface of the skin.

The Adaptive Significance of Human Variation 421

vasodilation expansion of blood ves- sels, permitting increased blood flow to the skin. Vasodilation permits warming of the skin and facilitates radiation of warmth as a means of cooling. Vasodilation is an involuntary response to warm temperatures, various drugs, and even emotional states (blushing).

occurred, but it represents a species wide adaptation.

Heat reduction through evapora- tion can be expensive, and indeed dan- gerous, in terms of water and sodium loss. For example, a person engaged in heavy work in high heat can lose up to 3 liters of water per hour. To appreci- ate the importance of this fact, consid- er that losing 1 liter of water is approxi- mately equivalent to losing 1.5 percent of total body weight, and losing 10 per- cent of body weight can be life threat- ening. Thus water must be continuous- ly replaced during exercise in heat.

Basically, there are two types of heat, arid and humid. Arid environ- ments, such as those of the southwest- ern United States, the Middle East, and parts of Africa, are characterized by high temperatures, wind, and low water vapor. Humid heat, associated with increased water vapor, occurs in regions with a great deal of vegetation and precipitation, conditions found in the eastern and southern United States, parts of Europe, and much of the trop- ics. Because the increased water vapor in humid climates inhibits the evapo- ration of sweat on the skin’s surface, humans adjust much more readily to dry heat. In fact, people exercis- ing in dry heat may be unaware that they’re sweating because the perspira- tion evaporates as soon as it reaches the skin’s surface. While rapid evapo- ration increases comfort, it can lead to dehydration. Therefore in dry heat, it’s important to keep drinking water, even if you aren’t particularly thirsty.

Another mechanism for radiating body heat is vasodilation, which occurs when capillaries near the skin’s sur- face widen to increase blood flow to the skin. The visible effect of vasodi- lation is flushing, or increased redness and warming of the skin, particularly of the face. But the physiological effect is to permit heat, carried by the blood from the interior of the body, to be emitted from the skin’s surface to the surrounding air. (Some drugs, includ- ing alcohol, also produce vasodilation; this accounts for the increased redness

and warmth of the face in some people after a couple of drinks.)

Body size and proportions are also important in regulating body tempera- ture. In fact, there seems to be a gen- eral relationship between climate and body size and shape in birds and mam- mals. In general, within a species, body size (weight) increases as distance from the equator increases. In humans, this relationship holds up fairly well, but there are many exceptions.

Two rules that pertain to the rela- tionship between body size, body pro- portions, and climate are Bergmann’s rule and Allen’s rule.

1. Bergmann’s rule concerns the rela- tionship of body mass or volume to surface area. Among mam- mals, body size tends to be greater in populations that live in colder climates. This is because as mass increases, the relative amount of surface area decreases proportion- ately. Since heat is lost at the sur- face, it follows that increased mass allows for greater heat retention and reduced heat loss. (Remem ber our discussion of basal metabolic rate and body size in Chapter 7.)

2. Allen’s rule concerns the shape of the body, especially appendages. In colder climates, shorter appendag- es, with increased mass-to-surface ratios, are adaptive because they’re more effective at preventing heat loss. Conversely, longer appendag- es, with increased surface area rel- ative to mass, are more adaptive in warmer climates because they pro- mote heat loss.

According to these rules, the most suitable body shape in hot climates is linear, with long arms and legs. In cold climates, a stockier body with shorter limbs is more adaptive. Considerable data gathered from several human pop- ulations demonstrate that, in general, humans conform to these principles. In colder climates, body mass tends, on average, to be greater and to be char- acterized by a larger trunk relative

422

Skin Cancer and UV Radiation

Even though we know we can’t live without it, most people tend to take their skin for granted. the many func- tions of this complex organ (and skin is an organ) are vital to life. Yet most of us thoughtlessly expose our skin to any number of environmental assaults and especially abuse it with overexposure to the sun, practically to the point of charbroiling. For these reasons, we think it’s appropriate here to examine a little more closely this watertight, evolutionary achievement that permits us to live on land, just as it allowed some vertebrates to leave the oceans sev- eral hundred million years ago.

Skin is composed of two layers, the epi- dermis and, just beneath it, the dermis (see Fig. 15-2). the upper portion of the epi- dermis is made up of flattened, somewhat overlapping squamous (scalelike) cells. Beneath these cells, near the base of the epidermis, are several layers of round basal cells. Interspersed within the basal cells are still two other cell types: melanocytes, which produce melanin, and keratinocytes, which are involved in vitamin D synthesis.

Skin cells are continuously produced at the base of the epidermis through mitosis. as they mature, they migrate to the surface, becoming flattened and avascular; that is,

they have no direct blood supply. approxi- mately one month after forming, skin cells die in a process of genetically directed cel- lular suicide. the results of this suicidal act are the little white flakes people with dry skin are uncomfortably aware of. (Inciden- tally, dead skin cells are a major component of common household dust.)

the dermis is composed of connective tissue and many structures, including blood vessels, lymphatic vessels, sweat glands, oil glands, and hair follicles. together, the epidermis and dermis allow the body to retain fluid, help regulate body temperature, synthesize a number of essential substanc- es, and provide protection from ultraviolet (UV) radiation.

there are three main types of UV radia- tion, but here we’re concerned with only two: UVa and UVB. UVa has the longest wavelength and can penetrate through to the bottom of the dermis, while the medium-length UVB waves usually pene- trate only to the basal layer of the epidermis (see Fig. 15-2).

the stimulation of vitamin D production by UVB waves is the only benefit we get from exposure to UV radiation. Following a sunburn, both UVB and UVa rays cause short-term suppression of the immune sys- tem. But because UVB is directly absorbed by the DNa within cells, it can potentially cause genetic damage, and this damage can lead to skin cancer.

You know that cancers are tumorous growths that invade organs, a process that

often results in death, even after treat- ment. But you may not know that a cell becomes cancerous when a carcinogenic agent, such as UV radiation, damages its DNa, and some DNa segments are more susceptible than others. this damage allows the affected cell to divide uncon- trollably. each subsequent generation of cells receives the mutant DNa, and with it, the potential to divide indefinitely. eventu- ally, cancer cells form a mass that invades other tissues. they can also break away from the original tumor and travel through the circulatory or lymphatic system to other parts of the body, where they estab- lish themselves and continue to divide. For example, cells from lung tumors (fre- quently caused by carcinogenic agents in tobacco) can travel to the brain or parts of the skeleton and develop tumors in these new sites before the lung tumor is even detectable. (Former Beatle George har- rison died of brain cancer that had spread from his lungs. It’s probably no coinci- dence that he was a heavy smoker when he was young.)

all three types of cells in the epidermis are susceptible to cancerous changes. the most common form of skin cancer is basal cell carcinoma (Bcc), which affects about 800,000 people per year in the United States. Fortunately Bccs are slow growing and, if detected early, can be successfully removed before they spread. they can appear as a raised lump and be uncolored, red-brown, or black (Fig. 1a).

A Closer Look

to arms and legs. People living in the Arctic tend to be short and stocky, while many sub-Saharan Africans, especially East African pastoralists, are tall and linear (Fig. 15-6). But there’s a great deal of variation in human body proportions, and not all populations conform so obviously to Bergmann’s and Allen’s rules.

Response to Cold There are two basic types of physiological responses to cold: those that retain heat and those

that increase heat production. Of the two, heat retention is more efficient because it requires less energy. This is an important point, because energy is obtained from dietary sources. Unless food is abundant, and in winter it fre- quently is not, any factor that con- serves energy can be beneficial.

Increases in metabolic rate and shiv- ering are short-term responses that generate body heat. Increases in meta- bolic rate (the rate at which cells break up nutrients into their components)

The Adaptive Significance of Human Variation 423

Squamous cell carcinoma (Scc) is the second most common skin cancer (Fig. 1b). these cancers grow faster than Bccs, but they’re also amenable to treat- ment if detected reasonably early. they usually appear as firm pinkish lesions and may spread rapidly on skin exposed to sunlight.

the third form is malignant melanoma, a cancer of the melanocytes. Melanoma is thought to be caused by UVa radiation and accounts for only about 4 percent of all skin cancers. But while it’s the least common of the three, melanoma is the fastest growing and the deadliest, killing 30 to 40 percent of affected people. Melanoma looks like an irregularly shaped, very dark or black mole (Fig. 1c). In fact, it may be a mole that has changed because some of its cells have been damaged. It’s extremely impor- tant to notice any changes in a mole or the appearance of a new dark, perhaps rough- ened spot on the skin and have it examined

as soon as possible. If a melanoma is less than a millimeter deep, it can be removed before it spreads. But if it has progressed into the dermis, it’s likely that it has already spread to other tissues.

Brash and colleagues (1991) and Ziegler and colleagues (1994) determined that the underlying genetic factor in most nonmelanoma skin cancers is a mutation of a gene called p53 located on chromo- some 17. this gene produces the protein p53, which prevents any cell (not just skin cells) with damaged DNa from dividing until the damage is repaired. In addition, if the damage to a cell’s DNa is too severe to repair, the p53 protein can cause the cell to die. thus, p53 is what’s known as a tumor suppressor gene (Vogelstein et al., 2000).

Unfortunately, the p53 gene is itself susceptible to mutation, and when certain mutations occur, it can no longer prevent cancer cells from dividing. Luckily, there

are other tumor suppressor genes. In fact, damaged p53 genes don’t appear to be involved in melanoma. Instead, a UV-induced mutation in another tumor sup- pressor gene on chromosome 9 appears to be the culprit.

Bccs and Sccs tend to appear in middle age, long after childhood and ado- lescence, when the underlying genetic damage occurred. If you’ve had even one serious sunburn in your life, your odds of developing one of the nonmelanoma skin cancers are dramatically increased. Malig- nant melanomas can occur at any age, although the DNa damage can precede the development of cancer by several years. the best advice is not to take the threat of skin cancer lightly and to avoid overexpos- ing your skin to the sun. Wear a hat and a broad-based sun block that will filter out both UVa and UVB rays. In other words, do your best to protect your tumor suppressor genes—and yourself.

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release energy in the form of heat. Shivering also generates muscle heat, as does voluntary exercise. But both these methods are costly because they require an increased intake of nutrients to provide needed energy. (Perhaps this explains why we tend to have a hearti- er appetite during the winter and why, during that season, we also tend to eat more fats and carbohydrates, the very sources of the energy we require.)

In general, people exposed to chron- ic cold (meaning much or most of the

year) maintain higher metabolic rates than people who live in warmer cli- mates. The Inuit (Eskimo) people living in the Arctic maintain metabolic rates between 13 and 45 percent higher than that observed in non-Inuit control sub- jects (Frisancho, 1993). What’s more, the highest metabolic rates are seen in inland Inuit, who are exposed to even greater cold stress than coastal popu- lations. Traditionally the Inuit had the highest animal protein and fat diet of any population in the world. Their diet

chapter 15 Modern Human Biology: Patterns of Adaptation424

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was dictated by the available resource base, and it served to maintain the high metabolic rates required by exposure to chronic cold.

Vasoconstriction is another short- term response, but instead of produc- ing heat, it minimizes heat loss and therefore is more energy efficient. Vasoconstriction restricts capillary blood flow to the surface of the skin, thus reducing heat loss at the body surface. Because retaining body heat is more economical than creating it, vasoconstriction is very efficient pro- vided that temperatures don’t drop below freezing. However, if tempera- tures do fall below freezing, continued vasoconstriction can lower skin tem- perature to the point of frostbite or worse.

Long-term responses to cold vary among human groups. For example, in the past, desert-dwelling native Australian populations experienced wide temperature fluctuations from day to night. Because they wore no clothing and didn’t build shelters, they built sleeping fires to protect them- selves from nighttime temperatures hovering only a few degrees above freezing. Also, they experienced con- tinuous vasoconstriction throughout the night, which permitted a degree of skin cooling most people would find

extremely uncomfortable. But since there was no threat of frostbite, contin- ued vasoconstriction helped prevent excessive internal heat loss.

By contrast, the Inuit experience intermittent periods of vasoconstric- tion and vasodilation. This compro- mise provides periodic warmth to the skin, which helps prevent frostbite in below-freezing temperatures. At the same time, because the vasodilation is intermittent, energy loss is restricted to retain more heat at the body’s core.

Humans and some other animals also have a subcutaneous (beneath the skin) fat layer that provides insulation throughout the body. In many overfed populations today, this fat layer is an annoyance to many and a major health issue for others. But in the not too dis- tant past, our hunting and gathering ancestors relied on it not only for some protection against the cold but also as a source of nutrients when food was scarce.

These examples illustrate two of the ways in which adaptations to cold vary among human populations. Obviously winter conditions exceed our ability to adapt physiologically in many parts of the world. Consequently, if our ances- tors hadn’t developed cultural innova- tions, they would have remained in the tropics.

▲ Figure 15-6 (a) These Samburu women (and men in the background) have the linear proportions character- istic of many inhabitants of East Africa. The Samburu are cattle herding peo- ple who live in northern Kenya. Here they are shown dancing. (b) By com- parison, these Canadian Inuit women are shorter and stockier. Although the people in these two pictures don’t typify everyone in their populations, they do serve as good examples of Bergmann’s and Allen’s rules.

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The Adaptive Significance of Human Variation 425

◀�Figure 15-7 (a) Namche Bazaar, Tibet, situated at an elevation of over 12,000 feet above sea level. (b) La Paz, Bolivia, at just over 12,000 feet, is home to more than 1 million people.

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High Altitude Studies of high-altitude residents have greatly contributed to our under- standing of physiological adaptation. As you’d expect, altitude studies have focused on inhabitants of mountainous regions, particularly in the Himalayas, Andes, and Rocky Mountains. Of these three areas, the Himalayas probably have the longest history of permanent human habitation (Moore et al., 1998). Today perhaps as many as 25 million people live at altitudes above 10,000 feet. In Tibet, permanent settlements exist above 15,000 feet; in the Andes,

they can be found as high as 17,000 feet (Fig. 15-7).

Because the mechanisms that main- tain homeostasis in humans evolved at lower altitudes, we’re compromised by the conditions at higher eleva- tions. At high altitudes, many factors result in stress on the human body. These include hypoxia, more intense solar radiation, cold temperatures, low humidity, wind (which amplifies cold stress), a reduced nutritional base, and rough terrain. Of these, hypoxia causes the most problems for human physi- ological functions, especially those involving the heart, lungs, and brain.

hypoxia Insufficient levels of oxygen in body tissues; oxygen deficiency.

chapter 15 Modern Human Biology: Patterns of Adaptation426

Hypoxia is caused by reduced baro- metric pressure. It’s not that there’s less oxygen in the atmosphere at high altitudes; rather, it’s less concentrated. Therefore to obtain the same amount of oxygen at 9,000 feet as at sea level, people must make certain physiologi- cal alterations that increase the body’s ability to transport and efficiently use the oxygen that’s available.

Reproduction in particular is affect- ed through increased infant mortality rates, miscarriage, low birth weights, and premature births. One cause of fetal and maternal death is preeclamp- sia, a severe elevation of blood pres- sure in pregnant women after the 20th gestational week. In another study of Colorado residents, Palmer and col- leagues (1999) reported that among pregnant women living at elevations over 10,000 feet, the prevalence of pre- eclampsia was 16 percent, compared with 3 percent at around 4,000 feet. In general, the problems related to child- bearing are attributed to issues that compromise the vascular supply (and thus oxygen transport) to the fetus.

People born at lower altitudes and high-altitude natives differ some- what in how they adapt to insufficient amounts of available oxygen. When people born at low elevations travel to higher ones, the process of acclimatiza- tion begins within a day or two. These changes include increases in meta- bolic rate, respiration, heart rate, and the production of red blood cells. (Red blood cells contain hemoglobin, the protein responsible for transporting oxygen to organs and tissues.)

In high-altitude natives, acclimati- zation occurs during growth and devel- opment. This type of developmen- tal acclimatization is present only in people who grow up in high-altitude areas, not in those who moved there as adults. Compared with populations at lower elevations, lifelong residents of high altitude grow somewhat more slowly and mature later. Other differ- ences include greater lung and heart capacity. People born at high altitudes are also more efficient than migrants at diffusing oxygen from blood to body

tissues, and the genes that regulate this ability are beginning to be identified. Developmental acclimatization to high altitude serves as a good example of physiological flexibility by illustrating how, within the limits set by genetic factors, development can be influenced by environmental factors.

But the best evidence for perma- nent high-altitude adaptation is pro- vided by the indigenous peoples of Tibet, who have inhabited regions higher than 12,000 feet for at least 7,000 (Simonson et al., 2010) and per- haps as long as 25,000 years. For this reason, these populations have been the subject of many studies. Altitude does not negatively affect reproduction in highland Tibetans to the degree it does in other populations. Infants have birth weights as high as those of low- land Tibetan groups and higher than those of recent (20 to 30 years) Chinese immigrants. This fact may be the result of alterations in maternal blood flow to the uterus during pregnancy (Moore et al., 2006).

Another line of evidence concerns how the body processes glucose (blood sugar). Glucose is critical because it’s the only source of energy used by the brain, and it’s also used, although not exclusively, by the heart. Both high- land Tibetans and the Quechua (inhab- itants of high-altitude regions of the Peruvian Andes) burn glucose in a way that permits more efficient oxygen use. This implies the presence of genetic mutations in the mitochondrial DNA, because mtDNA directs how cells pro- cess glucose. It also indicates that natu- ral selection has acted to increase the frequency of these advantageous muta- tions in these groups.

We now have solid evidence that natural selection has acted strongly and rapidly to increase the frequen- cy of certain alleles that have pro- duced adaptive responses to altitude in Tibetans. Ninety percent of Tibetan highlanders possess a point muta- tion in a gene called EPAS1, which is involved in red blood cell production. In effect, the EPAS1 mutation inhib- its the increased red blood cell pro-

Infectious Disease 427

duction we would expect to see in people living at high altitude. Thus Tibetans have red cell counts similar to those of populations living at sea level. Interestingly, the Quechua and other high-altitude residents of the Andes do not have this mutation and have elevat- ed red cell counts compared with low- land inhabitants. But if increased red blood cell production is advantageous at high altitude, why would selection favor a mutation that acts against it in Tibetans? The answer is that beyond certain levels, elevated numbers of red cells can actually “thicken” the blood and lead to increased risk of stroke, blood clots, and heart attack. In preg- nant women, they can also lead to impaired fetal growth and even fetal death. Thus, although the mecha- nisms aren’t yet understood, Tibetans have acquired a number of genetical- ly influenced adaptations to hypox- ic conditions while still producing the same amount of hemoglobin we would expect at sea level. This mutation is believed to have appeared only around 4,000 ya, yet it is present throughout most highland Tibetan populations. The fact that it has spread so rapidly indicates that it is extremely advanta- geous and that natural selection has acted very powerfully and quickly to increase its frequency (Yi et al., 2010).

Infectious Disease

Infection, as opposed to other disease categories such as degenerative or genetic disease, includes pathologi- cal conditions caused by microorgan- isms (viruses, bacteria, fungi, and other one-celled organisms). Throughout the course of human evolution, infectious disease has exerted enormous selective pressures on populations, influencing the frequency of alleles that affect the immune response. Indeed the impor- tance of infectious disease as an agent of natural selection in human popula- tions cannot be overemphasized. But as important as infectious disease has been, its role in this regard isn’t very well documented.

The effects of infectious disease on humans are mediated culturally as well as biologically. Innumerable cultur- al factors, such as architectural styles, subsistence techniques, exposure to domesticated animals, transportation, and even religious practices, affect how infectious disease develops and persists within and between populations.

Until about 15,000 years ago, all humans lived in small nomadic hunt- ing and gathering groups. These groups rarely stayed in one location more than a few days or weeks at a time, so they had little contact with refuse heaps that house disease vectors. But with the domestication of plants and ani- mals, people became more seden- tary and began living in small villages. Gradually, villages became towns; and towns, in turn, developed into densely crowded, unsanitary cities.

As long as humans lived in small bands, there was little opportunity for infectious disease to affect large numbers of people. Certainly people were sometimes infected with various pathogens through contact with ani- mals they killed and butchered; they were also exposed to infectious illness by drinking contaminated water, expo- sure to insects such as mosquitoes, and simply through association with each other. But even if an entire local group or band were wiped out, the effect on the overall population in a given area would have been negligible. Moreover, for a disease to become endemic in a population, there must be enough people to sustain it. Therefore small bands of hunter-gatherers weren’t faced with continuous exposure to endemic disease.

But with the advent of settled liv- ing and close proximity to domesti- cated animals, opportunities for expo- sure to disease increased. As sedentary life permitted larger group size, it became possible for several diseases to become permanently established in some populations. Moreover, exposure to domestic animals, such as cattle and fowl, provided an opportune environ- ment for the spread of several zoonotic diseases. The crowded, unsanitary

vectors agents that transmit disease from one carrier to another. Mosquitoes are vectors for malaria, just as fleas are vectors for bubonic plague.

pathogens Substances or micro- organisms, such as bacteria, fungi, or viruses, that cause disease.

endemic continuously present in a population.

zoonotic (zoh-oh-no´-tic) pertaining to a zoonosis (pl., zoonoses), a disease that’s transmitted to humans through contact with nonhuman animals.

chapter 15 Modern Human Biology: Patterns of Adaptation428

conditions that characterized parts of all cities until the late nineteenth century and that still persist in much of the world today further added to the disease burden borne by human populations.

Tuberculosis, discussed above, has been one of the most cited examples of zoonotic disease. It is believed to have been transmitted from cattle to humans after cattle were domesticat- ed some 10,000 ya. In fact, TB is widely considered to be one of the many pric- es humans have paid for living in close association with domesticated animals. Mycobacterium tuberculosis usually infects the lungs. It’s spread through sneezing and coughing, and symptoms include coughing, fatigue, and fever. Prior to the development of antibiot- ic therapies, the disease often proved fatal. In addition to the lungs, the bac- terium can attack other tissues, includ- ing bone. The area of the skeleton most commonly involved is the spine and when this occurs, two or three verte- brae may be destroyed and eventually collapse (Fig. 15-8).

Malaria provides perhaps the best- documented example of how dis- ease can act to change allele frequen- cies in human populations. In Chapter 4, you saw how, in some African and Mediterranean populations, malar- ia has altered allele frequencies at the locus that governs hemoglobin for-

mation, leading to an increased prev- alence of sickle-cell anemia. Despite extensive long-term eradication pro- grams, malaria still poses a serious threat to human health. Indeed, the World Health Organization estimates the number of people currently infect- ed with malaria to be between 300 and 500 million worldwide. And this number is increasing as drug-resistant strains of the disease-causing microor- ganism become more common (Olliaro et al., 1995).

Another example of the selective role of infectious disease is indirectly provided by AIDS (acquired immuno- deficiency syndrome). In the United States, the first cases of AIDS were reported in 1981. Since then, perhaps as many as 1.5 million Americans have been infected by HIV (human immunodeficiency virus), the agent that causes AIDS. However, most of the burden of AIDS is borne by devel- oping countries, where 95 percent of all HIV-infected people live (Fig. 15-9). According to World Health Organization estimates, between 32 and 35 million people worldwide were living with HIV infection as of November 2010, and more than 25 mil- lion had died (UNAIDS/WHO 2010 AIDS Epidemic Updates).

By the early 1990s, scientists were aware of some patients who had been HIV-positive for 10 to 15 years but con- tinued to show few if any symptoms, leading researchers to suspect that some individuals were naturally resis- tant to HIV. This was shown to be true in late 1996 with the publication of two independent studies that demonstrated a mechanism for HIV resistance (Dean et al., 1996; Samson et al., 1996).

These two reports describe a genetic mutation that involves a major receptor site on the surface of certain immune cells, including T4 cells. (Receptor sites are protein molecules that enable HIV and other viruses to invade cells.) As a result of the mutation, the receptor site doesn’t function properly and the virus can’t enter the cell. Current evidence strongly suggests that people who are homozygous for this allele may be

▶�Figure 15-8 Portion of a vertebral column from a 17 to 25 year-old male infected with tuberculosis. Most of the bodies of three lower thoracic verte- brae (attached to the ribs) have been destroyed, and the spine has col- lapsed. This vertebral column is from a medieval burial site in England.

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Infectious Disease 429

completely resistant to many types of HIV infection. In heterozygotes, infec- tion may still occur, but the course of HIV disease is significantly slowed.

For unknown reasons, the mutant allele occurs mainly in people of European descent, among whom its frequency is about 10 percent. However, the mutation appears to be absent in certain Japanese and West African groups that were stud- ied (Samson et al., 1996). Another research team reported an allele fre- quency of about 2 percent among African Americans; they speculat- ed that the presence of the allele in African Americans is due to genetic admixture (gene flow) with European Americans (Dean et al., 1996). They also suggested that this polymorphism exists in Europeans because of selec- tive pressures favoring an allele that originally occurred as a rare muta- tion. But it’s important to understand that the original selective agent was not HIV. Instead, it was some other as yet unidentified pathogen that requires the same receptor site as HIV, and some researchers have implicated the virus that causes smallpox. Lalani and col- leagues (1999) reported that a poxvirus,

related to the virus that causes small- pox, can use the same receptor site as HIV. While this conclusion hasn’t yet been firmly established, it offers a very interesting avenue of research. It may reveal how a mutation that has been favored by selection because it provides protection against one type of infection (perhaps smallpox) can also increase resistance to another (AIDS).

Smallpox, once a deadly viral dis- ease, is estimated to have accounted for 10 to 15 percent of all deaths in parts of Europe during the eighteenth cen- tury (Fig. 15-10). It’s possible that dur- ing its long history, smallpox may have altered the frequency of the ABO blood types by selecting against the A allele. Smallpox had a higher incidence in people with blood type A or AB than in type O individuals, a fact that may be explained by the presence of an antigen on the smallpox virus that’s similar to

▲ Figure 15-9 Geographical distri- bution of HIV infection as of the end of 2009.

▶�Figure 15-10 This 1974 photo shows a young boy in Bangladesh with smallpox. His body is covered with the painful pustules that are typical of the disease. These lesions frequently leave severe scarring on the skin of survivors. CD

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the A antigen. Thus, when some type A individuals were exposed to smallpox, their immune systems failed to rec- ognize the virus as foreign and didn’t mount an adequate immune response. This meant that people with the A allele died in greater numbers than those without it. So in regions where smallpox was common in the past, it could have altered allele frequencies at the ABO locus by selecting against the A allele.

Smallpox, once a devastating kill- er of millions, is the only condition to have been successfully eliminated by modern medical technology. By 1977, through massive vaccination pro- grams, the World Health Organization was able to declare the smallpox virus extinct except for a few colonies in research labs in the United States and Russia.*

The Continuing Impact of Infectious Disease

It’s important to understand that humans and pathogens exert selec- tive pressures on each other, creating a dynamic relationship between disease organisms and their human (and non- human) hosts. Just as disease exerts selective pressures on host populations to adapt, microorganisms also evolve and adapt to various pressures exerted on them by their hosts.

Evolutionarily speaking, it’s to the advantage of any pathogen not to be so deadly that it kills its host too quickly.

*Concern over the potential use of the smallpox virus by bioterrorists relates to these laboratory colonies. Although the virus is extinct outside these labs, some officials fear the possibility that samples of the virus could be stolen. Also, there are apparently some concerns that unknown colonies of the virus may exist in labs in countries other than Russia and the United States. Using disease organisms against enemies isn’t new. In the Middle Ages, armies catapulted the corpses of smallpox and plague victims into towns under siege, and during the U.S. colonial period, British soldiers knowingly gave Native Americans blankets that had been used by smallpox victims.

If the host dies shortly after becoming infected, the virus or bacterium may not have time to reproduce and infect other hosts. Thus selection sometimes acts to produce resistance in host pop- ulations and/or to reduce the virulence of disease organisms, to the benefit of both. However, members of popu- lations exposed for the first time to a new disease frequently die in huge numbers. This type of exposure was a major factor in the decimation of indig- enous New World populations after Europeans introduced smallpox into Native American groups. And it has also been the case with the current worldwide spread of HIV.

Of the known disease-causing organisms, HIV provides the best- documented example of evolution and adaptation in a pathogen. It’s also one of several examples of interspecies transfer of infection. For these reasons, we focus much of this discussion of evolutionary factors and infectious dis- ease on HIV.

The type of HIV responsible for the AIDS epidemic is HIV-1, which is extremely variable genetically. Since the late 1980s, researchers have been comparing the DNA sequences of HIV and a closely related virus called sim- ian immunodeficiency virus (SIV), which is found in chimpanzees and several African monkey species. Like HIV, SIV is genetically variable, and each strain appears to be specific to a given primate species. SIV produc- es no symptoms in the African mon- keys and chimpanzees that are its tra- ditional hosts, but when injected into Asian monkeys, it eventually causes immune suppression, AIDS-like symp- toms, and death. These findings indi- cate that the various forms of SIV have shared a long evolutionary history with a number of African primate species and that these primates have developed ways of accommodating this virus, which is deadly to their Asian rela- tives. These results also substantiate long-held hypotheses that SIV and HIV evolved in Africa. Furthermore, DNA comparisons have shown that HIV-1 almost certainly evolved from the form

The Continuing Impact of Infectious Disease 431

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of SIV that infects chimpanzees indig- enous to western central Africa (Gao et al., 1999).

As you read earlier, in parts of West Africa, chimpanzees are rou- tinely hunted by humans for food. So the most probable explanation for the transmission of SIV from chimpanzees to humans is the hunting and butcher- ing of chimpanzees (Gao et al., 1999; Weiss and Wrangham, 1999). Thus, HIV/AIDS is a zoonotic disease (Fig. 15-11). The DNA evidence further sug- gests that there were at least three sep- arate human exposures to chimpanzee SIV, and at some point the virus was altered to the form we call HIV. Exactly when chimpanzee SIV was transmit- ted to humans is unknown. The oldest evidence of human infection is a fro- zen HIV-positive blood sample taken from a West African patient in 1959. Therefore, although human expo- sure to SIV/HIV probably occurred many times in the past, the virus didn’t become firmly established in humans until the latter half of the twentieth century.

Influenza is a contagious respi- ratory disease caused by various strains of virus. It, too, is a zoonot- ic disease, and it has probably killed more humans than any other infec- tious disease. There were two flu

▼�Figure 15-11 These people, sell- ing butchered chimpanzees in West Africa, probably don’t realize that by handling this meat they could be exposing themselves to HIV.

Zoonoses and Human Infectious Disease

At a Glance

human population

Blood-blood contact

hIV in humans

Vectors: fleas and the rats that carry them

humans

Examples

transmission Indirectly

Directly

animal host SIV (Virus) in chimpanzees

Bubonic plague (bacterium) in fleas

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chapter 15 Modern Human Biology: Patterns of Adaptation432

pandemics in the twentieth century; the first of these killed an estimated 20 million people in 1918. Moreover, “seasonal flu,” which comes around every year, killed approximately 36,000 people annually in the United States during the 1990s (Centers for Disease Control, 2009). Worldwide, it accounts for several hundred thou- sand deaths every year.

The influenza viruses that infect humans are initially acquired through contact with domestic pigs and fowl (Fig. 15-12). For this reason, influen- za is frequently referred to as swine or avian (bird) flu, depending on which species transmitted it to humans. In 2009, a new swine flu virus called H1N1 caused great fear of another pan- demic, partly because it caused more severe illness in younger people than most flu viruses.

Because swine flu epidemics are less frequent than the seasonal avian flu, people have less resistance when con- fronted with a “new” swine flu virus. Swine flu can also be more deadly, and health professionals are always mind-

ful of, and haunted by, the memory of the catastrophic 1918 pandemic. For all these reasons, health profes- sionals worldwide mobilized an enor- mous effort in 2009 to prepare for a new swine flu pandemic. Hundreds of millions of doses of vaccine were dis- tributed, but the epidemic proved not to be as severe as originally feared. Still, health officials are always on the alert for the possibility of an influ- enza pandemic, partly because of the ever-present danger posed by close contact between humans, pigs, and domestic fowl.

Until the twentieth century, infec- tious disease was the number one cause of death in all human popula- tions. Even today in many developing countries, as much as half of all mor- tality is due to infectious disease, com- pared with only about 10 percent in the United States. For example, there are an estimated 1 million deaths due to malaria every year. That fig- ure computes to one malaria-related death every 30 seconds (Weiss, 2002)! Ninety percent of these deaths occur in sub-Saharan Africa, where 5 per- cent of children die of malaria before age 5 (Greenwood and Mutabingwa, 2002; Weiss, 2002). In the United States and other industrialized nations, with improved living conditions, better san- itation, and the widespread use of anti- biotics since the 1940s, infectious dis- ease has given way to heart disease and cancer as the leading causes of death.

Optimistic predictions held that infectious disease would one day be a thing of the past. You may be sur- prised to learn that in the United States mortality due to infectious disease has actually increased in recent years (Pinner et al., 1996). This increase may partly be due to the overuse of antibi- otics. It’s estimated that half of all anti- biotics prescribed in the United States are used to treat viral conditions such as colds and flu. Because antibiotics are completely ineffective against virus- es, antibiotic therapy in these cases is not only useless but may actually have dangerous long-term consequences. There’s considerable concern in the

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▲�Figure 15-12 This woman, selling chickens in a Chinese market, is wear- ing a scarf over her nose and mouth in an attempt to protect herself from exposure to avian flu.

Human Skeletal Biology: What Bones Can Tell Us about Ancient Diseases, Trauma, and Lifestyles 433

biomedical community over the indis- criminate use of antibiotics since the 1950s. Antibiotics have exerted selec- tive pressures on bacterial species that have, over time, evolved antibiotic- resistant strains (an excellent exam- ple of natural selection). So in the past few years, we’ve seen the reemergence of many bacterial diseases, including, pneumonia, cholera, and TB in forms that are less responsive to treatment.

The World Health Organization now lists tuberculosis as the world’s leading killer of adults (Colwell, 1996). In fact, the number of TB cases world- wide has risen 28 percent since the mid-1980s, with an estimated 10 mil- lion people infected in the United States alone. Although not all infected people develop active disease, in the 1990s an estimated 30 million persons worldwide are believed to have died from TB. One very troubling aspect of the increase in TB infection is that new strains of Mycobacterium tuberculo- sis are resistant to many antibiotics and other treatments.

Various treatments for nonbacterial conditions have also become ineffec- tive. One such example is the appear- ance of chloroquine-resistant malaria, which has rendered chloroquine (the traditional preventive medication) vir- tually useless in some parts of Africa. And many insect species have also developed resistance to commonly used pesticides.

Fundamental to all these factors is human population growth. As it con- tinues to soar, it causes more environ- mental disturbance and, through addi- tional human activity, increased global warming. Global warming is impor- tant in this regard because, as tempera- tures rise in previously cooler regions and as patterns of precipitation change, new habitats for disease vectors such as mosquitoes open up. Moreover, in developing countries, where as much as 50 percent of mortality is due to infec- tious disease, overcrowding and unsan- itary conditions increasingly contribute to higher rates of communicable illness. It’s hard to conceive of a better set of circumstances for the appearance and

spread of communicable disease, and it remains to be seen if scientific innova- tion, medical technology, and political views will be able to meet the challenge.

Human Skeletal Biology: What Bones Can Tell Us about Ancient Diseases, Trauma, and Lifestyles

Many physical anthropologists con-centrate on the study of human skeletons found in prehistoric archae- ological contexts. Similar expertise is also used in studies of very ancient remains dating back as far as several million years. Here we discuss investi- gations that focus on human remains dating to within the last 10,000 years. It’s during this period that human pop- ulations began living in permanent settlements and burying their dead in concentrated areas (i.e., cemeteries); as a result, there is far more available skel- etal material to study than is true for any prior period.

Evidence of Prehistoric Diseases Skeletal biologists who study disease and trauma in prehistoric remains are called paleopathologists. In prehistor- ic skeletons, numerous kinds of con- ditions have been recognized, includ- ing dental problems, infectious disease, neoplasms (cancer and other tumors), metabolic disorders (which typically affect growth), and degenerative arthri- tis and related conditions. In addition, paleopathologists are also interested in trauma, which can be recognized in skeletons in the form of broken bones or, occasionally, as weapon wounds.

Dental disease is the most com- mon category of pathological condi- tions found in prehistoric remains. Commonly seen dental problems include extreme tooth wear (see Fig. 15-13), abscesses, and tooth loss.

chapter 15 Modern Human Biology: Patterns of Adaptation434

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(For a very early example dating close to 2 mya, see Chapter 11, Fig. 11-7). Dental caries (cavities) were not com- mon among hunter-gatherers prior to the adoption of agriculture, but with the introduction of new foods contain- ing carbohydrates (especially grains such as corn or wheat), the frequency of caries increased dramatically. In fact, one “marker” of an agricultural lifestyle is the high frequency of caries.

As we have discussed in this chap- ter, infectious disease became the leading cause of death in human pop- ulations during the past few thou-

sand years and, consequently, a major adaptive challenge for our species. Paleopathologists have found numer- ous examples of severe infectious diseases such as TB and syphilis. In the New World there are a few cases of TB and several examples of fun- gal diseases including “valley fever,” found in California and the American Southwest (Fig. 15-14).

Non‒life-threatening benign bone tumors are quite common, but only a few cases of severe cancer have been reported (Fig. 15-15). There are several possible explanations for the apparent rarity of cancer in the past: People died younger, on average, in prehistory, and cancer primarily affects older people. Also, many cancers don’t affect bone or do so only in advanced cases. Thus many individuals who may have had cancer died before it progressed to their skeletons. Moreover, exposure to envi- ronmental carcinogens was less com- mon in prehistory than it is today.

Metabolic diseases such as rickets are most severe when they affect chil- dren during development (Fig. 15-16; also see Fig. 15-4, which shows rick- ets in a young child). Degenerative dis- eases include a wide variety of condi-

▲�Figure 15-13 Severe dental wear in the maxilla of a Native Californian. Such extreme wear is typical in this population and is hypothesized to have been the result of grit in the diet.

▲�Figure 15-15 Numerous lesions of the cranium (such erosive lesions were also found in other bones), probably the result of a disseminated (metastasized) cancer, pos- sibly originating from the breast, shown here in an Inuit (Eskimo) female.

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▲�Figure 15-14 Extreme reaction in a cra- nium from an Alaskan Eskimo, diagnostic of syphilis (although other possibilities must be considered).

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Human Skeletal Biology: What Bones Can Tell Us about Ancient Diseases, Trauma, and Lifestyles 435

▲�Figure 15-16 These lower leg bones of a child from an archaeologi- cal site in England are bowed. Such bowing is typical of rickets.

▲�Figure 15-17 Extreme degenerative arthritis in the knee of an adult female from Nubia (part of the modern country of Sudan, from about a.d. 700–1400).

tions, but those that directly affect the skeleton are colloquially referred to as “arthritis.” The most common location is the spine, especially in older individ- uals. The joints of the limbs, particu- larly hips and knees, are also frequently affected (Fig. 15-17).

As mentioned, paleopathologists also study trauma, which is found most typically in the form of healed fractures (Fig. 15-18). Fractures that occur at or very near the time of death exhibit no evidence of healing; therefore it’s dif- ficult to distinguish such perimortem traumatic lesions from damage that occurred perhaps centuries after the death of the individual. (Post-mortem damage can occur any time burial sites are disturbed due to construction, agri- cultural activities, and many other factors.)

Wounds caused by weapons can be dramatic; even if they healed long before the person died, they are often still very obvious. Sometimes, if such injuries occurred shortly before or at death, it’s possible to determine cause of death, something that usually is not possible in archaeological materi-

al. For example, there are cases where arrow points have been found embedded in bones such as vertebrae or the cranium, with no sign of healing. In such a situation, it’s safe to assume that the person didn’t die of natural causes (Fig. 15-19). In several Old World sites, burials with injuries caused by metal weap- ons have also been found, particularly in battlefield cemeteries. Not surprisingly, these skeletons display many fatal injuries (Fiorato et al., 2000).

In August, 2012, archaeologists excavated the skeletal remains of an adult male in Leicester, England. As of this writing, there are no offi- cial publications regarding the skel- eton, but it is likely to be that of King Richard III who died in battle in 1485. This is one of the most exciting

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◀�Figure 15-18 Fracture of a right femur (thigh bone) seen from the rear. (The normal left femur is shown for comparison.) Such an injury is extremely severe, even life- threatening, but in this individual the bone healed remarkably well.

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chapter 15 Modern Human Biology: Patterns of Adaptation436

archaeological discoveries in decades because it has the potential to answer questions about this infamous mon- arch that historians and others have been asking for 500 years. One near- contemporary account states that Richard III was killed by a blow to the back of the head. The rear por- tion of this newly discovered cranium exhibits a severe injury and addition- ally a barbed, metal projectile point was found in the “upper back.” Last, the spine exhibits evidence of sco- liosis and legend (strongly enhanced by Shakespeare) has always held that Richard III had a spinal deformity. Currently researchers are waiting for results of DNA analysis to help con- firm the identity of this individual (Burns, 2012).

Reconstruction of Prehistoric Behavioral Patterns Skeletal biologists are very much interested in learning how prehis- toric peoples behaved and how vari- ous behaviors influenced their health. In the last two decades many skeletal experts have identified this approach with the term bioarchaeology, the

use of which actually dates back to the 1970s (Buikstra, 1977). In current practice, most bioarchaeologists use a broad-based approach (Buzon, 2012). There are, however, some research- ers who regard bioarchaeology from a more limited perspective, especial- ly where attempts are made to recon- struct activity patterns in the past (Jurmain, 1999).

Reconstructing Prehistoric Activities Understanding what sorts of activities ancient peoples practiced is obviously a fascinating area of research. Can we learn about specific activities from skeletons? The answer is that some- times it’s possible but frequently it isn’t. The ways in which bone responds to activity (and other influences) involve complex physiological and biochemi- cal processes and are best approached using rigorous scientific methods. Thus the study of evidence of activity in skeletons provides a good example of hypothesis testing and verification.

Three different types of skeletal changes have been especially popular with bioarchaeologists attempting to reconstruct prehistoric activities: osteo- arthritis, areas where muscles attach to bones, and bone geometry (i.e., bone shape). Osteoarthritis (OA) is a very common condition seen in all human populations. A simple conclusion that is frequently made assumes that osteo- arthritis results mainly from activity; following this logic, people who work harder should end up with more OA in their skeletons. Think about this inter- pretation as a hypothesis. Let’s say we see more OA in the skeletons of some individuals than others in an ancient population. Did those with OA work harder? Did they participate in some particular activity that increased the amount of arthritic bone change?

The answer may be “yes,” but most likely it’s “no.” The safest conclusion is that we really cannot say. The prob- lem arises because we know from bio- medical research (including thou- sands of published studies) that OA is caused by structural and biochemical

▲�Figure 15-19 Embedded piece of an obsidian projectile point in a lumbar vertebra from a central California male, 25 to 40 years old. The portion being held was found with the burial and may have been retained during life in soft tissue (muscle?). The injury shows some healing.

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Human Skeletal Biology: What Bones Can Tell Us about Ancient Diseases, Trauma, and Lifestyles 437

▲�Figure 15-20 Bony lipping around the margins of two lumbar vertebrae. This condition is related to osteoarthri- tis and is caused by the same major factors (that is, age, genes, and prior acute injury). Although sometimes suggested by bioarchaeologists to be a result of activity, there are virtually no biomedical/clinical studies to substan- tiate this claim and much data to refute it. This is a very good example of how to confidently reject a hypothesis.

changes to the cartilage at the ends of bones and that these changes are primarily caused by advancing age, genetic influences (varying consid- erably among individuals), and pos- sibly previous injury. Because of the importance of age as a contributing factor to the development of OA, any comparison between groups must first consider age differences between them. If one group is primarily com- posed of younger individuals, then the prevalence of OA should be lower than it would be in a group composed mainly of older ones. Also, compari- sons among groups require statisti- cal testing, and this fact dictates that samples should be large enough for tests to be valid.

Many bioarchaeologists assume that OA (and other bone changes dis- cussed below) results from regular adult activities such as climbing, carry- ing heavy loads, grinding grain, etc. But once we consider particularly the influ- ences of age and genes, there is vey lit- tle remaining evidence to suggest that activity was the main cause of arthritic bone changes (Fig. 15-20). There are, however, a few exceptions. For exam- ple, elbow arthritis in Eskimo (Inuit) skeletons likely reflect, at least in part, extreme activities (Merbs, 1983; Jurmain, 1999).

Another type of skeletal change that has been related to specific activities is alterations to the areas where mus- cles attach to bones. In this type of research the basic assumption seems clear. That is, increased activity that repeatedly uses certain muscles pro- duces changes to points of attach- ment. This certainly can be the case for acute injury (such as a torn muscle). But what can we say about more typi- cal long-term adult activities? Once again, evidence from medical research indicates that the causes of such bone changes are numerous and include age and genetic influences (Milella et al., 2012).

One very useful way to test hypoth- eses and help control for these various influences (which medical experts call

“confounders”) is through investiga- tion of contempo- rary skeletal collec- tions where age and sex are known.*

Research of this kind has helped to standardize meth- ods, test specific hypotheses, and demonstrate that the underlying bio- logical influences on muscle attach- ment sites are com- plex (Alves Cardoso and Henderson, 2010; Milella et al., 2012; Jurmain et al., 2012).

Study of bone geometry is the third method that can potentially shed light on prehistoric activities. This approach has tended to be more biomedically oriented than the others discussed so far and has also been more successful in testing hypotheses. In particular, a study of student athletes at Cambridge University compared with a set of non- athletes provided strong confirmation that certain types of very strenuous activities can alter bone geometry (that is, the shape and strength of the bone) (Shaw and Stock, 2009a, b).

Reconstructing Prehistoric Diets Skel- etal biologists also study prehistoric diets. In the last several years chemical techniques have been developed that provide good information about what people were eating in the past. Stable isotope analysis has proven to be a very useful way to reconstruct the diets of ancient humans and has become wide- ly used. As discussed in Chapter 9, stable isotopes are different versions

*Such collections can be found in museums in the United States (for example, at the Smithsonian Institution), Portugal, and Italy. These skeletons sometimes come from individuals whose bodies were unclaimed or from cemeteries that, by law, were required to be excavated.

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The innovations in genetic research that allow researchers to examine SNPs in specific genes have facilitated the discovery of mutations that have spread in some human populations because they are advanta- geous in certain environments. As we discussed, one such mutation enables Tibetans to live at extremely high elevations while producing approximately the same amount of hemoglobin as seen in people living at sea level. This is advantageous because increased lev- els of hemoglobin, while adaptive at high elevations, do expose people to certain, potentially life-threatening conditions. Thus, there are other, as yet undiscovered mechanisms that have enabled highland Tibetans to

adapt to the extreme conditions of life at high altitude. While these mechanisms are unknown at present, it is likely that they will be identified through genetic research in the relatively near future.

Other recently discovered genetic mutations influ- ence the amount of melanin that cells produce, and natural selection has favored some of these mutations in northern latitudes. Such discoveries have provided a much greater understanding of human adaptive responses just within the past 20 years. As biologists continue to find more such mutations, our under- standing of how human phenotypic variation came about will continue to develop.

How Do We Know?

of the same element that vary in their structure (that is, in their atomic weight). For example, carbon has two stable isotopes, ¹³C and ¹²C, which dif- fer in atomic weight. Humans incorpo- rate different amounts of these isotopes into their tissues from foods that vary in isotopic composition. Stable isotopes in teeth specifically record childhood diet, and they do not change after they are formed; in adults, isotopic analysis of the organic and mineral content of bone provides a record of diet over the last several years of life.

Stable carbon and nitrogen isotope analyses of human bone provide the most information about diet. Carbon isotope ratios in plants vary based on one of three possible chemical path- ways; these ratios are incorporated into the bones and teeth of the people who ate these foods. In addition, marine organisms (for example, fish and sea mammals) have isotope ratios that dif- fer from those of most terrestrial plants and animals. Stable nitrogen isotope

ratios provide another source of infor- mation on diet. Plants typically have the lowest nitrogen isotope ratios, and these ratios increase in animals at each higher level in the food chain. Analysis of carbon and nitrogen isotopes togeth- er helps not only to identify the source of food (for example, marine or terres- trial), but can also indicate the gener- al position of human societies within a local food web.

For example, stable carbon and nitrogen isotope analysis has revealed that early prehistoric Native Americans from the San Francisco Bay area ate significant amounts of salmon and marine mammals, which are near the top of the food chain. However, later in time, bone isotope ratios record a change in diet toward greater con- sumption of land animals and plant foods (for example, deer and acorns). These changes in diet may reflect increasing resource stress associated with population growth in the region (Bartelink, 2009).

439Media Resources

▶▶ Humans have adapted to countless environmen- tal challenges as they evolved and migrated out of Africa to eventually inhabit most of the planet.

▶▶ Variation in skin color has enormous adaptive value in response to conflicting selective pres- sures, all having to do with ultraviolet (UV) radi- ation. Heavily pigmented skin is adaptive in the tropics because it provides protection from UV radiation, which can cause skin cancer and also degrade the B vitamin folate.

▶▶ As people moved away from the tropics, dark skin became disadvantageous because a decrease in sunlight meant insufficient exposure to UV radi- ation for the adequate production of vitamin D. This is important because vitamin D is essential for the proper mineralization of bone and insuf- ficient amounts of vitamin D causes rickets in children.

▶▶ Two genes (MC1R and SCL24A5) have been par- ticularly (but not exclusively) responsible for the geographical patterning of human skin color. Mutations in these genes that prevent the pro- duction of melanin are common in popula- tions outside the tropics and natural selection has increased the frequency of these mutations because it is advantageous to have less pigmented

skin in regions where exposure to solar radiation is reduced.

▶▶ Natural selection favoring several genetic muta- tions has allowed Tibetan highlanders to adapt to extremely high altitudes. There has been espe- cially rapid and strong selection favoring a particu- lar SNP that permits them to retain red cell counts that are normal for sea-level residents.

▶▶ Infectious disease has also played a critical role in human evolution, and the frequencies of cer- tain alleles have changed in various populations in response to diseases such as malaria.

▶▶ Cultural innovations and contact with nonhu- man animals have altered disease patterns and have increased the spread of infectious diseases. Examples of this type of spread are HIV/AIDS and malaria.

▶▶ We humans are still coping with infectious disease as we alter the environment and as global climate change facilitates the spread of disease vectors. Certainly without cultural adaptations, our species never would have left the tropics. But as in the case of sickle-cell anemia, HIV, and many bacterial dis- eases, some of our cultural innovations themselves have become selective agents.

Summary of Main Topics

1. If a friend of yours said that skin color is a valu- able tool to use in classifying humans, how would you explain that variations in human pigmenta- tion are the result of natural selection in different environments?

2. Why is less pigmented skin advantageous in northern latitudes? There is now evidence that at least some Neandertals who lived in northern Europe also had reduced melanin compared to populations in Africa. What is this evidence?

3. Why is HIV considered to be a zoonotic disease?

4. How has infectious disease played an important role in human evolution? Do you think it plays a current role in human adaptation? How have human cultural practices influenced the patterns of infectious disease seen today? List as many examples as you can, including some not discussed in this chapter.

5. What are the major kinds of pathological condi- tions paleopathologists study in skeletons from archaeological sites?

Critical Thinking Questions

Video See the video “Infectious Disease” to learn more

about topics covered in this chapter.

Media Resources

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Human development and adaptation is best under-

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Through natural selec- tion, humans have and

continue to adapt to environmental factors.

Humans have recently become disconnected from

other life and are rapidly altering the planet.

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After mastering the material in this chapter, you should be able to:

▶ �Compare the environmental conditions under which humans evolved with the environments in which we live today.

▶ �Explain the proposal that the human biology that evolved under dietary conditions of the past may be mismatched with the foods we consume today, resulting in a number of diseases and disorders such as hypertension, diabetes, and obesity.

▶ �Compare infancy and puberty as hypothesized for our ancestors with those life-cycle stages of modern humans and discuss what may result from the mismatches.

▶ �Discuss three proposals for why humans age.

▶ �Consider whether our evolved biology helps us to meet the challenges of the modern twenty-first-century world.

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In previous chapters, we saw that modern humans are a highly gen-eralized species. This means that we can live in a great variety of cli- mates, eat a wide variety of foods, and respond to most environmental chal- lenges in myriad ways. For example, as human populations moved into cold northern climates, they were able to respond both physiologically and behaviorally to the environmental challenges they faced. As noted pre- viously, adaptations to cold include physiological responses to conserve or increase heat, such as vasoconstriction of the capillaries, increased metabolic rate, and shivering. Considering these responses from an evolutionary per- spective, we can assume that, among the earliest human populations inhab- iting cold regions of the world, those individuals who had genotypes and phenotypes enabling them to respond physiologically had more surviving offspring to pass along these char- acteristics. Behavioral and cultural adaptations to cold climates probably included fire, house structures, warm clothing, and hunting for foods that provided energy to withstand the cold. In these examples we see evidence of human adaptations to cold that are both biological and cultural and are rooted in evolution.

A concern we have today, howev- er, is that the environments inhabited

16 Legacies of Human Evolutionary History and the Human Life Course

by humans are changing at rates far exceeding those experienced by pre- vious generations. In fact, the human environment has changed more radi- cally in the last few decades than it has at any point in the entire course of human evolutionary history. What are the consequences of these tremendous changes, some of which you have seen in your own lifetime? In this chap- ter and the next, we’ll explore ways in which the legacies of human evolution continue to have profound impacts on our biology and behavior throughout our lives and on the planet we inhab- it even in the face of ever-increasing rates of cultural and technological change.

Student Learning Objectives

chapter 16 Legacies of Human Evolutionary History and the Human Life Course 442

Evolved Biology and Contemporary Lifestyles—Is There a Mismatch?

A frequently expressed concern today is that our evolved biology may not be well matched with our con- temporary lives, thus resulting in poor- er health and shorter lives than those of even our recent ancestors. This is referred to variously as a mismatch or discordance. Reflecting the “connec- tions” theme of this book, we will pro- pose that our modern lives are in some ways disconnected from our evolved biology, with occasional harmful con- sequences. There are some who argue that if we could only return to the ways of living of our ancestors (“Stone-Age lives”), we would all become healthier. Certainly there are aspects of ances- tral ways of life that, if adopted, would probably result in improved health (e.g., exercise and dietary changes); but with more than 7 billion people liv- ing on earth, a “return” to lifestyles like those of our ancestors is highly unlike- ly (Fig. 16-1).

For most of human history, individ- uals were born and grew up in environ- ments not very different from those of their parents and grandparents. They faced few challenges in their lives that required significant cultural or bio- logical adaptations. With the origin of food production approximately 10,000 years ago, however, the pace of cul- tural change began to speed up. Of course biological evolution didn’t cease 10,000 years ago, but since that time there has been a veritable explosion of culture and technology, whereas bio- logical change has been relatively slow (Pritchard, 2010). With so many chang- es occurring within single lifetimes, many people are stressed to their lim- its to adapt physically, emotionally, and materially. How far can our flexible and generalized biology take us in this rap- idly changing world? These are some

of the questions we will explore in this chapter as we consider ways in which culture interacts with biology through- out the life course and in our everyday lives as well as the ways in which this interaction sometimes provides chal- lenges to our health and lifestyles.

Biocultural Evolution and the Life Course

A good place to explore the inter-action of biology and culture and potential mismatches is the human life course. If we consider how a human develops from an embryo into an adult and examine the forces that operate on that process, we will have a better per- spective of how both biology and cul- ture influence our lives and how our evolutionary history creates opportu- nities and sets limitations.

Of course, cultural factors interact with genetically based biological char- acteristics to widely varying degrees; these variable interactions influence how characteristics are expressed in individuals. Some genetically based characteristics will be exhibited no matter what the cultural context of a person’s life happens to be. If a woman inherits two alleles for albinism, for example, she will be deficient in the production of the pigment melanin, resulting in light-colored skin, hair, and eyes. This phenotype will emerge regardless of the woman’s cultural environment. Likewise, the sex-linked trait for hemophilia will be exhibited by all males who inherit it no matter where they live.

Other characteristics—such as intelligence, body shape, and growth— reflect the interaction of environment and genes. We know, for example, that each of us is born with a genetic make- up that influences the maximum stat- ure we can achieve in adulthood. But to reach that maximum stature, we must be properly nourished during growth (including during fetal development), and we must avoid many childhood

From Embryo to Adult: Human Growth and Development Today and in the Past 443

diseases and other stresses that inhib- it growth. What factors determine whether we are well fed and receive good medical care? In the United States, socioeconomic status is prob- ably the primary factor that determines nutrition and health. Socioeconomic status is thus an example of a cultur- al factor that affects growth. But in another culture, diet and health sta- tus might be influenced by wheth- er the individual is male or female. In some cultures, males receive the best care in infancy and childhood and are thus often larger and healthier as adults than are females (Fig. 16-2). If there’s a cultural value on slimness in women, young girls may try to restrict their food intake in ways that affect their growth; but if the culture values plumpness, the effect on diet in ado- lescence will likely be different. These are all examples of how cultural values affect growth and development.

From Embryo to Adult: Human Growth and Development Today and in the Past

In humans, growth begins at concep-tion and continues until the late teens or early 20s. Typically, well- nourished humans grow fairly rapidly during the first two trimesters (6 months) of fetal development, but growth slows dur- ing the third trimester. After birth, growth rates increase and remain

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fairly rapid for about 4 years, at which time they decrease again to rela- tively slow, steady levels, which are maintained until puberty. At puber- ty, there’s another very pronounced increase in growth. During this so-called adolescent growth spurt, West- ern teenagers typically grow around 4 inches per year. Following the ado- lescent growth spurt, the rate of growth declines again and remains slow- er until adult stature is achieved by the late teens (Fig. 16-3).

Growth curves for boys and girls are signifi- cantly different, with the adolescent growth spurt occurring approximate- ly 2 years earlier in girls

than in boys. At birth, there’s slight sexual dimorphism in many body mea- sures (for example, height, weight, head circumference, and body fat), but the major divergence in these characteris- tics doesn’t occur until puberty.

The head is a relatively large part of the body at birth. The continued growth of the brain after birth occurs at a rate far greater than that of any other part of the body with the excep- tion of the eyeball. At birth, the human brain is about 25 percent of its adult size. By 6 months of age, the brain has doubled in size, reaching 50 percent of adult size. It reaches 75 percent of adult size at age 2½ years, 90 percent by age 5, and 95 percent by age 10. There’s only a very small spurt in brain growth at adolescence, making the brain an exception to the growth curves char- acteristic of most other parts of the body. As we’ll see later in this chapter, this pattern of brain growth, including the relatively small amount of growth before birth, is unusual among pri- mates and other mammals. By con- trast, the typical picture for most

mammalian species is that at least 50 percent of adult brain size has been attained prior to birth. For humans, however, the narrow pelvis necessary for walking bipedally imposes limits on the size of the neonatal head that can be delivered through it (Rosenberg and Trevathan, 2001). That limitation, in addition to the value of having most brain growth occur in the more stimu- lating environment outside the womb, has caused human infants to be born with far less of their total adult brain size than most other mammals.

Nutritional Effects on Growth, Development, and Later-Life Health Nutrition has an impact on human growth at every stage of the life cycle, and few aspects of the human envi- ronment have changed as much in the last 10,000 years as diet. It is there- fore not surprising that there have also been changes in growth rates and out- comes. During pregnancy, for exam- ple, a woman’s diet can have a profound effect on the development of her fetus and the eventual health of the child. Moreover, the effects are transgenera- tional, because a woman’s own supply of eggs is developed during her own fetal development. So if a woman is malnourished during pregnancy, the eggs that develop in her female fetus may be damaged in a way that affects her future grandchildren’s health. And even if a baby girl whose mother was malnourished during pregnancy is well nourished from birth on (as often happens in adoptions), her growth, health, and future pregnancies appear to be compromised—a legacy that may extend for several generations (Kuza- wa, 2005). Furthermore, nutrition- al stress during pregnancy common- ly results in low-birth-weight babies, which are at great risk for develop- ing hypertension, cardiovascular dis- ease, and diabetes later in life (Barker, 1994; Gluckman and Hanson, 2005). Low-birth-weight babies are particu-

▲ Figure 16.2 This is a mother with her twin children. The one on the left is a boy and is breast-fed. The girl, on the right, is bottle-fed. This illustrates both differential treatment of boys and girls in many societies and the potential negative effects of bottle feeding for people with few resources.

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From Embryo to Adult: Human Growth and Development Today and in the Past 445

larly at risk if they are born into a world of abundant food resources (especially cheap fast food) and gain weight rap- idly in childhood (Kuzawa, 2005, 2008). These findings have clear implications for public health efforts that attempt to provide adequate nutritional support to pregnant women and infants through- out the world.

Nutrients needed for growth, devel- opment, and body maintenance include proteins, carbohydrates, lipids (fats), vitamins, and minerals. The specific amount that we need of each of these nutrients coevolved with the types of foods that were available to our ances- tors throughout our evolutionary his- tory. For example, the specific pat- tern of amino acids required in human nutrition (the essential amino acids) reflects an ancestral diet high in ani-

mal protein. We share with many other primates a dependence on dietary sources of organic nutrients such as vitamin C, reflecting a long history of consumption of fruits and other plant parts. In other words, our need for vita- min C coevolved with a diet high in that nutrient. Unfortunately for mod- ern humans, these coevolved nutrition- al requirements are often incompatible with the foods that are available and typically consumed today. To under- stand this mismatch of our nutritional needs and contemporary diets, we need to examine the impact of agriculture on human evolutionary history.

The preagricultural diet, basically encompassing the entirety of our evo- lutionary history prior to 10,000 years ago, was typically high in animal pro- tein, but it was probably low in fats,

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essential amino acids the 9 (of 22) amino acids that must be obtained from the food we eat because they are not syn- thesized in the body in sufficient amounts.

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nutrients. Human nutritional requirements coevolved with the foods consumed during the long period of human evolutionary history before agriculture, resulting in a mismatch between what we need to eat today and the composition of contemporary diets.

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From Embryo to Adult: Human Growth and Development Today and in the Past 447

particularly saturated fats. That diet was also most likely high in complex carbohydrates (including fiber), low in salt, and high in calcium. We don’t need to be reminded that the contem- porary diet typifying many industri- alized societies has the opposite con- figuration of the one just described. It’s high in saturated fats and salt and low in complex carbohydrates, fiber, and calcium (Fig. 16-4). There’s very good evidence that many of today’s diseases in industrialized countries are related to the lack of fit between our diet today and the one with which we evolved (Gluckman et al., 2009).

Along with agriculture and ani- mal domestication came a number of “new” food types that are important and common today but were rare or nonexistent in ancestral diets. Two examples include dairy products and cereal grains. In a previous chapter we discussed the difficulty that some people have digesting dairy products because they lack the enzyme neces- sary for breaking down the milk sugar lactose. Others have difficulty digest- ing the gluten found in some cereal grains, most commonly wheat and its close relatives. Both lactose intoler- ance and gluten intolerance are more common in populations that have only

recently adopted milk products and cereal grains into their diets (Wiley, 2008). The introduction of cattle and grains into early agricultural popula- tions may have increased food avail- ability for many people, but for some people, specific foods that were not part of their ancestral diets are mis- matched with their bodies in ways that lead to diarrhea and gastrointes- tinal upset. Unfortunately, food aid programs originating in parts of the world where milk and grains are sta- ples sometimes have negative impacts on the malnourished populations that they target.

Although we might reasonably expect that nutrition and health would have improved with the development of agriculture, human health actual- ly declined in most parts of the world beginning about 10,000 years ago. Some have referred to the changing patterns of disease that occurred with the devel- opment of agriculture as an “epidemio- logical transition,” marked by the rise of infectious and nutritional deficiency diseases. In many places, skeletal signs of malnutrition (for example, iron- deficiency anemia) (Fig. 16-5) appear for the first time with domesticated crops like corn (Cohen and Armelagos, 1984; Larsen, 2002). Life expectancy

◀�Figure 16.5 Bone changes to the eye orbits that likely indicate anemia caused by vitamin deficiency or per- haps iron deficiency. Other conditions can also cause these bone changes.

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also appears to have dropped. Clark Larsen refers to the adoption of agri- culture as an “environmental catastro- phe” (Larsen, 2006), and Jared Diamond has called it the worst mistake humans ever made (Diamond, 1987). But wheth- er for better or worse, we’re stuck with agriculture as a way of acquiring food because without agriculture the plan- et couldn’t possibly support the billions that live on it today.

It’s clear that both deficiencies and excesses of nutrients can cause health problems and interfere with childhood growth. Certainly many people in all parts of the world, both industrial- ized and developing, suffer from inad- equate supplies of food of any qual- ity. We read daily of thousands dying

from starvation due to drought, war- fare, or political instability. The blame must be placed not only on the nar- rowed food base that resulted from the emergence of agriculture but also on the increase in human population that occurred when people began settling in permanent villages and having more children. Today, the crush of billions of humans almost completely depen- dent on cereal grains (Cordain, 1999) means that millions face undernu- trition, malnutrition, and even star- vation. Even with these huge popula- tions, however, food scarcity may not be as big a problem as food inequality. In other words, there may be enough food produced for all the people on earth, but economic and political forc-

Diabetes

Perhaps no disorder is as clearly linked with dietary and lifestyle behaviors as diabetes. There are actually two differ- ent diseases referred to as diabetes. One, the less common, is type 1 diabetes, also called insulin-dependent diabetes mellitus (IDDM), or juvenile-onset diabetes, which occurs when the immune system interferes with the body’s ability to produce the insulin that converts sugars (glucose) to energy. This type of diabetes is usually first rec- ognized in childhood and requires lifelong insulin injections to avoid cell damage and death. It’s unlikely that children with type 1 diabetes lived very long in the past. Type 2 diabetes, also called noninsulin-dependent diabetes mellitus (NIDDM), is far more common today and has to do with the way insulin is used in the body. Sometimes this is described as “insulin resistance” in that sufficient insulin may be produced but the cells are not able to utilize it. This inabil- ity results in a buildup of glucose in the bloodstream that can cause a number of

complications of the cardiovascular system, kidneys, and nervous system. If it is not treated—usually with dietary changes, weight control, and exercise—type 2 dia- betes can also result in early death.

A few years ago, type 2 diabetes was something that happened to older people living primarily in the developed world. Sadly, this is no longer true. The World Dia- betes Foundation estimates that 80 percent of the new cases of type 2 diabetes that appear between now and 2025 will be seen in developing nations, and the World Health Organization (WHO) predicts that more than 70 percent of all diabetes cases in the world will be in developing nations in 2025. Furthermore, type 2 diabetes is now seen in children as young as 4 years of age (Pavkov et al., 2006), and the mean age of diagnosis in the United States dropped from 52 to 46 between 1988 and 2000 (Koopman et al., 2005). In fact, it is likely that almost everyone reading this book has a friend or family member who has diabetes. What’s happened to make this former “disease of old age” and “disease of civilization” reach what some have described as epidemic proportions?

Although there appears to be a genetic link (type 2 diabetes tends to run in fami- lies), most fingers point to lifestyle factors. Two lifestyle factors that have been impli- cated in this epidemic are poor diet and inadequate exercise. Noting that our current diets and activity levels are very different from those of our ancestors, proponents of evolutionary medicine suggest that diabetes is the price we pay for consum- ing excessive sugars and other refined carbohydrates while spending our days in front of the TV set or computer monitor. The reason that the incidence of diabetes is increasing in developing nations is that these bad habits are spreading to those nations. In fact, we may soon see what can be called an “epidemiological collision” in countries such as Zimbabwe, Ecuador, and Haiti, where malnutrition and infectious diseases are rampant but obesity is on the rise, so that people are dying not only from diseases of poverty but also from those more characteristic of wealthier populations (Trevathan, 2010).

A Closer Look

evolutionary medicine The appli- cation of principles of evolution to aspects of medical research and practice.

undernutrition A diet insufficient in quantity (calories) to support normal health.

malnutrition A diet insufficient in quality (i.e., lacking some essential compo- nent) to support normal health.

From Embryo to Adult: Human Growth and Development Today and in the Past 449

es keep it from reaching those who need it most. Of increasing concern are the effects of globalization (includ- ing liberalization of trade and agri- cultural policies) on food security, especially in developing nations, and what has become known as the Global South. In particular, the adoption of Western diets and lifestyles has con- tributed to declining health in much of the world (Young, 2004).

Thirty years ago, the primary focus of international health and nutrition organizations, including the WHO, was undernutrtion and infectious diseases (Prentice, 2006). Today, more and more attention is focused on overnutrition and the diseases and disorders associ- ated with obesity. By 2006, the num- ber of people in the world who were overweight exceeded the number who were malnourished and underweight (Popkin, 2007). In many countries, including the United States, more than half of the population are overweight or obese; Mexico has the highest rate, at almost 70%, with the United States not

far behind (to see obesity trends in the United States, visit the website http:// www.cdc.gov/obesity/data/trends.html). Clearly diets for many people are mis- matched with the nutrients required for healthy bodies.

In summary, our nutritional adapta- tions were shaped in environments that included times of scarcity alternating with times of abundance. The variety of foods consumed was so great that nutritional deficiency diseases were rare. Small amounts of animal foods were probably an important part of the diet in many parts of the world. In northern latitudes, after about 1 mya, meat was an important part of the diet. But because meat from wild animals is low in saturated fats, the negative effects of high meat intake that we see today were rare. Our diet today is often incompatible with the adaptations that evolved in the millions of years pre- ceding the development of agriculture. The consequences of that incompat- ibility include both starvation and obe- sity (Fig. 16-6).

Diet, Lifestyle, and Consequences

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Other Factors Affecting Growth and Development: Genes, Environment, and Hormones Genetic factors set the underlying lim- itations and potentialities for growth and development, but the life experi- ences and environment of the organ- ism determine how the body will grow within those parameters. In fact, there is increasing evidence that environ- mental factors can change the ways in which genes are expressed without having an effect on the genes them- selves, and that people with identi- cal genotypes (i.e., identical twins) could have very different phenotypes. In other words, identical twins aren’t really identical, and they become even more different as they age (Fraga et al., 2005; Gluckman et al., 2009). Pheno- typic differences emerge in identical twins because of the “software” that provides instructions to the unfold- ing genotype. These instructions are known as the epigenome; they are responsible for turning some genes on and some genes off. All of the cells in our body except the sex cells have the same genes, but they do different things because of the epigenome. In

different individuals, the epigenome may turn off some genes or turn on others, resulting in different pheno- types. This is one of the main ways in which the environment interacts with genes, and it helps to explain why one member of a pair of identical twins may suffer from a genetically based cancer while the other is disease-free. Lifestyle factors are particularly impor- tant influences on the epigenome, especially diet and smoking.

The ongoing “nature‒nurture debate” has pitted genetic factors against environmental factors in deter- mining how an individual grows, devel- ops, and behaves. The field of epi- genetics helps to resolve this conflict by revealing that structural changes to DNA and associated proteins (with- out causing changes in the nucleotide sequence) can underlie gene expres- sion. The changes are transmitted through mitosis, so that when they are established during development, they persist with further cell division. In this way, environmental factors (such as smoke or air pollution) can bring about changes during development that affect a person in adulthood, partially explaining differences in disease risk (Fig. 16-7). Although these changes in gene expression are not usually passed

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◀�Figure 16-6 Some people suffer from an overabundance of food (left), while others suffer from tragically insufficient amounts of food.

epigenome the instructions that determine which genes are expressed in cells and how.

epigenetics changes in pheno- type that are not related to changes in underlying DNa.

From Embryo to Adult: Human Growth and Development Today and in the Past 451

on to offspring, there is increasing evi- dence of epigenetic inheritance that transcends generations (Whitelaw and Whitelaw, 2006). Certainly, research in epigenetics calls into question the whole idea of genetic determinism for many traits.

One of the primary ways in which genes have an effect on growth and development is through their effects on hormones. Hormones are sub- stances produced in one cell that have an effect on another cell. Most hor- mones are produced by endocrine glands and are transported to other cells in the bloodstream; virtually all have an effect on growth. Just above the roof of your mouth are two of the most important organs related to hor- mone action: the hypothalamus and the pituitary gland. They are connect- ed to each other and are in almost con- stant communication. The hypothala- mus has been described as the central command center or relay station for all kinds of actions going on in the body. The pituitary, on the other hand, is the primary regulator of hormonal interactions related to reproduction, growth, and development. The hypo- thalamus “tells” the pituitary what to do based on input it receives from throughout the body and brain. There

are two parts of the pituitary, the ante- rior and the posterior. The anterior pituitary produces hormones that reg- ulate reproduction (follicle- stimulating hormone [FSH] and luteinizing hor- mone [LH]), milk production (pro- lactin), metabolism (adrenocortico- tropic hormone [ACTH]), and growth (growth hormone [GH]). The posteri- or pituitary secretes several hormones that, in turn, act on the gonads (ova- ries and testes) and the thyroid, adre- nal, and mammary glands.

We can use the hormone thyrox- ine, produced by the thyroid gland in the neck, to illustrate the action of hormones and the communica- tion system among the endocrine glands (Fig. 16-8). Thyroxine regu- lates metabolism and aids in body heat production. When thyroxine levels fall too low for normal metabolism, the brain senses this and sends a mes- sage to the hypothalamus. The hypo- thalamus reacts by releasing thyrotro- pin-releasing hormone (TRH), which goes to the anterior pituitary, where it stimulates the release of thyroid- stimulating hormone (TSH). TSH then goes to the thyroid gland, stim- ulating it to release thyroxine. When the brain senses that the levels of thy- roxine are adequate, it sends signals

◀�Figure 16.7 The severe stress that often accompanies poverty can have an epigenetic effect on gene expres- sion for some diseases and disorders.

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chapter 16 Legacies of Human Evolutionary History and the Human Life Course 452

relatively short adult stature of these people (Shea and Bailey, 1996), pro- viding another example of epigenetics and the interaction of biological and cultural forces. More recent research suggests that their short stature may be due to decreased expression of the receptors for growth hormone and that epigenetic factors such as diet could play a role in modifying how genes are expressed in both African and Philippine pygmies (Dávila et al., 2002; Bozzola et al., 2009).

Another hormone that influences growth and development is cortisol, which is elevated during stress. Up to a point, cortisol elevation is adaptive, but if the response is prolonged or severe, there appear to be negative effects on health and behavior (Flinn, 1999; Flinn and England, 2003). Under conditions of chronic emotional and psychosocial stress, cortisol levels may remain high and suppress normal immune func- tion. This means that a child living in a stressful situation is more vulnerable to infectious diseases and may expe- rience periods of slowed growth if the stress is prolonged. A reasonable argu- ment could be made that people today of all ages and in all parts of the world experience significantly higher levels of

that inhibit the further release of TRH and TSH. In many ways, this pro- cess is similar to what your house- hold thermostat does: When it senses that the temperature has dropped too low for comfort, it sends a message to the heating system to begin produc- ing more heat; when the temperature reaches or exceeds the preset level, the thermostat sends another message to turn the heat off.

Two other hormones that are important in growth include insulin and GH, already mentioned. Insulin, produced by the pancreas, regu- lates the use of glucose in the body, as noted in our discussion of diabetes. GH, secreted by the anterior pituitary, promotes growth and has an effect on just about every cell in the body. Tumors and other disorders can result in excessive or insufficient amounts of growth hormone secretion, which in turn can result in gigantism or dwarf- ism. Short stature is not always due to pathology, however. One group of people who have notably short stature are African Efe pygmies (Fig. 16-9). There is evidence that altered levels of growth hormone and its controlling factors interact with nutritional factors and infectious diseases to produce the

Hypothalamus

TRH

Pituitary

TSH

Thyroid

Feedback loop

Thyroxine

▲�Figure 16-8 Example of a feed- back loop. When thyroxine levels in the blood fall too low, the hypothala- mus releases thyrotropin-releasing hormone (TRG), which goes to the anterior pituitary, triggering the release of thyroid-stimulating hormone (TSH). TSH causes thyroxine to be released from the thyroid gland. Release of TRH and TSH is then inhibited.

▶�Figure 16-9 Charles Knowles of the Wildlife Conservation Network stands beside three Mbuti (Efe) staff members of the Okapi Conservation Project.

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stress than our ancestors did, suggest- ing that effects on growth may also be different. This is not to imply that our ancestors didn’t experience stress (few things are more stressful than a lion chasing you and your children), but the sources and duration of stressors were probably very different from those we experience today.

The levels of reproductive hor- mones in women from health-rich nations appear to be elevated over what is reported for women in tradi- tional societies and what was probably the ancestral profile (Vitzthum, 2009) (Fig. 16-10). Furthermore, women who use contraception, have few or no chil- dren, and breast-feed for only a few months have repeated menstrual cycles and the associated high levels of estro- gen for the majority of their reproduc- tive lives. This is a very different hor- monal profile from ancestral women, who spent most of their adult years either pregnant or nursing infants, yielding very few menstrual cycles. This disconnect between today’s hor- monal profiles and those of our ances- tors may result in a higher incidence of reproductive cancers, especially when coupled with high-fat diets and low lev- els of exercise (Trevathan, 2010).

Life History Theory and the Human Life Course

As noted in earlier chapters, pri-matologists and other physi- cal anthropologists view primate and human growth and development from an evolutionary perspective, with an interest in how natural selection has operated on the life cycle from concep- tion to death—a perspective known as life history theory. Why, for example, do humans have longer periods of infan- cy and childhood compared with other primates (Fig. 16-11)? What accounts for differences seen in the life cycles of such closely related species as humans and chimpanzees? Life history research seeks to answer such questions (e.g., Mace, 2000; Hawkes and Paine, 2006).

Life history theory allows us to pre- dict the timing of reproduction under favorable circumstances. It begins with the premise that there’s only a cer- tain amount of energy available to an organism for growth, maintenance of life, and reproduction. Energy invest- ed in one of these processes isn’t avail- able to another. Thus the entire life

◀ Figure 16-10 Hormonal variation in three populations. (Redrawn from Ellison, 1994.)

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course represents a series of trade-offs among various life history traits, such as length of gestation, age at wean- ing, time spent in growth to adult- hood, adult body size, and length of life span. For example, life history theo- ry provides the basis for understand- ing how fast an organism will grow and to what size, how many offspring can be produced, how long gestation will last, and how long an individual will live. Crucial to understanding life history theory is its link to the evolu- tionary process: It’s the action of nat- ural selection that shapes life histo- ry traits, determining which ones will succeed or fail in a given environment. Although it isn’t clear if life history theory works in contemporary human populations (Strassman and Gillespie, 2002), it serves as a useful guide for examining the various life cycle phas- es from evolutionary and ecological perspectives.

Most life cycle stages are well marked by biological transitions, such as those that occur at birth and puber- ty. Biological markers associated with life cycle changes are similar among higher primates, but for humans there’s an added complexity: They occur in cultural contexts that define and char- acterize them. Puberty, for example,

has very different meanings in differ- ent cultures. A girl’s first menstrua- tion (menarche) is often marked with ritual and celebration, and a change in social status typically occurs with this biological transition. Likewise, meno- pause is often associated with a rise in status for women in non-Western societies, whereas it’s commonly seen as a negative transition for women in many Western societies. As we shall see, collective and individual attitudes toward these life cycle transitions have an effect on growth, development, and health.

Pregnancy, Birth, Infancy, and Childhood The biological aspects of concep- tion and gestation can be discussed in a fairly straightforward way, draw- ing from what is now known about reproductive biology: A sperm fertil- izes an egg; the resulting zygote trav- els through a uterine (fallopian) tube to become implanted in the uterine lin- ing; and the embryo develops until it’s mature enough to survive outside the womb, at which time birth occurs. But this is clearly not all there is to human pregnancy and birth. Female biology

Adult phase

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▲�Figure 16-11 Primate life-cycle stages.

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menopause the end of menstrua- tion in women, usually occurring at around age 50.

Life History Theory and the Human Life Course 455

may be similar the world over, but cul- tural rules and practices are the prima- ry determinants of who will get preg- nant as well as when, where, how, and by whom.

Once a pregnancy has begun, there’s much variation in how a woman should behave, what she should eat, where she should and should not go, and how she should interact with other people. Almost every culture known, including our own, imposes dietary restrictions on pregnant women. Many of these appear to serve an important biologi- cal function, particularly that of keep- ing the woman from ingesting toxins that would be dangerous for the fetus. Alcohol is a good example of a poten- tial toxin whose consumption in preg- nancy is discouraged in the United States (Fig. 16-12). The food aver- sions to coffee, alcohol, and other bitter substances that many women experi- ence during pregnancy may be evolved adaptations to protect the embryo from toxins. The nausea of early preg- nancy may also function to limit the intake of foods potentially harmful to the embryo at a critical stage of devel- opment (Profet, 1988; Williams and Nesse 1991; but see Pike, 2000).

As noted above, there is increas- ing evidence that what happens dur- ing prenatal development has life- long consequences, many of which are irreversible. Scholars of fetal origins research propose that conditions dur- ing pregnancy affect such factors as disease susceptibility and metabolism (Kuzawa, 2008); some go even further to suggest that prenatal factors can affect intelligence and temperament as well (Paul, 2010). With evidence that stress, emotions, and pollution, in addi- tion to food and drink, have effects on a developing fetus, the old adage of “eat- ing for two” during pregnancy can be expanded to “living for two.” Given the effects on metabolism, it may be that pregnancy is the best place on which to focus efforts to curb the worldwide ris- ing obesity rates.

Birth is an event that’s celebrat- ed with ritual in almost every cul-

ture that has been studied. In fact, the relatively little fanfare associated with childbirth in the United States is unusual by world standards. Because the risk of death for both mother and child is so great at birth, it’s not sur- prising that it’s surrounded with ritu- al significance. Perhaps because of the high risk of death, we tend to think that birth is far more difficult for humans than it is for other mammals. But since almost all primate infants have large heads relative to body size, birth is challenging for many primates (Fig. 16-13).

As noted above, the human brain is far less developed at birth than it is in other primates. For a species as depen- dent on learning for survival as we are, it may be adaptive for most of our brain growth to take place in the presence of environmental stimuli rather than in the relatively unstimulating environ- ment of the uterus. This may be partic- ularly true for a species dependent on language. The language centers of the brain develop in the first 3 years of life, when the brain is undergoing its rapid expansion; these 3 years are considered a critical period for the development of language in the human child.

◀�Figure 16-12 Alcohol consump- tion in pregnancy is discouraged in many countries, including the United States.

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Infancy, as we noted, is the period of nursing; it typically lasts 2 to 3 years in humans. When we consider how unusual it is for a mother to breast-feed her child for even a year in the United States or Canada, this figure may sur- prise us. But considering that 2 to 4 years of breast-feeding is the norm for chimpanzees, gorillas, orangutans, and women in foraging societies, most anthropologists conclude that 2 to 3 years was the norm for most humans in the evolutionary past (Stuart- Macadam and Dettwyler, 1995). Other lines of evidence confirm this pattern, including the lack of other foods that infants could consume until the ori- gin of agriculture and the domesti- cation of milk- producing animals. In fact, if the mother died during child- birth in preagricultural populations, it’s very likely that the child would die also unless there was another woman

available who could nurse the child. Jane Goodall has noted that this is also true for chimpanzees: Infants who are orphaned before they are weaned do not usually survive. Even those orphaned after weaning, assuming they survive the trauma, are still emo- tionally dependent on their mothers and exhibit clinical signs of depres- sion for a few months or years after the mother’s death (Goodall, 1986).

Human milk, like that of other pri- mates, is extremely low in fats and pro- tein. Such a low nutrient content is typ- ical for species in which mothers are seldom or never separated from their infants and nurse in short, frequent bouts. Not coincidentally, prolonged, frequent nursing suppresses ovula- tion in marginally nourished women (Konner and Worthman, 1980), espe- cially when coupled with high activity levels and few calorie reserves (Ellison,

Spider monkey Proboscis monkey Macaque monkey

Gibbon Chimpanzee Human

Mother’s pelvis

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▶�Figure 16-13 The relationship between the average diameter of the birth canal of adult females and average head length and breadth of newborns of the same species. (After Jolly, 1985.)

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2001). Under these circumstanc- es, breast-feeding can help maintain a 4-year birth interval during which infants have no nutritional competition from siblings. Thus nursing served as a natural birth control mechanism in the evolutionary past, as it does in some populations today.

The fact that infants born today can survive and grow without breast milk is further evidence of our species’ flex- ibility and how cultural mechanisms have enabled us to transcend some of the biological limitations placed on our ancestors and on other mamma- lian species. But breast milk also pro- vides important antibodies and micro- biota that contribute to infant survival and are not available in formula and other milk substitutes. Throughout the world, breast-fed infants have far greater survival rates than those who aren’t breast-fed or who are weaned too early. The only exception is in societ- ies where scientifically developed milk substitutes are readily available and appropriately used; even then, infants don’t get several important antibodies and other immune factors. The impor- tance of adequate nutrients during this period of rapid brain growth can’t be overestimated. Thus it’s not surpris- ing that there are many cultural prac- tices designed to ensure successful nursing. Furthermore, there is increas- ing evidence that breast- feeding may be protective against later-life obesity, types 1 and 2 diabetes, and hyperten- sion (Pollard, 2008) as well as child- hood obesity (Thompson, 2012). On the other hand, for women in the United States, obesity is associated with a lower duration of breast-feeding (Hauff and Demerath, 2012). As in the case of prenatal care, the public health goal of increasing rates of successful breast-feeding around the world is a worthy one.

Humans have unusually long child- hoods and a slowed growth pro- cess, reflecting the importance of learning for our species (Bogin, 2006; Thompson and Nelson, 2011).

Childhood is the time between wean- ing and puberty; it is a time when growth in stature is occurring, the brain is completing its growth, and technical and social skills are being acquired. For most other mammals, once weaning has occurred, get- ting food is left to individual effort. Humans may be unique in the prac- tice of providing food for juveniles (Lancaster and Lancaster, 1983) (Fig. 16-14). In the course of human evolution, it’s possible that provi- sioning children between weaning and puberty may have doubled or even tripled the number of off- spring that sur- vived to adult- hood (Table 16.1). This long period of extend- ed child care prob- ably enhanced the time for learn- ing technological and social skills, also contrib- uting to greater survival and reproductive success. Thus the costs of extensive parental care were out- weighed in human evolutionary history by the benefits of greater reproductive success. It is during childhood that the roles of fathers, older siblings, grand- mothers, and other kin become very significant. While mothers are highly involved with caring for new infants, the socialization and care of other chil- dren often fall to other family or com- munity members. Clearly family envi- ronment, stress, and other biosocial factors have a major impact on chil- dren’s health (Flinn, 1999, 2008) ( see Fig. 16-12).

The major causes of childhood death worldwide today are infectious diseases exacerbated by poor nutri- tion (Caulfield et al., 2004; Pelletier et al., 1995). Noting how important it is to have sufficient caloric intake in

▲�Figure 16-14 Human children require several years of extensive parental care following weaning.

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infancy while the brain is developing, Christopher Eppig and his colleagues have suggested that infectious diseas- es and parasitic infections drain nutri- ents and energy necessary for brain development in ways that threaten cognitive development and may help to explain the variation in IQ scores seen across nations (Eppig et al., 2010). It’s notable that the leading causes of childhood death in the United States and western Europe aren’t typically related to malnutrition; for children under 5 years of age, accidents are the leading cause of death, followed by preterm births.

Onset of Reproductive Functioning in Humans For most animals, the juvenile, or childhood, stage ends when adulthood begins. For humans and apes and pos- sibly some monkeys, there’s an addi- tional life cycle stage called adoles- cence. This is a period of extremely rapid growth in humans (the “adoles- cent growth spurt”) that is not seen in most other primates (Bogin, 1999;

2010). A number of biological events mark the transition to adolescence for both males and females. These include increase in body size, change in body shape, and the development of the tes- tes and penis in boys and breasts in girls. Hormonal changes are the driv- ing forces behind all these physical alterations, especially increased testos- terone production in boys and estrogen production in girls. As already noted, menarche is a clear sign of puberty in girls and is usually the marker of this transition in cultures where the event is ritually celebrated.

A number of factors affect the onset of puberty in humans, includ- ing genetics, gestational experience, nutrition, disease, activity levels, and stress. In humans and other primates, females reach sexual maturity before males do. An illustration of the “mis- match” effect of diet and other life- style factors on puberty is seen in the trend toward a lower age of menarche that has been noted in human popula- tions over the last century (Fig. 16-15) and the tendency for girls who are very active and thin to mature later than those who are heavier and less active.

Table 16.1 Providing for Juveniles Percent of Those Who Survive

Weaning Adolescence

Lion 28 15

Baboon 45 33

Macaque 42 13

Chimpanzee 48 38

Provisioned macaques 82 58

Human populations

!Kung* 80 58

Yanomamo† 73 50

Paleoindian‡ 86 50

*Hunting and gathering population of southern Africa. †Horticultural population of South America. ‡ Preagricultural people of the Americas.

Source: Adapted from Lancaster and Lancaster, 1983.

Life History Theory and the Human Life Course 459

Socioeconomic factors are also impli- cated in this trend: In less industrial- ized nations, girls from higher social classes tend to mature earlier than girls from lower social classes. In gen- eral, physical development has acceler- ated in the past several decades, along with worldwide improvements in pub- lic health and nutrition. Although we have emphasized the gradual decline in the age of maturity observed in the last century, there’s a great range of variation within every population. An important lesson from life history the- ory is that maturation is sensitive to local environmental situations, includ- ing diet, health care, and parental care practices.

Until the advent of settled living, it’s likely that females became pregnant as soon as they were biologically able to do so, that is, as soon as they had fin- ished growing. This would have been advantageous under conditions when individual life expectancy would have been low. Paleodemographic studies indicate a mortality rate of at least 50 percent in subadults in preindustrial populations; and of the half that sur- vived to adulthood, most did not sur- vive to age 50. Considering the real-

ity of short life spans combined with the long period of infant dependency, producing offspring as early as possi- ble may have contributed to the repro- ductive success of females, particularly early hominin females. By giving birth as soon as she reached sexual maturi- ty, an early hominin female enhanced her chances of rearing at least one off- spring to the point it could survive without her.

Mothers and Grandmothers Pregnancy and child care occupy much of a woman’s adult life in most cultures, as they likely did throughout hominin evolution. For most women in devel- oped countries, the years from men- arche to menopause are marked by monthly menstruation except when they are pregnant or nursing. A woman who never becomes pregnant may have as many as 400 cycles between men- arche and menopause. Because reli- able contraceptives were unavailable in the past, this high number of menstru- al cycles is probably a relatively recent phenomenon. It’s been suggested, in fact, that highly frequent menstrual cycling and the associated cell turnover

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Source: Wood, James W., 1994 Dynamics of Human Reproduction, New York: Aldine de Gruyter, original redrawn from Eveleth, P. B. and J. M. Tanner, 1976. Worldwide Variation in Human Growth, Cambridge: Cambridge University Press.)

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rates may be impli- cated in sever- al cancers of the female reproduc- tive organs, espe- cially of the breast, uterus, and ova- ries (Eaton et al., 1994; Strassman, 1999; Greaves, 2008). During the course of human evolution, females, unless they were sterile or not sex- ually active, may have had as few as 60 menstrual cycles in their entire lives.

At the social level, adulthood for women in the majority of world’s cultures means, in addition to caring for children, par- ticipation in eco-

nomic activities. Adulthood for men typically includes activities related to subsistence, religion, politics, and family. Women may be equally or less involved in these activities, depending on the culture.

For women, menopause, or the end of menstruation, is a sign that they’re entering a new life cycle phase. Estrogen and progesterone production begin to decline toward the end of the reproductive years until ovulation (and thus menstruation) ceases altogether. This occurs at about age 50 in all parts of the world. As an example of the con- tinuing effects of natural selection, there is evidence that women with a later age at menopause have more sur- viving offspring (Stearns et al., 2010). If this pattern continues, the authors sug- gest, the average age of menopause may increase by a year in the next 10 gener- ations or 200 years.

Throughout human evolution, the majority of females (and males) did not survive to age 50; thus few women lived much past menopause. But today,

this event occurs when women have as much as one-third of their active, healthy lives ahead of them. As already noted, such a long postreproductive period isn’t found among other pri- mates. Female chimpanzees and mon- keys experience decreased fertility in their later years, but most continue to have reproductive cycles until their deaths. Occasional reports of meno- pause in apes and monkeys have been noted, but it’s far from a routine and expected event. In fact, in 2010, a 56-year-old chimpanzee at a Kansas zoo surprised everyone by giving birth to a healthy female infant 22 years after her last birth.

Why do human females have such a long period during which they can no longer reproduce? One theory relates to parenting. Because it takes about 12 to 15 years before a child becomes inde- pendent, it’s been argued that females are biologically “programmed” to live 12 to 15 years beyond the birth of their last child. This hypothesis assumes that the maximum human life span for preagricultural humans was about 65 years, a figure that corresponds to what is known for contemporary hunter-gatherers as well as prehistoric populations.

Another theory about a long postre- productive life is known as the “grand- mother hypothesis.” This proposal argues that natural selection may have favored this long period in women’s lives because, by ceasing to bear and raise their own children, postmeno- pausal women would be freed to pro- vide high-quality care for their grand- children (Fig. 16-16). In other words, an older woman would be more likely to increase her reproductive fitness by enhancing the survival of her grand- children (who share one-quarter of her genes) than by having her own, pos- sibly low-quality infants (Hawkes et al., 1997; Lahdenperä et al., 2004; but see Peccei, 2001). This is an exam- ple of the trade-offs considered by life history theory.

A third theory regarding menopause suggests that it wasn’t itself favored by

▲�Figure 16-16 Senior Hadza woman and grandchild.

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natural selection; rather it’s an arti- fact of the extension of the human life span that’s occurred in the last sever- al centuries. To put it another way, the long postreproductive years and asso- ciated menopause in women have been “uncovered” by an extended life expec- tancy because many causes of death are now reduced (Sievert, 2006).

Aging and Longevity Postreproductive years are physio- logically defined for women, but “old age” is a very ambiguous concept. In the United States, we tend to associ- ate old age with physical ailments and decreased activity. Thus a person who’s vigorous and active at age 70 might not be regarded as “old,” whereas anoth- er who is frail and debilitated at age 55 may be considered old.

One reason we’re concerned with this definition is that old age is gener- ally regarded negatively and is typically unwelcome in the United States, a cul- ture noted for its emphasis on youth. This attitude is quite different from that of many other societies, where old age brings with it wealth, higher sta- tus, and new freedoms, particularly for women. This is because high status is often correlated with knowledge, expe- rience, and wisdom, which are them- selves associated with greater age in most societies. Such has been the case throughout most of history. But today, in technologically developed countries, information is changing so rapidly that older people may no longer control the most relevant knowledge.

By and large, people are living lon- ger today than they did in the past because they aren’t dying from infec- tious disease. Currently, the top five killers in the United States, for exam- ple, are heart disease, cancer, stroke, accidents, and chronic obstructive lung disease. Together these account for more than 65 percent of deaths (Heron, 2010). All these conditions are consid- ered “diseases of civilization” in that most can be accounted for by condi- tions in the modern environment that

weren’t present in the past. Examples include cigarette smoke, air and water pollution, alcohol, automobiles, high- fat diets, and environmental carcin- ogens. It should be noted, however, that the high incidence of these dis- eases is also a result of people living to older ages because of factors such as improved hygiene, regular medical care, and new medical technologies. Compared with most other animals, humans have a long life span (Table 16.2). The maximum life span poten- tial, estimated to be about 120 years, probably hasn’t changed in the last sev- eral thousand years. But life expectan- cy at birth (the average length of life) has increased significantly in the last 100 years, owing to advances in stan- dard of living, hygiene, and medical care. The most important advance is probably the treatment and prevention of infectious diseases, which typically take their toll on the young (Crews and Harper, 1998).

To some extent, aging is something we do throughout our lives (Finch, 2007). But we usually think of aging as senescence, the process of physi- ological decline in all systems of the body that occurs toward the end of the life course. Actually, throughout adult- hood, there’s a gradual decline in our cells’ ability to synthesize proteins, in immune system function, in muscle mass (with a corresponding increase in fat mass) and strength, and in bone mineral density (Lamberts et al., 1997). This decline is associated with an increased risk for the chronic degener- ative diseases, which are usually listed as the causes of death in industrialized nations.

As you know, most causes of death that have their effects after the repro- ductive years won’t be subjected to the forces of natural selection. What’s more, in evolutionary terms, reproduc- tive success isn’t measured by how long we live. Instead, as we have emphasized throughout this textbook, it’s measured by how many offspring we produce. So organisms need to survive only long enough to produce offspring and rear senescence Decline in physiological

function usually associated with aging.

chapter 16 Legacies of Human Evolutionary History and the Human Life Course 462

them to maturity. Most wild animals die young of infection, starvation, pre- dation, injury, and cold. Obviously there are exceptions to this statement, especially among larger-bodied ani- mals. Elephants, for example, may live over 50 years, and we know of several chimpanzees at Gombe that have sur- vived into their 40s or even 50s.

One explanation for why we age and are affected by chronic degenera- tive diseases like atherosclerosis, can- cers, and hypertension is that the genes which enhance reproductive success in earlier years (and thus were favored by natural selection) may have det- rimental effects in later years. These are referred to as pleiotropic genes, meaning that they have multiple effects at different times in the life span or under different conditions (Williams, 1957). For example, genes that enhance the function of the immune system in the early years may also damage tissue, so that cancer susceptibility increas- es in later life (Nesse and Williams, 1994). An example of this may be a gene responsible for lipid transport known as apolipoprotein E (apoE). One variant of this gene enhances immune function early in life but appears to be

associated with an increased risk of Alzheimer’s and cardiovascular dis- ease. In populations in which infec- tious agents are common, this variant is advantageous, but where infectious diseases are rare and people live lon- ger, the variant that protects against Alzheimer’s and cardiovascular disease would be more beneficial (Finch and Sapolsky, 1999).

In another view of aging and pleiot- ropy, anticancer mechanisms operating in early life may have opposite effects in later life (Hornsby, 2010). What’s more, epigenetic mechanisms affect not only aging itself but also the dis- eases associated with aging. Current research on these mechanisms points to possible epigenetic-based thera- pies and prevention strategies for deal- ing with the negative consequenc- es of the aging process (Gravina and Vijg, 2010). Pleiotropy may help us to understand evolutionary reasons for aging, but what are the causes of senescence in the individual? Much attention has been focused recently on free radicals, highly reactive mol- ecules that can damage cells. These by-products of normal metabolism can be protected against by antioxi-

Table 16.2 Maximum Life Spans for Selected Species Organism Approximate Maximum Life Span (in years)

Bristlecone pine 5,000

Tortoise 170

Rockfish 140

Human 120

Blue whale 80

Indian elephant 70

Gorilla 39

Domestic dog 34

Rabbit 13

Rat 5

Source: Stini W. A. (1992). The Biology of Human Aging. In: Applications of Biological Anthropology to Human Affairs, C. G. N. Mascie-Taylor and G. W. Lasker (eds.), p. 215. Cambridge, UK: Cam- bridge University Press.

pleiotropic genes Genes that have more than one effect; genes that have different effects at different times in the life cycle.

Life History Theory and the Human Life Course 463

dants such as vitamins A, C, and E and by a number of enzymes (Kirkwood, 1997). Ultimately, damage to DNA can occur, which in turn contributes to the aging of cells, the immune system, and other functional systems of the body. Additionally, there is evidence that pro- grammed cell death is also a part of the normal processes of development that can obviously contribute to senescence.

The mitochondrial theory of aging proposes that the free radicals pro- duced by the normal action of the cell’s mitochondria as by-products of daily living (for example, eating, breath- ing, walking) contribute to declin- ing efficiency of energy production and accumulating mutations in mito- chondrial DNA (mtDNA). When the mitochondria of an organ fail, there’s a greater chance that the organ itself will fail. In this view, as mitochon- dria lose their ability to function, the body ages as well (Loeb et al., 2005; Kujoth et al., 2007). Two of the most promising strategies for enhancing health in later life are calorie reduction (Anderson and Weindruch, 2012) and aerobic exercise, both of which appear to improve mitochondrial function (Fig. 16-17) (Lanza and Nair, 2010).

Another hypothesis for senescence is known as the “telomere hypothe- sis.” In this view, the DNA sequence at the end of a chromosome, known as the telomere, is shortened each time a cell divides (Fig. 16-18). Cells that have divided many times through- out the life course have short telo- meres, eventually reaching the point at which they can no longer divide and are unable to maintain healthy tis- sues and organs. Changes in telomere length have also been implicated in cancers and other diseases associated with aging (Oeseburg et al., 2010). In the laboratory, the enzyme telomerase can lengthen telomeres, allowing the cell to continue to divide. For this rea- son, the gene for telomerase has been called the “immortalizing gene.” But this may not be a good thing, since the only cells that can divide indefinitely are cancer cells. Although this research

isn’t likely to lead to a lengthening of the life span, it may contribute to a bet- ter understanding of cellular functions and cancer.

Far more important than genes in the aging process, however, are life- style factors, such as smoking, physi- cal activity, diet, and medical care. Life expectancy at birth varies considerably from country to country and among socioeconomic classes within a coun- try. Throughout the world, women have higher life expectancies than men. A Japanese girl born in 2009, for exam- ple, can expect to live to age 86, a boy to age 80. Girls and boys born in that same year in the United States have life expectancies of 81 and 76, respective- ly. Unfortunately, gains in life expec- tancy in the United States appear to be slowing relative to other industrialized

▲�Figure 16-17 Exercise throughout life may help prolong healthy mito- chondrial function.

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nations, primarily because of smoking, obesity, and sedentary habits (Seppa, 2011). In 2006, the latest year for which data were available, the United States ranked 36th in life expectancy among nations of the world (United Nations Population Division, 2007).

In contrast to these children in industrialized nations, girls and boys in Mali have life expectancies of only 51 and 48, respectively (data from World Health Organization, WHO Global Health Indicators, 2011). Many African nations have seen life expectancy drop below 40 owing to deaths from AIDS. For example, before the AIDS epi- demic, Botswanans had a life expec- tancy of almost 65 years; at the height of the AIDS epidemic, life expectancy in Botswana was slightly more than 40 (Fig. 16-19). In 1990, Zimbabweans could expect to live to 61; but by 2000, that figure had dropped to 45.

One consequence of improved health and longer life expectancy in conjunction with declining birth rates is an aging population, leading in some parts of the world to a shift toward older median ages and greater numbers of people older than 65 than younger

than 20. In demographic terms, these two groups represent dependent cat- egories, and there’s increasing con- cern about the decline in the number of working-age adults available to sup- port the younger and older segments of a population. In other words, the dependency ratio is increasing, with significant consequences for local and global economies. This phenomenon is of growing concern in the United States and western Europe, where it is estimated that more than a third of the population will be older than age 65 and fewer than half will be in the workforce.

Effects of Technology on the Brain

Aspects of the human cultural envi-ronment that are changing espe- cially rapidly are computer technology and the ways in which people gath- er information. In the past, informa- tion was based on environmental cues derived from sights, sounds, smells, and tactile sensations. Although these

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▼�Figure 16-19 Changes in life expectancy due to AIDS in seven African nations. (United Nations Population Division, 1998.)

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Are We Still Evolving? 465

sensory sources of information are still very important, people are increasing- ly turning to the Internet for informa- tion and social contact. What effect will this change have on our brains? As we have argued throughout this text, our brains coevolved with technolo- gy and language development, and it is reasonable to think that evolutionary processes continue for the brain. But like so much of what has occurred in the last hundred or so years, the pace of technological change is becoming faster and faster. One concern is that as our brains adapt to new technological innovations, there may be decreases in the development of social skills (Small and Vogan, 2008).

Brain plasticity is well known, as demonstrated by the brains of musi- cians (showing more gray matter in the areas of the brain responsible for finger movement) and athletes (more neurons for hand-eye coordination), so it is rea- sonable to assume that spending hours on the Internet searching for informa- tion and playing computer games will result in brain modifications that are different from those seen in our grand- parents and great grandparents. This is not the same as evolution, of course, but it does suggest that the distinc- tive human brain is being modified by technology in new and unforeseen ways. The speed of change also rais- es concerns about generational differ- ences and what has become known as the “digital divide.” Other concerns include addiction to Internet browsing, decreased attention span, and effects on young children (Fig. 16-20). In fact, the American Academy of Pediatrics has issued a warning against too much screen time (computers and televi- sion) for children under age 2 for fear of negative consequences for the rap- idly developing brain in those years (AAP, 2001). On the other hand, there is evidence that becoming proficient in Internet skills may have a posi- tive effect on the aging brain (Small et al., 2009).

Are We Still Evolving?

In many ways it seems that culture has enabled us to transcend most of the limitations our biology imposes on us. But that biology was shaped during millions of years of evolution in envi- ronments very different from those in which most of us live today. There is, to a great extent, a lack of fit or a “mis- match” between our biology and our twenty-first-century cultural environ- ments. Our expectations that scien- tists can easily and quickly discover a “magic bullet” to enable us to resist any disease that arises have been pain- fully dashed as death tolls from AIDS reach catastrophic levels in many parts of the world. Obesity and related dis- orders are beginning to have a greater impact on human lives than undernu- trition and infectious diseases. Socio- economic and political concerns also have powerful effects on our spe- cies today. Whether you die of starva- tion or succumb to disorders associ- ated with overconsumption depends a great deal on where you live, what your socioeconomic status is, and how much power and control you have over your life—factors not related to biol- ogy. These factors also affect whether you’ll be killed in a war or spend most of your life in a safe, comfortable com- munity. Your chances of being exposed to one of the “new” (or newly virulent)

▲�Figure 16-20 Exposure to com- puters at a very young age and for many hours per day may have effects on the developing brain.

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pathogens—such as HIV, the corona- virus that causes severe acute respira- tory syndrome [SARS], or tuberculo- sis—have a lot to do with your lifestyle and other cultural factors. But your chances of dying of the disease or fail- ing to reproduce because of it still have a lot to do with your biology. The 4.3 million children dying annual- ly from respiratory infections are pri- marily those in the developing world, with limited access to adequate medi- cal care—clearly a cultural factor. But in those same areas, lacking that same medical care, are millions of other chil- dren who aren’t getting the infections or aren’t dying from them. Presumably among the factors affecting this dif- ference is resistance afforded by genes. It is clear that human gene frequen- cies are still changing from one genera- tion to the next in response to selective agents such as disease; thus our species is still evolving.

We can’t predict whether we will become a different species or become extinct as a species (remember that this has been the fate of almost every spe- cies that has ever existed). Will our brains get larger, or will our hands

evolve solely to push buttons? Or will we change genetically so that we no longer have to eat food? This is the stuff of science fiction, not anthro- pology. But as long as new patho- gens appear or new environments are introduced by technology, there’s little doubt that just like every other species on earth, the human species will either continue to evolve or become extinct.

Has our evolutionary history pre- pared us for the twenty-first century? We have discussed a number of the dis- connections between our evolved biol- ogies and contemporary lives, but we have also emphasized that one of the most significant legacies from our evo- lutionary history is our biological and behavioral flexibility, provided in part by the all-important phenomenon of culture. Culture has enabled us to tran- scend many limits imposed by our biol- ogy. Today, people who never would have been able to do so in the past are surviving and having children. This in itself means that we are adapting and evolving. How many of you would be reading this text if you had been born under the health and economic condi- tions prevalent 500 years ago?

Several times in this chapter we have discussed hypothesized behaviors and lifestyles of our ances- tors. But because behavior doesn’t fossilize, how can we know what people’s lives were like in the past? The truth is that we can never know for sure how people behaved in the past, but we can make reasonable infer- ences based on three important sources discussed throughout this book: the behaviors of our closest living relatives, the nonhuman primates; the ethno- graphic reports of people in Africa, South America, and Australia who were, until recently, foraging for their livelihoods; and the fossil and osteological records of health indicators. For example, in trying to understand how long mothers breast-fed their infants

in the past, we find it helpful to consider data from pri- matologists on chimpanzee nursing patterns and from anthropologists who observe breast-feeding among the !Kung and Hadza of southern Africa. Signs of malnu- trition in the skeletal remains of young infants from past populations may tell us the approximate age of weaning. As with any scientific explanation, the sce- narios we propose for ancestral human behaviors stand or fall on the basis of how well they explain the data. New fossil evidence, new observations of nonhuman primates, and new ethnographic reports can lead to modifications or even rejection of any scenario. This is how all aspects of science work, including aspects of science that explore ancestral biology and behavior.

How Do We Know?

467Media Resources

▶ Our biology, resulting from millions of years of evolution, may not be well matched with the diets and lifestyles we have today, perhaps contributing to many of the health problems we now face.

▶ The human life course is an excellent place to examine the interaction of culture and biology, given that patterns of human growth and nutri- tional requirements result from millions of years of biological evolution and thousands of years of cultural evolution.

▶ Nutrition has an impact on growth at every stage of the life cycle, and few aspects of the human environment have changed as much in the last 10,000 years as diet.

▶ In some ways, human health may have declined with the onset of agriculture and animal domesti- cation approximately 10,000 years ago.

▶ One result of the mismatch between contempo- rary lifestyles and evolved biology may be a rise in the worldwide incidence of type 2 diabetes and obesity.

▶ Studies in epigenetics have revealed that structural changes to DNA and associated proteins caused

by developmental and environmental factors can underlie gene expression, helping to resolve the age-old conflict between nature and nurture.

▶ Women in health-rich nations today have repro- ductive hormonal profiles that may differ greatly from those under which our ancestors evolved, suggesting a link to various reproductive disorders and diseases.

▶ Humans have unusually long childhoods during which much learning takes place.

▶ Unlike most mammals, human women live well beyond the termination of their reproductive years, suggesting a value in the contributions of grandmothers.

▶ With rapidly increasing developments in com- puters and other forms of information technol- ogy, new questions about the effects of technology on the developing and mature human brain have arisen.

▶ Although it appears that culture has enabled us to transcend biological evolutionary processes, there is little doubt that our species continues to evolve.

Summary of Main Topics

1. Do you think it’s possible to study humans without studying culture? Can we study humans only as cultural animals or do we need to know something about human biology to understand behavior?

2. Compare and contrast the human preagricultural diet with that seen today in places like the United States. Discuss at least one major health conse- quence of what has been termed the mismatch between the diet with which humans have evolved and that which many people now consume. Do

you think our health would improve if we were to adopt a diet more like that of our ancestors?

3. Briefly discuss some of the theories for why humans age. Do you think it will be possible to extend the human life span to longer than 125 years? Why or why not?

4. The authors of this text claim that humans are still subjected to the forces of evolution. Do you agree? What is the evidence for or against that claim?

Critical Thinking Questions

Video See the video “Diet, Lifestyle, and Consequences”

to learn more about topics covered in this chapter.

Media Resources

Humans have recently become disconnected from

other life and are rapidly altering the planet.

Connections

Human development and adaptation is best under- stood from an evolution-

ary perspective.

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▶ �Understand how human activities have led to a disconnect between ourselves and other species to which we are connected through our evolutionary past.

469

W hile reading this book, you have accompanied us through geological time to the present state of Homo sapi- ens: connecting us with earlier life through 225 million years of mamma- lian evolution, 65 million years of pri- mate evolution, 6 million years of hom- inin evolution, and 2 million years of evolution of the genus Homo. So what do you think now? Are we just another mammal—or just another primate? In most ways, of course, we are like other mammals and primates. But as we have emphasized throughout this book, modern human beings are the result of biocultural evolution. In other words, modern human biology and behavior have been shaped by the biological and cultural forces that operated on our ancestors. In fact, it would be fruitless to attempt an understanding of modern human biology and diversity without considering that humans have evolved in the context of culture. It would be like trying to understand the biology of fish without considering that they live in water.

In the last few chapters, we saw how the choices we make as cultural ani- mals have profound effects on human health. Although culture and technol- ogy have allowed us to adapt beyond our biological limits, they have also impacted other species and indeed the planet. Humans now have the ability to preserve or destroy a significant portion of the earth’s life-forms—the results of millions of years of evolu- tion. Here we will briefly discuss some

17 The Human Disconnection of the challenges that have emerged as a result of our own actions. Many peo- ple refuse to believe that the earth’s climate is changing, and of those who do, a large proportion think that this change is due to “natural” causes and not human activities. But the over- whelming consensus among climate scientists is that global warming is occurring, that the climate is changing more rapidly than anticipated, and that human activities are the cause. It is also a fact that the results of such rapid cli- mate change are going to be more than simply “inconvenient.”

Although physical anthropolo- gy textbooks don’t usually dwell on the topics included here, we feel that it’s important to consider them, how- ever brief and simplified our treat- ment must be. We are living during a critical period in the earth’s history. Indeed, the future of much of life as we know it will be decided in the next few decades, and these decisions will be irrevocable. It’s crucial that we, as individuals, cities, and nations, make wise decisions, and to do this we must be well informed. We also think that it’s important to consider these prob- lems from an anthropological per- spective. This is something not usual-

Student Learning Objectives

chapter 17 The Human Disconnection 470

ly done in the media and certainly not by politicians and heads of state. But if we are truly to comprehend the impact that human activities have had on the planet, then surely we must consider our biological and cultural evolution. We must also emphasize our place in nature and focus on how, from the time we began to domesticate plants and animals, we’ve altered the face of our planet while also shaping the des- tiny of thousands of species, including our own.

Human Impacts on the Planet and Other Life-Forms

By most standards, Homo sapiens is a successful species. There are currently 7 billion humans living on this planet. Even so, we and all other multicellular organisms contribute only a small fraction of all the cells on earth—most of which are bacteria. So if we see life ultimately as a competition among reproducing organisms, bacte- ria are the winners, hands down.

Nevertheless, no matter what cri- terion for success is used, there is no question that humans have had an inordinate impact on the earth and all other forms of life. In the past, our ancestors had to respond primarily to challenges posed by nature. Today the greatest challenges for our species (and all others) are the vastly altered envi- ronments of our own making. Through our actions, which have caused wide- spread devastation of ecosystems all over the world, from every continent, from the deep seas to the upper atmo- sphere, we have disconnected our spe- cies from its long evolutionary legacy. But at the same time we are still depen- dent on the ecosystems of which we remain a part. Can we survive as a spe- cies if we continue to challenge Mother Nature? Perhaps, but things will cer- tainly be different, and undoubtedly the planet will be able to support far fewer humans.

Increasing population size is per- haps the single most important reason that our impact has been so great. As human population pressure increas- es, more and more land is converted to crops, pasture, construction, and human habitation, providing more opportunities for still more humans and fewer (or no) habitats for most other species.

Scientists estimate that around 10,000 years ago, only about 5 million people inhabited the earth (almost half as many live in Los Angeles County or New York City today). By the year 1650, there were perhaps 500 million, and by 1800, around 1 billion (Fig. 17-1). Today we add 1 billion people to the world’s population approximately every 13 years (Barnosky et al., 2012). That comes out to about 77 million every year and roughly 200,000 every day— or just about 9,000 an hour.

The rate of population growth is not equally distributed among all nations. The most recent United Nations report on world population notes that 95 per- cent of this growth is occurring in the developing world. Likewise, resourc- es are not distributed equally among all nations. Only a small percentage of the world’s population, located in a few industrialized nations, controls and consumes most of the world’s resourc- es. A 2009 study estimated that 48 per- cent of the world’s population survives on less than $2 per day (Population Reference Bureau, 2009).

Humans and the Impact of Culture For most of human history, technol- ogy remained simple, and the rate of culture change was slow. From the archaeological record, it appears that around 15,000 ya, influenced in part by climate change (not induced by human activity) and the extinction of many large-bodied prey species, some human groups began to aban- don their nomadic hunting and gath- ering lifestyles and adopt a settled way of life. Moreover, by about 10,000 ya (and probably earlier), some peoples

Human Impacts on the Planet and Other Life-Forms 471

had learned that by keeping domes- tic animals and growing crops, they had more abundant and reliable food supplies. The domestication of plants and animals is seen as one of the most significant events in human history, one that was eventually to have far- reaching consequences for the entire planet. Human impact on local envi- ronments increased dramatically as soon as people began to live in perma- nent settlements.

Unfortunately humans began to exploit and increasingly depend on nonrenewable resources. Forests can be viewed as renewable resources pro- vided they’re given the opportunity for regrowth. But in many areas for- est clearing was virtually complete and was inevitably followed by soil erosion, frequent overgrazing, and overculti- vation, which in turn led to further soil erosion (Fig. 17-2). In those areas, trees became a nonrenewable resource,

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▲ Figure 17-1 Growth curve (orange) depicting the exponential growth of the world’s human population. The vertical axis depicts world popula- tion size in billions. It wasn’t until the mid-1800s that this figure reached 1 billion, but we now add 1 billion people every 13 years or so. Population increase occurs as a function of some percentage (in developing countries, the annual rate is over 3 percent). With advances in food production and medical technologies, humans are currently undergoing an unprec- edented population explosion, as this figure illustrates.

◀ Figure 17-2 Stumps of recently felled forest trees are still visible in this newly cleared field in the Amazon.

chapter 17 The Human Disconnection 472

perhaps the first resource to have this distinction.

Destruction of natural resources in the past has also had severe con- sequences for people living today. In 1990, a typhoon and subsequent flooding killed over 100,000 people in Bangladesh, and the flooding was at least partly due to previous deforesta- tion in parts of the Himalayas of north- ern India. There is also evidence that deforestation has contributed to con- tinued erosion and flooding in China. And millions of people in Pakistan were affected by flooding in 2010 and 2011 that resulted in part from defor- estation and dam construction along tributaries of the Indus River. This flooding affected one-fifth of the coun- try and set back years of infrastructure development.

Global Climate Change There are several atmospheric sub- stances that warm the earth by trapping heat; collectively we call them green- house gases. They include water vapor, ozone, nitrous oxide, methane, chlo- rofluorocarbons, and carbon dioxide (CO₂). Without them the earth would freeze, but in abundance they can raise temperatures to dangerous levels, and that is what is currently happening. We can say this unequivocally because climate scientists are unanimous in their view that the earth is heating up; it’s happening more quickly than pre- dicted, and it’s due to human activi- ties. Chief among these activities is the burning of fossil fuels (especially oil and coal) because they release CO₂ when burned, and CO₂ is the most significant contributor to global warming. Indeed, we currently release 35 billion tons of CO₂ into the atmosphere every year.

In 2012, scientists at the National Oceanic and Atmospheric Administration (NOAA) reported for the first time that CO₂ levels had reached 400 parts per million (ppm) in several northern locations. This fig- ure vastly exceeds the natural range for the last 800,000 years of 180 to 300 ppm (Smol, 2012). It is highly signifi-

cant because for several years clima- tologists have warned that if we are to keep average worldwide temperatures from increasing more than 2.5 degrees Fahrenheit, the level of CO₂ must be kept at 350 ppm. In turn, keeping the increase below 2.5 degrees is impor- tant because many researchers consid- er that to be the maximum we can sus- tain without disastrous consequences for the environment and for thousands of species.

Currently, about 70 percent of Americans believe the climate is changing and perhaps as many as 40 percent think this change is due to human activities. But this leaves around 50 to 60 percent (including many politicians and talk-show hosts) who believe that the warming is part of a “normal” trend that has little if anything to do with human activities. At best, this is wishful thinking. But reversing the warming trend would be monumentally expensive and it would require individual sacrifice as well as huge changes in business and industri- al practices. Partly because of the sac- rifices and expense, the topic of global warming is now as controversial in the United States as is evolution (Reardon, 2011). In fact, it is so controversial that in many school districts through- out the country, science teachers are strongly encouraged not to mention it.*

No one disputes that there have been dramatic climatic fluctuations throughout earth’s history that had

*Sir David Attenborough, the much loved British producer of nature programs for more than 40 years, produced a highly acclaimed television series called Frozen Planet. When it aired in the United Kingdom in 2011, this beautifully filmed series consisted of seven parts, the last of which concerned global warming. (Unfortunately it was a tepid treatment.) Curiously, when the program aired on the Discovery Channel in the United States, it was only six episodes long. The global warming finale was not shown and most American viewers never even knew about it. When questioned about this omission, spokespeople for the Discovery Channel explained that there had been a “scheduling conflict” that prevented them from showing the entire series.

Human Impacts on the Planet and Other Life-Forms 473

nothing to do with human activity. Furthermore, many of these fluctua- tions were sudden and had devastating consequences. But even if the current warming were part of a natural cycle, scientists are convinced that human- produced greenhouse gases could tip the balance toward a catastrophic glob- al climate change. One source of this concern is the study of ice core data, which show that there is significantly more carbon dioxide in the earth’s atmosphere than at any time in the last 800,000 years. In view of this fact, consider this prediction from an inter- national group of experts: “The mean [average] global temperature by 2070 (or possibly a few decades earlier) will be higher than it has been since the human species evolved” (Barnosky et al., 2012, p. 54).

In 2007, scientists became alarmed at a sudden unexpected increase in the loss of Arctic sea ice. Unlike icebergs and glaciers that form on land, sea ice is frozen ocean water. The importance of sea ice to global climate systems can’t be overemphasized because it reflects back into space about 80 percent of the sunlight (which contains heat) that hits it. But seawater absorbs approxi- mately 90 percent of the sunlight that hits it. Therefore as more ice melts, less sunlight is reflected and more heat is retained, resulting in yet more warm- ing and more melting. Because of this, the polar regions are the most sensi- tive areas on earth to warming, and the loss of sea ice can accelerate climate change.

Since 1979, scientists have been tracking Arctic sea ice maximum and sea ice minimum data collected from satellites. In the first decade of this century, there was a sudden and alarm- ing decline in the extent of sea ice dur- ing the summer months. Indeed, the 6 years between 2007 through 2012 (inclusive) saw the greatest declines in Arctic sea ice since the collection of satellite data began. The average mini- mum area covered by ice between 1979 and 2000 was 2.6 million square miles, but there was a significant change in 2005 when that figure was reduced to 2

million square miles. Just 2 years later, in 2007, the minimum was further reduced to less than 1.6 million square miles. Then, on September 16, the day that melting ceased in 2012, the extent of sea ice was 1.32 million square miles, 49 percent lower than the 1979‒2000 average. (Fig. 17-3) This difference of 1.28 million square miles represents an area nearly twice the size of the state of Alaska (National Snow and Ice Data Center, 2012).

Scientists are now greatly con- cerned that the polar regions may have reached a “tipping point,” a point beyond which the warming pro- cess cannot be reversed. In fact, the increase in warming is occurring faster than computer models were predicting just a few years ago. Recent estimates held that the Arctic could be ice-free for part of the summer by perhaps as soon as 2030, but some scientists now fear this could happen much soon- er. It goes without saying that without sea ice in the summer, polar bears and several other species that depend on it may well become extinct in the fore- seeable future.

However, there are more than a few who see financial opportunities in the melting sea ice. The absence of sea ice will drastically reduce the time it takes for ships to travel between Asia and Europe. Furthermore, it will make oil drilling possible and, in fact, Russia, Canada, and the United States already have oil exploration projects in progress.

Climate change is the result of the interactions of thousands of factors, and the consequences of these inter- actions aren’t possible to predict with complete accuracy. But the overwhelm- ing consensus among climate scientists points directly to “human-driven glob- al change” (Barnosky et al., 2012), espe- cially due to the burning of fossil fuels. They also agree that, as a consequence of such climate change, we are already experiencing severe fluctuations in weather patterns along with alterations in precipitation levels, and that these will dramatically accelerate in the next few decades. For example, the extreme

sea ice maximum In the arctic, the greatest amount of sea ice that is present in one year. It occurs in March at the end of winter, just as the ice stops forming and begins to melt.

sea ice minimum the least amount of ice that is present in the arctic in one year. Sea ice is at its minimum in September, just as the summer melting season ends but before the ice begins to form again.

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drought in the United States in the summer of 2012 (the worst in 50 years) forced many farmers to sell their farms and livestock and has caused dramatic increases in food prices. Ultimately this drought will cost at least a few billion dollars.

In late October of 2012, Hurricane Sandy caused billions of dollars worth of damage along the northeast coast of the United States. Streets in lower Manhattan and several subway tunnels were flooded, millions of households were without power, and thousands of homes were damaged or destroyed in New Jersey, New York, and several other states (Fig. 17-4). Moreover,

more than 200 people were killed. While scientists cannot state that any particular storm or severe weather pat- tern was specifically caused by global warming, they do say that weather will be increasingly unpredictable and that we can expect more extreme and destructive events as temperatures continue to rise.

The destructive results of chang- ing temperatures and precipitation pat- terns are incalculable. They include loss of agricultural lands due to desert- ification in some regions and flood- ing in others, rising sea levels inundat- ing coastal areas throughout the world, increased human hunger, extinction

▶ Figure 17-3 In this figure, the area in white represents the mini- mum amount of Arctic sea ice in mid-September. In 2007 (a), the sea ice minimum was 1.6 million square miles. In 2012 (b), the area covered by sea ice had been further reduced to 1.3 million square miles. Compare the white areas to the orange line which represents the median minimum sea ice extent for the years 1979–2000. (c) This graph compares the amount of sea ice in 2012 and 2007 compared to the average amount between 1979 and 2000. Note that in late September the amount of coverage increases as ice begins to form again.

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Human Impacts on the Planet and Other Life-Forms 475

of numerous plant and animal species, and altered patterns of infectious disease. Regarding the latter, health officials are particularly concerned about the spread of mosquito-borne diseases such as malaria, dengue fever, and yellow fever as warmer tempera- tures increase the geographical range of mosquitoes.

Another consequence of human- caused global climate change is increasing acidification of the oceans due to absorption of greater amounts of CO₂. The global dangers to ecosystems from ocean acidification are potential- ly as great as global warming, so much so, in fact, that some marine biologists have termed it “the other CO₂ problem” (Doney et al., 2009). Since the begin- ning of industrialization in the mid- 1700s, ocean acidity has increased by 30 percent. If current CO₂ emission rates continue, it could increase a fur- ther 150 percent by the end of this cen- tury, reaching levels not seen in the oceans for more than 20 million years (Turley et al., 2007).

Tropical coral reefs are particularly vulnerable to acidification. Coral reefs constitute the most diverse marine ecosystems on earth including an esti- mated one million species, which, in turn, represents up to 25 percent of all ocean-dwelling species. In addi- tion to a tragic loss of biodiversity, there are direct economic effects of

the destruction of coral reefs because more than 100 million people depend on them for food (Harrould-Kolieb and Savitz, 2009). As bad as this sounds, the longer-term effects of ocean acidi- fication could be far more catastroph- ic, affecting tens of thousands of other species. Unless major action is taken soon to reduce CO₂ emissions, ocean ecosystems will probably be seriously affected by 2050 (Gruber et al., 2012); these changes could well be irrevers- ible, or at best they will take genera- tions to rebound. If you think this won’t impact you and all of human- ity, just consider that today 20 to 25 percent of the animal protein con- sumed by humans comes from marine sources (Guinotte and Fabry, 2009) (see Fig. 17-5).

There has been international recog- nition of the enormity of the problems associated with global climate change, and unprecedented international coop- eration has begun. All this is happen- ing because the governments of most nations understand the gravity of the impending crisis. But even though these governments recognize the prob- lem, there is powerful opposition from industry to changes in existing policies.

In December 2009, the United Nations sponsored the International Convention on Climate Change in Copenhagen, Denmark; it was attend- ed by representatives from nearly 200

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◀ Figure 17-4 Partially submerged cars and severe flooding near Manhattan’s lower east side, caused by Hurricane Sandy in late October, 2012. Sandy destroyed thousands of homes and businesses and killed over 200 people in the United States and several Caribbean countries. Ultimately this “superstorm,” the larg- est recorded Atlantic hurricane, could ultimately cost an estimated 50 billion dollars in the United States alone.

chapter 17 The Human Disconnection 476

countries. Leading up to this meeting, worldwide expectations ran high that earlier agreements (reached in 1997 at a prior international convention in Kyoto, Japan) would be expanded and strengthened with broader and more rigorous, binding agreements to cut carbon emissions.

The world looked especially to the United States for leadership and, even more, for signs of real commitment. Yet nothing substantive occurred in Copenhagen. Most world leaders indi- cated that they were fully prepared to commit to major cuts in carbon emis- sions. But widespread lack of trust in American willingness to make real political commitments (that is, effec- tive legislation passed by Congress) as well as weak support from China led to no formal and certainly no bind- ing agreements. Instead, only a broad statement of goals was made, with no mechanisms to ensure that even these would be met.

Another major international meet- ing, the United Nations Conference on Sustainable Development, again attended by representatives from almost 200 countries, was held in June 2012 in Rio de Janeiro, Brazil. This ambitious conference, also called the

Earth Summit, was widely antici- pated as another major opportunity to advance serious global action on climate change and related issues. However, no major initiatives were approved and most knowledgeable observers considered the conference a failure.

Widespread disappointment has resulted from this repeated lack of progress. In fact, it now appears that there is less global consensus and less political leadership, especially by those countries that are the biggest carbon emitters, than there was two decades ago. Where we go from here is not clear, but one thing is certain: The cli- mate will continue to change. It will likely be at least 3 or 4 years before another truly global effort is attempt- ed. What will come of that? And will any decisions actually be implemented in time?

Impact on Biodiversity According to biologist Stephen Palumbi (2001), humans are the “world’s greatest evolutionary force.” What Palumbi means is that we humans, like no other species before us, have had a profound effect on the evolutionary histories of almost all forms of life, including the potential to alter global ecology and destroy our- selves and much life on earth. Even massive geological events and mass extinctions did not wreak the havoc that may result from modern human technology.

The geological record indicates that in the last 570 million years, there have been at least 15 mass extinction events, two of which altered all of the earth’s ecosystems (Ward, 1994). The first of these occurred some 250 mya and resulted from climate change that followed the merging of all the earth’s landmasses into one supercontinent. The second event happened around 65 mya and eradicated tens of thousands of species, including most dinosaurs (recall from Chapter 5 that birds are their living descendants).

▲ Figure 17-5 Coral reefs are the most biologically diverse habitats in the oceans, and also the most threatened.

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Human Impacts on the Planet and Other Life-Forms 477

A third major extinction event, per- haps of the same magnitude, is occur- ring now, and according to some sci- entists, it may have begun in the late Pleistocene or early Holocene (Ward, 1994). Unlike all other mass extinc- tions, this one hasn’t been caused by continental drift or collisions with asteroids. Today it’s due to the activities of a single species, Homo sapiens.

The overall effects of human activi- ties, particularly in the last 250 years, have had such a profound effect on the earth that many scientists are now rec- ognizing these sudden and dramatic changes as marking a new geological era, called the Anthropocene (Vince, 2011). As an example of just how much our species has altered the planet, one current estimate suggests that as much as 43 percent of terrestrial habitats have been transformed to either agri- cultural or urban landscapes (and this does not include roads outside urban areas) (Basnosky et al., 2012). Like ear- lier major shifts in the earth’s geology and biodiversity, the Anthropocene is comparable to the two planetary events mentioned above. These, however, were caused by gigantic asteroid collisions or super volcanoes; the Anthropocene (“the age of humans”) is the result of human behavior.

For at least the past 15,000 years, human activities such as hunting

and clearing land for cultivation have taken their toll on nonhuman species, but species are currently disappear- ing at an unprecedented rate. Hunting, which occurs for reasons other than acquiring food, is a major factor. This is particularly true for nonhuman pri- mates, tigers, elephants, and rhinoc- eroses. As you saw in Chapter 6, aside from being hunted for food, nonhu- man primate and tiger body parts are widely used in traditional medicines, mainly in Asia, and infant animals are commonly funneled into the exotic pet trade. Rhinoceros horns are also pop- ular in parts of the Middle East, espe- cially as knife handles, and in Asia for medicinal purposes. And there has been an enormous resurgence of ele- phant hunting in Africa for their ivory tusks. Competition with introduced non native species—such as pigs, goats, and rats—has also contributed enor- mously to the problems that wild ani- mals face (Fig. 17-6). But in most cases the most important cause of extinction is habitat reduction.

Habitat loss is a direct result of the burgeoning human population and the resulting need for building mate- rials, grazing and agricultural lands, and ever-expanding human habita- tions (Fig. 17-7). We’re all aware of the risk to such highly visible species as elephants, pandas, rhinoceroses, tigers,

◀ Figure 17-6 Feral goats, intro- duced into the Galápagos Islands, threaten the habitat of the giant Galápagos tortoise.

Holocene The most recent epoch of the Cenozoic. Following the Pleistocene, it’s estimated to have begun 10,000 years ago.

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and mountain gorillas, to name a few. These risks are real, and within your lifetime, some of these species will cer- tainly become extinct. But the greatest threats to biodiversity are to the count- less unknown species that live in the world’s rain forests and in the oceans (particularly coral reefs).

Should we care about the loss of bio- diversity? If so, why? In truth, many people don’t seem to be very con- cerned, and this may be because these topics aren’t extensively covered in most media. What’s more, when peo- ple explain why we should care, they usually point out the benefits (known and unknown) that humans may derive from wild species of plants and ani- mals. An example of such a benefit is the chemical taxol (derived from the Pacific yew tree), which may be an effective treatment for ovarian and breast cancer. These benefits are important, but preserving biodiver- sity for its own sake is every bit as crucial.

The United Nations recently organized another large interna- tional conference to address pressing issues concerning

biodiversity. The conference (an exten- sion of the Convention on Biological Diversity) took place in October 2010 in Nagoya, Japan, and was attended by representatives from 193 countries. Unlike the lack of agreement that char- acterized the conferences focusing on global climate change, the results of the biodiversity meeting were quite encouraging. Conference members agreed to increase cooperation and to share financial benefits that come from the development of new drugs from wild plants and animals. What’s more, they produced an impressive list of significant international goals to be reached by 2020, including an effort to reduce to half or bring close to zero the rate of loss of all natural habitats, to reduce pollution to levels that are not detrimental to ecosystems and bio- diversity, to conserve at least 17 per-

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▼ Figure 17-7 (a) Agricultural fields in China’s Yunnan Province and (b) an aerial view of São Paulo, Brazil; with a population of about 19 million, it is one of the 10 largest cities in the world. The fields and city occupy land that once provided habitat for thousands of plants and animals.

Human Impacts on the Planet and Other Life-Forms 479

cent of terrestrial areas and 10 percent of coastal and marine areas in pro- tected zones, to prevent the extinction of known threatened species, and to restore at least 15 percent of degraded ecosystems.

Acceleration of Evolutionary Processes Another major impact of human activ- ities is the acceleration of the evolu- tionary process for hundreds of bacte- ria and viruses. Many of these changes have occurred over a single human generation (that is, during the life- time of many people living today), not the millions of years usually associ- ated with evolution. As noted earlier, our use of antibiotics has dramatically altered the course of evolution of sever- al bacterial diseases to the point where many bacteria have become resistant to antibiotics. Antibiotics have now become the most significant selective factors causing many bacteria to evolve into more virulent forms. It’s even like- ly that human technology and lifestyles are responsible for the deadly nature of some of the so-called new diseases that have arisen in recent decades, such as HIV/AIDS, dengue hemorrhagic fever, Legionnaires’ disease, Lyme disease, and resistant strains of Mycobacterium tuberculosis, Staphylococcus, and Esch- erichia coli. We could reach a point where we have no antibiotics capable of fighting dangerous bacteria that live and constantly mutate in our midst. For example, there are billions of ben- eficial bacteria in a person’s digestive tract. We couldn’t live without these bacteria, but some can and occasion- ally do mutate into varieties that cause serious illness and even death. Without antibiotics, these and many other bac- teria in our environment would have the ability to drastically increase mor- tality due to infectious disease.

A similar phenomenon has occurred with the overuse and misuse of insec- ticides and pesticides on agricultural crops (Palumbi, 2001). As mentioned

previously, DDT is perhaps the best-known insecticide to have altered the course of a spe- cies’ evolution. When this insecticide was first developed, it was hailed as the best way to reduce malaria by eliminating the mos- quitoes that transmit the disease. DDT was highly effective when it was first applied to mosquito-ridden areas, but soon mosquitoes had evolved resistance to the powerful agent, rendering it almost useless in the fight against malaria. Moreover, the use of DDT proved disastrous to many bird species, including the bald eagle (Fig. 17-8). In the 1970s, its use was curtailed and even banned in some countries, but the failure of other efforts to treat malaria has led to a recent call to begin using DDT again.

From these examples, it’s clear that the human-caused accelerated process of microbial evolution is something that can lead to great harm to our spe- cies and the planet. Certainly none of the scientists developing anti biotics, insecticides, pesticides, and other bio- logical tools intend to cause harm. But unless they understand the evo- lutionary process, they may not be able to foresee the long-term conse- quences of their work. As the great geneticist Theodosius Dobzhansky (1973) said, “Nothing in biology makes sense except in the light of evolution.” Indeed, we can’t afford to have even a single generation of scientists who are not fully informed about evolution. If human actions can cause an organ- ism to evolve from a relatively benign state to a dangerously virulent one, there is no reason why we can’t turn that process around. In other words, it is theoretically possible to direct the course of evolution of a dangerous virus such as HIV to a more benign, less harmful state (Ewald, 1999).

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▲ Figure 17-8 DDT almost caused the extinction of the American bald eagle, the bird featured on the Great Seal of the United States.

chapter 17 The Human Disconnection 480

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▼ Figure 17-9 Today, air pollu- tion is a worldwide problem. (a) Two Vietnamese girls using scarves as protective masks. (b) Sunrise over Delhi, India. (c) Toronto, Canada, in the gloom. (d) Sunset over Beijing, China. (e) A smoggy day in Los Angeles.

Looking for Solutions

The problems facing our planet reflect an adaptive strategy gone awry. Indeed, it’s clear that we no lon- ger enjoy the harmonious relationship we once had with culture or with the planet. Instead, culture has become an unintentional transformer of the environment. All we need to do is examine the very air we breathe to realize that we have overstepped our limits (Fig. 17-9).

Can the problems we’ve created be solved? Perhaps, but any objective assessment of the future fails to pro- vide much optimism. Climate change, air pollution, depletion of the ozone layer, and loss of biodiversity are cata- strophic problems in a world of 7 bil- lion people. How well do we cope now with feeding, housing, and edu- cating these 7 billion? What quality of life do the majority of the world’s people enjoy right now? What kind of world have we wrought for the other

Is There Any Good News? 481

organisms that share our planet, as many are steadily isolated within frag- ments of what were once large habi- tats? If these concerns aren’t over- whelming enough now, what kind of world will we see in the year 2050, when the human population could reach 10 billion? Among other con- sequences of this population growth, the world’s food production would need to double in order for everyone to have enough to eat. (Millions are underfed and undernourished now.) Because our window of opportunity shrinks every year, industrialized nations must immediately help devel- oping countries to adopt fuel-efficient technologies that will allow them to raise their standard of living without increasing their output of greenhouse gases. Furthermore, family planning must be adopted to slow population growth. In most societies, however, behavioral change is very difficult, and sacrifice on the part of the devel- oping world alone wouldn’t adequate- ly stem the tide. It’s entirely too easy for someone from North America to ask that the people of Bangladesh con- trol their rate of reproduction (it runs two to three times that of the United States). But consider this: The average American uses an estimated 400 times the resources consumed by a resident of Bangladesh. The United States alone produces 25 to 30 percent of all carbon dioxide emissions that end up in the earth’s atmosphere. In 2007, China caught up with the United States in this regard, but over 1.3 billion people live in China, compared with 300 mil- lion in the United States. In his book The Future of Life (2002), E. O. Wilson discussed the issue in terms of “eco- logical footprints,” or the average amount of land and sea required for each person to support his or her life- style. This includes all resources con- sumed for energy, housing, transpor- tation, food, water, and waste disposal. In nonindustrialized nations, the eco- logical footprint per capita is about 2.5 acres, but in the United States it’s 24 acres! Wilson went on to point out that four additional planet earths would be

needed for every person on the planet to reach the current levels of consump- tion in the United States. Clearly much of the responsibility for the world’s problems rests squarely on the shoul- ders of the industrialized West.

Is There Any Good News?

Although world population growth continues, it appears that the rate of growth has slowed somewhat. It’s common knowledge among econo- mists that as income and education increase, family size decreases, and as infant and childhood mortality rates decrease, families have fewer chil- dren. In fact, one of the best strate- gies for reducing family size and thus world population is to educate girls and women. Educated women are more likely to be in the labor force and are better able to provide food for their families, seek health care for them- selves and their children, and practice family planning.

With decreases in family size and improvements in education and employment opportunities for both men and women throughout the world, we are also likely to see improvements in environmental conservation and habitat preservation. The small Central American country of Costa Rica has recognized the economic importance of its abundant and beautiful natural resources. By developing ecotourism as a means of generating income, Costa Rica has been able, for the present, to preserve much of its forests and wild- life. In fact, ecotourism has become its primary industry, and Costa Rica’s poverty levels are the lowest in Central America. Habitat destruction and pov- erty often go hand in hand. Although successes like those accomplished in Costa Rica can’t be replicated every- where, this small nation has been a model for making environmental con- cerns integral to social and economic development.

Annually since 2005, leaders from both developing and developed

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countries have come together to dis- cuss new ways of reducing global pov- erty, especially in sub-Saharan Africa. Additionally, some of the wealthiest people in the world (including Bill and Melinda Gates, George Soros, Warren Buffet, Richard Branson, and Ted Turner) have begun to invest their per- sonal fortunes to help reduce poverty and poor health and thus, to promote global peace and prosperity. Lastly, the degree of international cooperation shown at the 2010 conference on bio- diversity is a hopeful development that could be a foundation for slowing spe- cies extinctions and maintaining natu- ral habitats.

What should be obvious is that only by working together can nations and individuals hope to develop solu- tions to the world’s problems. As we discussed in Chapter 7, cooperation is important to survival in nonhuman primates, and this was no doubt true for our ancestors as well. The ques- tion now is whether or not we have the

collective will to see that our admirable goals are met. Many people believe that it’s our only hope.

Studies of human evolution have much to contribute to our understand- ing of how we, as a single species, came to exert such control over the destiny of our planet. It’s a truly phenomenal story of how a small apelike creature walking on two feet across the African savanna challenged nature by learn- ing to make stone tools. From these humble beginnings came large-brained humans who, instead of stone tools, now have telecommunications satel- lites, computers, and nuclear arsenals at their fingertips. The human story is indeed unique and wonderful. Our two feet have carried us not only across the plains of Africa but onto the polar caps, the ocean floor, and even on the surface of the moon! Surely, if we can accomplish so much in so short a time, we can act responsibly to preserve our home and the wondrous creatures that share it with us.

Scientists from all over the world have been collecting data on climate change for decades. In the last 30 years, attention has focused on understanding the nature and causes of global climate change. This information must be evaluated in the context of how the climate has changed over long periods of time (up to hundreds of thousands of years). For example, climatologists and other scientists collect data on the amount of CO₂ in the atmosphere by analyzing ice cores, especially from ice in Antarctica and Greenland. Atmospheric CO₂ is trapped in ice as it freezes; if the ice stays fro- zen, it is possible to melt it, collect the gas, and obtain a record of CO₂ concentrations dating as far back as 850,000 years. Climate scientists are also able to deter- mine the source of the CO₂ by measuring carbon iso-

topes. For example, an increase in one carbon isotope points to the burning of fossil fuels as the source of atmospheric CO₂). Using these methods, researchers can confirm with great accuracy that more green- house gases are currently present in the atmosphere than at any time in the last 800,000 years, and that the recent increase is due to the burning of fossil fuels by humans. In addition to ice cores, researchers use a variety of other methods to collect detailed informa- tion on how climate change is affecting the atmosphere as well as land and ocean environments. For example, the National Climate Data Center uses satellites, ships, buoys, weather stations, weather balloons, radar, and tree rings in its research.

How Do We Know?

483Critical Thinking Questions

▶▶ Humans are the product of millions of years of biocultural evolution; but in just the last few hun- dred years we have exerted a huge influence on other life-forms and the planet itself. No other organism in the earth’s history has had such an impact.

▶▶ A major contributor to the scope of recent human disruptions of the earth’s ecosystems is population growth.

▶▶ Probably the most immediate and crucial chal- lenge we face is to reduce our influence on global climate change.

Summary of Main Topics

1. What effects have recent population growth caused in the city or area in which you live? What do you think will happen in your local area, to the country, and to the planet if population growth continues?

2. Why do most scientists support the conclusion that CO₂ emissions are the primary cause of global climate change? If you think this conclusion is not

correct, can you point to a body of scientific evi- dence that supports your view?

3. What do you personally think individuals, large corporations, and world leaders should do to address the world’s environmental problems?

4. Do you think that it’s important to preserve biodi- versity? Why or why not?

Critical Thinking Questions

484

Frontal

Maxilla

Mandible

Clavicle

Scapula

Sternum

Ribs

Thoracic vertebrae (12)

Humerus

Ulna

Radius

Carpals (8)

Metacarpals (5)

Phalanges (14)

Parietal Temporal Zygomatic Occipital

Cervical vertebrae (7)

Lumbar vertebrae (5)

Ilium

Sacrum

Pubis

Ischium

Femur

Patella

Tibia

Fibula

Tarsals (7) Metatarsals (5)

Phalanges (14)

▲ Figure A–1 Human skeleton (Homo sapiens)—bipedal hominin.

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Atlas of Primate Skeletal Anatomy

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▲ Figure A-2 Chimpanzee skeleton (Pan troglodytes)—knuckle-walking ape.

Frontal

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Mandible

Humerus

Ilium

Radius

Ulna

Carpals

Metacarpals

Phalanges

Parietal

Temporal

Cervical vertebrae Clavicle

Thoracic vertebrae

Sternum

Lumbar vertebrae

Sacrum

Pubis

Ischium

Femur

Patella

Tibia Fibula Tarsals Metatarsals

Occipital

CHIMPANZEE SKELETON

Phalanges

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▲ Figure A-3 Monkey skeleton (rhesus macaque; Macaca mulatta)—a typical quadrupedal primate.

Parietal

Frontal

Maxilla

Mandible Clavicle

Humerus

Radius

Ulna

Metacarpals

Phalanges

Carpals

Cervical vertebrae

Lumbar vertebrae

Ilium

Caudal vertebrae

Ischium Pubis

Femur

Patella

Fibula

MONKEY SKELETON

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Tibia

Tarsals

Metatarsals

Phalanges

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Parietal

Squamosal suture

Temporal

Occipital

Lambdoidal suture

Mandibular condyle

Occipitomastoidal suture

Mastoid process

External auditory meatus

Styloid process

Ascending ramus of mandible

Body of mandible

Coronal suture

Frontal

Sphenoid

Nasal

Ethmoid Lacrimal

Maxilla

Zygomatic

Anterior nasal spine

Incisors

Canine

Mental foramen

Premolars Molars

(b) LATERAL VIEWb

Parietal

Greater wing of sphenoid

Zygomatic

Maxilla

Infraorbital foramen Vomer (nasal septum)

Ascending ramus of mandible

Mental foramen

Body of mandible

Frontal

Temporal Lacrimal Ethmoid

Anterior nasal spine

Nasal bone

(a) FRONTAL (ANTERIOR) VIEWa

▲ Figure A-4 Human cranium.

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▲ Figure A-4 Human cranium.

(continued)

Parietal

Lambdoidal suture

External occipital protuberance

Sagittal suture

Lambda

Occipital

Mastoid process

Frontal

Coronal suture

Parietal

Sagittal suture

Lambdoidal suture Occipital

Inferior temporal line

Superior temporal line

Bregma

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Zygomatic bone

Zygomatic process of maxilla

Zygomatic process of temporal

Sphenoid

Pterygoid process

Carotid canal

Stylomastoid foramen Foramen magnum Occipital condyle

Parietal

Occipital

Zygomatic arch

Molars

Vomer

Foramen spinosum Styloid process External auditory meatus Jugular foramen

Hypoglossal canal

Mastoid foramen

Inferior nuchal line

Superior nuchal line

External occipital protuberance

Maxilla

Premolars

Canine Incisors

Palatine bone

Mandibular fossa

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▲ Figure A-5 Human vertebral column (lateral view) and repre sentative cervical, thoracic, and lumbar vertebrae (superior views).

C1 (Atlas)

C2 (Axis)

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T10

T11

T12

Sacrovertebral joint

Sacrum (5 elements)

Coccyx (4 elements)

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CERVICAL CURVE

THORACIC CURVE

LUMBAR CURVE

PELVIC CURVE

Vertebral arch

Vertebral foramen

Superior articular facet Transverse process Foramen transversorium

Transverse costal facet

Superior articular process

Superior costal facet

Body (centrum)

Spinous process

Superior articular process

Transverse process

Pedicle

Body (centrum)

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▲ Figure A-6 Pelvic girdles.

Iliac crest

Ilium

Sacroiliac joint

Sacrum

Acetabulum

Pubis

Ischium

Obturator foramen

Subpubic angle

Os coxae

HUMAN (b) CHIMPANZEEba

▲ Figure A-7 Hand anatomy.

Lunate Pisiform Triangular

Hamate

Metacarpals

Phalanges

Navicular

Lesser multangular

Greater multangular

Capitate Lunate Navicular

Greater multangular

Lesser multangular

1st metacarpal

Phalanges

Pisiform

Triangular

Hamate

Capitate

5th metacarpal

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▲ Figure A-8 Foot (pedal) anatomy.

Calcaneus

Cuboid

3rd cuneiform

Calcaneus

Talus

Navicular

1st cuneiform

2nd cuneiform

1st metatarsal

Cuboid

3rd cuneiform

Talus

Navicular

2nd cuneiform 1st cuneiform

Metatarsals

Phalanges

(a) HUMAN (DORSAL VIEW)

5th metatarsal

Phalanges

(b) CHIMPANZEEba

Transverse arch

Longitudinal arch

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The field of physical anthropology that is directly concerned with the analysis of skeletal remains is called osteology. Using an osteological perspective allows researchers to study skeletons of both human and nonhuman primates to under- stand the ways in which hominins are similar to, and distinct from, other pri- mates. Moreover, paleoanthropologists also use many of the same techniques to analyze the remains of fossil hominins (which mostly consist of teeth and bones). In more recent contexts, encompassing the last few thousand years, skeletal remains of Homo sapiens have been investigated by osteologists to learn about the size, nutritional status, and diseases present in prior human populations.

Two very important questions that osteologists ask when analyzing a skeleton are the sex and age of the individual. Such basic demographic variables as sex and age are crucial in any comprehensive osteological analysis, especially of human remains.

Sexing the Skeleton

During infancy and childhood, male and female skeletons do not differ much. Consequently, osteologists usually cannot determine the sex of a skeleton of someone who died before 13 to 15 years of age. However, during development, sex- ual dimorphism is increasingly manifested in the skeleton, making sex determi- nation feasible in adult remains, provided enough of the skeleton is present. We should mention that molecular techniques are sometimes able to detect the pres- ence of the Y chromosome from bone or dental tissue (thus determining that a skeleton is that of a male). Though not yet used widely, molecularly based sexing is becoming more common in osteological analyses.

The differences between male and female skeletons are most clearly expressed in the pelvis (pl., pelves), and this variation is due to the requirements of childbirth in females. In particular, during hominin evolution, the dual influences of bipedal locomotion and relatively large-brained newborns placed adaptive constraints on pelvic anatomy. As a result, in females the pelvis is generally broader and more splayed out than in males. The most useful criteria for sex determination are listed in Table B.1 and illustrated in Figure B-1. Although these criteria, taken together, are good indicators of sex, you should be aware that none, taken in isolation, is accurate in all cases. Moreover, this is not a complete listing of all traits used in sexing skeletons, although it does include those most commonly used.

There are also sex differences in cranial dimensions, most especially relating to facial proportions. However, these differences are not as consistent as those in the pelvis. Therefore, it is important to recognize patterns of cranial variation as they are expressed in different populations. The cranial features most commonly used for sex determination are listed in Table B.2 (see also Fig. B-2). These differences reflect the fact that in males, the skeleton is larger than in females. The bones are denser, and areas of muscle attachment are frequently more robust. However, such

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Appendix B

Sexing and Aging the Skeleton 493

Ventral arc

Wider subpubic

angle

Sacrum

Ischiopubic ramus

Narrower subpubic

angle

Male

Greater sciatic notch (<68°)Greater sciatic

notch (>68°)

Female

▲ Figure B-1 Male and female pelves compared.

Table B.1 Differences Between the Male and Female Pelvis Pelvic Characteristic Female Male

General Muscle attachments less robust; overall appearance sometimes less massive

Muscle attachments more robust; overall appearance sometimes more massive

Subpubic angle Wider (more than 90°) Narrower (less than 90°)

Greater sciatic notch Wider—more open (more than 68°) Narrower—more closed (less than 68°)

Ischiopubic ramus (medial view) Thinner Thicker

Ventral arc (elevated ridge on ventral surface of pubis)

Frequently present Absent

Sacrum Wider and straighter Narrower and more curved

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differences are not consistently expressed across various populations, and knowl- edge of relevant population variation is thus important in drawing reasonable determinations of sex.

Determining Age

During growth, the skeleton and dentition undergo developmental changes that occur within known age ranges. Thus, estimating age in individuals who were younger than 20 when they died is based primarily on the presence of deciduous (baby) and permanent teeth, the appearance of ossification centers of bones, and the fusion of the ends of long bones to bone shafts.

Dental Eruption Age estimation based on dental eruption is useful in individuals up to approxi- mately 15 years of age. The third molar (wisdom tooth) erupts after this time, but the age of eruption of this tooth (if it forms at all) is highly variable. Thus, the third molar is not a very reliable indicator of age except that its presence indicates that the individual was at least a young adult (Fig. B-3).

Mandible

Cranium

Supraorbital torus (browridge)

Mastoid process

MaleFemale

▲ Figure B-2 Male and female cranium and mandible.

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Table B.2 Differences Between the Male and Female Cranium Cranial Feature Female Male

Points of muscle attachment (e.g., mastoid process)

Less pronounced Larger, more pronounced

Supraorbital torus (browridge) Less pronounced or absent More pronounced

Supraorbital rim (upper margin of eye orbit)

Sharper More rounded

Palate More shallow Deeper

Sexing and Aging the Skeleton 495

Bone Growth The size of the long bones, the develop ment of secondary ossifi- cation centers (epiphyses), and the degree of fusion of epiphyses (ends of the bones) to diaphy ses (bone shafts) are just as important as dental erup- tion. Postcranial bones are preceded by a cartilage model that is gradu- ally replaced by bone, both in the diaphyses and the secondary centers (epiphyses). In children and adoles- cents, bones continue to grow until the epiphyses fuse to the diaphyses. Because this fusion occurs within different age ranges in different bones, the age of an individual can be estimated by determining which epiphy ses have fused and which have not (Fig. B-4). The character- istic undulating appearance of the unfused surfaces helps differentiate immature elements from the broken end of a mature bone.

(a) Birth: The crowns for all the deciduous teeth (shown in color) are present; no roots, however, have yet formed.

Gumline

(b) 2 years: All deciduous teeth (shown in color) are erupted; the first permanent molars and permanent incisors have unerupted crowns but no roots.

Third molar

First permanent molar crown

Head fuses to shaft: males aged 16 to 18, females aged 15 to 17

Greater tubercle fuses to head at 2 to 4 years

Birth

(b) 5 years

10 years (d) 15 years (e) 16+ years

Trochlea fuses to lower shaft: males aged 14 to 16, females aged 13 to 15

Medial epicondyle fuses: males aged 16 to 18, females aged 15 to 17

Proximal epiphysis

Diaphysis

c ed

◀ Figure B-4 Skeletal age: epiphyseal union in the humerus. Some regions of the humerus exhibit some of the earliest fusion centers in the body, while others are among the latest to complete fusion (not until late adolescence).

▲ Figure B-3 Dental development.

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Other Skeletal Changes Once a person has reached physiological maturity (by the early 20s), determina- tions of age become more difficult and less precise. Several techniques are used, and these are based on the occurrence of progressive, regular changes in the face of the pubic symphysis (the most common technique), in the sternal ends of the ribs, and in the auricular surface of the ilium (where the ilium articulates with the sacrum). Other indicators are closure of the cranial sutures and cellular changes that are determined by microscopic examination of cross sections of long bones. Degenerative changes, such as arthritis, osteoporosis, and wear of dental enamel, can also aid in the determination of relative age (older versus younger), but they provide imprecise estimates. In fact, it is very difficult to age the skeletons of adults accurately. For example, the presence of severe tooth wear would imply that the individual was not young, but enamel attrition varies between populations and depends on many factors, including diet. Moreover, the appearance of many degenerative changes is influenced by disease, trauma, and the biological makeup of individuals. Thus, at present, osteologists must be content to use broad age ranges when estimating age at death in mature skeletons.

Pubic Symphyseal Face The face of the pubic symphysis in young individuals is characterized by a billowing surface (with ridges and furrows) such as that seen on the surface of an epiphysis (Fig. B-5). The symphyseal face undergoes regular age- related changes from the age of about 18 onward.

The first aging technique based on alterations of the pubic symphysis was developed by T. W. Todd (1920, 1921), utilizing dissection room cadavers. McKern and Stewart (1957) developed a technique by analyzing a sample of American males killed in the Korean War. Both of the samples from which these systems were derived, however, had limitations. The dissection room sample used by Todd contained some individuals of uncertain age, and the Korean War sample was predominantly made up of young white males, with few being older than 35.

More recently, a system has been developed by Judy Suchey and colleagues (Katz and Suchey, 1986) based on very well-documented autopsy samples of males and females. These samples have proved more representative of the general popu- lation than the earlier samples. Because this technique is derived from data col- lected from a large sample of people of known age at death, it is currently the most accurate method available for estimating age in adult human skeletal remains.

Pubic symphysis

(a) Position of the pubic symphysis.

(b) Age 21. The face of the symphysis shows the typical “billowed” appearance of a young joint; no rim present.

ba c

▼ Figure B-5 Skeletal age: remodeling of the pubic symphysis. This area of the pelvis shows system- atic changes progressively throughout adult life. Two of these stages are shown in (b) and (c).

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acclimatization Physiological responses to changes in the environ- ment that occur during an individual’s lifetime. Such responses may be tem- porary or permanent, depending on the duration of the environmental change and when in the individual’s life it occurs. The capacity for acclimatization may typify an entire population or species, and because it’s under genetic influence, it’s subject to evolutionary factors such as natural selection and genetic drift.

Acheulian (ash´-oo-lay-en) Pertaining to a stone tool industry from the Early and Middle Pleistocene; characterized by a large proportion of bifa- cial tools (flaked on both sides). Acheulian tool kits are common in Africa, Southwest Asia, and western Europe, but they’re thought to be less common elsewhere. Also spelled Acheulean.

adaptation An anatomical, physiological, or behavioral response of organisms or populations to the environment. Adaptations result from evolu- tionary change (specifically as a result of natural selection).

adaptive niche An organism’s entire way of life: where it lives, what it eats, how it gets food, how it avoids predators, and so on.

adaptive radiation The relatively rapid expansion and diversification of life-forms into new ecological niches.

adolescent growth spurt The period during adolescence when well-nourished teens typically increase in stature at greater rates than at other times in the life cycle.

affiliative behaviors Amicable associations between individuals. Affiliative behaviors, such as grooming, reinforce social bonds and promote group cohesion.

allele frequency In a population, the percentage of all the alleles at a locus accounted for by one specific allele.

alleles Alternate forms of a gene. Alleles occur at the same locus on paired chromosomes and thus govern the same trait, but because they’re dif- ferent, their action may result in different expressions of that trait.

altruism Actions that benefit another individual but at some potential risk or cost to oneself.

amino acids Small molecules that are the components of proteins.

analogies Similarities between organisms based strictly on common function, with no assumed common evolutionary descent.

ancestral Referring to characters inherited by a group of organisms from a remote ancestor and thus not diagnostic of groups (lineages) that diverged after the character first appeared; also called primitive.

anthropocentric Viewing nonhuman organisms in terms of human experience and capabilities. Emphasizing the importance of humans over everything else.

anthropoids Members of the primate infraorder Anthropoidea (pro- nounced “an-throw-poid´-ee-uh”), which includes monkeys, apes, and humans.

anthropology The field of inquiry that studies human culture and evo- lutionary aspects of human biology; includes cultural anthropology, archaeol- ogy, linguistics, and physical, or biological, anthropology.

antigens Large molecules found on the surface of cells. Several different loci govern various antigens on red and white blood cells. (Foreign antigens provoke an immune response.)

applied anthropology The practical application of anthropological and archaeological theories and techniques. For example, many biological anthropologists work in the public health sector.

arboreal Tree living; adapted to life in the trees.

artifacts Objects or materials made or modified for use by hominins. The earliest artifacts are usually tools made of stone or occasionally bone.

Aurignacian Pertaining to an Upper Paleolithic stone tool industry in Europe beginning at about 40,000 ya.

autonomic Pertaining to physiological responses not under voluntary control. An example in chimpanzees would be the erection of body hair during excitement. Blushing is a human example. Both convey information regarding emotional states, but neither is deliberate, and communication isn’t intended.

autosomes All chromosomes except the sex chromosomes.

balanced polymorphism The maintenance of two or more alleles in a population due to the selective advantage of the heterozygote.

behavior Anything organisms do that involves action in response to internal or external stimuli; the response of an individual, group, or species to its environment. Such responses may or may not be deliberate, and they aren’t necessarily the result of conscious decision making (which is absent in single-celled organisms, insects, and many other species).

behavioral ecology The study of the evolution of behavior, emphasiz- ing the role of ecological factors as agents of natural selection. Behaviors and behavioral patterns have been favored because they increase the reproduc- tive fitness of individuals (i.e., they are adaptive) in specific environmental contexts.

bilophodont Referring to molars that have four cusps oriented in two parallel rows, resembling ridges, or “lophs.” This trait is characteristic of Old World monkeys.

binocular vision Vision characterized by overlapping visual fields provided by forward-facing eyes. Binocular vision is essential to depth perception.

Glossary

Glossary498

binomial nomenclature (binomial, meaning “two names”) In tax- onomy, the convention established by Carolus Linnaeus whereby genus and species names are used to refer to living things. For example, Homo sapiens refers to human beings.

bioarchaeology The study of skeletal remains from archaeological sites.

biocultural evolution The mutual interactive evolution of human biology and culture; the concept that biology (anatomy, neurological attri- butes, etc.) makes culture possible and that developing culture further influences the direction of biological evolution; this is a basic concept in understanding the unique components of human evolution.

biological continuity A biological continuum. When expressions of a phenomenon continuously grade into one another so that there are no dis- crete categories, they exist on a continuum. Color is one such phenomenon, and life-forms are another.

biological continuum Refers to the fact that organisms are related through common ancestry and that behaviors and traits seen in one species are also seen in others to varying degrees. (When expressions of a phenome- non continuously grade into one another so that there are no discrete catego- ries, they are said to exist on a continuum. Color is one such phenomenon.)

biological determinism The concept that phenomena, including various aspects of behavior (e.g., intelligence, values, morals) are governed by biological (genetic) factors; the inaccurate association of various behavioral attributes with certain biological traits, such as skin color.

biological species concept A depiction of species as groups of individuals capable of fertile interbreeding but reproductively isolated from other such groups.

biostratigraphic/faunal correlation A method of dating strata that relates the fossil content of an unknown stratum to a like one that has been securely chronometrically dated.

biostratigraphy A relative dating technique based on the regular changes seen in evolving groups of animals as well as the presence or absence of particular species.

bipedally On two feet; walking habitually on two legs.

blanks In archaeology, stones suitably sized and shaped to be further worked into tools.

brachiation Arm swinging, a form of locomotion used by some pri- mates. Brachiation involves hanging from a branch and moving by alternately swinging from one arm to the other.

breeding isolates Populations that are clearly isolated geographically and/or socially from other breeding groups.

burins Small, chisel-like tools with a pointed end; thought to have been used to engrave bone, antler, ivory, or wood.

catarrhine Member of Catarrhini, a parvorder of Primates, one of the three major divisions of the suborder Haplorhini. It contains the Old World monkeys, apes, and humans.

catastrophism The view that the earth’s geological landscape is the result of violent cataclysmic events. Cuvier promoted this view, especially in opposition to Lamarck.

Cercopithecidae The taxonomic family that includes all Old World monkeys.

cercopithecines Common name for members of the subfamily of Old World monkeys that includes baboons, macaques, and guenons.

Chatelperronian Pertaining to an Upper Paleolithic industry found in France and Spain, containing blade tools and associated with Neandertals.

Chordata The phylum of the animal kingdom that includes vertebrates.

Christian fundamentalists Adherents to a movement in American Protestantism that began in the early twentieth century. This group holds that the teachings of the Bible are infallible and should be taken literally.

chromosomes Discrete structures composed of DNA and proteins found only in the nuclei of cells. Chromosomes are visible under magnification only during certain phases of cell division.

chronometric dating (chrono, meaning “time,” and metric, meaning “measure”) A dating technique that gives an estimate in actual numbers of years; also known as absolute dating.

clade A group of organisms sharing a common ancestor. The group includes the common ancestor and all descendants.

cladistics An approach to classification that attempts to make rigor- ous evolutionary interpretations based solely on analysis of certain types of homologous characters (those considered to be derived characters).

cladogram A chart showing evolutionary relationships as determined by cladistic analysis. It’s based solely on interpretation of shared derived charac- ters. It contains no time component and does not imply ancestor-descendant relationships.

classification In biology, the ordering of organisms into categories, such as orders, families, and genera, to show evolutionary relationships.

clones Organisms that are genetically identical to another organism. The term may also be used to refer to genetically identical DNA segments, mol- ecules, or cells.

codominance The expression of two alleles in heterozygotes. In this situation, neither allele is dominant or recessive, so they both influence the phenotype.

codons Triplets of messenger RNA bases that code for specific amino acids during protein synthesis.

colobines Common name for members of the subfamily of Old World monkeys that includes the African colobus monkeys and Asian langurs.

communication Any act that conveys information to another individ- ual. Frequently, the result of communication is a change in the behavior of the recipient. Communication may not be deliberate but may instead be the result of involuntary processes or a secondary consequence of an intentional action.

complementary In genetics, referring to the fact that DNA bases form pairs (called base pairs) in a precise manner. For example, adenine can bond only to thymine. These two bases are said to be complementary because one requires the other to form a complete DNA base pair.

context The environmental setting where an archaeological trace is found. Primary context is the setting in which the archaeological trace was originally deposited. A secondary context is one to which it has been moved (such as by the action of a stream).

continental drift The movement of continents on sliding plates of the earth’s surface. As a result, the positions of large landmasses have shifted drastically during the earth’s history.

Glossary 499

continuum A set of relationships in which all components fall along a single integrated spectrum (for example, color). All life reflects a single bio- logical continuum.

core area The portion of a home range containing the highest concentra- tion and most reliable supplies of food and water. The core area is defended.

core A stone reduced by flake removal. A core may or may not itself be used as a tool.

crown group All of the taxa that come after a major speciation event. Crown groups are easier to identify than stem groups because the members possess the clade’s shared derived traits.

culture Behavioral aspects of human adaptation, including technology, traditions, language, religion, marriage patterns, and social roles. Culture is a set of learned behaviors transmitted from one generation to the next by non- biological (i.e., nongenetic) means.

cusps The bumps on the chewing surface of premolars and molars.

cytoplasm The semifluid, gel-like substance contained within the cell membrane. The nucleus and numerous structures involved with cell function are found within the cytoplasm.

data (sing., datum) Facts from which conclusions can be drawn; scientific information.

dental formula Numerical device that indicates the number of each type of tooth in each side of the upper and lower jaws.

derived (modified) Referring to characters that are modified from the ancestral condition and thus diagnostic of particular evolutionary lineages.

direct percussion Striking a core or flake with a hammerstone.

displays Sequences of repetitious behaviors that serve to communicate emotional states. Nonhuman primate displays are most frequently associated with reproductive or agonistic behavior; examples include chest slapping in gorillas or, in male chimpanzees, dragging and waving branches while charg- ing and threatening other animals.

diurnal Active during the day.

DNA (deoxyribonucleic acid) The double-stranded molecule that contains the genetic code. DNA is a main component of chromosomes.

dominance hierarchies Systems of social organization wherein individuals within a group are ranked relative to one another. Higher-ranking animals have greater access to preferred food items and mating partners than lower-ranking individuals. Dominance hierarchies are sometimes called “pecking orders.”

dominant In genetics, describing a trait governed by an allele that’s expressed in the presence of another allele (i.e., in heterozygotes). Dominant alleles prevent the expression of recessive alleles in heterozygotes. (This is the definition of complete dominance.)

ecological Pertaining to the relationships between organisms and all aspects of their environment (temperature, predators, nonpredators, vegeta- tion, availability of food and water, types of food, disease organisms, para- sites, etc.).

ecological niche The position of a species within its physical and biological environments. A species’ ecological niche is defined by such com- ponents as diet, terrain, vegetation, type of predators, relationships with other species, and activity patterns, and each niche is unique to a given species. Together, ecological niches make up an ecosystem.

ecological species concept The concept that a species is a group of organisms exploiting a single niche. This view emphasizes the role of natural selection in separating species from one another.

empathy The ability to identify with the feelings and thoughts of another individual.

empirical Relying on experiment or observation; from the Latin empiri- cus, meaning “experienced.”

encephalization The proportional size of the brain relative to some estimate of overall body size, such as weight. More precisely, the term refers to increases in brain size beyond what would be expected given the body size of a particular species.

endemic Continuously present in a population.

endogamy Mating with individuals from the same group.

endothermic (endo, meaning “within” or “internal”) Able to maintain internal body temperature by producing energy through metabolic processes within cells; characteristic of mammals, birds, and perhaps some dinosaurs.

enzymes Specialized proteins that initiate and direct chemical reactions in the body.

epigenetics Changes in phenotype that are not related to changes in underlying DNA.

epigenome The instructions that determine which genes are expressed in cells and how.

epochs Categories of the geological time scale; subdivisions of periods. In the Cenozoic era, epochs include the Paleocene, Eocene, Oligocene, Miocene, and Pliocene (from the Tertiary Period) and the Pleistocene and Holocene (from the Quaternary Period).

essential amino acids The 9 (of 22) amino acids that must be obtained from the food we eat because they are not synthesized in the body in sufficient amounts.

ethnocentric Viewing other cultures from the inherently biased per- spective of one’s own culture. Ethnocentrism often causes other cultures to be seen as inferior to one’s own.

ethnographies Detailed descriptive studies of human societies. In cul- tural anthropology, an ethnography is traditionally the study of a non-Western society.

eugenics The philosophy of “race improvement” through the forced sterilization of members of some groups and increased reproduction among others; an overly simplified, often racist view that’s now discredited.

euprimates “True primates.” This term was coined by Elwyn Simons in 1972.

evaporative cooling A physiological mechanism that helps prevent the body from overheating. It occurs when perspiration is produced from sweat glands and then evaporates from the surface of the skin.

evolution A change in the genetic structure of a population. The term is also frequently used to refer to the appearance of a new species.

evolutionary medicine The application of principles of evolution to aspects of medical research and practice.

evolutionary systematics A traditional approach to classification (and evolutionary interpretation) in which presumed ancestors and descen- dants are traced in time by analysis of homologous characters.

Glossary500

exogamy Mating pattern whereby individuals obtain mates from groups other than their own.

exons Segments of genes that are transcribed and are involved in protein synthesis. (The prefix ex denotes that these segments are expressed.)

fertility The ability to conceive and produce healthy offspring.

fitness Pertaining to natural selection, a measure of the relative repro- ductive success of individuals. Fitness can be measured by an individual’s genetic contribution to the next generation compared with that of other indi- viduals. The terms genetic fitness, reproductive fitness, and differential net reproductive success are also used.

fixity of species The notion that species, once created, can never change is diametrically opposed to theories of biological evolution.

flake A thin-edged fragment removed from a core.

flexed The position of the body in a bent orientation, with arms and legs drawn up to the chest.

forensic anthropology An applied anthropological approach deal- ing with legal matters. Forensic anthropologists work with coroners and oth- ers in identifying and analyzing human remains.

fossils Traces or remnants of organisms found in geological beds on the earth’s surface.

founder effect A type of genetic drift in which allele frequencies are altered in small populations that are taken from larger populations or are rem- nants of the latter.

frugivorous Having a diet composed primarily of fruits.

gametes Reproductive cells (eggs and sperm in animals) developed from precursor cells in ovaries and testes.

gene flow Exchange of genes between populations.

gene pool All of the genes shared by the reproductive members of a population.

genetic Having to do with the study of gene structure and action and the patterns of inheritance of traits from parent to offspring. Genetic mechanisms are the foundation of evolutionary change.

genetic drift Evolutionary changes, or changes in allele frequencies, produced by random factors in small populations. Genetic drift is a result of small population size.

genome The entire genetic makeup of an individual or species. In humans, it’s estimated that the human genome comprises about 3 billion DNA bases.

genotype The genetic makeup of an individual. Genotype usually refers to an organism’s genetic makeup (or alleles) at a particular locus.

genus (pl., genera) A group of closely related species.

geological time scale The organization of earth history into eras, periods, and epochs; commonly used by geologists and paleoanthropologists.

glaciations Climatic intervals when continental ice sheets cover much of the northern continents. Glaciations are associated with colder temperatures in northern latitudes and more arid conditions in southern latitudes, most notably in Africa.

grooming Picking through fur to remove dirt, parasites, and other mate- rials that may be present. Social grooming is common among primates and reinforces social relationships.

half-life The time period in which one-half the amount of a radioactive isotope is converted chemically to a daughter product. For example, after 1.25 billion years, half the potassium-40 (40K) remains; after 2.5 billion years, one-fourth remains.

haplorhines (hap-lore´-ines) Members of the primate suborder Haplorhini, which includes tarsiers, monkeys, apes, and humans.

Haplorhini (hap’-lo-rin-ee) The primate suborder that includes tarsiers, monkeys, apes, and humans. (Colloquial form: haplorhine.)

Hardy-Weinberg theory of genetic equilibrium The mathematical relationship expressing—under conditions in which no evolu- tion is occurring—the predicted distribution of alleles in populations; the central theorem of population genetics.

hemisphere One of the two halves of the cerebrum, which are con- nected by a dense mass of fibers. (The cerebrum is the large rounded outer portion of the brain.)

hemoglobin A protein molecule that occurs in red blood cells and binds to oxygen molecules.

heterodont Having different kinds of teeth; characteristic of mammals, whose teeth consist of incisors, canines, premolars, and molars.

heterozygous Having different alleles at the same locus on members of a pair of chromosomes.

Holocene The most recent epoch of the Cenozoic. Following the Pleistocene, it’s estimated to have begun 10,000 years ago.

homeobox genes An evolutionarily ancient family of regulatory genes that directs the development of the overall body plan and the segmentation of body tissues. There are at least 20 families of homeobox genes.

homeostasis A condition of balance, or stability, within a biological system, maintained by the interaction of physiological mechanisms that com- pensate for changes (both external and internal).

hominins Colloquial term for members of the evolutionary group that includes modern humans and now-extinct bipedal relatives.

hominoids Members of the primate superfamily (Hominoidea), which includes apes and humans.

homologies Similarities between organisms based on descent from a common ancestor.

homoplasy (homo, meaning “same,” and plasy, meaning “growth”) The separate evolutionary development of similar characteristics in different groups of organisms.

homozygous Having the same allele at the same locus on both mem- bers of a pair of chromosomes.

hormones Substances (usually proteins) that are produced by special- ized cells and that travel to other parts of the body, where they influence chemical reactions and regulate various cellular functions.

Human Genome Project An international effort aimed at sequenc- ing and mapping the entire human genome, completed in 2003.

Glossary 501

hybrids Offspring of parents who differ from each other with regard to certain traits or certain aspects of genetic makeup; also known as heterozygotes.

hypotheses (sing., hypothesis) A provisional explanation of a phenom- enon. Hypotheses require verification or falsification through testing.

hypoxia Insufficient levels of oxygen in body tissues; oxygen deficiency.

inbreeding A type of nonrandom mating in which relatives mate more often than predicted under random mating conditions.

incest avoidance In animals, the tendency not to mate with close relatives. This tendency may be due to various social and ecological factors that keep the individuals apart. There may also be innate factors that lead to incest avoidance, but these aren’t well understood.

intelligence Mental capacity; ability to learn, reason, or comprehend and interpret information, facts, relationships, and meanings; the capacity to solve problems, whether through the application of previously acquired knowledge or through insight.

interglacials Climatic intervals when continental ice sheets are retreat- ing, eventually becoming much reduced in size. Interglacials in northern lati- tudes are associated with warmer temperatures, while in southern latitudes the climate becomes wetter.

interspecific Between species; refers to variation beyond that seen within the same species to include additional aspects seen between two dif- ferent species.

intraspecific Within species; refers to variation seen within the same species.

introns Segments of genes that are initially transcribed and then deleted. Because introns are not expressed, they aren’t involved in protein synthesis.

island hopping Traveling from one island to the next.

K-selected Pertaining to K-selection, an adaptive strategy whereby individuals produce relatively few offspring, in whom they invest increased parental care. Although only a few infants are born, chances of survival are increased for each one because of parental investments of time and energy. Birds, elephants, and canids (wolves, coyotes, and dogs) are examples of K-selected nonprimate species.

karyotype The chromosomes of an individual, or what is typical of a species, viewed microscopically and displayed in a photograph. The chro- mosomes are arranged in pairs and according to size and position of the centromere.

knappers People (frequently archaeologists) who make stone tools.

lactase persistence In adults, the continued production of lactase, the enzyme that breaks down lactose (milk sugar). This allows adults in some human populations to digest fresh milk products. The discontinued produc- tion of lactase in adults leads to lactose intolerance and the inability to digest fresh milk.

language A standardized system of arbitrary vocal sounds, written sym- bols, and gestures used in communication.

last common ancestor (LCA) The final evolutionary link between two related groups.

Late Pleistocene The portion of the Pleistocene epoch beginning 125,000 ya and ending approximately 10,000 ya.

life history traits Characteristics and developmental stages that influ- ence reproductive rates. Examples include longevity, age at sexual maturity, length of time between births, etc.

lithic (lith, meaning “stone”) Referring to stone tools.

locus (pl., loci) (lo’-kus, lo-sigh’) The position or location on a chromo- some where a given gene occurs. The term is sometimes used interchange- ably with gene.

macroevolution Changes produced only after many generations, such as the appearance of a new species.

Magdalenian Pertaining to the final phase of the Upper Paleolithic stone tool industry in Europe.

malnutrition A diet insufficient in quality (i.e., lacking some essential component) to support normal health.

matrilines Groups that consist of a female, her daughters, and their off- spring. Matrilines are common among macaques.

meiosis Cell division in specialized cells in ovaries and testes. Meiosis involves two divisions and results in four daughter cells, each containing only half the original number of chromosomes. These cells can develop into gametes.

menarche The first menstruation in girls, usually occurring in the early to midteens.

Mendelian traits Characteristics that are influenced by alleles at only one genetic locus. Examples include many blood types, such as ABO. Many genetic disorders, including sickle-cell anemia and Tay-Sachs disease, are also Mendelian traits.

menopause The end of menstruation in women, usually occurring at around age 50.

messenger RNA (mRNA) A form of RNA that’s assembled on a sequence of DNA bases. It carries the DNA code to the ribosome during pro- tein synthesis.

metabolism The chemical processes within cells that break down nutrients and release energy for the body to use. (When nutrients are broken down into their component parts, such as amino acids, energy is released and made available for the cells to use.)

microevolution Small changes occurring within species, such as changes in allele frequencies.

microliths (micro, meaning “small,” and lith, meaning “stone”) Small stone tools usually produced from narrow blades punched from a core; found especially in Africa during the latter part of the Pleistocene.

microwear Polishes, striations, and other diagnostic microscopic changes on the edges of stone tools.

Middle Pleistocene The portion of the Pleistocene epoch beginning 780,000 ya and ending 125,000 ya.

mineralization The process in which parts of animals (or some plants) become transformed into stonelike structures. Mineralization usually occurs very slowly, as water carrying minerals—such as silica or iron—seeps into the tiny spaces within a bone. In some cases, the original minerals within the bone or tooth can be completely replaced, molecule by molecule, with other minerals.

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mitochondria (sing., mitochondrion) Structures contained within the cytoplasm of eukaryotic cells that convert energy, derived from nutrients, to a form that can be used by the cell.

mitochondrial DNA (mtDNA) DNA found in the mitochondria. Mitochondrial DNA is inherited only from the mother.

mitosis Simple cell division; the process by which somatic cells divide to produce two identical daughter cells.

molecules Structures made up of two or more atoms. Molecules can combine with other molecules to form more complex structures.

monophyletic Referring to an evolutionary group (clade) composed of descendants all sharing a common ancestor.

morphology The form (shape, size) of anatomical structures; can also refer to the entire organism.

mosaic evolution A pattern of evolution in which the rate of evolution in one functional system varies from that in other systems. For example, in hominin evolution, the dental system, locomotor system, and neurological system (especially the brain) all evolved at markedly different rates.

Mousterian Pertaining to the stone tool industry associated with Neandertals and some modern H. sapiens groups; also called Middle Paleolithic. This industry is characterized by a larger proportion of flake tools than is found in Acheulian tool kits.

multidisciplinary Pertaining to research involving mutual contri- butions and the cooperation of experts from various scientific fields, or disciplines.

mutation A change in DNA. The term can refer to changes in DNA bases (specifically called point mutations) as well as to changes in chromosome number and/or structure.

natal group The group in which animals are born and raised. (Natal per- tains to birth.)

natural selection The most critical mechanism of evolutionary change, first described by Charles Darwin; the term refers to genetic change or changes in the frequencies of certain traits in populations due to differen- tial reproductive success between individuals.

neocortex The more recently evolved portions of the cortex (outer layer) of the brain that are involved with higher mental functions and composed of areas that integrate incoming information from different sensory organs.

neural tube In early embryonic development, the anatomical structure that develops to form the brain and spinal cord.

nocturnal Active during the night.

nonrandom mating Pattern of mating in which individuals choose mates preferentially, with mate choice based on criteria such as social sta- tus, ethnicity, or biological relationship. In nonrandom mating, an individual doesn’t have an equal chance of mating with all other individuals in the group.

nuchal torus (nuke´-ul) (nucha, meaning “neck”) A projection of bone in the back of the cranium where neck muscles attach. These muscles hold up the head.

nucleotides Basic units of the DNA molecule, composed of a sugar, a phosphate, and one of four DNA bases.

nucleus A structure (organelle) found in all eukaryotic cells. The nucleus contains DNA and RNA, among other things.

olfaction The sense of smell.

omnivorous Having a diet consisting of many food types, such as plant materials, meat, and insects.

orthograde Referring to an upright body position. This term relates to the position of the head and torso during sitting, climbing, etc., and doesn’t necessarily mean that an animal is bipedal.

osteology The study of skeletal material. Human osteology focuses on the interpretation of skeletal remains from archaeological sites, skeletal anatomy, bone physiology, and growth and development. Some of the same techniques are used in paleoanthropology to study early hominins.

paleoanthropology The interdisciplinary approach to the study of earlier hominins—their chronology, physical structure, archaeological remains, habitats, and so on.

paleomagnetism Dating method based on the earth’s shifting mag- netic pole.

paleopathology The branch of osteology that studies the evidence of disease and injury in human skeletal (or, occasionally, mummified) remains from archaeological sites.

paleoprimatologists Anthropologists specializing in the study of the nonhuman primate fossil record.

paleospecies Species defined from fossil evidence, often covering a long time span.

paradigm shift A transition from one conceptual framework or prevail- ing and widely accepted viewpoint to another. The acceptance of the discov- ery that the sun is the center of our solar system is an example of a paradigm shift.

parvorder A taxonomic group below infraorder.

pathogens Substances or microorganisms, such as bacteria, fungi, or viruses, that cause disease.

pedigree chart A diagram showing family relationships. It’s used to trace the hereditary pattern of particular genetic (usually Mendelian) traits.

phenotypes The observable or detectable physical characteristics of an organism; the detectable expressions of genotypes, frequently influenced by environmental factors.

phylogenetic tree A chart showing evolutionary relationships as determined by evolutionary systematics. It contains a time component and implies ancestor-descendant relationships.

phytoliths (phyto, meaning “hidden,” and lith, meaning “stone”) Microscopic silica structures formed in the cells of many plants, particularly grasses.

pigment In this context, molecules that influence the color of skin, hair, and eyes.

placental A type (subclass) of mammal. During the Cenozoic, placentals became the most widespread and numerous mammals and today are repre- sented by upward of 20 orders, including the primates.

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platyrrhines Members of Platyrrhini, a parvorder of Primates, one of the three major divisions of the suborder Haplorhini. These include only the New World monkeys.

pleiotropic genes Genes that have more than one effect; genes that have different effects at different times in the life cycle.

pleiotropy A situation where the action of one gene affects several dif- ferent traits.

Pleistocene The epoch of the Cenozoic from 1.8 mya until 10,000 ya. Frequently referred to as the Ice Age, this epoch is associated with continen- tal glaciations in northern latitudes.

point mutation A change in one of the four DNA bases.

polyandry A mating system wherein a female continuously associates with more than one male (usually two or three) with whom she mates. Among nonhuman primates, polyandry is seen only in marmosets and tamarins. It also occurs in a few human societies.

polygenic Referring to traits influenced by genes at two or more loci. Examples include stature, skin color, eye color, and hair color. Many polygenic traits are influenced by environmental factors such as nutrition and exposure to sunlight.

polygynous Pertaining to polygyny. A mating system in which a male mates with more than one female. This is the most common mating pattern found in mammals, including most primates.

polymerase chain reaction (PCR) A method of producing thou- sands of copies of a DNA sample.

polymorphisms Loci with more than one allele. Polymorphisms can be expressed in the phenotype as the result of gene action (as in ABO), or they can exist solely at the DNA level within noncoding regions.

polyphyletic Referring to an evolutionary group composed of descen- dants with more than one common ancestor (and thus not a true clade).

polytypic Referring to species composed of populations that differ in the expression of one or more traits.

population Within a species, a community of individuals where mates are usually found.

population genetics The study of the frequency of alleles, geno- types, and phenotypes in populations from a microevolutionary perspective.

postcranial Referring to all or part of the skeleton not including the skull. The term originates from the fact that in quadrupeds the body is posterior to the head; the term literally means “behind the head.”

pressure flaking A method of removing flakes from a core by pressing a pointed implement (e.g., bone or antler) against the stone.

primate paleontology The study of fossil primates, especially those that lived before the appearance of hominins.

primates Members of the mammalian order Primates (pronounced “pry- may´-tees”), which includes lemurs, lorises, tarsiers, monkeys, apes, and humans.

primatology The study of the biology and behavior of nonhuman pri- mates (lemurs, lorises, tarsiers, monkeys, and apes).

principle of independent assortment The distribution of one pair of alleles into gametes does not influence the distribution of another

pair. The genes controlling different traits are inherited independently of one another.

principle of segregation Genes (alleles) occur in pairs because chromosomes occur in pairs. During gamete formation, the members of each pair of alleles separate, so that each gamete contains one member of each pair.

principle of superposition In a stratigraphic sequence, the lower layers were deposited before the upper layers. Or, simply put, the stuff on top of a heap was put there last.

prosocial behaviors Actions that benefit other individuals and/or a society as a whole. Loosely speaking, the term “prosocial” is the opposite of “antisocial.”

proteins Three-dimensional molecules that serve a wide variety of func- tions through their ability to bind to other molecules.

protein synthesis The manufacture of proteins; that is, the assembly of chains of amino acids into functional protein molecules. Protein synthesis is directed by DNA.

quadrupedal Using all four limbs to support the body during locomo- tion; the basic mammalian (and primate) form of locomotion.

quantitatively Pertaining to measurements of quantity and including such properties as size, number, and capacity. When data are quantified, they’re expressed numerically and can be tested statistically.

r-selected Pertaining to r-selection, a reproductive strategy that empha- sizes relatively large numbers of offspring and reduced parental care com- pared with K-selected species. K-selection and r-selection are relative terms; for example, mice are r-selected compared with primates but K-selected compared with insects.

random assortment The chance distribution of chromosomes to daughter cells during meiosis. Along with recombination, random assortment is an important source of genetic variation (but not new alleles).

recessive Describing a trait that isn’t expressed in heterozygotes; it also refers to the allele that governs the trait. For a recessive allele to be expressed, an individual must have two copies of it (i.e., the individual must be homozygous).

recognition species concept A depiction of species in which the key aspect is the ability of individuals to identify members of their own species for purposes of mating (and to avoid mating with members of other species). In theory, this type of selective mating is a component of a species concept emphasizing mating and is therefore compatible with the biological species concept.

recombination The exchange of genetic material between paired chromosomes during meiosis; also called crossing over.

regulatory genes Genes that influence the activity of other genes. Regulatory genes direct embryonic development and are involved in physi- ological processes throughout life. They are critically important to the evolu- tionary process.

relativistic Viewing entities as they relate to something else. Cultural relativism is the view that cultures have merits within their own historical and environmental contexts.

replicate To duplicate. The DNA molecule is able to make copies of itself.

reproductive strategies Behaviors or behavioral complexes that have been favored by natural selection to increase individual reproductive

Glossary504

success. The behaviors need not be deliberate, and they often vary consider- ably between males and females.

reproductively isolated Pertaining to groups of organisms that, mainly because of genetic differences, are prevented from mating and pro- ducing offspring with members of other such groups. For example, dogs can- not mate and produce offspring with cats.

reproductive success The number of offspring an individual pro- duces and rears to reproductive age, or an individual’s genetic contribution to the next generation.

rhinarium (rine-air´-ee-um) The moist, hairless pad at the end of the nose seen in most mammalian species. The rhinarium enhances an animal’s ability to smell.

ribosomes Structures composed of a form of RNA called ribosomal RNA (rRNA) and protein. Ribosomes are found in a cell’s cytoplasm and are essen- tial to the manufacture of proteins.

RNA (ribonucleic acid) A single-stranded molecule similar in struc- ture to DNA. Three forms of RNA are essential to protein synthesis: messen- ger RNA (mRNA), transfer RNA (tRNA), and ribosomal RNA (rRNA)

savanna (also spelled savannah) A large flat grassland with scattered trees and shrubs. Savannas are found in many regions of the world with dry and warm-to-hot climates.

science A body of knowledge gained through observation and experi- mentation; from the Latin scientia, meaning “knowledge.”

scientific method An approach to research whereby a problem is identified, a hypothesis (provisional explanation) is stated, and that hypothesis is tested by collecting and analyzing data.

scientific testing The precise repetition of an experiment or expan- sion of observed data to provide verification; the procedure by which hypoth- eses and theories are verified, modified, or discarded.

sea ice maximum In the Arctic, the greatest amount of sea ice that is present in one year. It occurs in March at the end of winter, just as the ice stops forming and begins to melt.

sea ice minimum The least amount of ice that is present in the Arctic in one year. Sea ice is at its minimum in September, just as the summer melt- ing season ends but before the ice begins to form again.

selective breeding A practice whereby animal or plant breeders choose which individual animals or plants will be allowed to mate based on the traits (such as coat color or body size) they hope to produce in the off- spring. Animals or plants that don’t have the desirable traits aren’t allowed to breed.

selective pressures Forces in the environment that influence repro- ductive success in individuals.

semiorder The taxonomic category above suborder and below order.

senescence Decline in physiological function usually associated with aging.

sensory modalities Different forms of sensation (e.g., touch, pain, pressure, heat, cold, vision, taste, hearing, and smell).

sex chromosomes In mammals, the X and Y chromosomes.

females of the same population. Sexual dimorphism is very pronounced in many species, such as gorillas.

sexual selection A type of natural selection that operates on only one sex within a species. It’s the result of competition for mates, and it can lead to sexual dimorphism with regard to one or more traits.

shared derived Relating to specific character traits shared in common between two life-forms and considered the most useful for making evolution- ary interpretations.

sickle-cell anemia A severe inherited hemoglobin disorder in which red blood cells collapse when deprived of oxygen. It results from inheriting two copies of a mutant allele. The type of mutation that produces the sickle- cell allele is a point mutation.

sickle-cell trait Heterozygous condition where a person has one HbA allele and one HbS allele. Thus they have some normal hemoglobin.

sister groups The relationship of new clades that result from the split- ting of a single common lineage.

slash-and-burn agriculture A traditional land-clearing practice involving the cutting and burning of trees and vegetation. In many areas, fields are abandoned after a few years and clearing occurs elsewhere.

somatic cells Basically, all the cells in the body except those involved with reproduction.

speciation The process by which a new species evolves from an earlier species. Speciation is the most basic process in macroevolution.

species A group of organisms that can interbreed to produce fertile off- spring. Members of one species are reproductively isolated from members of all other species (i.e., they cannot mate with them to produce fertile offspring).

spina bifida A condition in which one or more of the vertebral arches fail to fuse and form a protective barrier around the spinal cord.

stable carbon isotopes Isotopes of carbon that are produced in plants in differing proportions, depending on environmental conditions. By analyzing the proportions of the isotopes contained in fossil remains of ani- mals (who ate the plants), it’s possible to reconstruct aspects of ancient diet and environments (particularly temperature and aridity).

stem group All of the taxa in a clade before a major speciation event. Stem groups are often difficult to recognize in the fossil record since they don’t often have the shared derived traits found in the crown group.

stereoscopic vision The condition whereby visual images are, to varying degrees, superimposed. This provides for depth perception, or view- ing the external environment in three dimensions. Stereoscopic vision is partly a function of structures in the brain.

stratigraphy Study of the sequential layering of deposits.

strepsirhines (strep-sir´-rines) Members of the primate suborder Strepsirhini, which includes lemurs and lorises.

Strepsirhini (strep’-sir-in-ee) The primate suborder that includes lemurs and lorises. (Colloquial form: strepsirhine.)

Glossary 505

stress In a physiological context, any factor that acts to disrupt homeosta- sis; more precisely, the body’s response to any factor that threatens its ability to maintain homeostasis.

subfossil Bone not old enough to have become completely mineralized as a fossil.

superorder A taxonomic group ranking above an order and below a class or subclass.

tandem repeats Short, adjacent segments of DNA within a gene that are repeated several times.

taphonomy (taphos, meaning “tomb”) The study of how bones and other materials came to be buried in the earth and preserved as fossils. Taphonomists study the processes of sedimentation, the action of streams, preservation properties of bone, and carnivore disturbance factors.

taxa (sing. taxon) A taxonomic group of any rank (e.g., species, family, or class).

taxonomy The branch of science concerned with the rules of classifying organisms on the basis of evolutionary relationships.

terrestrial Living and locomoting primarily on the ground.

territorial Pertaining to the protection of all or a part of the area occupied by an animal or group of animals. Territorial behaviors range from scent mark- ing to outright attacks on intruders.

territories Portions of an individual’s or group’s home range that are actively defended against intrusion, especially by members of the same species.

theory A broad statement of scientific relationships or underlying prin- ciples that has been substantially verified through the testing of hypotheses.

thermoluminescence (TL) (ther-mo-loo-min-ess´-ence) A tech- nique for dating certain archaeological materials (such as stone tools) that were heated in the past and that, upon reheating, release the stored energy of radioactive decay as light.

theropods Small- to medium-sized ground-living dinosaurs, dated to approximately 150 mya and thought to be related to birds.

transfer RNA (tRNA) A type of RNA that binds to specific amino acids and transports them to the ribosome during protein synthesis.

undernutrition A diet insufficient in quantity (calories) to support nor- mal health.

uniformitarianism The theory that the earth’s features are the result of long-term processes that continue to operate in the present just as they did in the past. Elaborated on by Lyell, this theory opposed catastrophism and greatly contributed to the concept of immense geological time.

Upper Paleolithic A cultural period usually associated with modern humans but also found with some Neandertals and distinguished by techno- logical innovation in various stone tool industries. Best known from western Europe, similar industries are also known from central and eastern Europe and Africa.

variation In genetics, inherited differences among individuals; the basis of all evolutionary change.

vasoconstriction Narrowing of blood vessels to reduce blood flow to the skin. Vasoconstriction is an involuntary response to cold and reduces heat loss at the skin’s surface.

vasodilation Expansion of blood vessels, permitting increased blood flow to the skin. Vasodilation permits warming of the skin and facilitates radia- tion of warmth as a means of cooling. Vasodilation is an involuntary response to warm temperatures, various drugs, and even emotional states (blushing).

vectors Agents that transmit disease from one carrier to another. Mosquitoes are vectors for malaria, just as fleas are vectors for bubonic plague.

vertebrates Animals with segmented, bony spinal columns; these include fishes, amphibians, reptiles (including birds), and mammals.

worldview General cultural orientation or perspective shared by the members of a society.

Y-5 molar Molar that has five cusps with grooves running between them, forming a Y shape. This is characteristic of hominoids.

zoonotic (zoh-oh-no´-tic) Pertaining to a zoonosis (pl., zoonoses), a dis- ease that’s transmitted to humans through contact with nonhuman animals.

zygomatics Cheekbones.

zygote A cell formed by the union of an egg cell and a sperm cell. It contains the full complement of chromosomes (in humans, 46) and has the potential of developing into an entire organism.

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532

Aboriginal populations, 367 Abrigo do Lagar Velho site, 377, 378 Absent permanent dentition, 84 Absolute dating, 264, 267 Acclimatization processes, 414–415, 426 Acheulian tool industry, 316, 323,

327–328, 340 Achondroplasia, 84, 85–86 Acquired characteristics, 30, 31 Adapis, 225 Adapoidea superfamily, 223–225 Adaptation, 5

African hominins, adaptive patterns of, 304

allele frequencies, shifts in, 100–101 bipedal adaptation, skeletal modifica-

tions and, 278–282 endothermic capability and, 129 generalized characteristics and, 131 morphological adaptations, 278 paleoanthropology and, 12 specialized characteristics and,

131–132 upper body erectness and, 278 See also Human adaptation; Primate

adaptations Adaptive niches, 139, 140–141 Adaptive radiation, 130–131 Adaptive significance, 13 Adaptive zones, 121 Adolescent growth spurt, 444 Aegyptopithecus, 233, 234, 237 Afar Locality (AL), 290, 292 Afar Triangle region, 285 Affiliative behaviors, 187–188, 210–212 Africa:

albinism and, 417 early hominins, adaptive patterns of,

304 early modern humans and, 368–371,

372, 373 malaria and, 102 melanin-producing allele and, 418,

419, 420 premodern humans and, 334–335, 338 primates in, 143, 160 sickle-cell anemia and, 101 two-stage migration model and, 367

Upper Paleolithic art and, 384–385 Upper Paleolithic industry and,

384, 385 See also Hominin origins

Afropithecus, 242, 244, 246 Aggressive behaviors, 186, 208–209 Agriculture:

agribusiness, 6, 72, 447–449, 479 animal products, growth hormones

and, 72 breeding stock and, 36, 60 declining human health and, 447–449 disease patterns, epidemiological tran-

sition and, 447–448 domesticated animals and, 10, 36, 37,

60, 427–428 food insecurity, trade/agricultural

policies and, 449 genetic manipulation and, 72 growth hormone use and, 72 habitat loss and, 159–160 insecticides/pesticides, misuse of, 479 malaria, expanded distribution of, 10 slash-and-burn agriculture, 408 subsistence agriculture, 6

Air pollution, 10, 39–40, 450, 480 Albinism, 84, 87–88, 91, 417 Alcohol abuse, 455 Alleles, 66, 70

allele frequency in populations, 94–95, 97, 100–101, 103

antigens and, 83 cross fertilization and, 80–81 dominant alleles, 84–85 heterozygous individuals, 80, 84, 102 homozygous individuals, 80, 83,

88, 101 human variation studies and, 394 Mendelian traits/discrete traits and,

83, 84 recessive alleles, 84 See also Population genetics

Allen’s rule, 421–422 Allia Bay site, 284 Altamira site, 382, 386 Altitude, 14, 425

acclimatization process and, 426

alleles, adaptive point mutations and, 426–427

developmental acclimatization and, 415, 426

glucose processing and, 426 hemoglobin production and, 414 high altitude stressors and, 425–426 hypoxia and, 425–426, 427 lighter skin, selection for, 417–419 oxygen availability and, 61 recent human adaptation to, 132 reproductive complications and, 426 See also Human adaptation

Altruism, 210–212 Amber, 122, 123 American Board of Forensic

Anthropology (ABFA), 21 American Civil Liberties Union (ACLU),

43 American Sign Language (ASL), 199 Amino acids, 54, 55

essential amino acids, 445 exons, coding process and, 57 heredity and, 58 mutation and, 61–63 See also DNA (deoxyribonucleic acid);

Protein synthesis; RNA (ribonucleic acid)

Amish microcephaly, 98–99 Amphibians, 128, 131 Amud site, 343, 344, 347, 354 Analogies, 110, 120, 202 Anatomy, 16–17, 18

argument from design and, 27 bipedal adaptation, skeletal modifica-

tions and, 278–282 body weight/stature table, 287 brachiation and, 145 catarrhine characteristic, 154, 231 derived skeletal traits and, 217 endocasts and, 296 evo-devo approach and, 112–113 foot structure, articulating elements in,

281, 282 foramen magnum repositioning and,

279, 280, 285 habitual bipedal locomotion and, 166 hyoid bone and, 353

Index

Index 533

language, anatomical structures for, 353

locomotion and, 22, 278–282 modular body plan and, 112 morphological adaptation and, 278 nuchal torus and, 312, 320 occipital bun and, 343, 345 pelvic/hip modifications and,

278–279, 281, 282 pentadactyly and, 217 platyrrhine characteristic, 152 primate cranial anatomy, 140–141 rhinarium, 148, 149 sagittal crest and, 294, 295 sagittal keel and, 320 sagittal ridge and, 312 soft tissue anatomy and, 17 vertebral column, curves in, 280, 282 zygomatics and, 247 See also Bones; Brain size; Dentition;

Skeletal remains Ancestral characters, 111, 114, 132 Anemia, 61

See also Sickle-cell anemia Anning, M., 32–33 Anthropocene, 477 Anthropocentric perspective, 206 Anthropoids, 136, 151–152

apes and, 158–165 characteristics of, 151–152 Eocene/Oligocene early anthropoids,

229–231 hominoids and, 158 humans and, 158, 165–166 New World anthropoids, 234–237 New World monkeys and, 152–154,

157–158, 234–235 Old World monkeys and, 155–158 true anthropoids, emergence of,

233–234 See also Apes; Fossil primates;

Modern humans; Monkeys; Primates

Anthropological perspective, 22–23 Anthropology, 4, 10

applied anthropology and, 10, 18, 20 archaeology and, 9, 10, 11 cultural anthropology and, 10, 11 forensic anthropology and, 16, 17, 21 four-field approach to, 10 linguistic anthropology and, 10, 11–12 medical anthropology and, 18, 20 molecular anthropology, 14, 15 nutritional anthropologists and, 14 paleopathology and, 16 primatology and, 17–18, 19 urban anthropology and, 11 See also Paleoanthropology; Physical

anthropology Antibiotic overuse, 10, 40, 432, 433, 479

Antigens, 83, 85 Ape gap, 250 Apes, 4, 25

African great apes, evolution of, 250–251

Asian true apes and, 247–250 bonobos and, 164–165 brachiation and, 145, 158 characteristics of, 151–152, 158 chimpanzees and, 162–164 civil rights for, 122 classification of, 146, 147 endangered primates and, 156, 159,

160–161, 164, 166–172 European true apes and, 246–247 geographical distribution of, 143, 158,

159, 160 gibbons and, 158–159 gorillas and, 160–162 hylobatids/lesser apes, evolution of,

250 knuckle walking and, 146 menopause and, 460 orangutans and, 159–160 siamangs and, 158–159 symbolic language and, 166 true apes, emergence of, 244, 246–250 See also Anthropoids; Fossil primates

Apidium, 232, 233, 241 Apollo 11 rock shelter site, 384, 386 Applied anthropology, 10, 18, 20

See also Anthropology; Physical anthropology; Scientific method

Arabian Plate, 244 Arago cave site, 336, 338, 340 Aramis site, 284, 285–286, 287, 288 Arboreal hypothesis, 139–140, 222 Archaeolemur, 226, 227 Archaeology, 9, 10, 11

artifacts and, 11 bioarchaeology, 16, 436–437 experimental archaeology and,

268–270 human behavior, evidence of, 11 settlements, dispersal of, 11 stone knappers and, 268 stone tool/lithic industry and,

268–270 See also Anthropology;

Paleoanthropology Ardipithecus, 251, 274, 284, 285–287, 293,

303, 304, 368 Ardipithecus ramidus, 288, 298 Ardi remains, 286–287 40Argon/39Argon dating method, 265–266 Aristotle, 28 Art:

African Upper Paleolithic art, 384–385 cave art, 382, 383–384 ceramic technology and, 382–383

engraving and, 382 European Upper Paleolithic art,

382–384 figurines and, 382 grave goods and, 381 musical instruments and, 382 Neandertal art/adornment and,

353–354 pigment use and, 353, 354, 382,

384–385 rock art, 383, 384 shell/bone ornament, 353, 354 technological advances and, 382–383,

385 Upper Paleolithic art, 382–383,

384–385, 386 Artifacts, 11, 260, 261, 268–270 Asia:

Central Asian Neandertals, 349–350, 355

Chinese Homo erectus, 319–323 Denisovans and, 73, 349–350,

356–357 Homo erectus, 310, 313, 315, 317–323 Homo floresiensis, 379–380 Indonesian Homo erectus, 317–319 melanin-producing allele and,

419, 420 modern human localities in, 373–375 premodern humans and, 337, 339, 340 true apes and, 247–250, 252 two-stage migration model and, 367 Western Asian Neandertals, 347–349

Assimilation, 6 Assortative mating, 407 Atapuerca region, 325, 326, 336, 338, 340 Atlatls, 351, 381, 383 Attenborough, D., 472 Aurignacian tool industry, 342, 380 Australia, 363

Aboriginal populations and, 367 modern human fossils and, 372, 374,

375 Australopithecus, 119, 195, 288, 294,

296–297, 304, 368 Australopithecus afarensis, 3, 274, 287,

289, 298, 303, 357 bridge role of, 292–293 cranial characteristics of, 290–291,

292, 293 dentition of, 290, 292 habitual bipedalism and, 292 juvenile skeletal remains of, 291–292 Laetoli footprints and, 3, 4, 289, 290,

291 locomotor behavior and, 289–290, 292 Lucy skeleton and, 284, 289, 290, 291 obligate bipedalism and, 292 postcranial material of, 291–292 primitive characteristics of, 290

Index534

Australopithecus afarensis, (continued) sexual dimorphism and, 292 See also Australopiths; Hominin

origins Australopithecus africanus, 287,

296–297, 298, 303 Australopithecus anamensis, 289, 293,

298, 303 Australopithecus boisei, 287 Australopithecus robustus, 287 Australopithecus sediba, 284, 298–299,

301, 303 Australopiths, 284, 288, 342

Australopithecus, 288, 289–293, 294, 296–297, 304, 368

Australopithecus afarensis and, 289–293

Australopithecus africanus and, 296–297, 298, 303

Australopithecus anamensis and, 289, 293, 298, 303

Australopithecus sediba and, 284, 298– 299, 301, 303

characteristics of, 288–289 contemporaneous lineages, coexis-

tence of, 293–294 cranial capacity comparison, 293 dentition in, 290, 292, 294, 295, 296,

297 ecological niches of, 288 evolutionary diversity of, 288 later australopiths, 294–297 locomotor behavior of, 289 Lucy skeleton and, 284, 289, 290, 291 Paranthropus aethiopicus and, 294, 298 Paranthropus and, 294–296, 297,

303, 304 Paranthropus boisei and, 296, 298 Paranthropus robustus and, 296, 298 sectorial premolars and, 289 subgroups of, 288 Taung child’s skull and, 284, 296 transitional australopiths and, 297–299 See also Early Homo; Hominin origins;

Pre-Australopiths Autosomal dominant traits, 85–87 Autosomal recessive traits, 87–88, 93, 104 Autosomes, 64, 65 Avian influenza, 432 Awash River region, 314 Aye-ayes, 131–132, 168

Baboons, 143 behavioral patterns of, 155 dentition in, 139 diet of, 144 estrus in, 157 infanticide and, 191, 192 locomotion of, 156–157 muzzles of, 139

one-male/multi-female groups and, 179

sexual dimorphism and, 157 speciation processes and, 118, 119 See also Apes

Bacteria, 50, 58 bacterial DNA, crop manipulation and,

72 insulin production and, 72 natural antibiotics, 418 See also Infectious disease

Basal metabolic rate (BMR), 178 Beagle voyage, 34–35 Begun, D., 246 Behavior, 175–176 Behavioral ecology, 176 Behavioral isolation, 119 Behavioral patterns, 5, 6, 175

affiliative behaviors, 187–188, 210–212

aggressive behaviors, 186, 208–209 altruism and, 210–212 behavioral continuity among species

and, 29 behavioral ecology and, 176 behavioral genetics and, 177 conflict behaviors, 207–209 culture, learned behaviors and, 6, 176 empathy and, 211, 212, 349 environment-genetics interplay and,

177 primate paleontological studies and,

12 primatology and, 17–18, 19 prosocial behaviors, 210–212 skeletal evidence of prehistoric behav-

iors, 436–437 social structures, factors in, 178–181 strategies of behavior and, 181 symbolic behavior, 352–354 territoriality, 159 See also Human behavior; Primate

behavior Berger, T., 351 Bergmann’s rule, 421–422 Bering land bridge, 222–223 Biblical accounts, 12, 44 Big Bang, 127 Bilophodont molars, 227, 237, 242 Binford, L., 260, 320 Binocular vision, 138, 139 Binomial nomenclature, 29 Bioarchaeology, 16, 436–437 Biocultural evolution, 6, 255

biology-culture interactions and, 6, 10 continuing process of, 465–466 culture, human capacity for, 6,

257–258 health/disease incidence and, 10

human biocultural evolution, 10, 408–410, 442–443

human life course and, 442–443, 444, 453–464

lactase persistence and, 409–410 marine-based food and, 341 primate cultural behavior and,

202–207 technology age, brain growth/function

and, 464–465 Upper Paleolithic humans and, 382 worldviews and, 6 See also Anthropology; Human adapta-

tion; Physical anthropology Biological anthropology, 4, 10, 12

biblical accounts, literal interpretation of, 12

human variation, interest in, 12 modern species, ancestry of, 12 origins of, 12 See also Physical anthropology

Biological continuum, 6, 8–9, 43, 60, 112–113, 212–213

Biological determinism, 390–391 Biological species concept, 118 Biology, 30, 34

cell division and, 67–71 cells, structure/function of, 50–51 chromosomes and, 63–67 DNA replication and, 52–53, 54 DNA structure and, 51–52, 53 embryonic development and, 58–60,

112 evo-devo approach and, 42, 112–113 genes and, 57–63, 119 human genome, biochemical function

of, 74 molecular biology, advances in,

354–357 mutation and, 57, 61–63, 70 new frontiers in, 71–74 protein synthesis and, 53–57 See also DNA (deoxyribonucleic acid);

Genetics; Heredity; Human adapta- tion; Mendelian inheritance; RNA (ribonucleic acid)

Biomedical research, 18 Biosocial perspective, 130 Biostratigraphic correlation, 228, 267 Bipedal locomotion, 3, 22, 271–274,

278–282 See also Locomotion

Bird evolution, 115–116, 129 Bird flu, 432 Biretia, 231, 239 Black, D., 247 Black Skull find, 294 Blanks, 268 Blending theory of inheritance, 42, 77 Blombos Cave site, 384, 386

Index 535

Blood types, 65–66 allele frequency in populations and,

94–95 antigens and, 83, 85 discontinuous traits and, 89–90 environmental factors and, 93 human polymorphisms and, 397–398,

399 human variation and, 395, 396 Mendelian inheritance and, 83, 85 red blood cell production and, 68 smallpox and, 429–430 See also Hemoglobin

Blumenschine, R., 260 Bodo cranium, 334–335, 338, 340 Bones:

analysis of bone and, 270 bone geometry, 437 fluorine analysis and, 264 osteology and, 15–16 tuberculosis and, 428 See also Anatomy; Skeletal remains

Bonobo Conservation Initiative, 171 Bonobos, 73, 164

behavioral patterns of, 165 body size of, 164–165 brachiation and, 145, 165 cognitive complexity and, 200 cranial capacity of, 293 culture, learned behaviors and, 6 diet of, 144 estrus in, 165 geographical distribution of, 143, 158,

160, 164 knuckle walking and, 146 problem-solving capacity/insight and,

166 sexual activity of, 165 social organization of, 165 See also Apes

Border Cave site, 368, 369, 370, 372 Boule, M., 345 Bouri Peninsula site, 261, 263 Brace, C. L., 382 Brachiation, 145–146 Brachydactyly, 84 Brain, C. K., 270 Brain function:

binocular vision and, 138 bipedalism, brain-cooling/radiator

theory and, 274 brain/body size, index of encephaliza-

tion and, 195–197 brain/nerve cell division and, 68 Broca’s area and, 201, 202 cerebrum and, 128 expanded gestation of mammals and,

128, 130 hemispheres and, 138, 201

human brain function, technology and, 464–465

intelligence and, 166, 197, 205 language, evolution of, 201–202, 203 motor cortex, 201 neocortex and, 128, 129, 139, 195, 196 neurological reorganization and, 10,

128, 129, 201–202, 203 plasticity and, 465 primate brain function, 138, 139 sensory modalities and, 139 speech production mechanisms and,

202 technology age, effects of, 464–465 visual centers and, 138 Wernicke’s area and, 201–202

Brain size: Australopithecus afarensis and, 3 cerebrum and, 128, 129 cranial capacity comparison, 293 Homo erectus and, 311 human evolutionary outcomes and,

10, 165 language, evolution of, 200–202, 203 large brains, metabolic costs of,

195, 197 mammalian evolution and, 128, 129 Neandertals and, 342, 345 premodern humans and, 333, 334, 337 prenatal brain growth and, 195 radiator theory, brain-cooling effect

and, 274 social brain hypothesis and, 197

Branisella, 234, 235, 239 Brassempouy site, 382, 386 Bräuer, G., 366 Breeding isolates, 96, 402–403 Breeding process, 36, 60, 77

breeding isolates and, 96, 402–403 gene flow and, 96–97 hybridization and, 78, 119, 121 inbreeding, 407–408 selective breeding and, 77, 96, 119 tandem repeats, mutation and, 95–96

Broca’s area, 201, 202 Broken Hill site, 334, 335 Brooks, A., 321 Buffon, G.-L. L. de, 29–30 Burial practices:

earliest evidence of, 336 flexed position and, 345 grave goods and, 381 Neandertal burials, 345, 346, 354 Upper Paleolithic burial sites and,

377, 381 Bush babies, 150, 226, 227 Bushmeat trade, 169–171, 431 Butchering practices, 270, 327, 345

Camptodactyly, 84 Cannibalism, 322, 323, 325, 335, 345 Capuchins, 153

diet of, 144 encephalization of, 206 tool use by, 206

Carbon-14 dating method, 266 Carbon isotope ratios, 427, 438 Carpolestes, 222, 223 Carpolestidae, 222 Catarrhines, 154, 231, 234 Catastrophism doctrine, 30–31 Catopithecus, 231 Cave art, 382, 383–384 Cell division, 63, 67

cancer, mechanisms of, 422 chromosomes and, 62, 63 daughter cells and, 66, 67, 68 DNA replication and, 52–53, 54 evolutionary significance of meiosis

and, 70 folate, role of, 417 genetic diversity and, 70 meiosis and, 66, 68–71 mitosis and, 66, 67–68 recombination process and, 68 reduction division and, 68, 69 skin cells and, 422 See also Biology; Cells; Chromosomes

Cells, 50–51 bacteria and, 50 cytoplasm and, 50, 51, 55 eukaryotic cells and, 50 gametes and, 51 mitochondria and, 51, 92 molecules and, 50–51 multicellular forms and, 50 nuclear membrane and, 50 nucleus in, 50, 51, 54 organelles in, 50, 51 protein synthesis and, 51 regulatory genes and, 58–59 ribosomes and, 51, 55, 56, 57 somatic cells, 51, 58 See also Biology; Cell division; DNA

(deoxyribonucleic acid); Mitochondrial DNA (mtDNA); Protein synthesis; RNA (ribonucleic acid)

Cenozoic era, 124, 125 age of mammals and, 128 continental drift and, 126 epochs of, 125, 127, 218 mammalian radiation and, 131 periods of, 127 primate origins and, 218–219, 221

Centromeres, 63, 65 Ceprano site, 308, 325–326 Cercopithecidae, 155, 239 Cercopithecines, 155–156

Index536

Cercopithecus, 143, 220 Cerebrum, 128, 129 Chatelperronian tool industry, 342,

347, 380 Cheetah genetics, 98 Chejiawo site, 309 Chimpanzees, 5, 19, 122, 135, 162–163,

220 aggressive behavior and, 207–209 altruism/empathy and, 211–212 behavioral patterns of, 163–164,

207–209 bipedal locomotion and, 163 brachiation and, 145, 163 bushmeat trade and, 431 chromosomes of, 63, 64 comparative genomics and, 148 cranial capacity and, 293 culture, predisposition for, 6 diet of, 144, 163, 205–206 displays by, 185 encephalization of, 206 genome sequencing and, 42, 73 geographical distribution of, 143, 158,

160, 163 knuckle walking and, 146 last common ancestor and, 25 natal groups and, 164 orphans, adoption of, 211, 456 problem-solving capacity/insight and,

166 sexual dimorphism and, 163 simian immunodeficiency virus and,

430–431 social organization of, 163–164 stone tools and, 205, 206 termite fishing and, 204–205 territoriality and, 164 thrust spear hunting and, 205 tool use by, 204–206 See also Apes; Primate behavior;

Primates Chimpanzee Sequencing and Analysis

Consortium, 73, 146 China:

bird-dinosaur links and, 115 Dali skull and, 337, 339 Dragon Bone Hill cave and, 319,

322–323 Hexian County site, 321, 322–323, 326 Homo erectus in, 319–323 Lantian County sites, 309, 321, 324,

326 modern human discoveries and, 372,

373, 374 Peking Man and, 247, 323 premodern humans and, 337, 339, 340 Yunxian County site and, 321–322, 326 Zhoukoudian Cave Homo erectus,

319–321, 324, 326

Chopping tool industry, 268, 320, 321 Chordata phyla, 108, 109 Christian fundamentalists, 43–45 Chromosomes, 57, 63

abnormal number of, 70–71 alleles and, 66, 70 autosomes and, 64, 65 cell division and, 63, 64 centromeres and, 63, 65 DNA, role of, 63, 65 gender determination and, 65, 71 gene locus and, 65, 66 genetic inheritance and, 65–66, 70 karyotyping chromosomes and, 66–67 meiosis and, 66, 68–71 mitosis and, 66, 67–68 numbers of, 63–64, 68, 70–71 pairing of, 65, 66 photomicrographs of, 66 random assortment of, 70, 82 sex chromosomes and, 64–65 somatic cells and, 63, 64

Chronometric dating, 264 Civilization collapse, 11 Clades, 111, 114 Cladistics, 111

bird-dinosaur links, evidence for, 115–116

clades and, 111, 114 cladistic analysis, real-world applica-

tions of, 114–116, 117, 121–122 cladistic analysis, simplified example

of, 114, 115 cladogram and, 116–117 crown group and, 219 derived/modified characters and, 114 homoplasy and, 115–116 monophyletic groups and, 111 phylogenetic trees and, 115, 116–117 polyphyletic groups and, 111, 114 shared derived characters and, 116 stem group and, 219 See also Classification systems

Cladogenesis, 118 Cladograms, 116–117 Clarke, R., 282, 297 Clarks Fork Basin, 221, 222, 223 Classification systems, 108

analogies and, 110 ancestral/primitive characters and,

111 chordata phyla and, 108, 109 clades and, 111, 114 cladistics and, 111, 114–117 derived/modified characters and, 114,

116, 121 evolutionary systematics and, 111, 114,

116–117 fossil genera, recognition of, 121–122 fossil species, recognition of, 120–121

homologies and, 108, 110 levels of classification, 108, 109 monophyletic groups and, 111 phyla within, 108 phylogenetic trees and, 115, 116–117 polyphyletic groups and, 111, 114 primate classification, 146–148 principles of classification, taxonomic

rules and, 108–110 shared derived characters and, 116 vertebrates and, 108 See also Macroevolution

Cleft chin, 84 Climatic conditions:

acclimatization response and, 414 desertification and, 332 glaciations and, 317, 332, 342, 381 interglacials and, 332, 333, 342 Pleistocene oscillations and, 332, 333 rainfall patterns and, 332 Upper Paleolithic climatic pulses and,

381 warming period, bountiful food

sources and, 380–381 See also Cold climates; Global climate

change; Hot climates Cloning, 70, 72–73, 113 Coding DNA, 57, 61 Codominance, 83, 183 Codons, 57 Cold climates, 14

body heat, retention of, 424 body size/proportions and, 342,

421–422 brain size and, 342 cultural innovations and, 424 dietary modifications and, 423–424 metabolic rate, increase in, 423 responses to cold, 422–424 shivering response and, 422–423 subcutaneous fat, insulating role of,

424 vasoconstriction and, 424 See also Hot climates; Human

adaptation Colobines, 143, 144, 155, 156, 220 Colobus monkeys, 143, 157, 166, 167 Color blindness, 88 Color vision, 138, 139 Combe Capelle site, 376 Common ancestors, 25, 30, 108, 113, 132,

209, 212 Communications technology, 7, 464–465 Communication strategies, 184–186

autonomic responses and, 184 facial expressions and, 184, 185, 197 grooming behavior and, 184 intentional behaviors and, 184 language, evolution of, 200–202, 203 social living, facilitation of, 186

Index 537

submissive stance and, 184 threat gestures and, 184 vocalizations and, 185, 197, 198 See also Language; Primate behavior

Comparative genomics, 42, 73, 113, 146, 148

Complementary bases, 53, 54 Complete replacement model, 365–366 Conservation International, 171 Conserved genes, 60, 91, 110 Context, 262 Continental drift, 124–126, 240, 244 Continuum, 6, 8–9 Convention on Biological Diversity,

478–479 Copernicus, 28 Copy number variants (CNVs), 95–96,

398, 401 Core area, 207 Cores, 268, 320 Cosmic calendar, 127 Creation science movement, 44 Crick, F., 51, 52 Crime investigations, 21 Cro-Magnon site, 370, 372, 376, 377–378 Cross River gorillas, 160, 167 Crown group, 219 Cultural anthropology, 10, 11

ethnographies and, 11 subcultures, interactions of, 11 traditional societies, study of, 11 urban anthropology and, 11

Culture, 6, 257, 408 biological makeup, influence on, 6 components of, 6, 7 human capacity for, 257–258 human cognitive abilities and, 258 learned nature of, 6 material culture, 258 relativistic view of, 22 technological innovation and, 7 worldview and, 6 See also Biocultural evolution

Cusps, 144 Cuvier, G., 30–31, 225 Cystic fibrosis, 84 Cytoplasm, 50, 51

Daka site, 308, 314, 315, 324, 326 Dali skull, 337, 339, 340 Dart, R., 296, 297 Darwin, C., 12, 26, 30, 31, 32, 33–37, 38,

39, 42, 60, 94, 113, 115, 118, 391 Darwin, E., 30, 33 Darwinius, 225 Data, 18, 19–20, 43 Dating techniques. See Paleoanthropology DDT spraying, 408–409, 479 Deep time, 27, 30, 32, 107, 124–125,

126–127

Deforestation, 168–169, 408, 471, 472 Denisova Cave site, 349, 367 Denisovans, 73, 349–350, 356–357, 367 Dentition:

absent permanent dentition, 84 bilophodont molars, 227, 237 biocultural evolution and, 10 canine teeth, 3 carnivorous diet and, 144 cusps and, 144 dental comb and, 148, 149, 226 developmental rates and, 304 fossil teeth, ecological inferences from,

121 heterodont dentition, 128–129 homodont dentition, 128 honing complex and, 283 mammalian evolution and, 128–129 omnivorous diet and, 144 primate dentition, 138, 144 sectorial premolars and, 289 Y-5 molar and, 240, 242

Depth perception, 138, 139 Derived characters, 114, 116, 121, 132,

217 Desertification, 332, 474 de Waal, F., 212 Diabetes, 448, 452 Diet:

aquatic plants, foraging for, 162 carnivorous diet, 144 contemporary human diet, 446,

447–449 diabetes and, 448 frugivorous diet, 160, 162 male-provisioning scenario and, 272,

273, 274 marine resources, 351, 438 mismatched diets/dietary needs and,

447, 449, 450, 458–459 nutritional anthropologists and, 14 nutritional deficiencies and, 16,

447–449 obesity/overnutrition and, 449, 450 omnivorous diet, 138, 139, 144 population growth, resource stress

and, 438 preagricultural diet, 445, 447, 449 prehistoric diet, evidence of, 437–438 primate diet, 138, 139, 144, 160, 162 regional preferences, cultural differ-

ences and, 205–206 reproductive cancers and, 453 resource scarcity constraint and,

31–32 scavenging strategy and, 260, 261,

320, 327 seed-eating hypothesis and, 272 social structure and, 178–179

undernutrition/malnutrition and, 448–449, 450

vegetarian diet, 162 See also Human growth/development;

Hunting; Subsistence patterns Differential net reproductive success,

41–42 Digital divide, 465 Dikika site, 261, 263, 291, 292 Dinosaurs, 107

birds, links with, 115–116 descendants of, 127 evolution of, 114–116, 126–127 extinction of, 125, 127, 131, 218 fossils of, 122 Great Age of, 129 theropods and, 115, 116 warm-bloodedness and, 127 See also Vertebrate evolution

Direct percussion method, 269 Discontinuous traits, 89–90 Discrete traits, 83, 89 Disease:

aging and, 462–463 agriculture, epidemiological transition

and, 447–448 air pollution and, 10 autoimmune conditions, 74 bacteria-derived insulin and, 72 biocultural evolution and, 10 cancers and, 422, 434, 453, 460, 462,

463 degenerative diseases, 436–437, 462 dental disease, evidence of, 433–434 diabetes, 448, 452 disease risk, epigenetics and, 450–451 diseases of civilization, 461 free radicals, oxidation and, 462–463 genetic disorders, 83, 84, 88, 88–89, 89 gene variants and, 399 obesity/overnutrition and, 449 osteoarthritis and, 436–437 paleopathology and, 16 parasitic infections, 458 regulatory genes and, 74 reproductive cancers, 453, 460 sickle-cell anemia and, 61–62, 101 skeletal evidence of prehistoric dis-

eases and, 433–435 skin cancer, 415, 416–417, 422–423 toxin exposure and, 10 vectors of, 10 Vitamin D and, 418 See also Health; Infectious disease

Dispersal. See Homo erectus; Migrations; Modern human origins/dispersal

Displays, 185 Diurnal habit, 138, 139 Dmanisi site, 308, 316–317, 325, 326, 328

Index538

DNA (deoxyribonucleic acid), 5, 9, 14, 51 ancient human migrations, DNA evi-

dence for, 400–401 bases and, 51–52, 53 base substitution/point mutation and,

62–63 cancer, mechanisms of, 422 coding sequences and, 57, 61, 74 complementary bases and, 53, 54 copy number variants and, 95–96,

398, 401 double helix formation and, 52, 54 enzymes, role of, 53 exons/introns and, 57–58 genes and, 57–58 heredity and, 58 infanticide studies and, 20 mitochondrial DNA and, 51, 92, 355,

366 molecular anthropology and, 14, 15 mutations and, 57 noncoding/junk DNA and, 57, 59, 61,

74, 148, 398 nuclear DNA, 51, 355 nucleotides and, 51–52, 53 polymerase chain reaction technique

and, 71 polymorphisms and, 398–402 recombinant DNA technology and, 72 regulatory genes, embryonic develop-

ment and, 58–59 replication and, 52–53, 54 single-nucleotide polymorphisms and,

398, 399, 414 structure of, 42, 51–52, 53 telomere hypothesis and, 463 terminator region and, 56 transcription and, 56, 113 See also Biology; Cell division;

Chromosomes; Genetics; Protein synthesis; RNA (ribonucleic acid)

DNA fingerprint, 71–72, 73, 398 Dobzhansky, T., 479 Dog breeds, 36–37 Dolní Věstonice site, 382, 386 Domesticated animals, 10, 36, 37, 60, 96,

414, 427–428, 432 Dominance, 79–82

autosomal dominant traits and, 85–87 codominance and, 83, 183 genetic disorders and, 83, 84 Mendelian traits in humans, 83, 84 misconceptions about, 83–85 See also Heredity; Mendelian

inheritance Dominance hierarchies, 182–184 Dragon Bone Hill cave, 322–323 Dragon bones, 319, 322, 323 Drimolen site, 284 Drought, 474

Dryopithecus, 245, 246, 248, 251 Duarte, C., 377 Dubois, E., 317 Dwarfism:

achondroplasia and, 84, 85–86 growth hormone, insufficient amount

of, 452 insular dwarfing and, 379–380 pygmies, 452

Early Homo, 283, 289, 298, 299, 304, 342, 357, 359

accelerated developmental pattern of, 304

cranial capacity of, 293, 300, 304 Homo erectus, coexistence with, 301 Homo habilis and, 299–300 parallel species development and, 301 Plio-Pleistocene hominins and, 299 tool making and, 300, 304 transitional australopiths and,

297–299, 301 See also Australopiths; Hominin ori-

gins; Homo erectus Earthquakes, 124, 125 East Lake Turkana site, 263, 284, 299, 300,

301, 302, 308, 313, 315, 326 Ecological niches, 119, 121, 126, 131

primates, adaptive niches of, 139, 140–141

specialized diet and, 144 Ecological perspective, 176 Ecological species concept, 119 Ectothermic capability, 129 Elandsfontein site, 335, 338 El Castillo site, 382 Electron spin resonance (ESR) dating

method, 266 El Sidrón site, 344, 345, 346, 347 Empathy, 211, 212, 349 Empirical approach, 18, 19, 21 Encephalization index, 195–197 ENCODE (Encyclopedia of DNA

Elements) project, 74 Endangered species, 18, 166–167

aye-ayes, superstitions about, 168 biodiversity, loss of, 172 body part trade and, 170, 171 bonobos and, 164 bushmeat trade and, 169–171 deforestation and, 168–169 exotic pet trade, 170, 171, 477 genetic bottlenecks and, 97–98, 99 gibbon species and, 159 gorillas and, 160–161, 169 habitat loss and, 159, 164, 168–169 human hunting activities and, 159, 164 live capture/illegal trade and, 171 logging industry and, 170 orangutans and, 159

poaching and, 169 tourism, positive aspects of, 169 warfare and, 164 wildlife protection, dangerous job of,

169 wildlife protection initiatives and,

171–172 Endemic disease, 427 Endocasts, 296 Endogamy, 403 Endothermic capability, 129, 136 Environmental degradation:

air pollution and, 10, 39–40, 450, 480 deforestation, 168–169, 408, 471, 472 desertification and, 332, 474 flood events and, 472 forest products, commercial harvest-

ing of, 169, 170 human impact and, 9, 470 nonrenewable resources, exploitation

of, 471–472 ocean acidification and, 475 soil erosion and, 471 toxins, exposure to, 10 See also Endangered species; Modern

human disconnect; Global climate change

Enzymes, 53 Eocene euprimates, 221, 222–231, 232 Epigenetics, 450–451, 452, 462 Epigenome, 450 Epochs, 125, 127, 218 Eppig, C., 458 An Essay on the Principle of Population, 31 Essential amino acids, 445 Establishment clause, 44–45 Estrus, 157, 165, 191 Ethnicity, 393 Ethnocentrism, 22 Ethnographies, 11 Eugenics movement, 391 Eukaryotic cells, 50 Euprimates, 221 Europe:

Central European modern human fossils, 372, 375–377

Central European Neandertals, 344, 346–347

Homo heidelbergensis and, 334–335, 336

premodern humans and, 335–337, 338 solar radiation, skin pigmentation and,

416, 417–418, 420 true apes and, 246–247 Upper Paleolithic art and, 382–384 Upper Paleolithic technology and,

380–382 vitamin D hypothesis and, 418 Western European Neandertals, 344,

345–346

Index 539

See also Cro-Magnon site; Neandertals; Premodern humans

Evaporative cooling, 420–421 Evo-devo approach, 42, 112–113 Evolution, 5

anthropocentric perspective and, 206 biological continuum and, 6, 8–9,

43, 60 conserved genes and, 60, 91 contemporary definition of, 94–95 genetic diversity and, 9, 13, 14–15, 70,

97–98 macroevolution and, 5, 107 meiosis, evolutionary significance of,

70 microevolution and, 5, 25, 97, 99–100,

104 mosaic evolution, 256, 257 pace of, 132 point mutation and, 62–63, 86, 91 population genetics, changes in, 5 primatology and, 17–18, 19 regulatory genes and, 58–61, 74, 96 teaching of, 43–45 See also Biocultural evolution;

Evolutionary theory; Heredity; Heritability; Human evolution; Modern evolutionary theory; Natural selection

Evolutionary medicine, 18 Evolutionary systematics, 111, 114,

116–117 See also Classification systems

Evolutionary theory, 25–26 acquired characteristics, use-disuse

theory and, 30, 31 anthropocentric perspective and, 206 argument from design and, 27 biological continuum, concept of, 43 blending theory of inheritance and, 42 brief history of, 26–33 catastrophism doctrine and, 30–31 common ancestor concept and, 25, 30 constraints on, 42 creation science movement and, 44 deep time concept and, 27, 30, 32 environment-organism relationship

and, 29–30, 39–40, 100–101 evo-devo approach and, 42 fixity of species concept and, 27,

29, 30 fossil hunters, role of, 32–33 microevolutionary changes and, 25 natural selection, discovery/develop-

ment of, 31, 33–38 opposition to, 42–45 paradigm shifts and, 28–29 population evolution and, 39 precursors of, 29–33 region-based diversification and, 29

religious beliefs, anti-scientific posi- tions and, 25–26, 34, 42, 43–45

reproductively isolated organisms and, 29

resource scarcity, constraint of, 31–32 scientific revolution and, 27–29 species, emerging concept of, 29 teaching of, 43–45 uniformitarianism and, 32 See also Evolution; Human evolution;

Modern evolutionary theory; Natural selection

Exogamy, 403 Exons, 57–58 Exotic pet trade, 170, 171, 477 Experimental archaeology, 268

bone, analysis of, 270 stone tool/lithic industry and, 268–270 See also Archaeology;

Paleoanthropology Extinction:

catastrophism doctrine and, 30–31 colobus monkeys and, 166 dinosaur extinction, 127, 129, 131, 218 global climate change and, 474–475 human activities and, 474–475,

477, 478 last common ancestor and, 25 major extinction events, 125, 127, 129,

131, 476–477 paleospecies, species comparison and,

120–121 vacated econiches and, 131 western lowland gorillas and, 160

Eye color, 91, 93

Facial expressions, 184, 185, 197 Falk, D., 274, 380 Falsification, 20, 21, 270 Familial hyper-cholesterolemia, 84 Faunal correlation, 228, 267 Fayum Depression, 226–227, 231, 232,

233–234 Fertility, 41 Finches. See Galápagos finches Fire use, 320–321, 341, 382 First Amendment, 44–45 First dispersal. See Homo erectus; Modern

human origins/dispersal Fishes, 128, 189 Fitness, 39, 41, 118, 176, 417 Fixity of species concept, 27, 29, 30 Flake tools, 268–269, 320, 325, 340, 341,

381, 382 Flexed position burial, 345 Floating islands, 236 Flood events, 472, 474, 475 Flores, 318 Florisbad site, 335, 338, 340, 354 Fluorine analysis, 264

Flowering plants, 140, 141 Food insecurity, 448–449, 474, 475 Footprints:

Laetoli footprints, 3, 4, 289, 290, 291 lunar footprints, 4, 5

Foramen magnum, 279, 280, 285 Forensic anthropology, 16, 17, 21,

394–395 Fossilization process, 264 Fossil primates, 217–218

Adapis and, 225 Adapoidea superfamily and, 223–225 Aegyptopithecus and, 233, 234, 237 African great apes, evolution of,

250–251 Afropithecus and, 242, 244, 246 anthropoids and, 224, 228, 229–231,

233 ape gap and, 250 apelike proconsuloids, 240–244 Apidium and, 232, 233, 241 arboreal adaptation, primate evolution

and, 222 Archaeolemur and, 226, 227 archaic primates, identification of, 219,

221–222 Asian great ape and, 252 Bering land bridge and, 222–223 bilophodont molars and, 227, 237, 242 biostratigraphic/faunal correlation

and, 228 Biretia and, 231 Branisella and, 234, 235 Carpolestes and, 222, 223 Carpolestidae and, 222 catarrhines and, 231, 234 Catopithecus and, 231 Cenozoic era, primate origins and,

218–219, 221 crown group and, 219 Darwinius and, 225, 226 dentition in, 222, 223, 225, 227, 228,

233, 240, 242 derived skeletal traits and, 217 dispersal/migration and, 222–223, 227,

236, 237, 244, 245, 250 Dryopithecus and, 245, 246, 248 euprimates, Eocene epoch and, 221,

222–231 European true apes and, 246–247 Fayum Depression and, 226–227, 231,

232, 233–234 Gigantopithecus and, 241, 244, 245,

247–248, 249, 252 Griphopithecus and, 241, 244, 245, 246,

247, 251, 252 haplorhines and, 217 hominoid evolution and, 250–252 homologies and, 225 homoplasy and, 225

Index540

Fossil primates (continued) island hopping and, 227, 235, 236 last common ancestor and, 219, 250 late Mesozoic era, primate evolution

and, 218, 219 lemuriforms and, 227, 230, 236 lesser apes, evolution of, 250 Lomorupithecus and, 244 lorisoids and, 226 Lufengpithecus and, 241, 244, 245,

248–249, 250, 252 Miocene primates, 237–250 molecular primate family tree and, 220 Nakalipithecus and, 250, 251 New World anthropoids and, 234–237 Old World monkeys and, 237–239, 243 Oligocene primates, 229, 231–237 Omomyoidea superfamily and, 223,

224, 228 orthograde body position and, 217 Ouranopithecus and, 241, 244, 245,

246–247, 250, 251 Parapithecus and, 233 platyrrhines and, 233, 234–237 plesiadapiforms and, 221, 222 Plesiadapis and, 222 Pliopithecoidea and, 242, 244, 250 Pongo and, 249, 250, 252 Purgatorius and, 221–222, 226 radiation, evidence of, 221–222, 223 Saadanius and, 234, 237, 244 semiorders and, 221 Sivapithecus and, 247, 252 stem group and, 219, 222 strepsirhines and, 217 subfossil lemurs and, 227 tarsier-like omomyoids and, 228 taxon/taxa and, 219 Teilhardina, 224, 226, 228, 229 Theropithecus and, 239, 240 true anthropoids and, 233–234 true apes and, 244, 246–250 true lemurs/lorises, evolution of,

226–228 true tarsiers, evolution of, 229 Victoriapithecus, 237, 239 wood/pollen samples and, 285 Y-5 molar and, 240, 242 See also Fossils; Primate adaptation;

Primates Fossils, 119–120, 122

amber and, 122, 123 biological diversity, evidence for, 113 catastrophism doctrine and, 30–31 cladistic analysis and, 121–122 DNA extraction and, 14, 15 extant organisms, ancestors of, 34–35 formation of, 122–124 fossil genera, recognition of, 121–122 fossil species, recognition of, 120–121

fossil hunters, role of, 32–33 humans, primate origins of, 9 hybridization and, 121 interspecific variation and, 120 intraspecific variation and, 120 Laetoli footprints, 3, 4, 289, 290, 291 limestone deposits and, 122 microfossils, 122 mineralization process and, 122–123 molecular clock and, 220 paleoanthropology and, 12, 13 paleospecies, variation in, 120–121 primate paleontology and, 12 sexual dimorphism and, 120 species, interpretation of, 119–122 splitters vs. lumpers and, 121 taphonomy and, 123–124 teeth, ecological inferences from, 121 teeth, prevalence of, 129 variation, representation of, 119–120 vertebrate fossils and, 124 See also Fossil primates;

Macroevolution; Mammalian evo- lution; Skeletal remains; Vertebrate evolution

Founder effect, 97 colonization and, 97 genetic diversity, reduction in, 97 isolated groups, distinctive genetic pat-

terning in, 397 See also Modern evolutionary theory

Franklin, R., 51, 52 Frugivorous diet, 160

G-6PD deficiency, 88 Galago species, 143, 150, 167, 205 Galápagos finches, 35–36, 40, 41, 60 Galápagos Islands, 34, 35, 477 Galileo, 28–29, 43 Galton, F., 391 Gametes, 51

chromosome number in, 64 egg cells, 51 heredity and, 51 recombination and, 100 sperm cells, 51 zygotes, formation of, 51 See also Biology; Cells

Garbani Channel, 222 Geissenklösterle Cave site, 382 Gene flow, 96–97, 98, 100, 104, 118 Gene pools, 94, 100, 402 Generalized characteristics, 131, 132, 136 Genes, 57

cloning and, 70, 72–73 coding sequences and, 57, 58, 74 conserved genes and, 60 definition of, 58 embryonic development and, 58–60 exons and, 57–58

function, shifting view of, 57 gene locus and, 65, 66, 83 genetic manipulation and, 72 homeobox/hox genes and, 59–60 immunity process and, 60 introns and, 57–58 mutation and, 57, 61–63 noncoding/junk DNA and, 57, 59 pleiotropic genes, 462 point mutation and, 62–63 recombinant DNA technology and, 72 regulatory genes and, 58–61, 74, 110 transcription and, 57 See also DNA (deoxyribonucleic acid);

Genetic code; Genetics; Protein synthesis; RNA (ribonucleic acid)

Genetic bottlenecks, 97–98, 99 Genetic code, 54–55, 58 Genetic determinism, 451 Genetic drift, 97–100, 103–104, 118, 358 Genetic tool kit, 112–113 Genetic variation, 9 Genetics, 49

comparative genomics and, 42, 73 evo-devo approach and, 42 genetic variation and, 9, 13, 14–15 macroevolutionary processes and, 5 microevolutionary processes and, 5 molecular anthropology and, 14, 15 polymorphisms, study of, 398–402 populations, evolutionary changes in,

5, 39 speciation and, 5 See also DNA (deoxyribonucleic acid);

Heritability; Human variation; Mendelian inheritance; Mendelian inheritance in humans; Population genetics

Genocide, 17, 392 Genomes, 42, 57

whole-genome analysis, 399–400 See also Genome sequencing; Human

Genome Project Genome sequencing, 42, 57, 60, 73, 130,

146, 220, 349, 355, 397 Genotypes, 80, 81, 82, 93 Genus/genera, 29, 121–122 Geographical distribution:

apes and, 143, 158, 159, 160, 161, 163, 164

biological species concept and, 118 gene flow and, 118 HIV/AIDS and, 429 malaria and, 10, 102, 103 New World monkeys and, 142, 152 Old World monkeys and, 143, 155, 156 Old World sickle-cell allele, 101 primate groups and, 141–143, 158, 160 skin color, indigenous human popula-

tions and, 415

Index 541

See also Fossil primates; Hominin origins; Homo erectus

Geographical isolation, 39, 104, 118 continental drift and, 126–127 insular dwarfing and, 379–380 Pleistocene world and, 340 See also Geographical distribution

Geological time scale, 27, 30, 32, 107, 124–125, 126–127

Geology, 9, 32 catastrophism doctrine and, 30–31 contemporary landscape, formation of,

32 continental drift/plate tectonics and,

124–126 deep time and, 27, 30, 32, 107,

124–125, 126–127 radioactive isotope decay and,

264–265 stratigraphy and, 264 uniformitarianism and, 32

Gibbons, 158–159, 220 behavioral patterns of, 158–159 brachiation and, 145, 158 diet of, 158 endangered status of, 159, 167 geographical distribution of, 143, 158 territoriality and, 159 See also Apes

Gibraltar site, 343, 344, 351 Gigantism, 452 Gigantopithecus, 13, 241, 244, 245,

247–248, 249, 252 Glaciations, 317, 332, 333, 342, 381 Global climate change, 10, 469, 472–476

anti-scientific positions and, 21 glaciations and, 317, 332 infectious disease and, 433 interglacials and, 332 international attention to, 475–476 Miocene continental drift and, 240 See also Modern human disconnect

Glucose processing, 426, 452 Gobi Desert, 107 Gombe National Park, 164, 183, 208–209,

462 Gona site, 263, 314, 315 Gondwanaland, 125, 126 Goodall, J., 208, 456 Gorilla gorilla, 160 Gorillas, 160, 220

behavioral patterns of, 161, 162 brachiation and, 145 bushmeat trade and, 169–171 chromosomes of, 63, 64 comparative genomics and, 148 cranial capacity and, 293 Cross River gorillas and, 160, 167 culture, learned behaviors and, 6 diet of, 162

eastern lowland gorillas, 161 endangered status of, 160–161,

167, 169 extinction, threat of, 160 genome sequencing and, 73 geographical distribution of, 143, 158,

160, 161 knuckle walking and, 146 Mountain gorillas, 161, 162 natal groups and, 161 problem-solving capacity/insight and,

166 silverback males and, 161, 162 tool use by, 204, 205 western lowland gorillas, 160, 161–162 See also Apes; Lowland gorillas;

Mountain gorillas; Primate adapta- tions; Primate behavior; Primates

Gould, S. J., 391 Grand Canyon sediment, 126 Grand Designer, 27 Grandmother hypothesis, 460 Gran Dolina site, 308, 325, 326, 335–336 Gravettian tool industry, 342, 380 Great Ape Project (GAP), 122 Great Ape Survival Project (GRASP),

171–172 Great Ape Trust, 171 Great Hall of Bulls, 383 Grimaldi site, 382 Griphopithecus, 241, 244, 245, 246, 247,

251, 252 Grooming behavior, 184, 187–188 Grotte Chauvet Cave site, 383–384 Group selection theory, 211–212 Growth hormones, 72, 451, 452 Guenon species, 156, 157, 167, 170

Habitat loss, 159, 160, 477–479 Habitual bipedalism, 3, 166, 281, 282, 292 Hadar region, 262, 284, 289, 290, 299,

301, 302 Hafting process, 385 Hailie-Selassie, Y., 285, 286 Half-life, 265, 386 Haplorhini, 146, 147, 151, 217, 220, 224 Hardy-Weinberg theory of genetic equi-

librium, 403–404, 407 Health:

evolutionary medicine and, 18 medical records, racial information

and, 402 See also Disease; Infectious disease

Heat. See Global climate change; Hot climates

Hemoglobin, 53, 54 high-altitude environment and, 414,

426–427 malaria-sickle-cell correlation and,

102

red blood cell production and, 68 sickle-cell anemia and, 61–62, 101,

102, 104 See also Blood types

Hemophilia, 88, 89 Henry, A., 298 Heredity, 77–78

acquired characteristics, use-disuse theory and, 30

blending theory of inheritance and, 42, 77

breeding stock, trait selection and, 36 chromosomes, genetic information

and, 65–66 conserved genes and, 60 DNA and, 58 gametes, role of, 51 homeobox/hox genes and, 59–60 mutation and, 61–63 natural selection and, 40–41 point mutation and, 62–63 sickle-cell anemia and, 61–63 variation, factors in, 95–100 See also Genes; Genetics; Heritability;

Mendelian inheritance; Mendelian inheritance in humans; Non- Mendelian inheritance; Natural selection

Heritability, 14 Herto site, 368, 369, 371, 372 Heterodont dentition, 128–129 Heterozygous individuals, 80, 84, 102 Hexian County site, 309, 321, 322–323,

326 HIV/AIDS, 428–429, 430–431, 464, 479 HMS Beagle, 34–35 Hobbits, 318, 378–380 Holloway, R., 353 Holocene epoch, 477 Homeobox genes, 59–60, 110, 113 Homes. See Settlements Homeostasis, 414, 425 Hominin behavior/ecology, 255, 258,

260–261 adaptive patterns of, 304 biocultural evolution and, 256–257 bipedal locomotion and, 258, 271–274,

278–282 bone accumulations, analysis of, 270 butchering practice and, 270 cross-environment migrations and,

261 diet, chemical signatures of, 261 hominoid classification and, 256, 257 male-provisioning scenario and, 272,

273, 274 material culture and, 258 mosaic evolution and, 256, 257 natural objects, modification of, 261 paleoecological settings and, 262

Index542

Hominin behavior/ecology (continued) radiator theory and, 274 reconstruction/interpretation of,

270–274 scavenging strategy and, 260, 261 seasonally available foods, exploitation

of, 261 seed-eating hypothesis and, 272 stable carbon isotope analysis and, 261 stone tools/lithic technology and, 260,

261–262, 263, 268–270 See also Hominin origins; Hominins;

Paleoanthropology Hominin origins, 277

adaptive patterns of, 304 African distribution, 282–283, 304 Australopiths and, 288–299 bipedal adaptation, skeletal modifica-

tions for, 278–282 contemporaneous lineages, coexis-

tence of, 293–294 early Homo and, 299–301 interpretations of, 301–303 paleoanthropological process and, 303 pre-australopiths and, 283–288 tentative hominin phylogeny and, 303 See also Hominin behavior/ecology;

Hominins; Homo erectus; Prehominins

Hominins, 3, 9, 22, 277 adaptive patterns of, 304 behavioral stimuli for bipedalism and,

280–281 bipedal locomotion and, 22, 278–282 body weight/stature table, 287 conflict behaviors and, 209 culture, predisposition for, 6 early tool use and, 3 foot grasping and, 281, 282 foot structure, articulating elements in,

281, 282 foramen magnum repositioning and,

279, 280 habitual bipedalism and, 281, 282 hominin evolution, splitter viewpoint

and, 121 obligate bipedalism and, 281, 282 pelvic/hip modifications and,

278–279, 281, 282 See also Hominin behavior/ecology;

Hominin origins; Prehominins; Premodern humans

Hominoids, 158 classification of, 256, 257 extant hominoids, evolution of,

250–252 See also Anthropoids; Apes; Modern

humans Homo, 119, 195, 231, 274

taxonomic debate over, 310, 358–360

See also Early Homo; Hominin origins Homo antecessor, 359 Homodont dentition, 128 Homo erectus, 301, 303, 307–310, 342,

357, 359, 368 Acheulian tool industry and, 316, 323 African emigration, first dispersal and,

307, 311, 313–315, 317, 323–325 Asian Homo erectus and, 309, 310, 313,

315, 317–325 body size of, 311, 314 brain size of, 311, 313, 314, 317 cannibalism and, 322, 323, 325 Chinese Homo erectus, 319–323, 324 classification debate and, 310 cranial shape of, 311, 312, 313 cultural remains of, 320–321 discovery of, 310 Dragon Bone Hill/Zhoukoudian cave,

322–323 Eastern European Homo erectus and,

308, 316–317, 325, 326 Eurasian land links and, 315 European later Homo erectus,

325–326 fire, deliberate control/use of,

320–321 growth/development of, 314 hobbits and, 318 hunting, debate about, 320, 327 in utero development, large-brained

infants and, 314 Indonesian/Javan Homo erectus,

317–319, 323, 324 interpretations of, 328 major sites for, 308–309 morphological characteristics of,

310–311, 312, 313, 314, 316–317 Nariokotome boy skeleton and,

313–314 Oldowan tool industry and, 316, 325 population sources for, 317–318 postcranial remains and, 313–315, 316 regional populations, variation among,

307, 310, 315–317, 323, 325 scavenging strategy and, 320, 328 sexual dimorphism and, 313 speciation and, 325 tool construction/use and, 320, 321 transitional premodern humans and,

326 Trinil skullcap and, 317 See also Early Homo; Neandertals;

Premodern humans Homo ergaster, 310, 324, 359 Homo florensiensis, 379–380 Homo habilis, 287, 299–300, 303, 317 Homo heidelbergensis, 334–335, 336, 340,

342, 357, 359, 364 Homo neanderthalensis, 341, 358, 359

Homo sapiens, 3, 5, 29, 119, 122, 165–166, 257, 274, 342, 357, 359, 373

archaic Homo sapiens and, 334 bipedal adaptations and, 282 classification of, 146, 147 culture, human capacity for, 257–258 early dispersal of, 99 Neandertals, coexistence/interbreed-

ing with, 346–347, 354, 355–356 See also Anthropoids; Modern human

origins/dispersal; Modern humans; Upper Paleolithic

Homo sapiens idaltu, 371, 373 Homo sapiens neanderthalensis, 341,

358, 359 Homo sapiens sapiens, 363, 373, 378 Homologies, 108, 110, 111, 225 Homoplasy, 110, 115–116, 157–158, 225 Homozygous individuals, 80, 83, 88, 101 H1N1 (swine flu) virus, 10, 432 Honing complex, 283 Hormones, 53–54, 451

adrenocorticotropic hormone, 451 animal products, growth hormones

and, 72 cortisol, 452–453 endocrine glands and, 451 estrogen, 453 feedback loop and, 452 follicle-stimulating hormone, 451 growth hormone, 451, 452 human growth/development and,

451–453 hypothalamus gland and, 451, 452 insulin, 452 luteinizing hormone, 451 metabolism regulation and, 451 pituitary gland and, 451, 452 reproduction and, 451, 453 stress response and, 452–453 thyroid-stimulating hormone, 451, 452 thyrotropin-releasing hormone, 451,

452 thyroxine, 451–452

Hot climates, 14 Allen’s rule and, 421–422 arid environments and, 421 Bergmann’s rule and, 421–422 body hair, loss of, 420–421 body size/proportion and, 421–422,

424 dehydration and, 421 evaporative cooling and, 420–421 humid environments and, 421 responses to heat, 420–422 sweating response and, 414, 420 vasodilation and, 421, 424 See also Cold climates; Human

adaptation Houle, A., 236

Index 543

Housing. See Settlements Howler monkeys, 142, 154 Hox genes, 59–60, 110, 113 Human adaptation, 8, 10, 413, 414

acclimatization processes and, 414–415, 426

biocultural forces in, 414 cold, responses to, 422–424 culture and, 408, 414, 424 dark skin, protective response of, 417 developmental acclimatization, perma-

nent nature of, 414–415, 426 endemic disease and, 427 environmental factors and, 13, 14, 15,

414–415 evaporative cooling and, 420–421 folate degradation, neural tube defects/

spina bifida and, 417 glucose processing and, 426 heat, responses to, 414, 420–422 high-altitude settlements and, 425–427 homeostasis and, 414, 425 hypoxia and, 425–426, 427 infectious disease and, 427–433 long-term adaptations and, 414, 415 molecular anthropology and, 14 natural selection, adaptive traits and,

413–414 physiological responses, factors in, 414 selective pressures and, 414 single nucleotide polymorphisms and,

414 skeletal evidence, disease/trauma/

lifestyle and, 433–438 skin cancer, solar radiation and, 415,

416–417, 422–423 solar radiation, pigmented skin and,

414, 415–416, 417 stress on physiological mechanisms

and, 414 temporary/rapid adjustments and, 414 thermal environment and, 419–424 vasoconstriction and, 424 vasodilation and, 421, 424 vitamin D hypothesis and, 418–419,

420 zoonotic diseases and, 427, 428,

430–432 Human behavior, 5, 9

archaeological excavations and, 11 culture, learned behaviors and, 6 global climate change and, 10 infectious disease, spread of, 10 language acquisition/use and, 166, 197,

198 primate behavior, model of, 194–195 See also Anthropology; Human adapta-

tion; Modern humans Human evolution, 5, 6, 441

biocultural evolution, human life course and, 442–443

biological continuum and, 6, 8–9 breeding isolates and, 96 contemporary lifestyles, evolved

human biology and, 442, 443 continuing process of, 465–466 culture, predisposition for, 6 language, development of, 12, 197,

198–199, 200–202, 203 mammalian evolution and, 128–130 mate selection and, 96, 97 molecular anthropology and, 14 noncoding DNA and, 148 population migration and, 96–97 religious perspective on, 43–45 resource scarcity constraint and,

31–32 vertebrate evolution and, 124–128 See also Biocultural evolution; Homo

erectus; Human variation; Modern evolutionary theory; Modern humans

Human Genome Project, 42, 57, 73, 74 Human growth/development, 443–444

adolescent growth spurt and, 444 agricultural industry, epidemiological

transition and, 447–448 brain growth patterns and, 444,

464–465 contemporary diet, deficiencies in,

446, 447–449, 450 epigenetics and, 450–451, 452 epigenome and, 451 essential amino acids and, 445 food insecurity, trade/agricultural poli-

cies and, 449 genetic factors in, 450–451 growth curves for children and, 444,

445 hormones, action of, 451–453 life expectancy, declines in, 447–448 low-birth-weight infants and, 444–445 malnutrition and, 448–449, 450 mismatched diets/dietary needs and,

447, 449, 450, 458–459 nature-nurture debate and, 450–451 nutrition, effects of, 444–449 nutritional elements for health and,

445 obesity/overnutrition and, 449, 450 preagricultural diet and, 445, 447, 449 pregnancy, diet during, 444–445 puberty and, 444 sexual dimorphism and, 444 stress response, cortisol elevation and,

452–453 technology, brain growth/function

and, 464–465 undernutrition and, 448–449 See also Life history theory; Modern

humans Human variation, 12, 13, 389

adaptive significance of, 13, 394, 413–415

allele frequencies, focus on, 394, 397–398

ancestry data, utility of, 401–402 ancient migration patterns, DNA evi-

dence for, 400–401 biocultural evolution, outcomes of,

408–410 biological determinism, cultural varia-

tions and, 390–391 blood type and, 395, 396 classification schemes and, 390–391,

394–396 contemporary interpretations of,

396–397 DNA-level polymorphisms and,

398–402 environmental stressors and, 14 eugenics movement and, 391 evolutionary principles, modern

human variation study and, 394 forensic anthropology practice and,

394–395 genetic variation and, 14–15 genomic studies and, 397 geographically patterned variation and,

393–394, 395, 401–402 historical perspectives on, 390–391 lactase persistence and, 409–410 language, development of, 362 outward appearance, prejudicial treat-

ment and, 390, 392–393 point mutation and, 62–63 polygenic characteristics and, 395–396 polymorphisms and, 397–402 polytypic species and, 391 race, concept of, 391–396 racial categorization and, 390–391,

394–396 racial purity ideology and, 392–393 single nucleotide polymorphisms and,

398, 399 skin color, ranking by, 390 two-stage migration model and,

400–401 typological/stereotypical classification

and, 395 unfit/inferior people, elimination of,

391 visible physical variation and, 13 whole-genome analysis and, 399–400 within-group/between-group variation

and, 398–399 See also Human evolution; Modern

evolutionary theory; Modern humans; Population genetics; Variation

Hunter/gatherers, 6, 320, 328, 345, 424, 427, 460, 470–471

Index544

Hunting: atlatls and, 381 bow and arrow hunting, 351, 381 butchering practice and, 270, 327, 345 Homo erectus, debate about, 320, 327 Neandertals and, 350, 351 premodern humans and, 341 thrust spear hunting, 205, 341, 351, 381

Huntington disease, 84 Hutton, J., 32, 126 Hybrids, 78, 119, 121 Hylobates, 250 Hypodontia of upper lateral incisors, 84 Hypotheses, 18, 19, 21 Hypothesis testing, 20, 21, 43, 44, 85 Hypoxia, 425–426, 427

Ice Age, 317, 332, 358 Ice Man, 355, 366 Ichthyosaurus fossil, 32 Ichthyosis, 88 Immense geological time, 27, 30, 32, 107,

124–125, 126–127, 265 Immigration Restriction Act of 1924, 393 Inbreeding, 407–408 Incest avoidance behavior, 408 Incest taboos, 407–408 Independent assortment principle, 81–82 Indonesia:

hobbits/little people and, 379–380 Homo erectus, 317–318, 326 Homo floresiensis, 379–380 modern human fossils and, 373, 374,

375 Industrial Revolution, 30, 39, 475 Infanticide, 20, 190–192, 211 Infectious disease, 10

accelerated disease emergence, human activity and, 479

antibiotics, overuse of, 10, 40, 432, 433, 479

bushmeat trade and, 431 childhood mortality and, 457–458 contemporary impact of, selective

pressures and, 430–433 cultural factors in, 427 domesticated animals/plants, contact

with, 10, 427–428, 432 endemic diseases and, 427 HIV/AIDS and, 428–429 host organism, longevity of, 430 human adaptation, selective pressure

and, 427–430 human behavior patterns and, 10 human mortality and, 432–433 human population growth, environ-

mental disturbance and, 433 influenza and, 10, 431–432 malaria, 10, 101–102, 408–409, 428, 432

microorganisms, altered genetic makeup of, 10, 479

paleopathology and, 16 pandemics, 10, 432 resistance, development of, 430, 479 settlements, establishment of, 427–428 severe acute respiratory syndrome, 466 skeletal evidence of, 434 smallpox and, 429–430 stress burden and, 452 swine flu, 10 syphilis, 434 treatment-resistant microorganisms

and, 10, 40, 432–433 tuberculosis, 10, 16, 418, 428, 433 undernutrition and, 449 valley fever, 434 vectors of, 10, 427 zoonotic diseases and, 427, 428,

430–432 See also Disease

Influenza, 10, 431–432 Inheritance. See Genetics; Heredity;

Heritability; Mendelian inheritance; Mendelian inheritance in humans; Non-Mendelian inheritance

Insects, 122, 124, 128, 176, 189 Intelligence, 166, 197, 205 Intelligent design (ID) argument, 44, 45 Interglacials, 332, 333, 342 International Convention on Climate

Change, 475–476 International Human Genome

Sequencing Consortium, 57, 73 International Primate Protection League,

171 International Union for Conservation of

Nature and Natural Resources (IUCN), 160–161

Interspecific variation, 120 Intraspecific variation, 120, 121 Introns, 57–58 Invertebrates, 112, 113, 176 Iraqi Neandertals, 344, 347, 348–349 Island hopping, 227, 235, 236 Isolation. See Geographical isolation;

Reproductive isolation Israel:

modern humans fossils and, 371–372, 373

Neandertals and, 344, 347–348

Jane Goodall Institute, 171 Java:

Homo erectus, 317, 318–319, 324, 326, 333

Homo floresiensis, 379–380 Jebel Qafzeh site, 369, 370, 372 Jinniushan site, 337, 339, 340 Johanson, D., 290

Jolly, C., 272 Junk DNA, 57, 59, 61, 74, 148, 398

Kabwe site, 334, 335, 338, 340, 354 Kanapoi site, 284 Kanzi, 200 Karyotyping chromosomes, 66–67 Katanda region, 385, 386 Kebara site, 344, 347–348, 354 Kibale National Park, 209 Kimeu, K., 313 Kin selection hypothesis, 211 Kipunji, 167 Klasies River Mouth site, 354, 368, 369,

372 Knappers, 268, 269, 381 Knowles, C., 452 Knuckle walking, 146 Koko, 199 Koobi Fora site, 263, 284, 295 Kow Swamp site, 372, 374 Krapina site, 344, 346, 347 K-selected species, 189 Ku Klux Klan, 393 Kulubnarti site, 16

La Chapelle site, 343, 344, 345, 347, 350, 354

La Ferrassie site, 343, 344, 347, 354 Lactase persistence, 409, 414 Lactose intolerance, 409, 4447 Laetoli site, 3–4, 284, 289, 290, 335 Lagar Velho site, 372 Lake Baringo site, 251 Lake Mungo site, 372, 374 Lake Turkana. See East Lake Turkana;

West Lake Turkana Lamarck, J. -B., 30, 31, 33, 34 Language, 6, 186

anatomical structures and, 353 biocultural evolution and, 10 brain regions/areas and, 201–202 cuneiform writing, 7 evolution of, 200–202, 203, 352–353 human predisposition for, 12, 166, 197,

198 Neandertals, speech/symbolic behav-

ior and, 351–354 primate communication and,

199–200, 202 regulatory genes, spoken language and,

202 speech production and, 202 symbolic language, 166, 198, 199 text messaging and, 7 See also Linguistic anthropology

Langur species, 143, 144, 156, 157, 167, 191, 192

Lantian County sites, 309, 321, 324, 326 Lascaux Cave site, 383, 386

Index 545

Last common ancestor (LCA), 25, 219, 250

Late Pleistocene, 332, 342 African premodern humans and, 334 Asian modern human discoveries and,

373–375 European fossil finds and, 342 transitional hominins and, 341,

344–345 See also Neandertals; Premodern

humans Laurasia, 125, 126 Leakey, L., 299, 300, 314 Leakey, R., 313 Lee-Thorp, J., 261 Lemurs, 4, 136, 148–150, 220

adaptive level of, 150 aye-ayes and, 131, 132, 168 behavioral patterns of, 149–150 classification of, 146, 147 dental comb of, 148, 149 endangered status of, 167 evolution of, 226–228 geographical distribution of, 143,

148, 149 grooming claw on, 138, 148 locomotion of, 145, 149 nocturnal habit of, 139 olfaction, reliance on, 148 rhinarium of, 148 See also Fossil primates; Primate adap-

tations; Primates Lesch-Nyhan disease, 88 Levallois tool industry, 340, 341, 351 Lewontin, R., 401 Liang Bua Cave site, 379 Life cycle stages, 453, 454 Life history theory, 453

adolescent stage and, 444, 458–459 adulthood, activities in, 459–460 aging/longevity, postreproductive

years and, 460, 461–464 aging populations and, 464 alcohol abuse and, 455 biological transitions/markers and, 454 childbirth process, 455, 456, 459 childhood stage and, 457–458 conception/gestation, biological

aspects of, 454–455 developing fetus, environmental

impact on, 455 diseases of aging and, 462–463 diseases of civilization and, 461 epigenetic mechanisms and, 462–463 expanded child care phase and,

457, 459 free-radicals, oxidation and, 462–463 grandmother hypothesis and, 460 grandmothers, role of, 460 HIV/AIDS, impact of, 464

infancy, growth/development in, 455–457, 458

infectious disease, childhood mortality and, 457–458

life course events, trade-offs and, 453–454, 460

life cycle stages and, 453, 454 life spans/life expectancies and, 459,

460, 461, 462, 463–464 lifestyle factors, aging progression and,

463–464 menarche and, 454, 458–459 menopause and, 454, 460–461 mismatched diets/dietary needs and,

458–459 mitochondrial theory of aging and,

462–463 motherhood, parenting stage and,

459–460 nursing infants and, 456–457 pleiotropic genes and, 462 puberty, onset of, 444, 458–459 reproductive functioning, onset of,

458–459 senescence and, 461, 462–464 socioeconomic status, adolescent mat-

uration and, 459 subadult mortality rates, preindustrial

populations and, 459 telomere hypothesis and, 463 See also Human growth/development;

Modern humans Life history traits, 180–181 Linguistic anthropology, 10, 11–12

language acquisition/use, study of, 12 language groups, historical develop-

ment of, 11 Linnaeus, C., 29, 109, 121, 390 Lithic tool industry, 268–270 Locomotion:

bipedal adaptation, skeletal modifica- tions and, 278–282

bipedal locomotion, 3, 22, 271–274 brachiation, 145–146 brain-cooling/radiator theory and, 274 habitual bipedalism and, 3, 166, 281,

282, 292 knuckle walking, 146 male-provisioning scenario and, 272,

273, 274 obligate bipedalism and, 281, 282, 292 orthograde body position and, 217 prehensile tails and, 145–146 primate locomotion, 137, 145–146 quadrupedal locomotion, 22, 145, 146 radiator theory, brain-cooling posture

and, 274 seed-eating hypothesis and, 272 semibrachiation, 145–146

soft tissue anatomy and, 17 vertical clinging/leaping and, 145

Locus, 65, 66, 83 Lomorupithecus, 244 Lontandong Cave site, 309 Lorises, 4, 148, 150, 220

adaptive level of, 150 classification of, 146, 147 dental comb of, 148, 149 endangered status of, 167 evolution of, 226–228 geographical distribution of, 143, 150 grooming claw on, 138, 148 infant care and, 150 locomotion of, 150 nocturnal habit of, 139, 150 olfaction, reliance on, 148 rhinarium of, 148 See also Fossil primates; Primate adap-

tations; Primates Lovejoy, O., 272 Lower Paleolithic, 342 Lowland gorillas, 143

diet of, 162 eastern lowland gorillas, 161 tool use by, 204, 205 western lowland gorillas, 160, 161–162 See also Gorillas; Mountain gorillas

Lucy skeleton, 284, 289, 290, 291 Lufengpithecus, 241, 244, 245, 248–249,

250, 252 Lumpers, 121 Lyell, C., 32, 37

Macaque species, 143, 156, 203, 239 Macroevolution, 5, 107

adaptive radiation and, 130–131 biological continuum and, 113 cladistics and, 111, 114–117 classification systems, need for, 108 conserved genes and, 110, 112 continental drift/plate tectonics and,

124–126 evo-devo approach and, 42, 112–113 evolutionary systematics and, 111,

114, 117 fossil record, interpretation of,

119–122 generalized characteristics and,

131, 132 genetic tool kit and, 112–113 geological time scale and, 124–125,

126–127 hox genes and, 110, 113 microevolutionary mechanisms and,

132 principles of classification, taxonomic

rules and, 108–110 processes of, 130–132

Index546

Macroevolution (continued) specialized characteristics and,

131–132 speciation process and, 118–119 species, definition of, 117–118 structural modifications, mechanisms

of, 108–109, 112–113 transcription factors and, 113 See also Fossils; Mammalian evolution;

Vertebrate evolution Madagascar:

aye-ayes, specialized characteristics and, 131–132, 168

bird-dinosaur links and, 115 lemurs in, 143, 148–150, 236 ocean currents and, 227 subfossil lemurs and, 227 See also Africa

Magdalenian tool industry, 342, 380, 381–382, 383

Malapa Cave site, 284, 297, 298, 299 Malaria, 10, 101

DDT spraying and, 408–409 geographical distribution of, 10,

102, 103 human adaptation, allele frequencies

and, 428 human leukocyte antigens and, 397 mortality rates and, 432 plasmodial parasites and, 101, 102 sickle-cell trait, correlation between,

101–102, 408 slash-and-burn agriculture and, 408 See also Infectious disease

Male-provisioning scenario, 272, 273, 274 Malnutrition, 448–449, 458 Malthus, T., 31–32, 36 Mammalian evolution, 107, 128

adaptive radiation and, 131 behavioral flexibility and, 128 brain size/complexity and, 128,

129, 130 cloning and, 73 endothermic capability and, 129 extinction events, vacated eco-niches

and, 131 generalized characteristics and, 131 heterodont dentition and, 128–129 learning, capacity for, 128, 130 major mammalian groups, emergence

of, 130 marsupial mammals, 129, 130 montremes and, 130 neocortex and, 128, 129 placental mammals, expanded pro-

tected development and, 128, 130 social systems, collateral evolution of,

130 specialized characteristics and,

131–132

See also Fossil primates; Fossils; Macroevolution; Speciation; Species; Vertebrate evolution

Marfan syndrome, 84, 85 Marmosets, 142, 154, 158 Marsupial mammals, 129, 130 Mass disasters, 16, 17, 97 Material culture, 258 Matrilines, 179 Mauer site, 338 MC1R gene, 418–419 McPhee, J., 126 Medical anthropology, 18, 20 Megaladapis, 227–228 Meiosis, 66, 67, 68–71

evolutionary significance of, 70 genetic variation and, 70 independent assortment and, 81–82 nondisjunction problem and, 70–71 trisomy and, 71

Melanin, 90, 93 Menarche, 454, 458–459 Mendel, G., 42, 78 Mendelian inheritance, 42, 78, 79

cross fertilization and, 80–81, 82 discontinuous traits and, 89–90 discrete traits and, 83, 89 dominance and, 79–82 F-1 generation and, 78, 80, 81, 82 F-2 generation and, 78–79, 80, 81, 82 genotypes and, 80, 81, 82 homozygous individuals and, 80, 83 hybridization and, 78 independent assortment principle and,

81–82 parent generation and, 78, 80, 81 phenotypes and, 81, 82, 83 polydactyly and, 77, 78 polygenic inheritance and, 89–92 random assortment and, 82 recessiveness and, 79–82 segregation principle and, 78–79, 88 See also Heredity; Mendelian inheri-

tance in humans Mendelian inheritance in humans, 83, 92

autosomal dominant traits and, 85–87 autosomal recessive traits and, 87–88,

93, 104 blood type system and, 83, 85 codominance and, 83 dominance/recessiveness, misconcep-

tions about, 83–85 genetic disorders and, 83, 84, 88–89 Mendelian traits in humans, 83, 84 patterns of Mendelian inheritance and,

85–89, 93 pedigree charts and, 85, 86, 87 segregation principle and, 88 sex-linked traits and, 88–89

See also Heredity; Mendelian inheri- tance; Non-Mendelian inheritance

Menopause, 454, 460–461 Mesozoic era, 124, 125

continental drift and, 125, 126 mammalian evolution and, 128 mammalian radiation and, 131 periods of, 125, 129 primate evolution and, 218, 219

Messenger RNA (mRNA), 55–56, 57 Microcephaly, 98–99, 380 Microevolution, 5, 25

gene flow, modern human populations and, 97, 99, 104

genetic drift and, 99–100, 104 macroevolutionary mechanisms and,

132 Microfossils, 122 Microliths, 385 Microwear polish, 269 Middle Awash area, 261, 284, 285, 286,

287, 288, 289, 315, 368 Middle Paleolithic, 342 Middle Pleistocene, 332, 342

Acheulian tool industry and, 340 African premodern humans and,

334–335, 338, 340 Asian premodern humans and, 337,

339, 340 Bodo cranium and, 334–335 burial practices, evidence of, 336, 354 cannibalism and, 335 cave/open-air living sites and,

340–341 climatic conditions and, 333 culture of, 340–341 Dali skull and, 337, 339 diet in, 341 dispersal of premodern humans, 333 European premodern humans and,

335–337, 338, 340 evolutionary trajectory in, 340 fire, deliberate control/use of, 341 Homo heidelbergensis and, 334–335,

336, 340 Levallois tool industry and, 340, 341 temporary structures, construction of,

341 terminology for hominins in, 333–334 transitional hominins and, 341,

344–345 See also Late Pleistocene; Neandertals;

Premodern humans Middle Stone Age, 386 Migrations, 73, 96, 104

Arabian Plate, movement of, 244 Bering land bridge and, 222–223 DNA evidence of ancient migrations,

400–401 floating island idea and, 236

Index 547

food resource availability and, 332 glacial advances and, 332–333 interbreeding patterns and, 356–357 island hopping and, 227, 235, 236 land bridges and, 222–223, 236,

244, 315 Mozambique Channel crossing, 227 Neandertal-Homo sapiens interbreed-

ing and, 355–356 rafting and, 157–158, 227, 236, 237 two-stage migration model, 367,

400–401 See also Homo erectus; Modern human

origins/dispersal; Premodern humans

Mineralization process, 122–123 Miocene hominins, 256, 257 Miocene primates, 237–250 Missing link, 317 Mitochondria, 51, 92 Mitochondrial DNA (mtDNA), 51, 92–93,

355, 366 Mitochondrial inheritance, 92–93 Mitochondrial theory of aging, 462–463 Mitosis, 66, 67–68 Mladeč site, 372, 376, 377 Modern evolutionary theory, 94

adaptation process and, 100–101 allele frequency in populations and,

94–95, 97, 100–101, 103 evo-devo approach and, 42, 112–113 evolution, contemporary definition of,

94–95 founder effect and, 97 gene flow and, 96–97, 98, 104 gene pools and, 94 genetic bottlenecks and, 97–98, 99 genetic diversity, reduction in, 97–98 genetic drift and, 97–100, 103–104 genetic-environmental interaction and,

100–101 mate selection and, 96, 97 mutation and, 95–96, 103 natural selection, directional nature of,

100–102, 104 organizational levels in evolutionary

process and, 100 recombination and, 100 sickle-cell trait, malaria resistance and,

101–102 tandem repeats and, 95–96 two-stage evolutionary process model

and, 94 variation, production/redistribution of,

94, 95–100, 102–103 See also Evolutionary theory; Human

variation Modern human disconnect, 469–470

accelerated disease emergence, human activity and, 479

agricultural activities, species disap- pearance and, 477

air pollution and, 480 Arctic commercial ventures and, 473 Arctic sea ice, loss of, 473, 474 biodiversity, impact on, 475, 476–479 climate crisis, international policy ini-

tiatives on, 475–476 coastal inundation and, 474 cultural change, accelerating pace of,

470–472 deforestation and, 471, 472 drought, 474 evolutionary processes, detrimental

acceleration of, 479 exotic pet trade and, 170, 171, 477 extinctions and, 474–475, 477, 478 flood events and, 472, 474, 475 food insecurity, increasing incidence

of, 474, 475 global climate change and, 469,

472–476 habitat loss and, 477–479 human-created problems, solutions

for, 480–482 natural resources, destruction of, 472,

474–475 nonnative species, introduction of, 477 nonrenewable resources, exploitation

of, 471–472 ocean acidification and, 475, 476 planet/life forms, impact on, 470,

474–475, 477–479 population growth rates and, 470, 471,

477–478, 481 precipitation patterns and, 474 recreational hunting and, 477 sea ice maximum/minimum data and,

473, 474 severe weather events and, 474 soil erosion and, 471 weather patterns, severe fluctuations

in, 473–474 See also Endangered species; Modern

humans Modern human origins/dispersal,

363–364, 372 African early modern humans,

368–371, 372, 373 Asian early modern humans, 373–375 Australian early modern humans, 372,

374, 375 Central European early modern

humans, 372, 375–377 Chinese early modern humans, 372,

373, 374 complete replacement model and,

366–367 controversy over, 364

Cro-Magnon site and, 370, 372, 376, 377–378

Denisovans and, 349–350, 356–357, 367

earliest modern humans, 368–378 hobbits/little people and, 378–380 interbreeding, assimilation model and,

367, 373, 377–378 mitochondrial DNA and, 366 multiregional continuity model and,

364–365 Neandertal-human interbreeding and,

346–347, 354, 355–356, 366–367 Near Eastern early modern humans

and, 371–372, 373 origins, perspectives on, 364–367 partial replacement models and,

366–367, 378 polytypic species and, 365 two-stage migration model and, 367 Western European early modern

humans, 376, 377–378 See also Homo sapiens; Modern

humans; Upper Paleolithic Modern humans, 8, 158, 165–166,

220, 342 behavioral patterns of, 5, 6 biocultural evolution and, 257–258,

442–443, 444 biological continuum and, 6, 8–9 brain/body size, index of encephaliza-

tion and, 195–197 brain size/complexity and, 165, 166,

293 cellular structures and, 5 comparative genomics and, 148 contemporary lifestyles, evolved

biology and, 442, 443 culture and, 6, 166, 257–258 diet, declining human health and,

447–449 evolutionary processes and, 5, 6 genetic foundation of, 5 habitual bipedal locomotion and, 166 human growth/development and,

443–453 intelligence and, 166 interbreeding, gene flow and, 96–97 language acquisition/use and, 166 life course, biocultural evolution and,

442–443, 444 life history theory, human life course

and, 453–464 migration, human evolution and,

96–97 Neandertal genes, human-Neandertal

interbreeding and, 355–356, 366–367

omnivorous diet and, 165 primate heritage of, 165

Index548

Modern humans (continued) protein coding genes, complexity/

evolution of, 74 technology, human brain function and,

464–465 See also Anthropoids; Biocultural evo-

lution; Homo sapiens; Human evo- lution; Human growth/develop- ment; Life history theory; Mendelian inheritance in humans; Modern human origins/dispersal; Premodern humans

Modern Synthesis, 94, 132, 310, 394 Modified characters, 114, 116, 121 Molecular anthropology, 14, 15, 73,

219–221, 354–357 Molecular clock, 220 Molecules, 50–51, 54

signaling molecules, 113 See also Biology; Cells

Monkeys, 4, 25 bushmeat trade and, 169–171 characteristics of, 151–152 classification of, 146, 147, 154 endangered primates and, 166–172 homoplasy and, 157–158 menopause and, 460 See also Anthropoids; Fossil primates;

New World monkeys; Old World monkeys; Primates

Monophyletic groups, 111 Monotremes, 130 Morphological adaptations, 278 Mosaic evolution, 256, 257 Mosquitos. See Malaria Moula-Guercy site, 347 Mountain gorillas:

behavioral patterns of, 161 diet of, 178 endangered status of, 169 geographical distribution of, 143, 161 habitat loss and, 478 sexual dimorphism and, 161 silverback males and, 161, 162, 169 See also Gorillas; Lowland gorillas

Mousterian tool industry, 342, 349, 350, 351, 353

Movement. See Locomotion Mozambique Channel crossing, 227 Multidisciplinary approach, 259 Multiregional continuity model,

364–365 Muriquis, 142, 145, 147, 153, 154 Muscular dystrophy, 88 Musical instruments, 382 Mutation, 57, 61–63, 70, 100

albinism and, 91 hox genes and, 110, 113 mitochondrial DNA and, 92–93 Modern Synthesis and, 94

point mutation and, 62–63, 86, 91, 103 skin cancer and, 415, 422–423 tandem repeats and, 95–96 variation, production/redistribution of,

95–96

Nakalipithecus, 250, 251 Nariokotome boy skeleton, 313–314, 315 Nariokotome site, 308, 313, 314, 326 Natal groups, 161, 164, 180 National Oceanic and Atomospheric

Administration (NOAA), 472 Natural History, 29 Naturalists, 29, 34 Natural selection, 8, 26, 31, 94, 100

adaptive traits, variation and, 413–414 basic principles of, 40–42 basic processes of, 38–39, 45 Beagle voyage and, 34–35 behavioral ecology and, 176 biological variation within species and,

36–37, 112–113 breeding stock, trait selection and,

36, 37 death rates and, 41 differential net reproductive success

and, 41–42 directional nature of, 100–102, 113 discovery/development of, 33–38 disease-causing microorganisms, resis-

tant strains of, 40 environment-organism relationship

and, 36, 39–40, 132 favorable variations, preservation of,

36, 38, 39 fertility and, 41 fitness criterion and, 39, 41 fixity of species and, 27 fossil evidence and, 34–35 Galápagos finches and, 35–36, 40, 41 genetic variation and, 9, 70 heritable traits and, 40–41 individual organisms and, 39 peppered moth case and, 39, 40 point mutation and, 63 populations, evolution of, 39 religion, anti-scientific position and,

34, 37 reproductive success and, 39, 40 resource scarcity constraint and,

36, 38 selective agents and, 39 selective pressures and, 39 sickle-cell anemia and, 101, 103, 104 speciation process and, 36, 118, 119 variation in population traits and,

41, 42 See also Evolutionary theory

Nature-nurture debate and, 450–451 Nazi atrocities, 393

Neandertals, 8, 71, 331, 342, 357, 359 art/adornment and, 353–354 Asian fossil finds and, 344, 347–350 brain complexity and, 353 brain size of, 342, 345 burial practices of, 345, 346, 354 cannibalism and, 345 Central Asian Neandertals, 349–350,

355 Central European Neandertals, 344,

346–347 Chatelperronian tool industry and,

342, 347 cognitive sophistication of, 352, 353 communication, speech/symbolic

behavior and, 351–354 cranial shape/size and, 342, 343, 344,

345 culture of, 345–346, 350–354 Denisovans, contemporary existence

of, 349–350 diet of, 351 disappearance of, 354 empathy/compassion and, 349 European fossil finds and, 342, 344,

345–347, 350 flexed position burial and, 345 genetic evidence, molecular connec-

tions and, 349, 352, 354–357 genome sequencing and, 73 glaciations and, 342 Homo heidelbergensis and, 334, 340 Homo sapiens, coexistence/

interbreeding with, 346–347, 354, 355–356, 366–367

Homo sapiens neanderthalensis and, 341

hunter-gatherer behavior and, 345, 351

hunting practices of, 350, 351 hyoid bone and, 353 marine resources, exploitation of, 351 modern Europeans/Asians, genetic

inheritance of, 73 morphological characteristics of, 337,

342, 343, 344, 345, 346, 347 Mousterian tool industry and, 342,

349, 350, 351, 353 occipital bun and, 343, 345 patrilocal mating pattern and,

345, 346 skin/hair color of, 419 specialized tools and, 350 subsistence strategies and, 351 symbolic behavior and, 352–354 transitional hominins and, 341,

344–345 Western Asian Neandertals, 344,

347–349, 350

Index 549

Western European Neandertals, 344, 345–346

See also Late Pleistocene; Middle Pleistocene; Modern human ori- gins/dispersal; Modern humans; Premodern humans; Upper Paleolithic

Neander Valley, 344 Neocortex, 128, 129, 139, 195, 196 Neural tube defects, 417 New World monkeys, 152, 153–154, 155

arboreal adaptations and, 158 behavioral patterns of, 152, 154 classification of, 146, 147 diet of, 154 fossil primates and, 238 geographical distribution of, 142, 152 locomotion of, 145, 154 nails vs. claws and, 136, 154 Old World monkeys, homoplasy and,

157–158 platyrrhine characteristic of, 152 prehensile tails and, 145–146, 154, 155 rafting and, 157 semibrchiation and, 145, 154 See also Anthropoids; Monkeys; Old

World monkeys; Primates Ngandong site, 309, 312, 318, 324, 326,

333 Niah Cave site, 372, 373, 374, 375, 378 Niah skull, 375 Nocturnal habit, 138, 139 Noncoding DNA, 57, 59, 61, 74, 148, 398 Noncoding RNA, 74 Nondisjunction problem, 70–71 Non-Mendelian inheritance, 89

continuous variation and, 90, 91 genetic-environmental interaction and,

93, 100–101 mitochondrial inheritance and, 92–93 pleiotropy and, 93 polygenic inheritance and, 89–92 skin/hair/eye color and, 90–91 statistical tests, summary statistics

and, 91 See also Heredity; Mendelian inheri-

tance; Mendelian inheritance in humans

Nonrandom mating pattern, 407–408 Nucleotides, 51–52, 56 Nucleus, 50 Nutritional anthropologists, 14

Oakley, K., 264 Oase Cave site, 372, 375, 376 Obesity, 449, 450 Obligate bipedalism, 281, 282, 292 Old World monkeys, 132, 143, 155

arboreal adaptations and, 158 behavioral patterns of, 155, 157

catarrhine characteristic of, 154 cercopithecines and, 155–156 classification of, 146, 147, 155 colobines and, 156–157 diet of, 155, 156 fossil primates and, 237–239, 243 geographical distribution of, 143,

155, 156 locomotion of, 155, 156–157 New World monkeys, homoplasy and,

157–158 sexual dimorphism and, 157 See also Monkeys; New World mon-

keys; Primates Oldowan tool industry, 316, 325, 327 Olduvai Gorge site, 259, 260, 261, 263,

284, 302, 308, 326 bone accumulations, analysis of, 270 hominin foot structure and, 282 Homo erectus and, 314, 315 Homo habilis and, 299–300 stone tool industry and, 268 Zinjanthropus cranium and, 265,

266, 295 Olfaction, 138–139 Oligocene euprimates, 229–231 Oligocene primates, 231–237 Omnivorous diet, 138, 139, 144 Omo Kibish site, 263, 284, 368, 369, 372 Omomyoidea superfamily, 223, 224 1000 Genomes Project, 399 On the Origin of Species, 12, 36, 38, 42,

113, 115, 317 Orangutan Conservancy, 171 Orangutans, 19, 73, 143, 220

behavioral patterns of, 160 brachiation and, 145, 160 cranial capacity of, 293 culture, learned behaviors and, 6, 203 diet of, 160 endangered status of, 159–160, 167 geographical distribution of, 158,

159, 160 habitat loss and, 159, 160 sexual dimorphism and, 160 See also Apes; Primate behavior;

Primates Ordos site, 372, 373 Orrorin, 285, 293, 303 Orrorin tugenensis, 288, 298 Orthograde body position, 217 Osteology, 15–16 Ouranopithecus, 241, 244, 245, 246–247,

250, 251

Pacific Rim, 124, 125 Paleoanthropology, 9, 12, 13, 255

absolute dating and, 264, 267 40argon-39argon dating method and,

265–266

artifacts and, 260, 261 biostratigraphic correlation and,

228, 267 bone, analysis of, 270 carbon-14 dating method and, 266 chronometric dating and, 264–267 context/environmental settings and,

262 dating accuracy, probability statements

and, 266, 267 dating methods and, 264–267 electron spin resonance dating method

and, 266 essential processes of, 262–263 experimental archaeology and,

268–270 faunal correlation and, 228, 267 financial support and, 262 fluorine analysis and, 264 half-life and, 265, 266 hominin behavior/ecology, reconstruc-

tion of, 270–274 hominoid classification and, 256, 257 knappers and, 268, 269 multidisciplinary approach of, 259 paleomagnetism and, 266–267 potassium-argon dating method and,

265–266, 267 primary contexts and, 262 radioactive isotope decay and,

264–265 relative dating and, 264 secondary contexts and, 262 site surveys and, 259, 262 splitters vs. lumpers and, 121, 310 stable carbon isotope analysis and, 261 stone tool/lithic technology and,

268–270 stratigraphic dating and, 264, 265 superposition principle and, 264 taphonomy and, 123–124, 262, 270 thermoluminescence dating method

and, 266 tool use, sites of, 263 tool use studies and, 269–270 uranium-lead dating method and, 265 uranium series dating method and, 266 See also Archaeology; Geology;

Physical anthropology Paleodemographic studies, 459 Paleolothic, 342 Paleomagnetism, 266–267 Paleopathology, 16 Paleoprimatologists, 228 Paleospecies, 120–121 Paleozoic era, 124, 125

continental drift and, 125 periods of, 125, 128–129

Palumbi, S., 476 Pan paniscus, 164, 251

Index550

Pan troglodytes, 122, 162, 251 See also Chimpanzees

Pandemics, 10, 432 Pangea, 125 Paradigm shifts, 28–29 Paranthropus, 288, 294–296, 297, 303, 304

Black Skull find and, 294 cranial capacity of, 294 dentition of, 294, 295, 296 descendents of, 296 diet of, 294 morphological characteristics of,

294, 295 sagittal crest and, 293, 295 sexual dimorphism and, 295 See also Australopiths

Paranthropus aethiopicus, 294, 298 Paranthropus boisei, 296, 298 Paranthropus robustus, 296, 298 Parapithecus, 233 Partial replacement models, 366–367, 378 Parvorders, 233 Patrilocal mating pattern, 345, 346 Patterson, F., 199 Pedigree charts, 85, 86, 87 Peking Man, 247, 323 Peppered moths, 39, 40 Periods, 125, 128–129 Petralona site, 336, 338 Phenotypes, 81, 82, 83, 93 Photomicrographs, 66 Phylogenetic relationships, 73 Phylogenetic trees, 115, 116–117 Phylum, 108 Physical anthropology, 4, 5, 10, 12

anatomy and, 16–17, 18 anthropological perspective and,

22–23 bioarchaeology and, 16 forensic anthropology and, 16, 17, 21 genetic mechanisms and, 14 heritable traits and, 14 human variation, adaptive significance

of, 13 language acquisition/use, study of, 12 nutritional anthropology and, 14 osteology and, 15–16 paleoanthropology and, 12, 13 paleopathology and, 16 primate paleontology and, 12 primatology and, 17–18, 19 scientific method and, 19–22 visible physical variation studies and,

13, 14 See also Anthropology; Biocultural

evolution; Evolution; Human evolution

Phytoliths, 269

Pigment: art applications, 353, 354, 382,

384–385 skin color, 90–91, 390, 392, 414,

415–416, 417, 418–419 Piltdown Man, 264 Pinnacle Point site, 384, 386 PKU (phenylkentonuria), 84, 93 Placental mammals, 128, 129, 130, 131 Plate tectonics, 124–126 Platyrrhines, 152, 220, 233, 234–237 Pleiosaurus fossil, 32 Pleiotropic genes, 462 Pleiotropy, 93, 462–463 Pleistocene, 317, 332–333, 342

geographical isolation and, 340 glaciations and, 332 interglacials and, 332 oscillations and, 332 See also Premodern humans

Plesiadapiforms, 221, 222 Plesiadapis, 222 Pliopithecoidea, 242, 244 Plio-Pleistocene hominins, 299–300 Point mutation, 62–63, 86, 91, 398,

426–427 Pollen fossil material, 285 Pollution. See Environmental degradation;

Modern human disconnect Polyandry, 180, 192 Polydactyly, 77, 78, 83 Polygenic characteristics, 395–396 Polygenic inheritance, 89–92, 93 Polygynous mating, 190 Polymerase chain reaction (PCR) tech-

nique, 71, 355 Polymorphisms:

balanced polymorphism and, 409 DNA-level polymorphisms, 398–402 human polymorphisms, 397–398, 399 single-nucleotide polymorphisms, 398,

399, 414 See also Human variation

Polyphyletic groups, 111, 114 Polytypic species, 365, 391 Pongo, 249, 250, 252 Pongo pygmaeus, 159 Population genetics, 398–399, 402, 405

allele frequencies, calculation of, 404–407

allele frequencies, measurement of, 403, 404

assortative mating and, 407 breeding isolates and, 402–403 endogamy and, 403 exogamy and, 403 gene pools, genetic relatedness and,

402 genetically closed systems and, 402

Hardy-Weinberg theory of genetic equilibrium and, 403–404, 407

inbreeding, congenital disorders and, 407–408

incest avoidance behavior and, 408 mates, selection of, 402–403 modern human populations and,

407–408 nonrandom mating and, 407–408 open local population groupings and,

403 See also Human variation; Populations;

Reproduction Populations, 94

adaptive radiation process and, 130–131

aging populations, 464 allele frequency in, 94–95, 97,

100–101, 103, 118 biological adaptations, environmental

influences on, 13 environmental stressors and, 14 evolutionary processes and, 5, 6, 39,

94–95, 97, 100–101, 103 founder populations, 104 frequency of Mendelian traits and, 91 gene pools of, 94 human population growth, 470, 471 macroevolutionary processes and, 5 microevolutionary processes and, 5 molecular anthropology and, 14, 15 point mutation and, 62–63 relativistic view of culture and, 22 resource scarcity constraint and,

31–32, 36, 131 systematic variation in, 120 See also Human adaptation; Human

variation; Migrations; Natural selection; Physical anthropology; Population genetics

Postcranial material, 222, 234 Potassium-argon (K/Ar) dating method,

265–266 Potts, R., 258, 268 Pre-australopiths, 283, 284

Ardi remains and, 286–287 Ardipithecus and, 285–287, 288 dental remains, 283, 285 environmental habitats of, 287 foramen magnum repositioning and,

285 honing complex and, 283 locomotor behavior and, 285, 286–287 Orrorin and, 285 postcranial skeletal remains, conclu-

sions from, 286–287 primitive characteristics of, 286–287 Sahenlanthropus and, 283, 285, 286 wood/pollen fossil material and, 285

Index 551