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ESSENTIALS OF PHYSICAL ANTHROPOLOGY

Bn W. W. NORTON & COMPANY NEW  YORK • LONDON

ESSENTIALS OF PHYSICAL ANTHROPOLOGY D I S C O V E R I N G O U R O R I G I N S

CLARK SPENCER LARSEN T H E O H I O S T A T E U N I V E R S I T Y

T H I R D   E D I T I O N

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Library of Congress Cataloging- in- Publication Data

Larsen, Clark Spencer. Essentials of physical anthropology : discovering our origins / Clark Spencer Larsen, The Ohio State University.—Third edition. pages cm Includes index. ISBN 978-0-393-93866-1 (pbk.) 1. Physical anthropology. I. Title. GN50.4.L367 2015 599.9—dc23 2015023645

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TO CHRIS AND SPENCER, WITH MY DEEPEST THANKS FOR THEIR HELP, ENCOURAGEMENT, AND

(UNWAVERING) PATIENCE

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CLARK SPENCER LARSEN heads the Department of Anthropology at The Ohio State University, Columbus. A native of Nebraska, he received his B.A. from Kansas State University and M.A. and Ph.D. from the Uni- versity of Michigan. Clark’s research is in bioarchaeology, skeletal biol- ogy, and paleoanthropology. He has worked in North America, Europe, and Asia. He has taught at the University of Massachusetts, Northern Illi- nois University, Purdue University, and the University of North Carolina. Since 2001, he has been a member of the faculty at Ohio State, where he is Distinguished Professor of Social and Behavioral Sciences. He teaches introductory physical anthropology, osteology, bioarchaeology, and paleoanthropology. Clark has served as president of the American Association of Physical Anthropologists and as editor- in- chief of the American Journal of Physical Anthropology. In addition to Our Origins, he has authored or edited 30 books and monographs, including Bioar- chaeology: Interpreting Behavior from the Human Skeleton, Skeletons in Our Closet, Advances in Dental Anthropology, and A Companion to Biological Anthropology.

ABOUT THE AUTHOR

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To the Instructor xx To the Student xxviii

CHAPTER 1 What Is Physical Anthropology? 2

PART I The Present: Foundation for the Past 19

CHAPTER 2 Evolution: Constructing a Fundamental Scientific Theory 20

CHAPTER 3 Genetics: Reproducing Life and Producing Variation 42

CHAPTER 4 Genes and Their Evolution: Population Genetics 70

CHAPTER 5 Biology in the Present: Living People 100

CHAPTER 6 Biology in the Present: The Other Living Primates 132

CHAPTER 7 Primate Sociality, Social Behavior, and Culture 164

PART II The Past: Evidence for the Present 183

CHAPTER 8 Fossils and Their Place in Time and Nature 184

CHAPTER 9 Primate Origins and Evolution: The First 50 Million Years 216

CHAPTER 10 Early Hominin Origins and Evolution: The Roots of Humanity 244

CHAPTER 11 The Origins and Evolution of Early Homo 282

CHAPTER 12 The Origins, Evolution, and Dispersal of Modern People 306

CHAPTER 13 Our Last 10,000 Years: Agriculture, Population, Biology 350

BASIC TABLE OF CONTENTS

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TABLE OF CONTENTS

Two-Page Spreads xix

To the Instructor xx

Tools for Teaching and Learning xxiii

Who Helped xxv

To the Student xxviii

CHAPTER 1 WHAT IS PHYSICAL ANTHROPOLOGY? 2

Big Questions 3 What Is Anthropology? 5 What Is Physical Anthropology? 7

What Do Physical Anthropologists Do? 7 What Makes Humans So Different from Other Animals?: The Six Steps to

Humanness 8 How We Know What We Know: The Scientific Method 14 Answering the Big Questions 16 Key Terms 17 Evolution Review 17 Additional Readings 17

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x Table of Contentsx Table of Contents

PART I THE PRESENT: FOUNDATION FOR THE PAST 19

CHAPTER 2 EVOLUTION: CONSTRUCTING A FUNDAMENTAL SCIENTIFIC THEORY 20

Big Questions 21 The Theory of Evolution: The Context for Darwin 23

Geology: Reconstructing Earth’s Dynamic History 24 Paleontology: Reconstructing the History of Life on Earth 25 Taxonomy and Systematics: Classifying Living Organisms and Identifying Their

Biological Relationships 26 Concept Check Pre-Darwinian Theory and Ideas: Groundwork for

Evolution 27 Demography: Influences on Population Size and Competition for Limited

Resources 28 Evolutionary Biology: Explaining the Transformation of Earlier Life-Forms into

Later Life-Forms 28 Concept Check Darwin Borrows from Malthus 30 The Theory of Evolution: Darwin’s Contribution 31 Since Darwin: Mechanisms of Inheritance, the Evolutionary Synthesis, and the

Discovery of DNA 33 Mechanisms of Inheritance 33 The Evolutionary Synthesis, the Study of Populations, and the Causes of

Evolution 36 DNA: Discovery of the Molecular Basis of Evolution 37

Answering the Big Questions 39 Key Terms 39 Evolution Review: Past, Present, and Future of a Fundamental Scientific

Theory 40 Additional Readings 41

CHAPTER 3 GENETICS: REPRODUCING LIFE AND PRODUCING VARIATION 42

Big Questions 43 The Cell: Its Role in Reproducing Life and Producing Variation 44 The DNA Molecule: The Genetic Code 46

DNA: The Blueprint of Life 48 The DNA Molecule: Replicating the Code 48 How Do We Know? Ancient DNA Opens New Windows on the Past 50 Concept Check The Two Steps of DNA Replication 51

Chromosome Types 51 Mitosis: Production of Identical Somatic Cells 52 Meiosis: Production of Gametes (Sex Cells) 54 Producing Proteins: The Other Function of DNA 56

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Concept Check The Two Steps of Protein Synthesis 60 Genes: Structural and Regulatory 61 Polymorphisms: Variations in Specific Genes 61

Genotypes and Phenotypes: Genes and Their Expression 63 The Complexity of Genetics 65 Answering the Big Questions 67 Key Terms 68 Evolution Review: Insights from Genetics 68 Additional Readings 69

CHAPTER 4 GENES AND THEIR EVOLUTION: POPULATION GENETICS 70

Big Questions 71 Demes, Reproductive Isolation, and Species 72 Hardy-Weinberg Law: Testing the Conditions of Genetic Equilibrium 76 Mutation: The Only Source of New Alleles 77 Natural Selection: Advantageous Characteristics, Survival, and

Reproduction 80 Patterns of Natural Selection 81 Natural Selection in Animals: The Case of the Peppered Moth and Industrial

Melanism 82 Natural Selection in Humans: Abnormal Hemoglobins and Resistance to

Malaria 84 The Geography of Sickle-Cell Anemia and the Association with Malaria 86 The Biology of Sickle-Cell Anemia and Malarial Infection 87 The History of Sickle-Cell Anemia and Malaria 87 Other Hemoglobin and Enzyme Abnormalities 89

Genetic Drift: Genetic Change due to Chance 90 Founder Effect: A Special Kind of Genetic Drift 93

Gene Flow: Spread of Genes across Population Boundaries 93 Concept Check What Causes Evolution? 97 Answering the Big Questions 97 Key Terms 98 Evolution Review: The Four Forces of Evolution 99 Additional Readings 99

CHAPTER 5 BIOLOGY IN THE PRESENT: LIVING PEOPLE 100

Big Questions 101 Is Race a Valid, Biologically Meaningful Concept? 102

Brief History of the Race Concept 102 Debunking the Race Concept: Franz Boas Shows that Human Biology Is Not

Static 103

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xii Table of Contentsxii Table of Contents

So-Called Racial Traits Are Not Concordant 103 Human Variation: Geographic Clines, Not Racial Categories 103

Life History: Growth and Development 104 The Growth Cycle: Conception through Adulthood 105 Prenatal Stage: Sensitive to Environmental Stress, Predictive of Adult Health

105 Postnatal Stage: The Maturing Brain, Preparing for Adulthood 106 Adult Stage: Aging and Senescence 109 Evolution of Human Life History: Food, Sex, and Strategies for Survival and

Reproduction 111 Concept Check Life History Stages in Humans: Prenatal, Postnatal, and

Adult 111 Prolonged Childhood: Fat-Bodied Moms and Their Big-Brained Babies 112 Grandmothering: Part of Human Adaptive Success 112

Adaptation: Meeting the Challenges of Living 113 Climate Adaptation: Living on the Margins 114

Heat Stress and Thermoregulation 114 Body Shape and Adaptation to Heat Stress 114 Cold Stress and Thermoregulation 115 Solar Radiation and Skin Color 116 Solar Radiation and Vitamin D Synthesis 117 Solar Radiation and Folate Protection 118 High Altitude and Access to Oxygen 118

Concept Check Adaptation: Heat, Cold, Solar Radiation, High Altitude 119 Nutritional Adaptation: Energy, Nutrients, and Function 120

Macronutrients and Micronutrients 120 Human Nutrition Today 121 Overnutrition and the Consequences of Dietary Excess 123

Concept Check Nutritional Adaptation 126 Workload Adaptation: Skeletal Homeostasis and Function 126 Excessive Activity and Reproductive Ecology 128

Answering the Big Questions 129 Key Terms 130 Evolution Review: Human Variation Today 130 Additional Readings 131

CHAPTER 6 BIOLOGY IN THE PRESENT: THE OTHER LIVING PRIMATES 132

Big Questions 133 What Is a Primate? 135

Arboreal Adaptation—Primates Live in Trees and Are Good at It 138 Primates Have a Versatile Skeletal Structure 138 Primates Have an Enhanced Sense of Touch 140

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Primates Have an Enhanced Sense of Vision 141 Primates Have a Reduced Reliance on Senses of Smell and Hearing 141

Concept Check What Makes Primates Good at Living in Trees? 142 Dietary Plasticity—Primates Eat a Highly Varied Diet, and Their Teeth Reflect This

Adaptive Versatility 142 Primates Have Retained Primitive Characteristics in Their Teeth 142 Primates Have a Reduced Number of Teeth 142 Primates Have Evolved Different Dental Specializations and Functional

Emphases 143 Concept Check What Gives Primates Their Dietary Flexibility? 143

Parental Investment—Primate Parents Provide Prolonged Care for Fewer but Smarter, More Socially Complex, and Longer-Lived Offspring 146

Concept Check Primate Parenting 148 What Are the Kinds of Primates? 148

The Strepsirhines 153 Concept Check Monkey or Ape? Differences Matter 154

The Haplorhines 155 Concept Check Strepsirhines and Haplorhines Differ in Their Anatomy and

Senses 161 Answering the Big Questions 162 Key Terms 162 Evolution Review: Our Closest Living Relatives 163 Additional Readings 163

CHAPTER 7 PRIMATE SOCIALITY, SOCIAL BEHAVIOR, AND CULTURE 164

Big Questions 165 Primate Societies: Diverse, Complex, Long-Lasting 166

Diversity of Primate Societies 166 Primate Social Behavior: Enhancing Survival and Reproduction 167 Primate Residence Patterns 168 Primate Reproductive Strategies: Males’ Differ from Females’ 169

Concept Check Male and Female Reproductive Strategies 170 The Other Side of Competition: Cooperation in Primates 170

Getting Food: Everybody Needs It, but the Burden Is on Mom 172 Acquiring Resources and Transmitting Knowledge: Got Culture? 173 Vocal Communication Is Fundamental Behavior in Primate Societies 175 Answering the Big Questions 181 Key Terms 181 Evolution Review: Primate Social Organization and Behavior 182 Additional Readings 182

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PART II THE PAST: EVIDENCE FOR THE PRESENT 183

CHAPTER 8 FOSSILS AND THEIR PLACE IN TIME AND NATURE 184

Big Questions 185 Fossils: Memories of the Biological Past 188

What Are Fossils? 188 Taphonomy and Fossilization 188 Types of Fossils 188 Limitations of the Fossil Record: Representation Is Important 191

Just How Old Is the Past? 192 Time in Perspective 192 Geologic Time: Earth History 193 Relative and Numerical Age 195 Relative Methods of Dating: Which Is Older, Younger, the Same Age? 196

Stratigraphic Correlation 196 Chemical Dating 196 Biostratigraphic (Faunal) Dating 197 Cultural Dating 198

Absolute Methods of Dating: What Is the Numerical Age? 198 The Radiometric Revolution and the Dating Clock 198 The Revolution Continues: Radiopotassium Dating 203 Non-Radiometric Absolute Dating Methods 205

Genetic Dating: The Molecular Clock 207 Concept Check How Old Is It? 208 Reconstruction of Ancient Environments and Landscapes 209

The Driving Force in Shaping Environment: Temperature 210 Chemistry of Animal Remains and Ancient Soils: Windows onto Diets and

Habitats 211 Answering the Big Questions 213 Key Terms 214 Evolution Review: The Fossil Record 214 Additional Readings 215

CHAPTER 9 PRIMATE ORIGINS AND EVOLUTION: THE FIRST 50 MILLION YEARS 216

Big Questions 217 Why Did Primates Emerge? 218 The First True Primate: Visual, Tree-Dwelling, Agile, Smart 220

Primates in the Paleocene? 220 Eocene Euprimates: The First True Primates 220 The Anthropoid Ancestor: Euprimate Contenders 224 The First Anthropoids 225

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Early Anthropoids Evolve and Thrive 227 Concept Check When Were They Primates?: Anatomy through Time 227 Coming to America: Origin of New World Higher Primates 230

How Anthropoids Got to South America 230 Apes Begin in Africa and Dominate the Miocene Primate World 231 Apes Leave Africa: On to New Habitats and New Adaptations 234

Apes in Europe: The Dryopithecids 234 Apes in Asia: The Sivapithecids 235 Dead End in Ape Evolution: The Oreopithecids 235 Climate Shifts and Habitat Changes 238 Miocene Ape Survivors Give Rise to Modern Apes 238

Apes Return to Africa? 238 Concept Check The First Apes: A Remarkable Radiation 239 Monkeys on the Move 239 Answering the Big Questions 241 Key Terms 242 Evolution Review: Primate Social Organization and Behavior:

The Deep Roots of the Order Primates 242 Additional Readings 243

CHAPTER 10 EARLY HOMININ ORIGINS AND EVOLUTION: THE ROOTS OF HUMANITY 244

Big Questions 245 What Is a Hominin? 246

Bipedal Locomotion: Getting Around on Two Feet 248 Nonhoning Chewing: No Slicing, Mainly Grinding 248

Why Did Hominins Emerge? 251 Charles Darwin’s Hunting Hypothesis 251

Concept Check What Makes a Hominin a Hominin? 252 Peter Rodman and Henry McHenry’s Patchy Forest Hypothesis 254 Owen Lovejoy’s Provisioning Hypothesis 254 Sexual Dimorphism and Human Behavior 255 Bipedality Had Its Benefits and Costs: An Evolutionary Trade-Off 255

What Were the First Hominins? 256 The Pre-Australopithecines 256

Sahelanthropus tchadensis (7–6 mya) 257 Orrorin tugenensis (6 mya) 257 Ardipithecus kadabba and Ardipithecus ramidus (5.8–4.4 mya) 258

Concept Check The Pre-Australopithecines 263 The Australopithecines (4–1 mya) 264

Australopithecus anamensis (4 mya) 265 Australopithecus afarensis (3.6–3.0 mya) 266 Australopithecus (Kenyanthropus) platyops (3.5 mya) 269

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Diversification of the Homininae: Emergence of Multiple Evolutionary Lineages from One (3–1 mya) 269

Australopithecus garhi (2.5 mya) 270 The First Tool Makers and Users: Australopithecus or Homo? 270

Evolution and Extinction of the Australopithecines 273 Concept Check The Australopithecines 276 Answering the Big Questions 280 Key Terms 280 Evolution Review: The First Hominins 281 Additional Readings 281

CHAPTER 11 THE ORIGINS AND EVOLUTION OF EARLY HOMO 282

Big Questions 283 Homo habilis: The First Species of the Genus Homo 285

The Path to Humanness: Bigger Brains, Tool Use, and Adaptive Flexibility 285

Homo habilis and Australopithecus: Similar in Body Plan 287 Homo habilis’s Adaptation: Intelligence and Tool Use Become Important 287 Habitat Changes and Increasing Adaptive Flexibility 288

Concept Check Homo habilis: The First Member of Our Lineage 288 Homo erectus: Early Homo Goes Global 289

Homo erectus in Africa (1.8–.3 mya) 290 Homo erectus in Asia (1.8–.3 mya) 293 Homo erectus in Europe (1.2 million–400,000 yBP) 296 Evolution of Homo erectus: Biological Change, Adaptation, and Improved

Nutrition 297 Patterns of Evolution in Homo erectus 302

Concept Check Homo erectus: Beginning Globalization 303 Answering the Big Questions 304 Key Terms 305 Evolution Review: The Origins of Homo 305 Additional Readings 305

CHAPTER 12 THE ORIGINS, EVOLUTION, AND DISPERSAL OF MODERN PEOPLE 306

Big Questions 307 What Is So Modern about Modern Humans? 309 Modern Homo sapiens: Single Origin and Global Dispersal or Regional

Continuity? 309 What Do Homo sapiens Fossils Tell Us about Modern Human Origins? 311

Early Archaic Homo sapiens 311 Archaic Homo sapiens in Africa (350,000–200,000 yBP) 312

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Early Archaic Homo sapiens in Asia (350,000–130,000 yBP) 312 Early Archaic Homo sapiens in Europe (500,000–130,000 yBP) 313 Early Archaic Homo sapiens’ Dietary Adaptations 313

Late Archaic Homo sapiens 314 Late Archaic Homo sapiens in Asia (60,000–40,000 yBP) 315 Late Archaic Homo sapiens in Europe (130,000–30,000 yBP) 316 The Neandertal Body Plan: Aberrant or Adapted? 319 Neandertal Hunting: Inefficient or Successful? 321 Neandertals Buried Their Dead 324 Neandertals Talked 325 Neandertals Used Symbols 327

Early Modern Homo sapiens 327 Concept Check Archaic Homo sapiens 328

Early Modern Homo sapiens in Africa (200,000–6,000 yBP) 329 Early Modern Homo sapiens in Asia (90,000–18,000 yBP) 331 Early Modern Homo sapiens in Europe (35,000–15,000 yBP) 332

Modern Behavioral and Cultural Transitions 334 How Has the Biological Variation in Fossil Homo sapiens Been

Interpreted? 335 Ancient DNA: Interbreeding between Neandertals and Early Modern People? 336

Concept Check Early Modern Homo sapiens 337 Living People’s Genetic Record: Settling the Debate on Modern Human Origins 338

Assimilation Model for Modern Human Variation: Neandertals Are Still with Us 339

Concept Check Models for Explaining Modern Homo sapiens’ Origins 340 Modern Humans’ Other Migrations: Colonization of Australia, the Pacific, and

the Americas 340 Down Under and Beyond: The Australian and Pacific Migrations 342 Arrival in the Western Hemisphere: The First Americans 344

Answering the Big Questions 348 Key Terms 349 Evolution Review: The Origins of Modern People 349 Additional Readings 349

CHAPTER 13 OUR LAST 10,000 YEARS: AGRICULTURE, POPULATION, BIOLOGY 350

Big Questions 351 The Agricultural Revolution: New Foods and New Adaptations 353

Population Pressure 354 Regional Variation 355 Survival and Growth 359

Agriculture: An Adaptive Trade-Off 360 Population Growth 360 Environmental Degradation 361

Concept Check The Good and Bad of Agriculture 362

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How Did Agriculture Affect Human Biology? 362 The Changing Face of Humanity 363

Two Hypotheses 363 Implications for Teeth 365

Concept Check Soft Food and Biological Change 365 Building a New Physique: Agriculture’s Changes to Workload/Activity 366 Health and the Agricultural Revolution 369

Population Crowding and Infectious Disease 369 Concept Check Labor, Lifestyle, and Adaptation in the Skeleton 370

The Consequences of Declining Nutrition: Tooth Decay 371 Nutritional Consequences Due to Missing Nutrients: Reduced Growth and

Abnormal Development 371 Nutritional Consequences of Iron Deficiency 373

Concept Check Health Costs of Agriculture 374 Nutritional Consequences: Heights on the Decline 375

If It Is So Bad for You, Why Farm? 375 The Past Is Our Future 375 Our Ongoing Evolution 376 Answering the Big Questions 378 Key Terms 379 Evolution Review: Setting the Stage for the Present and Future 379 Additional Readings 380

Appendix: The Skeleton A1

Glossary A11

Glossary of Place Names A19

Bibliography A21

Permissions Acknowledgments A47

Index A51

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T WO- PAGE SPRE ADS

I1

ENHANCED TOUCH

Primates have an enhanced sense of touch. This sensitivity is due in part to the presence of dermal ridges (fingerprints and toe prints) on the inside surfaces of the hands and feet. The potto, a prosimian, has primitive dermal ridges, whereas the human, a higher primate, has more derived ridges, which provide better gripping ability.

Em er

gi ng

c an

op y

M ai

n ca

no py

U nd

er st

or y

GENERALIZED SKELETAL STRUCTURE

Primates have a generalized skeletal structure. The bones that make up the shoulders, upper limbs, lower limbs, and other major joints such as the hands and feet are separate, giving primates a great deal of flexibility when moving in trees. In this monkey skeleton, note the grasping hands and feet, the long tail, and the equal length of the front and hind limbs relative to each other.

REDUCED SMELL

Primates have a reduced sense of smell. The smaller and less projecting snouts of most primates indicate their decreased reliance on smell.

DIETARY VERSATILITY

Primates have dietary plasticity. Part of the record of primate dietary adaptation is found in the teeth. The red colobus monkey dentition shown here is typical of a catarrhine dentition with a 2/1/2/3 dental formula. Note the differences in morphology of the four different tooth types: incisors (I1, I2), canines (C), premolars (P3, P4), and molars (M1, M2, M3).

ENHANCED VISION

Primates have an enhanced sense of vision. Evolution has given primates better vision, including increased depth perception and seeing in color. The eyes’ convergence provides significant overlap in the visual fields and thus greater sense of depth.

Human Potto

Overlapping visual fields

Taï Forest

MonkeyDog

Reduced snout length

I1 I2I2

CC

P3P3 P4P4 M1

M2

M3

M1

M2

M3

I1I1 I2I2 CC

P3P3

P4P4

M1

M2

M3

M1

M2

M3

Black-and-white colobus

Campbell’s

Chimpanzee

Demidoff’s galago

Diana monkey

Human

Lesser spot-nosed

Olive colobus

Potto

Putty-nosed

Red colobus

Sooty mangabey

Thomas’s galago

Eagle

F I G U R E

6.2 Primate Adaptation in Microcosm: The Taï Forest, Ivory Coast, West Africa

Apes Leave Africa: On to New Habitats and New Adaptations | 237236 | CHAPTER 9 Primate Origins and Evolution: The First 50 Million Years

Primate evolution began with primitive primates in the Eocene, setting the stage for the origin of all hominoids. Euprimates of the Eocene had the basic characteristics of living primates, such as convergent eye orbits and grasping digits. In the last 20 million years, primates diversified in appearance and behavior. These changes included the shift, for some, from life in the trees to life on the ground, and eventually the beginning of bipedality in the late miocene. (Based on Fleagle, J. G. Primate Adaptation and Evolution, 2nd ed. 1999. Academic Press.)

Scenes from the late Eocene in the Paris Basin. Top: The diurnal Adapis is feeding on leaves. Bottom: Several taxa of omomyids (Pseudoloris, Necrolemur, Microchoerus). Note the large eyes, a nocturnal adaptation, typical of both ancient and modern prosimians who are active at night.

Scene from the early Miocene of Rusinga Island, Kenya. Apes first appeared during this period, and these are the first apes (two species of Proconsul, Dendropithecus, Limnopithecus). These and other taxa form the ancestry of all later apes and hominins. Note the range of habitats occupied by these primates within the forest, including some in the middle and lower canopies and some on the forest floor. These primates show a combination of monkeylike and apelike features, in the skeleton and skull, respectively.

Scenes from the early Oligocene of the Fayum, Egypt. These anthropoid ancestors include Aegyptopithecus, Propliopithecus, and Apidium. These primates were adept arborealists, using their hands and feet for climbing and feeding.

Convergent eyes and grasping hands

Large eyes for nocturnal vision

Eocene 34–56 mya

Oligocene 23–34 mya Miocene 5.3–23 mya

Quadrupedal, monkeylike primate with superb arboreal skills

Quadrupedal, apelike primate. Note the lack of a tail, an ape characteristic.

Eocene-Oligocene-Miocene Habitats and Their Primates

F I G U R E

9.21

Figure 1.3 The Six Big Events of Human Evolution: Bipedalism, Nonhoning Chewing, Dependence on Material Culture, Speech, Hunting, and Domestication of Plants and Animals pp. 10–11

Figure 3.17 Protein Synthesis pp. 58–59

Figure 6.2 Primate Adaptation in Microcosm: The Taï Forest, Ivory Coast, West Africa pp. 136–137

Figure 9.21 Eocene– Oligocene– Miocene Habitats and Their Primates pp. 236–237

Figure 10.16 From Discovery to Understanding: Ardipithecus of Aramis pp. 260–261

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TO THE INSTRUCTOR

HOW THIS BOOK CAN HELP YOUR STUDENTS DISCOVER PHYSICAL ANTHROPOLOGY

IT IS ABOUT ENGAGEMENT

Teaching is about engagement— connecting the student with knowledge, making it real to the student, and having the student come away from the course with an understanding of core concepts. Essentials of Physical Anthropology seeks to engage the student in the learning process. Engaging the student is perhaps more of a challenge in the study of phys- ical anthropology than in the study of other sciences, mainly because the student has likely never heard of the subject. The average student has probably taken a precollege course in chemistry, physics, or biology. Physical anthropology, though, is rarely mentioned or taught in precollege settings. Commonly, the student first finds out about the subject when an academic advisor explains that physical anthro- pology is a popular course that fulfills the college’s natural science requirement.

Once taking the course, however, that same student usually connects quickly with the subject because so many of the topics are familiar— fossils, evolution, race, genet- ics, DNA, monkeys, forensic investigations, and origins of speech, to name a few. The student simply had not real- ized that these separately engaging topics come under the umbrella of one discipline, the subject of which is the study of human evolution and human variability.

Perhaps drawn to physical anthropology because it focuses on our past and our present as a species, the student quickly sees the fundamental importance of the discipline. In Discover magazine’s 100 top stories of 2009, 18 were from physical anthropology. Three topics from the field were in the top 10, including the remarkable new discovery of our earliest human ancestor, Ardipithecus. So important was this discovery that Science, the leading international professional science journal, called it the “Breakthrough of the Year” for

2009. The discussions in this textbook of topics familiar and unfamiliar give the student stepping- stones to science and to the centrality of physical anthropology as a window into understanding our world. Whether the students find the material familiar or unfamiliar, they will see that the book relates the discipline to human life: real concerns about human bodies and human identity. They will see themselves from an entirely different point of view and gain new awareness.

In writing this book, I made no assumptions about what the reader knows, except to assume that the reader— the stu- dent attending your physical anthropology class— has very little or no background in physical anthropology. As I wrote the book, I constantly reflected on the core concepts of phys- ical anthropology and how to make them understandable. I combined this quest for both accuracy and clarity with my philosophy of teaching— namely, engage the student to help the student learn. Simply, teaching is about engagement. While most students in an introductory physical anthro- pology class do not intend to become professional physical anthropologists, some of these students become interested enough to take more courses. So this book is written for stu- dents who will not continue their study of physical anthro- pology, those who get “hooked” by this fascinating subject (a common occurrence!), and those who now or eventually decide to become professionals in the field.

The book is unified by the subject of physical anthropol- ogy. But equally important is the central theme of science— what it is, how it is done, and how scientists (in our case, anthropologists) learn about the natural world. I wrote the book so as to create a picture of who humans are as organ- isms, how we got to where we are over the last millions of years of evolution, and where we are going in the future in light of current conditions. In regard to physical anthro- pology, the student should finish the book understanding human evolution and how it is studied, how the present helps us understand the past, the diversity of organisms living and past, and the nature of biological change over

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time and across geography. Such knowledge should help the student answer questions about the world. For example, how did primates emerge as a unique group of mammals? Why do people look different from place to place around the world? Why is it important to gain exposure to sunlight yet unsafe to prolong that exposure? Why is it unhealthy to be excessively overweight? Throughout their history, what have humans eaten, and why is it important to know?

I have presented such topics so that the student can come to understand the central concepts and build from them a fuller understanding of physical anthropology. Throughout the book, I emphasize hypothesis testing, the core of the scientific method, and focus on that process and the excite- ment of discovery. The narrative style is personalized. Often I draw on my own experiences and those of scientists I know or am familiar with through their teaching and writing, to show the student how problems are addressed through field- work or through laboratory investigations.

Scientists do not just collect facts. Rather, they collect data and make observations that help them answer questions about the complex natural world we all inhabit. Reflecting this practice, Essentials of Physical Anthropology is a collec- tion not of facts for the student to learn but of answers to questions that help all of us understand who we are as living organisms and our place in the world. Science is a way of knowing, it is a learning process, and it connects our lives with our world. In these ways, it is liberating.

HOW THE BOOK IS ORGANIZED

The book is divided into two parts. Following an introduc- tory overview of anthropology and physical anthropology, Part  I presents the key principles and concepts in biology, especially from an evolutionary perspective. This material draws largely on the study of living organisms, including humans and nonhuman primates. Because much of our understanding of the past is drawn from what we have learned from the present, this part lays the foundation for the presentation in Part II— the past record of primate and human evolution. In putting the record of the living up front, this book departs from the style of most other introductory physical anthropology textbooks, which start out with the earliest record and end with the living. This book takes the position that most of what we learn about the past is based on theory and principles learned from the living record. Just as all of Charles Darwin’s ideas were first derived from seeing living plants and animals, much of our understanding of function and adaptation comes from living organisms as models. Therefore, this book views the living as the window

into what came before— the present contextualizes and informs our understanding of the past. It is no mistake, then, that Discovering Our Origins is the subtitle of the book. The origins of who we are today do not just lie in the record of the past, but are very much embodied in the living. Our origins are expressed in our physical makeup (bone, teeth, and muscles), in our behavior, and in so many other ways that the student taking this course will learn about from this book and from you. You can teach individual chapters in any order, and that is partly because each chapter reinforces the central point: we understand our past via what we see in the living.

Part II presents evidence of the past, covering more than 50  million years of primate and human evolution. Most textbooks of this kind end the record of human evolution at about 25,000 years ago, when modern Homo sapiens evolved worldwide. This textbook also provides the record since the appearance of modern humans, showing that important bio- logical changes occurred in just the last 10,000 years, largely relating to the shift from hunting and gathering to the domestication of plants and animals. Food production was a revolutionary development in the human story, and Part II presents this remarkable record, including changes in health and well- being that continue today. A new subdiscipline of physical anthropology, bioarchaeology, is contributing pro- found insights into the last 10,000 years, one of the most dynamic periods of human evolution.

During this period, a fundamental change occurred in how humans obtained food. This change set the stage for our current environmental disruptions and modern living conditions, including global warming, the alarming global increase in obesity, and the rise of health threats such as newly emerging infectious diseases, of which there is little under- standing and for which scientists are far from finding cures.

CHANGES IN THE THIRD EDITION

Reflecting the dynamic nature of physical anthropology, there are numerous revisions and updates throughout this new, third edition of Essentials of Physical Anthropology. These updates provide content on the cutting- edge developments in the discipline, give new ways of looking at older findings, and keep the book engaging and timely for both you and your students. Although the core principle of the book remains the same, namely the focus on evolution, the revi- sions throughout the book present new insights, new discov- eries, and new perspectives. Other changes are intended to give added focus and clarity and to increase the visual appeal that supports the pedagogy of engagement and learning:

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• New content on biocultural adaptation. Anthropol- ogists provide important insights into how humans’ remarkable intelligence is related to their evolution- ary success. This third edition presents new research on the role of social learning and the retention of knowledge— the accumulation of information— over many generations.

• New primate taxonomy. In order to inform students about the latest developments in primate classifica- tion, the third edition has shifted from the tradi- tional, grade- based approach used in the previous editions to the cladistics, or phylogenetic, approach. This approach provides students with a classifica- tion based on ancestor- descendant evolutionary relationships.

• New content on developments in genetics that are altering our understanding of phenotype. We are learning that non- protein coding DNA, often considered “junk” DNA, has important implications for various other instructions in the genome. Similarly, the rapidly expanding field of epigenetics is revealing evolution- ary change without alteration of DNA.

• New content on race and human variation in Chapter 5. • New content on maladaptive human behavior and health

outcomes such as obesity. The role of environment is fundamental in understanding patterns of health in very recent human evolution, including the impacts of the creation of obesogenic environments, the alarming rise in obesity globally, and the causes and consequences of these changing circumstances and outcomes.

• New content on fossil primate and hominin discoveries. Exciting new discoveries in early primate evolution from Africa and Asia are revealing the enormous variety and complexity of species. New discoveries from East Africa reveal that although all australo- pithecines were bipedal, some retained arboreal behavior relatively late in the evolution of these early hominins. New discovery of stone tools dat- ing to 3.3 million years ago—700,000 years earlier than previously known—from East Africa shows the beginnings of humankind’s reliance on material culture. Once thought to be the domain of Homo, these early dates show use of tools by earlier aus- tralopithecines, long before the origins of our genus. These discoveries continue to illustrate the com- plexity of early hominin evolution. New evidence from chemical and tooth wear analyses reveals that at least some later australopithecines were eating significant quantities of low- quality vegetation,

including grasses on the African savanna, confirming the long- held notion that some had highly specialized diets.

• New findings on the origins of cooking and its importance in human evolution. Controlled use of fire dates to as early as 1 mya in South Africa. This innovation provided a means for cooking meats and starches, thereby increasing the digestibility of these foods. New research suggests that cooking and nutri- tional changes associated with cooking may have “fueled” the increase in brain and body size in early hominins.

• New content on the appearance and evolution of modern Homo sapiens and the Neandertal genome. Analysis of the direction and pattern of scratches on the incisors of Neandertals reveals that they were pre- dominantly right- handed. In addition to showing this modern characteristic, this finding reveals that this earlier form of H. sapiens had brain laterality, a feature linked to speech. Neandertals talked. New genetic evidence reveals the presence of Neander- tal genes in modern humans, consistent with the hypothesis that modern H. sapiens interbred with Neandertals. Newly discovered hominin fossils from Denisova, Siberia, dating to the late Pleistocene represent a genome that is different from Neander- tals’ and modern H. sapiens’. This newly discovered “Denisovan” genome is also found in people living today in East Asia, suggesting that modern H. sapiens encountered Neandertals as well as other populations once in Europe.

• New findings on the future of humankind. The study of melting ice caps and glaciers around the world today reveals a dramatic warming trend. As temperatures rise, habitats are in the process of changing. These environmental changes will provide a context for evolution, both in plants and in animals. These fac- tors, coupled with reduction in species diversity, are creating new health challenges for humans today and for the foreseeable future.

• Revision of content to enhance clarity. I have contin- ued to focus on helping students understand core concepts, with considerable attention given to cell biology, genetics, DNA, race and human variation, primate taxonomy, locomotion, and dating methods. As in previous editions, I paid careful attention to the clarity of figure captions. The captions do not simply repeat text. Instead, they offer the student additional details relevant to the topic and occasional questions about concepts that the figures convey.

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• Greatly enhanced art program. The new edition con- tains over 100 new or revised figures, often using a new “photorealistic” style. The book adds several full- color two- page spreads developed by Mauri- cio Antón, a world- renowned artist with expertise in conveying past life through wonderful visual presentations.

• “Evolution Review” sections. At the end of each chapter, an “Evolution Review” section summarizes material on evolution in that chapter and includes assignable questions about concepts and content. Suggested answers appear in the Instructor’s Manual.

• InQuizitive. Norton’s new formative and adaptive online learning resource improves student under- standing of the big picture concepts of physical anthropology. Students receive personalized quiz questions on the topics they need the most help with. Engaging, game- like elements motivate students as they learn. These are intended for use in teaching face- to- face, blended, or online class formats.

• New lab manual. This text now has a new lab manual, the Lab Manual for Biological Anthropology—Engaging with Human Evolution by K. Elizabeth Soluri and Sabrina C. Agarwal. This flexible and richly illus- trated manual is designed to support or enhance your current labs and collections, or work on its own. Attractively priced, discount bundles can be pur- chased including this text.

AIDS TO THE LEARNING PROCESS

Each chapter opens with a vignette telling the story of one person’s discovery that relates directly to the central theme of the chapter. This vignette is intended to draw your stu- dents into the excitement of the topic and to set the stage for the Big Questions that the chapter addresses.

BIG QUESTION learning objectives are introduced early in the chapter to help your students organize their reading and understand the topic.

CONCEPT CHECKS are scattered throughout each chap- ter and immediately follow a major section. These aids are intended to help your students briefly revisit the key points they have been reading about.

LOCATOR MAPS are placed liberally throughout the book. College- level instructors tend to hope that students have a good sense of geography, but like a lot of people who do not

look at places around the world on a daily basis, students often need reminders about geography. In recognition of this, locator maps in the book’s margins show the names and locations of places that are likely not common knowledge.

PHOTOREALISTIC ART YOU CAN “TOUCH”: Designed to give students an even better appreciation for the feel of the discipline, the art program has been substantially reworked. Now most illustrations of bones and skeletons have an almost photorealistic feel, and most primates were redrawn for a high degree of realism. This book helps your students visualize what they are reading about by including hundreds of images, many specially prepared for the book. These illustrations tell the story of physical anthropology, including key processes, central players, and important con- cepts. As much thought went into the pedagogy behind the illustration program as into the writing of the text.

DEFINITIONS are also presented in the text’s margins, giving your students ready access to what a term means generally in addition to its use in the associated text. For convenient reference, defined terms are signaled with bold- face page numbers in the index.

At the end of each chapter, ANSWERING THE BIG QUESTIONS presents a summary of the chapter’s central points organized along the lines of the Big Questions pre- sented at the beginning of the chapter.

The study of evolution is the central core concept of physical anthropology. The newly introduced EVOLUTION REVIEW section at the end of each chapter discusses topics on evolution featured in the chapter and asks questions that will help the student develop a focused understanding of content and ideas.

INQUIZITIVE is our new game- like, formative, adaptive assessment program featuring visual and conceptual ques- tions keyed to each chapter’s learning objectives from the text. InQuizitive helps you track and report on your students’ progress to make sure they are better prepared for class.

Join me now in engaging your students in the excitement of discovering physical anthropology.

TOOLS FOR TEACHING AND LEARNING

The Essentials of Physical Anthropology teaching and learning package provides instructors and students with all the tools they need to visualize anthropological concepts, learn key vocabulary, and test knowledge.

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FOR INSTRUCTORS

InQuizitive

New InQuizitive online formative and adaptive assessment is available for use with Essentials of Physical Anthropology, Third Edition, featuring interactive and engaging questions with answer- specific feedback. InQuizitive features ques- tions designed to help students better understand the core objectives of each chapter. Built to be intuitive and easy to use, InQuizitive makes it a snap to assign, assess, and report on student performance and help keep your class on track. Options are available to integrate InQuizitive into your LMS or Coursepack. Contact your local  W.  W.  Norton representative for details.

Lab Manual and Workbook for Biological Anthropology— Engaging with Human Evolution by K. Elizabeth Soluri and Sabrina C. Agarwal.

This new manual captures student interest and illustrates the discipline with the vivid images— every chapter contains large detailed figures, photographs that are properly scaled, and drawings of bones and fossils with an almost three- dimensional appearance. The labs are grouped into four units of four chapters each: 1) genetics/evolutionary theory; 2) human osteology and forensics; 3) primatology; and 4) paleoanthropology. No topic is over- or underemphasized, and the manual is flexibly designed to be used as a whole, or as individual labs, and with a school’s cast and photo collec- tion or with the sample photos provided. Each lab has unique Critical Thinking Questions to go with Chapter Review and Lab Exercises. This manual is available at student friendly prices, either as a stand- alone volume or bundled with this text, or as a custom volume.

Coursepacks

Available at no cost to professors or students, Norton Coursepacks for online or hybrid courses are available in a variety of formats, including all versions of Blackboard and WebCT. Content includes review quizzes, flash cards, and links to animations and videos. Coursepacks are available from wwnorton.com/instructors.

New Animations

These new animations of key concepts from each chapter are available in either the Coursepacks, or from wwnorton.com/ instructors. Animations are brief, easy to use, and great for explaining concepts either in class or in a distance- learning environment.

New Videos

This new streaming video service is now available through Norton Coursepacks and at wwnorton.com/instructors. These one- to seven- minute educational film clips from across the discipline but with an emphasis on paleoanthro- pology and primatology help students see and think like anthropologists and make it easy for instructors to illustrate key concepts and spark classroom discussion.

Update PowerPoint Service

To help cover what is new in the discipline, each semester we will provide a new set of supplemental lectures, notes, and assessment material covering current and breaking research. Prepared by Laurie Reitsema (University of Georgia) and with previous updates from Kathy Droesch (Suffolk County Community College), this material is available for download at wwnorton.com/instructors.

PowerPoint Slides and Art JPEGs

Designed for instant classroom use, these slides prepared by Jeremy DeSilva (Boston University) using art from the text are a great resource for your lectures. All art from the book is also available in PowerPoint and JPEG formats. Download these resources from wwnorton.com/instructors.

Instructor’s Manual

Prepared by Nancy Tatarek (Ohio University) and Greg Laden, this innovative resource provides chapter summaries, chapter outlines, lecture ideas, discussion topics, suggested reading lists for instructors and students, a guide to “Writ- ing about Anthropology,” suggested answers to Evolution Matters questions, and teaching materials for each video.

Test Bank

Prepared by Renee Garcia (Saddleback College) and Greg Laden, this Test Bank contains multiple- choice and essay questions for each chapter. It is downloadable from Norton’s Instructor’s Website and available in Word, PDF, and ExamView® Assessment Suite formats. Visit wwnorton.com/ instructors.

Ebook

An affordable and convenient alternative, Norton ebooks retain the content and design of the print book and allow students to highlight and take notes with ease, print chap- ters as needed, and search the text.

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WHO HELPED

I owe much to the many people who made this book possible, from the planning and writing of the first and sec- ond editions, and now this third edition. First and foremost, I thank my wife, Christine, and son, Spencer, who helped in innumerable ways. They were my captive audience: without protest, they listened to my ideas at the dinner table, on family trips, and in other places where we probably should have been talking about other things. Chris read many drafts of chapters and gave great advice on when and where to cut, add, or rethink. I thank my parents, the late Leon and Patricia Larsen, who introduced me to things old and sparked my interest in the human past.

Jack Repcheck first approached me about writing a text- book on introductory physical anthropology. His power of persuasion, combined with my own interest in the discipline and its presentation to college students, was instrumental in reeling me in and getting the project off the ground. Jack and others at W. W. Norton & Company made the process of writing the book a great experience in all ways, from writ- ing to publication. On the first  edition, I began work with editors John Byram and then Leo Wiegman. I am indebted to Pete Lesser, who took on the project after Leo. Pete gave direction on writing and production, provided very helpful feedback on presentation and pedagogy, and orchestrated the process of review, revision, and production— all without a hitch. Under Pete’s guidance, the first edition became the most widely used textbook in physical anthropology. Jack Repcheck continued the project in preparation for the sec- ond edition. The preparation of the third edition was over- seen by editor Eric Svendsen. His advice and guidance were central to seeing the book come to fruition. Tacy Quinn recently joined the team and has spearheaded the develop- ment of new media for this edition including InQuizitive. Marina Rozova does an excellent job developing the core supplement package for each edition. Kurt Wildermuth edited the entire manuscript for the first two editions. His skill as an editor and staying on top of content from begin- ning to end added enormously to the book’s presentation and readability. Sunny Hwang has now taken Kurt’s place and has especially helped with revisions in the end- of- chapter mate- rial and the on- line supplements program. Diane Cipollone was instrumental in producing these pages and directing a wide variety of editing issues that arose, and the entire team is now supported by Rachel Goodman. Ben Reynolds guided the process of production from beginning to end. I am also grateful to Mauricio Antón for his wonderful new illustra- tions of six “big events” of human evolution in chapter 1, the new rendition of the Taï Forest primates as a microcosm of

primate adaptation in chapter 6, and the Eocene, Oligocene, and Miocene primates and their habitats in chapter 9. Greg Laden, Renee Garcia, and Nancy Tatarek’s timely and effi- cient completion of the Test Bank and Instructor’s Manual is much appreciated. Laurie Reitsema has been recently added to the team producing our valuable update PowerPoints each semester, and I thank Kathy Droesch for her past work on these updates.

With the input of instructors and focus group attendees who are included in the reviewer list, we have created an extensive new media and assessment suite for the third  edi- tion. However, my thanks for extensive work in developing InQuizitive and our new animations go to Tracy Betsinger of SUNY Oneonta, Ashley Hurst of University of Texas at San Antonio, Kristina Killgrove of University of West Florida, Greg Laden, Joanna Lambert of the University of Colorado, and Heather Worne of University of Kentucky, with further thanks to contributors Jaime Ullinger, Quinnipiac University, and Nancy Cordell, South Puget Sound Community College. And thanks to Sandra Wheeler of University of Central Flor- ida, Ellen Miller of Wake Forest University, Bonnie Yoshida of Grossmont College, Jacqueline Eng of Western Michigan University, Jeremy DeSilva of Boston University,  K.  Eliza- beth Soluri of College of Marin, and again Nancy Cordell of South Puget Sound Community College for their important feedback and reviews of these resources.

Thanks go to former and current graduate students and faculty colleagues at the Ohio State University who helped in so many ways. I offer a very special thanks to Tracy Betsinger, who assisted in a number of aspects of the book. For the first edition, she read drafts of chapters at various stages and helped in figure selection, in glossary compilation, and as a sounding board in general for ideas that went into the book. For the second edition, she offered very helpful suggestions for revisions. Thanks to Jaime Ullinger, who provided the content and data for the box on PTC tasting. Tracy, Jaime, Jim Gosman, Dan Temple, Haagen Klaus, and Josh Sadvari read parts or all of the manuscript and offered great advice. For all three editions, I had many helpful discussions with Scott McGraw about primate behavior, evolution, and tax- onomy. Scott also provided advice on the production  of the two- page spreads on both primate diversity and eagle predation in the Taï Forest, Ivory Coast (chapters  6 and 7). For this edition, John Fleagle provided valuable support reviewing details in most of the new primate illustrations, in particular the two- page spreads, and every new piece of art was first reviewed in the larger Our  Origins volume by Arthur Durband, Andrew Kramer, and Sandra Wheeler. Doug Crews gave advice on the complexities of primate (including human) biology and  life history. Haagen Klaus

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provided materials for and help on the two- page spread on the biological consequences of the agricultural revolution and many other helpful comments and suggestions for revision. Barbara Piperata advised me on key aspects of modern human biology and nutrition science, and Dawn Kitchen provided discussion and help on the fundamentals of primate communication and how best to present it. Josh Sadvari was indispensable in the creation of the Evolution Review sections at the end of each chapter.

Over the years, I have had helpful conversations with my teachers, colleagues, and students about areas of their exper- tise, and these people have influenced the development of the book in so many ways. I am grateful to Patricia  J.  O’Brien and Milford  H.  Wolpoff, my respective undergraduate and graduate advisors. Both were instrumental in developing my interest in science and the wonderful profession I work in. I thank Barry Bogin, Kristen Hawkes, Jim O’Connell, David Thomas, Bob Kelly, Jerry Milanich, Bruce Smith, Kris Gremillion, Bonnie McEwan, Matt Cartmill, Dale Hutchinson, Chris Ruff, Simon Hillson, Michael Schultz, Sam Stout, Doug Ubelaker, Dan Sellen, Clark Howell, Rick Steckel, Phil Walker, John Relethford, Mark Weiss, Mar- garet Schoeninger, Karen Rosenberg, Lynne Schepartz, Fred Smith, Brian Hemphill, Bruce Winterhalder, Meg Conkey, Desmond Clark, Erik Trinkaus, Katherine Russell, Vin Steponaitis, Mark Teaford, Richard Wrangham, Jerry Rose, Mark Cohen, William Bass, Loring Brace, Stanley Garn, Frank Livingstone, Phil Gingerich,  T.  Dale Stew- art, Larry Angel, Mike Finnegan, Harriet Ottenheimer, Marty Ottenheimer, Roberto Frisancho, Randy Susman, Karen Strier, Joanna Lambert, Jim Hijiya, Cecil Brown, Bill Fash, Rich Blanton, Henry Wright, James Griffin, Bill Jungers, David Frayer, Bill Pollitzer, George Armelagos, Jane Buikstra, Elwyn Simons, Steve Churchill, Neil Tubbs, Bob Bettinger, Tim White, Dean Falk, Owen Lovejoy, Scott Simpson, David Carlson, Alan Goodman, Bill Dancey, Debbie Guatelli- Steinberg, Sam Stout, Clark Mallam, and Chris Peebles.

I would like to thank Joanna E. Lambert, University of Colorado–Boulder and Friderun Ankel-Simons, Duke Uni- versity for their help and their words used to prepare the back cover description. Their response was helpful, timely, and their suggested wording was perfect.

The book benefited from the expertise of many anthro- pologists and other experts. I especially acknowledge the fol- lowing reviewers for their insights, advice, and suggestions for revision of the text and creation of the support package:

Sabrina Agarwal, University of California, Berkeley Paul Aiello, Ventura College Lon Alterman, North Carolina State University

Tara Devi Ashok, University of Massachusetts Boston Diana Ayers- Darling, Mohawk Valley Community

College Philip de Barros, Palomar College Thad Bartlett, University of Texas at San Antonio Cynthia Beall, Case Western Reserve University Owen Beattie, University of Alberta Anna Bellisari, Wright State University Daniel Benyshek, University of Nevada, Las Vegas Tracy Betsinger, State University of New York at Oneonta Deborah Blom, University of Vermont Amy Bogaard, Oxford University Günter Bräuer, University of Hamburg Emily Brunson, University of Washington Victoria Buresch, Glendale Community College Isabelle Champlin, University of Pittsburgh at Bradford Joyce Chan, California State University, Dominguez

Hills Chi- hua Chiu, Kent State University David Clark, Catholic University of America Robert Corruccini, Southern Illinois University Herbert Covert, University of Colorado Douglas Crews, Ohio State University Eric Delson, Lehman College, City University of

New York Katherine Dettwyler, University of Delaware Joanne Devlin, University of Tennessee Paul Erickson, St. Mary’s University Becky Floyd, Cypress College David Frayer, University of Kansas Daniel Gebo, Northern Illinois University Anne Grauer, Loyola University of Chicago Mark Griffin, San Francisco State University Michael Grimes, Western Washington University Gregg Gunnell, Duke University Lesley Harrington, University of Alberta Lauren Hasten, Las Positas College John Hawks, University of Wisconsin– Madison Samantha Hens, California State University, Sacramento James Higham, New York University Madeleine Hinkes, San Diego Mesa College Homes Hogue, Ball State University Nina Jablonski, Pennsylvania State University Karin Enstam Jaffe, Sonoma State University Gabriela Jakubowska, Ohio State University Gail Kennedy, University of California, Los Angeles Dawn Kitchen, Ohio State University Haagen Klaus, George Mason University Patricia Lambert, Utah State University Michael Little, Binghamton University Chris Loeffler, Irvine Valley College

xxvi Instructor

Sara Lynch, Queens College, City University of New York Lorena Madrigal, University of South Florida Ann Magennis, Colorado State University Stephen Marshak, University of Illinois at

Urbana– Champaign Debra Martin, University of Nevada, Las Vegas Thomas McDade, Northwestern University William McFarlane, Johnson County Community

College Scott McGraw, Ohio State University Rachel Messinger, Moorpark College Ellen Miller, Wake Forest University Leonor Monreal, Fullerton College Ellen Mosley- Thompson, Ohio State University Michael Muehlenbein, Indiana University Dawn Neill, California Polytechnic State University, San

Luis Obispo Wesley Niewoehner, California State University, San

Bernardino Kevin Nolan, Ball State University Rachel Nuger, Hunter College, City University of

New York Dennis O’Rourke, University of Utah Janet Padiak, McMaster University Amanda Wolcott Paskey, Cosumnes River College Michael Pilakowski, Butte College Janine Pliska, Golden West College Deborah Poole, Austin Community College Leila Porter, Northern Illinois University Frances E. Purifoy, University of Louisville Mary Ann Raghanti, Kent State University Lesley M.  Rankin- Hill, University of Oklahoma Jeffrey Ratcliffe, Penn State Abington Laurie Reitsema, University of Georgia Melissa Remis, Purdue University Analiese Richard, University of the Pacific Charles Roseman, University of Illinois Karen Rosenberg, University of Delaware John Rush, Sierra College Andrew Scherer, Brown University Timothy Sefczek, Ohio State University Lynette Leidy Sievert, University of Massachusetts

Scott W. Simpson, Case Western Reserve University Cynthia Smith, Ohio State University Fred Smith, Illinois State University Richard Smith, Washington University Sara Smith, Delta College Lilian Spencer, Glendale Community College Sara Stinson, Queens College, City University of

New York Christopher Stojanowski, Arizona State University Margaret Streeter, Boise State University Karen Strier, University of Wisconsin– Madison Nancy Tatarek, Ohio University Lonnie Thompson, Ohio State University Victor Thompson, University of Georgia Christopher Tillquist, University of Louisville Sebina Trumble, Hartnell College Lisa Valkenier, Merritt College Dennis Van Gerven, University of Colorado Boulder Ronald Wallace, University of Central Florida David Webb, Kutztown University Daniel Wescott, Texas State University Tim White, University of California, Berkeley Janet Wiebold, Spokane Community College Caleb Wild, Mira Costa College Leslie Williams, Beloit College Sharon Williams, Purdue University Kristen Wilson, Cabrillo College Milford Wolpoff, University of Michigan Thomas Wynn, University of Colorado Colorado Springs

Thanks, everyone, for your help! Lastly, a very special thanks goes to all of the faculty around the globe who adopted the previous two editions of Essentials of Physical Anthropology for their introductory physical anthropology classes. I am also grateful to the hundreds of students who connected with the book— many of whom have written me with their comments. Please continue to send me your com- ments ([email protected]).

Columbus, Ohio August 10, 2015

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TO THE STUDENT

PHYSICAL ANTHROPOLOGY IS ABOUT DISCOVERING WHO WE ARE

THINKING LIKE AN ANTHROPOLOGIST

Who are we? Where do we come from? Why do we look and act the way we do? This book is a journey that addresses these and other big questions about us, Homo sapiens. This journey emphasizes humans’ discovery of the fascinating record of our diversity and of our evolution, a record that serves as a collective memory of our shared biological pres- ence on Earth. From here to the end of the book, I will share with you all kinds of ideas that add up to our current understanding of human beings as living organisms. Along the way, you will experience scientific breakthroughs such as the Human Genome Project and forensics (you might even watch CSI and Bones in a whole new way). You will gain new understandings of phenomena such as race and human diversity, global warming and its impact on our evolution and our well- being, the origins of human violence, global disease, and the growing worldwide obesity epidemic. Like an anthropologist tackling important questions, you will discover places on nearly every continent and come to see what life was like for millions of years before the present, before the emergence and evolution of humans.

Neither your instructor nor I can expect you as an intro- ductory student to understand all the developments in phys- ical anthropology. Both of us can, however, present you with a clear and concise framework of the field. By the time you are finished reading this book and completing this course, you will have a solid background in the basic tenets of the discipline. This knowledge will help you understand your place in nature and the world that we— more than 7 billion of us and growing— live in. The framework for developing your understanding of physical anthropology is  the scien- tific method, a universal approach to understanding the very complex natural world. You should not assume that this book and this course are about only knowing the right

answers, the “facts” of physical anthropology. Rather, they are also about seeing how physical anthropologists know what they know— understanding the scientific method. So as you read, keep in mind the key questions that scientists try to answer, their processes and methods for finding the answers, and the answers themselves.

In writing this book, I have focused on the big ques- tions in physical anthropology, how scientists have tackled them, and what key discoveries have been made. I have not shied away from identifying the scientists who made these discoveries— real people, young and old, from all over the world. Whether you need to learn all these individuals’ names and what they contributed to the growth of physical anthropology and to our knowledge of human evolution and variation is up to your instructor. But in the introductory physical anthropology class that I teach, I encourage my stu- dents to learn about the people behind the ideas. By seeing the field through these people’s eyes, you can start thinking like an anthropologist.

SEEING LIKE AN ANTHROPOLOGIST

Thinking like an anthropologist includes seeing what anthropologists see. We anthropologists are constantly looking at things— fossilized human teeth, ancient DNA, excavated stone tools, primate skeletons, and much more— and using what we see to understand biology in the past and in the present. The photos and drawn art throughout this book have been chosen to help you see what anthropologists see. I strongly encourage you to pay close attention to the visuals in the book and their captions because much of our anthropological understanding is in the art program.

THE STRUCTURE OF THE BOOK

The book is divided into two parts. Following an overview of anthropology and physical anthropology (chapter 1), Part I provides the basic context for how we understand human (and our nonhuman primate relatives’) biology in the present

(and how that helps us understand the past). From this section of the book you should come away with an under- standing of evolution and the biology associated with it. Evolution as an idea has a long history (chapter 2). You will need to fully grasp the meaning and power of this theory, which explains humans’ biological variation today and in the past. Part I also has the important job of providing you with an understanding of genetics (chapters  3 and 4). This information is a central part of the evidence for evolution, from the level of the molecule to the level of the population.

Part I also looks at the biology of living people, that of the other living primates, and the variation among primate spe- cies. I am keen on debunking the common notion that there are discrete categories— races— of human beings (chapter 5). In fact, nothing about the biology of people, present or past, indicates that we can be divided into distinct groups. After looking at how environment and culture help shape the way humans look and behave, I will look similarly at nonhuman primates (chapters  6 and 7). Because nonhuman primates’ appearances are much more categorical than humans’ are, nonhuman primate appearance lends itself to classification or taxonomy. In these chapters, we will look at what nonhu- man primates do in the wild, what they are adapted to, and especially the environment’s role in shaping their behavior and biology. By looking at living people and living nonhu- man primates, we will be better equipped to understand the biological evidence drawn from the past.

Part II examines the processes and evidence physical anthropologists and other scientists use to understand the past (chapter  8), the evolution of prehuman primate ances- tors that lived more than 50  million years ago (chapter  9), and both the emergence of our humanlike ancestors and their evolution into modern humans (chapters  10, 11, and 12). Contrary to popular (and some scientific) opinion, human evolution did not stop when anatomically modern people first made their appearance in various corners of the globe. Rather, even into the last 10,000 years a considerable amount of biological change has occurred. Anthropologists have learned that agriculture, which began some 10,000 years ago, has been a fundamental force behind population increase. The downside of this shift to new kinds of food and the resulting population increase was a general decline in health. The later section of Part II (chapter 13) explores the nature and cause of biological change, including the changes associated with health and well- being that led to the biological and environmental conditions we face today.

With this book in hand and our goals— thinking and see- ing like anthropologists— in mind, let us set off on this excit- ing journey. Consider it a voyage of discovery, on which our shipmates include your instructor and your fellow students. If we work hard and work together, we will find perhaps the most interesting thing on Earth: ourselves.

To the Student xxix

Gorilla meets hominin and author of Essentials of Physical Anthropology Clark Larsen.

ESSENTIALS OF PHYSICAL ANTHROPOLOGY

THE GEORGIA COAST WAS A FOCAL point for Spanish colonization in the sixteenth and seventeenth centuries. European colo- nization set in motion changes in human living conditions that eventually affected human biology on a global scale.

3 3

1 What is anthropology?

What is physical anthropology?

What makes us human and different from other animals?

How do physical anthropologists know what they know?

1

2

3

4

What Is Physical Anthropology?

In the heat of the midday summer sun, our boat slowly made its way across the five miles of water that separate mainland Georgia from St. Catherines Island, one of a series of barrier islands dotting the Atlantic seaboard. Today, the island is covered by dense vegetation typical of the subtropical American South— palmettos and other palm trees, pines, hickories, and live oaks— and is infested with a wide array of stinging and biting insects. It is hard to imagine that this setting was once a focal point of the Span- ish colonial “New World,” representing the northernmost extension of Spain’s claim on eastern North America. This was the location of the Roman Catholic church and mis- sion Santa Catalina de Guale, where several hundred Indians and a dozen Spaniards lived and worked during the late 1500s and most of the 1600s.

What could possibly have motivated my field team and me to work for months under a blazing sun, fighting insects? Like any scientific investigation, our fieldwork was moti- vated by specific questions that we keenly wanted to answer. Buried in the sands of St. Catherines were the mortal remains— skeletons— of the native people who had lived at this long- abandoned place. These remains held answers to questions about the biology of modern people. Native Americans had lived in this area of the world for most of the last 10,000 years. We wanted to know about their biological evolution and vari- ation: How had these people changed biologically over this time span? What caused these changes? What circumstances led to the changes that we hoped to identify and interpret?

When we first set foot on St. Catherines Island in the summer of 1982 to begin our work at Mission Santa Catalina, we were excited about our project, but little did we

B I G Q U E S T I O N S ?

4 | CHAPTER 1 What Is Physical Anthropology?

realize just what a spectacular scientific journey we were undertaking. The skel- etons we sought turned out to provide wonderfully rich biological details about a little- understood region of the world, especially relating to the health consequences and behavioral consequences of European contact on native peoples. In setting up the research project, I had envisioned that our findings would provide a microcosm of what had unfolded globally— in the Americas, Asia, Africa, and Australia— during the previous 500 years of human history. During this period, significant biological changes had taken place in humans. Some of these changes were evolutionary— they resulted in genetic change. Other biological changes, nonevolutionary ones, reflected significant alterations in health and lifestyle, alterations that had left impressions on the skeletons we studied. Such study— of genetic and nongenetic changes— here and elsewhere in the world has proven fundamental to human beings’ understanding of their biology in the early twenty- first century.

Like any scientific investigation, the research project at Mission Santa Catalina did not develop in a vacuum. Prior to our work there, my team and I had devoted nearly a decade to studying hundreds of skeletons we had excavated from the region, dating from before the arrival of Spaniards. We had learned from archaeological evidence that before AD 1000 or so the people there ate exclusively wild animals, fish, and wild plants— they were hunters and gatherers. Never settling into one place for any period of time, they moved from place to place over the year, hunting animals, fishing on the coastline, and collecting plants. Then, their descendants— the ancestors of the mission Indians— acquired corn agriculture, becoming the first farmers in the region. These people did lots of fishing, but farming produced the mainstay of their diet. This major shift in lifestyle led to the establishment of semipermanent villages. In comparison with the hunter– gatherers living before AD 1000, the later agricultural people were shorter, their skulls and limb bones were smaller, and they had more dental disease and more infections. All of this information— scientific discoveries about the prehistoric people, their biological changes, and their adaptations— set the stage for our return to the island to study the people who lived at Santa Catalina, the descendants of the prehistoric hunter– gatherers and later farmers. From our study of their remains, we learned that after the Spaniards’ arrival the native people worked hard, they became more focused on producing and eating corn, and their health declined. The combination of declining quality of life and new diseases introduced by the Spaniards led to the native people’s extinction in this area of North America.

The research just described is one small part of the broader discipline known as physical anthropology. My work concerns life on the southeastern United States Atlantic coast, but physical anthropologists explore and study everywhere how humans and their ancestors lived. This enterprise covers a lot of ground and a lot of time, basi- cally the entire world and the last 50 million years or so! The territorial coverage of physical anthropology is so widespread and so diverse because the field addresses broad issues, seeking to understand human evolution— what we were in the past, who we are today, and where we will go in the future. Physical anthropologists seek answers to questions about why we are what we are as biological organisms. How we answer these questions is oftentimes difficult. The questions, though, motivate physical anthropologists to spend months in the subtropics of coastal Georgia, learning about an extinct native people; in the deserts of central Ethiopia, finding and studying the remains of people who lived hundreds, thousands, or even millions

What Is Anthropology? | 5

of years ago; or at the high altitudes of the Andes Mountains, studying living people and their responses and long- term adaptation to low oxygen and extreme cold, to name just a few of the settings you will learn about in this book. In this chapter, we will explore in more detail the nature of physical anthropology and its subject matter.

What Is Anthropology? When European explorers first undertook transcontinental travel (for example, Marco Polo into Asia in the late 1200s) or transoceanic voyages to faraway lands (for example, Christopher Columbus to the Americas in the late 1400s and early 1500s), they encountered people that looked, talked, dressed, and behaved very differently from themselves. When these travelers returned to their home coun- tries, they described the peoples and cultures they saw. Building on these accounts, early scholars speculated on the relationships between humans living in Europe and those encountered in distant places. Eventually, later scholars developed new ideas about other cultures, resulting in the development of the discipline of anthropology.

Anthropology is the study of humankind, viewed from the perspective of all people and all times. As it is practiced in the United States, it includes four branches or subdisciplines: cultural anthropology, archaeology, linguistic anthropology, and physical anthropology, also called biological anthropology (Figure 1.1).

Cultural anthropologists typically study present- day societies in non- Western settings, such as in Africa, South America, or Australia. Culture— defined as learned behavior that is transmitted from person to person— is the unifying theme of study in cultural anthropology.

Archaeologists study past human societies, focusing mostly on their material remains— such as animal and plant remains and places where people lived in the past. Archaeologists are best known for their study of material objects— artifacts— from past cultures, such as weaponry and ceramics. Archaeologists study the processes behind past human behaviors— for example, why people lived where they did, why some societies were simple and others complex, and why people shifted from hunting and gathering to agriculture beginning more than 10,000 years ago. Archaeologists are the cultural anthropologists of the past— they seek to reassemble cultures of the past as though those cultures were alive today.

Linguistic anthropologists study the construction and use of language by human  societies. Language— defined as a set of written or spoken symbols that refer to things (people, places, concepts, etc.) other than themselves— makes possible the transfer of knowledge from one person to the next and from one gen- eration to the next. Popular among linguistic anthropologists is a subfield called sociolinguistics, the investigation of language’s social contexts.

Physical (or biological) anthropologists study all aspects of present and past human biology. As we will explore in the next section, physical anthropology deals with the evolution of and variation among human beings and their living and past relatives.

No anthropologist is expected to be an expert in all four branches. Anthropol- ogists in all four areas and with very different interests, however, acknowledge the diversity of humankind in all contexts. No other discipline embraces the breadth of the human condition in this manner. In fact, this remarkably diverse discipline

anthropology The study of humankind, viewed from the perspectives of all peo- ple and all times.

cultural anthropology The study of modern human societies through the analysis of the origins, evolution, and variation of culture.

archaeology The study of historic of pre- historic human populations through the analysis of material remains.

linguistic anthropology The study of the construction, use, and form of language in human populations.

physical anthropology The original term for biological anthropology.

biological (physical) anthropology The study of the evolution, variation, and adaptation of humans and their past and present relatives.

culture Learned behavior that is transmit- ted from person to person.

artifacts Material objects from past cultures.

language A set of written or spoken sym- bols that refer to things (people, places, concepts, etc.) other than themselves.

sociolinguistics The science of investigat- ing language’s social contexts.

6 | CHAPTER 1 What Is Physical Anthropology?

differs from other disciplines in its commitment to the notion that, unlike other animals, humans are biocultural— both biological and cultural beings. Anthro- pologists are interested in the interrelationship between biology and culture. Anthropologists call this focus the biocultural approach. Anthropology also differs from other disciplines in emphasizing a broad comparative approach to the study of biology and culture, looking at all people (and their ancestors) and all cultures in all times and all places. Anthropologists are interested in people and their ancestors, wherever or whenever they lived. Simply, you are studying a field that is holistic, unlike any you have studied before.

biocultural approach The scientific study of the interrelationship between what humans have inherited genetically and culture.

The Four Branches of Anthropology

Cultural Anthropology Archaeology Linguistic Anthropology Physical Anthropology

The study of cultures and societies of human beings and their very recent past.

Traditional cultural anthropologists study

living cultures and present their observations in

an ethnography.

The study of past societies and their cultures,

especially the material remains of the past, such

as tools, food remains, and places where people lived.

The study of language, especially how language

is structured, the evolution of language, and the social

and cultural contexts for language.

Also called biological anthropology, physical

anthropology is the study of human evolution and variation, both past and current.

FIGURE 1.1 The Four Branches of Anthropology (a) Cultural anthropologists, who study living populations, often spend time living with cultural groups to gain more intimate perspectives on those cultures. The American anthropologist Margaret Mead (1901–1978), one of the most recognizable names in cultural anthropology, studied the peoples of the Admiralty Islands, near Papua New Guinea. (b) Archaeologists study past human behaviors by investigating material remains that humans leave behind, such as buildings and other structures. In the Peruvian Andes, this archaeologist examines the remnants of a brewery used by the Wari Empire (ca. AD 750–1000). (c) Linguistic anthropologists study all aspects of language and language use. Here, Leslie Moore, a linguistic anthropologist working in a Fulbe community in northern Cameroon, records as a teacher guides a boy in memorizing Koranic verses. (d) Physical anthropologists study human evolution and variation. Some physical anthropologists study skeletons from the past to investigate evolution and variation throughout human history. Those working in forensic anthropology, a specialty within physical anthropology, examine skeletons to identify who they were in life. Such an identification may be of a single person or of thousands. For example, the forensic anthropologist pictured here was called on to help identify the estimated 30,000 victims of Argentina’s “Dirty War,” which followed the country’s 1976 coup.

(a) (b) (c) (d)

forensic anthropology The scientific exam- ination of skeletons in hope of identifying the people whose bodies they came from.

What Is Physical Anthropology? | 7

What Is Physical Anthropology? The short answer to this question is, Physical anthropology is the study of human biologi- cal evolution and human biocultural variation. Two key concepts underlie this definition.

Number one, every person is a product of evolutionary history, or all the bio- logical changes that have brought humanity to its present form. The remains of humanlike beings, or hominins, indicate that the earliest human ancestors, in Africa, date to sometime around 6–8  million years ago (mya). Since that time, the physical appearance of hominins and their descendants, including modern humans, has changed dramatically. Our physical appearance, our intelligence, and everything else that makes us distinctive biological organisms evolved in our predecessors, whose genes led to the species we are today. (Genes and species are among the subjects of chapters 3 and 4.)

Number two, each of us is the product of his or her own individual life history. From the moment you were conceived, your biological makeup has been deter- mined mostly by your genes. (The human genome— that is, all the genetic mate- rial in a person— includes some 20,000–25,000 genes.) Your biological makeup is also strongly influenced by your environment. Environment here refers not just to the obvious factors such as climate but to everything that has affected you— the physical activities you have engaged in (which have placed stress on your muscles and bones), the food you have eaten, and many other factors that affect overall health and well- being. Environment also includes social and cultural factors. A disadvantaged social environment, such as one in which infants and children receive poor- quality nutrition, can result in negative consequences such as poor health, reduced height, and shortened life expectancy. The Indian child who lived after the shift from foraging to farming on the Georgia coast ate more corn than did the Indian child who lived in the same place before AD 1000. Because of the corn- rich diet, the later child’s teeth had more cavities. Each child’s condition reflects millions of years of evolution as well as more immediate circumstances, such as diet, exposure to disease, and the stresses of day- to- day living.

WHAT DO PHYSICAL ANTHROPOLOGISTS DO? Physical anthropologists routinely travel to places throughout the United States and around the world to investigate populations. Some physical anthropologists study living people, while others study extinct and living species of our nearest biological relatives, primates such as lemurs, monkeys, and apes. I am among the physical anthropologists who travel to museum collections and archaeological localities to study past societies. When I tell people outside the field what I do for a living, they often think physical anthropology is quite odd, bizarre even. Frequently they ask, “Why would anyone want to study dead people and old bones and teeth?” Everyone has heard of physics, chemistry, and biology; but the average person has never heard of this field. Compared to other areas of science, physical anthropology is small. But smallness does not make it unimportant. It is practical and important, providing answers to fundamental questions that have been asked by scholars and scientists for centuries, such as Who are we as a species? What does it mean to be human? Where did we come from? Moreover, physical anthropology plays a vital role in address- ing questions that are central to our society, sometimes involving circumstances that all of us wish had never come about. For example, the tragedy that Americans identify as 9/11 called immediately for the assistance of specialists from forensic anthropology.

hominin Humans and humanlike ancestors.

genome The complete set of genetic information— chromosomal and mito- chondrial DNA— for an organism or spe- cies that represents all of the inheritable traits.

primates A group of mammals in the order Primates that have complex behavior, varied forms of locomotion, and a unique suite of traits, including large brains, forward- facing eyes, fingernails, and reduced snouts.

8 | CHAPTER 1 What Is Physical Anthropology?

The discipline as practiced in the United States began in the first half of the twentieth century, especially under the guidance of three key figures: Franz Boas for American anthropology generally; Czech- born Aleš HrdliČka, who started the professional scientific journal and professional society devoted to the field; and Earnest Hooton, who trained most of the first generation of physical anthro- pologists. While the theory and methods of physical anthropologists today have changed greatly since the early 1900s, the same basic topics first envisioned by these founders form what we do.

Physical anthropologists study all aspects of human biology, specifically looking at the evolution and variation of human beings and their living and past relatives. This focus on biology means that physical anthropologists practice a biological science. But they also practice a social science, in that they study biology within the context of culture and behavior. Depending on their areas of interest, physical anthropologists might examine molecular structure, bones and teeth, blood types, breathing capacity and lung volume, genetics and genetic history, infectious and other types of disease, origins of language and speech, nutrition, reproduction, growth and development, aging, primate origins, primate social behavior, brain biology, and many other topics dealing with variation in both the living and the dead— sometimes the very long dead (Figure 1.2)!

In dealing with such topics, physical anthropologists apply methods and theo- ries developed in other disciplines as well as in their own as they answer questions that help us understand who we are, a point that I will raise over and over again throughout this book. The very nature of their discipline and their constant borrowing from other disciplines mean that physical anthropologists practice an interdisciplinary science. For example, they might draw on the work of geologists who study the landforms and layering of deposits of soil and rock that tell us when earlier humans lived. Or they might obtain information from paleontologists, who study the evolution of life- forms in the distant past and thus provide the essential context for understanding the world in which earlier humans lived. Some physical anthropologists are trained in chemistry, so they can analyze the chemical properties of bones and teeth to determine what kinds of foods were eaten by those earlier humans. Or to learn how living humans adapt to reduced- oxygen settings, such as in the high altitudes of the Peruvian Andes Mountains, physical anthropologists might work with physiologists who study the lungs’ ability to absorb oxygen. The firm yet flexible identity of their science allows physical anthropologists to gather data from other disciplines in order to address key questions. Questions drive what they do.

What Makes Humans So Different from Other Animals?: The Six Steps to Humanness Human beings clearly differ from other animals. From humanity’s earliest origin— about 6–8 mya, when an apelike primate began walking on two feet— to the period beginning about 10,000 years ago, when modern climates and environments emerged following what is commonly known as the Ice Age, six key attributes developed that make us unique. These attributes are bipedalism, nonhoning chewing, complex material culture and tool use, hunting, speech, and dependence on domesticated foods (Figure 1.3, pp. 10–11). The first development represents

FIGURE 1.2 A Sample of What Physical Anthropologists Do (a) Human remains excavated at Bactia Pozzeveri, a medieval church cemetery in Tuscany, Italy, provide a window onto health and living conditions in Europe. (b) Geneticists analyze samples of human DNA for various anthropological purposes. DNA studies are used to determine how closely related humans are to other primate species, to examine human origins, and to determine individual identities. (c) A human biologist records the physical activities of a lactating woman (right, weaving basket) living in a rural community in the eastern Amazon, Brazil. These data will be used to calculate the woman’s energy expenditure and to understand how she copes with reproduction’s great energy demands. (d) In a lab, a forensic anthropologist measures and assesses human bones. If the bones came from a contemporary grave, this forensic information might help to identify the victim. If the bones belonged to a past population, physical anthropologists might use these data to gain insight into the population’s health and lifestyle. (e) Laboratory investigations of human ancestors’ bones help paleoanthropologists to determine where these ancestors fit in the human family tree. (f) Primatologists, such as the British researcher Jane Goodall (b. 1934), study our closest living relatives, nonhuman primates. The behavior and lifestyle of chimpanzees, for example, help physical anthropologists to understand our evolutionary past.

(c)

(a)

(e)

(b)

(d)

(f)

What Makes Humans So Different from Other Animals?: The Six Steps to Humanness | 9

The discipline as practiced in the United States began in the first half of the twentieth century, especially under the guidance of three key figures: Franz Boas for American anthropology generally; Czech- born Aleš HrdliČka, who started the professional scientific journal and professional society devoted to the field; and Earnest Hooton, who trained most of the first generation of physical anthro- pologists. While the theory and methods of physical anthropologists today have changed greatly since the early 1900s, the same basic topics first envisioned by these founders form what we do.

Physical anthropologists study all aspects of human biology, specifically looking at the evolution and variation of human beings and their living and past relatives. This focus on biology means that physical anthropologists practice a biological science. But they also practice a social science, in that they study biology within the context of culture and behavior. Depending on their areas of interest, physical anthropologists might examine molecular structure, bones and teeth, blood types, breathing capacity and lung volume, genetics and genetic history, infectious and other types of disease, origins of language and speech, nutrition, reproduction, growth and development, aging, primate origins, primate social behavior, brain biology, and many other topics dealing with variation in both the living and the dead— sometimes the very long dead (Figure 1.2)!

In dealing with such topics, physical anthropologists apply methods and theo- ries developed in other disciplines as well as in their own as they answer questions that help us understand who we are, a point that I will raise over and over again throughout this book. The very nature of their discipline and their constant borrowing from other disciplines mean that physical anthropologists practice an interdisciplinary science. For example, they might draw on the work of geologists who study the landforms and layering of deposits of soil and rock that tell us when earlier humans lived. Or they might obtain information from paleontologists, who study the evolution of life- forms in the distant past and thus provide the essential context for understanding the world in which earlier humans lived. Some physical anthropologists are trained in chemistry, so they can analyze the chemical properties of bones and teeth to determine what kinds of foods were eaten by those earlier humans. Or to learn how living humans adapt to reduced- oxygen settings, such as in the high altitudes of the Peruvian Andes Mountains, physical anthropologists might work with physiologists who study the lungs’ ability to absorb oxygen. The firm yet flexible identity of their science allows physical anthropologists to gather data from other disciplines in order to address key questions. Questions drive what they do.

What Makes Humans So Different from Other Animals?: The Six Steps to Humanness Human beings clearly differ from other animals. From humanity’s earliest origin— about 6–8 mya, when an apelike primate began walking on two feet— to the period beginning about 10,000 years ago, when modern climates and environments emerged following what is commonly known as the Ice Age, six key attributes developed that make us unique. These attributes are bipedalism, nonhoning chewing, complex material culture and tool use, hunting, speech, and dependence on domesticated foods (Figure 1.3, pp. 10–11). The first development represents

FIGURE 1.2 A Sample of What Physical Anthropologists Do (a) Human remains excavated at Bactia Pozzeveri, a medieval church cemetery in Tuscany, Italy, provide a window onto health and living conditions in Europe. (b) Geneticists analyze samples of human DNA for various anthropological purposes. DNA studies are used to determine how closely related humans are to other primate species, to examine human origins, and to determine individual identities. (c) A human biologist records the physical activities of a lactating woman (right, weaving basket) living in a rural community in the eastern Amazon, Brazil. These data will be used to calculate the woman’s energy expenditure and to understand how she copes with reproduction’s great energy demands. (d) In a lab, a forensic anthropologist measures and assesses human bones. If the bones came from a contemporary grave, this forensic information might help to identify the victim. If the bones belonged to a past population, physical anthropologists might use these data to gain insight into the population’s health and lifestyle. (e) Laboratory investigations of human ancestors’ bones help paleoanthropologists to determine where these ancestors fit in the human family tree. (f) Primatologists, such as the British researcher Jane Goodall (b. 1934), study our closest living relatives, nonhuman primates. The behavior and lifestyle of chimpanzees, for example, help physical anthropologists to understand our evolutionary past.

(c)

(a)

(e)

(b)

(d)

(f)

BIPEDALISM 6 MYA

The upright, bipedal (two-footed) gait was the first hallmark feature of our hominin ancestors.

SPEECH 2.5 MYA

In the entire animal kingdom, only humans can speak and, through speech, express complex thoughts and ideas. The shape of the hyoid bone is unique to hominins and reflects their ability to speak. Speech is part of the overall package in the human lineage of increased cognition, intelligence, and brain-size expansion.

HUNTING 1 MYA

Humans’ relatively large brains require lots of energy to develop and function. Animal protein is an ideal source of that energy, and humans obtained it for most of their evolution by eating animals they hunted. To increase their chances of success in hunting, humans employed tools they made and cooperative strategies.

NONHONING CHEWING 5.5 MYA

Humans’ nonhoning chewing complex (below) lacks large, projecting canines in the upper jaw and a diastema, or gap, between the lower canine and the third premolar.

The chewing complex of apes such as gorillas (below) has large, projecting upper canines and a diastema in the lower jaw to accommodate them.

MATERIAL CULTURE AND TOOLS 3.3 MYA

Humans’ production and use of stone tools is one example of complex material culture. The tools of our closest living relatives, the chimpanzees, do not approach the complexity and diversity of modern and ancestral humans’ tools

DOMESTICATED FOODS 11,000 YEARS AGO

In recent evolution—within the last 10,000 years or so—humans domesticated a wide variety of plants and animals, controlling their life cycles and using them for food and other products, such as clothing and shelter.

Human Ape Diastema

Hyoid bone

F I G U R E

1.3 The Six Big Events of Human Evolution: Bipedalism, Nonhoning Chewing, Dependence on Material Culture, Speech, Hunting, and Domestication of Plants and Animals

BIPEDALISM 6 MYA

The upright, bipedal (two-footed) gait was the first hallmark feature of our hominin ancestors.

SPEECH 2.5 MYA

In the entire animal kingdom, only humans can speak and, through speech, express complex thoughts and ideas. The shape of the hyoid bone is unique to hominins and reflects their ability to speak. Speech is part of the overall package in the human lineage of increased cognition, intelligence, and brain-size expansion.

HUNTING 1 MYA

Humans’ relatively large brains require lots of energy to develop and function. Animal protein is an ideal source of that energy, and humans obtained it for most of their evolution by eating animals they hunted. To increase their chances of success in hunting, humans employed tools they made and cooperative strategies.

NONHONING CHEWING 5.5 MYA

Humans’ nonhoning chewing complex (below) lacks large, projecting canines in the upper jaw and a diastema, or gap, between the lower canine and the third premolar.

The chewing complex of apes such as gorillas (below) has large, projecting upper canines and a diastema in the lower jaw to accommodate them.

MATERIAL CULTURE AND TOOLS 3.3 MYA

Humans’ production and use of stone tools is one example of complex material culture. The tools of our closest living relatives, the chimpanzees, do not approach the complexity and diversity of modern and ancestral humans’ tools

DOMESTICATED FOODS 11,000 YEARS AGO

In recent evolution—within the last 10,000 years or so—humans domesticated a wide variety of plants and animals, controlling their life cycles and using them for food and other products, such as clothing and shelter.

Human Ape Diastema

Hyoid bone

12 | CHAPTER 1 What Is Physical Anthropology?

the most profound physical difference between humans and other animals, namely the manner in which we get around: we are committed to bipedalism, that is, walking on two feet. The next development was the loss of a large, honing canine tooth, like the one that apes typically use to shred their food (mostly plants), to the simple nonhoning canine, with which we simply process food. Our ancestors’ honing canine disappeared because they developed the ability to make and use tools for processing food.

Today, our species completely depends on culture— and especially material culture— for its day- to- day living and its very survival. Culture is a complex human characteristic that facilitates our survival by enabling us to adapt to different settings. Material culture is the part of culture that is expressed as objects that humans use to manipulate environments. For example, hammers and nails are forms of material culture that enable us to make cabinets, tables, and countless other forms of material culture. The material remains of past cultures go back hundreds of thousands of years, to the first simple tools made from rocks 3.3 mya (Figure 1.4). Material culture today makes our lifestyles possible. Can you imag- ine your life without it? We could survive without modern additions to material culture, such as cars, computers, TVs, plumbing, and electricity, as our ancestors did before the last century. What about living without basic material culture, such as shelter and clothing, especially in climates where it can be very, very cold in the winter? Without material culture, how would any of us get food? The answer to both questions is simple: we could not make it without some forms of technology— to regulate temperature, to acquire food, and so on. Some societies are much less technologically complex than others, but no society functions with- out any technology.

Anthropologists and animal behaviorists have shown that human beings are not, however, the only type of animal that has or can employ material culture. Primatologists have observed some chimpanzee societies in Africa, for example, making simple tools from twigs (Figure  1.5). In laboratories, chimpanzees have been taught to use physical symbols that approximate human communication. Still, these and other forms of material culture used by nonhuman species are nowhere near as complex as those created by humans.

The other three key attributes of humanness— hunting, speech, and depen- dence on domesticated foods— appeared much later in human evolution than bipedalism, nonhoning chewing, and complex material culture and tool use. Hunting here refers to the social behavior whereby a group, adult men in general, organize themselves to pursue animals for food. This behavior likely dates back to a million or more years ago. Some nonhuman primates organize to pursue prey, but they do not use tools or travel long distances as humans distinctively do when they hunt.

An equally distinctive human behavior is speech. We are the only animal that communicates by talking. Unfortunately for research purposes, recording- and- listening technology was invented only about a century ago. For information about long- past speech, anthropologists rely on indirect evidence within the skeleton. For example, the hyoid bone, in the neck, is part of the vocal structure that helps produce words. The unique appearance of the human hyoid helps anthropologists conjecture about the origins of speech.

The most recently developed unique human behavior is the domesticated manner in which we acquire our food. About 10,000–11,000 years before the pres- ent (yBP), humans began to raise animals and grow plants. This development led

bipedalism Walking on two feet.

nonhoning canine An upper canine that, as part of a nonhoning chewing mechanism, is not sharpened against the lower third premolar.

material culture The part of culture that is expressed as objects that humans use to manipulate environments.

FIGURE 1.4 First Tools The earliest stone tools date to 3.3 mya and are associated with early human ancestors in East Africa. The example shown here is from Lomekwi, West Turkana, Kenya. This tool had various functions, including the processing of plants and meat for food.

What Makes Humans So Different from Other Animals?: The Six Steps to Humanness | 13

to our current reliance on domesticated species. This reliance has had a profound impact on human biology and behavior and represents a pivotal step in human evolution.

Human beings’ unique behaviors and survival mechanisms, and the anatomical features related to them, arose through the complex interaction of biology and culture. Indeed, our ancestors’ increasing dependence on culture for survival has made us entirely culture- dependent for survival. The behaviors that are unique to humans— speech, tool use, and dependence on culture— are also related to the fact that humans are very smart. Our remarkable intelligence is reflected in our abilities to think and interact in the ways we do (and take for granted), to communicate in complex ways, and to accomplish diverse tasks on a daily basis to survive. Our brains are bigger and have more complex analytical skills than do the brains of both other primates and animals in general. These biological advantages enable us to figure out complex problems, including how to survive in a wide range of environments.

The American anthropologist Robert Boyd and his colleagues argue that while humans are the smartest animals, in no way are we individually smart enough to acquire all the complex information necessary to survive in any particular envi- ronment. Today and through much of human evolution, our species has survived owing to our complex culture, including tool use and technology generally, prac- tices, and beliefs. For hundreds of thousands of years, humans have had a record of unique ways of learning from other humans. Retaining new knowledge, we pass this information to our offspring and other members of our societies, and this pro- cess extends over many generations. That is, social learning makes it possible for humans to accumulate an amazing amount of information over long time periods.

In the following chapters, you will be looking at these processes and behaviors— the particulars of physical anthropology— from a biocultural perspective. It is the unique and phenomenal interplay between biology, culture, and behavior that makes us human.

FIGURE 1.5 Tool- Making Once thought to be a uniquely human phenomenon, tool- making has been observed in chimpanzees, the closest biological relatives of humans. As seen here, chimpanzees have modified twigs to scoop termites from nests. Other chimpanzees have used two rocks as a hammer and anvil to crack open nuts. More recently, gorillas were seen using a stick to test the depth of a pool of water they wanted to cross. Tool use such as this likely preceded the first identified tools (see Figure 1.4).

social learning The capacity to learn from other humans, enabling the accu- mulation of knowledge across many generations.

14 | CHAPTER 1 What Is Physical Anthropology?

How We Know What We Know: The Scientific Method How do physical anthropologists make decisions about what their subject matter means? More specifically, how do we know what we know about human evolution and human variation? Like all other scientists, physical anthropologists carefully and systematically observe and ask questions about the natural world around them. These observations and questions form the basis for identifying problems and gath- ering evidence— data— that will help answer questions and solve problems— that is, fill gaps in scientific knowledge about how the natural world operates. These data are used to test hypotheses, possible explanations for the processes under study. Scientists observe and then reject or accept these hypotheses. This process of determining whether ideas are right or wrong is called the scientific method (Figure 1.6). It is the foundation of science.

Science (Latin scientia, meaning “knowledge”), then, is more than just knowl- edge of facts about the natural world. Science is also much more than technical details. Certainly, facts and technical details are important in developing answers to questions, but facts and technical skills are not science. Rather, science is a process that provides new discoveries that connect our lives with the world we live in— it is a way of knowing through observation of natural phenomena. This repeated acquisition results in an ever- expanding knowledge base, one built from measurable, repeatable, and highly tangible observations. In this way, science is empirical, or based on observation or experiment. After the systematic collection of observations, the scientist develops a theory— an explanation as to why a natural phenomenon takes place. For many nonscientists, a theory is simply a guess or a hunch; but for a scientist, a theory is not just some stab at an explanation. Rather, a theory is an explanation grounded in a great deal of evidence, or what a lawyer calls the “evidentiary record.” A scientist builds a case by identifying incontrovertible facts. To arrive at these facts, the scientist examines and reexamines the evidence, putting it through many tests.

The scientist thus employs observation, documentation, and testing to gener- ate hypotheses and, eventually, to construct a theory based on those hypotheses. Hypotheses explain observations, predict the results of future investigation, and can be refuted by new evidence.

data Evidence gathered to help answer questions, solve problems, and fill gaps in scientific knowledge.

hypotheses Testable statements that potentially explain specific phenomena observed in the natural world.

scientific method An empirical research method in which data are gathered from observations of phenomena, hypotheses are formulated and tested, and conclu- sions are drawn that validate or modify the original hypotheses.

empirical Verified through observation and experiment.

theory A set of hypotheses that have been rigorously tested and validated, leading to their establishment as a gen- erally accepted explanation of specific phenomena.

Observations

Hypothesis supported Hypothesis rejected

Hypothesis

Predictions (“If... then...”)

Test (observations, experiments)

Further tests

New or revised

hypothesis

FIGURE 1.6 The Scientific Method: How We Know What We Know

How We Know What We Know: The Scientific Method | 15

For example, the great English naturalist Charles Robert Darwin (1809–1882) (Figure  1.7) developed the hypothesis that the origin of human bipedalism was linked to the shift from life in the trees to life on the ground (Figure 1.8). Darwin’s hypothesis was based on his own observations of humans walking, other scientists’ then- limited observations of nonhuman primate behavior, and other scientists’ anatomical evidence, or information (about structural makeup) drawn from dis- sections, in this case of apes. Darwin’s hypothesis led to an additional hypothesis, based on evidence that accumulated over the following century and a half, that the first hominins arose in the open grasslands of Africa from some apelike animal that was formerly arboreal— that is, had once lived in trees.

Support for Darwin’s hypothesis about human origins— and in particular the origin of bipedal locomotion— began to erode in 2001, when a group of scientists discovered early hominins, from 5.2 to 5.8 mya, in the modern country of Ethiopia. Contrary to expectation and accepted wisdom, these hominins had lived not in grasslands but in woodlands. Moreover, unlike modern humans, whose fingers and toes are straight because we are fully terrestrial— we live on the ground—the early hominins had slightly curved fingers and toes. The physical shape and appearance, what physical anthropologists call morphology, of the hominins’ finger and toe bones indicate a lot of time spent in trees, holding on to branches, moving from limb to limb. These findings forced scientists to reject Darwin’s hypothesis, to toss out what had been a fundamental tenet of physical anthropology.

This story does not end, however, with the understanding that the earliest hominins lived in forests. Instead, this new hypothesis generated new questions. For example, why did the earliest hominins arise in a wooded setting, and why did they “come out of the woods” as time went on? Later in this book, we will consider these questions. For now, the point is that science is a self- correcting approach to knowledge acquisition. Scientists develop new hypotheses as new findings are made. Scientists use these hypotheses to build theories. And like the hypotheses that underlie them, theories can be modified or even replaced by better theories, depending on findings made through meticulous observation. As new observations are made and hypotheses and theories are subjected to the test of time, science revises its own errors.

A scientific law is a statement of irrefutable truth of some action or actions occurring in the natural world. Among the few scientific laws, the well- known ones are the laws of gravity, thermodynamics, and motion. But scientific truth seldom gets finalized into law. Rather, truth is continuously developed— new facts are discovered and new understandings about natural phenomena are made. Unlike theories, scientific laws do not address the larger questions as to why a natural action or actions take place.

FIGURE 1.7 Charles Darwin George Richmond painted this portrait of Darwin in 1840.

anatomical Pertaining to an organism’s physical structure.

arboreal Tree- dwelling, adapted to living in the trees.

terrestrial Life- forms, including humans, that live on land versus living in water or in trees.

morphology Physical shape and appearance.

scientific law A statement of fact describ- ing natural phenomena.

FIGURE 1.8 Bipedalism These 1887 photographs by Eadweard Muybridge capture humans’ habitual upright stance. Other animals, such as chimpanzees, occasionally walk on two feet; but humans alone make bipedalism their main form of locomotion. As Darwin observed, this stance frees the hands to hold objects. What are some other advantages of bipedalism?

16

As my crew and I traveled to St. Catherines Island, we were intent on discovering new facts and forming new understandings about the prehistoric farmers’ descen- dants who were first encountered by Spaniards in the late 1500s. These facts and understandings would enable us to test hypotheses about human evolution and human variation. Once we completed the months of arduous fieldwork and the years of laboratory investigations on the remains that fieldwork uncovered, we would have some answers. The scientific method would guide us in provid- ing insights into this part of the human lineage— human beings’ most recent evolution— and how our species came to be what it is in the early twenty- first century.

C H A P T E R   1 R E V I E W

A N S W E R I N G T H E B I G Q U E S T I O N S

What is anthropology? • Anthropology is the study of humankind. In two

major ways, it differs from other sciences that study humankind. First, anthropology views humans as both biological and cultural beings. Second, anthropology emphasizes a holistic, comparative approach, encompassing all people at all times and all places.

• The four branches of anthropology are cultural anthropology (study of living cultures), archaeology (study of past cultures), linguistic anthropology (study of language), and physical anthropology.

What is physical anthropology? • Physical (or biological) anthropology is the study

of human biology, specifically of the evolution and variation of humans (and their relatives, past and present).

• Physical anthropology is an eclectic field, deriving theory and method both from within the discipline and from other sciences that address important questions about human evolution and human variation.

What makes us human and different from other animals? • Humans living today are the product of millions of

years of evolutionary history and their own personal life histories.

• Humans have six unique physical and behavioral characteristics: bipedalism, nonhoning chewing, complex material culture and tool use, hunting, speech, and dependence on domesticated foods.

How do physical anthropologists know what they know? • Physical anthropologists derive knowledge via the

scientific method. This method involves observations, the development of questions, and the answering of those questions. Scientists formulate and test hypotheses that they hope will lead to theories about the natural world.

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REVIEW THIS CHAPTER WITH PERSONALIZED, INTERACTIVE QUESTIONS THROUGH IJK, INQUIZITIVE.WWNORTON.COM q

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K E Y T E R M S anatomical anthropology arboreal archaeology artifacts biocultural approach biological anthropology bipedalism cultural anthropology culture

data empirical forensic anthropology genome hominin hypotheses language linguistic anthropology material culture morphology

nonhoning canine physical anthropology primates scientific law scientific method social learning sociolinguistics terrestrial theory

E V O L U T I O N R E V I E W Physical Anthropology as Science

Synopsis Anthropology is a holistic discipline in that it views humankind from the perspectives of all people and all times. Anthropology is also an interdisciplinary science in that it both draws on and influences research in many related fields. Physi- cal anthropology is one of the four subfields (along with cultural anthropology, archaeology, and linguistic anthropology) that make up anthropology as both a biological and a social science. The two main concepts that define physical anthropology are human biological evo- lution and human biocultural variation. Through the employment of the scientific method, physical anthropologists study many different aspects of living humans, modern and extinct nonhuman primates, and fossil hominins, among other lines of research. Through all of these different ways of gathering knowledge about the human con- dition, physical anthropologists ultimately address research questions related to the two broad themes of evolution and variation.

Q1. Define the biocultural approach—a hallmark of physical anthropology.

Q2. Focusing on Figure 1.3, The Six Big Events of Human Evolution, identify which two of these events were caused primarily by biological changes in humans and which four were caused by changes in both human biology and human culture.

Q3. Over time, has culture had more or less of an effect on human evolution? Focusing on Figure 1.3, briefly explain your answer.

Q4 . As a species, humans are unique in the degree to which culture influences our evolution. Consider Figure 1.3 again. How might aspects of human culture have affected the evolution of other species, such as livestock or wild animals?

Q5. Many nonscientists often critique evolution as “just a theory.” What does it mean for evolution to be a theory in the context of the scientific method? How does the study of evolution illustrate the interdisciplinary nature of physical anthropology?

Hint What other scientific fields might contribute data that are used to test hypotheses related to biological evolution?

A D D I T I O N A L R E A D I N G S

Larsen, C. S., ed. 2010. A Companion to Biological Anthropology. Chichester, UK: Wiley- Blackwell.

Molnar,  S.  2005. Human Variation: Races, Types, and Ethnic Groups. Upper Saddle River, NJ: Prentice Hall.

Moore, J. A. 1999. Science as a Way of Knowing: The Foundations of Modern Biology. Cambridge, MA: Harvard University Press.

Spencer,  F., ed. 1997. History of Physical Anthropology: An Ency- clopedia. New York: Garland.

Stocking,  G., ed. 1974. The Shaping of American Anthropology, 1883–1911: A Franz Boas Reader. New York: Basic Books.

Some Periodicals in Anthropology

Physical anthropology: American Journal of Human Biology, Amer- ican Journal of Physical Anthropology, American Journal of Prima- tology, Evolutionary Anthropology, Human Biology, International

Journal of Paleopathology, Journal of Human Evolution, Yearbook of Physical Anthropology.

Archaeology: American Antiquity, Antiquity, Archaeology, Journal of Archaeological Science, Latin American Antiquity, World Archaeology.

Cultural anthropology: American Anthropologist, Cultural Anthro pology.

General anthropology: American Anthropologist, Annual Review of Anthropology, Current Anthropology.

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A D D I T I O N A L R E A D I N G S

19

The Present: Foundation for the Past

Some physical anthropologists learn about human evolution by studying living plants and animals, including humans. Other physical anthropologists learn about human evolution by investigating the past, now represented mostly by fossilized bones and fossilized teeth. Together, living and past enable us to understand evolution in the largest context. The fossil record provides us with the history of humans and of humanlike ancestors, while the living record provides the essential picture through which to view that history. Charles Darwin, the pioneering force behind our knowledge about evolution and natural selection, developed his ideas by studying living plants and animals. He had the extraordinary insight to realize that his

theories and hypotheses applied to past organisms. For Darwin, living organisms were key to interpreting the past because they displayed evidence of evolution’s elements and mechanics. In the same way, living organisms pro- vide insights— into fundamental forces such as reproduc- tion, DNA synthesis, protein synthesis, and behavior— that are not available, at least in the same way, within the past record. Part I of this book lays out observations and princi- ples based on the study of living populations, the essential background for understanding evolution. Part II then digs into the past, into the study of ancestors whose descen- dants are present in the world (all of us now living) and of those evolutionary lineages that did not survive.

The living primates— such as, here, orangutans and humans— have much in common, biological and behavioral. Their study provides essential context for understanding variation and evolution, now and in the past.

P A R T I

CHARLES DARWIN’S OBSERVATIONS provided the groundwork for his theory of natural selection, the basis of his 1859 book On the Origin of Species.

21 21

2 How did the theory of evolution come to be?

What was Darwin’s contribution to the theory of evolution?

What has happened since Darwin in the development of our understanding of evolution?

Evolution Constructing a Fundamental Scientific Theory

T he nineteenth century was the century of scientific collecting. During the 1800s, the world discovered itself through collections. Expeditions large and small— involving scientists, explorers, and adventurers— crossed the continents and investigated landmasses around the globe. These teams collected hundreds of thou- sands of samples: plants, animals, rocks, and preserved remains (or fossils— the sub- ject of chapter 8). If it seemed worth picking off the ground or exposing in some other fashion, it was fair game. This kind of work, on one of these international expeditions, helped lay the foundation for the most important biological theory, arguably among the half- dozen most important scientific theories— the theory of evolution.

In 1831, a 22- year- old Englishman and recent graduate of Cambridge University, Charles Darwin, was appointed the naturalist for a five- year voyage around the world on the ship HMS Beagle (Figure 2.1). Imagine that as your first job right out of col- lege! Young Mr. Darwin, who was trained in medicine and theology, accepted a difficult task. He was to collect, document, and study the natural world— plants and animals, especially— everywhere the ship harbored. By the end of that voyage, Darwin had amassed a wonderfully comprehensive collection of plants, insects, birds, shells, fossils, and lots of other materials. The specimens he collected and the observations he made about the things he saw on that trip would form the basis of his lifetime of research. His discoveries would do no less than shape the future of the biological sciences, including physical anthropology. His ideas would provide the key to understanding the origin and evolution of life itself.

Soon after returning home from the voyage, Darwin began to formulate questions about the origins of plants and animals living in the many lands he and his shipmates

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fossils Physical remains of part or all of once- living organisms, mostly bones and teeth, that have become mineralized by the replacement of organic with inorganic materials.

22 | CHAPTER 2 Evolution: Constructing a Fundamental Scientific Theory

had explored. His most prominent observations concerned the physical differences, or variation, between and among members of species, or like animals and like plants. He articulated the phenomenon best in his notes on finches that live in the Galápagos, a small cluster of islands 965 km (600 mi) off the coast of Ecuador. Not only did these birds differ from island to island, but even within a single island they seemed to vary according to habitat, or surroundings. For example, finches living on an island’s coast had a different beak shape from finches living in an island’s inte- rior (Figure 2.2). These observations raised two questions for Darwin: Why were the birds different from island to island and from habitat to habitat? How did differ- ent species of finches arise? After years of study, Darwin answered these questions with an idea called “descent with modification,” or the theory of evolution.

Darwin also came to realize that the variations in physical characteristics of the different species of finches and other organisms were adaptations— physical characteristics that enhance an organism’s ability to survive and reproduce. Dar- win recognized many other adaptations in the natural world, and he concluded that adaptation was the crux of evolution. To connect these processes, he coined the term natural selection. According to this principle, biological characteristics that enhance survival increase in frequency from generation to generation. Members of a population endowed with these characteristics produce more offspring that survive to reproductive age than members that are not endowed with these characteristics. Natural selection is thus the primary driver of evolution. Recognizing that the differ- ent species of finches all derived from a single common ancestor that had originated in South America, Darwin also postulated the process of adaptive radiation: out of one species branch multiple closely related species.

FIGURE 2.1 Darwin’s Voyage (a) Charles Darwin ca. 1855, about 25 years after he set out on HMS Beagle. (b) In this illustration, the ship is passing through the Strait of Magellan, during the South American stretch of (c) its worldwide journey, whose ports of call are here mapped.

(a)

(b)

Galápagos Islands

Western Islands Canary

Islands

Marquesas

Cape Horn

Strait of Magellan

Madagascar Bay of Islands

N O R T H A M E R I C A

B R I T I S H I S L E S

E U R O P E

A F R I C A

A U S T R A L I A

A S I A

S O U T H A M E R I C A

P A C I F I C O C E A N

K I N G G E O R G E ’ S S O U N D

AT L A N T I C O C E A N

Rio de Janeiro

Bahia

Falkland Islands

Montevideo Valparaiso

Hobart

SydneyCape of Good Hope

(c)

species A group of related organisms that can interbreed and produce fertile, viable offspring.

habitat The specific area of the natural environment in which an organism lives.

adaptations Changes in physical struc- ture, function, or behavior that allow an organism or species to survive and repro- duce in a given environment.

natural selection The process by which some organisms, with features that enable them to adapt to the environment, preferentially survive and reproduce, thereby increasing the frequency of those features in the population.

adaptive radiation The diversification of an ancestral group of organisms into new forms that are adapted to specific environmental niches.

The Theory of Evolution: The Context for Darwin | 23

Darwin regarded evolution as simply biological change from generation to gener- ation. Many evolutionary biologists today limit their definition of evolution to genetic change only. However, nongenetic developmental change— biological change occurring within an individual’s lifetime— can give an adaptive advantage (or disad- vantage) to an individual or individuals within a population. Moreover, genes control developmental processes, which likewise influence other genes.

In subsequent chapters, we will further explore these and other aspects of evolu- tion. Although the core of this book is human evolution or how human biology came to be, understanding human evolution requires understanding the term evolution as it applies to all living organisms. In this chapter, we will take a historical approach to the term and the theory behind it. After reading about its intellectual history before Darwin, Darwin’s contribution, and developments since Darwin, you should have a clear idea of what physical anthropologists and other evolutionary biologists mean by evolution.

The Theory of Evolution: The Context for Darwin Before Darwin’s time, Western scientists’ understanding of Earth and the organ- isms that inhabit it was strongly influenced by religious doctrine. In the Judeo- Christian view, the planet was relatively young, and both its surface and the life- forms on it had not changed since their miraculous creation. By the late 1700s, scientists had realized three key things about the world and its inhabitants: Earth is quite ancient, its surface is very different from what it was in the past, and plants

FIGURE 2.2 Darwin’s Finches Darwin studied the physical variation in finches living on different islands of the Galápagos. Among other attributes, he studied beak shape, which varied from island to island. Eventually, Darwin related each beak shape to diet, especially to the texture of food and how the food was acquired. Finches with larger beaks typically consumed harder foods, such as seeds and nuts, while finches with smaller beaks ate softer foods, such as berries. Darwin concluded that each finch species had adapted to the particular environment and food resources of its island.

24 | CHAPTER 2 Evolution: Constructing a Fundamental Scientific Theory

and animals have changed over time. These realizations about the natural world provided the context for Darwin’s theory of evolution.

To generate his theory, Darwin drew on information from five scientific dis- ciplines: geology, paleontology, taxonomy and systematics, demography, and what is now called evolutionary biology. Geology is the study of Earth, especially with regard to its composition, activity, and history. This discipline has demonstrated the great age of our planet and the development of its landscape. Paleontology is the study of fossils. This discipline has detailed past life- forms, many now extinct. Taxonomy is the classification of past and living life- forms. This disci- pline laid the foundation for systematics, the study of biological relationships over time. Demography is the study of population, especially with regard to birth, survival, and death and the major factors that influence these three key parts of life. Evolutionary biology is the study of organisms and their changes. By investigating the fundamental principles by which evolution operates, Darwin founded this  discipline. In the following sections, we will look at these fields in more detail.

GEOLOGY: RECONSTRUCTING EARTH’S DYNAMIC HISTORY We now know that our planet is 4.6 billion years old and that over time its surface has changed dramatically. If you had espoused these ideas in, say, the late 1600s, you would not have been believed, and you would have been condemned by the Church because you had contradicted the Bible. According to a literal interpre- tation of the Bible, Earth is a few thousand years old and its surface is static. The Scottish scientist James Hutton (1726–1797) became dissatisfied with the biblical interpretation of the planet’s history (Figure 2.3). He devoted his life to studying natural forces, such as wind and rain, and how they affected the landscape in Scotland. Hutton inferred from his observations that these forces changed Earth’s surface in the past just as they do in the present. Wind and rain created erosion, which provided the raw materials— sand, rock, and soil— for the formation of new land surfaces. Over time, these surfaces became stacked one on top of the other, forming layers, or strata, of geologic deposits (Figure  2.4). From the (very long) time it took for these strata to build up, he calculated Earth’s age in the millions of years. This was a revolutionary, indeed heretical, realization.

FIGURE 2.3 James Hutton Hutton (here depicted ca. 1790) founded modern geology with his theory of Earth’s formation. Hutton realized that the same natural processes he observed in Scotland had occurred in the past.

geology The study of Earth’s physical history.

paleontology The study of extinct life- forms through the analysis of fossils.

taxonomy The classification of organisms into a system that reflects degree of relatedness.

systematics The study and classification of living organisms to determine their evo- lutionary relationships with one another.

demography The study of a population’s features and vital statistics, including birth rate, death rate, population size, and population density.

evolutionary biology A specialty within the field of biology; the study of the process of change in organisms.

FIGURE 2.4 Geologic Strata The succession of strata from oldest at the bottom to youngest at the top (as here, in Utah’s Bryce Canyon) marks the formation of new land surfaces over time.

The Theory of Evolution: The Context for Darwin | 25

Hutton’s idea— that the natural processes operating today are the same as the natural processes that operated in the past— is called uniformitarianism. Few paid much attention to Hutton’s important contribution to our understanding of Earth’s history until the rediscovery of the idea by the Scottish geologist Charles Lyell (1797–1875; Figure  2.5). Lyell devoted considerable energy to thinking and writing about uniformitarianism and its implications for explaining the history of our planet. His calculations of how long it would have taken for all known strata to build up created a mountain of evidence, an undeniable record, that Earth was millions of years old. Hutton and Lyell, relying on empirical evidence and personal observation to develop their ideas and to test clear hypotheses about the natural world, had revised the timescale for the study of past life.

PALEONTOLOGY: RECONSTRUCTING THE HISTORY OF LIFE ON EARTH For hundreds of years, people have been finding the preserved— that is, fossilized— remains of organisms all over the world (see also the full discussion in chapter 8). To test his hypothesis that fossils are the remains of past life, the English scientist Robert Hooke (1635–1703) studied the microscopic structure of fossil wood. After observing that the tissue structure of the fossil wood was identical to the tissue structure of living trees, Hooke concluded that the fossil wood derived from once- living trees (Figure 2.6).

Fossils’ potential to illuminate the past was demonstrated by the French nat- uralist and zoologist Georges Cuvier (1769–1832). Cuvier devoted considerable effort to learning the anatomy, or structural makeup, of many kinds of animals (Figure  2.7). Pioneering what we now call paleontology and comparative anat- omy,  he applied his extensive knowledge of comparative anatomy to fossils. By doing so, he reconstructed the physical characteristics of past animals— their appearance, physiology, and behavior. Although not very accurate by today’s standards, these efforts provided early tools for understanding past life- forms as once- living organisms. Through detailed reconstructions, Cuvier demonstrated

FIGURE 2.5 Charles Lyell Lyell (here depicted ca. 1845) rediscovered Hutton’s work and the idea of uniformitarianism. Lyell’s research, based on examinations of geologic strata, confirmed Hutton’s estimate of Earth’s very old age.

uniformitarianism The theory that pro- cesses that occurred in the geologic past are still at work today.

FIGURE 2.6 Robert Hooke (a) Hooke did pioneering biological research using a very simple microscope. He was the first to identify cells; in fact, he coined the term cell. (b) This illustration of cork wood cells appeared in Hooke’s Micrographia (1667), the first major book on microscopy. His examinations of cells like this enabled Hooke to determine that fossils represented past life- forms.(a) (b)

26 | CHAPTER 2 Evolution: Constructing a Fundamental Scientific Theory

that fossils found in geologic strata in France were the remains of animals that had gone extinct at some point in the remote past. Cuvier’s work provided the first basic understanding of the history of life, from the earliest forms to recent ones.

Cuvier observed that each stratum seemed to contain a unique set of fos- sils.  What happened to the animals represented by each set, each layer? Cuvier concluded that they must have gone extinct due to some powerful catastrophe, such as an earthquake or a volcanic eruption. He surmised that following each catastrophe, the region was vacant of all life and was subsequently repopulated by a different group of animals moving into it from elsewhere. This perspective is called catastrophism.

We now know that Earth’s history does not consist of sequential catastrophes and resulting extinctions. Past catastrophes, such as the extinction of the dinosaurs at around 65 mya, have profoundly affected the direction of evolution, but they were not the leading factor in evolution.

However, such events are rare and do not explain even the sequence of fossils Cuvier observed, mostly in the region called the Paris Basin. In addition to con- firming that fossils were the remains of life in the distant past, though, Cuvier revealed that the most recent geologic strata contain mostly mammals and earlier geologic strata contain mostly reptiles, including the dinosaurs.

TAXONOMY AND SYSTEMATICS: CLASSIFYING LIVING ORGANISMS AND IDENTIFYING THEIR BIOLOGICAL RELATIONSHIPS In the pre- Darwinian world, most scientists who studied life- forms realized the importance of developing a taxonomy— a classification of life- forms— for identifying biological relationships. Early efforts at taxonomy took a commonsense approach. Animals were placed within major groups such as dogs, cats, horses, cattle, and people. Plants were placed within major groups such as trees, shrubs, vines, and weeds.

(b)(a)

FIGURE 2.7 Georges Cuvier (a) One of Cuvier’s most important contributions to science was the concept of extinction. Here, Cuvier is depicted examining a fish fossil. (b) In his 1796 paper on fossil and living elephants, Cuvier suggested that mammoth remains— such as those shown here, from one of his many publications— represented a species different from any living elephant species and, therefore, were from a species that had gone extinct. This idea was revolutionary because the common perception was that God had created all species, none of which had ever gone extinct.

catastrophism The doctrine asserting that cataclysmic events (such as volcanoes, earthquakes, and floods), rather than evolutionary processes, are responsible for geologic changes throughout Earth’s history.

The Theory of Evolution: The Context for Darwin | 27

As late as the seventeenth century, scientists generally believed that species were immutable. In their view, life had changed very little, or not at all, since the time of the single Creation. Thus, early taxonomists were not motivated by an interest in evolution. Rather, they were motivated by their desire to present the fullest and most accurate picture of the Creator’s intentions for His newly created world. To construct the best possible taxonomy, the English naturalist John Ray (1627–1705) advocated personal observation, careful description, and consideration of plants’ and animals’ many attributes. Ray’s attention to detail laid the

Pre- Darwinian Theory and Ideas: Groundwork for Evolution

Charles Darwin first presented his theory of evolution in his book On the Origin of Species (1859). Based on years of personal observation and of study, this unifying biological theory drew on geology, paleontology, taxonomy and systematics, and demography.

Scientist Contribution (and year of publication) Significance

James Hutton Calculated Earth’s age as millions of years (1788)

Provided geologic evidence necessary for calculating time span of evolution

Charles Lyell Rediscovered and reinforced Hutton’s ideas (1830)

Provided more geologic evidence

Robert Hooke Proved that fossils are organisms’ remains (1665)

Revealed that fossils would provide the history of past life

Georges Cuvier

Extensively studied fossils (1796)

Revealed much variation in the fossil record

John Ray Pioneered taxonomy based on physical appearance (1660)

Created the first scientific classification of plants and animals

Carolus Linnaeus

Wrote Systems of Nature (1735)

Presented the binomial nomenclature taxonomy of plants and animals

Thomas Malthus

Founded demography: only some will find enough food to survive (1798)

Provided the concept of characteristics advantageous for survival

Jean- Baptiste de Lamarck

Posited characteristics acquired via inheritance (Lamarckism) (1809)

Provided first serious model of physical traits’ passing from parents to offspring

Erasmus Darwin

Also posited characteristics (determined by wants and needs) acquired via inheritance (1794)

Advanced the notion that physical changes occurred in the past

C O N C E P T C H E C K !

28 | CHAPTER 2 Evolution: Constructing a Fundamental Scientific Theory

groundwork for later taxonomy, especially for the binomial nomenclature ( two- name) system developed by the Swedish naturalist Carl von Linné (1707–1778). Von Linné, better known by his Latinized name, Carolus Linnaeus, gave each plant and animal a higher- level genus (plural, genera) name and a lower- level species (plural is also species) name (Figure 2.8). A single genus could include one or more spe- cies. For example, when Linnaeus named human beings Homo sapiens— Homo being the genus, sapiens being the species— he thought there were species and subspecies of living humans (an idea discussed further in chapter  5). The presence of more than one level in his taxonomy acknowledged different degrees of physical simi- larity. Today, we recognize that sapiens is the one living species in the genus Homo.

Linnaeus presented the first version of his taxonomy in his book Systema Naturae (1735), or System of Nature. As he revised the taxonomy— his book would eventually go through 10 editions— he added more and more levels to the hierarchy. He clas- sified groups of genera into orders and groups of orders into classes. For example, he named the order “Primates,” the group of mammals that includes humans, apes, monkeys, and prosimians. Since the eighteenth century, this taxonomic system has evolved into multiple levels of classification, going from the subspecies at the bottom to the kingdom at the top (Figure 2.9).

Like Ray, Linnaeus was committed to the notion that life- forms were static, fixed at the time of the Creation. In later editions of his book, he hinted at the pos- sibility that some species may be related to each other because of common descent, but he never developed these ideas. His taxonomy is still used today, although viewed with a much stronger sense of present and past variation. The system’s flexibility aided evolutionary biologists in their study of biological diversity, and the focus on taxonomic relationships over time is now called systematics.

DEMOGRAPHY: INFLUENCES ON POPULATION SIZE AND COMPETITION FOR LIMITED RESOURCES After returning to England and while developing his ideas on natural selection, Darwin read the works of all the great scientists of the time. Probably the most important influence on his ideas was An Essay on the Principle of Population, by the English political economist Thomas Malthus (1766–1834). First published in 1798, Malthus’s book made the case that an abundance of food— enough to feed anyone born— would allow the human population to increase geometrically and indefinitely. In reality, the Essay argued, there simply is not enough food for every- one born, so population is limited by food supply (Figure 2.10). Who survives to reproductive age? Those who can successfully compete for food. Whose children thrive? Those of survivors who manage to feed their offspring. Applying Malthus’s demographic ideas to human and nonhuman animals, Darwin concluded that some members of any species successfully compete for food because they have some special attribute or attributes. That an individual characteristic could facilitate survival was a revelation!

EVOLUTIONARY BIOLOGY: EXPLAINING THE TRANSFORMATION OF EARLIER LIFE- FORMS INTO LATER LIFE- FORMS By the late 1700s, a handful of scientists had begun to argue that, contrary to religious doctrine, organisms are not fixed— they change over time, sometimes in dramatic ways. Simply, life evolved in the past and evolution is an ongoing,

genus A group of related species.

FIGURE 2.8 Carolus Linnaeus Linnaeus, a botanist, zoologist, and physician, is known for his contributions to the system of classification used today by all biological scientists, including physical anthropologists. He is also a founder of modern ecology.

FIGURE 2.10 Thomas Malthus Malthus, the founder of demography, theorized that population size was limited by food supply.

TAXONOMIC CATEGORY

Subfamily Homininae

Homo

sapiens

sapiens Modern humans alone.

Tribe Hominini

Genus

Species

Subspecies

TAXONOMIC LEVEL COMMON CHARACTERISTICS

Group of hominins including modern humans, their direct ancestors, and extinct relatives (e.g., Neandertals). They have the largest brains in the Hominini.

Modern and ancestral modern humans. They have culture, use language, and inhabit every continent except Antarctica.

Chimpanzees, humans, and humanlike ancestors

Family Hominidae Great apes, humans, and humanlike ancestors.

Superfamily Hominoidea Group of anthropoids, including humans, great apes, lesser apes, and humanlike ancestors. They have the largest bodies and brains of all primates.

Parvorder Catarrhini Group of anthropoids, including humans, apes, and Old World monkeys.

Infraorder Anthropoidea Group of haplorhines, including humans, apes, and monkeys.

Suborder

Order Primates

Haplorhini Group of primates, including monkeys, apes, humans, and tarsiers. They have in general long life cycles and are relatively large-bodied.

Group of mammals specialized for life in the trees, with large brains, stereoscopic vision, opposable thumbs, and grasping hands and feet.

Subclass Theria Group of mammals that produce live young without a shelled egg (including placental and marsupial mammals).

Class Mammalia Group of warm-blooded vertebrate animals that produce milk for their young in mammary glands. They have hair or fur and specialized teeth.

Superclass Tetrapoda Vertebrate animals with four feet or legs, including amphibians, birds, dinosaurs, and mammals.

Subphylum Vertebrata Animals with vertebral columns or backbones (including fish, amphibians, reptiles, birds, and mammals).

Phylum Chordata Group of vertebrate and invertebrate animals that have a notochord, which becomes the vertebral column in humans and other primates.

Subkingdom Eumetazoa All major animals (except sponges) that contain true tissue layers, organized as germ layers, which develop into organs in humans.

Kingdom Animalia Mobile multicellular organisms that consume other organims for food and develop during an embryo stage.

Commonly called “hominins,” this level includes humans and humanlike ancestors, all of which are obligate bipeds.

FIGURE 2.9 The Place of Humans in Linnaeus’s Taxonomy Linnaeus’s system organized living things into various levels of hierarchical classification. Kingdom, at the top of the taxonomy, is the largest classification. The five kingdoms of the natural world— animals, plants, fungi, protists, monera— include all living organisms. Through descending taxonomic levels, each group’s size gets progressively smaller. For example, there are fewer organisms in a genus than there are in a phylum. Additionally, these classifications reflect organisms’ relationships to one another. For example, organisms within a genus are more closely related than are those from different genera.

30 | CHAPTER 2 Evolution: Constructing a Fundamental Scientific Theory

undirected process. Building on this concept, the French naturalist Jean- Baptiste de Monet (1744–1829), better known by his title, Chevalier de Lamarck, speculated that plants and animals not only change in form over time but do so for purposes of self- improvement. Lamarck believed that in response to new demands or needs, life- forms develop new anatomical modifications, such as new organs. His central idea— that when life- forms reproduce, they pass on to their offspring the modifications they have acquired to that point— is called Lamarckian inheritance of acquired characteristics, or Lamarckism (Figure  2.11). We now know Lamarck’s mechanism for evolution to be wrong— offspring do not inherit traits acquired by their parents— but his work was the first major attempt to develop a theory built on the premise that living organisms arose from precursor species. Lamarck was also convinced that humans evolved from some apelike animal.

Among the other scholars who believed that life had changed over time was the English physician, naturalist, and poet Erasmus Darwin (1731–1802), grandfather of Charles Darwin. Like Lamarck, he hypothesized about the inheritance of char- acteristics acquired thanks to wants and needs; but he, too, was wrong about the mechanism for change.

Lamarckism First proposed by Lamarck, the theory of evolution through the inheritance of acquired characteristics in which an organism can pass on features acquired during its lifetime.

Darwin Borrows from Malthus

Five of Malthus’s observations inspired Darwin’s principle of natural selection.

Observation 1 For most organisms, every pair of parents produces multiple (sometimes many) offspring.

Observation 2 For most organisms, the population size remains the same. No increase occurs over time.

Observation 3 Population is limited by the food supply.

Observation 4 Members of populations compete for access to food.

Observation 5 No two members of a species are alike in their physical attributes— variation exists.

Theory: Evolution by Means of Natural Selection Individuals having variation that is advantageous for survival to reproductive age produce more offspring (and more offspring that survive) than individuals lacking this variation.

C O N C E P T C H E C K !

The Theory of Evolution: Darwin’s Contribution | 31

The Theory of Evolution: Darwin’s Contribution Darwin’s remarkable attention to detail enabled him to connect his voluminous reading with his personal observations from the Beagle voyage. For example, while in Chile, Darwin had observed firsthand the power of earthquakes in shaping the

(a)

Original short-necked ancestor.

Descendants keep stretching to reach leaves higher up on tree …

… and stretching until neck becomes progressively longer in descendants.

… and stretching …

(b)

FIGURE 2.11 Jean- Baptiste Lamarck (a) Lamarck developed an early theory of evolution involving the inheritance of acquired characteristics. Although his mechanism of evolution was wrong, Lamarck’s recognition of the dynamic nature of life in the past made an important contribution to the development of evolutionary theory. (b) According to the classic (though incorrect) example of Lamarckism, giraffes stretched to reach food at the tops of trees, their necks grew as a result, and they passed on these long necks to their offspring.

32 | CHAPTER 2 Evolution: Constructing a Fundamental Scientific Theory

landscape. Hutton’s and Lyell’s uniformitarianism led him to recognize that the accumulation of such catastrophes over a long period of time explains, at least in part, the appearance of the present- day landscape. This understanding of Earth’s remarkably dynamic geologic history laid the groundwork for Darwin’s view of evolution as a long, gradual process.

That process, he saw, could be reconstructed through the fossil record. He had read carefully Cuvier’s studies of fossils, and in South America he saw fossils first- hand. Some of these fossils resembled living animals native to South America, such as the armadillo, ground sloth, and llama. This evidence strongly suggested that an earlier species had transformed into the modern species, most likely through a succession of species over time. Drawing on Malthus’s ideas about reproduction, population, and variation, Darwin wrote, “it at once struck me that under these circumstances [i.e., specific environmental conditions] favorable variations would

(a)

(b)

FIGURE 2.12 Writing a Masterpiece (a) Darwin wrote most of On the Origin of Species at his beloved home, Down House, in Kent, England. (b) He generally worked in his study there.

Since Darwin: Mechanisms of Inheritance, the Evolutionary Synthesis, and the Discovery of DNA | 33

tend to be preserved and unfavorable ones to be destroyed. The result of this would be the formation of new species.” Another revelation.

Darwin hypothesized that surviving offspring had attributes advantageous for acquiring food. Because these offspring survived, the frequency of their advanta- geous characteristics increased over time. Meanwhile, as environmental conditions changed— such as when rainfall decreased— offspring lacking adaptive attributes suited to their survival in the new environment died off. Building on these obser- vations and their implications, Darwin deduced that natural selection was the primary mechanism of evolution. Over a long period of time, through generations’ adaptation to different environments and different foods, a common ancestor gave rise to related species. Darwin’s hypothesis was revolutionary, undermining the mid- nineteenth- century consensus that species were fixed types in a defined natural order of life. Now, species would have to be considered as populations with no predetermined limit on variation.

Darwin’s background research had begun in the 1830s. It was not until 1856, however— fully two decades after his voyage around the world— that Darwin had gathered enough evidence and developed his ideas enough to begin writing his great work about evolution by means of natural selection, On the Origin of Species (Figure 2.12). His colleagues had warned him that if he did not write his book soon, someone else might receive credit for the idea. Indeed, in 1858, Darwin received from the English naturalist and explorer Alfred Russel Wallace (1823–1913) a letter and a 20-page report outlining Wallace’s theory of evolution by means of natural selection (Figure 2.13). Independently from Darwin, Wallace had arrived at most of the same conclusions that Darwin had. Both men had been aware of their shared interest in the subject, and both men formulated their theories independently. Concerned that Wallace would publish first, Darwin completed Origin over the next 15 months and published it in London in 1859. Who, then, “discovered” natu- ral selection, the key mechanism that explains evolution? Some argue that Wallace should be given primary credit for the theory. However, because Wallace had not amassed the extensive body of evidence needed to support the theory, Darwin is generally recognized as the discoverer.

Darwin and Wallace made monumental discoveries, but neither man could come up with a compelling explanation of the physical mechanisms by which evolution takes place. That is, what mechanisms result in evolutionary change? Half a continent away, a series of novel experiments led to the discovery of these biological mechanisms, paving the way for remarkable new insights into evolution.

Since Darwin: Mechanisms of Inheritance, the Evolutionary Synthesis, and the Discovery of DNA MECHANISMS OF INHERITANCE Having articulated and supported his theory of evolution by means of natural selection, Darwin turned to the next fundamental question about natural selec- tion: How do the traits that are being selected for (or against) pass from parent to offspring? Like other scientists of his day, Darwin believed that each body part contained invisible particles called gemmules. Darwin hypothesized that

FIGURE 2.13 Alfred Russel Wallace Although Darwin often gets sole credit for the development of the theory of evolution through natural selection, Wallace (here depicted ca. 1860) contributed substantially to evolutionary theory. Wallace was the leading authority on the geographic distribution of animals, for example, and was the first to recognize the concept of warning coloration in animals. In addition, he raised the issue of human impact on the environment a full century before it became a concern for the general public.

gemmules As proposed by Darwin, the units of inheritance, supposedly accu- mulated in the gametes so they could be passed on to offspring.

34 | CHAPTER 2 Evolution: Constructing a Fundamental Scientific Theory

representative gemmules for all body parts resided in the reproductive organs. During fertilization, each parent contributed his or her gemmules to the poten- tial offspring. The father’s and the mother’s gemmules then intermingled to form the characteristics observed in their progeny. Called blending inheritance, this process was a popular notion at the time.

Unknown to Darwin, research elsewhere in Europe was calling into question the idea of blending inheritance. In 1865, just six years after the publication of On the Origin of Species, Gregor Mendel (1822–1884), an Augustinian monk living in a mon- astery in what is now Brno, Czech Republic, published in an obscure local scientific journal the results of his work on inheritance (Figure 2.14). Mendel had spent the previous eight years crossbreeding different varieties of garden pea plants. Over the course of his experiments, he grew some 28,000 plants. These plants enabled him to identify and carefully observe seven characteristics, or traits, that were especially informative about breeding and its outcome over generations (Figure 2.15). From his results, Mendel inferred that a discrete physical unit was responsible for each characteristic. This unit passed from parent to offspring, and in this way the charac- teristic was inherited. In fact, the discrete unit could be traced through generations, and its passage (the inheritance) was determined by mathematical laws.

Mendel also discovered that the garden peas’ traits did not blend. For example, plants and their offspring were either tall or short. Over time, the short plants diminished in frequency and eventually disappeared. Later scientists determined that the physical unit of inheritance— now known as a gene— has two subunits, one from the father and one from the mother, each called an allele. Each allele is either dominant or recessive. In garden peas, the allele for tallness is dominant and the allele for shortness is recessive. If one parent provides a “tall” allele (T ) and the other parent provides a “short” allele (t), then the offspring having one of each allele (Tt) would be tall because of the presence of the “tall” allele— the dominant allele is physically expressed, whereas the recessive allele is hidden. The pure strain for tall (TT ) includes one tall maternal allele (T ) and one tall paternal allele (T ). The pure strain for short (tt) includes one short maternal allele (t) and one short paternal allele (t) (Figure 2.16).

FIGURE 2.14 Gregor Mendel Mendel, the father of modern genetics, was a Christian monk by profession but a scientist by nature. His observations provided the foundation for our understanding of genetics (the subject of chapters 3 and 4).

FIGURE 2.15 Mendel’s Peas (a) This illustration— from the 1876 catalog of one of Mendel’s seed suppliers— shows some of (b) the seven characteristics Mendel studied, each of which had two variants. Flower position, for example, could be axial or terminal, while flower color could be white or purple.

Flower Position Flower Color Plant Height Pea Shape Pea Color Pod Shape Pod Color

Axial White Tall Round Yellow In ated Yellow

Terminal Purple Short Wrinkled Green Constricted Green

(a) (b)

Parent 1 (TT ): Tall

Generation 1

Parent 2 (tt): Short

100% Tt = Tall

t

T

25% TT = Tall 50% Tt = Tall 25% tt = Short

3:1 Tall:Short

t

Tt Tt

T

Tt Tt

Parent 1 (Tt): Tall

Generation 2

Parent 2 (Tt): Tall

T

T

t Tt tt

t

TT Tt

If the tallness allele is expressed as T and the shortness allele is expressed as t, the pure strain for tall is TT (one T is the maternal allele, the other T is the paternal allele), and the pure strain for short is tt (one t is the maternal allele, and the other t is the paternal allele).

When a TT plant is crossbred with a tt plant, one allele must come from the father (paternal) and one allele (maternal) must come from the mother, thereby producing a Tt offspring.

When the offspring from the TT and tt parental plants are bred, the offspring’s alleles independently redistribute, producing about equal numbers of the four possible combinations of T and t alleles: TT, Tt, tT, and tt.

Thus, three of the four plants (75%) will be tall owing to the dominance of the T allele and one plant (25%) will be short owing to the recessiveness of the t allele. Note, however, that 25% of the offspring are tall with two dominant tall alleles (TT ), while 50% are tall with one of each allele (Tt).

Because T is dominant, the offspring is tall.

FIGURE 2.16 Mendel’s Genetics

blending inheritance An outdated, dis- reputed theory that the phenotype of an offspring was a uniform blend of the parents’ phenotypes.

gene The basic unit of inheritance; a sequence of DNA on a chromosome, coded to produce a specific protein.

allele One or more alternative forms of a gene.

dominant Refers to an allele that is expressed in an organism’s phenotype and that simultaneously masks the effects of another allele, if another one is present.

recessive An allele that is expressed in an organism’s phenotype if two copies are present but is masked if the dominant allele is present.

Since Darwin: Mechanisms of Inheritance, the Evolutionary Synthesis, and the Discovery of DNA | 35

representative gemmules for all body parts resided in the reproductive organs. During fertilization, each parent contributed his or her gemmules to the poten- tial offspring. The father’s and the mother’s gemmules then intermingled to form the characteristics observed in their progeny. Called blending inheritance, this process was a popular notion at the time.

Unknown to Darwin, research elsewhere in Europe was calling into question the idea of blending inheritance. In 1865, just six years after the publication of On the Origin of Species, Gregor Mendel (1822–1884), an Augustinian monk living in a mon- astery in what is now Brno, Czech Republic, published in an obscure local scientific journal the results of his work on inheritance (Figure 2.14). Mendel had spent the previous eight years crossbreeding different varieties of garden pea plants. Over the course of his experiments, he grew some 28,000 plants. These plants enabled him to identify and carefully observe seven characteristics, or traits, that were especially informative about breeding and its outcome over generations (Figure 2.15). From his results, Mendel inferred that a discrete physical unit was responsible for each characteristic. This unit passed from parent to offspring, and in this way the charac- teristic was inherited. In fact, the discrete unit could be traced through generations, and its passage (the inheritance) was determined by mathematical laws.

Mendel also discovered that the garden peas’ traits did not blend. For example, plants and their offspring were either tall or short. Over time, the short plants diminished in frequency and eventually disappeared. Later scientists determined that the physical unit of inheritance— now known as a gene— has two subunits, one from the father and one from the mother, each called an allele. Each allele is either dominant or recessive. In garden peas, the allele for tallness is dominant and the allele for shortness is recessive. If one parent provides a “tall” allele (T ) and the other parent provides a “short” allele (t), then the offspring having one of each allele (Tt) would be tall because of the presence of the “tall” allele— the dominant allele is physically expressed, whereas the recessive allele is hidden. The pure strain for tall (TT ) includes one tall maternal allele (T ) and one tall paternal allele (T ). The pure strain for short (tt) includes one short maternal allele (t) and one short paternal allele (t) (Figure 2.16).

FIGURE 2.14 Gregor Mendel Mendel, the father of modern genetics, was a Christian monk by profession but a scientist by nature. His observations provided the foundation for our understanding of genetics (the subject of chapters 3 and 4).

FIGURE 2.15 Mendel’s Peas (a) This illustration— from the 1876 catalog of one of Mendel’s seed suppliers— shows some of (b) the seven characteristics Mendel studied, each of which had two variants. Flower position, for example, could be axial or terminal, while flower color could be white or purple.

Flower Position Flower Color Plant Height Pea Shape Pea Color Pod Shape Pod Color

Axial White Tall Round Yellow In ated Yellow

Terminal Purple Short Wrinkled Green Constricted Green

(a) (b)

Parent 1 (TT ): Tall

Generation 1

Parent 2 (tt): Short

100% Tt = Tall

t

T

25% TT = Tall 50% Tt = Tall 25% tt = Short

3:1 Tall:Short

t

Tt Tt

T

Tt Tt

Parent 1 (Tt): Tall

Generation 2

Parent 2 (Tt): Tall

T

T

t Tt tt

t

TT Tt

If the tallness allele is expressed as T and the shortness allele is expressed as t, the pure strain for tall is TT (one T is the maternal allele, the other T is the paternal allele), and the pure strain for short is tt (one t is the maternal allele, and the other t is the paternal allele).

When a TT plant is crossbred with a tt plant, one allele must come from the father (paternal) and one allele (maternal) must come from the mother, thereby producing a Tt offspring.

When the offspring from the TT and tt parental plants are bred, the offspring’s alleles independently redistribute, producing about equal numbers of the four possible combinations of T and t alleles: TT, Tt, tT, and tt.

Thus, three of the four plants (75%) will be tall owing to the dominance of the T allele and one plant (25%) will be short owing to the recessiveness of the t allele. Note, however, that 25% of the offspring are tall with two dominant tall alleles (TT ), while 50% are tall with one of each allele (Tt).

Because T is dominant, the offspring is tall.

FIGURE 2.16 Mendel’s Genetics

blending inheritance An outdated, dis- reputed theory that the phenotype of an offspring was a uniform blend of the parents’ phenotypes.

gene The basic unit of inheritance; a sequence of DNA on a chromosome, coded to produce a specific protein.

allele One or more alternative forms of a gene.

dominant Refers to an allele that is expressed in an organism’s phenotype and that simultaneously masks the effects of another allele, if another one is present.

recessive An allele that is expressed in an organism’s phenotype if two copies are present but is masked if the dominant allele is present.

36 | CHAPTER 2 Evolution: Constructing a Fundamental Scientific Theory

While Darwin’s theory generated immediate excitement in the scientific com- munity and among the public and was supported by leading scientists of the time such as Thomas Henry Huxley (Figure  2.17), Mendel’s crucial discovery (now known as Mendelian inheritance) went unnoticed. His writing was not widely distributed, and his work was simply ahead of its time. But in 1900, three scientists working independently— the German botanist Carl Erich Correns (1864–1933), the Austrian botanist Erich Tschermak von Seysenegg (1871–1962), and the Dutch botanist Hugo de Vries (1848–1935)—discovered Mendel’s research and replicated his findings. The Danish botanist Wilhelm Ludvig Johannsen (1857–1927) called the pair of alleles (e.g., TT, Tt, tt) the genotype and the actual physical appearance (tall, short) the phenotype.

Mendel’s theory of inheritance forms the basis of the modern discipline of genetics (the subject of chapters 3 and 4). It makes clear that the physical units— the genes and the two component alleles of each gene— responsible for physical attributes are located in the reproductive cells, eggs and sperm. When microscope technology improved in the late nineteenth century, the cell structure and the units of inheritance were defined (see chapter 3).

Beginning in 1908, the American geneticist Thomas Hunt Morgan (1866–1945) and his associates bred the common fruit fly in experiments that built on Mendel’s pea breeding. All genes, they discovered, are transmitted from parents to offspring in the ratios identified by Mendel. The genes are on chromosomes, and both the hereditary material and its carriers are duplicated during reproductive cell division.

THE EVOLUTIONARY SYNTHESIS, THE STUDY OF POPULATIONS, AND THE CAUSES OF EVOLUTION The combination of Darwin’s theory of evolution and Mendel’s theory of heredity resulted in an evolutionary synthesis. Darwin’s theory provided the mechanism for evolution (natural selection), and Mendel’s theory showed how traits are passed on systematically and predictably (Mendelian inheritance). The melding of natural selection and Mendelian inheritance led biologists to ask further questions about evolution, specifically about the origins of particular genes, genetic variation in general, and change in physical characteristics over time. Why do some genes increase in frequency, some decrease in frequency, and some show no change? How do completely new genes appear? These questions and a focus on population— viewed as the gene pool— provided the basis for a newly emerging field in evolution- ary biology called population genetics (among the subjects of chapter 4).

Natural selection, the guiding force of evolution, could operate only on variation that already existed in a population. How did new variation— new characteristics— arise in a population? Through his experiments with fruit flies, Morgan showed that a new gene could appear as a result of spontaneous change in an existing gene. This kind of genetic change is called mutation (Figure 2.18). The only source of new genetic material, mutation is another cause of evolution.

Gene flow, a third cause of evolution, is the diffusion, or spread, of new genetic material from one population to another of the same species. In other words, via reproduction, genes from one gene pool are transferred to another gene pool. Take, for example, the gene that causes sickle- cell anemia (this disorder is discussed extensively in chapter 4). Among West African blacks, it has a frequency of about 10%. Among American whites, it has a frequency of 0%. Because West African blacks and their descendants have long reproduced with American whites, the

FIGURE 2.17 Thomas Henry Huxley Huxley (1825–1895), an English biologist, was known as “Darwin’s bulldog” because he so forcefully promoted Darwin’s theory of evolution by natural selection. Among Huxley’s contributions to evolutionary theory was the concept that humans evolved from an apelike animal.

Mendelian inheritance The basic principles associated with the transmission of genetic material, forming the basis of genetics, including the law of segregation and the law of independent assortment.

genotype The genetic makeup of an organism; the combination of alleles for a given gene.

phenotype The physical expression of the genotype; it may be influenced by the environment.

chromosomes The strand of DNA found in the nucleus of eukaryotes that contains hundreds or thousands of genes.

evolutionary synthesis A unified theory of evolution that combines genetics with natural selection.

population genetics A specialty within the field of genetics; it focuses on the changes in gene frequencies and the effects of those changes on adaptation and evolution.

frequency among people descended from both West African blacks and American whites of the gene that causes sickle- cell anemia is approximately 5%, halfway between that of the two original populations. Over time, as the two populations have mixed, gene flow has decreased genetic difference.

Genetic drift, the fourth cause of evolution, is random change in the frequency of alleles— that is, of the different forms of a gene. Such change affects a small population more powerfully than it affects a large population (Figure 2.19). Over time, it increases the genetic difference between two genetically related but not interbreeding populations.

By the mid- twentieth century, the four causes of evolution— natural selection, mutation, gene flow, and genetic drift— were well defined, thanks to a synthesis of ideas drawn from the full range of sciences that deal with biological variation. In effect, evolutionary synthesis unified the branches of biology and its affiliated sci- ences, including genetics, taxonomy, morphology, comparative anatomy, paleontol- ogy, and the subject of this book, physical anthropology. Similarly, evolution unites living and past worlds. All organisms are related through common descent, and organisms more closely related than others share a more recent common ancestor.

DNA: DISCOVERY OF THE MOLECULAR BASIS OF EVOLUTION Once chromosomes were recognized as the carriers of genes, scientists sought to understand the structure of deoxyribonucleic acid (DNA), the chemical that makes up chromosomes. In 1953, the American geneticist James Watson (b. 1928) and the British biophysicist Francis Crick (1916–2004) published their discovery that DNA molecules have a ladderlike, double- helix structure. Crucial to their discovery was the work of the British X- ray crystallographer Rosalind Franklin (1920–1958), who used a special technique, X- ray diffraction, to produce high- quality images of  DNA.  The combined efforts of Franklin, Watson, and Crick opened up a whole new vista for biology by helping explain how chromosomes are replicated.

Analysis of the DNA from a wide variety of organisms, including primates, has provided both new perspectives on biological relationships and a molecular “clock” with which to time the branches of evolution (based on the similarity of species within those branches). In addition, DNA analysis has begun to shed light on a growing list of illnesses such as viral and bacterial infections, cancer, heart disease, and stroke.

mutation A random change in a gene or chromosome, creating a new trait that may be advantageous, deleterious, or neutral in its effects on the organism.

gene flow Admixture, or the exchange of alleles between two populations.

genetic drift The random change in allele frequency from one generation to the next, with greater effect in small populations.

deoxyribonucleic acid (DNA) A double- stranded molecule that provides the genetic code for an organism, consisting of phosphate, deoxyribose sugar, and four types of nitrogen bases.

(a) (b)

FIGURE 2.18 Fruit Fly Mutations (a) The normal fruit fly has two wings, while (b) the four- wing mutation has two wings on each side.

Since Darwin: Mechanisms of Inheritance, the Evolutionary Synthesis, and the Discovery of DNA | 37

38 | CHAPTER 2 Evolution: Constructing a Fundamental Scientific Theory

Little did Darwin realize just what a powerful foundation his evolutionary theory would build for science, ushering in modern biology and its allied disciplines, including physical anthropology. Long after his death, Darwin’s search for the biological mechanisms involved in evolution would continue to inspire scientists. The questions Darwin and his colleagues asked, especially about how physical attributes pass from parents to offspring, laid the foundation for the study of inheritance— the science of genetics— and eventually the DNA revolution. Darwin would have been impressed.

One month later

One red fish lost from each population

1:5 8:16

A B A B

0:5 7:16

16.6% Red 33.3% Red 0% Red 32.8% Red

Two populations of fish include red and gold varieties.

In the smaller population (6 fish), the ratio of red to gold is 1:5. Red fish represent 16.6% of the total.

In the smaller population (now 5 fish), the ratio of red to gold changes to 0:5. Red fish represent 0% of the total, a substantial change in the makeup of the population.

In the larger population (24 fish), the ratio of red fish to gold fish is 8:16 or 1:2. Red fish represent 33.3% of the total.

Over time, each population loses one red fish.

In the larger population (now 23 fish), the ratio of red to gold changes to 7:16. Red fish represent 32.8% of the total, a very small change in the makeup of the population.

FIGURE 2.19 Genetic Drift’s Effects on Small and Large Populations

39

A N S W E R I N G T H E B I G Q U E S T I O N S

C H A P T E R   2 R E V I E W

How did the theory of evolution come to be? • In developing his theory of evolution by means

of natural selection, Darwin drew on geology, paleontology, taxonomy and systematics, demography, and what is now called evolutionary biology.

• Scientists working in these disciplines had shown that — Earth is quite old and has changed considerably

over its history — fossils represent the remains of once- living, often

extinct organisms and thus provide a record of the history of life on the planet

— life evolves over time — groups of related species provide insight into

evolutionary history — the number of adults in a population tends to

remain the same over time

What was Darwin’s contribution to the theory of evolution? • Darwin’s key contribution was the principle of natural

selection. Three observations and inferences allowed him to deduce that natural selection is the primary driver of evolution: — the number of adults in a population tends to

remain the same over time even though, for most

organisms, parents tend to produce multiple and sometimes many offspring

— variation exists among members of populations — individuals having variation that is advantageous

for survival and reproduction increase in relative frequency over time

What has happened since Darwin in the development of our understanding of evolution? • Gregor Mendel discovered the principles of

inheritance, the basis for our understanding of how physical attributes are passed from parents to offspring.

• Mendel’s revelation that attributes are passed as discrete units, which we now know as genes, laid the groundwork for our understanding of cell biology, our understanding of chromosomes, and eventually the field of population genetics.

• We now know that evolution— genetic change in a population or species— is caused by one or a combination of four forces: natural selection, mutation, gene flow, and genetic drift.

• We now know that each chromosome in an organism’s cells consists of DNA molecules. DNA is the blueprint for all biological characteristics and functions.

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REVIEW THIS CHAPTER WITH PERSONALIZED, INTERACTIVE QUESTIONS THROUGH IJK, INQUIZITIVE.WWNORTON.COM q

K E Y T E R M S adaptations adaptive radiation allele

blending inheritance catastrophism chromosomes

demography deoxyribonucleic acid (DNA) dominant

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K E Y T E R M S

evolutionary biology evolutionary synthesis fossils gemmules gene gene flow genetic drift genotype

genus geology habitat Lamarckism Mendelian inheritance mutation natural selection paleontology

phenotype population genetics recessive species systematics taxonomy uniformitarianism

E V O L U T I O N R E V I E W Past, Present, and Future of a Fundamental Scientific Theory

Synopsis The theory of evolution forms the foundation of all the biological sciences, including physical anthropology. Although Charles Darwin is the most famous contributor to the formulation of this theory, his innovative idea of natural selection was partly influenced by the work of scientists across a number of disciplines, including geology, paleontology, taxonomy, and demography. The work of Gregor Mendel, rediscovered years after his death, provided a genetic basis for the evolutionary processes envisioned by Darwin and showed how evolution can occur in the natural world. Darwin’s principle of natural selection and Mendel’s principles of inheritance are intertwined in the modern evolutionary synthesis, the frame- work by which physical anthropologists address research questions related to human biological evolution and biocultural variation.

Q1. Charles Darwin is one of the most admired scientists of all time, and his principle of natural selection laid the foundations for all future biological thinking and discoveries. However, other scientists before Darwin argued in favor of biological evolution. Who is credited with one of the first major attempts at explaining the process of evolutionary change through time? What is the name of the erroneous mechanism hypothesized by this scientist to be a driving force of evolution?

Q2. Before the discoveries of Gregor Mendel, Darwin hypothesized that the characteristics of the father and mother intermingled

in the offspring. What was this idea called at the time? What  discovery, first made by Mendel and later by scientists such as Thomas Hunt Morgan, proved this hypothesis to be wrong?

Q3. In formulating his principle of natural selection, Darwin was inspired by the idea of the demographer Thomas Malthus that population is limited by food supply. How is this idea a concern for human populations today? What steps might be taken to address this issue in the future?

Q4 . Darwin originally did not publish his theory of evolution by means of natural selection as he was well aware of the con- troversy it would generate. Over 150 years later, and backed by massive amounts of evidence spanning many scientific disciplines, evolution remains a subject of controversy among the general public. Why has evolution always been the subject of fierce debate?

Q5. Darwin gathered information from the fields of geology, paleontology, taxonomy, demography, and what is now called evolutionary biology to develop his theory of evolution, which includes the idea of variation and natural selection. What are the five most important ideas from these other fields (described in this chapter) that contributed to Darwin’s devel- opment of his theory of evolution?

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A D D I T I O N A L R E A D I N G S

Alvarez, W. 1997. T. rex and the Crater of Doom. Princeton: Prince- ton University Press.

Berra, T. M. 2009. Charles Darwin: The Concise Story of an Extraor- dinary Man. Baltimore: Johns Hopkins University Press.

Bowler,  P.  J.  2003. Evolution: The History of an Idea. Berkeley: University of California Press.

Carroll,  S.  B.  2009. Remarkable Creatures: Epic Adventures in the Search for the Origins of Species. Boston: Houghton Mifflin Harcourt.

Gould, S. J. 1992. Ever since Darwin: Reflections on Natural History. New York: Norton.

Huxley,  R.  2007. The Great Naturalists. New  York: Thames & Hudson.

Repcheck, J. 2003. The Man Who Found Time: James Hutton and the Discovery of the Earth’s Antiquity. Cambridge, MA: Perseus Publishing.

Ridley, M. 2004. Evolution. Malden, MA: Blackwell Science.

Stott,  R.  2012. Darwin’s Ghosts: The Secret History of Evolution. New York: Spiegel & Grau.

Wilson,  E.  O.  2006. From So Simple a Beginning: Darwin’s Four Great Books [Voyage of the H.M.S. Beagle, The Origin of Species, The Descent of Man, The Expression of Emotions in Man and Ani- mals]. New York: Norton.

ON THE SURFACE, A HUMAN BEING and a chimpanzee might not seem to have much in common. However, they share 98% of their DNA. Chimpanzees are humans’ closest living relatives, and both primates often have similar facial expres- sions, emotions, and body movements. In these and many other ways, these two primates share a considerable amount of biology.

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3 What is the genetic code?

What does the genetic code (DNA) do?

What is the genetic basis for human variation?

Genetics Reproducing Life and Producing Variation

There is a revolution going on in science: the discovery of DNA and the identifi-cation of its molecular structure have brought about a “DNA Revolution.” At no time in history have humans learned so much so quickly about the biology of plants and animals. In addition to bringing about developments in agriculture and food production, medicine, and other areas that affect billions of people every day, the infor- mation derived from DNA has transformed a number of scientific disciplines. Consider forensic science, where fingerprints and blood types were once the primary evidence. Thanks to DNA, far smaller samples— of tissue, bone, hair, and blood— can be used to identify victims’ remains and to identify criminals with far greater accuracy. DNA in samples saved from old crime scenes has helped free scores of individuals con- victed of crimes they had not committed. Beyond forensics, DNA analysis has helped determine family relationships. It has helped genealogists reach into the past to chart ancestry. It has even been used to detect the presence of diseases, such as leprosy and syphilis, in ancient skeletons. Given the long and growing list of ways in which DNA can be used, no wonder former US president Bill Clinton referred to the human DNA sequence, right after it was presented to the public in 2003, as “the most important, most wondrous map ever produced by mankind.”

When I studied introductory biology in college, in the early 1970s, knowledge of DNA was just a tiny fraction of what it is today. Evolution was understood in terms of entire organisms and their biological history. Now, DNA provides us with the information— a whole new window— whereby we can see how organisms are put together and what is actually evolving. Powerful stuff! In anthropology, it has meant new insights into

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44 | CHAPTER 3 Genetics: Reproducing Life and Producing Variation

primate and human evolution. Before we can tie together the growing strands of DNA and evolution, though, we need to back up and examine the foundational work in genetics— the study of heredity.

Although the great nineteenth- century biologists discussed in chapter 2 knew a lot about variation in species, they did not fully understand how this variation is produced or how it is transmitted from parents to offspring. For example, how do an organism’s attributes grow from a fertilized egg? The answers to questions about variation— its ori- gin and continuation— lie in the cell, its structures, and the myriad functions it performs from conception through full maturity. And governing each cell is the genetic code.

The Cell: Its Role in Reproducing Life and Producing Variation The cell is the basic unit of life for all organisms (Figure  3.1). Every organism has at least one cell (that is the baseline definition of an organism). Organisms having cells with no internal compartments are called prokaryotes. These were likely the first life on Earth, appearing about 3.5 billion years ago (bya). Today, the prokaryotes are single- cell bacteria. Organisms with internal compartments sepa- rated by membranes are called eukaryotes. The membranes enclose the two main

prokaryotes Single- celled organisms with no nuclear membranes or organelles and with their genetic material as a single strand in the cytoplasm.

eukaryotes Multicelled organisms that have a membrane- bound nucleus con- taining both the genetic material and specialized organelles.

The nucleus is the largest organelle in a cell. It houses one copy of nearly all the genetic material, or DNA, of that organism. It is covered by a nuclear membrane, or nuclear envelope, which keeps the contents of the nucleus separate from the rest of the cell. The cell membrane is a semipermeable

membrane surrounding the entire cell, separating one cell from the next.

The mitochondrion is considered the “powerhouse” of the cell, because it generates most of the energy. The number of mitochondria per cell varies by tissue type and by organism.

The endoplasmic reticulum is an organelle that usually surrounds the nucleus. It plays an especially important role in protein synthesis (a process discussed later in this chapter).

The cytoplasm is fluid that fills the cell and maintains the cell’s shape. Organelles are suspended in the cytoplasm, which can also store chemical substances. The extranuclear DNA is in the mitochondria.

FIGURE 3.1 Cells and Their Organelles This illustration depicts the many components of cells found in plants and animals. Among the components are organelles, specialized parts analogous to organs.

The Cell: Its Role in Reproducing Life and Producing Variation | 45

parts of individual cells, the nucleus and the cytoplasm, between which various communications and activities happen (Figure  3.2). Eukaryotes evolved much later than prokaryotes, appearing some 1.2 bya. Their quite complex structures require enormous amounts of energy to survive and reproduce. As they did in the past, eukaryotes come in many different forms, ranging from single- cell yeasts to large, complex, multicellular organisms, such as us.

nucleus A membrane- bound structure in eukaryotic cells that contains the genetic material.

cytoplasm The jellylike substance inside the cell membrane that surrounds the nucleus and in which the organelles are suspended.

FIGURE 3.2 Prokaryotes and Eukaryotes (a) The many types of bacteria that we encounter in our daily lives are prokaryotic cells like this one. (b) For example, Escherichia coli (E. coli), two single cells of which are shown here, is a bacterium that aids digestion in the intestines of mammals, including humans. (c) This image shows the eukaryotic cells of a primate’s kidney.

Outer membrane

FlagellaeRibosome

Fimbriae

Cell wall Plasma membrane

Cytoplasm

The nucleoid region houses the genetic material of the prokaryotic cell, but unlike the nucleus of a eukaryotic cell it is not contained within a membrane. A prokaryotic cell has about one- thousandth the genetic material of a eukaryotic cell.

The cell wall provides a rigid shape and controls the movement of molecules into and out of the cell.

The flagellum is a whiplike structure attached to some prokaryotes. Rotated by a motorlike system located in the outer layers of the cell, the flagellum enables locomotion.

(a)

Nucleus Cytoplasm Plasma membrane (also called cell membrane)

(c)(b)

46 | CHAPTER 3 Genetics: Reproducing Life and Producing Variation

In all animals and plants, there are two types of eukaryotic cells. Somatic cells, also called body cells, comprise most tissues, such as bone, muscle, skin, brain, lung, fat, and hair (Figure 3.3). Gametes are the sex cells, sperm in males and ova (or eggs) in females (Figure  3.4). The root of somatic cell and gamete production is in the chromosomes, located in the nucleus of each cell. In humans, somatic cells have 46 chromosomes and gametes have 23 (Figure 3.5).

The DNA Molecule: The Genetic Code The chemical that makes up each chromosome, DNA, is the body’s genetic code. Because chromosomal DNA is contained in the nucleus of the cell, it is referred to as nuclear DNA, or nDNA.  Within each chromosome, DNA molecules form a sequence, or code, that is a template for the production of a protein, or part of a protein, in the body. Each protein has a specific function, and collectively the proteins determine all physical characteristics and govern the functions of all cells, tissues, and organs. Each DNA sequence, each protein- generating code, is a gene; and the complete set of genes in an individual cell is called the genome.

Although the number of chromosomes varies according to species (see Figure  3.5), all organisms share much the same genome. Chimpanzees have two more chromosomes than humans, but the DNA in chimpanzees and in humans is about 98% identical. Even the DNA in baker’s yeast is 45% similar to human  DNA.  Within any organism, nDNA is homoplasmic, meaning it is the same in each and every cell— the DNA in a skin cell matches the DNA in a bone cell. (An exception to the rule is mature red blood cells, which have no nuclei and, hence, no nuclear DNA.)

FIGURE 3.3 Somatic Cells Somatic cells in different tissues have different characteristics, but most somatic cells share a number of features. Every somatic cell has a nucleus, which contains a complete copy of the organism’s DNA. As a result, throughout the organism’s body there are millions of copies of that DNA. Note the nuclei in these images of human anatomy: (a) brain tissue, (b) red blood cells (the larger cells are white blood cells, and the small dots are platelets), (c) osteocyte (bone cell), (d) skin cells.

(a) (b)

(c) (d)

FIGURE 3.4 Gametes Only one of the sperm surrounding this ovum will penetrate the external membrane and fertilize the ovum.

somatic cells Diploid cells that form the organs, tissues, and other parts of an organism’s body.

gametes Sexual reproductive cells, ova and sperm, that have a haploid number of chromosomes and that can unite with a gamete of the opposite type to form a new organism.

homoplasmic Refers to nuclear DNA, which is identical in the nucleus of each cell type (except red blood cells).

The DNA Molecule: The Genetic Code | 47

A small but significant amount of DNA is contained in tiny organelles, called mitochondria, within each cell’s cytoplasm. These structures use oxygen to turn food molecules, especially sugar and fat, into adenosine triphosphate (ATP), a high- energy molecule that powers cells and, in turn, powers every tissue in the body. The number of mitochondria in a cell varies according to the cell’s

Organism Chromosome

Number Organism Chromosome

Number

FIGURE 3.5 Chromosomes (a) To get an idea of the incredibly minute size of chromosomes, consider that this pair has been magnified 35,000 times. If a penny (approximately 2 cm, or .8 in, in diameter) were magnified 35,000 times, it would be approximately .7 km, or .44 mi, in diameter. (b) An organism’s complexity is not related to its number of chromosomes, as this comparison illustrates. While humans have 46 chromosomes, other primates have more (e.g., ring- tailed lemurs) or fewer (e.g., black- and- white colobus monkeys).

Camel: 70

Guinea pig: 64

Salamander: 24

Housefly: 12

Apple: 34

Potato: 48

Petunia: 14

Algae: 148

Ring-tailed lemur: 56

Black-and- white colobus monkey: 44

Orangutan: 48

(b)

(a)

Camel: 70

Guinea pig: 64

Salamander: 24

Housefly: 12

Apple: 34

Potato: 48

Petunia: 14

Algae: 148

Ring-tailed lemur: 56

Black-and- white colobus monkey: 44

Orangutan: 48

(b)

(a)

mitochondria Energy- producing (ATP) organelles in eukaryotic cells; they pos- sess their own independent DNA.

adenosine triphosphate (ATP) An import- ant cellular molecule, created by the mitochondria and carrying the energy necessary for cellular functions.

48 | CHAPTER 3 Genetics: Reproducing Life and Producing Variation

activity level. For example, the cells in highly active body tissues, such as muscles, contain far more mitochondria than do cells in relatively inactive tissues, such as hair.

The mitochondrial DNA (mtDNA), a kind of miniature chromosome contain- ing 37 genes, is inherited just from the mother. That is, the mtDNA comes from the ovum. Each of us, then, carries our mother’s mtDNA, she carries or carried her mother’s mtDNA, and so on for generation after generation. In theory, a maternal lineage, or matriline, can be traced back hundreds of thousands of years. (Ancient matrilines in fossil hominins are discussed in chapter 10.) Unlike nDNA, mtDNA is heteroplasmic, meaning it can differ among different parts of a person’s body or even within the same kinds of cells.

DNA: THE BLUEPRINT OF LIFE The DNA molecule is the blueprint of life. It serves as the chemical template for every aspect of biological organisms. As Watson and Crick discovered, the molecule has a right- twisted, double- helix structure (see “DNA: Discovery of the Molecular Basis of Evolution” in chapter  2). Understanding this structure is key to understanding the growth of any organism and the transmission of genes from parents to offspring. The starting point for looking at the DNA molecule in any detail is to unravel a chromosome and look at a tiny segment of it under supermagnification. Its helical, ladderlike structure consists of two uprights and many rungs. The uprights of the structure are made up of alternating sugar and phosphate molecules, while the rungs are composed of paired nitrogen bases linked by a weak hydrogen bond (Figure 3.6).

On each side of the ladder, every unit of sugar, phosphate, and nitrogen base forms a single nucleotide (Figure  3.7). While the sugar and phosphate are the same throughout DNA, the base can be adenine (A), thymine (T), guanine (G), or cytosine (C). Owing to the bases’ unvarying chemical configurations, adenine and thymine always pair with each other and guanine and cytosine always pair up. In other words, apart from the rare errors in matching, adenine and thymine are complementary bases and guanine and cytosine are complementary bases. This means that if on one side of the ladder the sequence is ATGCAG, on the other side the sequence will be complementary, TACGTC. This predictability of base pair- ings assures the high reliability of one key function of the DNA molecule, that of self- reproduction. Anthropologists and geneticists investigate the many thousands of single DNA base pairings that produce genetic differences between individuals. Known as single nucleotide polymorphisms (SNPs, pronounced “snips”), these pairings are spread uniformly throughout the genome. Groups of SNPs play a crit- ical role in determining various attributes, such as hair color and blood type (see “Polymorphisms: Variations in Specific Genes,” later in this chapter).

The DNA Molecule: Replicating the Code One function of the DNA molecule is to replicate itself. Replication takes place in the nucleus and is part of cell division, leading to the production of new somatic cells (mitosis) or the production of new gametes (meiosis). Replication thus results

matriline DNA, such as mitochondrial DNA, whose inheritance can be traced from mother to daughter or to son.

heteroplasmic Refers to a mixture of more than one type of organellar DNA, such as mitochondrial DNA, within a cell or a single organism’s body, usually due to the mutation of the DNA in some organelles but not in others.

FIGURE 3.6 The Structure of DNA

The compact chromo- somal packaging of DNA enables thousands of genes to be housed inside a cell’s nucleus. The unwinding of this packaging reveals the genetic material.

DNA includes four different types of nitrogen bases. A gene is a specific and unique sequence of these bases.

DNA includes only one type of sugar (deoxyribose, the first part of the chemical name of DNA) and one type of phosphate group.

A T

GC

G C

P

PP

P

P

S

S

S S

S

S

The DNA Molecule: Replicating the Code | 49

in continued cell production, from the single- celled zygote (the fertilized egg) to two cells, then four cells, and so on, to the fully mature body with all of its many different tissues and organs— within which cells are continuously dying and being replaced.

In replication, DNA makes identical copies of itself, going from one double- stranded parent molecule of DNA to two double strands of daughter DNA. This means that where there was one chromosome, now there are two (Figure 3.8).

Nitrogen baseSugar

Phosphate

FIGURE 3.7 Nucleotide A nucleotide is the building block of DNA, made up of a phosphate group, a sugar, and a single nitrogen base.

complementary bases The predictable pairing of nitrogen bases in the structure of DNA and RNA, such that adenine and thymine always pair together (adenine and uracil in RNA) and cytosine and guanine pair together.

single nucleotide polymorphisms (SNPs) Variations in the DNA sequence due to the change of a single nitrogen base.

replication The process of copying nuclear DNA prior to cell division so that each new daughter cell receives a com- plete complement of DNA.

mitosis The process of cellular and nuclear division that creates two identical diploid daughter cells.

meiosis The production of gametes through one DNA replication and two cell (and nuclear) divisions, creating four haploid gametic cells.

zygote The cell that results from a sperm’s fertilization of an ovum.

C T TA

G A AT

C T TA

G A AT

C T TA

G A AT

C T

T A

C T

T A

G A

A T

G A

A TC

T T

A

G A

A T

Old strand

New strand

Old strand

New strand

The two strands of DNA become the parent template strands for replication. Each strand will replicate, using its nitrogen bases to synthesize a complementary strand.

Replication begins with the separation of the two strands of DNA. Enzymes break the relatively weak hydrogen bonds that hold together the paired nitrogen bases. In effect, the DNA is “unzipped,” creating the two parent template strands.

Each parent strand serves as a template for the creation of a new complementary DNA strand. The exposed, unpaired nitrogen bases on the parent strands attract complementary free-floating nucleotides. The nitrogen bases of these nucleotides form hydrogen bonds with the existing nitrogen bases—for example, a free-floating nucleotide with a cytosine base will attach itself to a guanine base.

New strands

New strands forming

When all the nitrogen bases of the parent strands are paired with (formerly free-floating) nucleotides, replication is complete. There are now two complete DNA molecules, each consisting of one parent strand and one new strand.

FIGURE 3.8 The Steps of DNA Replication

Imagine if we could look at ancient organisms’ DNA to understand their evolution. In fact, new tech- nology is enabling anthropologi- cal geneticists to routinely extract DNA from the tissues (mostly bones and teeth) of ancient remains. This emerging field, called paleoge- netics, has been made possible by the development of polymerase chain reaction (PCR), a method of amplifying a tiny sequence of DNA for study by incrementally increas- ing the sizes of a billion copies made from a single template of DNA. PCR has opened new windows onto the genetics of ancient populations, including the identification of sex chromosomes, the documentation of diseases, and the isolation of unique repetitions of DNA segments. It has yielded insight into the genetic dis- similarity of Neandertals and modern humans, and it has enabled explora- tion into population origins and move- ments (both subjects are among the topics of chapter 12).

Anthropologists have long specu- lated about the origins of Native Ameri- cans (where they came from is another subject of chapter 12). Key to under- standing their origins is their genetic diversity. Studies have revealed that the haplogroups of mtDNA— A, B, C, and D— in living Native Americans are quite similar to the haplogroups of their ancestors. This resemblance strongly suggests that Native Amer- icans’ genetic structure is quite

By examining the distribution of haplogroups A, B, C, and D in North and South America as well as eastern Asia, researchers have estimated that Native Americans arrived in the West- ern Hemisphere between 15,000 and 40,000 yBP. The presence of the same haplogroups in the northeastern part of Asia suggests that Native Americans originated from this area.

A B

CD A

AB

D C AB

CD

Ancient DNA Opens New Windows on the Past

old. Based on current assumptions about mutation rates in mtDNA, anthropologists and geneticists have estimated that people arrived in the Americas sometime between 15,000 and 40,000 yBP, earlier than what is documented in the archaeo- logical record (among the subjects of chapter  13). But a new variant of haplogroup D, discovered in the DNA of a 10,300- year- old skeleton from Alaska by paleogeneticist Brian Kemp and his collaborators, sug- gests that the molecular clock may be off and that humans first arrived

in the New World around 13,500 yBP, a date that jibes well with the archaeological evidence.

In addition, the presence of all four haplogroups and their variants in the skeletons of Native Ameri- cans dating to before 1492 tells us that the widespread decline of the Native American population after Columbus’s arrival did not reduce their genetic, and therefore biologic, diversity. Native Americans living today are likely as diverse genetically as were their ancestors living hun- dreds and thousands of years ago.

H O W D O W E K N O W ?

CHROMOSOME TYPES Within somatic cells, chromosomes occur in homologous, or matching, pairs (Figure  3.9). Each pair includes the father’s contribution (the paternal chromo- some) and the mother’s contribution (the maternal chromosome). These nonsex chromosomes are called autosomes.

The karyotype, or complete set of chromosomes, includes all of the autosomes and one pair of sex chromosomes, so called because they determine an individ- ual’s biological sex. Females have two X chromosomes, and males have one X and one Y chromosome (Figure 3.10). The Y chromosome contains a small amount of genetic material, which determines only male characteristics. The interaction of

FIGURE 3.9 Chromosome Pairs Homologous chromosomes are virtually identical in their physical and chemical structure. Each pair of chromosomes has the same genes, but the pair may have different alleles for specific genes.

FIGURE 3.10 Karyotype Contained within each somatic cell, the human karyotype typically consists of 46 chromosomes of various sizes in 23 pairs. Of those 23, one pair determines the person’s sex. Here, the label “X” means that these sex chromosomes are both Xs and thus belong to a human female.

free- floating nucleotides Nucleotides (the basic building block of DNA and RNA) that are present in the nucleus and are used during DNA replication and mRNA synthesis.

homologous Refers to each set of paired chromosomes in the genome.

autosomes All chromosomes, except the sex chromosomes, that occur in pairs in all somatic cells (not the gametes).

karyotype The characteristics of the chro- mosomes for an individual organism or a species, such as number, size, and type. The karyotype is typically presented as a photograph of a person’s chromosomes that have been arranged in homologous pairs and put in numerical order by size.

sex chromosomes The pair of chromo- somes that determine an organism’s biological sex.

The Two Steps of DNA Replication

The first function of DNA is to replicate itself. Templates from the original (parental) strand of DNA yield two exact (daughter) copies.

Step Activity

1. Strand of DNA unzips to form templates.

Weak nucleotide bonds between bases break, exposing two parental strands of DNA.

2. Templates plus nucleotides yield daughters.

Free- floating nucleotides in the nucleus match with the newly exposed template strands of DNA.

C O N C E P T C H E C K !

The DNA Molecule: Replicating the Code | 51

52 | CHAPTER 3 Genetics: Reproducing Life and Producing Variation

gametes during fertilization determines the combination of chromosomes in the offspring. If an X- carrying sperm fertilizes an egg (which always carries an X), the offspring will be female. If a Y- carrying sperm fertilizes an egg, the offspring will be male. Therefore, the male parent’s gamete determines the sex of his offspring because the Y chromosome is present in males only; it is passed from father to son.

The Y chromosome can be highly informative about paternity over many gen- erations. This patriline is in part analogous to the matriline- based mtDNA, which is passed on only by females. However, mtDNA goes to all of a woman’s children, whereas the Y chromosome is passed only to a man’s son.

Mitosis: Production of Identical Somatic Cells An organism starts life as a single cell, the zygote, which then produces identical copies of itself many, many times. A single human zygote, for example, even- tually results in more than 10 trillion cells, each having the exact same DNA (Figure  3.11). Here, the production of identical daughter cells from an original

patriline DNA whose inheritance can be traced from father to son via the Y chromosome.

Fertilization occurs when one sperm penetrates the outer membrane of the ovum, or egg.

A zygote is the single cell that forms at the beginning of an organism’s life. This cell must replicate itself millions of times to form a fully developed fetus.

After the regions of the body are established and different types of tissue have formed, the fetus grows until it reaches full-term size.

Following many replications, the embryo begins to differentiate different types of tissues and separate regions of the body, such as the head and limbs.

FIGURE 3.11 Prenatal Development The stages of human development from fertilization to a full- term infant.

diploid cell A cell that has a full comple- ment of paired chromosomes.

parental cell, mitosis, involves one DNA replication followed by one cell division (Figure 3.12). In this kind of cell division, a diploid cell— a cell having its organ- ism’s full set of chromosomes— divides to produce two cells, each of which also has the full set of chromosomes.

Chromatin

46 chromosomes

46 chromosomes

46 chromosomes

Chromosome duplication

Line up, spindle forms

The DNA in the cell is replicated, as described in Figure 3.8. This parent cell has a full set (23 pairs) of chromosomes.

The replicated DNA lines up in the middle of the cell.

As the cell divides, the DNA sep- arates. One complete complement of DNA goes into one new cell, and the other full complement goes into the second new cell.

Each new cell has a full set of DNA, with 23 pairs of chromosomes.

(b)

(a)

FIGURE 3.12 Mitosis (a) The steps of mitosis in humans. (b) A human skin cell undergoing mitosis, dividing into two new daughter cells.

46 chromo- somes

Chromo- some

duplication

Homologous chromosome

pairing

The pairs are separated and pulled to opposite sides as the cell divides.

The cell divides, forming two daughter cells.

The chromosomes line up in the middle of the cell, but are not paired.

A second cell division follows, without DNA replication. The chromosomes are separated into single strands and are pulled to opposite sides as the cell divides.

Four haploid daughter cells result, each with 23 chromosomes, but no pairs.

The parent cell is diploid, hav- ing 23 pairs of chromosomes.

Meiosis begins like mitosis. Initially, the cell’s DNA is replicated.

Homologous pairs of chromosomes line up in the middle of the cell.

FIGURE 3.13 Meiosis The steps of meiosis in humans. Compare this process to mitosis, shown in Figure 3.12.

Mitosis: Production of Identical Somatic Cells | 53

54 | CHAPTER 3 Genetics: Reproducing Life and Producing Variation

Meiosis: Production of Gametes (Sex Cells) The genetic code is transmitted from parents to offspring via the female and male gametes. Gametes, remember, have only half the chromosomes that are in somatic cells— they are haploid, containing one chromosome from each pair. Unlike mito- sis, the production of these cells, meiosis, does not result in identical copies of the parent cell and the parent cell’s DNA. Meiosis involves one DNA replication followed by two cell divisions (Figure 3.13).

Meiosis plays a critical role in the inheritance of biological characteristics and the variation seen in offspring. Because each gamete contains just one chromosome from a homologous pair and just one sex chromosome, during reproduction each parent contributes only half of his or her genetic material. For example, in your somatic cells, each homologous pair includes one chromosome from your mother and one chromosome from your father. Whether a particular gamete contains your mother’s chromosome or your father’s chromosome is completely random. In addition, homologous chromosomes often exchange parts when they pair up and intertwine. This exchange of parts is called crossing- over. The outcome of such reshuffling is that gene variants originally on the maternal chromosome are now on the paternal chromosome (or vice versa), a common development called recombination. Genes that are close together on a chromosome are much less likely to recombine. These units or blocks of genetic material are called haplo- types. Geneticists prefer to study haplotypes because they do not recombine and are passed on for many generations, potentially hundreds, over time. Groups of related haplotypes, called haplogroups, are an important tool for studying both long- term evolution and populations’ histories.

In rare instances, during meiosis nonhomologous chromosomes exchange seg- ments. These rare exchanges are called translocations. The most common form in humans, involving both chromosome 13 and chromosome 14, affects about 1 in 1,300 people. Translocations may cause infertility, Down syndrome (when one- third of chromosome 21 joins onto chromosome 14), and a number of diseases, including several forms of cancer (some leukemias). On occasion, chromosome pairs fail to separate during meiosis or mitosis. These nondisjunctions result in an incorrect number of chromosomes in the person’s genome. A loss in number of chromosomes is a monosomy. A gain in number of chromosomes is a trisomy, the most common being trisomy- 21, or Down syndrome (in this form, caused by an extra or part of an extra chromosome 21). As with many chromosomal abnor- malities, the age of the mother determines the risk of the offspring’s having Down syndrome. For 20- to 24- year- old mothers, the risk is 1/1,490. It rises to 1/106 by age 40 and 1/11 beyond age 49.

As Mendel had recognized (see “Since Darwin: Mechanisms of Inheritance, the Evolutionary Synthesis, and the Discovery of DNA” in chapter  2), each physical unit (that is, gene) passes from parent to offspring independently of other physical units. This independent inheritance— often called Mendel’s law of independent assortment (Figure  3.14)—applies to genes from different chromosomes. How- ever, what happens when genes are on the same chromosome? Because meiosis involves the separation of chromosome pairs (homologous chromosomes), genes on the same chromosome, especially ones near each other on that chromosome, have a greater chance of being inherited as a package. They are less subject to

haploid cell A cell that has a single set of unpaired chromosomes; half of the num- ber of chromosomes as a diploid cell.

crossing- over The process by which homologous chromosomes partially wrap around each other and exchange genetic information during meiosis.

recombination The exchange of genetic material between homologous chromo- somes, resulting from a cross- over event.

haplotypes A group of alleles that tend to be inherited as a unit due to their closely spaced loci on a single chromosome.

haplogroups A large set of haplotypes, such as the Y chromosome or mitochon- drial DNA, that may be used to define a population.

translocations Rearrangements of chromosomes due to the insertion of genetic material from one chromosome to another.

nondisjunctions Refers to the failure of the chromosomes to properly segregate during meiosis, creating some gametes with abnormal numbers of chromosomes.

monosomy Refers to the condition in which only one of a specific pair of chro- mosomes is present in a cell’s nucleus.

trisomy Refers to the condition in which an additional chromosome exists with the homologous pair.

law of independent assortment Mendel’s second law, which asserts that the inher- itance of one trait does not affect the inheritance of other traits.

F1 GgYy

F1 GgYy

GY

GY

Gy

gY

gy

GGYy GGyy

Gy gY gy

GGYY GGYy

GgYy Ggyy

GgYY GgYy

GgYy Ggyy

GgYY GgYy

ggYy ggyy

ggYY ggYy

This Punnett square shows all possible combinations of two different genes, pod color and seed color: G = green pod g = yellow pod Y = yellow seed y = green seed

Since both parents have two different alleles for both traits, there are 16 possible combinations.

Of the 16 combinations, nine have green pods and yellow seeds. The genotypes vary and include: GGYY, GGYy, GgYY, GgYy.

Three of the resulting combinations have green pods and green seeds. They have one of two genotypes: GGyy or Ggyy.

Three of the resulting combinations have yellow pods and yellow seeds. There are two possible genotypes: ggYY or ggYy.

One of the resulting combinations has yellow pods and green seeds, with the genotype ggyy.

FIGURE 3.14 Law of Independent Assortment Through his research with pea plants, Mendel created several laws pertaining to inheritance. (a) His second law, the law of independent assortment, asserts that traits linked to different chromosomes are inherited independently from one another. (b) Hair color, for example, is inherited independently from eye color.

Two equally probable chromosome arrangements in

meiosis I: OR

meiosis II: OR

gametes OR

with genotypes OR

The large chromosomes have a gene that determines eye color: red represents brown eyes, and blue represents blue eyes.

Alternatively, following the first cell division of meiosis, one cell has genes for brown eyes and blond hair, while the second has genes for blue eyes and brown hair.

Again, the four daughter cells, or gametes, follow suit: two gametes have genes for brown eyes and blond hair, while the other two gametes have genes for blue eyes and brown hair.

The small chromosomes have a gene that determines hair color: red represents brown hair, and blue represents blond hair.

Following the first cell division of meiosis, one cell has genes for brown eyes and brown hair, while the second cell has genes for blue eyes and blond hair.

The four daughter cells, or gametes, follow suit: two gametes have genes for brown eyes and brown hair, while the other two gametes have genes for blue eyes and blond hair.

(a)

(b)

Meiosis: Production of Gametes (Sex Cells) The genetic code is transmitted from parents to offspring via the female and male gametes. Gametes, remember, have only half the chromosomes that are in somatic cells— they are haploid, containing one chromosome from each pair. Unlike mito- sis, the production of these cells, meiosis, does not result in identical copies of the parent cell and the parent cell’s DNA. Meiosis involves one DNA replication followed by two cell divisions (Figure 3.13).

Meiosis plays a critical role in the inheritance of biological characteristics and the variation seen in offspring. Because each gamete contains just one chromosome from a homologous pair and just one sex chromosome, during reproduction each parent contributes only half of his or her genetic material. For example, in your somatic cells, each homologous pair includes one chromosome from your mother and one chromosome from your father. Whether a particular gamete contains your mother’s chromosome or your father’s chromosome is completely random. In addition, homologous chromosomes often exchange parts when they pair up and intertwine. This exchange of parts is called crossing- over. The outcome of such reshuffling is that gene variants originally on the maternal chromosome are now on the paternal chromosome (or vice versa), a common development called recombination. Genes that are close together on a chromosome are much less likely to recombine. These units or blocks of genetic material are called haplo- types. Geneticists prefer to study haplotypes because they do not recombine and are passed on for many generations, potentially hundreds, over time. Groups of related haplotypes, called haplogroups, are an important tool for studying both long- term evolution and populations’ histories.

In rare instances, during meiosis nonhomologous chromosomes exchange seg- ments. These rare exchanges are called translocations. The most common form in humans, involving both chromosome 13 and chromosome 14, affects about 1 in 1,300 people. Translocations may cause infertility, Down syndrome (when one- third of chromosome 21 joins onto chromosome 14), and a number of diseases, including several forms of cancer (some leukemias). On occasion, chromosome pairs fail to separate during meiosis or mitosis. These nondisjunctions result in an incorrect number of chromosomes in the person’s genome. A loss in number of chromosomes is a monosomy. A gain in number of chromosomes is a trisomy, the most common being trisomy- 21, or Down syndrome (in this form, caused by an extra or part of an extra chromosome 21). As with many chromosomal abnor- malities, the age of the mother determines the risk of the offspring’s having Down syndrome. For 20- to 24- year- old mothers, the risk is 1/1,490. It rises to 1/106 by age 40 and 1/11 beyond age 49.

As Mendel had recognized (see “Since Darwin: Mechanisms of Inheritance, the Evolutionary Synthesis, and the Discovery of DNA” in chapter  2), each physical unit (that is, gene) passes from parent to offspring independently of other physical units. This independent inheritance— often called Mendel’s law of independent assortment (Figure  3.14)—applies to genes from different chromosomes. How- ever, what happens when genes are on the same chromosome? Because meiosis involves the separation of chromosome pairs (homologous chromosomes), genes on the same chromosome, especially ones near each other on that chromosome, have a greater chance of being inherited as a package. They are less subject to

haploid cell A cell that has a single set of unpaired chromosomes; half of the num- ber of chromosomes as a diploid cell.

crossing- over The process by which homologous chromosomes partially wrap around each other and exchange genetic information during meiosis.

recombination The exchange of genetic material between homologous chromo- somes, resulting from a cross- over event.

haplotypes A group of alleles that tend to be inherited as a unit due to their closely spaced loci on a single chromosome.

haplogroups A large set of haplotypes, such as the Y chromosome or mitochon- drial DNA, that may be used to define a population.

translocations Rearrangements of chromosomes due to the insertion of genetic material from one chromosome to another.

nondisjunctions Refers to the failure of the chromosomes to properly segregate during meiosis, creating some gametes with abnormal numbers of chromosomes.

monosomy Refers to the condition in which only one of a specific pair of chro- mosomes is present in a cell’s nucleus.

trisomy Refers to the condition in which an additional chromosome exists with the homologous pair.

law of independent assortment Mendel’s second law, which asserts that the inher- itance of one trait does not affect the inheritance of other traits.

F1 GgYy

F1 GgYy

GY

GY

Gy

gY

gy

GGYy GGyy

Gy gY gy

GGYY GGYy

GgYy Ggyy

GgYY GgYy

GgYy Ggyy

GgYY GgYy

ggYy ggyy

ggYY ggYy

This Punnett square shows all possible combinations of two different genes, pod color and seed color: G = green pod g = yellow pod Y = yellow seed y = green seed

Since both parents have two different alleles for both traits, there are 16 possible combinations.

Of the 16 combinations, nine have green pods and yellow seeds. The genotypes vary and include: GGYY, GGYy, GgYY, GgYy.

Three of the resulting combinations have green pods and green seeds. They have one of two genotypes: GGyy or Ggyy.

Three of the resulting combinations have yellow pods and yellow seeds. There are two possible genotypes: ggYY or ggYy.

One of the resulting combinations has yellow pods and green seeds, with the genotype ggyy.

FIGURE 3.14 Law of Independent Assortment Through his research with pea plants, Mendel created several laws pertaining to inheritance. (a) His second law, the law of independent assortment, asserts that traits linked to different chromosomes are inherited independently from one another. (b) Hair color, for example, is inherited independently from eye color.

Two equally probable chromosome arrangements in

meiosis I: OR

meiosis II: OR

gametes OR

with genotypes OR

The large chromosomes have a gene that determines eye color: red represents brown eyes, and blue represents blue eyes.

Alternatively, following the first cell division of meiosis, one cell has genes for brown eyes and blond hair, while the second has genes for blue eyes and brown hair.

Again, the four daughter cells, or gametes, follow suit: two gametes have genes for brown eyes and blond hair, while the other two gametes have genes for blue eyes and brown hair.

The small chromosomes have a gene that determines hair color: red represents brown hair, and blue represents blond hair.

Following the first cell division of meiosis, one cell has genes for brown eyes and brown hair, while the second cell has genes for blue eyes and blond hair.

The four daughter cells, or gametes, follow suit: two gametes have genes for brown eyes and brown hair, while the other two gametes have genes for blue eyes and blond hair.

(a)

(b)

Meiosis: Production of Gametes (Sex Cells) | 55

56 | CHAPTER 3 Genetics: Reproducing Life and Producing Variation

recombination. This gene linkage— the inheritance of a package of genes (such as haplotypes) from the same chromosome (Figure 3.15)—is an exception to Mendel’s law of independent assortment.

Producing Proteins: The Other Function of DNA In addition to replicating itself, DNA serves as the template for protein synthe- sis. Proteins are the complex chemicals that make up tissues and bring about the functions, repair, and growth of tissues (Table  3.1). While some work within cells— for example, the enzymes that unzip DNA during replication— others, such as hormones, work within the whole body. Proteins consist of amino acids, of which there are 20. Each kind of protein is defined by its particular combination and number of linked amino acids. Most of the human body is comprised of pro- teins, and the body produces 12 of the amino acids. The other eight, also called essential amino acids, come from particular foods.

Two main categories of proteins are constantly being synthesized. Structural proteins are responsible for physical characteristics, such as hair form, eye color, tooth size, and basic bone shape (Figure  3.16). The other category, regulatory (also called functional ) proteins, includes enzymes, hormones, and antibodies. Enzymes regulate activities within cells, hormones regulate activities between cells, and antibodies are key to fighting infections.

Protein synthesis is a two- step process (Figure 3.17). The first step, transcrip- tion, takes place mostly in the cell’s nucleus. The second, translation, takes place in the cytoplasm. Transcription starts out just like the first step of DNA replica- tion: a double strand of parental DNA unzips. Rather than producing daughter strands of DNA, the now- exposed bases in the DNA molecule serve as a single

A B C

a b c

FIGURE 3.15 Linkage Since alleles A, B, and C are on the same chromosome, they have a better chance of being inherited as a unit than of being combined and inherited with alleles a, b, and c, which are together on a separate chromosome and thus also have a good chance of being inherited as a unit. Meanwhile, because they are close together, alleles A and B (like alleles a and b) stand a better chance of being inherited together than do alleles B and C (like alleles b and c). If, for example, eye color and hair color were on the same chromosome, especially if they were close together on that chromosome, they would most likely not be inherited separately with all the combinations examined in Figure 3.14.

linkage Refers to the inheritance, as a unit, of individual genes closely located on a chromosome; an exception to the law of independent assortment.

amino acids Organic molecules combined in a specific sequence by the ribosomes to form a protein.

essential amino acids Those amino acids that cannot be synthesized in the body; they must be supplied by the diet.

structural proteins Proteins that form an organism’s physical attributes.

regulatory proteins Proteins involved in the expression of control genes.

transcription The first step of protein synthesis, involving the creation of mRNA based on the DNA template.

translation The second step of protein synthesis, involving the transfer of amino acids by tRNA to the ribosomes, which are then added to the protein chain.

ribonucleic acid (RNA) A single- stranded molecule involved in protein synthesis, consisting of a phosphate, ribose sugar, and one of four nitrogen bases.

TABLE 3.1 The Seven Types of Proteins

Name Function Examples

Enzymes Catalyze chemical reactions

Lactase— breaks down lactose in milk products

Structural Proteins

Give structure or support to tissues

Keratin— hair; collagen— bone

Gas Transport Proteins

Carry vital gases to tissues

Hemoglobin— oxygen

Antibodies Part of immune system Anti- A and anti- B in ABO blood system

Hormones Regulate metabolism Insulin— regulates metabolism of carbohydrates and fats

Mechanical Proteins

Carry out specific functions or work

Actin and myosin— help muscles contract

Nutrients Provide vital nutrients to tissues

Ovalbumin— main protein of egg whites

Producing Proteins: The Other Function of DNA | 57

template for another kind of nucleic acid, ribonucleic acid (RNA). RNA has the same nitrogen bases as DNA, except that uracil (U) replaces thymine (T). Uracil always matches with adenine (A), while guanine (G) continues to pair with cytosine (C).

Only one of the two DNA strands serves as the template for the production of RNA. This strand attracts free- floating RNA nucleotides. The strand of RNA— now called messenger RNA (mRNA)—then splits off from the DNA template, leaves the nucleus, and moves into the cytoplasm.

In the translation step, the mRNA attaches itself to structures called ribo- somes. The mRNA is a “messenger” because (in the form of its own open bases) it carries the code for the protein being synthesized from the nucleus to the ribo- somes. Ribosomes are made up of another kind of ribonucleic acid, ribosomal RNA (rRNA). Once the mRNA is attached to the ribosome, the transcription step of protein synthesis is complete.

Floating in the cytoplasm is yet another kind of ribonucleic acid, transfer RNA (tRNA). tRNA occurs as triplets, or anticodons, that seek complementary triplet strands of mRNA, known as triplets or codons. For example, a triplet of AUC mRNA would pair with the complementary UAG tRNA. The three bases of the tRNA triplet represent a specific amino acid.

As the tRNA strand builds off the mRNA template, the amino acids are chemically linked together by a peptide bond, resulting in a chain of amino acids. A chain of these peptide bonds is called a polypeptide. Although a single polypeptide may function as a protein, in many cases multiple polypeptides must bind together and fold into a three- dimensional structure to form a functional protein. For example, hemoglobin, a molecule found on the surface of red blood cells, is comprised of two pairs of polypeptide chains. Once the protein has formed, it breaks away from the tRNA and commences with its task, either structural or functional.

(a) (b)

FIGURE 3.16 Structural Proteins While culture and environment strongly influence the development of biological structures, those structures are initially determined by structural proteins. Two important structural proteins are keratin and collagen. (a) In humans, keratin is the primary component of hair (pictured here), skin, and fingernails. In other mammals and in amphibians, birds, and reptiles, it also contributes to structures such as hooves, antlers, claws, beaks, scales, and shells. (b) Collagen is the most abundant protein in humans and other mammals and is essential for connective tissues, such as bone (pictured here), cartilage, ligaments, and tendons. In addition, collagen strengthens the walls of blood vessels and, along with keratin, gives strength and elasticity to skin. In its crystalline form, collagen is found in the cornea and lens of the eye.

uracil One of four nitrogen bases that make up RNA; it pairs with adenine.

messenger RNA (mRNA) The molecules that are responsible for making a chemical copy of a gene needed for a specific pro- tein, that is, for the transcription phase of protein synthesis.

ribosomes The organelles attached to the surface of endoplasmic reticulum, located in the cytoplasm of a cell; they are the site of protein synthesis.

ribosomal RNA (rRNA) A fundamental structural component of a ribosome.

transfer RNA (tRNA) The molecules that are responsible for transporting amino acids to the ribosomes during protein synthesis.

anticodons Sequences of three nitrogen bases carried by tRNA, they match up with the complementary mRNA codons and each designate a specific amino acid during protein synthesis.

triplets Sequences of three nitrogen bases each in DNA, known as codons in mRNA.

codons The sequences of three nitrogen bases carried by mRNA that are coded to produce specific amino acids in protein synthesis.

peptide bond Chemical bond that joins amino acids into a protein chain.

polypeptide Also known as a protein, a chain of amino acids held together by multiple peptide bonds.

Amino acid

Protein

RibosomeNucleus

DNA

mRNA

Cytoplasm

Transcription, which occurs in the nucleus, involves the creation of mRNA from one strand of DNA.

After the mRNA strand is completed, it leaves the nucleus and goes to the ribosomes, in the cytoplasm.

Translation takes place at the ribo- somes. A protein is formed as the mRNA is “read” and the appropriate amino acids are linked together.

Transcription

Translation

Transcription Translation

As in DNA replication, transcription begins with enzymes “unzipping” the DNA. Unlike replication, however, transcription uses only one strand of DNA.

Once the DNA strands have opened, messenger RNA (mRNA) attaches free-floating RNA nitrogen bases to the exposed, unpaired DNA nitrogen bases.

Once completed, the DNA closes back up, and the mRNA strand leaves the nucleus and goes to one of the ribosomes on the endoplasmic reticulum.

At a ribosome, a molecule of tRNA brings the anticodon for each codon on the mRNA. The tRNA carries its anticodon on one end and the associated amino acid on the other.

Translation begins as the mRNA binds to a ribosome. In effect, the “message” carried by the mRNA is “translated” by a ribosome.

The ribosome “reads” the mRNA three nitrogen bases at a time. When a codon matches the transfer RNA (tRNA) molecule’s anticodon, the tRNA’s amino acid is added to the protein chain. For example, if the codon has the bases AUG, then the tRNA with the anticodon of UAC will attach the amino acid methionine to the chain.

mRNA

tRNA

(a)

(b)

DNA template

in nucleus

Ribosome

at ribosome

mRNA strand

A

U

T

A

T

A

C

G

G

C …

Completed mRNA strand

Moves out of nucleus to ribosomes in cytoplasm

U UUAA G AG A GG G ……

U

UU

A

A

G

A

G

A GG G ……

Anticodon

Codon

tRNA

Amino acid

AU C

… U

As the ribosome moves the mRNA one codon at a time, tRNA continues to attach the appropriate amino acid to the protein chain. The amino acids are attached by a peptide bond, creating a polypeptide chain, which when completed is the protein. As each amino acid is added, the tRNA is released.

Peptide bond

Protein: polypeptide chain

AU C A

U

C

UA G

UA G

Eventually, a “stop” codon is reached, which indicates that the protein is completed. The mRNA leaves the ribosome, and the protein is released.

A U C

Anticodon

Amino acid

Anticodon

Codon

(c)

met

glysermetleutyrlys

sermet

stop

Serine

UUA AG A GG G …

UU AA A GG G G …

AG G U A G …

UA G… Protein Synthesis (a) As this overview of protein synthesis shows, transcription occurs mostly within the cell’s nucleus and translation follows at the ribosomes. (b) Here, the steps of protein synthesis are diagrammed for a hypothetical protein. (c) At the top is a computer model of a tRNA molecule, and below that is a diagram of the molecule.

F I G U R E

3.17 Protein Synthesis

Amino acid

Protein

RibosomeNucleus

DNA

mRNA

Cytoplasm

Transcription, which occurs in the nucleus, involves the creation of mRNA from one strand of DNA.

After the mRNA strand is completed, it leaves the nucleus and goes to the ribosomes, in the cytoplasm.

Translation takes place at the ribo- somes. A protein is formed as the mRNA is “read” and the appropriate amino acids are linked together.

Transcription

Translation

Transcription Translation

As in DNA replication, transcription begins with enzymes “unzipping” the DNA. Unlike replication, however, transcription uses only one strand of DNA.

Once the DNA strands have opened, messenger RNA (mRNA) attaches free-floating RNA nitrogen bases to the exposed, unpaired DNA nitrogen bases.

Once completed, the DNA closes back up, and the mRNA strand leaves the nucleus and goes to one of the ribosomes on the endoplasmic reticulum.

At a ribosome, a molecule of tRNA brings the anticodon for each codon on the mRNA. The tRNA carries its anticodon on one end and the associated amino acid on the other.

Translation begins as the mRNA binds to a ribosome. In effect, the “message” carried by the mRNA is “translated” by a ribosome.

The ribosome “reads” the mRNA three nitrogen bases at a time. When a codon matches the transfer RNA (tRNA) molecule’s anticodon, the tRNA’s amino acid is added to the protein chain. For example, if the codon has the bases AUG, then the tRNA with the anticodon of UAC will attach the amino acid methionine to the chain.

mRNA

tRNA

(a)

(b)

DNA template

in nucleus

Ribosome

at ribosome

mRNA strand

A

U

T

A

T

A

C

G

G

C …

Completed mRNA strand

Moves out of nucleus to ribosomes in cytoplasm

U UUAA G AG A GG G ……

U

UU

A

A

G

A

G

A GG G ……

Anticodon

Codon

tRNA

Amino acid

AU C

… U

As the ribosome moves the mRNA one codon at a time, tRNA continues to attach the appropriate amino acid to the protein chain. The amino acids are attached by a peptide bond, creating a polypeptide chain, which when completed is the protein. As each amino acid is added, the tRNA is released.

Peptide bond

Protein: polypeptide chain

AU C A

U

C

UA G

UA G

Eventually, a “stop” codon is reached, which indicates that the protein is completed. The mRNA leaves the ribosome, and the protein is released.

A U C

Anticodon

Amino acid

Anticodon

Codon

(c)

met

glysermetleutyrlys

sermet

stop

Serine

UUA AG A GG G …

UU AA A GG G G …

AG G U A G …

UA G…

60 | CHAPTER 3 Genetics: Reproducing Life and Producing Variation

All of the DNA involved in protein synthesis is coding DNA, the molecular segments encoded for particular proteins. The total length of DNA in humans is about 3 billion nucleotides. Each of the 20,000 or so genes has about 5,000 nucle- otides, so (according to the math) only about 5% of the DNA contains protein- coding material. Thus, most human DNA is noncoding. Often interspersed with coding DNA from one end of the chromosome to the other, this noncoding “junk” DNA has long been thought to have no function. However, non- protein- coding DNA is now known to have considerable regulatory functions throughout the genome, specifically regulating gene activities by helping to turn them on or off. New work on the genome suggests that 80% of the noncoding DNA is functional in some manner, containing instructions for proteins such as which genes a cell uses and when or determining if a cell becomes a bone cell or a brain cell. In pro- tein synthesis, the noncoding DNA is cut out before translation. Recent studies by anthropological geneticists have suggested that noncoding DNA located close to genes that control brain function may have a role in the overall wiring of the brain cells to each other. Most research, however, focuses on the DNA that codes for particular body structures or particular regulatory functions. This DNA makes up the two main types of genes, structural and regulatory.

coding DNA Sequences of a gene’s DNA (also known as exons) that are coded to produce a specific protein and are transcribed and translated during protein synthesis.

noncoding DNA Sequences of a gene’s DNA (also known as introns) that are not coded to produce specific proteins and are excised before protein synthesis.

structural genes Genes coded to produce particular products, such as an enzyme or hormone, rather than for regulatory proteins.

regulatory genes Those genes that deter- mine when structural genes and other regulatory genes are turned on and off for protein synthesis.

homeotic (Hox) genes Also known as homeobox genes, they are responsible for differentiating the specific segments of the body, such as the head, tail, and limbs, during embryological development.

locus The location on a chromosome of a specific gene.

The Two Steps of Protein Synthesis

The second function of DNA is to synthesize proteins, which are responsible for all the structures and functions of the body.

Step Activity

1. Transcription (nucleus)

Parental strand of DNA unzips, exposing two daughter strands of DNA.

Free- floating RNA nucleotides match one exposed daughter strand of DNA.

The strand of messenger RNA (mRNA) moves out of the nucleus and into the cytoplasm.

2. Translation (cytoplasm)

The mRNA attaches to a ribosome in the cytoplasm.

Triplets of transfer RNA (tRNA), with exposed bases and each carrying an amino acid specific to its set of three bases, recognize and bind with complementary base pairs of mRNA.

The amino acids, linked by peptide bonds, form a chain called a polypeptide.

The protein forms, either as a single polypeptide or as multiple polypeptides bound together.

C O N C E P T C H E C K !

Polymorphisms: Variations in Specific Genes | 61

Genes: Structural and Regulatory Structural genes are responsible for body structures, such as hair, blood, and other tissues. Regulatory genes turn other genes on and off, an essential activity in growth and development. If the genes that determine bones, for example, did not turn off at a certain point, bones would continue to grow well beyond what would be acceptable for a normal life (Figure 3.18).

Chickens have the genes for tooth development, but they do not develop teeth because those genes are permanently turned off. Humans have a gene for complete body hair coverage, but that gene is not turned on completely. The human genes for sexual maturity turn on during puberty, somewhat earlier in girls than in boys. Finally, regulatory genes can lead to lactose intolerance in humans (among the topics of chapter 4). In this instance, the gene that produces lactase— the enzyme for the digestion of milk— is turned off for most human populations around the world following weaning, usually by about age four. However, most humans of northern European and East African descent have inherited a different regulatory gene, which creates lactase persistence. A person who lacks this gene and eats dairy products experiences great gastrointestinal discomfort. A person who retains the gene is able to digest lactose owing to the persistence of lactase, thus enjoying the nutritional benefits of milk.

An organism’s form and the arrangement of its tissues and organs are deter- mined by regulatory genes called homeotic (Hox) genes. These master genes guide, for example, the embryological development of all the regions of an animal’s body, such as the head, trunk, and limbs (Figure  3.19). This means that in the process of development particular sets of Hox genes are turned on in a particular sequence, causing the correct structure or part of a structure to develop in each region. Until recently, scientists thought that the genes that control the develop- ment of the key structures and functions of the body differed from organism to organism. We now know, however, that the development of various body parts in complex organisms— such as the limbs, eyes, and vital organs— is governed by the same genes. Hox genes were first found in fruit flies, but research has shown that a common ancestral lineage has given organisms— ranging from flies to mice to humans— the same basic DNA structure in the key areas that control the development of form. Flies look like flies, mice look like mice, and humans look like humans because the Hox genes are turned on and off at different places and different times during the development process.

Polymorphisms: Variations in Specific Genes Along each chromosome, a specific gene has a specific physical location, or locus (plural, loci). This locus is of intense interest to geneticists, especially in under- standing the appearance and evolution of genetic variation (among the topics of chapter 4). Alleles, the genetic subunits (see “Mechanisms of Inheritance” in chap- ter  2), are slightly different chemical structures at the same loci on homologous chromosomes. That is, they are simply chemically alternative versions of the same gene. Some genes have only one allele, while others have 20 or more.

FIGURE 3.18 Marfan Syndrome (a) The hand on the right shows normal finger growth. The hand on the left has much longer and thinner fingers due to Marfan syndrome, a hereditary disorder of the regulatory genes that control connective tissue. As a result of Marfan syndrome, uncontrolled bone growth leads to long and thin fingers and toes, long and thin arms and legs, and increased stature. Organs such as the lungs and heart can also be negatively affected. (b) In the 1960s, a scientific paper asserted that US president Abraham Lincoln (1809–1865) was afflicted with Marfan syndrome. This still- controversial assessment was based entirely on Lincoln’s unusual tallness and the length of his limbs.

(a)

(b)

62 | CHAPTER 3 Genetics: Reproducing Life and Producing Variation

Human blood type is one genetic trait with different alleles. Each person has one of four blood types— A, B, AB, or O— and these four types comprise the ABO blood group system, first discovered in 1900 (Figure 3.20). Because it has two or more vari- ants, a genetic trait such as this one is called a polymorphism (Greek poly, meaning “many”; Greek morph, meaning “form”). Each person has one A, B, or O allele on one chromosome of the homologous pair and another A, B, or O allele on the other chromosome of that pair. The combination determines the person’s blood type.

Although Mendel did not know about chromosomes, he recognized that phys- ical units of inheritance— which we now know to be the genes— segregate in a very patterned fashion. That is, his experiments with garden peas showed that the father contributes one physical unit and the mother contributes the other. This is Mendel’s law of segregation (Figure  3.21). For example, a person with blood type AB will pass on either an A or a B allele to a child but not both. The other allele will come from the other parent. This discovery was revolutionary because it explained how new variation arises in reproduction.

Some of the most exciting contemporary DNA research has revealed a whole new array of genetic markers. Showing a tremendous amount of variation within and between human populations, these SNPs are known from well over 1 million sites on the human genome. Closer examination of the human genome has also revealed that DNA segments are often repeated, sometimes many times and for no apparent reason. These repeated sections, or microsatellites, are highly

Chromosome

Antp gene

Fruit fly Hox genes Mouse Hox genes Goose Python Human

Hoxc6 gene

Neck

Thorax

Hox genes have been identified in all animals, plants, and fungi. They are found as a unique cluster known as the Hox cluster or Hox complex.

Unlike vertebrate animals, insects such as fruit flies have distinct body regions, including the head and the middle, or thorax. In fruit flies, the Hox gene that determines the thoracic region of the body during the larval stage of development is called Antp.

Other vertebrates, such as birds and reptiles, have a Hoxc6 gene, which determines the location of the thorax in the embryo. However, the location of the Hoxc6 gene varies with each animal, allowing for variation in the length of the cervical, or neck, region. If the Hoxc6 gene is lower in the body, as it is in geese, the animal will have a much longer neck than if the gene is located close to the head, as it is in pythons. Pythons, as a result of this placement, have virtually no neck.

While the body regions of vertebrates, such as mice, are not as distinct as those of flies and other insects, Hox genes determine their body regions during embryological development. The Hoxc6 gene in mice delimits the thoracic region, which is indicated by the thoracic vertebrae.

Humans, being vertebrates, also have a Hoxc6 gene, which determines the location of the thoracic region. Humans have a neck of intermediate length when compared to geese and pythons; the Hoxc6 gene is closer to the head in humans than in geese, but is lower than in pythons. The Hoxc6 gene is responsible not just for determining the location of the thorax; in humans, this gene determines the development of the entire thoracic region, including mammary glands.

FIGURE 3.19 Homeotic (Hox) Genes Discovered in 1983 by Swiss and American researchers, these regulatory genes are coded to produce proteins that turn on many other genes, in particular those that determine the regions of the body during prenatal development. Without these genes, or if there are mutations in these genes, body development may be altered. For example, a mutation in the Hox genes of a fruit fly can cause a leg instead of an antenna to grow from the head.

polymorphism Refers to the presence of two or more alleles at a locus and where the frequency of the alleles is greater than 1% in the population.

law of segregation Mendel’s first law, which asserts that the two alleles for any given gene (or trait) are inherited, one from each parent; during gamete produc- tion, only one of the two alleles will be present in each ovum or sperm.

microsatellites Also called short tandem repeats (STRs); refers to sequences of repeated base pairs of DNA, usually no more than two to six. If repeated exces- sively, they are often associated with neu- rological disorders, such as Huntington’s chorea.

individualistic, forming a unique DNA signature for each person. Microsatellites have quickly become the most important tool for individual identification, and they have proven especially valuable in forensic science. For example, they have been used to identify victims of the 9/11 attacks as well as genocide and mass- murder fatalities in the Balkans, Iraq, and Argentina.

GENOTYPES AND PHENOTYPES: GENES AND THEIR EXPRESSION The two alleles, whether they are chemically identical (e.g., AA) or chemically different (e.g., AO), identify the genotype— the actual genetic material in the pair of homologous chromosomes. Chemically identical alleles are called homozygous.

Red blood cells

Antigens

Antibody

Agglutination

(a)

(b)

FIGURE 3.20 Antibody–Antigen System When a person receives a blood transfusion, the transfused blood must have the same blood type as the recipient’s own to avoid an antibody– antigen reaction. (a) Each red blood cell has structures on its surface, known as antigens, that identify the cell as being type A, B, AB, or O. If the wrong type of blood is given to a person, the body’s immune system recognizes the new antigens as foreign. Special proteins called antibodies are then produced in the blood in response to the “invaders.” (b) The antibodies attach themselves to the foreign antigens, causing agglutination, or clumping, of the blood cells. Because the coagulated blood cannot pass through blood vessels properly, the recipient’s tissues do not receive the blood they need. If not treated, the person might die.

For all the blood types in the ABO blood group system, Table 3.2 shows the antigens, antibodies, and acceptable and unacceptable blood types. For example, type A blood, which can result from AO alleles or AA alleles, has A antigens on its surface and anti- B antibodies, which will react with B or AB blood. (Genotypes and phenotypes are defined and discussed below.)

antigens Specific proteins, on the surface of cells, that stimulate the immune sys- tem’s antibody production.

antibodies Molecules that form as part of the primary immune response to the presence of foreign substances; they attach to the foreign antigens.

homozygous Refers to the condition in which a pair of alleles at a single locus on homologous chromosomes are the same.

TABLE 3.2 The ABO Blood Group System

Phenotypes Genotypes Antigens Antibodies Unacceptable Blood Types

Acceptable Blood Types

A AO, AA A anti-B B, AB A, O

B BO, BB B anti-A A, AB B, O

AB AB A, B none none (universal recipient) A, B, AB, O

O OO none (universal donor) anti-A, anti-B A, B, AB O

Polymorphisms: Variations in Specific Genes | 63

64 | CHAPTER 3 Genetics: Reproducing Life and Producing Variation

Chemically different alleles are called heterozygous. When alleles are hetero- zygous, the dominant one will be expressed in the phenotype— the visible mani- festation of the gene. For example, individuals who are AA or who are AO have the same phenotype— A expresses dominance over O, and both individuals are blood type A. The recessive allele is not expressed. When you know simply that a person’s blood type is A, you cannot tell whether that person’s genotype is AA or  AO.  Rather, the blood type refers to the phenotype and not the genotype. If the person is AO, then the O allele is hidden because that allele is recessive. For the recessive allele to be expressed, each of the homologous chromosomes must have the recessive allele. For example, the alleles for type O blood are OO. For a

Pure red sweet peas (RR)

First (F1) Generation

Pure white sweet peas (rr)

R

100% Rr = red

r

r

Hybrid red (Rr)

Hybrid red (Rr)

R

Hybrid red (Rr)

Hybrid red (Rr)

Hybrid red (Rr)

Second (F2) Generation

Hybrid red (Rr)

R

25% RR = red, 50% Rr = red, 25% rr = white

R

r

Hybrid red (Rr)

Pure white (rr)

r

Pure red (RR)

Hybrid red (Rr)

The pure red parent has two R (red) alleles, so it can contribute only the R allele.

Each parent is a hybrid, with one R allele and one r allele.

The pure white parent has two r (white) alleles, so it can contribute only the r allele.

All the offspring will have Rr alleles. Since R (red) is dominant to r (white), all offspring will be red.

There is a 25% chance for an offspring plant with RR alleles (red), a 25% chance for one with rr alleles (white), and a 50% chance for one with Rr alleles (red).

FIGURE 3.21 Law of Segregation Mendel’s first law, the law of segregation, declares that the mother and father contribute equally to an offspring’s genetic makeup. For each gene, a person has two alleles (which can be the same or different). One allele is from the person’s mother, and one is from the person’s father.

Remember that meiosis (see Figure 3.13) creates four gametes, each of which has only one set of chromosomes, no pairs. Each gamete, having this one set, can pass on only one allele for each gene. If the gamete that the father contributes to fertilization has the allele for brown hair, for example, that is the only allele the father will contribute to the offspring. The other allele, for brown or a different color, will come from the mother.

heterozygous Refers to the condition in which a pair of alleles at a single locus on homologous chromosomes are different.

The Complexity of Genetics | 65

person to have type O blood, both alleles in the pair of homologous chromosomes have to be O.

Sometimes alleles exhibit codominance, where neither chemically different version dominates the other. In the ABO blood group system, the A and B alleles are codominant and both are expressed. If someone has type AB blood, you know that person’s phenotype and genotype.

The Complexity of Genetics Since the discovery of how the genetic code works (see chapter  2), the general impression about genes has been that they represent specific locations of DNA coded to produce specific proteins. Much of the field of genetics, including anthropological genetics, is based on this “one gene– one protein” model. How- ever, the relationship between genes and their physical expression turns out to be considerably more complex than previously thought. For example, many traits are polygenic, affected by genes at two or more loci. On the other hand, pleiotropy may be operating, whereby a single gene can have multiple effects. One example of pleiotropic effects is Marfan syndrome (see Figure  3.18). This condition is a dominant collagen disorder caused by a gene on chromosome 15. Collagen is a major protein, representing 25%–35% of all protein in the body. Because colla- gen is found in so many types of body tissues— for example, skeletal, visual, and cardiovascular— this single gene’s effects are pervasive.

The physical manifestations also may be influenced by environmental factors. In humans, thousands of complex phenotypes— such as birth weight, height, skin color, head form, tooth size, and eye shape— have multiple genetic components and are influenced by environmental factors. Many other complex phenotypes— such as autism spectrum and other behavioral and cognitive disorders— may have envi- ronmental influences.

Scientists have long understood that environment plays an important role in the physical manifestations of various aspects of one’s genome. For example, environmental factors affecting the mother can also affect the developing fetus. If the fetus is female, then those offspring resulting from the developing ova of that fetus may also be affected. In this way, environmental factors operating at a given point in time can affect the health and well- being of subsequent generations. Such epigenetic effects represent potentially heritable changes in behavior or biology but without alteration in the DNA sequence. These changes alter the way that DNA is regulated, without altering the DNA itself. A new and exciting area of research is showing that epigenetic mechanisms occurring within cells may be activated by a variety of behavioral and environmental factors, such as smoking, alcohol consumption, nutrition, physical activity, temperature extremes, and disease. In this regard, regulation of DNA in the offspring may be altered due to epigenetic phenomena contributing to birth defects and other outcomes.

The interaction between the environment and the genes of the mother and her embryo, from conception to birth, has considerable impact on the normal growth of the fetus as well as risk for disease following birth. Indeed, obesity and some birth defects, common diseases, and cancers appear to be influenced by epigene- tic factors. For example, key nutrients— including vitamins A, B3, C, and D— play roles in regulating DNA. An insufficiency of these nutrients is linked to diabetes, atherosclerosis, and cancer. By investigating the epigenetics of health and behavior, scientists have opened up a pathway toward understanding factors that influence

codominance Refers to two different alleles that are equally dominant; both are fully expressed in a heterozygote’s phenotype.

polygenic Refers to one phenotypic trait that is affected by two or more genes.

epigenetic Refers to heritable changes but without alteration in the genome.

66 | CHAPTER 3 Genetics: Reproducing Life and Producing Variation

parent and offspring health. In short, researchers have helped show how environ- ment interacts with the genome across generations.

For some phenotypic traits, scientists can determine only the relative pro- portions of genetic and environmental contributions. A trait’s heritability, the proportion of its variation that is genetic, can be calculated this way:

genetic variation heritability (H2) = (genetic variation + environmental variation)

Heritability estimates are presented as values ranging from 0, where none of the variation is genetic in origin, to 1, where all of the variation is genetic. In traits with heritability estimates greater than .5, most of the variation is genetic. For example, in the United States, the heritabilities for height and weight are estimated to be .6 and .3, respectively. Tooth size has among the highest levels of heritability, about .7, and brain size and fingerprints are even higher, at .9. Physical anthropologists and other evolutionary biologists are very interested in heritability for one simple reason: because only heritable traits respond to natural selection, they are the primary driving force of evolution.

Measurement of heritability, however, is complicated by pleiotropy— a single allele can have multiple effects. In fact, most complex traits are polygenic and pleiotropic (Figure 3.22).

The DNA Revolution has made it possible to understand in much greater detail the underlying principles of inheritance laid out so eloquently by Gregor Mendel a century and a half ago. In presenting the great breadth of knowledge about how genetic variation is transmitted from parents to offspring and maintained devel- opmentally within individuals, this chapter has laid the groundwork for the topic of the next chapter, the study of genetic change in populations.

heritability The proportion of phenotypic variation in a population that is due to genetic variation across individuals rather than variation in the environmental condi- tions experienced by the individuals. This proportion can vary from one population to another, and thus it provides a sense of the contribution of genetic influence for each population.

Each gene has a distinct biological effect.

Gene Effect

Polygenic trait: many genes contribute to a single effect.

Gene Effect

Pleiotropy: one gene has multiple biological effects.

(a) (b)

(c) (d)

Gene Effect

Polygenic traits and pleiotropy.

Gene Effect

FIGURE 3.22 Polygenic Traits and Pleiotropic Genes (a) Mendel’s simple rules of inheritance (b) do not apply when one trait is affected by many genes. Eye color, for example, is determined by at least three genes. Because this trait is polygenic, some children’s eye colors are very different from their parents’. (c) Pleiotropic genes affect more than one physical trait. The PKU allele, for example, affects mental abilities and the coloration of hair and skin. A person who inherits this allele will have the disease phenylketonuria, in which a missing enzyme leads to mental retardation as well as reduced hair and skin pigmentation. (d) One trait can be affected by several genes, and each of those genes can affect several other traits as well.

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A N S W E R I N G T H E B I G Q U E S T I O N S

C H A P T E R   3 R E V I E W

What is the genetic code? • The genetic code is DNA, packaged in individual

chromosomes. • One type of DNA exists in the cell’s nucleus (nuclear

DNA), and the other type exists in the cytoplasm (mitochondrial DNA). Nuclear DNA provides most of the genetic code.

What does the genetic code (DNA) do? • DNA serves as the chemical template for its own

replication. DNA replication is the first step toward the production of new cells: somatic cells and gametes. — Mitosis results in the production of two identical

somatic cells. In humans, each parental or daughter cell has 46 chromosomes in 23 homologous pairs.

— Meiosis results in the production of four gametes. In humans, each parental cell has 46 chromosomes, and each gamete has 23 chromosomes.

• DNA serves as the chemical template for the creation of proteins. — Proteins are combinations of amino acids. They

are responsible for all physical characteristics (structural proteins), the regulation (regulatory or functional proteins) of activities within cells (enzymes), the regulation of activities between cells (hormones), and the fighting of foreign antigens (antibodies). Thus, proteins comprise the entire body and determine all of its functions, from conception through maturity.

— The two types of proteins are governed by the two corresponding types of genes, structural and regulatory.

— Hox genes are regulatory genes that control the development of body parts, such as limbs and internal organs, and their locations relative to each other.

What is the genetic basis for human variation? • Each chromosome has a linear sequence of

nucleotides that are coded to produce specific bodily structures and functions. These linear sequences are genes, and each gene has a particular locus on each chromosome— and the same locus on the like (homologous) chromosome.

• Each pair of homologous chromosomes consists of a paternal chromosome and a maternal chromosome.

• An individual’s genotype, or actual genetic composition, is identified on the basis of two alleles, one from the father and one from the mother. Alleles can be chemically identical or chemically different. The genotype is expressed physically as a phenotype.

• For most traits, no direct map yet exists for the translation of genotype to phenotype. That is, one gene may result in the construction of one functional protein, or multiple polypeptides each produced by a different gene may form the functional protein. The genetic basis for such a protein, therefore, is difficult to determine.

• Most physical characteristics are determined by more than one gene (polygenic), and some genes can have multiple effects (pleiotropy).

• Epigenetics is the source of a new revolution in our understanding of how genes work. By viewing the profound impact of environment on gene function, an impact created by both biological and cultural circumstances, we can gain new insight into inheritance, health, and behavior.

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K E Y T E R M S adenine adenosine triphosphate (ATP) amino acids antibodies anticodons antigens autosomes coding DNA codominance codons complementary bases crossing- over cytoplasm cytosine diploid cell epigenetic essential amino acids eukaryotes free- floating nucleotides gametes genome guanine haplogroups haploid cell haplotypes heritability

heteroplasmic heterozygous homeotic (Hox) genes homologous homoplasmic homozygous karyotype law of independent assortment law of segregation linkage locus matriline meiosis messenger RNA (mRNA) microsatellites mitochondria mitosis monosomy noncoding DNA nondisjunctions nucleotide nucleus paleogenetics patriline peptide bond polygenic

polymerase chain reaction (PCR) polymorphism polypeptide prokaryotes recombination regulatory genes regulatory proteins replication ribonucleic acid (RNA) ribosomal RNA (rRNA) ribosomes sex chromosomes single nucleotide polymorphisms (SNPs) somatic cells structural genes structural proteins thymine transcription transfer RNA (tRNA) translation translocations triplets trisomy uracil zygote

E V O L U T I O N R E V I E W Insights from Genetics

Synopsis DNA is often described as a genetic blueprint as it encodes the plan for an organism’s traits and ensures that these traits are passed on to future generations. One of the major func- tions of the DNA molecule is replication: creating identical copies of itself. The reliability of this process influences evolution by making variation heritable—that is, traits will be passed on to offspring, who will be similar to their parents. The second major function of DNA is directing protein synthesis, which is how genotype (genetic code) is translated to phenotype (physical expression of this code). Protein synthesis is the basis for the traits that allow organisms to interact with their environment and undergo natural selection. As our knowledge of molecular genetics has expanded, so has our appre- ciation for its complexity. Many traits are polygenic (influenced by

more than one gene), and many genes are pleiotropic (operating on more than one trait). Furthermore, epigenetic (environmental, nonge- netic) phenomena can alter DNA regulation and phenotype without altering the DNA sequence itself. Thus, genetics both complicates and illuminates our understanding of human variation and evolution.

Q1. What are the two types of cell division? How does each type affect individual genetic variation?

Q2. What is recombination? How does the effect of recombination differ from that of mutation or a random change in the DNA sequence?

Q3. Given the modern “DNA Revolution” and our growing know- ledge of humans from a genetic perspective, why is it

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still important for physical anthropologists to study physical remains (e.g., bones and teeth) when testing hypotheses about evolution and variation among ourselves and our closest living and fossil relatives?

Hint Think about the types of remains available for living and fossil organisms and about how genetics are related to physical characteristics.

Q4 . Consider various human characteristics, such as height, weight, skin color, head form, and eye shape. Are the phe- notypic expressions of these characteristics discontinuous

(able to be assigned to discrete categories) or continuous (on a continuum rather than separable into discrete categories)? What might they tell us about the mechanisms behind human variation?

Q5. Epigenetic phenomena are environmental factors that affect the way DNA is regulated and may affect future generations. How do epigenetic phenomena differ from Lamarckian inheritance of acquired characteristics (discussed in the previous chapter)?

Hint Compare the heritability of characteristics involved in epigenetics and Lamarckism.

A D D I T I O N A L R E A D I N G S

Carey, N. 2012. The Epigenetics Revolution: How Modern Biology Is Rewriting Our Understanding of Genetics, Disease, and Inheritance. New York: Columbia University Press.

Kaestle, F. A. 2010. Paleogenetics: Ancient DNA in anthropology. Pp. 427–441 in C. S. Larsen, ed. A Companion to Biological Anthro- pology. Chichester, UK: Wiley- Blackwell.

Mielke, J. H., L. W. Konigsberg, and J. H. Relethford. 2006. Human Biological Variation. New York: Oxford University Press.

Portugal, F. H. and J. S. Cohen. 1977. A Century of DNA: A History of the Discovery of the Structure and Function of the Genetic Sub- stance. Cambridge, MA: MIT Press.

Relethford, J. H. 2003. Reflections of Our Past: How Human History Is Revealed in Our Genes. Boulder, CO: Westview Press.

Sapolsky,  R.  M.  2004. Of mice, men, and genes. Natural History May: 21–24, 31.

Sykes,  B.  2001. The Seven Daughters of Eve: The Science That Reveals Our Genetic Ancestry. New York: Norton.

Weiss,  M.  L.  and  J.  Tackney. 2012. An introduction to genetics. Pp. 53–98 in S. Stinson, B. Bogin, and D. O’Rourke, eds. Human Biology: An Evolutionary and Biocultural Perspective, 2nd ed. Hobo- ken, NJ: Wiley- Blackwell.

E V O L U T I O N R E V I E W

THE KEY DRIVER OF EVOLUTION is natural selection. Members of species having genetic variation that enhances survival to reproductive age will tend to live to reproductive age. In these three very different animals— the leafy sea dragon, deer mouse, and peppered moth— there is selection for genes con- trolling for pigmentation and other attributes of body phenotype. These pheno- types make it difficult for predators to see these prey. This “visual” selection is commonplace worldwide now, as it must have been in the past.

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4 What causes evolutionary (genetic) change?

How is evolutionary (genetic) change measured, and how is the cause determined?

Genes and Their Evolution Population Genetics

One of the great stories about genetics comes not from a research program of a famous scientist in charge of a large laboratory filled with technicians, grad-uate students, and postdoctoral fellows and funded by a multimillion- dollar grant but rather from a student with a simple hypothesis and a passionate interest in testing a hypothesis. At Oxford University in the late 1940s, a 20-something Anthony Allison was finishing his coursework in basic sciences and was about to start his clinical medical training. Allison had grown up in Kenya; his interest in anthropology reflected his intellectual curiosity, but his desire to become a doctor was motivated by an ambi- tion to help improve native Kenyans’ quality of life. While at Oxford, he was exposed to the ideas of the English scientists R. A. Fisher and J. B. S. Haldane and the American scientist Sewall Wright, pioneers of the new field of population genetics and advocates of the novel idea that gene frequencies were tied to natural selection.

Following a bout of malaria, Allison decided to help Kenyans (and other peoples) by seeking a cure for this disease. In 1949, he joined an expedition to document blood groups and genetic traits in native Kenyans. On this expedition, Allison discov- ered that in areas affected by malaria, especially along Kenya’s coast (southeast) and near Lake Victoria (southwest), a remarkably high 20%–30% of the population carried the gene for sickle- cell anemia. But in the highlands (west), where there was no malaria, less than 1% of the people carried the gene. In what he described as a “flash of inspiration,” he hypothesized that individuals with the sickle- cell allele were resistant to malaria and that natural selection was operating on the gene. But how? he wondered.

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72 | CHAPTER 4 Genes and Their Evolution: Population Genetics

Before pursuing these ideas, Allison completed his medical education. In 1953, with just enough money to buy passage back to Kenya and for food and simple lodging, he spent a year researching the relationship between malaria and sickle- cell anemia. He generated lab and field data, looking at malaria infection rates in people with and without the sickle- cell allele. His results showed that carriers of the gene are much more likely to survive malaria than are noncarriers. Natural selection was favoring the carriers.

The next year, Allison published three landmark scientific articles in rapid succes- sion, laying out the proof for his hypothesis. Gene frequencies are tied to natural selec- tion: carriers of the sickle- cell allele survive longer and produce more offspring than do noncarriers. In Allison’s words, “disease is an agent of natural selection.” Although his ideas met with strong skepticism, eventually Allison’s hypothesis was accepted by most scientists. His research enabled generations of geneticists and anthropologists to further investigate genes and their evolution, all of these researchers asking why some gene frequencies remain the same while others change over time.

Human populations exhibit some remarkable biological differences, and the sci- ence of genetics helps biologists answer questions about those differences. The questions and the answers are founded on Darwin’s discovery that phenotypes— the physical manifestations of genes— change over time. In addition, Mendel’s research on garden peas revealed how the inheritance of genes produces variation in phe- notypes. These two revolutionary scientific discoveries inform our understanding of biological variation and its evolution.

Before considering this chapter’s big question, we need to look at populations and species, the units that evolutionary biologists work with.

Demes, Reproductive Isolation, and Species To show how genetic variation is produced, the previous chapter focused on the individual and the transmission of genes from parents to offspring. When phys- ical anthropologists and geneticists study the genetics of individuals, they focus on the reproductive population, or deme: members of a species that produce offspring. That is, evolution is about groups of organisms that have the potential to reproduce. When physical anthropologists talk about populations, they often refer to the gene pool, which is all the genetic material within a population. When geneticists talk about the gene pool, they are even more specific, referring to all the variation within a specific genetic locus. For example, some people carry the sickle- cell allele and some do not.

The concept of the breeding population is also central to the definition of species. A species is comprised of all the populations (and their individual mem- bers) that are capable of breeding with each other and producing viable (fertile) offspring. Species, therefore, are defined on the basis of reproductive isolation (Figure  4.1). In biological terms, if two populations are reproductively isolated, members of one population cannot interbreed with members of the other. Repro- ductive isolation is largely related to geographic isolation. If two populations of the same species become isolated, such as by a mountain range or a large body

deme A local population of organisms that have similar genes, interbreed, and produce offspring.

gene pool All the genetic information in the breeding population.

reproductive isolation Any circumstance that prevents two populations from interbreeding and exchanging genetic material, such as when two populations are separated by a large body of water or a major mountain range.

Demes, Reproductive Isolation, and Species | 73

of water, enough  genetic differences could accumulate for two entirely different species to emerge.

In the living world, we can observe members of a species to verify that they can produce offspring. Obviously, we cannot do this with fossils. Rather, we have to infer reproductive isolation in fossil populations on the basis of geographic dis- tance and the physical resemblance between fossils. Fossil remains that share the same characteristics in morphology of teeth and bones likely represent members of the same species (Figure 4.2). (This important concept will inform the discussion of primate evolution in chapters 9–13. Fossils are the subject of chapter 8.)

(a)

(b) (c)

FIGURE 4.1 Reproductive Isolation (a) This map depicts the distribution of two related bird species: (b) ostriches are found in Africa, while (c) emus are found in Australia. These two species share a common ancestor, but the ocean between the two groups prevented them from interbreeding for thousands of years. Eventually, this geographic isolation led to reproductive isolation and two separate species.

74 | CHAPTER 4 Genes and Their Evolution: Population Genetics

Population genetics (see “The Evolutionary Synthesis, the Study of Popula- tions, and the Causes of Evolution” in chapter 2) is the study of changes in genetic material— specifically, the change in frequency of alleles (genes). Genes are the records from which evolution is reconstructed, both over the course of a few genera- tions (microevolution) and over many generations (macroevolution; Figure 4.3). Geneticists strive to document genetic change and to explain why it occurred. Such documentation and explanation are the central issues of evolutionary biology. Pop- ulation geneticists, physical anthropologists, and other evolutionary biologists tend to focus on genetic change over time. For example, if a trait in a population has two alleles, A and a, and the parent generation is 60% A and 40% a and the next generation is 65% A and 35% a, scientists would want to know why the evolution occurred— why the frequency of the A allele increased in the population.

Just as interesting, however, are instances in which frequency does not change over time— that is, when the frequencies of a population’s alleles for a particular

FIGURE 4.2 Living Fossils Fossilized remains might represent animals and plants that lived thousands or millions of years ago, but a number of such organisms have counterparts that live today. Compare the forms of the following organisms: (a) living horseshoe crab and (b) fossil of Mesolimulus walchii, the ancestor to the modern horseshoe crab; (c) living cockroach and (d) a 49  million– year- old fossil cockroach; (e) living American opossum (“playing possum,” i.e., feigning death) and (f) fossil skull of Didelphis albirentris, an ancestor to modern opossums. Which features have been maintained and which have been lost?

(a) (c)

living fossil

(b) (d)

(e) (f)

microevolution Small- scale evolution, such as changes in allele frequency, that occurs from one generation to the next.

macroevolution Large- scale evolution, such as a speciation event, that occurs after hundreds or thousands of generations.

FIGURE 4.3 Microevolution and Macroevolution (a) Microevolution is change in gene frequency over a few generations. For example, the beetles in this diagram have either of two colors, represented by two alleles. In the first generation, 75% of the color alleles are green and 25% are brown. In the second generation, 71% of the color alleles are green and 29% are brown. Thus, the frequencies of the green and brown alleles have undergone a microevolutionary change. (b) Macroevolution is substantial change over many generations, the creation of new species. For example, over 60 million years, the eohippus— a small, dog- sized animal, with multitoed feet, that inhabited rainforests— evolved into the modern horse. Among the species’ large- scale changes were increases in overall body size and height as well as the loss of toes. Horses’ single- toed hooves enable them to run more efficiently in the open grasslands they naturally inhabit.

First generation

75% 25%

Second generation

×

×

×

Modern horse

Pliohippus

Merychippus

Mesohippus

Eohippus

height 1.6 m (5.25 ft)

height 1.0 m (3.28 ft)

height 1.0 m (3.28 ft)

height .6 m (1.97 ft)

height .4 m (1.31 ft)

1 m

ya 10

m ya

30 m

ya 40

m ya

60 m

ya

71% 29%

(b)

(a)

Demes, Reproductive Isolation, and Species | 75

Population genetics (see “The Evolutionary Synthesis, the Study of Popula- tions, and the Causes of Evolution” in chapter 2) is the study of changes in genetic material— specifically, the change in frequency of alleles (genes). Genes are the records from which evolution is reconstructed, both over the course of a few genera- tions (microevolution) and over many generations (macroevolution; Figure 4.3). Geneticists strive to document genetic change and to explain why it occurred. Such documentation and explanation are the central issues of evolutionary biology. Pop- ulation geneticists, physical anthropologists, and other evolutionary biologists tend to focus on genetic change over time. For example, if a trait in a population has two alleles, A and a, and the parent generation is 60% A and 40% a and the next generation is 65% A and 35% a, scientists would want to know why the evolution occurred— why the frequency of the A allele increased in the population.

Just as interesting, however, are instances in which frequency does not change over time— that is, when the frequencies of a population’s alleles for a particular

FIGURE 4.2 Living Fossils Fossilized remains might represent animals and plants that lived thousands or millions of years ago, but a number of such organisms have counterparts that live today. Compare the forms of the following organisms: (a) living horseshoe crab and (b) fossil of Mesolimulus walchii, the ancestor to the modern horseshoe crab; (c) living cockroach and (d) a 49  million– year- old fossil cockroach; (e) living American opossum (“playing possum,” i.e., feigning death) and (f) fossil skull of Didelphis albirentris, an ancestor to modern opossums. Which features have been maintained and which have been lost?

(a) (c)

living fossil

(b) (d)

(e) (f)

microevolution Small- scale evolution, such as changes in allele frequency, that occurs from one generation to the next.

macroevolution Large- scale evolution, such as a speciation event, that occurs after hundreds or thousands of generations.

FIGURE 4.3 Microevolution and Macroevolution (a) Microevolution is change in gene frequency over a few generations. For example, the beetles in this diagram have either of two colors, represented by two alleles. In the first generation, 75% of the color alleles are green and 25% are brown. In the second generation, 71% of the color alleles are green and 29% are brown. Thus, the frequencies of the green and brown alleles have undergone a microevolutionary change. (b) Macroevolution is substantial change over many generations, the creation of new species. For example, over 60 million years, the eohippus— a small, dog- sized animal, with multitoed feet, that inhabited rainforests— evolved into the modern horse. Among the species’ large- scale changes were increases in overall body size and height as well as the loss of toes. Horses’ single- toed hooves enable them to run more efficiently in the open grasslands they naturally inhabit.

First generation

75% 25%

Second generation

×

×

×

Modern horse

Pliohippus

Merychippus

Mesohippus

Eohippus

height 1.6 m (5.25 ft)

height 1.0 m (3.28 ft)

height 1.0 m (3.28 ft)

height .6 m (1.97 ft)

height .4 m (1.31 ft)

1 m

ya 10

m ya

30 m

ya 40

m ya

60 m

ya

71% 29%

(b)

(a)

76 | CHAPTER 4 Genes and Their Evolution: Population Genetics

trait are in a state of equilibrium. For example, in areas of West Africa where malaria is common, the frequency of the sickle- cell allele remains relatively con- stant. What factors— forces of evolution— account for deviations from equilibrium?

Hardy- Weinberg Law: Testing the Conditions of Genetic Equilibrium In 1908, Godfrey Hardy (1877–1947), an English mathematician, and Wilhelm Weinberg (1862–1937), a German obstetrician, independently recognized that some alleles are in a state of equilibrium. If no mutation or natural selection or gene flow occurs, if the population is large, if mating is random, and if all members of the population produce the same number of offspring, then genotype frequencies at a single gene locus will remain the same after one generation. Moreover, the equilibrium frequencies will be a function of the allele frequencies at the locus. This is called the Hardy- Weinberg law of equilibrium. In the simplest case (Table 4.1), a single locus has A (dominant) and a (recessive) alleles, with respective frequencies of p and q. In assessing the population as a whole, it is assumed that males and females have both alleles. The Hardy- Weinberg law predicts the geno- type frequencies for the next generation after one mating, where p2 is the genotype frequency for the AA homozygous alleles, 2pq is the genotype frequency for the Aa (heterozygous) alleles, and q2 is the genotype frequency for the aa homozygous alleles. In other words, the total population (100%) should be the sum of the frequencies of three genotypes, expressed by the simple mathematical equation p2 + 2pq + q2 = 1. If a hypothetical population were 60% A ( p = .6) and 40% a (q = .4), then the genotype frequencies in the next generation would work out to AA = .36, Aa = .48, and aa = .16. The frequencies can be expressed as decimals or percentages, but they are expressed most often as decimals. Since the three genotypes are the only genotypes for the gene in question in the population, the frequencies must add up to 1 or 100%. So, if the frequency of AA is .36 (or 36%), the frequency of Aa is .48 (or 48%), and the frequency of aa is .16 (or 16%), together they add up to 1 (or 100%).

In the absence of evolution, the frequencies of the genotypes will in theory remain the same forever. In this way, the Hardy- Weinberg equilibrium hypothe- sizes that gene frequencies remain the same because no evolutionary change takes place (Figure 4.4).

By determining the genotype frequencies for a population at different points in time, however, the Hardy- Weinberg equation establishes expectations as to whether evolution is operating on a particular gene. If the genotype frequencies

equilibrium A condition in which the sys- tem is stable, balanced, and unchanging.

TABLE 4.1 Punnett Square for Hardy- Weinberg Equilibrium

Females

A (p) a (q)

Males A (p) AA (p2) Aa (pq)

a (q) Aa (pq) aa (q2)

Hardy- Weinberg law of equilibrium A math- ematical model in population genetics that reflects the relationship between frequencies of alleles and of genotypes; it can be used to determine whether a population is undergoing evolutionary changes.

Mutation: The Only Source of New Alleles | 77

change from one generation to the next, the population is not in equilibrium— it is evolving. If the frequencies remain the same, the population is in equilibrium— the population is not evolving, at least with respect to the locus being studied.

What might cause a population to change its allele frequencies and go out of equilibrium? As noted in chapters  2 and 3, genes are passed from generation to generation by interbreeding within populations in particular and among members of the same species in general, and genetic changes result from one or a combina- tion of the four forces of evolution: mutation, natural selection, genetic drift, and gene flow.

Mutation: The Only Source of New Alleles During cell reproduction, DNA almost always replicates itself exactly. Sometimes, however, the replication process produces an error or a collection of errors in the DNA code. If the problem is not at once detected and corrected by a set of enzymes that monitor DNA, a mutation results. The mutation can be any heritable change in the structure or amount of genetic material.

FIGURE 4.4 Gene Frequencies in Equilibrium As this Punnett square illustrates, the Hardy- Weinberg equilibrium captures gene frequencies in a static moment, when no evolutionary change is taking place. Crossing the males (sperm pool) and females (egg pool) of the population produces theoretical genotype frequencies of the next generation.

Once evolutionary change takes place, the actual genotype frequencies will differ significantly from the theoretical genotype frequencies expressed in this Punnett square. For example, if the population later turns out to be 5% AA, 65% aa, and 30% Aa, an evolutionary force has most likely altered its genotype frequencies.

A p = .6

Sperm pool

a q = .4

A p = .6

a q = .4

Aa pq .24

Aa pq .24

Eg g

po ol

AA p2

0.36

aa p2

0.16

AA p2

.36

aa q2

.16

The allele frequencies for males and females in this population are the same: p (frequency of A allele) is .6 and q (frequency of a allele) is .4.

Approximately 36% of the offspring will have the genotype AA. The estimate is made by multiplying the male p (frequency of A allele = .6) with the female p (.6). Thus, p × p = p2, and .6 × .6 = .36. The frequency of the AA genotype is represented by p2.

Approximately 48% of the offspring population will have the genotype Aa. This estimate is made by multiplying the male p (.6) with the female q (.4) and the male q (.4) with the female p (.6). Thus, p × q = pq and q × p = qp; .6 × .4 = .24 and .4 × .6 = .24. Since both p × q and q × p must be included, the two results are added together. 2pq = 2 × .24 (or .24 + .24) = .48. The frequency of the Aa genotype is represented by 2pq.

Approximately 16% of the offspring will have the geno- type aa. This estimate is made by multiplying the male q (frequency of a allele = .4) with the female q (.4). Thus, q × q = q2, and .4 × .4 = .16. The frequency of the aa genotype is represented by q2.

78 | CHAPTER 4 Genes and Their Evolution: Population Genetics

Because so much of any person’s DNA is noncoding (see “Producing Proteins: The Other Function of DNA” in chapter 3), many mutations do not affect the indi- vidual’s health, well- being, or survival. A new sequence of coding DNA that results from mutation may have profound consequences, positive or negative. For example, the mutation might code the DNA for a protein with an altered or different func- tion from that performed by the protein coded for in the original parent strand of DNA, or the mutation might create a sequence that results in either no protein or an abnormal protein (Figure 4.5). Mutations occur at random and can occur in any cell, but the ones with consequences for future generations take place in gametes. Gametes may transfer mutations to offspring, depending on what happens during meiosis in the parents. Regardless of their causes or outcomes, mutations are the only source of new genetic variation in a population.

Mutations involving incorrect base pairing are called point mutations. A syn- onymous point mutation creates an altered triplet in the DNA, but the alteration carries with it the original amino acid. Because the amino acid is the same, the pro- tein formed is the same. A nonsynonymous point mutation results in a matchup that brings along a different amino acid. Such a mutation can have dramatic results for the individual carrying it. For example, a mutation on human chromosome 11 results in a GUG codon instead of a GAG codon. The GUG codon is encoded to produce the amino acid valine, whereas the GAG codon would have normally led to the production of glutamic acid. This substitution leads to the abnormal hemo- globin that results in sickle- cell anemia (discussed later in this chapter).

As a result of the shifting base pairs caused by base insertion, the reading frame of a gene is altered or stopped entirely. This frameshift mutation produces a protein having no function. Such a mutation usually involves a small part of the DNA sequence, often just a base pair or a relatively limited number of base pairs.

Other kinds of mutations can affect far more of the genome. Transposable ele- ments are genes that can copy themselves to entirely different places along the DNA sequence. If such a gene inserts itself into another gene, it can fundamentally alter the other gene, doing real damage. If, as is strongly likely, the gene transposes itself to a noncoding area of the DNA sequence, little or no significant alteration will occur.

Large parts of DNA sequences or entire chromosomes can be affected by muta- tions. An entire piece of chromosome can be moved to another chromosome, can be placed differently on the same chromosome, or can be positioned in a chromo- some backward. The impacts of these mutations are highly variable and depend on the mutations’ loci.

In the most extreme mutations, entire chromosomes can be duplicated (a tri- somy) or lost altogether (a monosomy). Examples of trisomies are Down syndrome, with its extra twenty- first chromosome (see “Meiosis: Production of Gametes [Sex Cells]” in chapter  3) and Klinefelter’s syndrome, a common sex chromosome variant that appears in about 1 of 500–1,000 births.

All mutations fall into either of two types: spontaneous mutations have no known cause (Figure 4.6); induced mutations are caused by specific environmen- tal agents, usually associated with human activity. These agents, or mutagens, are increasingly becoming known. For example, ionizing radiation ( X- rays) and various toxic chemicals have been linked to mutations in animals and humans. Most mutations are spontaneous, however, and are simply DNA copying errors. The human mutation rate is higher in male sex cells (sperm) than in female sex cells (eggs) but is generally on the order of one per million per nucleotide per generation. The human genome includes about 3 billion base pairs, about 1.5% of which are protein- coding, so the average mutation rate in humans is .45 mutations

point mutations Replacements of a single nitrogen base with another base, which may or may not affect the amino acid for which the triplet codes.

synonymous point mutation A neutral point mutation in which the substituted nitrogen base creates a triplet coded to produce the same amino acid as that of the original triplet.

nonsynonymous point mutation A point mutation that creates a triplet coded to produce a different amino acid from that of the original triplet.

frameshift mutation The change in a gene due to the insertion or deletion of one or more nitrogen bases, which causes the subsequent triplets to be rearranged and the codons to be read incorrectly during translation.

transposable elements Mobile pieces of DNA that can copy themselves into entirely new areas of the chromosomes.

Klinefelter’s syndrome A chromosomal trisomy in which males have an extra X chromosome, resulting in an XXY con- dition; affected individuals typically have reduced fertility.

spontaneous mutations Random changes in DNA that occur during cell division.

induced mutations Refers to those muta- tions in the DNA resulting from exposure to toxic chemicals or to radiation.

mutagens Substances, such as toxins, chemicals, or radiation, that may induce genetic mutations.

T

A

Base substitution

(a) Base substitution

(b) Base insertion

A base substitution, the simplest kind of mutation, occurs when a single nitrogen base is substituted by another base. Here, thymine is being replaced by cytosine.

T

A

U

A

U

A

U

A

U

T

A

T

A

T

A

C

G

G

C

G

C

G

C

G

C

G

C

G

C

C

G

C

G

C

G

C

Valine Serine Serine Valine Proline

Base insertion

A

U

A

U

A

U

A

U

A

A

U

T

A

T

A

C

G

G

C

G

C

G

C

G

C

G

CG

C

G

C

Valine Serine Serine Tyrosine Serine

Normal gene

Mutation

Mutation

DNA template

mRNA

Protein

A

U

A

U

A

U

A

U

T

A

T

A

C

G

G

C

G

C

G

C

G

C

G

C

G

CG

C

G

C

Valine Serine Serine Isoleucine Proline

The mRNA receives the appropriate complementary nitrogen base, uracil. When the mRNA reaches the ribosomes, the series of codons is changed because of the insertion. Instead of reading the correct AUU, the ribosomes read UAU, which codes for the amino acid tyrosine instead of isoleucine. Again, this amino acid change may or may not affect the resulting protein.

A base insertion occurs when a nitrogen base is added to the DNA template. Here, adenine is inserted.

As a result of the base substitution, the mRNA strand receives complementary guanine rather than the adenine that pairs with thymine. This further substitution changes the amino acid that is added to the polypeptide chain at the ribosomes. Instead of isoleucine, valine is inserted (see Table 3.2 in chapter 3). This amino acid change may or may not affect the resulting protein.

FIGURE 4.5 DNA Mutations During the transcription phase of protein synthesis, errors in the DNA template can affect the resulting protein. Two types of DNA mutation are illustrated in these diagrams: (a) base substitutions and (b) base insertions.

Mutation: The Only Source of New Alleles | 79

Because so much of any person’s DNA is noncoding (see “Producing Proteins: The Other Function of DNA” in chapter 3), many mutations do not affect the indi- vidual’s health, well- being, or survival. A new sequence of coding DNA that results from mutation may have profound consequences, positive or negative. For example, the mutation might code the DNA for a protein with an altered or different func- tion from that performed by the protein coded for in the original parent strand of DNA, or the mutation might create a sequence that results in either no protein or an abnormal protein (Figure 4.5). Mutations occur at random and can occur in any cell, but the ones with consequences for future generations take place in gametes. Gametes may transfer mutations to offspring, depending on what happens during meiosis in the parents. Regardless of their causes or outcomes, mutations are the only source of new genetic variation in a population.

Mutations involving incorrect base pairing are called point mutations. A syn- onymous point mutation creates an altered triplet in the DNA, but the alteration carries with it the original amino acid. Because the amino acid is the same, the pro- tein formed is the same. A nonsynonymous point mutation results in a matchup that brings along a different amino acid. Such a mutation can have dramatic results for the individual carrying it. For example, a mutation on human chromosome 11 results in a GUG codon instead of a GAG codon. The GUG codon is encoded to produce the amino acid valine, whereas the GAG codon would have normally led to the production of glutamic acid. This substitution leads to the abnormal hemo- globin that results in sickle- cell anemia (discussed later in this chapter).

As a result of the shifting base pairs caused by base insertion, the reading frame of a gene is altered or stopped entirely. This frameshift mutation produces a protein having no function. Such a mutation usually involves a small part of the DNA sequence, often just a base pair or a relatively limited number of base pairs.

Other kinds of mutations can affect far more of the genome. Transposable ele- ments are genes that can copy themselves to entirely different places along the DNA sequence. If such a gene inserts itself into another gene, it can fundamentally alter the other gene, doing real damage. If, as is strongly likely, the gene transposes itself to a noncoding area of the DNA sequence, little or no significant alteration will occur.

Large parts of DNA sequences or entire chromosomes can be affected by muta- tions. An entire piece of chromosome can be moved to another chromosome, can be placed differently on the same chromosome, or can be positioned in a chromo- some backward. The impacts of these mutations are highly variable and depend on the mutations’ loci.

In the most extreme mutations, entire chromosomes can be duplicated (a tri- somy) or lost altogether (a monosomy). Examples of trisomies are Down syndrome, with its extra twenty- first chromosome (see “Meiosis: Production of Gametes [Sex Cells]” in chapter  3) and Klinefelter’s syndrome, a common sex chromosome variant that appears in about 1 of 500–1,000 births.

All mutations fall into either of two types: spontaneous mutations have no known cause (Figure 4.6); induced mutations are caused by specific environmen- tal agents, usually associated with human activity. These agents, or mutagens, are increasingly becoming known. For example, ionizing radiation ( X- rays) and various toxic chemicals have been linked to mutations in animals and humans. Most mutations are spontaneous, however, and are simply DNA copying errors. The human mutation rate is higher in male sex cells (sperm) than in female sex cells (eggs) but is generally on the order of one per million per nucleotide per generation. The human genome includes about 3 billion base pairs, about 1.5% of which are protein- coding, so the average mutation rate in humans is .45 mutations

point mutations Replacements of a single nitrogen base with another base, which may or may not affect the amino acid for which the triplet codes.

synonymous point mutation A neutral point mutation in which the substituted nitrogen base creates a triplet coded to produce the same amino acid as that of the original triplet.

nonsynonymous point mutation A point mutation that creates a triplet coded to produce a different amino acid from that of the original triplet.

frameshift mutation The change in a gene due to the insertion or deletion of one or more nitrogen bases, which causes the subsequent triplets to be rearranged and the codons to be read incorrectly during translation.

transposable elements Mobile pieces of DNA that can copy themselves into entirely new areas of the chromosomes.

Klinefelter’s syndrome A chromosomal trisomy in which males have an extra X chromosome, resulting in an XXY con- dition; affected individuals typically have reduced fertility.

spontaneous mutations Random changes in DNA that occur during cell division.

induced mutations Refers to those muta- tions in the DNA resulting from exposure to toxic chemicals or to radiation.

mutagens Substances, such as toxins, chemicals, or radiation, that may induce genetic mutations.

T

A

Base substitution

(a) Base substitution

(b) Base insertion

A base substitution, the simplest kind of mutation, occurs when a single nitrogen base is substituted by another base. Here, thymine is being replaced by cytosine.

T

A

U

A

U

A

U

A

U

T

A

T

A

T

A

C

G

G

C

G

C

G

C

G

C

G

C

G

C

C

G

C

G

C

G

C

Valine Serine Serine Valine Proline

Base insertion

A

U

A

U

A

U

A

U

A

A

U

T

A

T

A

C

G

G

C

G

C

G

C

G

C

G

CG

C

G

C

Valine Serine Serine Tyrosine Serine

Normal gene

Mutation

Mutation

DNA template

mRNA

Protein

A

U

A

U

A

U

A

U

T

A

T

A

C

G

G

C

G

C

G

C

G

C

G

C

G

CG

C

G

C

Valine Serine Serine Isoleucine Proline

The mRNA receives the appropriate complementary nitrogen base, uracil. When the mRNA reaches the ribosomes, the series of codons is changed because of the insertion. Instead of reading the correct AUU, the ribosomes read UAU, which codes for the amino acid tyrosine instead of isoleucine. Again, this amino acid change may or may not affect the resulting protein.

A base insertion occurs when a nitrogen base is added to the DNA template. Here, adenine is inserted.

As a result of the base substitution, the mRNA strand receives complementary guanine rather than the adenine that pairs with thymine. This further substitution changes the amino acid that is added to the polypeptide chain at the ribosomes. Instead of isoleucine, valine is inserted (see Table 3.2 in chapter 3). This amino acid change may or may not affect the resulting protein.

FIGURE 4.5 DNA Mutations During the transcription phase of protein synthesis, errors in the DNA template can affect the resulting protein. Two types of DNA mutation are illustrated in these diagrams: (a) base substitutions and (b) base insertions.

80 | CHAPTER 4 Genes and Their Evolution: Population Genetics

in protein- coding genes per generation, or about one new, potentially significant mutation in every other person born.

For individuals, most mutations are relatively harmless, while a few may have profound consequences. For populations, mutations are inconsequential unless they offer selective adaptive advantages.

Natural Selection: Advantageous Characteristics, Survival, and Reproduction Darwin’s theory of evolution by means of natural selection provided the conceptual framework for understanding adaptation. That framework has become even more powerful over the last 150 years because it has allowed for many refinements. The principle of natural selection is based on Darwin’s conclusion that individuals with advantageous characteristics will survive in higher numbers and produce more

FIGURE 4.6 Spontaneous Mutations Spontaneous mutations can affect only physical appearance or can have health consequences, sometimes extreme ones. (a) A mutation called leucism has made this American alligator white. On its head are some spots of alligators’ normal, dark color. (b) The mutation that gives some cats white fur and blue eyes can also produce deafness and timidity. (c) Cheetahs normally have spotted coats, but a genetic mutation has produced stripes on this cheetah’s back. (d) Mutations can affect the wing count, eye color, and eye placement of fruit flies. A mutation has given this fruit fly abnormally placed, or ectopic, eyes, one of which is visible here as the red area on the wing.

(a)

(b)

(c) (d)

Natural Selection: Advantageous Characteristics, Survival, and Reproduction | 81

offspring than members of a population lacking advantageous characteristics. Natural selection, therefore, focuses on reproductive success, or fitness. In par- ticular, fitness is defined as some measure of the propensity to contribute offspring to future generations, usually by the next generation. Fitness can be defined in reference to individuals in a population or to specific genotypes. For our purposes, fitness is defined on the basis of genotypes. This means that some genotypes have more (or less) fitness than other genotypes. The implication is that fitness differ- ences can result in changes to allele frequencies. For example, if the genotype for darker coloring confers an adaptive advantage over the genotype for lighter color- ing, the dark- color genotype will likely increase in frequency over time.

PATTERNS OF NATURAL SELECTION Evolutionary biologists have identified three alternative patterns by which natural selection can act on a specific trait. Directional selection favors one extreme form of a trait— more children are produced by individuals who have that extreme trait, so selection moves in that direction. Human evolution, for example, has clearly favored larger brains (for more on these topics, see chapters 10 and 11). Stabilizing selection favors the average version of a trait. For example, living humans whose birth weights are in the middle of the range have a better chance of surviving and reproducing than do those born with the lowest and highest weights. In disruptive selection, the pattern of variation is discontinuous. Individuals at both extreme ends of the range produce more offspring than do the remainder of the population. Given enough time, this pattern can result in a speciation event as those in the middle fail to survive and reproduce and two new species arise at the extremes (Figure 4.7).

fitness Average number of offspring produced by parents with a particular genotype compared to the number of off- spring produced by parents with another genotype.

directional selection Selection for one allele over the other alleles, causing the allele frequencies to shift in one direction.

stabilizing selection Selection against the extremes of the phenotypic distribution, decreasing the genetic diversity for this trait in the population.

disruptive selection Selection for both extremes of the phenotypic distribution; may eventually lead to a speciation event.

Fr eq

ue nc

y

Body size

Directional selection

Body size

Stabilizing selection

Body size

Disruptive selection

Body size

Fi tn

es s

(n um

be r o

f of

fs pr

in g

pr od

uc ed

)

Body size Body size Body size Body size

Av er

ag e

si ze

(i n

po pu

la tio

n)

Time Time Time Time

No selection

(a) (b) (c) (d) FIGURE 4.7 Types of Selection (a) Top: In the population represented here, smaller body size is more favorable than larger body size, so the frequency of smaller body size will increase thanks to directional selection. Middle: The fitness of individuals with smaller body sizes will be greater than that of individuals with larger body sizes. Bottom: Over time, the population’s average body size will decrease. (b) Top: In this population, medium body size is favored, so the frequency of medium body size will increase thanks to stabilizing selection. Middle: The fitness of individuals with medium body sizes will be much greater. Bottom: However, the population’s average body size will remain relatively stable over time. (c) Top: Here, owing to disruptive selection, the frequencies of small and large body sizes will increase, while the frequency of medium body size will decrease. Middle: The fitness levels are highest at the extremes and lowest in the middle. Bottom: Over time, the population will split between those with large bodies and those with small bodies. (d) Top: In the absence of selection, the population will have a range of sizes. Middle: Fitness levels will vary independently of size. Bottom: The population’s average body size will not change over time.

82 | CHAPTER 4 Genes and Their Evolution: Population Genetics

NATURAL SELECTION IN ANIMALS: THE CASE OF THE PEPPERED MOTH AND INDUSTRIAL MELANISM Examples of natural selection in animals are wide- ranging. Among them are animals that “blend in” with their surrounding habitat (Figure 4.8). Perhaps the best evidence ever documented of natural selection operating on a heritable trait concerns the peppered moth, Biston betularia, a species common throughout Great Britain (Figure  4.9). This moth is nocturnal, eating and breeding by night and attaching itself to trees, especially in the upper branches, during the day. Prior to the mid- 1800s, all members of the species had a peppered appearance, their white coloring sprinkled with black. Trees throughout Great Britain were covered with lichen, and the moths’ coloration provided excellent camouflage against the trees’ variable- colored surface and thus protected the moths from their major predator, birds. In 1848, a naturalist exploring the countryside near Manchester, England, spotted a completely black variety of the moth. A new species name, Biston car- bonaria, distinguished this melanic (dark) form from the nonmelanic (light) form. The frequency of the melanic form remained relatively low for a couple of decades but climbed rapidly in the late nineteenth century. By the 1950s, 90% or more of peppered moths were melanic (Figure 4.10).

This rapid increase in melanic frequency was a case of evolution profoundly changing phenotype. Directional selection had favored the melanic form over the nonmelanic form, and the melanic form exhibited a greater fitness. But what was this form’s adaptive advantage?

The selecting factor was the Industrial Revolution. With the rise of industry throughout England and elsewhere in the middle to late nineteenth century, mills, fueled entirely by coal, spewed coal particles from smokestacks— 50 tons per square mile per month, in some places— blackening the sky and covering the landscape. The trees survived this pollution onslaught, but the lichen covering the trees did not. The trees’ surfaces went from light- colored to black, greatly altering the peppered moth’s habitat. This pollution crisis provided a huge selective advantage for the melanic moths, which were now perfectly camouflaged against blackened trees. Nonmelanic moths became easy prey.

FIGURE 4.8 Leafy Sea Dragon As a result of natural selection, the leafy sea dragon looks just like the sea plants around it in its ocean setting.

melanic Refers to an individual with high concentrations of melanin.

nonmelanic Refers to an individual with low concentrations of melanin.

FIGURE 4.9 Peppered Moths The genus Biston includes two species: Biston betularia (light) and Biston carbonaria (dark).

Natural Selection: Advantageous Characteristics, Survival, and Reproduction | 83

How did the genetics of this evolutionary change work? Breeding experiments revealed that, in a classic case of Mendelian genetics, the color difference between the two Biston species was determined by one locus. The nonmelanic variety had a genotype of cc (homozygous recessive), while the melanic variety was either het- erozygous, Cc, or homozygous,  CC.  The dominant allele, C, likely first appeared as a mutation, perhaps in the first half of the nineteenth century or earlier, long before the first melanic moth was observed, in 1848. The C allele may have been in the population, maintained by the mutation’s reoccurrence. Recent estimates suggest that the frequency of the nonmelanic variety was only 1%–10% in polluted regions of England and no more than 5% around Manchester. Plugged into the Hardy- Weinberg equilibrium, this information in turn suggests that 46% of the population had the CC genotype, 44% had the Cc genotype, and 10% had the cc genotype (Table 4.2).

TABLE 4.2 Moth Genotype Frequencies— Industrialization Period

Phenotype Melanic Nonmelanic

Phenotype Frequencies .90 .10

Genotype CC + Cc cc

Genotype Frequencies p2 + 2pq q2

Allele Frequency* Calculations:

Step 1 q2 = .10 (q2 = f[cc])

Step 2 q = √q2 = √.10 = .32

Step 3 p = 1 − q = 1 − .32 = .68

Genotype Frequency Calculations: p2 = f(CC) = .682 = .46

2pq = f(Cc) = 2 × .68 × .32 = .44

q2 = f(cc) = .322 = .10

Check: p2 + 2pq + q2 = 1

.46 + .44 + .10 = 1

*f = frequency

FIGURE 4.10 Changes in the Peppered Moth Gene Frequency The frequency of the melanic gene in peppered moths increased from 1848 through 1948. The frequency of the nonmelanic gene decreased during that same period.

G en

e Fr

eq ue

nc y

Generation Date

1.0

0.8

0.1

0.2

0.9

0.3

0.4

0.5

0.6

0.7

1848 1858 1868 1878 1888 1898 1908 1918 1928 1938 1948 0

84 | CHAPTER 4 Genes and Their Evolution: Population Genetics

Beginning in the late 1960s and early 1970s, the stricter pollution laws, changes in coal burning, and decline of mill- based industry in Great Britain profoundly affected the moth population, once again illustrating natural selection. That is, in areas that were no longer polluted, the frequency of Biston carbonaria dropped. In Manchester, for example, the frequency of the melanic moth decreased from 90% in 1983 to well under 10% in the late 1990s. Plugged into the Hardy- Weinberg equilibrium, these numbers reveal that the CC genotype decreased to 0.25%, the Cc genotype decreased to 9.5%, and the cc genotype increased to 90% (Table 4.3). This rapid evolutionary change reflected the return of the trees’ original col- oration, which conferred a selective disadvantage— predation visibility— on the melanic variety. This postscript adds even more power to the story of how natural selection brought about biological changes in the genus Biston.

NATURAL SELECTION IN HUMANS: ABNORMAL HEMOGLOBINS AND RESISTANCE TO MALARIA The above case of industrial melanism is an example of positive selection, whereby an organism’s biology is shaped by selection for beneficial traits. Natural selection for beneficial traits in humans is best understood by studying genes that control specific traits. Of the 90 or so different loci that are targets of natural selection (Figure  4.11), among the most compelling examples is the sickle- cell allele— the hemoglobin S (or simply S) allele— which causes sickle- cell anemia (Figure  4.12). Millions of people suffer from such hemolytic anemias, which involve the destruction of red blood cells. A low number of red blood cells can produce health problems because of the resultant lack of hemoglobin, the chemical in red blood cells that carries oxygen to all the body tissues. The S gene yields a specific kind of abnormal hemoglobin.

positive selection Process in which advan- tageous genetic variants quickly increase in frequency in a population.

sickle- cell anemia A genetic blood dis- ease in which the red blood cells become deformed and sickle- shaped, decreasing their ability to carry oxygen to tissues.

hemolytic anemias Conditions of insuf- ficient iron in the blood due to the destruction of red blood cells resulting from genetic blood diseases, toxins, or infectious pathogens.

abnormal hemoglobin Hemoglobin altered so that it is less efficient in binding to and carrying oxygen.

TABLE 4.3 Moth Genotype Frequencies— Postindustrialization Period

Phenotype Melanic Nonmelanic

Phenotype Frequencies .10 .90

Genotype CC + Cc cc

Genotype Frequencies p2 + 2pq q2

Allele Frequency* Calculations:

Step 1 q2 = .90 (q2 = f[cc])

Step 2 q = √q2 = √.90 = .95

Step 3 p = 1 − q = 1 − .95 = .05

Genotype Frequency Calculations: p2 = f(CC) = .052 = .0025

2pq = f(Cc) = 2 × .05 × .95 = .095

q2 = f(cc) = .952 = .90

Check: p2 + 2pq + q2 = 1

.0025 + .095 + .90 = 1

*f = frequency

Natural Selection: Advantageous Characteristics, Survival, and Reproduction | 85

Sickle- cell anemia has been known since the early 1900s, and the genetics behind it were documented in the 1950s. The S gene is a simple base- pair mutation (Figure  4.13). Genetically, people with normal hemoglobin have the alleles AA, the homozygous condition. People who carry the sickle- cell allele on one of the two homologous chromosomes only are AS, and people who have the homozygous form of the disease are SS. AS individuals are for all practical purposes normal in their survival and reproduction rates. There is no cure for sickle- cell anemia, and in the absence of modern medical treatment, some 80% of people who are SS die before the reproductive years, usually considerably earlier. The SS genotype results in many red blood cells’ having a sickle shape caused by the abnormal hemoglobin, in sharp contrast to the round appearance of red blood cells in people with normal hemoglobin (Figure 4.14). The cells’ abnormal shape prevents them from passing through the capillaries, the narrow blood vessels that form networks throughout tissues. When the clogging of capillaries cuts off the oxygen supply in vital tissues, severe anemia and death can result.

Chromosome 11

Hemoglobin S

X chromosome

G6pd

FIGURE 4.11 G6pd One target of natural selection in humans is the G6pd gene, located on the X chromosome.

FIGURE 4.12 Sickle- Cell Gene Hemoglobin S appears on human chromosome 11.

capillaries Small blood vessels between the terminal ends of arteries and the veins.

86 | CHAPTER 4 Genes and Their Evolution: Population Genetics

THE GEOGRAPHY OF SICKLE- CELL ANEMIA AND THE ASSOCIATION WITH MALARIA Beginning in the mid- twentieth century, the medical commu- nity observed that many people living in equatorial Africa— as many as 20%– 30%—had the S gene. This finding represented a huge puzzle: since the gene was so bad for survival, why was its frequency so high? In other words, one would expect strong selection against this nonbeneficial gene. The solution to the puzzle began to emerge with the discovery that high heterozygous (AS) frequencies appear in regions of Africa where malaria is endemic. In other words, where malaria— a potentially lethal parasitic infection in which the parasite is introduced to a human host by a mosquito— is always present, there is a high frequency of carriers of the gene (Figure 4.15). Moreover, AS people ( sickle- gene carriers) die of malaria in far fewer numbers than do AA people.

As described at the beginning of this chapter, Anthony Allison discovered that in low- lying, wet areas of Kenya (where the number of mosquitoes was great and the rate of malaria was high), the frequency of the sickle- cell allele was consid- erably higher than in highland or arid areas. He developed the simple but elegant hypothesis that the infection and the genetic mutation were related. Individuals homozygous for normal hemoglobin (AA) were highly susceptible to dying from malaria; individuals homozygous for sickle- cell anemia (SS) did not survive to reproduce; however, individuals heterozygous for normal hemoglobin and the sickle- cell mutation (AS) either did not contract malaria or suffered a less severe malarial infection. That these frequencies were being maintained indicated that the AS heterozygote was a balanced polymorphism. It was also a fitness trade- off: car- riers could pass on the sickle- cell allele, but they received immunity from malaria.

FIGURE 4.14 Sickle- Shaped Red Blood Cells This image shows normal red blood cells, which are round; a long, slender, sickle- shaped cell (at top); and other irregularly shaped cells. The abnormal cells are very fragile and easily damaged or destroyed.

The S allele arises from a nitrogen base substitution: adenine replaces thymine in the hemoglobin DNA.

The codon changes from GAG in normal hemoglobin mRNA to GUG in the sickle-cell hemoglobin mRNA (the adenine in the normal mRNA is replaced with uracil).

A

U

T

A

C

G

C

G

Transcription

Normal hemoglobin DNA

C

G

C

G

Sickle-cell hemoglobin DNA

mRNA

Translation

Normal hemoglobin

Sickle-cell hemoglobin

mRNA

The changed codon in the mRNA is coded to produce a different amino acid. Instead of glutamate, valine is inserted in the polypeptide chain. This amino acid change causes a change in the functioning of the hemoglobin so that it cannot bind to oxygen.

Glutamatic acid Valine

FIGURE 4.13 Sickle- Cell Mutation Sickle- cell anemia begins with a single nitrogen base mutation— a base substitution. The abnormal hemoglobin that results is less efficient at binding oxygen and causes red blood cells to become sickle- shaped.

Natural Selection: Advantageous Characteristics, Survival, and Reproduction | 87

THE BIOLOGY OF SICKLE- CELL ANEMIA AND MALARIAL INFECTION Why do people who are heterozygous for the sickle- cell allele survive malaria or not con- tract it at all? Unlike SS red blood cells, AS red blood cells do not sickle under most conditions (that is, except when severely deprived of oxygen). They are, however, somewhat smaller than normal cells, and their oxygen levels are somewhat lower. For reasons not yet understood, the AS red blood cells are simply a poor host— a nonconducive living and reproduction environment— for the parasite that causes malaria (Figure 4.16).

THE HISTORY OF SICKLE- CELL ANEMIA AND MALARIA In the late 1950s, the American physical anthropologist Frank B. Livingstone (1928–2005) sought to strengthen the case for natural selection by historically linking sickle- cell anemia and malaria. Livingstone asked two important questions: Where and when did the sickle- cell allele first appear in equatorial Africa? and What conditions led to the allele’s being naturally selected? He hypothesized that the Bantu, a group of peoples who speak Bantu languages, carried the mutation with them when they migrated south- ward from the region of Cameroon and Nigeria (Figure 4.17). Prior to the Bantu’s arrival, the region was a largely unbroken forest. Bantu populations introduced agri- culture there, clearing large swaths of the forest for cultivation. The peoples’ iron- working technology made possible the creation of tools for cutting down large trees, clearing and plowing fields, and planting crops— mostly yams and cassava.

Even under the best conditions, tropical forests are fragile ecosystems. Once their trees have been cleared and their fields have been planted, their relatively poor soil, which normally soaks up rainwater, becomes thin or disappears. Geo- logical evidence shows a dramatic increase in soil erosion in the region after the arrival of Bantu populations, due in large part to anthropogenic deforestation and the overall environmental impact of humans on the landscape. As a result of these erosive processes, pools of water collect and become stagnant, providing ideal conditions for the breeding of parasite- carrying mosquitoes (Figure  4.18). This picture became clear to Livingstone as he developed his research: the newly created ecological circumstances fostered mosquito reproduction and the spread of malaria, and the growing host of humans made possible by agriculture- fueled population growth provided the food resources needed by the mosquitoes. The

(b)(a)

Greater than 14% 12–14% 10–11.9% 8–9.9% 6–7.9% 4–5.9% 2–3.9% 0–1.9%

Areas where malaria is present

FIGURE 4.15 Distributions of the Sickle- Cell Allele and Malaria In equatorial Africa, (a) the distribution of the sickle- cell allele coincides with (b) areas of high malarial parasite concentration.

balanced polymorphism Situation in which selection maintains two or more phenotypes for a specific gene in a population.

anthropogenic Refers to any effect caused by humans.

88 | CHAPTER 4 Genes and Their Evolution: Population Genetics

infectious disease gave those individuals with a very rare mutation— the sickle- cell allele— an adaptive advantage and the ability to survive and reproduce in these new environmental circumstances. Due to the advantage the heterozygous condition provides, the S allele was maintained and passed from generation to generation. For this reason, sickle- cell anemia predominantly affects those whose descendants came from the malarial environments in large parts of equatorial Africa. Outside of such malarial environments, the S allele never became advantageous.

OTHER HEMOGLOBIN AND ENZYME ABNORMALITIES  Sickle- cell anemia turns out to be just one of a number of hemoglobinopathies and other genetic abnormalities in Africa, Asia, and Europe that provide a strong selective advantage in regions of endemic malaria (Figure  4.19). Heterozygous carriers of abnormal hemoglobins apparently make poor hosts for malarial parasites.

Thalassemia, a genetic anemia found in Europe (especially in Italy and Greece), Asia, and the Pacific, reduces or eliminates hemoglobin synthesis. In some homozygous forms of the mutation, hemoglobin becomes clumped inside the red blood cells. The spleen then destroys the red blood cells, resulting in severe anemia. In the areas around the Mediterranean where the genetic frequency is highest— as high as 80%—the presence of malaria makes a strong case for a selective advantage for heterozygous individuals, for whom the condition and malaria are not lethal.

An association has long been recognized between deficiency of the enzyme glucose- 6-phosphate dehydrogenase (G6PD) and malaria. A recessive hered- itary mutation leads more males than females to lack the gene that is coded to produce this enzyme (see Figure 4.11). Without the G6PD enzyme, a person who takes sulfa- based antibiotics or eats fava beans risks the destruction of red blood cells, severe anemia, and occasionally death. Because of the connection with fava beans, this severe hemolytic disease is called favism. Its 130 genetic variants occur in high frequencies in some populations, the highest being 70% among Kurdish Jews. Heterozygous carriers have a strong selective advantage because they pro- duce some of the enzyme but are protected from malaria (here again, the parasite cannot live in the abnormal red blood cells).

Analysis of genetic data by the anthropologist Sara Tishkoff indicates that the mutation for the disease arose between about 4,000 and 12,000 yBP, at the same time as the abnormal hemoglobins. Populations whose descendants did not encounter malaria do not have the G6pd mutation or abnormal hemoglobins.

Once inside the human, the sporozoites travel through the bloodstream to the liver. In the liver, the sporozoites create thousands of merozoites. A merozoite is a daughter cell that results from asexual reproduction.

The newly produced merozoites enter the bloodstream and infect the red blood cells. Within these cells, the merozoites continue to multiply, eventually causing the cells to rupture. The merozoites then invade other red blood cells in the bloodstream, and the cycle continues.

a Sporozoite: The goal of sporozoite vaccines is to block parasites from entering or growing within human liver cells.

b Merozoite: Vaccines based on merozoite antigens lessen malaria’s severity by hobbling the invasion of new generations of red blood cells or by reducing complications.

c Gametocyte: So-called altruistic gametocyte- based vaccines do not affect human disease but are designed to evoke human antibodies that derail parasite development within the mosquito.

Over time, some of the merozoites develop into male and female gametocytes, which may be transferred to another mosquito that bites the human host. Gametocytes are cells that can divide to produce gametes, or sex cells.

Within the mosquito, sexual reproduction occurs, as the male gamete fertilizes the female gamete. Oocysts, or zygotes, develop and even- tually release sporozoites. These newly formed sporozoites travel to the salivary glands of the mosquito, where they can be transmitted to the next human the mosquito bites.

Within the mosquito, sexual reproduction occurs, as the male gamete fertilizes the female gamete. Oocysts, or zygotes, develop and even- tually release sporozoites. These newly formed sporozoites travel to the salivary glands of the mosquito, where they can be transmitted to the next human the mosquito bites.

Merozoites

Host’s liver

Host’s red blood cell

INSIDE HUMAN

VACCINE TARGETS

INSIDE MOSQUITO

Female gametocyte

Female gamete

Male gamete

Oocyst

Male gametocyte

Fertilizationc

Sporozoites

A mosquito bites a human, passing sporozoites to the new host. A sporozoite is a motile form of the parasite.

a

b

1

5 2

4

3

FIGURE 4.16 The Spread of Malaria The life cycle of the malarial parasite, Plasmodium falciparum, takes place in two hosts: mosquito and human. Both hosts are needed if the parasite is to survive.

Natural Selection: Advantageous Characteristics, Survival, and Reproduction | 89

infectious disease gave those individuals with a very rare mutation— the sickle- cell allele— an adaptive advantage and the ability to survive and reproduce in these new environmental circumstances. Due to the advantage the heterozygous condition provides, the S allele was maintained and passed from generation to generation. For this reason, sickle- cell anemia predominantly affects those whose descendants came from the malarial environments in large parts of equatorial Africa. Outside of such malarial environments, the S allele never became advantageous.

OTHER HEMOGLOBIN AND ENZYME ABNORMALITIES  Sickle- cell anemia turns out to be just one of a number of hemoglobinopathies and other genetic abnormalities in Africa, Asia, and Europe that provide a strong selective advantage in regions of endemic malaria (Figure  4.19). Heterozygous carriers of abnormal hemoglobins apparently make poor hosts for malarial parasites.

Thalassemia, a genetic anemia found in Europe (especially in Italy and Greece), Asia, and the Pacific, reduces or eliminates hemoglobin synthesis. In some homozygous forms of the mutation, hemoglobin becomes clumped inside the red blood cells. The spleen then destroys the red blood cells, resulting in severe anemia. In the areas around the Mediterranean where the genetic frequency is highest— as high as 80%—the presence of malaria makes a strong case for a selective advantage for heterozygous individuals, for whom the condition and malaria are not lethal.

An association has long been recognized between deficiency of the enzyme glucose- 6-phosphate dehydrogenase (G6PD) and malaria. A recessive hered- itary mutation leads more males than females to lack the gene that is coded to produce this enzyme (see Figure 4.11). Without the G6PD enzyme, a person who takes sulfa- based antibiotics or eats fava beans risks the destruction of red blood cells, severe anemia, and occasionally death. Because of the connection with fava beans, this severe hemolytic disease is called favism. Its 130 genetic variants occur in high frequencies in some populations, the highest being 70% among Kurdish Jews. Heterozygous carriers have a strong selective advantage because they pro- duce some of the enzyme but are protected from malaria (here again, the parasite cannot live in the abnormal red blood cells).

Analysis of genetic data by the anthropologist Sara Tishkoff indicates that the mutation for the disease arose between about 4,000 and 12,000 yBP, at the same time as the abnormal hemoglobins. Populations whose descendants did not encounter malaria do not have the G6pd mutation or abnormal hemoglobins.

Once inside the human, the sporozoites travel through the bloodstream to the liver. In the liver, the sporozoites create thousands of merozoites. A merozoite is a daughter cell that results from asexual reproduction.

The newly produced merozoites enter the bloodstream and infect the red blood cells. Within these cells, the merozoites continue to multiply, eventually causing the cells to rupture. The merozoites then invade other red blood cells in the bloodstream, and the cycle continues.

a Sporozoite: The goal of sporozoite vaccines is to block parasites from entering or growing within human liver cells.

b Merozoite: Vaccines based on merozoite antigens lessen malaria’s severity by hobbling the invasion of new generations of red blood cells or by reducing complications.

c Gametocyte: So-called altruistic gametocyte- based vaccines do not affect human disease but are designed to evoke human antibodies that derail parasite development within the mosquito.

Over time, some of the merozoites develop into male and female gametocytes, which may be transferred to another mosquito that bites the human host. Gametocytes are cells that can divide to produce gametes, or sex cells.

Within the mosquito, sexual reproduction occurs, as the male gamete fertilizes the female gamete. Oocysts, or zygotes, develop and even- tually release sporozoites. These newly formed sporozoites travel to the salivary glands of the mosquito, where they can be transmitted to the next human the mosquito bites.

Within the mosquito, sexual reproduction occurs, as the male gamete fertilizes the female gamete. Oocysts, or zygotes, develop and even- tually release sporozoites. These newly formed sporozoites travel to the salivary glands of the mosquito, where they can be transmitted to the next human the mosquito bites.

Merozoites

Host’s liver

Host’s red blood cell

INSIDE HUMAN

VACCINE TARGETS

INSIDE MOSQUITO

Female gametocyte

Female gamete

Male gamete

Oocyst

Male gametocyte

Fertilizationc

Sporozoites

A mosquito bites a human, passing sporozoites to the new host. A sporozoite is a motile form of the parasite.

a

b

1

5 2

4

3

FIGURE 4.16 The Spread of Malaria The life cycle of the malarial parasite, Plasmodium falciparum, takes place in two hosts: mosquito and human. Both hosts are needed if the parasite is to survive.

FIGURE 4.17 Bantu Expansion Beginning by about 1000 BC, Bantu people began a series of migrations, originating in central Africa and pushing southward eventually into southern Africa. In addition to agriculture, they carried the mutation for the sickle- cell allele.

Bantu Khoisan

hemoglobinopathies A group of related genetic blood diseases characterized by abnormal hemoglobin.

thalassemia A genetic blood disease in which the hemoglobin is improperly synthesized, causing the red blood cells to have a much shorter life span.

glucose- 6-phosphate dehydrogenase (G6PD) An enzyme that aids in the proper functioning of red blood cells; its deficiency, a genetic condition, leads to hemolytic anemia.

(a) (b)

FIGURE 4.18 The Spread of Malaria As the Bantu cleared forests for agricultural fields, (a) pools of stagnant water (b) became an ideal breeding ground for mosquito larvae, which carried the malarial parasites.

90 | CHAPTER 4 Genes and Their Evolution: Population Genetics

Today, for example, malaria appears throughout the tropical regions of the Amer- icas, but Native Americans are 100% homozygous for normal alleles at the G6pd and hemoglobin loci. That these particular genes do not appear to have mutated in the New World strongly suggests that malaria was introduced to North and South America only after the Europeans’ arrival. Indeed, the introduction of malaria and other Old World diseases— by either Spaniards or their African slaves— likely played an instrumental role in the precipitous decline in the native populations.

If malaria had been introduced in the Americas much earlier than the last few centuries— say thousands of years ago— and the mutations occurred, there might have been time for a natural selection to develop for the mutations. If the mutations did appear before the Europeans’ arrival, however, they would have exhibited a clear selective disadvantage in the absence of malaria and been weeded out of the gene pool. Thus, red blood cell polymorphisms in the abnormal hemoglobin and G6pd loci reflect the fundamental interactions among environment, genes, and culture that have resulted in the modern human genome. The genes provide an important record about human evolution and the role of natural selection in shaping genetic variation.

Genetic Drift: Genetic Change due to Chance One of the four forces of evolution (see “The Evolutionary Synthesis, the Study of Populations, and the Causes of Evolution” in chapter  2), genetic drift, is random change in allele frequency over time. Provided that no allele confers a selective advantage over another, a random change can lead to a change in gene frequency, such as one allele being lost and the other becoming fixated— or fixed, the only allele of its kind, in the population. This force, this kind of change, makes possible the measuring of evolution as a statistical probability.

Hb C Hb E Hb S

FIGURE 4.19 Distribution of Hemoglobinopathies This map shows the distribution of hemoglobin E in Southeast Asia. People with hemoglobin E, an uncommon but severe blood abnormality, may have mild hemolytic anemia or other mild effects. Like hemoglobin S, hemoglobin C appears primarily in equatorial Africa. Like hemoglobin E, hemoglobin C has generally minor effects, most often mild hemolytic anemia.

Genetic Drift: Genetic Change due to Chance | 91

Coin tosses can demonstrate the effects of genetic drift (Table  4.4). Imagine that heads and tails are two alleles in a population. If there are only two members of the population (two coin tosses), there is a great chance that both will be heads. In effect, the “heads” allele will become fixed in the small population, while the “tails” allele will be lost. As the population size (number of coin tosses) increases, it becomes less likely that one allele will become fixed and the other lost. In very large populations (1  million coin tosses), both alleles may be present in equal proportions.

How does such statistical probability translate to populations? Now imagine that before the election of your student government you have been asked to predict the winners. The best way for you to predict would be to ask each voting- eligible student how he or she planned to vote. It is highly likely that the outcome of such a comprehensive poll would be close to the actual election results. The shortcom- ings of this approach might include the very large size of the target population. No one would interview, for example, 50,000 students! The second- best approach would be to select a sample, preferably a random sample that represented the entire student body. If you selected five students out of the 50,000, chances are very slim that those five would represent all the ethnic, national, regional, and economic backgrounds of the student body. In fact, chances are very high that this sample (.01% of the total population) would provide a voting outcome very different from the actual one. If you interviewed 500 students (1% of the population), the chances of representation would be much greater; and if you chose 5,000 students (10% of the population), they would be greater still. The larger the sample size, the greater the probability of an accurate prediction.

Variations in human populations work the exact same way, except that genetic drift operates over a period of time rather than at a single point. The probability of an allele’s frequency changing in a relatively short period of time increases with

TABLE 4.4 Heads versus Tails: Genetic Drift and Probability

Coin Tosses Heads Tails Heads: Tails Rat io

2 2 0 2:0

10 4 6 4:6

50 22 28 11:14

100 55 45 11:9

200 199 201 199:201

500 253 247 253:247

1,000 501 499 501:499

5,000 2,500 2,500 1:1

10,000 5,000 5,000 1:1

100,000 50,000 50,000 1:1

500,000 250,000 250,000 1:1

1,000,000 500,000 500,000 1:1

92 | CHAPTER 4 Genes and Their Evolution: Population Genetics

decreasing population size. The larger the population, the less divergence from the original gene frequency over time (Figure 4.20).

How does this effect play out in real life? Among humans, for example, genetic drift might occur in a small group that is endogamous, discouraging reproduc- tion outside the group. (An exogamous society extends reproduction outside its community.) Within such a group, the chances are great that the frequencies of genetic markers will differ from those of a larger population. When the Dunkers, a small religious sect that discourages outside marriage (and thus reproduction), first emigrated from Germany to Pennsylvania, in 1719, the group included just 28 members. Over the next few decades, several hundred more arrived in Pennsylvania; the breeding population remained quite small. Comparisons of contemporary blood type percentages among Dunkers, Germans, and Americans reflect significant changes in the Dunkers and a likely lack of change in the larger populations (Figure  4.21). That is, blood type frequencies among Germans and Americans remain basically the same as they were in the 1700s. The Dunkers’ original frequencies were probably much like those of the Germans, but the small

endogamous Refers to a population in which individuals breed only with other members of the population.

exogamous Refers to a population in which individuals breed only with non- members of their population.

founder effect The accumulation of random genetic changes in a small population that has become isolated from the parent population due to the genetic input of only a few colonizers.

G en

e fre

qu en

cy (%

)

Number of generations

100

50

200 10 30 40 50 0

A

C

B

FIGURE 4.20 Genetic Drift over Time The effects of genetic drift appear in this graph, which plots the frequencies over time (by generations) of one gene in three differently sized populations. Assume that population A is the smallest of the three and that population C is the largest. At the start, each population has the gene at 50% frequency. Around 38 generations, population A has drifted significantly; the gene is fixed at 100% frequency, a 50% increase. At 50 generations, population B has also drifted. Its gene frequency has declined by 40%. Although the frequency in population C has changed over time, it is still approximately 50% after 50 generations, owing to the largeness of the population.

(a) ABO Blood Type Frequencies (b) MN Blood Type Frequencies

Pe rc

en ta

ge

70

0

Populations

AmericansGermansDunkers

Pe rc

en ta

ge

60

0

Populations

AmericansGermansDunkers

60

50

40

30

20

10

50

40

30

20

10

A B AB O MM MN NN 70

FIGURE 4.21 Genetic Drift in the Dunker Population Comparisons of ABO and MN blood type frequencies among Dunkers, Germans, and Americans reveal genetic drift: (a) Dunkers have a higher percentage of blood type A and lower percentages of blood types O, B, and AB than do Germans and Americans; (b) Dunkers have a higher percentage of blood type M and lower percentages of MN and N.

Gene Flow: Spread of Genes across Population Boundaries | 93

Dunker population meant a much greater chance for genetic drift. The frequencies diverged dramatically over time simply due to chance.

FOUNDER EFFECT: A SPECIAL KIND OF GENETIC DRIFT Founder effect, one form of genetic drift, occurs when a small group (fewer than several hundred members) of a large parent population migrates to a new region and is reproductively isolated. The new region is either unoccupied or occupied by species with which the small group cannot breed. Because the founding population is so small, there is a very good chance that its genetic composition is not representative of the parent population’s. Thanks to the founder effect, as the founding population grows its gene pool diverges even further from the source (Figure  4.22). For example, around 12,000 yBP a very small number of individuals— perhaps just a few hundred— migrated from eastern Asia to North America (this movement is among the topics of chapter 12). Today, Native Amer- icans have very high frequencies of type O blood— in many places the frequency is 100%—while eastern Asian populations have among the world’s lowest frequencies of it. This discrepancy strongly suggests that the original east Asian immigrants, the founding “Native Americans,” had a higher frequency of type O blood than their parent population had.

Founder effect has also been documented in several genetic diseases that affect humans. Among the best known is a type of microsatellite called Hun- tington’s chorea, a genetic abnormality caused by an autosomal dominant gene (Figure  4.23). The gene is located on chromosome 4 at the locus that codes for the Huntington protein, and a person needs only one allele from a parent to have the disease. At the end of the normal gene is a sequence of three DNA bases, CAG (the code for valine). If the sequence is repeated numerous times, usually more than 35 times, the individual has the mutation. Huntington’s chorea causes degenera- tion of parts of the brain that control body movement and abilities such as speech production, triggering involuntary jerky movements of the arms and legs as well as dementia. These multiple and debilitating symptoms normally do not manifest until late in life or after the reproductive years, usually after about age 40. For- tunately, the disease is quite rare, affecting only five to eight people per 100,000.

Why had such a debilitating disease not been removed from the gene pool via natural selection? Since the effects of the gene are not expressed until later in life, people might not have known they had the disease until after they had passed on the detrimental allele to their offspring (Figure 4.24).

Today, most human populations are not small and isolated, and they interbreed relatively freely with surrounding groups. Whenever interbreeding occurs across population boundaries, gene flow occurs.

Gene Flow: Spread of Genes across Population Boundaries Another force of evolution, gene flow (or admixture; see “The Evolutionary Synthesis, the Study of Populations, and the Causes of Evolution” in chapter  2) is the transfer of genes across population boundaries. Simply, members of two

FIGURE 4.22 Founder Effect The large circle on the left represents a parent population, from which a very small proportion is removed to begin a new population. Over time, the founding population grows, and its gene pool looks less and less like that of the parent population.

FIGURE 4.23 Huntington’s Chorea The woman in the wheelchair suffers from Huntington’s chorea, a degenerative genetic disorder.

Huntington’s chorea A rare genetic disease in which the central nervous system degenerates and the individual loses control over voluntary movements, with the symptoms often appearing between ages 30 and 50.

admixture The exchange of genetic mate- rial between two or more populations.

94 | CHAPTER 4 Genes and Their Evolution: Population Genetics

populations produce offspring (Figure 4.25). The key determinant for the amount of gene flow is accessibility to mates— the less the physical distance between pop- ulations, the greater the chance of gene flow. While mutation increases genetic variation between two populations over time, gene flow decreases such variation. Anthropologists and geneticists have found that for many kinds of biological traits, ranging from cranial shapes to blood types to microsatellite DNA markers (see “Polymorphisms: Variations in Specific Genes” in chapter 3), similarity increases the closer one population is to another population.

Migration does not necessarily bring about gene flow. For example, when east Asians first migrated to North America (see “Founder Effect: A Special Kind of Genetic Drift,” above), they reached a continental landmass where no humans had ever lived. Written records suggest that Vikings first traveled from Greenland to Newfoundland around AD 1000, but there is no evidence that they interbred with the native people. The first significant gene flow involving Native Americans and Europeans seems to have occurred when or soon after Christopher Columbus and his crew arrived in the New World, in 1492. From that point on, gene flow in the Americas, North and South, has been extensive.

Gene flow and genetic variation are also highly influenced by social structure (Figure  4.26). Endogamous societies— for example, Australian aborigines— have relatively little genetic diversity because few individuals migrate into the commu- nity and thus little new genetic material is introduced. Exogamous societies have relatively high genetic diversity because proportionately more genetic material is brought into the gene pool.

Gene flow has always affected human evolution, but its effects have increased greatly over time. Originally, human populations tended to be small and isolated (among the topics of chapter  13). Only during the last 10,000 years, with the development of agriculture and with major population increases, have humans had widespread interaction.

FIGURE 4.25 Gene Flow New genetic material can be introduced into a population through gene flow from another population. Say, for example, that a population in one place has genes for only brown hair. Members of that population interbreed with an adjacent population, which has genes for only blond hair. After interbreeding for a generation, both populations have genes for blond and brown hair. As a result, when people from either population interbreed with yet another population, they may contribute alleles for brown, blond, or both.

Generation 1 Generation 2

D ive

rs ity

1.00

.95

.90

.85

.80

.75 Matrilocal mtDNA

Patrilocal mtDNA

Matrilocal Y chromosome

Patrilocal Y chromosome

mtDNA and Y chromosome variation

FIGURE 4.26 Social Structure in mtDNA and Y Chromosome Diversity In patrilocal societies, generally speaking, males stay in the birthplace, females migrate out, and female mates come from elsewhere. In matrilocal societies, females stay in the birthplace, males migrate out, and male mates come from elsewhere. To test the hypothesis that the out- migration of females and the out- migration of males produce different patterns of genetic diversity, the geneticist Hiroki Oota and colleagues studied six groups in Thailand, three of them patrilocal and three matrilocal. They found predictable patterns in the diversity of mtDNA and of Y chromosomes. Since mtDNA is passed from mother to daughter and son, the patrilocal groups showed high mtDNA variation (brought about by females moving into new villages) and the matrilocal groups showed low mtDNA variation (brought about by females remaining in place). Since the Y chromosome is passed from father to son, the patrilocal societies showed low Y chromosome variation (from males not migrating) and the matrilocal societies showed high Y chromosome variation (from males moving to new villages and introducing new Y chromosomes).

FIGURE 4.24 Nancy Wexler Wexler, whose mother died of Huntington's chorea, here stands in front of a chart showing genetic histories she tracked in studying the disease.

Gene Flow: Spread of Genes across Population Boundaries | 95

populations produce offspring (Figure 4.25). The key determinant for the amount of gene flow is accessibility to mates— the less the physical distance between pop- ulations, the greater the chance of gene flow. While mutation increases genetic variation between two populations over time, gene flow decreases such variation. Anthropologists and geneticists have found that for many kinds of biological traits, ranging from cranial shapes to blood types to microsatellite DNA markers (see “Polymorphisms: Variations in Specific Genes” in chapter 3), similarity increases the closer one population is to another population.

Migration does not necessarily bring about gene flow. For example, when east Asians first migrated to North America (see “Founder Effect: A Special Kind of Genetic Drift,” above), they reached a continental landmass where no humans had ever lived. Written records suggest that Vikings first traveled from Greenland to Newfoundland around AD 1000, but there is no evidence that they interbred with the native people. The first significant gene flow involving Native Americans and Europeans seems to have occurred when or soon after Christopher Columbus and his crew arrived in the New World, in 1492. From that point on, gene flow in the Americas, North and South, has been extensive.

Gene flow and genetic variation are also highly influenced by social structure (Figure  4.26). Endogamous societies— for example, Australian aborigines— have relatively little genetic diversity because few individuals migrate into the commu- nity and thus little new genetic material is introduced. Exogamous societies have relatively high genetic diversity because proportionately more genetic material is brought into the gene pool.

Gene flow has always affected human evolution, but its effects have increased greatly over time. Originally, human populations tended to be small and isolated (among the topics of chapter  13). Only during the last 10,000 years, with the development of agriculture and with major population increases, have humans had widespread interaction.

FIGURE 4.25 Gene Flow New genetic material can be introduced into a population through gene flow from another population. Say, for example, that a population in one place has genes for only brown hair. Members of that population interbreed with an adjacent population, which has genes for only blond hair. After interbreeding for a generation, both populations have genes for blond and brown hair. As a result, when people from either population interbreed with yet another population, they may contribute alleles for brown, blond, or both.

Generation 1 Generation 2

D ive

rs ity

1.00

.95

.90

.85

.80

.75 Matrilocal mtDNA

Patrilocal mtDNA

Matrilocal Y chromosome

Patrilocal Y chromosome

mtDNA and Y chromosome variation

FIGURE 4.26 Social Structure in mtDNA and Y Chromosome Diversity In patrilocal societies, generally speaking, males stay in the birthplace, females migrate out, and female mates come from elsewhere. In matrilocal societies, females stay in the birthplace, males migrate out, and male mates come from elsewhere. To test the hypothesis that the out- migration of females and the out- migration of males produce different patterns of genetic diversity, the geneticist Hiroki Oota and colleagues studied six groups in Thailand, three of them patrilocal and three matrilocal. They found predictable patterns in the diversity of mtDNA and of Y chromosomes. Since mtDNA is passed from mother to daughter and son, the patrilocal groups showed high mtDNA variation (brought about by females moving into new villages) and the matrilocal groups showed low mtDNA variation (brought about by females remaining in place). Since the Y chromosome is passed from father to son, the patrilocal societies showed low Y chromosome variation (from males not migrating) and the matrilocal societies showed high Y chromosome variation (from males moving to new villages and introducing new Y chromosomes).

96 | CHAPTER 4 Genes and Their Evolution: Population Genetics

Specific genetic markers in living populations, such as the ABO blood group system, provide evidence of gene flow across large regions. For example, the fre- quencies of type B blood change gradually from eastern Asia to far western Europe (Figure  4.27). This clinal— that is, sloping— trend was first noted, in the early 1940s, by the American geneticist Pompeo Candela, who made the case that the gradient from east to west reflects significant gene flow that occurred as Mongol populations migrated westward from AD 500 to 1500. That is, if Mongols had higher frequencies of the B allele, they might have passed on that allele as they interbred with local populations.

Subsequent data on blood groups, however, have revealed sharp distinctions in frequencies between adjacent populations. These distinctions suggest that, in addition to gene flow, genetic drift within small, isolated groups contributed to the frequency variations.

This chapter and the previous one have discussed inheritance, the genetic code, and genetic change in terms of evolution. Prior to the emergence of evolutionary approaches to the study of human variation, many scientists believed that human variation could be understood through discrete categories called races. The next chapter will address the study of biological diversity, the uses and misuses of biolog- ical classification, and the ways that variation in living people reflects adaptations to diverse and sometimes extreme environments across the earth.

<6% 6–9%

9–12% 12–15%

>15%

FIGURE 4.27 B Blood Type Distribution The frequency of blood type B ranges from 30% in eastern Asia to almost 0% in far western Europe. The main factor contributing to this change was probably gene flow between populations in an east- to- west direction (shown by arrow).

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What Causes Evolution?

Evolution is caused by one or a combination of four forces: mutation, natural selection, genetic drift, and gene flow. Although all four forces are important, natural selection accounts for most evolution.

Cause Definition Examples

Mutation Heritable change in structure or amount of DNA

Sickle- cell anemia Huntington’s chorea Klinefelter’s syndrome Down syndrome

Natural selection

Favoring of individuals with characteristics that enhance survival and reproduction

Sickle- cell anemia Industrial melanism Thalassemia G6PD deficiency Lactase deficiency

Genetic drift Genetic change due to chance

Klinefelter’s syndrome Blood types Hemophilia Achromatopsia Porphyria

Gene flow Transfer of genes across population boundaries

Blood types

C O N C E P T C H E C K !

A N S W E R I N G T H E B I G Q U E S T I O N S

C H A P T E R   4 R E V I E W

What causes evolutionary (genetic) change? • There are four forces of evolution: mutation, natural

selection, genetic drift, and gene flow. These forces result in genetic change over time.

• Mutations are DNA coding errors that are biochemically manifested as permanent changes in the structure or amount of genetic material within cells. Mutations are the only source of new genetic material.

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REVIEW THIS CHAPTER WITH PERSONALIZED, INTERACTIVE QUESTIONS THROUGH IJK, INQUIZITIVE.WWNORTON.COM q

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K E Y T E R M S abnormal hemoglobin admixture anthropogenic balanced polymorphism capillaries deme directional selection disruptive selection endogamous equilibrium exogamous fitness founder effect

frameshift mutation gene pool glucose- 6-phosphate dehydrogenase

(G6PD) Hardy- Weinberg law of equilibrium hemoglobinopathies hemolytic anemias Huntington’s chorea induced mutations Klinefelter’s syndrome macroevolution melanic microevolution

mutagens nonmelanic nonsynonymous point mutation point mutations positive selection reproductive isolation sickle- cell anemia spontaneous mutations stabilizing selection synonymous point mutation thalassemia transposable elements

A N S W E R I N G T H E B I G Q U E S T I O N S

• Although a mutation can occur in any cell, only mutations in gametes have implications for offspring, and therefore they have greater importance for evolution than do mutations in somatic cells.

• Natural selection begins with variation among the individual members of a population. Members with advantageous characteristics survive and reproduce in greater numbers than do members lacking the same characteristics. Allele frequencies can increase, decrease, or remain the same owing to natural selection.

• Advantageous characteristics can be visible, physical attributes (e.g., the peppered moth’s color); invisible, biochemical attributes (e.g., in regions of endemic malaria, the heterozygote advantage of hemolytic anemias or enzyme deficiency); or some combination of the physical and the biochemical.

• Genetic drift is change in gene frequency due to chance. Within smaller populations, chances are greater that gene frequencies will change randomly. Drift was likely an important force in most human evolution, since prior to 10,000 yBP most human populations included fewer than several hundred individuals.

• Gene flow is the transfer of genes across population boundaries. In humans, gene flow became a major force of evolution mostly within the last 10,000 years,

when population sizes increased and created greater opportunities for contact and reproduction

How is evolutionary (genetic) change measured, and how is the cause determined? • Deviation from the proportions of gene frequencies

and genotype frequencies as defined by the Hardy- Weinberg law of equilibrium is used to measure evolutionary change.

• No apparent evolution for a gene or genes is occurring in a population if there is no change in frequency over time (i.e., no proportion change in a population over time).

• If gene frequency is changing, then evolution is likely occurring owing to one or more forces of evolution. The Hardy- Weinberg law of equilibrium only indicates if populations are undergoing evolutionary change (disequilibrium) or not (equilibrium). If evolutionary change is occurring, then the Hardy- Weinberg law does not indicate which particular force (or forces) is the cause. The scientist examines the context for change via various factors, such as change in climate, migration of populations across territorial or geographic boundaries, introduction of new diseases, and change in diet.

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E V O L U T I O N R E V I E W The Four Forces of Evolution Synopsis Physical anthropologists carry out population genet- ics studies to measure the changes in genetic makeup (allele frequencies) from one generation to the next and to explain the evolutionary processes behind these changes. Researchers use the Hardy-Weinberg law to mathematically demonstrate whether or not a population is undergoing evolutionary change with respect to a particular trait. When there is no change in allele frequencies for a trait (and therefore no evolutionary change), the population is said to be in genetic equilibrium for that trait. Deviations from genetic equilibrium are brought about by the four forces of evolution: muta- tion, natural selection, genetic drift, and gene flow. Each of these four forces affects the level of genetic variation within a popula- tion and between populations in different ways, and any one or a combination of these forces may be acting on a population at any given time. Throughout our evolutionary history, humans have been and continue to be subject to the operation of these four forces. Physical anthropologists explain much of the variation observed among modern humans today within the specific context of one or more of these forces.

Q1. In the chapter, microevolution is defined as small-scale evolu- tion that occurs over a few generations, while macroevolution is defined as large-scale evolution that occurs over many (hun- dreds or thousands) of generations. Microevolution can also be defined as changes occurring below the level of species (such as within or between populations), while macroevolution is defined as changes at the species level or above (family, class, order, etc.). Provide an example for each type of evolu- tion. Considering these definitions and your examples, which

one of the four forces of evolution will not be operating on groups undergoing macroevolution?

Hint Think about what defines a species.

Q2. Describe the three patterns of natural selection discussed in this chapter. Of these three, which pattern of selection would be most likely to eventually result in a speciation event?

Q3. Mutations can be either spontaneous (no known cause) or induced (caused by specific environmental agents). What are some environmental agents that could increase the rates of genetic mutations among humans today? What types of mutation have the potential to be the most significant from an evolutionary perspective?

Hint Think about how mutations are passed from one gen- eration to the next.

Q4 . Discuss the example of lactase persistence as it relates to human biocultural variation. Under what environmental condi- tions would those individuals carrying alleles for lactase per- sistence be favored, while their counterparts unable to produce this enzyme would be strongly selected against?

Hint Think about the ways this trait would contribute to greater fitness or reproductive success.

Q5. Provide at least one example each of a modern human popula- tion and nonhuman population in which genetic drift may be an especially important factor impacting variation and evolution.

Hint Think about whether genetic drift is more influential in smaller populations or larger populations.

A D D I T I O N A L R E A D I N G S

Kettlewell, H. B. D.  1973. The Evolution of Melanism. Oxford, UK: Oxford University Press.

Livingstone,  F.  B.  1958. Anthropological implications of sickle cell gene distribution in West Africa. American Anthropologist 60: 533–562.

Mielke, J. H., L. W. Konigsberg, and J. H. Relethford. 2006. Human Biological Variation. New York: Oxford University Press.

Relethford, J. H. 2011. Human Population Genetics. Hoboken, NJ: Wiley- Blackwell.

Ridley, M. 2004. Evolution. Malden, MA: Blackwell Science.

MODERN HUMANS’ SKIN COLORS range from very light to very dark. If all the variants were lined up from lightest to darkest, it would be hard to determine the dividing lines between so- called racial categories. In fact, the number of racial categories differs by whom you ask, from three to 10 or more. Although skin color is an easily observable form of variation among humans, it is not the main form. Most of our variation as a species is invisible to the naked eye and does not divide up into discrete categories.

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5Biology in the Present Living People

I was first introduced to the biology of living people in high school, when my biology teacher assigned the section on race in our textbook. From that reading and class discussion about it, I learned that in America race is complex and important, espe- cially with regard to poverty and inequality. I also learned that, from a biological per- spective, race is a useful way to classify human beings. The teacher informed the class that each human being belongs to one of three races: “Caucasoid,” “Negroid,” and “Mongoloid,” referring respectively to Europeans and western Asians, Africans south of the Sahara Desert, and all other Asians and Native Americans. Simple.

Is racial categorization all that simple? Can human variation be classified? Is race a means of understanding why humans differ in appearance and biology around the world? If the answer to these questions is no, then is there a better way to comprehend the enormous variation among humans today? In addressing these questions in this chapter, I will show that race, as it was presented in my high school biology class, has historical roots. These historical roots have led to a largely incorrect understanding of human biological variation.

In fact, race symbolizes the misperceptions that many Americans and others around the world have about human variation. Traits that are often seen as racial in origin are actually biological adaptations that have been strongly influenced by natural selection. As interpreted by anthropologists, human biological variation consists not of categories but of an evolutionary continuum. A key, underlying concept here is humans’ flexibil- ity toward their environmental circumstances, a process that begins before birth and

Is race a valid, biologically meaningful concept?

What do growth and development tell us about human variation? What are the benefits of our life history pattern?

How do people adapt to environmental extremes and other circumstances?

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continues through adulthood. The study of living human biology, then, emphasizes the enormous developmental flexibility that characterizes Homo sapiens. Simply, the popular perception of race is that race is biology. As you will explore in this chapter, race is not biology. Human biological variation is driven by evolution.

Is Race a Valid, Biologically Meaningful Concept? BRIEF HISTORY OF THE RACE CONCEPT The idea of race— that human variation can be classified— is a recent invention. Early written records do not employ the concept. For example, even though ancient Egyptians represented sub- Saharan Africans in their art, they never referred to the Africans’ race. The Greek historian Herodotus (ca. 484–ca. 420 BC) traveled widely but never wrote about race. Similarly, the great Venetian historian and traveler Marco Polo (1254–1324), who saw more of the known world than anyone else of his day, recorded huge amounts of information about his sojourns in Asia without mentioning race.

The American physical anthropologist C. Loring Brace has argued that the race concept got its start in the fourteenth century, during the Renaissance. Before that time, people traveled gradually, either by walking or on horseback. A day’s journey averaged 40 km (25 mi), over which travelers could observe subtle changes in human variation, such as in skin color, from place to place. When Renaissance- era travelers began covering long distances via oceangoing vessels, they also began categorizing people into discrete groups. In simply taking off from seaports, cov- ering vast bodies of water, and landing at their destinations, these travelers noted obvious  and sometimes profound physical differences in people— say between western Europeans and equatorial Africans— without all the gradations that came between.

The early scientific articulation of the race concept— namely, that living humans could be lumped into different taxonomic groups— first emerged in the eighteenth century. By the 1700s, Europeans had encountered most of the biological diver- sity of the world’s populations. Building on Linnaeus’s taxonomy of organisms (see “Taxonomy and Systematics: Classifying Living Organisms and Identifying Their Biological Relationships” in chapter  2), the eminent German anatomist Johann Friedrich Blumenbach (1752–1840) developed a biological taxonomy of human races, published as his MD thesis at the University of Göttingen in 1775. Blumenbach based his taxonomy on human skin color and other physical traits but mainly on features of the skull, such as the facial projection (Figure  5.1). After studying several hundred skulls he had collected from around the world, he concluded that there were five races of people: Mongoloids, Malays, Ethiopians (Africans), American Indians, and Caucasoids. These types were static— they did not change over time. And while Blumenbach had focused on skulls, his racial taxonomy was subsequently applied to the living populations represented by those skulls. More than any other work, Blumenbach’s study set the tone for the popu- lar perception  of  human variation: that human beings come in categorical types called races.

FIGURE 5.1 Blumenbach’s Skulls Johann Blumenbach created a classification system for humans based on the shapes of crania he collected. Here, he has sketched the four skulls representing four of his five main groups: (from top to bottom) African (Aethiopis), Asian or Mongoloid (Tungusae), Caucasoid (Georgianae), and American Indian (Americani illinoici). This scheme as applied to living humans is still prevalent in the popular perception of human variation. What differences do you see in these skulls?

Is Race a Valid, Biologically Meaningful Concept? | 103

DEBUNKING THE RACE CONCEPT: FRANZ BOAS SHOWS THAT HUMAN BIOLOGY IS NOT STATIC Franz Boas, the founder of American anthropology, was among the first scientists to challenge the taxonomic approach to human biological variation. Specifically, he wanted to test the widely held notion that head shape and other so- called racial markers were static entities, essentially unchanging through time. In the early 1900s, he and his researchers studied some 18,000 immigrant families, calculating the cephalic index— the ratio of head length to head breadth— of parents born in Europe and their children born in the United States. Their results revealed that the adults’ and children’s head shapes differed, not by a lot but by a degree that could be expressed mathematically. This finding undermined the idea, prevalent at the time, that racial types were innately stable. Because the differences that had been cited among various races were not immutable, Boas concluded, the race concept was invalid. Boas’s work laid the foundation for a scientific focus on biological process rather than on typological classification.

SO- CALLED RACIAL TRAITS ARE NOT CONCORDANT Single biological traits, such as cranial shape, had seemed like such a firm basis for racial categories in part because it is so easy to classify when focusing on just one characteristic. What happens when human populations are grouped according to multiple characteristics? In the early 1970s, the American geneticist R. C. Lewontin (b. 1929) tested the race concept by studying global genetic variation. If human races existed, most genetic diversity would be accounted for by them. Focusing on blood groups, serum proteins, and red blood cell enzyme variants, Lewontin found that the so- called races accounted for only about 5%–10% of the genetic diversity. In other words, most variation occurred across human populations regardless of “racial” makeup— human “races” have no taxonomic significance. Since Lewontin’s study, many other genetic studies have reached the same conclusion.

Subsequent studies by other scientists— of wide- ranging characteristics such as genetic traits and cranial morphology— have all shown the same thing: so- called races account for a very small amount of biological variation. Multiple biological traits do not lead to clear- cut racial classifications because traits simply do not agree in their frequency or distribution. One trait might cut across human popu- lations in one way, but another trait cuts across them in another way.

HUMAN VARIATION: GEOGRAPHIC CLINES, NOT RACIAL CATEGORIES If race is not a valid way to account for human diversity, how do we speak mean- ingfully about the enormous range of variation in all kinds of human characteristics around the globe? One important finding from physical anthropologists’ study of human variation is that specific biological traits generally follow a geographic continuum, also called a cline. Think, for example, of two patterns discussed in chapter  4: first, the frequencies of type B blood change gradually from eastern Asia to far western Europe (see Figure 4.26 in chapter 4); second, the human gene that causes the disorder sickle- cell anemia, hemoglobin S, increases in frequency in areas where the parasitic disease malaria is endemic, and it decreases in frequency (to nearly zero) in areas where malaria is not endemic (see Figure 4.15 in chapter 4).

cline A gradual change in some pheno- typic characteristic from one population to the next.

104 | CHAPTER 5 Biology in the Present: Living People

Because living humans are a single, geographically diverse species, their variation is continuously distributed in ways like these and not grouped into discrete categories.

Among the best examples of clinal variation are the skin pigmentations of liv- ing people. From equatorial to higher latitudes, skin color changes in a gradient from dark to light. Exceptions exist, such as the relatively dark skin of Native Americans in the Canadian Arctic, but the single strongest factor in determining skin pigmentation is exposure to ultraviolet radiation (discussed below, see “Solar Radiation and Skin Color”).

One of the most important lessons that physical anthropologists have learned regarding race and human variation is how remarkably variable we are as a species. Yes, there is a common human genome, but each of us possesses biological varia- tions that give us our own personal genetic signature. When we look at the genome at the individual level— the basis of the science of personal genomics— we see how impossible it is to place individuals in biological categories, the so- called races.

Some of the uniqueness of individual genomes, now available for thousands of persons around the globe, is documented in their microsatellites. Microsatellites are repeated segments of DNA that are so different from person to person that they have become an important tool in the identification of humans— living and deceased— in forensic, archaeological, and other contexts (see chapter  3, “Poly- morphisms: Variations in Specific Genes”). However, in circumstances where small populations have been relatively isolated, they can recombine microsatellites through sexual reproduction. Over time, continued population isolation results in the presence of common microsatellite characteristics that may no longer be unique to a person. Using microsatellite analysis, it is possible to identify patterns of genetic variation within and between traditional ethnic groups. For example, in the United States, a study of genomic variation in traditional ethnic groups (e.g., African- descent, European- descent, East Asian- descent) by geneticist Hua Tang and his research team revealed clear clusters of associated microsatellite markers related to ethnicity. However, these clusters do not reveal biological categories but rather are a result of social histories and migration patterns. Over time, these cul- tural trends produce the clinal and other geography-associated variation discussed in this chapter. While this kind of microsatellite study is important in understand- ing genomic variation, the medical community is also exploring potential practical uses of individual genetic variation. Still in its preliminary stages, personal genomic research may lead to a better understanding of individual genetic markers that are linked with specific diseases and their associated health risks, and not with so- called races.

Human variation, then, cannot be subdivided into racial categories. As said best by the physical anthropologist Frank B. Livingstone, “There are no races, there are only clines.” Human variation can be understood far more meaningfully in terms of life history, the biology of growth and development.

Life History: Growth and Development Various factors, genetic and external, influence the human body’s growth (increase in size) and development (progression from immaturity to maturity). DNA pro- vides a blueprint that schedules growth, but environment and events very much influence the actual development from conception through death.

personal genomics The branch of genom- ics focused on sequencing individual genomes.

life history The timing and details of growth events and development events from conception through senescence and death.

Life History: Growth and Development | 105

THE GROWTH CYCLE: CONCEPTION THROUGH ADULTHOOD The bodies of large mammals such as adult humans are made of more than 10 trillion cells, which are produced over the course of about 238 mitoses (or cell divi- sions; see “Mitosis: Production of Identical Somatic Cells” in chapter 3). Mitoses result in all the various types of tissues (bone, blood, and muscle, for example) and organs (brain, stomach, heart, and so on), and they begin from the moment of fertilization. The human growth cycle, from embryo to fetus to child to adult, consists of three stages:

1. The prenatal stage, which includes the three periods, or trimesters, of pregnancy and ends with birth (9 months after conception)

2. The postnatal stage, which includes the neonatal period (about the first month), infancy (the second month to the end of lactation, usually by the end of the third year), childhood (ages 3–7, generally postweaning), the juvenile period (ages 7–10 for girls and 7–12 for boys), puberty (days or weeks), and adolescence (5–10 years after puberty)

3. The adult stage, which includes the reproductive period (from about age 20 to the end of the childbearing years, usually by age 50 for women and later for men) and senescence (the period of time after the childbearing years).

PRENATAL STAGE: SENSITIVE TO ENVIRONMENTAL STRESS, PREDICTIVE OF ADULT HEALTH In humans, the prenatal stage, or pregnancy, lasts nine months. In the first trimes- ter, or three- month period, the fertilized ovum multiplies into millions of cells. Distinctive cell groupings first represent different kinds of tissues, then give rise to the tissues, the organs, the brain, and the various physiological systems. By the end of the second month, the embryo is about 2.5 cm (1 in) long but is recogniz- ably human. Because growth and development are at their most dynamic during this trimester, the embryo is highly susceptible to disruption and disease caused by mutation or environmental factors. Specific stressors, or potentially harmful agents, include the mother’s smoking, consuming alcohol, taking drugs, and pro- viding inadequate nutrition.

In the second trimester, the fetus mainly grows longer, from about 20.3 cm (8 in) at the end of the first month of this trimester to about 35.6 cm (14 in), or three- quarters the length of an average newborn.

The third trimester involves rapid weight growth and organ development. During the final month, the lungs develop and most reflexes become fully coor- dinated. The fetus’s wide range of movement includes the ability to grasp and to respond to light, sound, and touch.

This trimester culminates in birth, the profoundly stressful transition from the intrauterine environment to the external environment. Half of all neonatal deaths occur during the first 24 hours. Most of these deaths are caused by low birth weight (less than 2.5 kg, or 5.5 lb), which is generally linked to one or a combination of multiple stressors, such as maternal malnutrition, smoking, and excessive alcohol consumption. Because individuals of low socioeconomic status tend to be exposed to environmental stresses, their children are prone to low birth weights and early deaths. And a poor intrauterine environment predisposes the person to developing specific diseases later in life.

prenatal stage The first stage of life, beginning with the zygote in utero, termi- nating with birth, and involving multiple mitotic events and the differentiation of the body into the appropriate segments and regions.

postnatal stage The second stage of life, beginning with birth, terminating with the shift to the adult stage, and involving substantial increases in height, weight, and brain growth and development.

lactation The production and secretion of milk from a female mammal’s mammary glands, providing a food source to the female’s young.

adult stage The third stage of life, involving the reproductive years and senescence.

stressors Any factor that can cause stress in an organism, potentially affect- ing the body’s proper functioning and its homeostasis.

intrauterine Refers to the area within the uterus.

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POSTNATAL STAGE: THE MATURING BRAIN, PREPARING FOR ADULTHOOD Each of the five postnatal periods has a different growth velocity, or rate of growth per year (Figure 5.2). During infancy, the period of most rapid growth, the deciduous (or primary) dentition erupts through the gums (Figure 5.3). By the time an infant has completed weaning— when the infant shifts from consuming only milk provided by the mother to consuming external foods— all 20 deciduous teeth have erupted. The time of weaning varies, but the process is often finished by the end of the second or third year. Motor skills such as walking and run- ning develop during the first two years. Cognitive abilities also progress rapidly during this time, reflecting the very rapid growth and development of the brain during infancy (Figure 5.4).

During childhood, general growth levels off but the still rapidly growing brain requires the child to have a diet rich in fats, protein, and energy. The child learns behaviors important to later survival but still depends on adults for food and other resources. Because the child’s dentition and digestive systems are immature, adults sometimes prepare food that is soft and easy to chew. By age two, however, children normally can consume most adult foods.

By about age six, permanent teeth begin to replace primary teeth, and brain growth is completed (Figure  5.5). These hallmark developmental events occur nearly simultaneously, as they do in many other primate species. The eruption of the first permanent molar signals the ability to eat adult food, very high nutritional requirements ceasing once the brain reaches its final weight.

During the juvenile years, growth slows. Although much learning occurs in child- hood, the full- size brain makes possible formalized education and social learning.

Adolescence presents a number of profound biological developments. Sexual maturation commences with puberty, and its visible characteristics are the begin- ning of breast development and menstruation (menarche) in girls, the deepening of the voice and emergence of facial hair in boys, the development of secondary sexual characteristics (changes to genitals), and sexual dimorphism of girls’ and boys’ body sizes. Unlike other primates, humans experience increased growth velocity during this time. When nutrition is adequate and stressors are minimal, the adolescent growth spurt can add as much as 8.9 cm (3.5 in) to boys and some- what less than 7.6  cm (3 in) to girls. Boys complete their growth later than girls, whose growth spurts peak earlier than boys’. Growth spurts either do not happen

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FIGURE 5.2 Human Growth Curve During postnatal life, a human grows at different rates. The highest rate of growth (on this graph, 20 cm/year) occurs during the first few months following birth. Growth velocity decreases through the rest of life, apart from a mid- growth spurt (here, approaching 7 cm/ year) around age eight and an adolescent growth spurt (10 cm/year) following the onset of puberty.

FIGURE 5.3 Deciduous Teeth Deciduous, or baby, teeth form in the fetus and erupt shortly after birth.

FIGURE 5.4 Growth Curves of Body Tissues This chart shows the varying growth curves of the brain, body, dentition, and reproductive system in humans. The brain grows the fastest, reaching full cognitive development around age six. In fact, humans have such a large brain that much of it needs to be attained after birth; if the brain reached full size before birth, women would not be able to pass newborns’ heads through their pelvic regions. Dentition has the next highest growth velocity (see Figures 5.3 and 5.5). The body grows more slowly and continues until as late as 24 or 25 years of age. The reproductive system does not begin substantial growth and development until the onset of puberty, but it reaches completion around age 15–16 for girls.

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Life History: Growth and Development | 107

or are minimized in very highly stressed populations, such as the Quechua Indians, who live in high altitudes of Peru and suffer from cold, overwork, malnutrition, and hypoxia (a condition discussed below, see “High Altitude and Access to Oxygen”).

Prior to the completion of growth, the ends of the long bones— the humerus, radius, and ulna in the arm and the femur, tibia, and fibula in the leg— are separate growth centers called epiphyses. The epiphyses are separated from the main shaft, or diaphysis, by a growth plate containing cells that produce nonmineralized bone substance. As long as bone cells are producing bone substance and the epiph- yses remain unfused, the long bone will continue to grow. The bone continuously grows in width throughout life, but once the epiphyses have fused to the diaphyses the growth in length stops and the individual’s height is set (Figure 5.6).

FIGURE 5.5 Molar Eruption and Brain Development (a) Permanent teeth form during the early years of life and begin to erupt around age six. In this X- ray image, the first permanent molars, called the six- year molars, have erupted. The second permanent molars, the 12-year molars, are still forming and will not erupt for another six years. The crowded anterior dentition, or front teeth, includes the deciduous teeth and new permanent teeth waiting to erupt and take their places. (b) Brain growth and development finish at around the same time as the full eruption of the first permanent molar.

First permanent molar

Second permanent molar

In the 11-week-old fetus’s brain, major regions are differentiated but not fully developed.

The six-year-old child’s brain has reached full size and nearly complete development.

(a) (b)

(a) (b)

FIGURE 5.6 Long Bone Growth (a) This magnetic resonance image (MRI) of a child’s knee shows the joining of the femur, or upper leg bone, with the tibia, or lower leg bone. Long bones like these begin as three separate bones— the diaphysis, or shaft, and two epiphyses, or ends— separated by a growth plate. (b) In this photo of a child’s knee joint, the epiphyses have not yet fused to the diaphysis. The line of union may be visible for several years after the attachment occurs; when it eventually disappears, the bone appears as a single element.

Patella, or kneecap

Diaphysis of femur

Diaphysis of tibia

Epiphysis of femur

Growth plate

(b)(a) Epiphysis of tibia

deciduous dentition Also known as baby teeth or milk teeth, this is the first set of teeth, which forms in utero and erupts shortly after birth.

motor skills Refers to the performance of complex movements and actions that require the control of nerves and muscles.

cognitive abilities Refers to the capacity of the brain to perceive, process, and judge information from the surrounding environment.

sexual dimorphism A difference in a physical attribute between the males and females of a species.

nonmineralized Refers to bone reduced to its organic component.

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Biologically, adulthood is signaled by the completion of sexual maturity, the reaching of full height, and the fusion of the epiphyses. The social maturity and behavioral maturity associated with adulthood, however, are difficult to define. In fact, sociologists and social psychologists argue that social maturity is a lifelong process, developing earlier in some biologically mature individuals than in others.

While bone growth and epiphyseal fusion are influenced by genes and sex hor- mones (androgens and estrogens), the amount of growth and the terminal length of bones are strongly affected by environment, especially by nutrition and general health. Negative environmental effects in the present and in the historical past, such as downturns in nutrition, have been documented worldwide. The American economic historians Dora Costa and Richard Steckel have shown, for example, that between 1710 and 1970 substantial changes occurred in the heights of Ameri- can males of European descent (Figure 5.7). Initially, a gradual increase in heights likely reflected improved living conditions and food availability. The sharp decline in heights around 1830 coincided with the urbanization trend. As people moved from rural, agricultural settings to overly crowded cities, they were exposed to more diseases that were easily passed from person to person. In addition, high population densities caused great accumulations of garbage and waste, which may have polluted water supplies and thus exposed people to more bacteria, viruses, and parasites that caused infection and disease. As living conditions improved at the beginning of the twentieth century, as trash removal became mandatory and sewers were constructed, height increased. Today, Americans’ heights are among the greatest in the country’s history, thanks to reliable food supplies, unpolluted water, and access to medical care.

This twentieth- century trend of increasing tallness, sometimes called a secu- lar trend, has been noted in many other countries as well. Multiple factors have contributed to particular causes from place to place, but the collective increase in stature has resulted from improvements in disease control and nutrition. In wealthy nations, the increase in height has come to a stop or slowed considerably, most likely because growth has reached its genetic limit. In many less wealthy (and thus less healthy) nations, growth potential has not been reached and growth periods are comparatively slow. For example, as the American anthropologist Barbara Piperata has documented, in Brazil’s Amazon River basin the suboptimal nutrition and exposure to infectious disease have resulted in less- than- optimal growth (Figure 5.8).

secular trend A phenotypic change over time, due to multiple factors; such trends can be positive (e.g., increased height) or negative (e.g., decreased height).

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FIGURE 5.7 Changes in Height Beginning in the 1700s, the heights of soldiers, students, and slaves were routinely collected for identification or registration purposes. By combining these data with subsequent figures, Costa and Steckel discovered patterns of increase and decline in the heights of American- born males of European descent. From about 171.5 cm (67.5 in) in the early 1700s, heights rose to about 174 cm (68.5 in) around 1830, then sharply declined by 5.1 cm (2 in) over the next 70 years. After the late 1800s, heights increased by a few centimeters or a couple of inches per year throughout the twentieth century. Simply, the extraordinarily poor sanitation and health conditions in nineteenth- century cities resulted in increased disease, stress, and attenuated growth. The subsequent increase in Americans’ heights reflected improvements in sanitation, nutrition, and health.

Life History: Growth and Development | 109

The growth and development of males, prenatally and postnatally, are more sensitive to environmental insult than are the growth and development of females. Human biologists have found much evidence of these differences in developing countries, but they have not been able to explain the mechanisms at work. In terms of evolution, it would make sense for females to have developed buffers from stress because females’ roles in reproduction, including pregnancy and lactation, are much more demanding than males’.

When a period of growth disruption occurs before adulthood, the resulting height deficit can be made up through rapid growth. In one long- term study, of the Turkana in Kenya, growth has been documented to continue into early adulthood. Turkana children tend to be shorter than American children. However, the Turka- na’s growth extends well into their 20s, and Turkana adults are as tall as American adults. Few long- term growth studies have been done of nutritionally stressed pop- ulations, so we do not know about many other settings in which growth extends into adulthood. By and large, in areas of the world experiencing nutritional stress, adults are short owing to lifelong nutritional deprivation.

ADULT STAGE: AGING AND SENESCENCE Throughout life, the body continuously grows and develops. By adulthood, its basic structure has been formed, so during this period most growth and development involve the replacement of cells and of tissues. In fact, over a person’s lifetime nearly every cell and tissue in the body is replaced at least once every seven years.

Aging basically means “becoming older,” but it refers collectively to various social, cultural, biological, and behavioral events that occur over a lifetime but do not by themselves increase the probability of death. Senescence, which accom- panies aging, is a biological process characterized by a reduction in homeostasis, the body’s ability to keep its organs and its physiological systems stable in the face of environmental stress. Senescing persons are increasingly susceptible to stress and death and have a decreased capacity to reproduce. For example, older adults

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FIGURE 5.8 Height and Economically Disadvantaged Populations As this graph shows, some populations of (a) Brazilian boys and (b) Brazilian girls grow at rates less than the smallest 5% of American children. In countries such as Brazil, as in late nineteenth- century America, poor environmental conditions have led to slowed growth and shorter adult height.

aging The process of maturation.

senescence Refers to an organism’s bio- logical changes in later adulthood.

homeostasis The maintenance of the inter- nal environment of an organism within an acceptable range.

110 | CHAPTER 5 Biology in the Present: Living People

produce less body heat than younger adults and hence are more uncomfortable in cold temperatures.

Whereas the previous life stages are generally predictable in their timing (mostly due to genetic programming), the chronology of senescence is highly variable. Menopause, the loss of ovarian function, is a key element of female senescence, marking the end of the reproductive phase and the end of childbear- ing. As a human biological universal, menopause usually occurs by age 50, but it varies by several years in different populations. Male senescence is different in that men normally produce sperm well into their 70s and 80s. However, the number of well- formed sperm and their motility decline by half after age 70. Male and female individuals older than 70 years, having lived through senescence, are considered elderly.

As discussed in chapter  3, bone loss is a senescence universal. That is, after age 40 humans suffer increased bone porosity and reduction in bone mass. The increased susceptibility to bone fracture that comes with this loss is called oste- oporosis (Figure  5.9). In extreme cases, osteoporosis can weaken bone to the point that it easily fractures under small amounts of stress. This fragile nature commonly leads to fractures such as broken hips or to “compression” fractures of vertebrae, in which the bone simply cannot support the normal body weight and collapses. The collapse of several vertebrae can give the person a hunchback. Far more common in women than in men— because a loss of the hormone estrogen is linked to bone loss— osteoporosis shows less age variation than menopause does. Other factors that can predispose people to this condition are smoking, chronic diseases, and some medications.

For every stage from conception through senescence, humans (and other primates) have evolved strategies for enhancing their survival and reproductive potential, the prime movers of natural selection. In the next section, we will examine behaviors that are central to this adaptive success.

menopause The cessation of the men- strual cycle, signifying the end of a female’s ability to bear children.

osteoporosis The loss of bone mass, often due to age, causing the bones to become porous, brittle, and easily fractured.

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FIGURE 5.9 Osteoporosis (a) As this graph shows, men and women reach their maximum bone mass around age 30. (b) The loss of bone mass becomes evident in the grayish areas of X- rays (arrows). Notice the porous pelvic bones, which with normal bone mass would be solid white.

Life History: Growth and Development | 111

EVOLUTION OF HUMAN LIFE HISTORY: FOOD, SEX, AND STRATEGIES FOR SURVIVAL AND REPRODUCTION Two behaviors make possible the survival and adaptive success of humans and other primates: acquisition of food and reproduction. Unlike the other primates, humans acquire food and reproduce within the contexts of culture and society.

Life History Stages in Humans: Prenatal, Postnatal, and Adult

A life history is the biological story, from conception to death, of an individual, a population, or a species. A life history provides insight into how energy is allocated to key events, such as reproduction, brain growth, and the care of offspring. It also sheds light on the interactions between genes and environment at crucial stages.

Stage Period Timing and Characteristics

Prenatal First trimester Fertilization to twelfth week; embryo development; organ development

Second trimester

Fourth through sixth lunar months; rapid growth in length

Third trimester Seventh month to birth; rapid growth in weight and organ development

Postnatal Neonatal Birth to 28 days; first exposure to extrauterine environment; most rapid postnatal growth and development

Infancy Second month to 36 months; rapid growth; breast- feeding; deciduous tooth development; other milestones (e.g., walking); weaning at end of period

Childhood Three to seven years; moderate growth; eruption of first permanent molar; completion of brain growth

Juvenile Seven to 10 years (girls), seven to 12 years (boys); slower growth; self- feeding; cognitive transition in learning and increased ability to learn

Puberty Days to few weeks at end of juvenile years; activation of sexual development; marked increase in secretion of sex hormones

Adolescence Five- to 10-year period after puberty; growth spurt (earlier in girls than boys); completion of permanent dental development and eruption; development of secondary sex characteristics; interest in adult social, sexual, and economic behaviors

Adult Prime Twenty years to end of reproductive years; stability in physiology, behavior, and cognition; menopause in women, commencing at about age 50

Senescence End of reproductive years to death; decline in function of many tissues and organs; homeostasis more easily disrupted than in earlier years; grandmother social behaviors

C O N C E P T C H E C K !

SOURCE: Adapted from Table 11.1 in B. Bogin and B. H. Smith. 2012. Evolution of the human life cycle. Pp. 515–586 in S. Stinson, B. Bogin, and D. O’Rourke, eds. Human Biology: An Evolutionary and Biocultural Perspective. 2nd ed. Hoboken, NJ: Wiley- Blackwell.

112 | CHAPTER 5 Biology in the Present: Living People

For example, humans have created social institutions— especially kinship and marriage— and beliefs and rules supporting these institutions. Anthropologists are keenly interested in the relations between humans’ sociocultural behaviors and the evolution of our unique life history, especially in comparison with other primates’ life histories.

PROLONGED CHILDHOOD: FAT- BODIED MOMS AND THEIR BIG- BRAINED BABIES Humans have a relatively prolonged childhood. However, within this life period the spans of infancy and lactation are quite short. The mother’s brief intensive child care allows her, theoretically, to have more births and to invest her resources among all her children.

The cost of this fertility advantage is the large amount of food the mother must provide for her children. The energy demands of the children’s maturing brains require that this food be highly nutritious: rich in fats, protein, and energy. For only the first several years of a child’s postnatal life can the mother provide these resources, via lactation, from her own stored body fats and other nutrients. Even during this period, a mother will begin to supplement the child’s diet with other solids (around four to six months).

GRANDMOTHERING: PART OF HUMAN ADAPTIVE SUCCESS Humans are also the only primates that experience, at the other end of the life history, prolonged  postmenopausal survival. Some apes have a postmenopausal period, but it is briefer than humans’. Ethnographic evidence from cultures around the world shows that postmenopausal women, most often grandmothers, play import- ant roles in caring for children, provisioning food to children, and providing essential information about the world to various members of their social groups (Figure  5.10). Because older people can become key repositories of knowledge about culture and society, longevity may have a selective advantage in humans but not in other primates.

FIGURE 5.10 Grandmother Postmenopausal women are often caregivers to children, frequently to their grandchildren. As more and more families have both parents working, child care by grandparents, and grandmothers in particular, has become especially important.

Adaptation: Meeting the Challenges of Living | 113

Adaptation: Meeting the Challenges of Living Humans adjust remarkably well to new conditions and to challenges. As in other organisms, such adaptations— functional responses within particular environ- mental contexts— occur at four different levels. Genetic adaptation, as discussed in previous chapters, occurs at the population level via natural selection. Here, the biological change is inherited and is not reversible in a person (e.g., someone with sickle- cell anemia). Developmental (or ontogenetic) adaptation occurs at the level of the individual during a critical period of growth and development, child- hood especially. The capacity to make the change is inherited, but the change is not inherited and is not reversible. For example, children living at high altitudes develop greater chest size prior to reaching adulthood than do children living at low altitudes. The expanded chest reflects the need for increased lung capacity in settings where less oxygen is available (discussed further below, see “High Altitude and Access to Oxygen”). Acclimatization (or physiological adaptation) occurs at the individual level, but unlike developmental adaptation, it can occur anytime during a person’s life. In this kind of adaptation, the change is not inherited and can be reversed. For example, exposure to sunlight for extended periods of time results in tanning (also discussed further below, see “Solar Radiation and Skin Color”). Lastly, cultural (or behavioral) adaptation involves the use of material culture to make living possible in certain settings. For example, wearing insulated clothing keeps people from freezing in extreme cold.

The American physical anthropologist Roberto Frisancho applies the term functional adaptations to the biological adjustments that occur within the indi- vidual’s lifetime (that is, developmental adaptations and acclimatizations). Most functional adaptations are associated with extreme environmental conditions, such as heat, cold, high altitude, and heavy workload. Some of these conditions appear to have brought about genetic changes in humans. That is, over hundreds of generations humans have adapted to settings in which specific attributes enhance the potential for survival and reproduction. Skin pigmentation, for example, is related genetically to solar radiation exposure.

All adaptations have one purpose: maintenance of internal homeostasis, or main- tenance of the normal functioning of all organs and physiological systems. Not to maintain homeostasis in body temperature, for example, or in oxygen accessi- bility or in strength of the bones of the skeleton has severe consequences for the individual, including work impairment and loss of productivity, decline in quality of life, and even death. The maintenance of homeostasis involves all levels of any organism’s biology, from biochemical pathways to cells, tissues, organs, and ulti- mately the entire organism.

To determine how humans maintain internal homeostasis, anthropologists employ indirect approaches and direct ones. Indirect approaches involve the study of populations in their natural environments, such as the Quechua Indians living in highland Peru or the Inuit living in Greenland. The observation of living populations as they engage in various activities in various settings provides great insight into functional adaptations, helping establish associations between specific biological attributes and environmental settings or circumstances. Direct approaches, by con- trast, involve the replication of environmental conditions and of human responses

functional adaptations Biological changes that occur during an individual’s lifetime, increasing the individual’s fitness in the given environment.

114 | CHAPTER 5 Biology in the Present: Living People

to these conditions. In the course of such experiments, anthropologists determine cause- and- effect relationships, such as body response to temperature extremes.

CLIMATE ADAPTATION: LIVING ON THE MARGINS HEAT STRESS AND THERMOREGULATION Like all other mammals, humans are homeothermic, meaning they maintain a constant body temperature. A con- stant core temperature is essential for normal physiology, including brain function, limb function, and general body mobility. Humans can tolerate a body temperature higher than their normal 98.6 °F, but a body temperature above 104–107 °F for an extended period leads to organ failure and eventually death. Extremely hot weather can thus result in many deaths, such as in the summer of 2003, when at least 35,000 and perhaps as many as 50,000 people died in Europe during one of the hottest seasons ever recorded. Severe heat stress is experienced mostly in tropical settings, where it is hot much of the year, and during hot spells in temperate regions.

A body experiencing heat stress attempts to rid itself of internally and exter- nally derived heat sources. Internal heat is produced by the body’s metabolism, especially during activities involving movement, such as physical labor, walking, and running. External heat is derived from the air temperature. The initial physiological response to an elevated temperature is vasodilation, the dilation (expansion) of the blood vessels near the body’s surface. By increasing blood vessels’ diameter, the body is able to move more blood (and associated heat) away from the body’s core to the body’s surface. The red face of a person who is in a hot environ- ment is the visible expression of vasodilation.

Sweating is another response to heat. Sweat is mostly water produced by the eccrine glands, which are located over the entire body’s surface. Evaporation of the thin layer of water on the skin results in cooling of the surface. Humans can sweat a remarkably high volume of water, and this physiological process is central to humans’ long- term functional adaptation to heat.

Sweating is less effective in areas of the body having a dense hair cover than in areas of the body having little or no hair. This relationship suggests that sweating evolved as a thermoregulatory adaptation in association with the general loss of body hair. Humans’ loss of body hair is unique among the primates, indicating that the ther- moregulatory adaptation of hair loss and sweating occurred in human evolution only.

Humans have a strong capacity to adapt to excessive heat. Individuals who have not often experienced such heat are less able to conduct heat away from their cores and less able to sweat than are individuals living in hot climates. Individuals exposed for the first time to a hot climate, however, rapidly adjust over a period of 10–14 days. This adjustment involves a lowering of the body’s core temperature, a lowering of the threshold for when vasodilation and sweating begin, and a reduc- tion of the heart rate and metabolic rate. Overall, women are less able to tolerate heat than are men, in part due to a relatively reduced ability to move blood to the skin through vasodilation and the presence of greater body fat.

Human populations who have lived in hot climates for most of their history— such as native equatorial Africans and South Americans— have the same number of sweat glands as other populations. However, heat- adapted populations sweat less and perform their jobs and other physical functions better in conditions involving excessive heat than do non- heat- adapted populations.

BODY SHAPE AND ADAPTATION TO HEAT STRESS The relationship between body shape and temperature adaptation was first described in the 1800s by a

homeothermic Refers to an organism’s ability to maintain a constant body temperature despite great variations in environmental temperature.

vasodilation The increase in blood vessels’ diameter due to the action of a nerve or of a drug; it can also occur in response to hot temperatures.

Adaptation: Meeting the Challenges of Living | 115

combination of two biogeographic rules, one developed by the German biologist Carl Bergmann (1814–1865) and the other developed by the American zoologist Joel Allen (1838–1921). Bergmann’s rule states that heat- adapted mammal popu- lations will have smaller bodies than will cold- adapted mammal populations. Rel- ative to body volume, small bodies have more surface area, facilitating more rapid heat dissipation. Conversely, large bodies have less surface area, thus conserving heat in cold climates (Figure  5.11). Consequently, human populations adapted to hot climates tend to have small and narrow bodies (discussed further in chap- ter 12). Allen’s rule states that heat- adapted mammal populations will have long limbs, which maximize the body’s surface area and thus promote heat dissipation, whereas cold- adapted mammal populations will have short limbs, which minimize the body’s surface area and thus promote heat conservation.

Exceptions exist to Bergmann’s and Allen’s rules, but by and large these rules explain variation in human shapes that goes back at least 1.5 million years. Popula- tions living in hot climates tend to have narrow bodies and long limbs. Populations living in cold climates tend to have wide bodies and short limbs. This long- term association between body shape and climate means that body shape is mostly a genetic adaptation. However, body shape also involves childhood developmental processes that respond to climatic and other stressors, such as poor nutrition. For example, poor nutrition during early childhood can retard limb growth, especially of the forearm and lower leg, resulting in shorter arms and legs. Ultimately, then, body shape and morphology reflect evolutionary and developmental processes.

COLD STRESS AND THERMOREGULATION Severe cold stress is experienced mostly in places close to Earth’s magnetic poles, such as the Arctic; at altitudes higher than 3 km (10,000 ft); and during cold spells in temperate settings. Hypothermia, or low body temperature, occurs in excessively cold air or immersion in cold water. During the great Titanic disaster, in 1912, many hundreds of passengers and ship’s crew members escaped the sinking vessel but died from hypothermia after floating in the northern Atlantic Ocean (28 °F) for two hours before rescue ships arrived.

Maintaining homeostasis against cold stress involves heat conservation and heat production. The human body’s first response to cold stress is vasoconstriction, the constriction of the blood vessels beneath the skin. Decreasing the diameter

Bergmann’s rule The principle that an animal’s size is heat- related; smaller bodies are adapted to hot environments, and larger bodies are adapted to cold environments.

Allen’s rule The principle that an animal’s limb lengths are heat- related; limbs are longer in hot environments and shorter in cold environments.

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FIGURE 5.11 Bergmann’s Rule This graph illustrates Carl Bergmann’s biogeographic rule: as latitude increases (and temperature decreases), body breadth (as measured by bi- iliac breadth or the maximum breadth between the pelvic bones) also increases. Bergmann’s rule applies to all warm- blooded animals (including humans), which need to maintain a constant body temperature. Physically and physiologically, humans can adapt to a wide range of climates; but since humans are able to move about the earth, human body size may not strictly adhere to the latitude at which a person is living.

hypothermia A condition in which an organism’s body temperature falls below the normal range, which may lead to the loss of proper body functions and, even- tually, death.

vasoconstriction The decrease in blood vessels’ diameter due to the action of a nerve or of a drug; it can also occur in response to cold temperatures.

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of the blood vessels reduces blood flow and heat loss, from the body’s core to the skin. The chief mechanism for producing heat is shivering.

Humans adapt to cold, but the adaptation includes cultural and behavioral factors, practices that societies living in extremely cold settings pass from one generation to the next. That is, people teach their children how to avoid situations involving heat loss. They teach them what clothing to wear, what kinds of shelters to build, and how to keep the interiors of shelters warm. Cold- adapted cultures also know that alcohol consumption contributes to the loss of body heat, increasing the chances of hypothermia and death.

After being exposed to survivable cold for more than a few days, humans shiver less, produce more heat, and have higher skin temperatures. Overall, adjusting to cold means becoming able to tolerate lower temperatures— simply, feeling better in the cold.

To measure heat production, anthropologists take a specific kind of measure- ment called the basal metabolic rate (BMR). Indigenous people living in cold settings, such as the Indians at high altitudes in the Peruvian Andes, have a sig- nificantly higher BMR than do other human populations. The Inuit are among the most studied populations on Earth, owing to their adaptation to the very cold, dry conditions in the Arctic Circle, where average winter temperatures range from –50 °F to –35 °F and even summer temperatures usually do not climb above 46 °F. In part, their high BMR is produced by their diet, which is high in animal protein and fat (about 9 calories per gram) and low in carbohydrates (about 3 calories per gram). Like most cold- adapted populations, however, the Inuit have adapted physiologically by developing a capacity for tolerating excessive cold. For example, their peripheral body temperatures, in the hands and feet, are higher than other peoples’ because of a higher rate of blood flow from the body’s core to the skin.

The Inuit conform to Bergmann’s and Allen’s rules, having large, wide bodies and short limbs. Moreover, they have developed a technology that conserves heat: their traditional housing focuses on insulation; for example, the walls of ice- constructed “igloos” include whale rib rafters that are covered with alternating layers of seal skin and moss. Heat conductivity from a fire built beneath the main floor of the house serves to warm cold air as it rises, which is a simple but highly efficient way to heat a small interior environment.

SOLAR RADIATION AND SKIN COLOR One of the most profound environ- mental factors that humans deal with daily is solar radiation, or the sun’s energy output, which plays a central role in the evolution and development of skin color (Figure 5.12). In daylight, skin— the largest organ and the most conspicuous fea- ture of the human body, accounting for 15% of total body weight— is exposed to ultraviolet (UV) radiation, a component of solar radiation. The American anthro- pologists Nina Jablonski and George Chaplin have shown that the best predictor of skin color, as measured by skin reflectance, is UV radiation exposure. That is, the darkest skin (low skin reflectance) is associated with the highest UV radiation, and the lightest skin (high skin reflectance) is associated with the lowest UV radi- ation. UV radiation is highest at noon, during the summer, at the equator, and in higher altitudes; and skin becomes darker (more pigmented) at these times and in these settings. As a result, individuals living in low latitudes or equatorial regions of the globe have some of the darkest skin pigmentation due to the more direct and prolonged UV light throughout the year. As latitude increases, the amount of UV radiation decreases and so, too, does the amount of melanin in the skin; therefore,

basal metabolic rate (BMR) The rate at which an organism’s body, while at rest, expends energy to maintain basic bodily functions; measured by the amount of heat given off per kilogram of body weight.

Epidermis

Hair follicle

Oil gland

Sweat gland

Dermis

FIGURE 5.12 Structure of Skin Skin’s two main layers are the epidermis, which is external, and the dermis, which is internal. The epidermis makes the skin waterproof and contains keratinocytes, building blocks that manufacture the protein keratin, and melanocytes, specialized cells that produce the skin pigment melanin. The dermis, a thicker layer of tissue, contains hair follicles, sweat glands, blood vessels, and oil glands.

skin reflectance Refers to the amount of light reflected from the skin that can be measured and used to assess skin color.

Adaptation: Meeting the Challenges of Living | 117

the lightest- skinned individuals are usually in the highest latitudes. In general, populations between 20°N latitude and 20°S latitude have the darkest skin.

When first exposed to UV radiation, light skin reddens— the process commonly called sunburn. With ongoing exposure, the melanocytes increase the number and size of melanin granules. In addition, the outer layer of the epidermis thickens. This darkening— that is, tanning— and thickening serves to retard penetration of the epidermis and dermis by UV radiation, protecting the individual from sunburn and possibly cancer. Because melanin is a natural sunscreen, individuals with high melanin content receive the most protection. Thus, people with dark skin, such as in equatorial Africa, are able to tolerate more exposure to sun than are those with light skin. Dark- skinned people have a sun protection factor (SPF) of 10–15; light- skinned people have an SPF of between 2 and 3. Around the world, populations with the most melanin have the fewest skin cancers and malignant melanomas. However, these effects occur largely during or after the late repro- ductive years, suggesting that skin cancer is not an element of natural selection.

SOLAR RADIATION AND VITAMIN D SYNTHESIS The body needs UV radi- ation for the synthesis of vitamin D, a steroid hormone that regulates calcium absorption and mineralization of the skeleton. Today, we obtain some vitamin D through fortified foods and by eating fatty fish such as salmon, but most vitamin D is produced in the skin. UV radiation in the form of UV photons penetrates the skin and is absorbed by a cholesterol- like substance, 7-dehydrocholesterol,  in the epidermis (keratinocytes) and dermis (fibroblasts) layers (see Figure 5.12). This process produces a previtamin D that eventually converts to vitamin D, which is released from the skin and transported via the circulatory system to the liver and kidneys. There, more chemical reactions produce the active form of vita- min  D.  Without this form, the bones do not mineralize properly, resulting in a condition called rickets in children and osteomalacia in adults (Figure 5.13).

In addition to lower- limb deformation, a telltale sign of rickets in children is malformed pelvic bones. Both conditions result when poorly developed bone is unable to withstand the forces of body weight. Women who as children had rickets severe enough to affect the pelvic bones have trouble giving birth because the space for the fetus’s passage during birth is restricted. Because a key element of natural selection is a greater number of births, this decreased reproductive capacity means that the trait— malformed pelvic bones caused by rickets— is disadvantageous.

Melanin, the primary influence on vitamin D synthesis, can be advantageous or nonadvantageous. That is, because melanin provides protection from solar radiation, substantial amounts of this pigment can inhibit vitamin D production. As a result, at high latitudes where there is less UV radiation, lighter skin, with less melanin, is favorable because it allows more solar radiation to be absorbed, enabling vitamin D production. In fact, as world populations today reveal, there is a strong correlation between distance of a population from the equator and degree of skin pigmentation: the closer a population is to the equator, the darker the skin pigmentation. Simply, skin needs to be dark enough to protect from UV radiation but light enough to allow solar radiation sufficient for vitamin D production.

The American physiologist William Loomis has hypothesized that as human ancestors moved out of Africa into the more northerly latitudes of Europe and elsewhere, their dark skin would not have produced enough vitamin D to bring about calcium absorption and skeletal development. Therefore, in those latitudes, natural selection strongly favored alleles for light skin. This scenario suggests that

melanocytes Melanin- producing cells located in the skin’s epidermis.

melanin A brown pigment that determines the darkness or lightness of a human’s skin color due to its concentration in the skin.

sun protection factor (SPF) The rating calculated by comparing the length of time needed for protected skin to burn to the length of time needed for unprotected skin to burn.

FIGURE 5.13 Rickets Photographed in Hungary in 1895, these children are suffering from rickets, a disorder in which poorly mineralized bones, especially the weight- bearing leg bones, become soft, are prone to fracture, and can warp or bow. Rickets was especially prevalent in the 1800s in Europe and America. In urban settings, in particular, indoor work and air pollution decreased access to sunlight and exposure to UV radiation.

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prior to 1 mya all of our ancestors lived in what is now Africa and that their skin was pigmented highly so that it would block dangerous UV radiation.

SOLAR RADIATION AND FOLATE PROTECTION Support for the evolution of skin pigmentation in humans is provided by the fundamental role of melanin in the protection of stored folate (folic acid) in our bodies. New research shows that folate is essential for the synthesis and repair of DNA and therefore directly affects cell division and homeostasis. Even very tiny deficiencies of folate have been linked to a range of health issues, including neural tube defects whereby the brain or spinal cord does not form properly, cleft palate, pregnancy loss, and reduced sperm production. Folate levels decline dramatically with exposure to high and prolonged levels of UV radiation. However, skin color and melanin production are key elements in protecting the body from folate depletion. Thus, natural selection would have played a key role in maintaining relatively dark skin in regions of the world with high UV- radiation exposure.

HIGH ALTITUDE AND ACCESS TO OXYGEN At high altitudes, generally defined as greater than 3 km (10,000 ft) above sea level, a fall in barometric pres- sure reduces oxygen molecules. The primary environmental stress in such places is hypoxia, the condition in which body tissues receive insufficient amounts of oxygen (Figure 5.14). Secondary stresses include high UV radiation, cold, wind, nutritional deprivation, and the rigors of living in highly variable, generally rugged terrain.

The severity of hypoxia increases as a person moves higher, and the associated risk increases because all body tissues and physiological processes require an unin- terrupted oxygen supply. Hypoxia results in mountain sickness, with headache, nausea, loss of appetite, fatigue, and breathlessness occurring at about 2.4  km (8,000 ft) during rest and about 1.9 km (6,500 ft) during physical activity. For some individuals living at sea level or in prehypoxic conditions who travel to high alti- tudes or otherwise experience hypoxia, mountain sickness becomes a life- threatening condition. For most people, the symptoms disappear within the first

FIGURE 5.14 High Altitudes As this map shows, each continent except for Australia and Antarctica has at least one high- altitude area (shaded in red). A lack of oxygen is among the conditions to which humans must adapt at high altitudes.

hypoxia Less than usual sea- level amount of oxygen in the air or in the body.

Adaptation: Meeting the Challenges of Living | 119

few days of exposure as the body begins to more efficiently use reduced amounts of oxygen in the air and homeostasis is restored. Extra red blood cells and oxygen- saturated hemoglobin are produced. The hemoglobin transports oxygen to body tissues, while an expansion in the diameter of arteries and of veins allows increased blood flow and increased access to oxygen.

Additional physiological changes represent a long- term response to hypoxia. A person who moved to the high- altitude settings of the Himalayas, for example, would function better there over time. A young child who moved there would,

Adaptation: Heat, Cold, Solar Radiation, High Altitude

Humans display both short- term adjustments and long- term adaptations to environmental extremes. These responses are crucial for maintaining homeostasis.

Setting Exposure and Adaptation Characteristics

Heat First exposure Vasodilation, profuse sweating; but effects reduce with continuous exposure

Functional adaptation Less sweating, normal work performance

Genetic adaptation Narrow body, long limbs

Cold First exposure Vasoconstriction, shivering; but effects reduce after continuous exposure brings warmer skin temperature

Functional adaptation Tolerance to cold and to lowering of skin temperature, metabolic rate higher than that of nonadapted populations, peripheral body temperature higher than that of nonadapted populations

Genetic adaptation Large, wide body; short limbs

Solar/UV radiation

First exposure Reddening of skin (sunburn), followed by increased melanin production by melanocytes

Functional adaptation Tanning, thickening of skin

Genetic adaptation High melanin production (dark skin)

High altitude

First exposure Hypoxia results in headache, nausea, loss of appetite, fatigue, and breathlessness; but symptoms disappear after a few days

Functional adaptation Greater diameter of arteries and veins and greater relative blood flow to body tissues, greater lung volume, more efficient use of oxygen, larger chest size in some populations (reflecting greater lung volume)

Genetic adaptation High oxygen saturation in hemoglobin

C O N C E P T C H E C K !

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through the process of growth, develop greater lung volume and the ability to use oxygen more efficiently. Human populations who have lived at high altitudes for many generations— such as those in the Peruvian Andes— have larger chest cavi- ties than do populations at low altitudes, reflecting the high- altitude populations’ inherited increases in lung volume. However, these populations are generally shorter than their low- altitude counterparts. Widespread growth retardation results from the increased energy required to live in cold environments with little oxygen and poor nutrition. But some biological attributes associated with living at high altitudes may offer selective advantages. For example, the American phys- ical anthropologist Cynthia Beall and colleagues have found that Tibetan women with alleles for high oxygen saturation in their hemoglobin, a factor that enhances the body’s access to oxygen, have more surviving children. Thus, hypoxia at high altitudes can be an agent of natural selection (Figure 5.15).

NUTRITIONAL ADAPTATION: ENERGY, NUTRIENTS, AND FUNCTION MACRONUTRIENTS AND MICRONUTRIENTS Climate is only one key area in which humans adapt. We also adapt to diet, or the kinds of foods we eat, and nutrition, the deriving of nutrients from those foods. Such adaptation is crucial to acquiring the necessary energy and nutrients for reproduction, growth, and development.

Each body function requires a certain amount of energy and particular nutri- ents, and a lack of energy or of nutrients can hamper body functions. Like many other primates (the other primates are discussed in chapter  6), humans are omnivorous, eating a wide range of both plants and animals. This dietary plas- ticity enhances our access to the nutrients we need for function and survival, and in terms of adaptability and evolution it reflects humans’ unique combination of biology and culture.

FIGURE 5.15 Tibetan Farmers Tibetan farmers live in high- altitude areas and are shorter than Tibetans living in lowlands. Among the nomads’ physical and physiological adaptations to their environment are large lungs, better lung function, and higher oxygen saturation in arteries.

Adaptation: Meeting the Challenges of Living | 121

Nutritionists have developed two sets of dietary recommendations: those based on energy requirements and those based on nutrient requirements. Measured in calories, the minimum energy needed to keep a person alive is called the basal metabolic requirement. A person needs additional energy for other functions, such as work and exercise, thermoregulation, growth, and reproduction (pregnancy and lactation). The total daily energy expenditure (TDEE) consists of the basal metabolic requirement plus all the other energy requirements, and we fulfill all these energy requirements by consuming specific macronutrients (carbohydrates, fats, and proteins) in food and micronutrients (vitamins and minerals) in food as well as in multivitamins. Table  5.1 shows the daily minimum amounts of nutri- ents recommended in the United States. The lack of these essential vitamins and minerals, even those recommended in small amounts, can have devastating effects. For example, lack of folate in a pregnant woman can lead to neural tube defects, such as spina bifida, in the fetus. Many foods we commonly eat in the United States, such as cereal, bread, and milk, are fortified with some of these essential nutrients.

HUMAN NUTRITION TODAY The majority of human populations across the world are undernourished (consuming fewer than 2,000 calories per day), espe- cially in developing nations of Africa, of South and Central America, and across large regions of Asia (Figure  5.16). In the later twentieth century, governments across the world collaborated on increasing agricultural production to relieve fam- ine and starvation. Currently, resources are directed at enhancing the nutritional attributes of key grains, particularly rice and corn. As a result of these international efforts, grains are more readily available and of better quality. This focus on grains has contributed, however, to a growing decline in the diversity of foods consumed by human populations, especially in nutritionally stressed settings. Increased agri- cultural production might help meet populations’ caloric needs, but attention is shifting to increasing the availability of additional micronutrients— such as vitamin A, vitamins B6 and B12, vitamin D, iodine, iron, and zinc— through meat and other animal products.

Among the consequences of poor nutrition is the suppression of the immune system. Owing to poor living circumstances and poor sanitation conditions, mean- while, undernourished populations are especially susceptible to the spread and maintenance of infectious disease. Thus, undernutrition and infection work hand in hand— each exacerbates the other, and the combination is much worse for the health and well- being of the individual than is either one alone.

FIGURE 5.16 Malnutrition Malnutrition is a substantial problem in many parts of the world. Both of its forms— undernutrition, or insufficient consumption of calories and/ or micronutrients, and overnutrition, or excessive consumption of calories and/or micronutrients— can have detrimental health consequences. Chronic undernutrition is a persistent problem for populations of many developing nations. This emaciated Somalian man, for example, has not been able to consume enough food to sustain normal body weight.

basal metabolic requirement The minimum amount of energy needed to keep an organism alive.

total daily energy expenditure (TDEE) The number of calories used by an organism’s body during a 24-hour period.

macronutrients Essential chemical nutri- ents, including fat, carbohydrates, and protein, that a body needs to live and to function normally.

micronutrients Essential substances, such as minerals or vitamins, needed in very small amounts to maintain normal body functioning.

TABLE 5.1 Dietary Reference Intakes for Selected Nutrients

Nutrient (units) Child 1–3 Female 19 –30 Male 19 –30

Macronutrients

Protein (g) 13 46 56

(% of calories) 5–20 10–35 10–35

Carbohydrate (g) 130 130 130

(% of calories) 45–65 45–65 45–65

Total fiber (g) 14 28 34

(Continued)

122 | CHAPTER 5 Biology in the Present: Living People

Nutrient (units) Child 1–3 Female 19 –30 Male 19 –30

Total fat (% kcal) 30–40 20–35 20–35

Saturated fat (% kcal) <10% <10% <10%

Linoleic acid (g) 7 12 17

(% kcal) 5–10 5–10 5–10

α-Linoleic acid (g) 0.7 1.1 1.6

(% kcal) 0.6–1.2 0.6–1.2 0.6–1.2

Cholesterol (mg) <300 <300 <300

Minerals

Calcium (mg) 500 1,000 1,000

Iron (mg) 7 18 8

Magnesium (mg) 80 310 400

Phosphorus (mg) 460 700 700

Potassium (mg) 3,000 4,700 4,700

Sodium (mg) <1,500 <2,300 <2,300

Zinc (mg) 3 8 11

Copper (g) 340 900 900

Selenium (g) 20 55 55

Vitamins

Vitamin A (g RAE) 300 700 900

Vitamin D (g) 5 5 5

Vitamin E (mg AT) 6 15 15

Vitamin C (mg) 15 75 90

Thiamin (mg) 0.5 1.1 1.2

Riboflavin (mg) 0.5 1.1 1.3

Niacin (mg) 6 14 16

Vitamin B6 (mg) 0.5 1.3 1.3

Vitamin B12 (g) 0.9 2.4 2.4

Choline (mg) 200 425 550

Vitamin K (g) 30 90 120

Folate (g DFE) 150 400 400

USDA food pattern using goals as targets

1,000 2,000 2,400

RAE = retinol activity equivalent; AT = alpha- tocopherol; DFE = dietary folate equivalent.

SOURCE: United States Department of Agriculture, fnic.nal.usda.gov.

TABLE 5.1 (Continued)

Adaptation: Meeting the Challenges of Living | 123

Universally, undernourished populations experience stunted growth, resulting in shortness for age. The American economist David Seckler has hypothesized that shortness in height is an adaptation to reduced food supplies, one with no costs to individual health. The record shows quite the opposite, however: individuals who are undernourished typically have poor general functioning, reduced work capac- ity, ill health, and shortened life expectancy. Short individuals might require fewer calories and nutrients, but the associated health cost for them can be profound. Moreover, it is highly unlikely that undernourished populations’ shortness is a genetic adaptation. Where energy and nutrition became adequate or abundant fol- lowing periods of disruption and deprivation, body size rebounded. For example, in many countries, especially in Europe and Asia, World War II had a profoundly negative impact on growth. In the Netherlands, 1944 and 1945 were known as the “starving years.” Following the war, children and adults began growing again thanks to the return of adequate nutrition (Figure 5.17).

OVERNUTRITION AND THE CONSEQUENCES OF DIETARY EXCESS Much of the above discussion about nutrition focused on shortfalls and the consequences of not getting enough of some nutrient or food or energy. Increasingly around the

World War I World War II

H ei

gh t (

cm )

160

150

140

130

120

100

Year

1910 1920 1930 1940 1950 1960

Boys Girls

Ages 14–15

Ages 12–13

Ages 10–11

Ages 7–8

FIGURE 5.17 Malnutrition and Height Height is a sensitive indicator of diet and health. During periods of insufficient nutrition, growth can be slowed or arrested, leading to reduced adult stature. If, however, proper nutrition is restored before adulthood, a recovery period can follow, during which growth “catches up” to where it should be. This graph shows the heights of boys and girls of various ages in Germany during and after World Wars I and II. During the wars, food shortages negatively affected growth in height. Following the wars, food was more abundant and growth was not inhibited. What might account for the general increase in growth from 1910 through 1950?

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world, the problem is becoming just the opposite: too much food and too many of the wrong kinds of food. These dietary choices have negative consequences for health and well- being (Figure  5.18). In the United States, adults have increased their body weight by an average of 11 kg (24 lb) over the last four decades, and over 50% of adults are overweight. The average weight of six- to 11- year- old children increased from 29 kg (65 lb) in 1963–65 to 33 kg (74 lb) in 1999–2002. Today, 20% of American children are overweight or obese. Obesity was mostly unknown in the 1950s, but since the early 1990s it has become a “growing” problem, not only in the United States but also in some areas of the Pacific, most of Europe and the Middle East, Latin America, and South Africa. The World Health Organization reported that in 2015 nearly 2 billion people globally are overweight.

The reasons for the remarkable increase in numbers of overweight and obese people are complex, but they basically boil down to the increased ability of our society to produce inexpensive food, most of which is high in fat, and advances in transportation technology, which provides greater access to cheap food sources. In general, people are consuming more at home and elsewhere. For example, the portions of food consumed in restaurants are vastly greater now than several decades ago. Calorie- dense pasta servings are as much as five times greater than US Department of Agriculture recommendations. In the last century, single serv- ings of soft drinks more than tripled. More and more people, in other words, are expending less and less energy to consume a poor diet, rich in calories and low in micronutrients. The combination of increased calorie consumption and reduced activity and energy expenditure is fueling the obesity pandemic.

As obesity rates have climbed, so have rates of hypercholesterolemia, or high cholesterol, a predisposing factor for coronary heart disease. The cholesterol levels of traditional hunter– gatherers (and of our ancestors) averaged 125 mg/dl (milligrams per deciliter of blood), but the average level of Americans today well exceeds 200 mg/dl. The hunter– gatherers ate a lot of meat, just as we do; but the nondomesticated animals of 15,000 yBP contained very low levels of cholesterol- elevating saturated fatty acids, especially compared with the very high fat content

FIGURE 5.18 Overnutrition Like undernutrition, overnutrition has many negative consequences for health and well- being. As this graph shows, the risks of diabetes, high blood pressure, and high cholesterol increase substantially as BMI increases. BMI, or body mass index, is a statistical measure of weight according to height. A BMI between 18.5 and 24.9 indicates that a person has normal weight for his or her height. A BMI between 25 and 29.9 means “overweight,” while 30 or above means “obese,” where excess weight is so extreme that health and function are compromised.

% o

f a du

lts b

y B

M I c

at eg

or y

BMI (kg/m2)

60

40

20

10

50

30

18.5–24.9 ≥3530.0–34.927.0–29.925.0–26.9 0

Type 2 diabetes High blood pressure High cholesterol

hypercholesterolemia The presence of high levels of cholesterol in an organism’s blood; this condition may result from the dietary consumption of foods that promote high cholesterol or through the inheritance of a genetic disorder.

Adaptation: Meeting the Challenges of Living | 125

of today’s domesticated animals. In addition, hydrogenated vegetable fats and oils and very high levels of trans- fatty acids contribute some 15% of the energy in the average American diet. Clearly, these changes in consumption are culturally influenced. That is, people learn to eat what they eat. This is an important char- acteristic of our evolution.

At the same time that the global epidemic of obesity is taking place, there is an epidemic of non- insulin- dependent diabetes mellitus, or type 2 diabetes. More than 100 million people suffer from the disease worldwide. Historically, type 2 dia- betes was associated with overweight individuals older than 40. Since about 1990, however, more and more young adults and adolescents have been affected. The key elements of this complex disease are abnormally high blood glucose levels and excessive body weight, both of which result from excessive caloric consumption. Glucose, weight, and other biological signals prompt the pancreas to produce and secrete abnormal amounts of the hormone insulin. Eventually, insulin resistance develops at specific target tissues: muscle, fat, and the liver. The lack of insulin denies these target tissues key nutrients used for fuel and storage. This denial of nutrients is not the major health problem, however, because glucose— a necessary source of energy— is still stored as fatty acids in fat tissue. From the fat tissue, it is pushed into liver and muscle cells, so a person with type 2 diabetes typically becomes fatter and fatter.

The major health problem is that the extra glucose increases the blood’s vis- cosity, and the thickened blood damages blood vessels in the kidneys, eyes, and extremities. In advanced stages of the disease, the kidneys function poorly, vision is reduced, and blood does not flow adequately to the hands, arms, feet, and legs. There is also a greater chance of cardiac disease and stroke.

Is there an adaptive component to the disease? In the early 1960s, the Ameri- can geneticist James V. Neel noted the high percentages of type 2 diabetes among Native Americans. In the early twentieth century, the disease had been virtually nonexistent in Native Americans; but after World War II, it increased to the point of affecting more than half of some Native American tribes. Neel hypothesized a “thrifty genotype,” one that during times of plenty stored energy efficiently in the form of glucose in fat tissue. For Native Americans, who lived a feast- or- famine lifeway, such a thrifty genotype for a rapid insulin trigger would have been a ben- efit. For populations that lived an abundant lifeway, the consequences of type 2 diabetes would have triggered a selection against the thrifty genotype.

Given the data in the 1960s, when only some populations around the world had type 2 diabetes, Neel’s hypothesis made a lot of sense. Since that time, however, populations around the world have been experiencing an alarming increase in the disease, all in regions where people are becoming obese. Current projections indicate that by 2020 one- quarter of the US population will develop the disease. Little evidence supports the idea that some populations, such as Native Americans, have a thrifty genotype.

If genetic causes or susceptibilities do not explain the remarkable increase in type 2 diabetes, then why is there such a high frequency in some Native Americans, such as in the Pima of the American Southwest, where 50% of adults are afflicted?  To understand the cause of the disease among Native American and other high- susceptibility groups, we need to view the disease in terms of nutritional history. Studies of populations show a strong association between poor maternal nutrition during pregnancy (usually leading to low- birth- weight babies) and devel- opment of type 2 diabetes among these offspring in later life. The American anthropologist Daniel Benyshek and his colleagues have made a strong case that

type 2 diabetes A disease in which the body does not produce sufficient amounts of insulin or the cells do not use available insulin, causing a buildup of glucose in the cells.

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Native Americans and other populations with a high incidence of type 2 diabetes share a common history of severe nutritional deprivation. Moreover, the effects of malnutrition are perpetuated for generations, even in subsequent generations no longer experiencing malnutrition. That is, the metabolism of children gestated under such conditions becomes permanently “programmed,” in turn leading to comparable developmental programming effects in their children. Thus, the cycle can continue for generations.

In other Native American populations, such as those inhabiting the Aleutian Islands, Alaska, the incidence of type 2 diabetes is relatively low. Unlike native populations in the American Southwest, Aleutian Islanders do not have a history of severe malnutrition. During adulthood, too little activity and too many calories are risk factors for any population. But the impact of poor diet on the growing fetus is crucial for understanding the high prevalence of type 2 diabetes in humans today.

WORKLOAD ADAPTATION: SKELETAL HOMEOSTASIS AND FUNCTION Homeostasis depends on the health of all the body’s tissues, including the bone tissues. The skeleton must be maintained so that it can support the body and enable the body to move. Without this essential framework, where would tendons, ligaments, and muscles be attached and how would they get the leverage needed for their use?

Bones’ growth and development are subject to a range of factors. Strongly con- trolled by genes, they are also affected by various physiological processes, disease, and nutrition. As discussed above, poor nutrition in childhood may result in short

Nutritional Adaptation

Food and the nutrition it provides are critical aspects of human life. Both under- and overnourishment have negative consequences for all human populations.

Condition Characteristics

Undernutrition Too few calories and/or specific required nutrients; reduced growth, slower growth, susceptibility to infection, predisposition to adult disease (e.g., cardiovascular disease), and early adult death

Overnutrition Too many calories, resulting in excess stored fat (obesity); associated health risks include type 2 diabetes, osteoarthritis, hypertension, cardiovascular disease, stroke, early adult death

C O N C E P T C H E C K !

FIGURE 5.19 Framework of the Human Body Just as a building needs its framework, the human body needs the skeleton for support and rigidity. In addition to maintaining the body’s shape and enabling its movement, the skeleton protects the many vital organs (such as by encasing the brain in the cranium). It makes possible the production of red blood cells (within the marrow cavities of bones). And it serves as a storage facility for minerals, which can be retrieved at any time (but which minerals would you expect to be stored in bone?).

Adaptation: Meeting the Challenges of Living | 127

stature, both in children and in the adults they become. Various mechanical forces also affect bones’ growth and development. The bones of the arms and legs, for example, are subject to bending and torsion, or twisting, whenever they are used. Bones’ rigidity, or strength, is a functional adaptation to these forces, preventing fracture in the course of normal use (Figure  5.19). During growth and develop- ment, physical activity stimulates bone- forming cells, called osteoblasts, which produce bone mass where it is needed to maintain the rigidity of specific bones and bone regions. In the absence of physical activity, other cells, called osteo- clasts, remove bone mass. A principle called Wolff’s Law lays out the homeostatic balance of osteoblastic and osteoclastic activity, in which bone mass is produced where it is needed and taken away where it is not needed.

Wolff’s Law also accounts for the remodeling of bone that occurs during life, the changing of certain bones’ shapes as the result of particular activities. Because the movements of tendons, ligaments, and muscles put stress on individual bones, repetitive actions eventually can cause those bones to reinforce themselves by add- ing more material. Just as you need to reinforce a shelf if it starts to buckle under the weight it holds, so the body is likely to try preventing a bone from breaking under added weight or stress (Figure 5.20).

At the other end of the spectrum, people who are physically inactive— such as from partial or full immobilization— have less dense bones because osteoblasts are not stimulated to produce bone mass (Figure  5.21). The resulting decline in bone density may weaken the skeleton. For example, the skeletons of astronauts who have been in outer space for extended periods of time have remarkable loss in bone density. Around the world, children who are less physically active tend

rigidity (bone) Refers to the strength of bone to resist bending and torsion.

osteoblasts Cells responsible for bone formation.

bone mass The density of bone per unit of measure.

osteoclasts Cells responsible for bone resorption.

Wolff’s Law The principle that bone is placed in the direction of functional demand; that is, bone develops where needed and recedes where it is not needed.

Left humerus

Right humerus

(a) (b)(a) (b)

FIGURE 5.20 Skeletal Remodeling and Athletics The “playing” arms of athletes in certain sports undergo remodeling as a result of stress. (a) A baseball pitcher or a tennis player (such as, here, the professional player Amelie Mauresmo) typically has a dominant arm, which is used to a much greater degree than the nondominant arm. (b) The upper arm bone, or humerus, of the dominant arm may be much stronger than that of the nondominant arm. In these cross sections, note the greater diameter of the right humerus.

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to have smaller and less developed bones than children who are more physically active. Children with less bone mass due to habitual physical inactivity become predisposed, as adults, to osteoporosis and fracture. Similarly, in one study of mili- tary recruits’ leg bones, young men and women who had better- developed muscles and greater bone mass were less susceptible to fractures than were young men and women who had less- developed muscles and less bone mass.

Studying the larger picture of human variation, anthropologists have learned that highly physically active human populations— those that do lots of walking, lifting, carrying, or anything else that “stresses” the skeleton— have bones with optimum density. In addition, the diameters of long bones in populations with active lifestyles are greater than those in populations that are physically inactive. These greater diameters provide the bones with higher rigidity, increasing their ability to resist bending and torsion (this phenomenon is discussed further in chapter 12).

EXCESSIVE ACTIVITY AND REPRODUCTIVE ECOLOGY The biological benefits of physical activity are clear. Exercise improves physical fitness by contributing to bone strength, helping lower blood pressure and cho- lesterol, increasing heart function and lung function, and so on. Exercise that becomes an excessive workload, however, can hinder female reproductive function, a crucial factor in evolution. Many studies have shown that an excessive work- load, such as regular intense aerobic exercise, can interrupt menstrual function, resulting in lower fertility. Even milder levels of physical activity have reduced the reproductive potential of some women. For example, a study of a large number of women from Washington State revealed that those who engage in more than an hour of exercise per day and whose body weights are 85% that of the average Amer- ican woman are five to six times more likely to not be able to conceive within one year than are women who do not exercise and have normal weight. Two important implications stand out from this and other studies on workload and ovarian func- tion. First, human populations requiring heavy work by reproductive- age women will have reduced birthrates. Second, and in the larger picture of human adaptation and evolution, amount of work is an important selective factor— a population with relatively high fitness will likely not require excessive energy expenditure, at least for reproductive- age women.

Anthropologists have shown that the classification of humans into different types, or races, simply does not provide meaningful information about variation. While race may be an enduring social concept, it is not valid biologically. Understand- ing human variation in an evolutionary context— that is, understanding people’s remarkable adaptability to a wide range of environmental circumstances through- out the stages of growth, from conception through old age and senescence— is far more productive than attempting to classify different types of the human organism. Just as humans represent a continuum, so they are part of a larger continuum that includes their fellow primates, with whom they share a range of characteristics, many common adaptations, and much evolutionary history. As we will explore in the next chapter, the nonhuman primates provide an important record of adaptability and flexibility, one of the great success stories of mammalian evolution.

Strong compact bone

Weak compact bone

Healthy bone Bone showing signs of osteoporosis

FIGURE 5.21 Bone Disuse When bones are not used routinely or for extended periods of time, bone density can decrease. Typically, the loss occurs on the inner surface of the bone, making the bone more fragile. The outer, compact bone becomes thinner as the bone marrow, or medullary cavity, in the middle increases in diameter. In this drawing, the osteoporotic bone, on the right, has a much thinner outer compact bone and a larger bone marrow cavity than does the healthy bone.

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Is race a valid, biologically meaningful concept? • Race is a typological leftover from pre- evolutionary,

taxonomic interpretations of biological variation. Race is neither a useful nor an appropriate biological concept.

• Human variation is clinal. In general, traits (skin color, cranial form, and genetic polymorphisms) do not correlate in their distribution. There would have to be a concordance of traits for races to exist.

What do growth and development tell us about human variation? What are the benefits of our life history pattern? • Differentiation and development of all the body

organs occur during the prenatal stage of life. Environmental stress during this stage predisposes the individual to disease later in adulthood.

• The postnatal stage— from infancy to childhood to the juvenile period to adolescence to adulthood— involves growth acceleration and deceleration. Childhood and adolescence are long events, in which adult behaviors are learned, individuals become completely mature, and the reproductive capacity develops.

• Old age and senescence have long been ignored as important life stages. The length of the period is unique to humans. Individuals older than 50 play important roles in the care of young, in food provisioning for the young, and as sources of information for other members of their kin groups and societies.

How do people adapt to environmental extremes and other circumstances? • Humans are remarkably responsive to their

surrounding environments. Some adaptations to the environment are genetic (e.g., skin color), whereas

others occur within the individual’s lifetime and either have a genetic basis and are irreversible (e.g., lung volume in high altitude) or have a genetic basis and are reversible (e.g., skin tanning). Biological change associated with all forms of adaptation occurs to maintain homeostasis.

• Most functional adaptations— adaptations that occur during the individual’s lifetime— have important implications for evolution, such as selection for darker skin near the equator and for lighter skin in northern latitudes.

• Skin color (pigmentation) is subject to forces of evolution. Evolution of skin color is strongly influenced by environmental circumstances, especially by the amount of UV radiation. UV radiation is the catalyst for the skin’s synthesis of vitamin D. Light skin evolved in areas with reduced UV radiation.

• Adaptation in high altitudes where less oxygen is available includes increased lung volume and a circulatory system that more efficiently transports oxygen throughout the body. Some differences between high- altitude populations and other populations may be evolutionary (genetic), such as high oxygen saturation in the high- altitude populations.

• Undernutrition is not the result of adaptation— the body either receives adequate nutrition and access to energy (calories) and nutrients or it is deficient in these resources. Nutritional deficiencies promote growth disruption, disease, and reduced fertility. Much of the human population globally is deficient in energy, nutrients, or both. In developed and underdeveloped nations around the world, obesity is a growing health threat, and associated health problems include high blood pressure, type 2 diabetes, osteoarthritis, various cancers, and heart disease.

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• The key element of workload adaptation is skeletal function and maintenance of bone strength. Strength of bone and its ability to support the body are determined by the density and distribution of bone tissue in cross section.

• High levels of physical activity have a negative effect on women’s reproductive potential.

K E Y T E R M S adult stage aging Allen’s rule basal metabolic rate (BMR) basal metabolic requirement Bergmann’s rule bone mass cline cognitive abilities deciduous dentition diaphyses epiphyses functional adaptations growth velocity homeostasis homeothermic hypercholesterolemia

hypothermia hypoxia intrauterine lactation life history macronutrients melanin melanocytes menarche menopause micronutrients motor skills nonmineralized osteoblasts osteoclasts osteoporosis personal genomics

postnatal stage prenatal stage rigidity (bone) secular trend senescence sexual dimorphism skin reflectance stressors sun protection factor (SPF) total daily energy expenditure

(TDEE) type 2 diabetes vasoconstriction vasodilation weaning Wolff’s Law

E V O L U T I O N R E V I E W Human Variation Today

Synopsis The biocultural approach of physical anthropology emphasizes that human evolution and variation are shaped by both biology and culture, that is, by both genetic factors and envi- ronmental factors. Physical anthropologists apply this concept in various ways. For instance, human life history stages are unique compared with those of other primate species, and the relationship between our unique life history and sociocultural behaviors is an area of interest. Additionally, human populations across the globe vary in the ways that homeostasis (physiological equilibrium) is maintained, and such adaptations are a product of evolutionary

processes operating over a wide range of environmental settings. The broad range of human adaptability—to life in hot and cold cli- mates, among extremes of latitude and altitude, and with variable access to key nutrients—is a major contributor to the success of our species: humans survive and reproduce across a diverse array of environments worldwide.

Q1. Define Bergmann’s rule and Allen’s rule in relation to climate adaptation. What is one example of an environmental factor that can lead to the development of body-shape characteris- tics that deviate from those predicted by these two rules?

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Q2. What is clinal variation? Identify two physiological effects of solar radiation that likely acted as selective pressures in shap- ing the pattern of clinal variation observed for human skin color.

Q3. In early life, human females are more highly buffered against environmental stresses than are human males. In addition, human females enter puberty, adolescence, and reproductive senescence earlier than human males do. Why are such fea- tures advantageous from an evolutionary standpoint?

Hint Focus on implications for fitness, or reproductive success.

Q4 . In what ways have each of the four types of adaptation dis- cussed in this chapter contributed to the ability of human populations to inhabit areas spanning the entire surface of

the globe? Consider various factors, including climate and nutrition.

Hint Think about an extreme geographical setting. How might the ways that a resident maintains homeostasis differ from the ways a visitor maintains homeostasis?

Q5. Many scientists characterize the conditions of modern pop- ulations worldwide (but especially Western societies) as conducive to an obesity pandemic. Discuss the ways in which adaptive features from our evolutionary past may have become modern maladaptations.

Hint Think about the differences in nutritional resources and activity patterns between ourselves and our hominin ancestors.

A D D I T I O N A L R E A D I N G S

Barker, D. J. P. 1996. The origins of coronary heart disease in early life. Pp. 155–162 in C. J. K. Henry and S. J. Ulijaszek, eds. Long- Term Consequences of Early Environment: Growth, Development and the Lifespan Developmental Perspective. Cambridge, UK: Cambridge University Press.

Bogin,  B.  1999. Patterns of Human Growth. 2nd  ed. Cambridge, UK: Cambridge University Press.

Brace, C. L. 2005. “Race” Is a Four- Letter Word: The Genesis of a Concept. New York: Oxford University Press.

Crews, D. E. 2003. Human Senescence: Evolutionary and Biocul- tural Perspectives. Cambridge, UK: Cambridge University Press.

Edgar,  H.  J.  H.  and  K.  L.  Hunley, eds. 2009. Race reconciled. American Journal of Physical Anthropology (Special Symposium Issue) 139:1–102.

Frisancho, A. R. 1993. Human Adaptation and Accommodation. Ann Arbor: University of Michigan Press.

Gould, S. J. 1996. The Mismeasure of Man. New York: Norton.

Jablonski, N. G. 2006. Skin: A Natural History. Berkeley: University of California Press.

Marks,  J.  1995. Human Biodiversity: Genes, Race, and History. New York: Aldine de Gruyter.

Muehlenbein,  M.  P., ed. 2010. Human Evolutionary Biology. Cam- bridge, UK: Cambridge University Press.

Stinson, S., B. Bogin, and D. O’Rourke, eds. 2012. Human Biology: An Evolutionary and Biocultural Perspective. 2nd ed. Hoboken, NJ: Wiley- Blackwell.

Wolpoff, M. H. and R. Caspari. 1997. Race and Human Evolution: A Fatal Attraction. New York: Simon & Schuster.

E V O L U T I O N R E V I E W

THE ORANGUTANS (Pongo pygmaeus) of Borneo and Sumatra represent the remarkable arboreal adaptation in the living great apes. They live in tropical settings that range from mountains to swamps. Close and long- lasting social bonds develop between mothers and their offspring.

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6 Why study primates?

What is a primate?

What are the kinds of primates?

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Biology in the Present The Other Living Primates

B I G Q U E S T I O N S ?Do you remember the first time you saw a primate (besides a human one, that is)?1 I first saw a primate on a school trip to the Kansas City Zoo. My third- grade class and our teacher walked up to an enclosure containing several monkeys. I could not take my eyes off the faces of those animals. In so many ways, they looked just like us! Their eyes were on the fronts of their faces, they had different facial expres- sions, and they had grasping hands. For fear of retaliation from my fellow classmates, I did not point out the resemblances I saw between monkeys and people, including them. But I came away from that experience wondering why monkeys shared so many physical attributes with humans.

I did not think much about that trip to the zoo until I took my first physical anthro- pology class in college, 10 years later. My introduction to physical anthropology pro- fessor explained that monkeys, like humans, are members of the order Primates and that one key unifying feature of all primates is forward- facing eyes. This feature is part of the generalized and arboreal adaptation that unites this amazing group of ani- mals and indicates their common ancestry. Research by primatologists— scientists who study primates— had revealed one of the most impressive characteristics of primates: their marvelous ability to adapt to new or changing circumstances. My question was answered! Monkeys and humans share features because they share ancestry. They are not identical today because at some point in the remote past their ancestors diverged.

1Throughout this chapter and the remainder of the book, primate or primates refer to nonhuman primates except where otherwise specified.

134 | CHAPTER 6 Biology in the Present: The Other Living Primates

One key indicator of primates’ adaptability is the fact that they are able to live almost anywhere— they inhabit many kinds of landscapes and widely diverse cli- mates, ranging from the bitter cold of northern Japan to the humid tropics of Brazil (Figure 6.1). Anyone who has ever studied nonhuman primates for any length of time will tell you that they have other characteristics as impressive as their adapt- ability: their intelligence, their long lives, their variable diets, and their complex social behavior.

Primatologists come from a range of disciplines. Many are in anthropology departments in universities and colleges around the world, but primate studies are also part of disciplines such as biology, ecology, psychology, paleontology, anatomy, zoology, and genetics. In addition, animal and plant conservationists study primates as a barometer of species losses and extinctions. Many primates live in the tropics, which are disappearing by the hundreds of thousands of acres around the world annually, mostly due to forest clearing and encroachment by people; if primates are disappearing, then so are many other animals.

Prosimians

Tree shrews

Lemurs

Lorises

Tarsiers

New World Monkeys

Cebids

Marmosets

Old World Monkeys

Baboons and macaques

Colobuses and langurs

Guenons and mangabeys

Apes

Gibbons

Orangutans

Chimpanzees

Bonobos

Gorillas

FIGURE 6.1 Primate Distribution As shown on this map, primates inhabit every continent except Antarctica and Australia. New World primates live in North and South America, while Old World primates live in Europe, Africa, and Asia. Although they are often considered tropical animals that live in forested settings, primate species exist in a wide range of environments.

What Is a Primate? | 135

Among the practical applications for the study of primates are advances in med- icine. Many types of primates have some of the same or closely related diseases as humans. In the last 50 years, millions of human lives have been saved around the world because of the study of diseases found in primates and humans. For example, chimpanzees are susceptible to polio. The vaccine for polio, a once- dreaded dis- ease that killed and debilitated millions around the world, was developed via primate research in the 1950s.

The physical and behavioral similarities between apes and humans provide important clues about the origins of humans (discussed further in chapter 9). The similarities between the muscles and bones of apes and of humans, for example, enable us to conjecture about what the common ancestor and the earliest hominin may have looked like. The study of primate behavior provides insights into our own behavior and perhaps even the origins of specific behaviors, such as cognition, par- enting, social interactions, and (some argue) even conflict and warfare.

These diverse issues make the study of primates so interesting and important, far more than I imagined that day at the zoo. In this chapter, we will define the order Pri- mates and discuss how primates are classified (taxonomy), where they live (ecology and geography), and their physical characteristics (anatomy). In the next chapter, we will look at key aspects of primates’ social behavior, especially in the important link- age between social organization, ecology, and diet (socioecology). What you learn in this and the following chapter will provide the essential context for your under- standing Part II of this book, which is about the evolution of primates and of humans.

What Is a Primate? When Linnaeus first defined the order Primates, in the eighteenth century (see “Taxonomy and Systematics: Classifying Living Organisms and Identifying Their Biological Relationships” in chapter 2), he did so purely for classification purposes and focused on descriptive traits. Physical anthropologists, however, define pri- mates on the basis of behavioral, adaptive, or evolutionary tendencies. The emi- nent British anatomist Sir Wilfrid E. Le Gros Clark (1895–1971) identified three prominent tendencies:

1. Primates are adapted to life in the trees— they express arboreal adaptation in a set of behaviors and anatomical characteristics that is unique among mammals;

2. Primates eat a wide variety of foods— they express dietary plasticity; 3. Primates invest a lot of time and care in few offspring— they express parental

investment.

In addition to these tendencies, the physical and behavioral characteristics dis- cussed below identify primates as a separate order of mammals.

One thing that all anthropologists agree on when they talk about primates is the order’s remarkable diversity. The panoramic view displayed in Figure  6.2 provides a sense of that diversity. Depicted in the Taï Forest, in Ivory Coast, West Africa, are one kind of ape (chimpanzee), eight kinds of monkeys ( black- and- white colobus, Campbell’s, Diana, lesser spot- nosed, putty- nosed, red colobus, olive colo- bus, sooty mangabey), and three kinds of strepsirhines (potto, Demidoff’s galago,

arboreal adaptation A suite of physical traits that enable an organism to live in trees.

dietary plasticity A diet’s flexibility in adapting to a given environment.

parental investment The time and energy parents expend for their offspring’s benefit.

I1

ENHANCED TOUCH

Primates have an enhanced sense of touch. This sensitivity is due in part to the presence of dermal ridges (fingerprints and toe prints) on the inside surfaces of the hands and feet. The potto, a prosimian, has primitive dermal ridges, whereas the human, a higher primate, has more derived ridges, which provide better gripping ability.

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GENERALIZED SKELETAL STRUCTURE

Primates have a generalized skeletal structure. The bones that make up the shoulders, upper limbs, lower limbs, and other major joints such as the hands and feet are separate, giving primates a great deal of flexibility when moving in trees. In this monkey skeleton, note the grasping hands and feet, the long tail, and the equal length of the front and hind limbs relative to each other.

REDUCED SMELL

Primates have a reduced sense of smell. The smaller and less projecting snouts of most primates indicate their decreased reliance on smell.

DIETARY VERSATILITY

Primates have dietary plasticity. Part of the record of primate dietary adaptation is found in the teeth. The red colobus monkey dentition shown here is typical of a catarrhine dentition with a 2/1/2/3 dental formula. Note the differences in morphology of the four different tooth types: incisors (I1, I2), canines (C), premolars (P3, P4), and molars (M1, M2, M3).

ENHANCED VISION

Primates have an enhanced sense of vision. Evolution has given primates better vision, including increased depth perception and seeing in color. The eyes’ convergence provides significant overlap in the visual fields and thus greater sense of depth.

Human Potto

Overlapping visual fields

Taï Forest

MonkeyDog

Reduced snout length

I1 I2I2

CC

P3P3 P4P4 M1

M2

M3

M1

M2

M3

I1I1 I2I2 CC

P3P3

P4P4

M1

M2

M3

M1

M2

M3

Black-and-white colobus

Campbell’s

Chimpanzee

Demidoff’s galago

Diana monkey

Human

Lesser spot-nosed

Olive colobus

Potto

Putty-nosed

Red colobus

Sooty mangabey

Thomas’s galago

Eagle

F I G U R E

6.2 Primate Adaptation in Microcosm: The Taï Forest, Ivory Coast, West Africa

I1

ENHANCED TOUCH

Primates have an enhanced sense of touch. This sensitivity is due in part to the presence of dermal ridges (fingerprints and toe prints) on the inside surfaces of the hands and feet. The potto, a prosimian, has primitive dermal ridges, whereas the human, a higher primate, has more derived ridges, which provide better gripping ability.

Em er

gi ng

c an

op y

M ai

n ca

no py

U nd

er st

or y

GENERALIZED SKELETAL STRUCTURE

Primates have a generalized skeletal structure. The bones that make up the shoulders, upper limbs, lower limbs, and other major joints such as the hands and feet are separate, giving primates a great deal of flexibility when moving in trees. In this monkey skeleton, note the grasping hands and feet, the long tail, and the equal length of the front and hind limbs relative to each other.

REDUCED SMELL

Primates have a reduced sense of smell. The smaller and less projecting snouts of most primates indicate their decreased reliance on smell.

DIETARY VERSATILITY

Primates have dietary plasticity. Part of the record of primate dietary adaptation is found in the teeth. The red colobus monkey dentition shown here is typical of a catarrhine dentition with a 2/1/2/3 dental formula. Note the differences in morphology of the four different tooth types: incisors (I1, I2), canines (C), premolars (P3, P4), and molars (M1, M2, M3).

ENHANCED VISION

Primates have an enhanced sense of vision. Evolution has given primates better vision, including increased depth perception and seeing in color. The eyes’ convergence provides significant overlap in the visual fields and thus greater sense of depth.

Human Potto

Overlapping visual fields

Taï Forest

MonkeyDog

Reduced snout length

I1 I2I2

CC

P3P3 P4P4 M1

M2

M3

M1

M2

M3

I1I1 I2I2 CC

P3P3

P4P4

M1

M2

M3

M1

M2

M3

Black-and-white colobus

Campbell’s

Chimpanzee

Demidoff’s galago

Diana monkey

Human

Lesser spot-nosed

Olive colobus

Potto

Putty-nosed

Red colobus

Sooty mangabey

Thomas’s galago

Eagle

138 | CHAPTER 6 Biology in the Present: The Other Living Primates

Thomas’s galago). All but the strepsirhines are active during the day. (The humans are, of course, primates as well. The eagle is an important predator of monkeys, especially the red colobus.)

ARBOREAL ADAPTATION— PRIMATES LIVE IN TREES AND ARE GOOD AT IT Many animals— such as squirrels, nondomesticated cats, some snakes, and birds— have successfully adapted to living in trees. Primates, however, display a unique combination of specific arboreal adaptations. Even the few primates that spend all or most of their time on the ground have retained, over the course of their evolution, a number of features shared with an arboreal common ancestor.

PRIMATES HAVE A VERSATILE SKELETAL STRUCTURE Primates get around in trees using an unusually wide range of motions involving the limbs and body trunk. One has only to watch many of the primates perform their acrobatics in the forest canopy to appreciate this versatility, a function of the primate body’s anatomy. That is, the bones making up the shoulders, limbs, hands, and feet tend to be separate. These separate bones are articulated at highly mobile joints.

Atop the list of separate bones is the collarbone (the clavicle), which acts as a strut, keeping the upper limbs to the sides of the body. The lower forelimb (the ulna and radius) and the fingers and toes (the phalanges) also have separate bones. The forearm rotates from side to side with relative ease, and the dexterity of the hands and feet is unparalleled among mammals.

One of the most important attributes of the primate hand is the opposable thumb— on either hand, the tip of the thumb can touch the tips of the other four fingers. Thus, the primate can grasp an object or manipulate a small one. Humans have the longest thumb, or pollex, among primates and therefore the greatest opposability (Figure  6.3). This elongated thumb is part of the unique adaptation of the human hand for what the English anatomist and evolutionary biologist John Napier calls the power grip and the precision grip. In the power

(a) Power grip (human)

(b) Precision grip (ape)

(c) Precision grip (human)

FIGURE 6.3 Grips and Opposable Thumbs Apes and humans have two kinds of grips: power and precision. (a) The power grip shown here, as a human holds a hammer, preceded the evolution of the precision grip. (b) The apes’ precision grip is not nearly as developed as humans’. (c) The finer precision grip of humans— in part due to the greater opposability of their thumbs— lets them finely manipulate objects.

opposable Refers to primates’ thumb, in that it can touch each of the four finger- tips, enabling a grasping ability.

power grip A fistlike grip in which the fin- gers and thumbs wrap around an object in opposite directions.

precision grip A precise grip in which the tips of the fingers and thumbs come together, enabling fine manipulation.

What Is a Primate? | 139

grip, the palm grips an object, such as a hammer’s handle, while the thumb and fingers wrap around it in opposite directions. In the precision grip, the thumb and one or more of the other fingers’ ends provide fine dexterity, as when holding a screwdriver, picking up a small object (such as a coin), or writing with a pen or pencil. The American paleoanthropologist Randall Susman has identified in early hominins the anatomy that would have supported a power grip and a precision grip (discussed further in chapter 9).

Many primates also have opposable big toes (the halluces). Humans are not among these primates, mainly because of changes in the foot that took place when our pre- human ancestors shifted from quadrupedal locomotion to bipedalism (Figure 6.4).

(b) (c)

Phalanges

Hallux

Metatarsals

Tarsals

Chimpanzee Human

Hallux

(a)

FIGURE 6.4 Opposable Big Toes Nonhuman primates’ opposable big toes, like their opposable thumbs, enable their feet to grasp things such as tree branches. Humans lack this feature due to their adaptation to life on the ground. (a) Its curved hallux and large gap between the hallux and second toe make (b) the chimpanzee foot look more like a human hand (not shown) than like (c) a human foot.

140 | CHAPTER 6 Biology in the Present: The Other Living Primates

(See also “What Makes Humans So Different from Other Animals?: The Six Steps to Humanness” in chapter  1.) To walk or run, humans need all five toes firmly planted on the ground. The mobility of recent humans’ toes has been even further reduced by the wearing of shoes.

The body trunk of primates is also distinctive. The backbone has five function- ally distinct types of vertebra— from top to bottom, the cervical, thoracic, lumbar, sacral (forming the sacrum of the pelvis), and coccyx vertebrae— which give it a greater range of movements than other animals have (Figure 6.5). The body trunk also tends to be vertically oriented, such as when the primate climbs, swings from tree limb to tree limb, or sits. The vertical tendency in a prehuman ancestor was an essential preadaptation to humans’ bipedality.

PRIMATES HAVE AN ENHANCED SENSE OF TOUCH The ends of the fingers and toes are highly sensitive in primates. This enhancement helps inform primates about texture and other physical properties of objects, such as potential food items. On the inside surfaces of the fingers and toes and on the palms and soles, respec- tively, of the hands and feet, the skin surface is covered with series of fine ridges called dermal ridges (fingerprints and toe prints). These ridges further enhance the tactile sense, and they increase the amount of friction, or resistance to slipping, when grasping an object, such as a tree branch. On the backs of the ends of the fingers and toes, most primates have nails instead of claws (Figure 6.6). Made of keratin, the strong protein also found in hair, these nails may protect the ends of the fingers and toes. They may aid in picking up small objects. Most importantly, however, they provide broad support to the ends of the fingers and toes by spread- ing out the forces generated in the digits by gripping.

preadaptation An organism’s use of an anatomical feature in a way unrelated to the feature’s original function.

Cervical

Thoracic

Lumbar

Sacrum

Coccyx Lemur spine

Human spine

FIGURE 6.5 Primate Vertebrae The five types of vertebrae in primates, including lemurs and humans, create a flexible column allowing a wide range of movement. The cervical, thoracic, and lumbar vertebrae are the true, or movable, vertebrae, responsible for bending, twisting, and stretching. The sacral vertebrae are much less movable because they form part of the pelvis. In most nonhuman primates, the vertebrae of the coccyx form the tail; in humans, these vertebrae are reduced to three to five very short, fused segments. Notice, too, the S- shaped spine in humans versus the C- shaped spine in other primates, such as the lemur.

FIGURE 6.6 Fingernails Finger pads with nail support help primates, such as this orangutan, securely hold tree branches that are smaller than their hands. By contrast, claws enable nonprimate mammals to dig into tree bark, an especially helpful ability when limbs or tree trunks are larger than the animals’ paws.

What Is a Primate? | 141

PRIMATES HAVE AN ENHANCED SENSE OF VISION Primates’ enhanced vision stems from two developments in the order’s evolutionary history. First, very early in primate evolution, the eyes rotated forward from the sides of the head to the front of the head (Figure 6.7). As a result, the two fields of vision overlap, pro- viding the primate with depth perception. (Along with the eyes’ convergence, fully enclosed or partially enclosed eye orbits evolved.) Second, color vision evolved. Crucial for spotting insects and other prey within the surrounding vegetation, color vision likely evolved as early primates shifted from a nocturnal adaptation to a diurnal adaptation.

PRIMATES HAVE A REDUCED RELIANCE ON SENSES OF SMELL AND HEARING For most primates, enhanced vision led to greatly reduced senses of smell and hearing. Most higher primates have lost the rhinarium (the external wet nose, which most mammals have) and the long snout. Some of the strepsirhines— the more primitive primates, such as lemurs and lorises— have retained the rhinar- ium, and they continue to rely on a well- developed sense of smell. The reduction in snout length resulted from a loss of internal surface area of the nasal passage, the location of the chemistry involved in smell. But some primates, such as baboons, later evolved a large and projecting snout to accommodate massive canine roots, especially in adult males.

(a)

(b)

Gibbon

Raccoon

Lemur

FIGURE 6.7 Primate Vision (a) Primates’ forward- facing eyes enable depth perception, a vital adaptation to life in the trees that has a selective advantage beyond arboreal life. Consider what would happen if a primate attempted to leap from one branch to another without being able to determine the distance between the two branches. Now imagine a human leaping over a (relatively) narrow chasm without knowing how far to leap. (b) In most primates, such as the gibbon, the eye orbit is fully enclosed. In animals such as the lemur, a postorbital bar lines the back of the eye orbit but does not fully enclose it. In other animals, such as the raccoon, the eye orbit is open, with no bone enclosing it at the rear.

nocturnal Refers to those organisms that are awake and active during the night.

diurnal Refers to those organisms that normally are awake and active during daylight hours.

rhinarium The naked surface around the nostrils, typically wet in mammals.

142 | CHAPTER 6 Biology in the Present: The Other Living Primates

DIETARY PLASTICITY— PRIMATES EAT A HIGHLY VARIED DIET, AND THEIR TEETH REFLECT THIS ADAPTIVE VERSATILITY PRIMATES HAVE RETAINED PRIMITIVE CHARACTERISTICS IN THEIR TEETH One fundamental anatomical feature in primates that reflects their high degree of dietary diversity is the retention of primitive dental characteristics, espe- cially of four functionally distinctive tooth types: incisors, canines, premolars, and molars (Figure 6.8). Primates’ mammalian ancestors had these same tooth types and so must have eaten a range of foods.

PRIMATES HAVE A REDUCED NUMBER OF TEETH Because the numbers of the different types of teeth are the same in the upper and lower jaws and the left and right sides of the jaws, anthropologists record each species’ dental formula with respect to one quadrant of the dentition. Primates’ early mammalian ances- tor, for example, had a dental formula of 3/1/4/3—three incisors, one canine, four premolars, and three molars— in one quadrant of its dentition. As indicated in Table 6.1, the Old World higher primates (anthropoids) have a dental formula of 2/1/2/3. Most New World primates have retained one more premolar and have a dental formula of 2/1/3/3. Some primates, such as tarsiers, have different numbers of teeth in the upper and lower jaws. Over the course of the order’s evolution, pri- mates’ teeth have tended to reduce in number, and the dental formula can be very useful in studies of ancestral primate species. For example, if fossilized remains of a primate ancestor have a dental formula of 2/1/3/3, the ancestor was likely related

What Makes Primates Good at Living in Trees?

Primates show a series of behavioral and anatomical tendencies that make them especially good at living in trees.

Characteristic Features

Versatile skeletal structure emphasizing mobility and flexibility

Separation of bones in articular joints associated with mobility: clavicle, radius and ulna, wrist, opposable thumb, opposable big toe in many primates

Five functionally distinct vertebral types: cervical, thoracic, lumbar, sacral, coccygeal

Enhanced sense of touch Dermal ridges at ends of fingers and toes, nails instead of claws

Enhanced sense of vision Convergence of eyes, color vision

C O N C E P T C H E C K !

dental formula The numerical description of a species’ teeth, listing the number, in one quadrant of the jaws, of incisors, canines, premolars, and molars.

FIGURE 6.8 Primate Dentitions These five sets of dentitions represent, from top to bottom, human, chimpanzee, gorilla, orangutan, and baboon. Notice that humans do not have the large projecting canines evident in the other four dentitions. In the side view, the large upper canines fit into a diastema, or space, between the lower canines and the third premolars. Each time the jaws are closed, the upper canines are sharpened against the lower third premolars.

What Is a Primate? | 143

to New World monkeys, strepsirhines (lemurs, lorises, galagos), or perhaps tarsiers since these primates have retained the extra premolar.

PRIMATES HAVE EVOLVED DIFFERENT DENTAL SPECIALIZATIONS AND FUNCTIONAL EMPHASES The premolars and molars of primates have under- gone little evolutionary change compared with those of other mammals. This evolutionary conservatism reflects the continued function of these teeth, espe- cially of the molars: grinding and crushing food. Specialized attributes of some primates’ teeth reflect particular food preferences. For example, some primates have high, pointed cusps on the occlusal, or chewing, surfaces of their molars, for puncturing and crushing insects. Others have crests on their molars, for shearing leaves. The many primates that eat fruit and seeds tend to have low, round cusps on their molars, for crushing and pulping.

TABLE 6.1 Primate Dental Formulae

T H E M A J O R P R I M AT E G R O U P S A R E D I S T I N G U I S H E D D E N TA L LY B Y T H E N U M B E R O F I N C I S O R S , C A N I N E S , P R E M O L A R S , A N D M O L A R S

Upper Lower

Tarsiers 2.1.3.3 1.1.3.3

Lemurs 2.1.3.3 2.1.3.3 (although there is much variation with lemurs)

Lorises 2.1.3.3 2.1.3.3

New World Monkeys 2.1.3.2 or 2.1.3.3 2.1.3.2 or 2.1.3.3

Old World Monkeys 2.1.2.3 2.1.2.3

Apes and Humans 2.1.2.3 2.1.2.3

What Gives Primates Their Dietary Flexibility?

Primates display a broad range of dietary adaptations. Although strepsirhines’ and haplorhines’ teeth have evolved specializations, such as the tooth comb in lemurs, the overall retention of a nonspecialized, primitive dentition reflects the order’s diverse diet.

Characteristic Features

Multiple tooth types Incisors, canines, premolars, molars

Reduced number of teeth Fewer incisors, premolars, and molars

C O N C E P T C H E C K !

144 | CHAPTER 6 Biology in the Present: The Other Living Primates

Tooth comb

Tooth comb

(a)

(b)

FIGURE 6.10 Tooth Comb Lemurs and lorises possess this unique morphology of lower incisors and canines— here seen from (a) below and (b) the side— useful for scraping and for grooming fur.

(a) (b) (c) (d)

Bilophodont

Y-5

FIGURE 6.9 Primate Molars The morphology of lower molars in primates has two main variants: Old World monkeys’ bilophodont pattern, such as in (a) the colobus monkey, and apes’ Y- 5 pattern, such as in (b) the gibbon, (c) the chimpanzee, and (d) the orangutan. Like the dental formula, molar morphology can be used to determine whether fossilized remains of a primate represent an ancestor of Old World monkeys or of apes and humans.

tooth comb Anterior teeth (incisors and canines) that have been tilted forward, creating a scraper.

What Is a Primate? | 145

The molars of monkeys, apes, and humans have distinctive occlusal surfaces (Figure 6.9). Old World monkeys have four cusps on upper and lower molars, with two of the cusps on the front and two of the cusps on the back of the tooth’s occlu- sal surface. Each pair of cusps, front and back, is connected by an enamel ridge, or loph. This is called a bilophodont (meaning “ two- ridge tooth”) molar. Apes and humans have a lower molar with five separate cusps that are separated by grooves. A Y- shaped groove is dominant, with the fork of the Y directed toward the outside of the tooth. This is called a Y- 5 molar. Apes’ and humans’ upper molars generally have four cusps, separated by grooves.

While most primates’ incisors are flat, vertically oriented, and used to prepare food before it is chewed by the premolars and molars, strepsirhines’ lower inci- sors and canines are elongated, crowded together, and projecting forward. This specialized feature, a tooth comb, is especially useful for grooming (Figure 6.10).

The horizontally oriented canine is one of three different kinds of canines in primates. The small, vertical, incisor- shaped canine appears only in humans. Only in humans (and all their hominin ancestors) does the canine wear on its tip. The projecting, pointed canine is present in all monkeys and all apes. In Old World monkeys and apes, the canines are part of a canine– premolar honing complex, in which the upper canine fits in a space, or diastema, between the lower canine and lower third premolar. This configuration slices food, especially leaves and other plants. When the primate chews, the movement of the back of the upper canine against the front of the lower first premolar creates a continuously sharp- ened edge on each of the two teeth (Figure 6.11).

The lower third premolar is sectorial, meaning that it has a single dominant cusp and a sharp cutting edge. The upper canine tends to be large, especially in males. In addition to its masticatory function, the large upper canine provides a strong social signal for establishing and maintaining dominance among male members of the primate society, such as in baboons, and as a warning signal to potential predators (Figure 6.12).

loph An enamel ridge connecting cusps on a tooth’s surface.

bilophodont Refers to lower molars, in Old World monkeys, that have two ridges.

Y- 5 Hominoids’ pattern of lower molar cusps.

canine– premolar honing complex The dental form in which the upper canines are sharp- ened against the lower third premolars when the jaws are opened and closed.

diastema A space between two teeth.

sectorial (premolar) Refers to a premolar adapted for cutting.

FIGURE 6.12 Canine Size In some primate species, such as baboons, the canines differ in size between males and females. Because the canines can be used as weapons, the fierce appearance of these large teeth serves to warn competitors and predators.

(a) (b)

No diastemaDiastema

FIGURE 6.11 Honing Complex (a) In Old World monkeys and apes, the lower jaw has a diastema to accommodate the very large upper canines. (b) Humans lack such a space because they do not have large, projecting upper canines. Notice the different size and orientation of the canines in (a) and (b) and in Figure 6.10.

146 | CHAPTER 6 Biology in the Present: The Other Living Primates

Thickness of tooth enamel varies across primate species. Orangutans and humans have thick enamel, whereas chim- panzees and gorillas have thin enamel. Thick enamel reflects an adaptation to eating tough, hard foods. Although humans today rarely eat hard foods, they have retained this primitive characteristic.

PARENTAL INVESTMENT— PRIMATE PARENTS PROVIDE PROLONGED CARE FOR FEWER BUT SMARTER, MORE SOCIALLY COMPLEX, AND LONGER- LIVED OFFSPRING Female primates give birth to fewer offspring than do other female mammals. A single female primate’s births are spaced out over time— sometimes by several years, in the cases of some apes. Primate mothers invest a lot of time and energy in caring for each of their offspring (Figure 6.13). By caring for their offspring,

providing them with food, and teaching them about social roles and social behavior generally, primates increase the chances of their species’ survival.

Lemur Macaque Gibbon Orangutan Chimpanzee Human

Adult

Infancy Prenatal

Juvenile through adolescence

128 days 167 days 210 days 260 days 228 days 267 days

2 years 6 years 6.5 years

7 years 7 years

14–19 years

1.5 years 2 years 3.5 years 3.5 years 3 years

11 years

20 years 20 years

20 years

30 years

55 years

.5 year

FIGURE 6.14 Growth Stages of Five Primates Lemurs and macaques have the shortest growth period; apes and humans, the longest. The longer growth reflects the greater behavioral complexity in apes and humans than in lemurs and macaques.

FIGURE 6.13 Parental Investment Because a female primate generally expends so much energy in rearing each of her offspring, she generally will have few offspring. Here, a chimpanzee mother holds her baby.

What Is a Primate? | 147

Primates have long growth and development periods, in part because of their high level of intelligence relative to other animals (Figure  6.14). That primates’ brains are so large and complex reflects the crucial importance of intelligence— brainpower— in primate evolution (Figure  6.15). The back portion of the brain where visual signals are processed is expanded in primates, whereas the areas of the brain associated with smell (olfactory bulb) and hearing are considerably smaller than in other mammals. Among all primates, humans have the largest brain relative to body size and the most elaborate neural connections between different regions of the brain. This combination of greater mass and complexity provides humans with greater intelligence compared with other primates and has led humans to develop language and advanced culture.

olfactory bulb The portion of the anterior brain that detects odors.

B ra

in m

as s

(g )

Body mass (kg)

10,000

100

1

1,000

10

0.10.01 1 10 100 1000 0.1

Average mammal Prosimian Cebid Cercopithecoid Hominoid Homo sapiens

Parietal lobe

Frontal lobe

Olfactory bulb

Cerebellum

Prosimian

Frontal Occipital lobe

Cerebellum

Parietal lobe

Parietal lobe

Monkey

Chimpanzee

Occipital lobe

Cerebellum

Brain- stem

Brain- stem

Occipital lobe

Brain- stem

Temporal lobe

Olfactory bulb

Temporal lobe

Temporal lobe

Olfactory bulb

Frontal lobe

FIGURE 6.15 Primate Brain Morphology (a) The main regions of the brain are delineated in these drawings of primates’ brains. The drawings are out of scale to show differences in anatomy. (b) As this graph shows, primates with the greatest body mass also have the greatest brain mass and thus the greatest intelligence. Most primates also have a larger brain relative to body size than the average mammal, a reflection of primates’ higher intelligence. The Homo sapiens dot is way off the line because humans have a much bigger brain relative to body mass. The human brain is not just a large version of an ape’s, monkey’s, or prosimian’s brain. Rather, during evolution, in addition to a size increase the human brain has undergone important qualitative and quantitative changes in some key regions. What are these changes, and how are they associated with behavior?

(a)

(b)

148 | CHAPTER 6 Biology in the Present: The Other Living Primates

Primate Parenting

Compared with other mammals, primates display unique parenting characteristics. These relate to the fact that primate offspring are more intelligent and behaviorally complex than are other mammals’ offspring.

Characteristic Features

Fertility Birth to relatively few offspring at a time, commonly just one

Birth interval Relatively long period between births

Preadult care Elongated and intensive

C O N C E P T C H E C K !

What Are the Kinds of Primates? Today, more than 200 taxa— number of species— of primates live in various parts of the world. If we count subspecies, there are more than 600 kinds of primates, from the mouse lemur, which weighs less than .5 kg (1 lb), to the gorilla, which weighs several hundred pounds. Primate biological diversity is reflected in two different classification systems. The long- standing approach, called traditional or gradistic, separates the order Primates into two suborders, the Prosimii (prosim- ians, or lower primates) and the Anthropoidea (anthropoids, or higher primates; Figure 6.16, pp. 150– 51). This approach is based on grades, or levels of anatomical complexity, without consideration of identifying ancestral– descendant relation- ships. Physical anthropologists are increasingly using an alternative form of clas- sification, which groups primates on the basis of lines of descent and identification of shared common ancestry (Figure 6.17). This cladistic, or evolutionary (sometimes called phylogenetic), approach uses anatomical and genetic evidence to establish the ancestral– descendant lines that link clades. This approach divides the order Primates into two clades, the Strepsirhini (or strepsirhines) and the Haplorhini (or haplorhines). The strepsirhines have retained primitive characteristics, such as the rhinarium and heightened sense of smell; and they tend to have relatively specialized diets and behaviors. The haplorhines have the range of features that define primates as described above, but they have also lost a number of primitive primate characteristics that strepsirhines have retained, such as the rhinarium.

The classification approaches— traditional/gradistic and evolutionary / cladistic— result in similar outcomes in the way primates are categorized (see Figure  6.17). The major difference is that the traditional approach groups tarsiers, a relatively specialized primate, with the prosimians. However, tarsiers share a number of derived characteristics with anthropoids, such as both lacking a rhinarium.

grade Group of organisms sharing the same complexity and level of evolution.

clade Group of organisms that evolved from a common ancestor.

primitive characteristics Characteristics present in multiple species of a group.

derived characteristics Characteristics present in only one or a few species of a group.

What Are the Kinds of Primates? | 149

Tarsiers’ teeth are like higher primates’—their canines are large and projecting, the lower incisors are relatively small, and the upper central incisors are large. Many authorities argue that tarsiers share a common ancestor with anthropoids and not with the other prosimians (lorises, galagos, and lemurs) and should be considered part of a single (haplorhine) clade. Given the priority of and focus on evolution and not description in this book, I use the cladistic approach, placing the tarsiers with the anthropoids (monkeys, apes, and humans) in a haplorhine clade and the lorises, galagos, and lemurs in the strepsirhine clade.

There are two clades of haplorhines, the anthropoids and tarsiers. Anthropoids include catarrhines (Old World higher primates) and platyrrhines (New World higher primates): monkeys (cercopithecoids, or Old World monkeys, and ceboids, or New World monkeys), apes (hylobatids, or lesser apes, and nonhuman homi- nids, or great apes), and humans (hominins). Tarsiers have a number of primitive features, and they are highly specialized, especially with respect to having large, bulbous eyes for nocturnal vision. Rather than having four lower incisors, two on  the left and two on the right, tarsiers have only two. Like some of the strep- sirhines, they have retained three premolars on each side of the upper and lower jaws, giving them 34 teeth. Their name refers to the presence of two highly elon- gated tarsal bones in their feet. These long bones give extra leverage for leaping in search of prey, such as small birds. Tarsiers’ eyes and eye sockets are enormous, reflecting their nocturnal adaptation (Figure  6.18). Their brain’s smallness and relatively simple structure make it more similar to lemurs’ and lorises’ brains than to the higher primates’.

Anthropoids are found in many places around the world, whereas tarsiers are restricted to a series of islands, especially Sulawesi, Borneo, and the Philippines. Both major clades of primates— strepsirhines and haplorhines— are hierarchically arranged, culminating at the bottom with genus and species (see Figure 6.16). Some genera are very diverse and are represented by multiple species, whereas others are not as diverse and have today just one species (e.g., living humans). Among the hominoids, humans and African great apes (gorillas, chimpanzees, and bono- bos) are more closely related to each other than they are to the Asian great apes

Strepsirhines Haplorhines

Anthropoids

Prosimians

lemurs lorises

tarsiers FIGURE 6.17 Cladistic (Evolutionary or Phylogenetic) versus Gradistic (Traditional) Classification According to the cladistic categorization (upper left), lorises and lemurs belong to the category strepsirhines and anthropoids and tarsiers belong to the category haplorhines. By contrast, according to the gradistic categorization (right), lorises, lemurs, and tarsiers belong to the category prosimians, which is distinct from anthropoids.

hominin Humans and humanlike ancestors.

150 | CHAPTER 6 Biology in the Present: The Other Living Primates

Primates (living)

Strepsirhini Haplorhini

Anthropoidea (monkeys, apes, and humans)

Catarrhini (Old World monkeys, apes, and humans)

Lorisoidea (lorises and galagos)

Tarsiiformes (tarsiers)

Lemuroidea (lemurs)

Lemuriformes (lemurs, lorises, and galagos)

Platyrrhini (New World monkeys)

Cercopithecoidea (Old World monkeys)

Hominoidea (apes and humans)

Ceboidea (New World monkeys)

Cebidae

Callimico (Goeldi’s monkeys)

Callithrix (marmosets)

Cebuella (pygmy marmosets)

Cebus (capuchin monkeys)

Leontopithecus (lion tamarins)

Sanguinus (tamarins)

Saimiri (squirrel monkeys)

Atelidae

Alouatta (howler monkeys)

Aotus (owl monkeys)

Ateles (spider monkeys)

Brachyteles (muriquis) Cacajao (uakaris)

Callicebus (titi monkeys) Chiropotes

(bearded sakis) Lagothrix

(woolly monkeys) Pithecia (sakis)

Hylobatidae (lesser apes)

Hylobates (gibbons and

siamangs)

Ponginae (orangutans)

Gorillinae (gorillas)

Homininae (chimpanzees, bonobos,

and humans)

Panini Hominini

Gorilla (gorillas)

Pan (chimpanzees,

including bonobos)

Pongo (orangutans)

Hominidae (great apes and humans)

Homo (humans)

Colobinae

Colobus (black-and-white

colobus monkeys) Nasalis

(proboscis monkeys) Presbytis

(leaf monkeys) Procolobus

(red and olive colobus monkeys)

Pygathrix (snub-nosed monkeys)

Semnopithecus (Hanuman langurs)

Simias (pig-tailed monkeys)

Trachypithecus (langurs)

Order

Suborder

Infraorder

Parvorder

Superfamily

Family

Subfamily

Tribe

Genus

Cercopithecinae

Allenopithecus (swamp monkeys)

Cercocebus (mangabeys)

Cercopithecus (guenons)

Erythrocebus (patas monkeys)

Macaca (macaques) Mandrillus

(drills, mandrills) Miopithecus

(talapoin monkeys) Papio

(baboons) Theropithecus

(geladas)

Euoticus (needle-clawed bushbabies)

Galago (bushbabies) Galagoides

(Demidoff’s, Thomas’s, and Zanzibar bushbabies)

Otolemur (greater bushbabies)

Arctocebus (angwantibos, golden pottos)

Loris (slender lorises)

Nycticebus (slow lorises) Perodicticus

(pottos) Pseudopotto

(pseudo pottos)

Tarsius (tarsiers)

Eulemur (true lemurs) Hapalemur (bamboo or

gentle lemurs) Lemur

(ring-tailed lemurs) Varecia

(ruffed lemurs) Lepilemur

(sportive lemurs) Allocebus

(hairy-eared dwarf lemurs) Cheirogaleus (dwarf lemurs) Microcebus

(mouse lemurs) Mirza

(Coquerel’s dwarf lemur)

Phaner (fork-marked lemurs)

Avahi (woolly lemurs)

Indri (indris)

Propithecus (sifakas)

Daubentonia (aye-ayes)

What Are the Kinds of Primates? | 151

Primates (living)

Strepsirhini Haplorhini

Anthropoidea (monkeys, apes, and humans)

Catarrhini (Old World monkeys, apes, and humans)

Lorisoidea (lorises and galagos)

Tarsiiformes (tarsiers)

Lemuroidea (lemurs)

Lemuriformes (lemurs, lorises, and galagos)

Platyrrhini (New World monkeys)

Cercopithecoidea (Old World monkeys)

Hominoidea (apes and humans)

Ceboidea (New World monkeys)

Cebidae

Callimico (Goeldi’s monkeys)

Callithrix (marmosets)

Cebuella (pygmy marmosets)

Cebus (capuchin monkeys)

Leontopithecus (lion tamarins)

Sanguinus (tamarins)

Saimiri (squirrel monkeys)

Atelidae

Alouatta (howler monkeys)

Aotus (owl monkeys)

Ateles (spider monkeys)

Brachyteles (muriquis) Cacajao (uakaris)

Callicebus (titi monkeys) Chiropotes

(bearded sakis) Lagothrix

(woolly monkeys) Pithecia (sakis)

Hylobatidae (lesser apes)

Hylobates (gibbons and

siamangs)

Ponginae (orangutans)

Gorillinae (gorillas)

Homininae (chimpanzees, bonobos,

and humans)

Panini Hominini

Gorilla (gorillas)

Pan (chimpanzees,

including bonobos)

Pongo (orangutans)

Hominidae (great apes and humans)

Homo (humans)

Colobinae

Colobus (black-and-white

colobus monkeys) Nasalis

(proboscis monkeys) Presbytis

(leaf monkeys) Procolobus

(red and olive colobus monkeys)

Pygathrix (snub-nosed monkeys)

Semnopithecus (Hanuman langurs)

Simias (pig-tailed monkeys)

Trachypithecus (langurs)

Order

Suborder

Infraorder

Parvorder

Superfamily

Family

Subfamily

Tribe

Genus

Cercopithecinae

Allenopithecus (swamp monkeys)

Cercocebus (mangabeys)

Cercopithecus (guenons)

Erythrocebus (patas monkeys)

Macaca (macaques) Mandrillus

(drills, mandrills) Miopithecus

(talapoin monkeys) Papio

(baboons) Theropithecus

(geladas)

Euoticus (needle-clawed bushbabies)

Galago (bushbabies) Galagoides

(Demidoff’s, Thomas’s, and Zanzibar bushbabies)

Otolemur (greater bushbabies)

Arctocebus (angwantibos, golden pottos)

Loris (slender lorises)

Nycticebus (slow lorises) Perodicticus

(pottos) Pseudopotto

(pseudo pottos)

Tarsius (tarsiers)

Eulemur (true lemurs) Hapalemur (bamboo or

gentle lemurs) Lemur

(ring-tailed lemurs) Varecia

(ruffed lemurs) Lepilemur

(sportive lemurs) Allocebus

(hairy-eared dwarf lemurs) Cheirogaleus (dwarf lemurs) Microcebus

(mouse lemurs) Mirza

(Coquerel’s dwarf lemur)

Phaner (fork-marked lemurs)

Avahi (woolly lemurs)

Indri (indris)

Propithecus (sifakas)

Daubentonia (aye-ayes)

FIGURE 6.16 Order Primates This classification of primate species uses the Linnaean taxonomy and places primates into two major groups— strepsirhines and haplorhines. Shared adaptive physical features help determine the degree of relatedness among primate species. (Not all species of primates are listed.)

152 | CHAPTER 6 Biology in the Present: The Other Living Primates

(orangutans). In addition, DNA comparisons reveal that chimpanzees and humans are more closely related than either is to gorillas. Therefore, traditional and cladis- tic taxonomies produce somewhat different results for these primates (Table 6.2). The traditional classification includes three families: hylobatids (gibbons), pon- gids (great apes), and hominids (humans). By contrast, the cladistic classification includes two families, hylobatids (gibbons) and hominids (great apes, including humans), and three subfamilies, pongines (orangutans), gorillines (gorillas), and hominines (chimpanzees, bonobos, and humans). The hominines are further sub- divided into two tribes: panins (chimpanzees, bonobos) and hominins (humans).

The differences between the major primate groups— for example, the differ- ences between an ape and a monkey— matter, first, because they are a means of understanding the variation among primates. Second, the key characteristics of the different primate taxa appear at specific points in the evolutionary record. Paleon- tologists look for these characteristics in their study of the origins and evolution of the different primate groups. For example, when did the Y- 5 molar, a defining characteristic of apes, first appear? When did bipedalism first occur? When did monkeys living in the New World first differ noticeably from those living in the Old World? Such questions are central to the study of primates and of their evolu- tion. They can be answered only by knowing the characteristics unique to different primate taxa. These characteristics, then, help paleontologists and anthropologists reconstruct the evolutionary relationships and history of living species and their fossil ancestors. These evolutionary relationships, or phylogeny, are based on shared characteristics, including physical traits, genetics, and behavior. Organisms that share characteristics are more closely related than are organisms that do not

Tarsier foot

Human foot

Calcaneus

Talus

Talus

Calcaneus

FIGURE 6.18 Tarsier’s Eyes and Feet (a) Tarsiers are unique among prosimians in that their eyes have a fovea, a region of the retina that enables the sharp central vision needed for seeing details. This trait is unusual in nocturnal animals because dim light typically prevents them from seeing things that clearly. (b) Thanks to their elongated tarsals (shown in color), especially the talus and calcaneus bones, tarsiers are superb leapers.

(a)

(b)

phylogeny The evolutionary relationships of a group of organisms.

What Are the Kinds of Primates? | 153

TABLE 6.2 Hominoid Classifications

Gradist ic ( Tradit ional) Classif icat ion Cladist ic (Phylogenet ic) Classif icat ion

Superfamily Hominoid Hominoid

Family

Subfamily

Tribe

Genus

Common Name

Hylobatid Pongid Hominid

Hylobates Pongo Pan Gorilla Homo

Gibbon Orangutan Chimpanzee Gorilla Human Bonobo

Hylobatid Hominid

Pongine Gorilline Hominine

Panin Hominin

Hylobates Pongo Gorilla Pan Homo

Gibbon Orangutan Gorilla Chimpanzee Human Bonobo

share characteristics. For example, all mammals are homeothermic— all mammal species share this primitive trait. All apes have a sectorial complex— but humans lack this derived trait.

In addition, it is important to know about the physical differences between pri- mate taxa because the variation in the living primates provides models for under- standing the morphology, the behavior, and the adaptation in the evolutionary past. For example, the Y- 5 lower molar pattern seen today in apes and humans first appeared in anthropoids 20–30 mya. This morphology indicates that apes origi- nated at that time. (Humans have the pattern but evolved after apes.) Similarly, characteristics that define bipedality in humans— long lower limbs and short upper limbs— first appeared 5 mya or so. When they find these anatomical characteristics in fossilized remains (fossils are the subject of chapter 8), anthropologists are able to identify the origins of humanlike ancestors. And knowing how those ancestors walked helps complete a timeline of adaptation.

THE STREPSIRHINES In acquiring food, strepsirhines rely heavily on their highly developed sense of smell. As a result, they have enlarged nasal passages, a rhinarium, scent glands, and a large and distinctive olfactory bulb in the front of the brain. At the ends of their fingers and toes, most strepsirhines have some combination of nails and claws. On the second digit of strepsirhine feet, there is a grooming or toilet claw. They also have the aforementioned tooth comb. Ring- tailed lemurs, among the most fascinating and adaptable strepsirhines, spend considerable time on the ground.

In evolutionary terms, lemurs, lorises, and galagos are among the most primitive primates (primate evolution is the subject of chapter  9). Many of the primitive characteristics they retain have been around for many millions of years. Although lemurs are found only on the island of Madagascar, they represent some 21% of pri- mate genera worldwide. Until humans first occupied the island, about 1,000 years

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ago, very large species of lemurs lived on Madagascar, including some that were the size of a cow (Figure 6.19). Lorises live in Africa and Southeast Asia, and galagos live in Africa. Many of these animals feed and breed at night. Their most distinc- tive physical characteristics, very large eyes and very large eye orbits, reflect their strongly nocturnal adaptation. Lemurs and lorises have primitive dentitions— some have 36 teeth, having retained three premolars in their dental formula. They also have the specialized tooth comb (see Figure 6.10).

Monkey or Ape? Differences Matter

Differences between monkeys and apes track different evolutionary histories.

Characteristic Monkeys Apes

Body size Generally smaller Generally larger

Posture/locomotion Generally horizontal body trunk

Relatively vertical body trunk

Body trunk Narrow Broad

Tail Have a tail Lack a tail

Lower molars Bilophodont lower molar (cercopithecoids only)

Y- 5 molar pattern

Brain Relatively small Relatively large

Growth Relatively fast Relatively slow

Interspecies variability High Low

C O N C E P T C H E C K !

Indri

Gorilla

Magaladaptis Mouse lemur

(a) (b)

FIGURE 6.19 Megaladapis (a) These skulls belonged to a species of very large lemurs, the now extinct Megaladapis, on Madagascar. Skulls of Megaladapis were larger than a modern gorilla’s, though Megaladapis’s body was smaller than a gorilla’s. (b) In the right foreground, the skulls of a modern mouse lemur (middle) and an indri (right) represent the range of sizes in living lemurs. The crania in the back row and the skull to the left of the mouse lemur’s show the range of sizes in extinct lemurs. The sizes of living and extinct lemurs overlap somewhat, but Megaladapis, the largest extinct lemur, was substantially larger than any living lemur.

What Are the Kinds of Primates? | 155

THE HAPLORHINES Haplorhines differ from strepsirhines in a number of ways. In general, haplorhines have larger brains, they are more dimorphic sexually in body size and other ana- tomical characteristics, they have fewer teeth (premolars, in particular), their eyes are convergent and enclosed by a continuous ring of bone, and they see in color.

The two parvorders of anthropoids— platyrrhines, or New World monkeys, and catarrhines— are named for the morphologies of their noses (Figure 6.20). Platyr- rhine (from the Greek, meaning “ broad- nosed”) nostrils are round and separated by a wide nasal septum, the area of soft tissue that separates the nostrils. Catarrhine (“ hook- nosed”) nostrils are close together and point downward. (To understand nostril orientation, look at your own nostrils in a mirror. They should be directed downward since you are a catarrhine.)

The one superfamily of platyrrhines is the ceboids. The two ceboid families, cebids and atelids, are widespread in Latin America, from southern Argentina to Mexico. Ceboids are arboreal, spending nearly all their time in trees. They use suspensory locomotion, in which all four limbs grasp on to branches and help move the body from one tree or branch to another. Within the atelids are two subfami- lies, one of which, the atelines, is distinctive in that each of its four types (howler monkeys, spider monkeys, woolly monkeys, and woolly spider monkeys) has a prehensile tail (Figure 6.21). In addition to locomotion functions in the trees, the prehensile tail can be used to suspend the body from a branch so that the hands and feet can be used to feed. Ceboids have a diverse diet, ranging from insects (i.e., they practice insectivory) to fruits (frugivory) and leaves (folivory). Smaller ceboids obtain protein from insects, whereas larger ones obtain it from leaves.

The Old World monkeys, cercopithecoids, are the most diverse and most successful nonhuman primates. They inhabit a wide range of habitats throughout Africa and Asia but mostly live in the tropics or subtropics. Some are arboreal and

Platyrrhines New World

FIGURE 6.20 Platyrrhines versus Catarrhines In addition to their differently shaped noses, these two groups differ in their numbers of premolars; platyrrhines have six upper and six lower premolars, while catarrhines have four upper and four lower premolars.

Catarrhines Old World

prehensile tail A tail that acts as a kind of a hand for support in trees, common in New World monkeys.

FIGURE 6.21 Prehensile Tails Atelines, such as muriquis or woolly spider monkeys (shown here), are the only primates with a fully prehensile tail. (Opossums and kinkajous are among the other mammals with a fully prehensile tail.) The prehensile tail is very muscular, and its undersurface has dermal ridges, like fingerprints and toe prints, that improve the tail’s grip.

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some are terrestrial. Cercopithecoids have bilophodont upper and lower molars, a narrow face, a sitting pad on the rear, and a long body trunk that terminates with a nonprehensile tail. Their canines are highly dimorphic sexually— males’ canines are larger than females’ canines, sometimes considerably so.

Cercopithecoids are divided into two subfamilies, colobines and cercopithe- cines  (Figure  6.22). Colobines are closely related, medium- sized primates with

(a) (b) (c) (d)

(e) (f) (g)

(h)

FIGURE 6.22 Old World Monkeys Colobines include (a) black- and- white colobus monkeys, (b) gray langurs, (c) proboscis monkeys, and (d) douc langurs. Cercopithecines include (e) mandrills, (f) De Brazza’s monkeys, (g) olive baboons, and (h) vervet monkeys.

What Are the Kinds of Primates? | 157

a long tail and a wide array of coloration. They are mostly arboreal and live in a variety of climates, though not in dry areas. Colobines are folivores, and their anatomical features have adapted to accommodate a diet rich in leaves. The high, pointed cusps of their molars shear leaves and thus maximize the amount of nutrition obtained from them. Conversely, cercopithecines have rounded, lower

(a) (b) (c)

(d) (e)

FIGURE 6.23 Great Apes and Lesser Apes The great apes—(a) chimpanzees, (b) bonobos, (c) orangutans, and (d) gorillas— tend to be larger than other primates. All but gorillas are smaller than humans, with whom they are highly similar genetically. While great apes have a variety of social groupings (discussed below), lesser apes—(e) gibbons and (not pictured) siamangs— are unique in that they form pair bonds, in which one male, one female, and their offspring are the basic social unit.

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cusps on their molars as their diet is rich in fruit, which does not need as much processing to extract its nutrients. Colobines’ large, three- or four- chambered stomach, resembling a cow’s stomach, contains microorganisms that break down cellulose, again to maximize the amount of nutrition extracted from the leaves. By contrast, cercopithecines are often called “ cheek- pouch monkeys” because inside each cheek they have a pouch that extends into the neck and serves as a kind of stomach. While foraging, they store food in their cheek pouches, which are especially useful when they need to gather food quickly in a dangerous area. Arboreal cercopithecines tend to have a longer tail, while terrestrial species have a short or no tail.

Colobines are receiving a lot of attention because some taxa are highly threat- ened. One colobine species, Miss Waldron’s red colobus monkey, is the first pri- mate to have gone extinct in the last five centuries.

The most studied cercopithecoids are the cercopithecines, which include baboons and baboonlike monkeys (geladas, mandrills, macaques). Many cercopith- ecines live in the savannas of East Africa. Some of them have highly dexterous fin- gers, adapted for picking up small seeds from the ground. Because these primates live in habitats similar to those of early hominins (see chapter  10), they provide anthropologists with the means of understanding both the origins and evolution of early human social behavior and some physical attributes characteristic of pri- mates living in open grasslands.

The hominoids are, in addition to humans, great apes and lesser apes (Figure 6.23). Humans live on every continent. Today, the only great ape that lives in Asia is the orangutan. The lesser apes live in Southeast Asia. The great apes of Africa— the chimpanzee, the closely related bonobo (or pygmy chimpanzee), and the gorilla— are restricted to small equatorial areas. All of these hominoids have large brains, broad faces, and premolars and molars with little occlusal surface relief. They all have a Y- 5 lower molar pattern. All apes have the canine– premolar honing complex. None of the hominoids have an external tail.

All hominoids except humans— gibbons, siamangs, gorillas, chimpanzees, bonobos, and orangutans— have very long forelimbs (arms) compared with the hind limbs. The fingers and toes are also quite long, for grasping trees and branches of various shapes and sizes. These characteristics are important adaptations used in the forest in a range of suspensory postures and movements (Figure  6.24). Gib- bons and siamangs are skilled brachiators, using their upper limbs to move from tree limb to tree limb. Chimpanzees, bonobos, and gorillas are efficient at various suspensory postures; but their large sizes— especially in adult males— lead them to spend significant amounts of time on the ground in feeding and in locomotion. They employ a specialized form of quadrupedalism called knuckle- walking, in which the very strong arms are used to support the upper body weight while posi- tioned on the backs of the fingers’ middle phalanges. The knuckles bear the weight, while the fingers are flexed toward the palms (Figure 6.25).

In orangutans and gorillas, males have enormous masticatory muscles, which are accommodated by a large, well- developed sagittal crest, the ridge of bone running along the midline ( mid- sagittal) plane of the skull. The sagittal crest is the  terminal attachment site for the temporalis muscle (Figure  6.26). Gorillas devote considerable time to eating leaves and plant stems. In contrast, chimpan- zees are omnivorous— they eat fruit, leaves, bark, insects, and meat, depending on the season, their habitat (ranging from dense rainforests to savanna- woodlands), and local tradition. When meat is not available, chimpanzees’ body weight goes down, suggesting that they rely on animal sources for protein.

Long arms

Long, curved fingers

FIGURE 6.24 Suspensory Apes That the great apes and lesser apes regularly use suspensory locomotion can be seen in various features of their skeletal anatomy. For example, this gibbon’s arms are long compared with its legs, its fingers and toes are long, and its fingers are curved and thus have enhanced grasping ability. If an ancestral primate’s forelimbs were considerably longer than its hind limbs, the animal was likely suspensory.

brachiators Organisms that move by bra- chiation, or arm- swinging.

What Are the Kinds of Primates? | 159

Humans’ general body plan resembles that of the large- bodied apes of Africa, a fact that has been recognized since at least the middle of the nineteenth cen- tury, when Thomas Huxley wrote his famous treatise on primate anatomy and human evolution, Man’s Place in Nature (Huxley’s research is discussed further in chapter  10). Humans have several unique anatomical attributes, however, many of which are related to the fact that humans are the only obligate, or restrictedly, bipedal primate (see “What Makes Humans So Different from Other Animals?: The Six Steps to Humanness” in chapter 1).

The skeletal indicators of bipedalism are found in the skull and the postcranial skeleton. In bipeds, the foramen magnum— the large opening for the passage of the spinal cord to the brain— is located at the bottom of the skull. The skull sits atop the body, whereas in quadrupeds the foramen magnum is located on the back of the skull and the skull is positioned on the front of the body. Many of the postcranial  characteristics associated with bipedality are in the pelvis. The pelvis of the human (the biped) is short and directed to the side of the body, whereas the pelvis of the ape (the quadruped) is long and directed to the back of the body. These differently shaped pelvises reflect the different positions and functions of two gluteal muscles— gluteus medius and gluteus minimus— which attach across the hip joints of both human and ape. In apes, these two muscles act as thigh straighteners, or extensors; but in humans, they abduct the thigh on the side of the hip that supports the body weight when a person walks. The muscles’ contraction on the abducted side keeps the hip stable while the other leg swings forward (Figure  6.27). (Next time you walk, notice how only one foot is on the ground at any one time, and feel how on that side of your hip the gluteal muscles have contracted.)

FIGURE 6.25 Knuckle- Walking This unique type of quadrupedalism enables chimpanzees and gorillas, like the gorilla pictured here, to move very quickly. In contrast, orangutans typically use fist- walking, supporting their upper body weight on the palms, which are closed in fists.

Sagittal crest Temporalis muscle

Masseter muscle

Nuchal crest

(a)

(b) FIGURE 6.26 Sagittal Crest (a) This ridge of bone is located at the sagittal suture along the midline of the cranium. (b) The more highly developed the sagittal crest is, the more highly developed the masticatory muscles are. This feature appears in gorillas and orangutans, as well as a variety of other animals, especially carnivores. It has been found in some human and primate ancestors.

(a)

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Among the other anatomical differences between humans and apes are the relative lengths of the limbs, the curvature of the spine, and the angle of the femur in standing, walking, and running bipeds (Figure 6.28). In addition, unlike apes and monkeys, humans do not hone their canines and premolars. These differences are discussed more fully in chapter 10.

The position of the foramen magnum in apes, monkeys, and other quadrupedal animals is toward the back of the skull.

In humans, the foramen magnum is on the bottom of the skull.

In humans, the medius and minimus gluteal muscles abduct the leg; that is, they pull the thigh away from the midline of the body when the leg is extended. As the thigh is abducted, it is also rotated inward, providing a more stable support for the hip during walking.

In apes, the medius and minimus gluteal muscles pull the leg backward, extending the leg at the hip.

FIGURE 6.27 Quadrupedalism versus Bipedalism Various morphological features indicate these two forms of locomotion.

What Are the Kinds of Primates? | 161

FIGURE 6.28 Limb Proportions In suspensory apes (left), the arms are long compared with the legs. In humans (right), the arms are relatively short because they are no longer used in locomotion. In addition, humans’ fingers and toes are relatively shorter and straighter than apes’, again as a result of bipedalism.

Strepsirhines and Haplorhines Differ in Their Anatomy and Senses

Strepsirhines tend to be more primitive than haplorhines.

Characteristic/ Adaptation

Strepsirhine Tendencies

Haplorhine Tendencies

Smell More developed Less developed

Vision Nocturnal for many Diurnal

Touch Claws in some Nails

Less developed More developed

Diet More specialized More generalized

More teeth in some Reduced number of teeth

Intelligence Less developed More developed

Small brain Large brain

C O N C E P T C H E C K !

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K E Y T E R M S arboreal adaptation bilophodont brachiators canine– premolar honing complex

clade dental formula derived characteristics diastema

dietary plasticity diurnal grade hominin

A N S W E R I N G T H E B I G Q U E S T I O N S

C H A P T E R   6 R E V I E W

Why study primates? • Primates are physically and behaviorally similar to

humans in numerous ways. For example, the forward- facing eyes and grasping hands tell scientists that there is a common ancestry.

• Primates, including humans, are remarkably diverse, yet they all show ability to adapt to a wide range of circumstances.

• Owing to biological similarities between primates and humans, the study of diseases in primates helps us understand and cure diseases in humans.

• Primate diversity reflects the diversity of animal species. Reduction in primate diversity is a barometer of the “health” of the animal kingdom.

What is a primate? • Primates, an order of mammals, are best defined

on the basis of their evolutionary trends: they are arboreal, have highly flexible diets, and invest a great deal of time in their young. Overall, they are generalized— primates have specialized in not specializing.

• Their physical characteristics reflect primates’ adaptation to life in the trees. A highly versatile body structure facilitates great mobility and manual dexterity. Vision is highly developed, but the senses of hearing and smell are greatly de- emphasized in most primate taxa.

• Primates’ highly varied diet is reflected in a generally nonspecialized dentition including functionally distinctive tooth types.

• Primates’ prolonged care for young reflects the fact that primates have a lot to teach, especially in the area of complex social behaviors.

What are the kinds of primates? • The more than 200 primate species living today are

subdivided into two suborders, strepsirhines and haplorhines. Strepsirhines are the lesser, or lower, primates. Haplorhines are the higher primates. Tarsiers are included in the haplorhines but retain a significant suite of primitive characteristics.

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REVIEW THIS CHAPTER WITH PERSONALIZED, INTERACTIVE QUESTIONS THROUGH IJK, INQUIZITIVE.WWNORTON.COM q

So far, we have concentrated on the anatomical differences among the different taxa of living primates. Of course, primates are not just about bones and teeth and other physical components. Like their anatomical variation, primates’ behavioral variation reflects millions of years of evolution, during which adaptive strategies have enhanced the survival and reproduction of individuals and societies.

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E V O L U T I O N R E V I E W Our Closest Living Relatives

Synopsis As a group, the members of the order Primates differ from other mammals in three key respects related to the evolution- ary history that shaped their morphology and behavior. Primates are characterized by arboreal adaptations (associated with life in the trees), dietary flexibility (associated with the wide variety of foods that they eat), and parental investment (associated with offspring that require a large amount of care). Despite these key similarities among its members, perhaps the most remarkable fea- ture of the order Primates is its immense diversity. Some primates are nocturnal, whereas others are diurnal. Some primates spend most of their time in the trees, whereas others spend a great deal of time on the ground. Some primates have specialized diets, whereas others might eat just about anything. The immense diver- sity among living primates was shaped by evolutionary forces over tens of millions of years, and this diversity reflects the interactions between species and their environmental settings.

Q1. Primates are characterized by adaptations for life in trees and for eating a broad diet. Provide two examples of primate adaptations for life in the trees and two examples of primate adaptations for eating a wide variety of foods.

Q2. Primates are also characterized by unique patterns of parental investment compared to other mammalian species. Describe three major features of primate parenting. What are the impli- cations of these parenting features for intelligence, socializa- tion, and fitness?

Q3. Compare and contrast the traditional/gradistic and evolu- tionary/cladistic approaches to primate classification. How do morphological and genetic features contribute to defining evolutionary (ancestral–descendant) relationships more accu- rately in the cladistic approach? Does the traditional/gradistic or evolutionary/cladistic scheme more accurately represent the similarities and differences between all members of the order Primates?

Hint See Table 6.2.

Q4 . Discuss the ways in which evolutionary forces might operate to produce the huge amount of anatomical and behavioral diversity seen in the order Primates today. How does such diversity reflect the adaptability and evolutionary “success” of the order?

Hint Consider the ways in which different primates occupy distinct ecological niches.

Q5. As humans, we are obviously accustomed to thinking about most issues from a “people-centric” perspective. Pretend for a moment that you are a chimpanzee, gorilla, howler monkey, tarsier, ring- tailed lemur, or one of the many other nonhuman primate species discussed in this chapter. Which ecological and environmental factors have the greatest potential to affect the evolutionary future of your species? What types of adaptations might be most beneficial in response to these selective pressures?

K E Y T E R M S loph nocturnal olfactory bulb opposable parental investment

phylogeny power grip preadaptation precision grip prehensile tail

primitive characteristics rhinarium sectorial (premolar) tooth comb Y- 5

A D D I T I O N A L R E A D I N G S

Caldecott,  J.  and  L.  Miles, eds. 2005. World Atlas of Great Apes and Their Conservation. Berkeley: University of California Press.

Campbell,  C.  J.,  A.  Fuentes,  K.  C.  MacKinnon,  M.  Panger, and S. K. Bearder, eds. 2006. Primates in Perspective. New York: Oxford University Press.

Falk, D. 2000. Primate Diversity. New York: Norton.

McGraw, W. S. 2010. Primates defined. Pp. 222–242 in C. S. Larsen, ed. A Companion to Biological Anthropology. Chichester, UK: Wiley- Blackwell.

Nowak,  R.  M.  1999. Walker’s Primates of the World. Baltimore: Johns Hopkins University Press.

Rowe, N. 1996. The Pictorial Guide to the Living Primates. Charles- town, RI: Pogonias.

Swindler,  D.  R.  1998. Introduction to Primates. Seattle: University of Washington Press.

Gombe National Park, Tanzania

AT GOMBE NATIONAL PARK, Tanzania, in 1972, one of her research subjects exam- ines Jane Goodall, who sometimes hid bananas for the chimpanzees beneath her shirt. A world-renowned primatologist, Goodall established the Jane Goodall Institute, dedicated to preserving wildlife worldwide. Projects spearheaded by the Institute, such as sanctuaries in Africa for orphaned chimpanzees, provide opportunities for continued research and educa- tional outreach, as well as jobs for local communities.

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7 Why are primates social?

What is special about primate societies and social behavior?

How do primates acquire food?

How do primates communicate?

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Primate Sociality, Social Behavior, and Culture

B I G Q U E S T I O N S ?Of all the scientists mentioned in this book so far, Jane Goodall (see Figure 1.2) may be the most famous. But when Goodall began doing what she most loves— observing primates and talking about them— about the only people who had heard of her were family and friends in her native England. Since childhood, Goodall had dreamed of living in Africa; and in 1957, after graduating from secretarial school and holding a series of odd jobs, she traveled with a friend to Kenya. Within two months, she had met the famous fossil hunter Louis Leakey (fossils are the subject of chapter 8; you will hear more about Leakey in chapter 10), who eventually employed her at the national museum in Nairobi.

Leakey was interested in human origins and had long thought that studying chim- panzees in the wild would be a window onto the behavior and social organization of early apes and humans. Other scientists, such as the American physical anthropolo- gists Sherwood Washburn and Irven DeVore, were doing pioneering field studies of baboon behavior in Kenya; but Leakey thought that chimpanzees would provide an even better understanding of the origins of ape and human social behavior. After get- ting to know the energetic and highly competent Goodall, he decided she was the right person to pursue this line of inquiry. She enthusiastically agreed to live among and study chimpanzees in Gombe, a remote area along the shores of Lake Tanganyika, in western Tanzania. This venture would have been discouraging to most. No one had

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ever observed chimpanzees in the wild for an extended period or in the kind of detail needed to record behavior and draw conclusions. Moreover, living in the jungle was no easy undertaking— it was full of uncertainty and danger.

The outcome proved even more amazing than Leakey might have imagined. A few months after reaching her field site in 1960, Goodall was able to habituate the chimpanzees to her presence, observe them for hours on end, and record their behaviors in unprecedented detail. Her findings bowled over the anthropological world. Chimpanzees proved highly intelligent, for example; and close social bonds existed between chimpanzee mothers and their offspring and between chimpanzee siblings. Goodall also discovered behaviors that other scientists found quite hard to believe, mainly because the behaviors did not fit expectations about the species. First, Goodall documented in words and on film how chimps made stick probes to harvest termites from termite nests and how they crumpled up leaves to make a kind of sponge, with which they soaked up rainwater from the crooks of trees and then squeezed the water into their mouths. That chimps used tools was an exciting discovery because it narrowed the perceived behavioral chasm between humans and apes, our closest living relatives. Second, Goodall discovered that chimpanzees regularly hunted other primates and animals. Chimps were not vegetarians!

A skilled scientist, formulating hypotheses, testing them with careful field obser- vations, and drawing conclusions based on her observations, Goodall performed pioneering research that underscored the importance of the study of primates to understanding ourselves. Among her many accomplishments, Goodall documented key elements of primate societies and of primate social behavior in its broadest terms. This chapter considers primate social behavior, especially in the important linkage between learning, behavior, and socioecology (this latter term refers to the connections between social organization, ecology, and diet). Exciting new devel- opments in the study of primates challenge long- held notions in the social and behavioral sciences that only humans have distinctive cultural traditions and that knowledge of these traditions is socially transmitted.

Underlying much of what motivates primatologists to study primate social behav- ior is one central question: Why are primates social? To seek answers to this ques- tion, primatologists study primate societies all over the world with an eye toward social diversity and ways that primate societies are organized.

Primate Societies: Diverse, Complex, Long- Lasting DIVERSITY OF PRIMATE SOCIETIES Primate societies are diverse in several ways. First, primates express themselves socially through a range of behaviors. Some of the more obvious behaviors include touching, hugging, mouthing, mounting, lip smacking, vocalizing, greeting, and grooming. Far more so than any other animal, primates use these social signals to express different kinds of relationships, many of them complex and reciprocal. These sig- nals can serve as a kind of “currency” for items or activities they are interested in,

habituate Refers to the process of animals becoming accustomed to human observers.

Primate Societies: Diverse, Complex, Long- Lasting | 167

such as grooming another individual to establish an alliance at the moment or in some future event.

Second, many primate societies are complexly organized. Within any primate group, individuals representing different kinships, ranks, ages, and sexes often form alliances.

Third, primates form various social relationships for the long term. Primates form relationships for immediate payoff (e.g., access to food or to mates), but they also establish and maintain long- term alliances that at first glance do not appear to be beneficial, especially with regard to reproductive success. For example, chim- panzee males that groom each other frequently, travel together, or engage in other cooperative activities might later compete, for food or mates, against other groups.

PRIMATE SOCIAL BEHAVIOR: ENHANCING SURVIVAL AND REPRODUCTION The theory underlying the study of primate social behavior is simple. That is, as recognized by the American biologist Edward O. Wilson in his study of animals generally, primate social behavior is influenced by evolution. Basically, natural selection favors primate behaviors that enhance survival and reproduction. In this way, the genes of individuals who engage in those behaviors pass from generation to generation. Primatologists explore the relationships between specific social behaviors and reproductive fitness. Such behaviors may be purely natural or they may be learned. In other words, sometimes primates are not conscious of their actions, and other times they strategize, learning by observation and imitation. These extremely important processes are highly elaborated in primates.

Males and females have very different reproductive roles and very different life histories in adulthood. Males provide the sperm to produce offspring. Females provide the ova to conceive the young, grow the young within them, give birth, and nurse the young. Overall, females expend far more energy in the creation of and caring for offspring than males do. As a general rule for many animals, including primates, those members of the sex that expends less energy in this way (the males) compete more aggressively among themselves for sexual access to members of the sex that expends more energy (the females).

When male primates compete for females, whether they are competing singly or in groups, the males’ bodies adapt. Sexual dimorphism in body size and in canine size is considerably higher in such societies than in societies where males do not compete. This difference reflects the fact that to compete for females suc- cessfully, males must be big and aggressive (Figure 7.1). In these societies, males are generally unrelated. In societies where males are related, live in the group in which they were born (the natal group), and compete with related males, sexual dimorphism tends to be lower than in groups where males disperse and compete with nonrelated males.

Finally, although all the life periods of primates are generally longer than those of other animals, humans have the longest life span of the primates (see Figure 6.14). The average human life lasts nearly 70 years, longer than that of the chimpanzee (44 years), the gibbon (30 years), the macaque (29 years), and the lemur (27 years). The American anthropologist Timothy Gage suggests that humans are the only primate to have “baby booms”—that is, variation in numbers of offspring in a population, fluctuating from large numbers to small numbers over time.

Body size dimorphism

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FIGURE 7.1 Competition and Dimorphism Among primates, as shown in these charts, sexual dimorphism in body size and in canine size is directly related to group composition. Here, a value of 1.0 indicates no sexual dimorphism. In primate species with monogamous pairs (such as gibbons), there is less competition for females and thus little sexual dimorphism. In primate species with multiple females but only a single male (such as gorillas), there is substantial competition among males to hold the dominant position and thus great sexual dimorphism. In primate species with multiple males competing for multiple females (such as chimpanzees), the sexual dimorphism is not as extreme as in single- male groups.

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PRIMATE RESIDENCE PATTERNS Animals such as birds and nonprimate mammals tend to be regimented in their social structures and residence patterns. By contrast, individual primate species combine different patterns, and their social groups are strongly influenced by fac- tors such as food availability, environment, and competition. Although it is thus exceedingly difficult to fully understand primate social behavior, primatologists have identified six main types of primate residence patterns (Figure 7.2):

1. One- male, multifemale. This haremlike organization consists of one reproductive- age male, several mature females, and the immature offspring. The society is polygynous, meaning that the one male has more than one partner. Gorillas, orangutans, some howler monkeys, some langurs, and some Old World monkeys, such as gelada baboons, practice this social system.

2. One- female, multimale. This group consists of one reproductive- age female, several mature males, and the immature offspring. The society is polyan- drous, meaning that the one female mates with nonpolygynous males. The males often cooperate with the females in parenting activities. Only some New World monkeys practice this social system, and only rarely.

3. Multimale, multifemale. This group consists of many adults, male and female, and the offspring. Both sexes mate promiscuously. Competition for mates tends to be relatively low, especially among males. Many Old World mon- keys, a few New World monkeys, and chimpanzees fit in this category.

polygynous Refers to a social group that includes one adult male, several adult females, and their offspring.

polyandrous Refers to a social group that includes one reproductively active female, several adult males, and their offspring.

1 One-male, multifemale 2 One-female, multimale

4 All-male 5 One-male, one-female 6 Solitary

3 Multimale, multifemale

FIGURE 7.2 Primate Residence Patterns Primates exhibit these six social groupings, which in many cases can change. In some species, for example, groups break apart if food is scarce and reunite when food becomes more ample.

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4. All- male. In some species, such as baboons, males form at least temporary groups, typically before joining or forming groups that include males and females. All- male groups commonly exist together with multimale, multife- male groups.

5. One- male, one- female. This group consists of an adult male, an adult female, and their immature offspring. Mating is typically monogamous, so each partner’s reproductive success is tied to that of the other, and the male invests a relatively large amount of time and energy in the young (e.g., through protection and food acquisition). Gibbons, siamangs, two ceboids (owl monkeys and titi monkeys), and several species of strepsirhines practice this form of society.

6. Solitary. Solitary primates go it alone— rarely are individuals seen with oth- ers. Interaction between adult males and adult females occurs only for sexual activity. Only orangutans and a few strepsirhines are solitary. An orangutan male has greater reproductive success if he maintains a territory with areas traversed by two or more females. Orangutan sexual dimorphism is predict- ably quite high— adult males are twice the size of adult females and have large canines, large cheek pads, and very loud calls over long distances. Males that have been relatively unsuccessful at competing for access to females tend to be more solitary than more successful males.

PRIMATE REPRODUCTIVE STRATEGIES: MALES’ DIFFER FROM FEMALES’ Because reproduction makes very different demands on males and females in terms of energy expenditure and time investment, each sex has a different set of reproductive strategies and interests. As discussed above, males’ primary strategy is to physically compete for access to reproductively mature females, resulting in a strong degree of natural selection in males for both large bodies and large canines. This form of natural selection is called sexual selection. Another male strategy is infanticide, the killing of a nursing infant, primarily by a foreign male that has driven the single male out of a one- male, multifemale group. The American primatologist Sarah Blaffer Hrdy has hypothesized that the new male kills the nursing infant so that its mother stops lactating, resumes ovulation, and becomes sexually receptive to him. As a result, the new male enhances his reproductive fitness, largely at the expense of the previous male.

Whereas males compete with each other for mates, females compete with each other for resources that enable them to care for young. In various New World and Old World monkeys, including macaques and some baboons, the competition for resources happens within the context of stable dominance hierarchies. Hierarchi- cal ranks usually pass from mother to daughter, and younger sisters usually rank higher than older sisters. The higher the rank, the greater the ability to acquire important resources, such as food. Higher- ranked females also tend to have more offspring, such as in gelada baboons in East Africa (Figure 7.3). In some primates, higher- ranked females have a greater number of offspring because they begin reproducing months before lower- ranked females. For example, dominant yellow baboons in Kenya start reproducing some 200 days before lower- ranked ones.

In addition, some female primates are relatively more selective in choosing mates than are others, making the selection on the basis of characteristics such as disposition, physical appearance, and position in social hierarchy. Some adult

monogamous Refers to a social group that includes an adult male, an adult female, and their offspring.

sexual selection The frequency of traits that change due to those traits’ attrac- tiveness to members of the opposite sex.

infanticide The killing of a juvenile.

0

Female rank

LowMiddleHigh

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FIGURE 7.3 Female Dominance Hierarchy This graph compares the birthrates among high-, middle-, and low- ranked female gelada baboons. The higher the rank, the greater a female’s access to resources and the more offspring she will bear.

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females’ social behaviors encourage support for and investment in their offspring by other members of the group. And some adult females protect their infants from aggression, as when they attempt to prevent infanticide.

THE OTHER SIDE OF COMPETITION: COOPERATION IN PRIMATES Although competition is central to primate social behavior, primates are also highly cooperative social animals. About half the size of gorillas and not very dimorphic sexually, chimpanzees hunt in groups of cooperating males, often preying on juvenile monkeys, such as red colobus. Chimpanzees also share food following a hunt. Other primates issue warning calls to their social group when predators approach. Many primates groom each other (Figure 7.4). In nonhuman primates, grooming involves one individual picking through the skin and hair of another individual, removing insects or other foreign objects, sometimes eating these materials. Among this practice’s functions are bonding two members of a social group, calming the primate being groomed, or appeasing that primate if he or she has a higher position in a dominance hierarchy.

Some cooperative behaviors are altruistic, in that they appear to reduce the reproductive fitness of the individuals performing them but enhance the recipi- ents’ reproductive fitness. For example, adult baboons might give warning calls to

Male and Female Reproductive Strategies

Reproductive strategies differ in male and female primates. Males compete for mates, but females both compete for resources and invest time and energy in care of offspring.

Sex Reproductive Strategy and Outcome

Males Behavior: Physical competition for access to females Outcome: Selection for large body size and for large canines; selection for loud vocalization ability in some territorial primates Behavior: Sometime killing of nursing young (infanticide) Outcome: Suppressed lactation, resumption of ovulation, and receptiveness to new male partner

Females Behavior: Acquisition of resources for raising young, usually in competition with other females Outcome: Higher- ranked females provide more resources than low- ranked females do

C O N C E P T C H E C K !

altruistic Refers to a behavior that bene- fits others while being a disadvantage to the individual.

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their social group or even attack predators and, in doing so, place themselves at jeopardy. Grooming, food sharing, and caregiving are also altruistic because one primate invests time and effort in another.

Why should a primate engage in altruistic behavior? Altruism seems not to be  directed haphazardly but rather is directed primarily at relatives. According to the British evolutionary theorist William Hamilton’s hypothesis of kin selec- tion, the evolutionary benefits of an altruistic behavior to the kin group outweigh costs to the individual acting altruistically. A primate will most strongly and consis- tently act altruistically when living with relatives. This is particularly true among cercopithecoids, such as baboons and macaques, where females live mostly in the natal group, or in chimpanzees, where males live in the natal group. Wrangham has observed groups of cooperating (related) male chimpanzees attacking groups of male chimps unrelated to them. He has also observed groups of cooperating male chimps patrolling territorial boundaries. Such behaviors in living chimpanzees may be the best model for early hominin behavior and for the origins of human aggression.

Cooperation has many advantages, but it ultimately provides most primate taxa with their distinctive behavioral characteristic: primates live in social groups. And the primary reason for sociality is probably that while many primates are profi- cient predators, primates are preyed upon by a range of predators. The American primatologist Susanne Shultz and her associates suggest that the earliest primates were largely nocturnal and led a solitary existence. This understanding is suggested by the fossil record (see chapter  8) and by the fact that the nocturnal primates today are also the most primitive (many of the strepsirhines). As soon as primates began a diurnal lifestyle, they became subject to increased predation, which in turn placed an adaptive advantage on cooperative behavior and group living. Under circumstances of increased predation, primates’ joining together to defend themselves from predators would seem to be an important form of cooperative behavior. While primatologists have observed the kinds of warning calls and direct

(a) (b)

FIGURE 7.4 Grooming Among many primates, including (a) chimpanzees and (b) humans, grooming is one of the most important social bonding behaviors. While helping ensure proper hygiene and good health, it can also cement social bonds between individuals, resolve conflicts, and reinforce social structures or family links.

kin selection Altruistic behaviors that increase the donor’s inclusive fitness, that is, the fitness of the donor’s relatives.

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physical defenses described above, however, the evidence of primates’ protecting each other from predators is slim. It is difficult to directly observe predation, for example, because predators tend to be afraid of humans and they avoid primate groups being studied.

Many primates are preyed upon by large birds, such as eagles. Susanne Shultz and the American primatologist Scott McGraw have studied eagles’ nests since the remains left in them— representative samples of “meals”—provide proxy informa- tion about what the eagles hunt and how often. The results show that predation rates are lower among larger primate groups than among smaller primate groups. Predation is a very strong selective pressure, and mutual cooperation— sociality— has been favored among primates because of the protection it provides. Sociality also provides access to mates, but the advantage of cooperation within a society is the underlying explanation for primates’ living in social groups.

Getting Food: Everybody Needs It, but the Burden Is on Mom Primates acquire their food through a wide variety of foraging practices, which entail looking for food, then handling and processing the food for consumption. The American physical anthropologist Karen Strier estimates that on average for- aging can take up over 50% of a primate’s waking time. This burden is especially great on mothers. Not only do mothers need to eat food that will provide  the energy for gestation and lactation, but they also need to look for food and then han- dle and process it for their young to consume. In a few primate species, the father is involved in caring for and providing food for the young, but generally the mother is the sole provider of her offspring’s food. The American primatologist P. C. Lee estimates that in adult female primates, a mother’s energy requirements are between two and five times higher than a nonmother’s. For the female primate, success in caring for young, both before and after their birth, is very much tied to adequate nutrition. Females with good nutrition have young at an earlier age, have healthier young, experience shorter intervals between births, and live longer than those with suboptimal nutrition.

Three key factors contribute to a female primate’s success at feeding: quality, distribution, and availability of food. Quality refers to food’s providing energy and protein that are readily digestible. Mature leaves and mature grasses, for example, are of relatively little value to many primates because the cellulose and dietary fiber are much harder to digest for nutrients than are the cellulose and dietary fiber of young leaves and young grasses. As discussed in chapter 6, sharp- crested teeth and compartmentalized stomachs have evolved in some primates, especially in leaf- eating monkeys. For example, folivorous Old World monkeys have sharper crests connecting the cusps on the fronts and backs of the occlusal surfaces of their bilophodont molars.

Distribution refers to the locations of food across the landscape. Ideally, the primate would have to expend relatively little energy to acquire food. In terms of evolution, behaviors that minimize the costs of acquiring food are selected for. Many primates focus on patches of food, such as a fruit- bearing tree or a group of such trees, whose fruit provides a ready and concentrated source of nutrients.

Acquiring Resources and Transmitting Knowledge: Got Culture? | 173

However, a small patch will support only a relatively small group. All primates are able to adjust the size of the feeding group in relation to the amount of food avail- able in a patch. Some primates, such as chimpanzees, can be enormously flexible in making such adjustments.

Food availability can be highly fluid, depending on season and rainfall. The farther a region is from the equator, the more defined are its seasons and the less available are fruit and leaves, primates’ main food sources. Thus, primates are generally restricted to equatorial regions.

Acquiring Resources and Transmitting Knowledge: Got Culture? Primates and humans acquire food in vastly different ways. While primates can acquire food using only their bodies, humans depend on technology— material culture— to acquire food. But this distinction does not mean that primates have no material culture.

In the 1960s, Jane Goodall became the first to question that assumption when she observed adult chimps poking twigs into a termite hill, withdrawing them, and eating the termites that clung to the twigs (Figure 7.5). Goodall realized that one fundamental assumption about what it means to be human— namely, that material

FIGURE 7.5 Chimpanzee Tool Use When “fishing” for termites (which are highly nutritious), a chimpanzee selects a branch or twig thin enough to pass through holes of a termite nest, then removes all extra branches and leaves and inserts the twig into the nest. Simple and disposable, even primitive, tools like this might have been used by our ancestors long before the appearance of stone tools some 2.5 mya.

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culture (and culture in general) is exclusive to human beings— seemed incorrect. Other scientists then realized that living chimpanzees’ tool use may be the best model for understanding our prehuman ancestors’ earliest cultures (among the topics of chapter 10).

Based on Goodall’s research and a great deal of work since, anthropologists have identified three central features about chimpanzees’ tool use. First, chimpanzees are extraordinarily intelligent and have the complex cognitive skills necessary for at least some kinds of behaviors that require learning and the ability to under- stand complex symbolization. The evidence for this ability is impressive, and it is growing. For example, chimpanzees are able to accomplish a number of complex behaviors for which visual acumen and ability to think abstractly are essential ele- ments. In laboratory or otherwise controlled settings, humans have taught young chimpanzees to crack open nuts with stones. In turn, these chimpanzees have taught other young chimpanzees to crack open nuts. Chimpanzees have also been shown how to use a sharp stone tool to cut a cord in order to gain access to food in a box. Similarly, they have been shown how to make simple stone tools, and they subsequently have passed on that behavior to relatives. Second, in natural settings where chimpanzees have not been taught by humans, mothers have also shown their young how to use tools (Figure 7.6). Most of the tools chimpanzees produce are for acquiring and consuming food. Among the rare examples of primate tool use unrelated to food is that of chimpanzees in Gombe throwing stones as part of a dominance conflict between adult males. One of chimps’ most fascinating food- based innovations, observed by the American primatologist Jill Pruetz, is the creation and use of a spearlike object— a trimmed, pointed twig— to skewer strep- sirhines for food (Figure 7.7). Third, tool production and tool use are sometimes highly localized. For example, although some adjacent chimpanzee groups in West Africa use stones to crack open hard- shelled nuts, this tool use has not been seen anywhere else in Africa.

While chimpanzees do not depend on material culture for survival— certainly not to the extent of living humans— they nonetheless use material culture. Labo- ratory experiments and natural- setting research from a range of places in Africa show that chimpanzees use several forms of tools and that not all forms occur in all chimpanzee groups. Perhaps local traditions are passed from generation to generation via social learning— parents pass the information to offspring, and the young share it with other young. In a very real sense, then, tool use in primates is

FIGURE 7.6 Chimpanzee Social Learning A chimpanzee juvenile watches its mother crack open palm nuts with a stone hammer and anvil in Guinea, West Africa.

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an important form of social and cultural transmission. Moreover, the widespread nature of chimpanzee tool use suggests that it dates back to antiquity. Sites on the Ivory Coast of West Africa contain chimpanzee tools from 4,000–5,000 yBP, but tool use likely started earlier than that.

What about other primates? Field observations by the Swiss anthropologist Carel van Schaik and his associates show that, like chimpanzees, orangutans in Borneo and Sumatra habitually use probes to obtain insects for food. Across the Atlantic in South America, some capuchin (Cebus) monkeys use stones to dig for food and to crack open nuts. The complexity here is far less than that of human technology, but these simple behaviors show that chimpanzees are not the only primates that interact with the environment through tools they make.

Vocal Communication Is Fundamental Behavior in Primate Societies All primates produce vocalizations of some type that serve various functions. Some quiet calls can be heard only by nearby group members, while some loud calls convey information over great distances and through dense vegetation. Scientists once believed that primate vocalizations were merely innate, emotional utterances produced involuntarily in response to stimuli and that, therefore, these vocaliza- tions could tell us nothing about the evolution of human language. Research has shown, however, that these vocal systems are rich and complex and largely under the callers’ control. The study of primate vocal communication can give us insights into the selective pressures that may have shaped the evolution of language.

To “translate” primates’ calls, scientists first catalog a population’s vocal reper- toire. They then determine the contexts in which the members of that population produce the different vocalizations. Primate voices vary just as human voices do, but individuals in groups produce similar calls in categories.

FIGURE 7.7 Chimpanzee Spears (a) A chimpanzee made this spear from a tree branch, sharpening one end with its teeth. (b) Chimpanzees that make such spears use them to thrust into the hollows of trees and kill bushbabies. Here, an adolescent female holds a dead bushbaby. This method is primates’ first use of tools to hunt other mammals.

(a)

(b)

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Determining the context of a given call does not unequivocally prove that call’s function. The use of playback experiments has revolutionized what scientists can say about a call’s meaning, albeit only from the listener’s perspective. In conducting such an experiment, the researchers record naturally occurring calls (Figure 7.8). They then use hidden speakers to broadcast call sequences to the primate group. In a classic example, the American primatologists Dorothy Cheney and Robert Seyfarth played the sound of an infant vervet monkey screaming to a group of mothers whose infants had all wandered off. Only the mother of that particular infant looked toward the hidden speaker, a finding that suggests females recognize the voices of their own infants. To Cheney and Seyfarth’s surprise, however, the other females looked at the mother of the screaming infant. This finding gave the researchers insight into what primates “know” about each other. Their study laid the groundwork for a field of research in which scientists use carefully designed playback experiments to “interview” free- ranging primates about their social cognitive abilities.

In this way, researchers have determined that some quiet calls produced by primates mediate social encounters within a group. For example, Cheney, Sey- farth, and their colleagues, in studying chacma baboons in Botswana, found that a subordinate baboon was less likely to move away from a dominant animal if the dominant quietly “grunted” as it approached the subordinate. Conversely, if the dominant animal did not grunt, the subordinate would almost always move off. If the approaching dominant produced a “ threat- grunt,” a version of the call that indicates aggressive intent, the listener would likely flee rapidly.

Unlike quiet calls exchanged between nearby animals, the loudest calls in a pri- mate species’ repertoire transmit information over long distances and are typically produced during events such as an encounter with predators, an aggressive contest

FIGURE 7.8 Recording Alarm Calls Dawn Kitchen records chacma baboon alarm calls in Botswana. The lion prompting these calls is lying in the grass, about 75 m (250 ft) behind Kitchen.

Vocal Communication Is Fundamental Behavior in Primate Societies | 177

with another group, and one animal’s separation from its group. In howler monkey societies, for example, adult males in different groups compete through their long, loud calls, warning potential competitors to stay off their turf. (Once you hear one of these bizarre calls, you understand why they are called “howlers.”) The American primatologist Dawn Kitchen documented extremely loud choruses by male black howler monkeys in Belize. She found that the voices of individual callers within a group do not completely overlap during a chorus; thus, it is possible for listeners in another group to “count” the number of rivals they will face based on vocal cues alone. Howlers can assess the strength of opposing groups according to these cri- teria. Using playback experiments, Kitchen found that howler groups that thought they were outnumbered by invaders retreated, whereas groups that thought they outnumbered intruders not only vocalized in return but also advanced on the sim- ulated rivals (Figure  7.9). Likewise, Kitchen found that during aggressive male/ male competition in chacma baboons, the loud, repetitive call displays (“wahoos”) produced by adult males reliably indicated the caller’s physical condition. By judg- ing each other’s calls, rival baboons can assess an opponent’s fighting ability and avoid a contest with a superior opponent.

Although primate vocalizations (such as the screams of an attack victim) can indicate a caller’s emotional state, many also seem to convey information about the world around the caller. In the Taï Forest of the Ivory Coast in western Africa (see Figure 6.2), Diana monkeys produce two different loud alarm calls in response to predators, depending on whether the predator is terrestrial (such as a leopard) or aerial (such as an eagle). Importantly, each type of predator requires a very different escape response from the Diana monkey. Using playback experiments, the Swiss primatologist Klaus Zuberbühler and his team found that listeners treat all sounds in the forest associated with one type of predator the same. For example, a leop- ard’s growl produces the same response as the leopard alarm call of a male Diana monkey, despite the acoustic differences between these sounds. These and other experimental results suggest that primate calls can be functionally referential.

(a) (b)

FIGURE 7.9 Primate Vocalizations (a) Male howler monkeys, such as the one in action here, are among the male primates that vocalize to protect their territories, their resources, and/or their females. Despite the name, howler monkeys roar more than howl, and their notorious calls can be heard over great distances. Howler monkeys are the loudest land animal and the second loudest of all animals, outdone only by the blue whale. (b) This chimpanzee is presenting a series of grunts, perhaps characterizing a food source. Chimpanzee vocalizations are diverse and difficult to interpret.

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That is, these calls convey semantic- like meaning, which makes them similar to human words, at least from the listener’s perspective.

The variation in predator- specific vocalizations indicates that Diana monkeys have evolved an ability to modify their vocalizations and behavior based on the type of predator and the predator’s attack strategy. For example, Diana monkeys issue loud alarm calls when they are confronted by “ambush” predators such as leopards or eagles, both of which are especially efficient hunters when they are able to surprise their prey. When “pursuit” predators such as chimpanzees or humans are also nearby, however, the Diana monkeys’ loud alarm calls enable the preda- tors to locate the monkeys. Zuberbühler found that Diana monkeys with a lot of exposure to chimpanzees respond more appropriately to playbacks of chimpanzee vocalizations— remaining silent and quietly moving away— than did monkeys with little chimpanzee experience. This finding strongly suggests that the perception of and response to certain vocalizations is learned.

Like monkeys, chimpanzees can label events and objects. They and many other primates have displayed food- associated vocalizations. In controlled laboratory studies of chimpanzees, Zuberbühler and his colleague Katie Slocombe found that chimpanzees express a specific kind of “rough grunt” when they see food. This grunt can vary in specific ways, depending on the type of food and how much the chimpanzee wants that food. Interpretations of distinctive sounds made by chimpanzees in field settings are beginning to provide new insights into how these apes communicate, insights going far beyond what can be learned in laboratory settings alone. The English primatologist Cathy Crockford and her associates have been studying chimpanzee communication in the Budongo Forest, Uganda. Their work shows that chimpanzee communication involves different combinations of sounds— grunts, pants, hoots, screams, barks, and other vocalizations— most of which have meaning for the individual that is vocalizing and for the intended audience. The work of Crockford and her colleagues shows that, as with most communication in other primates, understanding chimpanzee communication requires knowledge of both the vocalizations and their contexts. The vocaliza- tions can be studied through recordings, but the contexts must be observed in the primates’ natural setting. The natural environment provides critical clues to the meanings of vocalizations.

Because some calls within a species’ repertoire vary so subtly that the human ear cannot easily differentiate them, the analysis of acoustic properties of vocal recordings (such as duration, amplitude, and frequency of a call) is a critical step in translating primate vocalizations. For example, the German scientist Julia Fischer and her colleagues found that female baboons produce two loud calls that are very similar: one when they encounter a predator and another when they are separated from their group. Using specially designed computer software, Fischer found that these two call types grade into each other along an acoustic continuum (in the same way that the words fire and far seem to overlap when spoken with a southern US accent). Furthermore, these subtle differences were detectable to baboons— adult females hearing the two call types during playback experiments responded strongly only to the alarm calls. These and other experiments suggest that, like humans, primates can perceive acoustically graded calls in discrete ways.

Primatologists are also learning that vocalizations have clear patterns, some of which bear a striking resemblance to the structural elements of human language. Humans change word structure to change meaning. One of the most important examples is what linguists call affixation, whereby a small unit is added at either the beginning (prefix) or the end (suffix) of the word stem (the part of the word that

FIGURE 7.10 Research on animal communication with a habituated group of chimpanzees in the Budongo Forest Reserve in Uganda.

FIGURE 7.11 Campbell’s monkeys use specific alarm calls containing prefixes and suffixes.

Vocal Communication Is Fundamental Behavior in Primate Societies | 179

is never altered). Exciting new work by Zuberbühler and his group on Campbell’s monkeys, also inhabitants of the Taï Forest, reveals that these primates use a kind of affixation by adding suffixes (similar in some respects to English- speakers’ changing the present tense of a verb to past tense by adding -ed ). These researchers recorded a loud “krak” sound produced by adult male Campbell’s monkeys that had seen a leopard in the area. Sharing the same forest, Diana monkeys and Campbell’s monkeys have learned to respond to one another’s alarm calls with their own alarm calls. However, when Campbell’s monkeys issue a leopard alarm call in response to the leopard alarm call of Diana monkeys, they affix an “oo” sound to the warning call. This “ krak- oo” alarm call indicates that they have heard the initial alarm call from a different primate taxa. These primates’ altering of a stem term through the addition of a suffix is a very important discovery because it provides a strong parallel with human word construction. While human language is extremely com- plex and most of its characteristics are completely different from other animals’ (including nonhuman primates’) communication, this parallel suggests what the early hominins’ first form of speech may have been like.

Humans routinely invent new vocalizations throughout their lives, but nonhu- man primates appear to be basically preprogrammed, producing most of the calls typical of their species shortly after birth. However, as the Diana monkey example above illustrates, primates must still learn to use and to respond to these vocaliza- tions appropriately. For example, vervet monkeys are susceptible to predation by raptors (birds of prey) and are born able to produce predator- specific alarm calls. Cheney and Seyfarth, in systematically recording the developmental changes in vocal usage among vervets living in Kenya, discovered that very young monkeys will produce these alarm calls in response to anything startling that appears in the sky— an actual raptor, a harmless songbird, even a falling leaf. As vervets age, they refine their call production, limiting it first to all raptors and finally, by the time they are adults, to only that subset of raptors large enough to prey on vervets. Likewise, until a vervet is about seven months old, before it reacts to alarm calls with an appropriate predator- escape response, it will look toward an adult or run toward its mother.

In addition to warning of predators in the neighborhood, primate vocalizations serve to name resources or monitor the changing political landscape within a social group. They are an essential part of the repertoire of primate communication, which includes visual, chemical, and tactile channels. Like humans, apes gesture with their hands, limbs, and bodies; and many of these behaviors are learned. Some 20 different gestures have been cataloged in siamangs, for example. Chimpanzees have been found to extensively and flexibly use gestural communication, even developing novel gestures in new situations. The primatologist Bill McGrew and his colleagues, while observing chimpanzees in Mahale National Park, Tanzania, were the first to note an unusual grooming technique, the hand clasp. The two participants face one another. Each one holds a hand up over his or her head and clasps the other’s hand, forming an A- frame; and each uses his or her free hand to pick parasites and other detritus off the other participant (Figure 7.12). Although this is the customary way to groom at Mahale, the nearby chimpanzees of Gombe National Park, Tanzania, do not groom in this manner; and these differences are not likely explained by ecological or genetic differences in the two populations. In addition to differences in grooming, chimpanzees show different kinds of vocaliza- tions unique to specific groups and regions. These differences suggest that some vocal features may be transmitted through social learning. Group- specific patterns of grooming, gesturing, and vocalizing are just a sample of the many behaviors

FIGURE 7.12 Hand Clasp Grooming The distinctive type of grooming depicted here has been observed only in groups of chimpanzees in Tanzania. Here, the paired chimpanzees grasp each other’s wrist, while in other groups they grasp each other’s hand. Such specific social customs are unique to individual groups of chimpanzees and thus must be learned within each group, a fundamental aspect of culture.

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identified by primatologists that represent nonmaterial aspects of primate culture. In the larger picture, the great apes— especially chimpanzees— are the nonhuman primates with the highest degree of flexibility and most extensive use of material and nonmaterial culture.

Although great apes lack the physical ability to produce human speech, the find- ings of several “ape language” research projects indicate that they have some of the rudimentary cognitive abilities necessary to understand human speech. Different groups of scientists have taught orangutan, gorilla, chimpanzee, and bonobo sub- jects to communicate with humans using either American Sign Language or graph- ical symbols on computerized keyboards (lexigrams). While watching his mother being taught by Sue Savage- Rumbaugh and her colleagues, a captive bonobo named Kanzi spontaneously learned to use lexigrams (this process is in fact similar to the way human children learn to speak). Kanzi remains one of the most successful nonhuman users of such a symbolic communication system. He can understand English at the level of a two- year- old human, and he combines lexigrams in new ways according to a set of rules. The researchers argue that Kanzi’s competence reflects an ancient history for a form of proto- grammar. Although such research has its share of critics, the ape language projects will continue to enrich what we know about the cognitive abilities of our closest living relatives, and they may shed light on the behaviors and linguistic abilities of our common ancestor.

This chapter has discussed primates’ social behaviors, the methods that primates use for acquiring food, and the growing understanding of the essential role of material culture and nonmaterial culture and communication. All the information presented in this and the previous chapter lays the foundation for understanding the next part of this book, on roughly the last 50  million years of primate and human evolution.

FIGURE 7.13 Student teacher Joyce Butler of Columbia University shows famous chimpanzee Nim Chimpsky the sign configuration for “drink,” and Nim imitates her.

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Why are primates social? • Generally, primates that cooperate in social groups

are better able to protect themselves from predators. Those in larger groups are better able to protect themselves than those in smaller groups.

• Living in social groups provides access to mates and enhances reproductive success. In the short term, sexually mature males and females living in the same group have reproductive access. In the long term, young are taught normative behaviors that reduce stress, promote longevity, and enhance success overall.

What is special about primate societies and social behavior? • Primate societies are highly diverse, ranging from

solitary animals to complex multimale, multifemale groups. Most primates live in some kind of social group and do so on a long- term basis.

• Male reproductive strategies emphasize competition between males for access to reproductive- age females. Female reproductive strategies emphasize care of young and access to food for young and for the support of mothers’ and their offspring’s nutritional needs.

How do primates acquire food? • Primates’ wide variety of habitats require them

to use a wide variety of food- foraging strategies. Chimpanzees are the only primate known to

systematically hunt other animals, including other kinds of primates.

• Primates rely entirely on their bodies for acquiring and processing food for consumption. Humans rely on extrasomatic means— material culture— to acquire and process food. Chimpanzees, orangutans, and some New World monkeys employ rudimentary technology, reflecting socially transmitted knowledge.

• Some primates (chimpanzees, for example) have material culture. They and other primates have displayed some learned behavior and cultural tradition, such as forms of social grooming and vocalization that are unique to specific groups and regions.

How do primates communicate? • Primates communicate information through a wide

variety of means, especially through vocalization. • Vocalizations in all primates serve a range of

functions and vary in different contexts; they include the transmissions from one individual to another individual or one group to another group, as in warning about predators, sending of alarms, “labeling” of events or objects, and identification of territory.

• Humans are the only primate to have speech, but use of symbols by apes (e.g., chimpanzees) in experimental contexts provides important insight into their cognitive abilities.

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REVIEW THIS CHAPTER WITH PERSONALIZED, INTERACTIVE QUESTIONS THROUGH IJK, INQUIZITIVE.WWNORTON.COM q

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infanticide kin selection

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E V O L U T I O N R E V I E W Primate Social Organization and Behavior

Synopsis In addition to the wide variation of morphological characteristics present within the order Primates (see chapter 6), nonhuman primate species exhibit considerable diversity in social organization and behavior. Different primate species engage in various primary patterns of residence (social groupings), which influence the number of males, females, and juveniles present within the group at any one time. Within a species, males and females might have vastly different reproductive strategies, which can be associated with morphological and behavioral disparities between the two sexes. Primates also engage in cooperation, communication, and cultural behaviors, all of which vary drastically across this taxonomic order. As with their morphological charac- teristics, the immense diversity of behaviors among living primates has been shaped by the evolutionary histories of different species and continues to be shaped by environmental and social pressures.

Q1. List three ways in which reproductive strategies might dif- fer among male and female primates of the same species. Describe the outcomes, in relation to morphology, behavior, and fitness, of these different reproductive strategies for both males and females.

Q2. Refer to Figure  7.1 and consider the following three primate species: bonobos, owl monkeys, and howler monkeys. Bono- bos live in multimale, multifemale groups; owl monkeys in one- male, one- female (monogamous) groups; and howler monkeys

in one- male, multifemale (polygynous) groups. Based on their residence patterns, which of these species do you expect is the most sexually dimorphic in terms of body size and canine size, which is the least sexually dimorphic, and which falls somewhere in between the others?

Q3. What kinds of advantages, in terms of evolutionary fitness, do cooperative behaviors provide among different species of nonhuman primates? Under what selective pressures would behaviors such as altruism (toward kin and nonkin) be likely to evolve?

Q4 . Provide at least three examples (material or nonmaterial) from studies of chimpanzees or other nonhuman primate species that fit the definition of culture outlined earlier in this textbook (i.e., learned behavior transmitted from individual to individual). Among the behaviors you identify, list those that are likely adaptations that help the primate species survive and any that are more likely differences in behavior occurring between two populations for no apparent (or at least adaptive) reason.

Q5. In the strictest sense, anthropology is defined as “the study of humankind.” Explain why studies of nonhuman primates are within the scope of physical anthropology. How can studies of nonhuman primate sociality and behavior enhance our under- standing of our evolutionary past, and why are they important (and anthropological) in their own right?

A D D I T I O N A L R E A D I N G S

Cheney, D. L. and R. M. Seyfarth. 2007. Baboon Metaphysics: The Evolution of a Social Mind. Chicago: University of Chicago Press.

Goodall, J. 1986. The Chimpanzees of Gombe: Patterns of Behavior. Cambridge, MA: Harvard University Press.

Hart,  D.  and  R.  W.  Sussman. 2005. Man the Hunted: Primates, Predators, and Human Evolution. Jackson, TN: Westview Press.

McGrew, W. C. 1998. Culture in nonhuman primates. Annual Review of Anthropology 27: 301–328.

Peterson, D. 2006. Jane Goodall: The Woman Who Redefined Man. New York: Houghton Mifflin.

Stanford,  C.  B.  2001. The Hunting Apes. Princeton: Princeton University Press.

Strier,  K.  B.  2011. Primate Behavioral Ecology. 4th  ed. Boston: Allyn & Bacon.

Wrangham,  R.  and  D.  Peterson. 1996. Demonic Males: Apes and the Origins of Human Violence. Pearson/Prentice Hall.

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The Past: Evidence for the Present

The past record of evolution comes from fossils. This record shows us what ancestral species looked like. For exam- ple, a 6- million- year sequence of fossils from the Middle Awash River valley, in Ethiopia, illustrates human evolution from Ardipithecus— the first bipeds— who lived 6 mya, to the earliest Homo sapiens, who lived more than 100,000 years ago. Just as important, the thousands of fossil remains of plants and animals found in this setting reveal details of the environ- ment and ecology related to this lineage, whose evolution led to all of us now living around the globe. (Photo © 1996 David L. Brill, humanoriginsphotos.com)

Living organisms have resulted from millions of years of both natural selection and other evolutionary forces. This living record has provided natural his- torians and biologists, Charles Darwin first and foremost, with important information about how evolution works and what forces are behind it. Fundamental as it is, however, the living record provides a limited picture of evolution, a record of just the surviving lineages. The other funda- mental part of the evolutionary picture is found in the past, thanks to the fossil record, which portrays the lineages and extinct species that gave rise to living species. The focus of the remainder of this book, the fossil record, is the basis for documenting and interpreting biological history.

Because fossils are the only source of evidence for what past organisms were like, where they lived, and how they behaved, living and past records are essential for under- standing evolution— one is incomplete without the other.

Part II begins with a look at what fossils are and how they can be interpreted. Once this window onto the past has been opened, we will explore the diversity and abun- dance of primate species, starting with the first true pri- mates (strepsirhines), followed by the origins and evolution of the first higher primates (haplorhines); then the appear- ance, evolution, and diversity of the first apes (hominoids); and, beginning around 6–7 mya, the origins and evolution of primitive, humanlike ancestors (hominins).

P A R T I I

THIS SKULL OF SIVAPITHECUS dates to about 8 mya. It was found in the Potwar Plateau, a region in Pakistan that has yielded many fossils. Fossils such as this one help scientists understand the physical appearance of past species. (Photo © 1995 David L. Brill, humanoriginsphotos.com)

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8 What are fossils?

What do fossils tell us about the past?

What methods do anthropologists and other scientists use to study fossils?

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Fossils and Their Place in Time and Nature

Although Charles Darwin’s theory of evolution was based mostly on his obser-vations of living species, Darwin certainly knew about fossils. His extensive reading must have included the ancient Greek historian Herodotus, who had recognized the shells preserved in rock as the remains of organisms. Darwin was no doubt familiar with discoveries of fossils in the Americas. He even had a hand in pros- pecting for fossils in Argentina, noting in his journal that “the great size of the bones . . . is truly wonderful.” He likely heard about discoveries in the United States, such as by the American president Thomas Jefferson (1743–1826), an avid fossil collector who reported on an extinct ground sloth found in Virginia (Figure 8.1). Darwin definitely knew the work of the French paleontologist Georges Cuvier (discussed in chapter 2), who had meticulously studied and published on the fossils of many different plants and animals around Paris.

Though Darwin and these other figures made important contributions to scientific and anthropological thought, none of these people fully appreciated the importance of fossils as a record of the past. Cuvier recognized the fact that fossils are the remains of once- living organisms. Darwin saw the significance of the similarity in features between living ground sloths and the extinct forms in Argentina. But fossils’ larger role in recon- structing the history of life and a time frame in which to place that history was not at the forefront of either Cuvier’s or Darwin’s thinking. In science, it sometimes takes one person with just the right combination of background, experience, and intellect to put together various lines of evidence and draw conclusions from this evidence that result in a breakthrough. The breakthrough setting the stage for fossils as a fundamental source of information about the past came not from a respected scientist but from an

B I G Q U E S T I O N S ?

186 | CHAPTER 8 Fossils and Their Place in Time and Nature

engineering surveyor with a remarkable attentiveness to detail and pattern. Unlike many of the great scientists of the eighteenth and nineteenth centuries, the English- man William Smith (1769–1839) was born into a family of very modest means. At 18, he apprenticed as a surveyor, and he eventually worked for a coal- mining and canal- construction company. In the mines, he observed that layers of rock— strata— were always positioned the same way relative to each other. He deduced this pattern from the colors and other physical properties of each stratum. He also realized that each stratum contained a unique collection of fossils representing long- extinct life- forms. From these observations, he hypothesized that the relative positions of strata and the kinds of fossils found in the layers were the same throughout England. He called his hypothesis the Principle of Faunal Succession, and he tested it with a research program that correlated strata and fossils throughout Britain.

Smith was fired from his job in 1799, likely because of his distractions from his surveying work. Despite going into abject poverty and spending time in debtors’ prison, he continued recording data across the country, ultimately, in 1815, producing the first geologic map of the British Isles. What motivated him? Like the other sci- entists we have studied, Smith was motivated by questions about the natural world around him. And he believed that fossils provided an important record of past life and of time’s passage. Although his passion was to produce a geologic map, he rec- ognized fossils’ importance in the creation of a time frame for once- living organisms. The scientific world grew to realize what an important thing he had accomplished, and in the last years of his life Smith was recognized by the leading scientists of the time. Owing to his pursuit of answers to questions, fossils became a means of docu- menting the evolution of life on Earth and a means of reconstructing geologic time.

Fossils are the very heart of the study of evolution. They provide us with the only direct physical evidence of past life and its evolution, from the simple bacterial organisms that lived over 3 billion years ago to the complex organisms that evolved later (Figure 8.2). The scientific study of fossils centers around two components:

strata Layers of rock, representing vari- ous periods of deposition.

FIGURE 8.1 Megalonyx jeffersonii Fossil Claws In 1796, Thomas Jefferson (right) discovered the bones of an extinct ground sloth. The paper he presented on his finding to the American Philosophical Society helped launch the field of vertebrate paleontology in America.

Fossils and Their Place in Time and Nature | 187

FIGURE 8.2 Kinds of Fossils Information about past organisms comes from various sources, such as (a) 250  million– year- old bacteria (Bacillus permians); (b) stromatolites, which resemble bacterial colonies that dominated life on Earth for more than 2 billion years; and fossils: (c) ammonite, (d) trilobite, (e) fern, (f) crab, (g) soft- shelled turtle, (h) fish, (i) Tyrannosaurus skeleton, and (j) Eocene primate, Darwinius masillae. Fossils like these have been found all over the world.(j)

(a) (b) (c)

(d) (e) (f)

(g) (h) (i)

188 | CHAPTER 8 Fossils and Their Place in Time and Nature

time and environment. Placement of fossils in time allows us to document phylogeny, or biological change and evolutionary relationships (see chapter 6). Placement of fossils in their environmental contexts helps us understand the factors that shaped the evolution of the organisms the fossils represent.

In this chapter, you will learn about the study of fossils, or paleontology, and the vast chronology within which scientists place the fossil record. You will also learn how paleontologists— the scientists who study fossils— determine how long ago organisms lived and what their environments were like. Paleontologists are the time- keepers of the past.

Fossils: Memories of the Biological Past WHAT ARE FOSSILS? Fossils (Latin fossilis, meaning “dug up”) are the remains of once- living organisms. More specifically, they are the remains of organisms that have been wholly or partially transformed into rock through a long process of chemical replacement. In the replacement process, the minerals in bones and teeth, such as calcium and phosphorus, are very gradually replaced with rock- forming minerals like iron and silica.

TAPHONOMY AND FOSSILIZATION Fossils can derive from any body parts, but bones and teeth are by far the most common sources, providing more than 99% of the fossil record. Taphonomy— the study of what happens to an organism’s remains— describes the multiple circum- stances that must (and must not) occur for a dead organism to become a fossil (Figure 8.3). An organism will not become a fossil, for example, if its remains are left exposed for any length of time. If the remains are exposed for more than a day or so after death, scavengers such as dogs, wolves, or birds may eat the soft tissues. Maggots will quickly consume flesh. Once the flesh is gone, the bones of the skele- ton will weather, break, or disappear. Because of the unlikelihood of a quick burial not brought about by humans, very few once- living organisms end up as fossils.

If an organism is buried soon after its death, such as under soil sediments deposited by water, the remains will be at least partly protected from scavengers. To become fossilized, however, the remains must stay in an oxygen- free (anoxic) environment, where scavengers cannot access the body and where bacterial activity and decomposition are limited.

Even in this ideal burial environment, other factors can lead to the decay or alteration of the remains. For example, groundwater or acidic soils can dissolve bones and teeth, and ground pressure or geologic activity can distort the appear- ance of any potential fossils.

TYPES OF FOSSILS Fossils are found in various types of rock, but most commonly in sedimentary rock, which is produced by water and wind carrying and then dropping tiny bits

A hominin collapses and dies on shore.

After the soft-tissue remains of the hominin decay, only the skeleton is left.

The water level of the lake rises, and the lake sediments settle and cover the hominin’s bones and footprints.

A physical anthropologist examines the fossilized hominin remains. The bones provide material for study. The ancient soils (paleosols) provide material for environmental reconstruction.

TIM E

The hominin’s footprints are left in the mud.

The bones fossilize in the thick layer of sediment at the bottom of the lake, while sediments continue to be deposited as layers. The lake dries, and other geologic processes occur. A volcanic eruption, for example, spews ash over the region, providing more layers. The fossil is now embedded in a geologic stratum.

Erosion exposes deep strata in a geologic column, revealing the fossil skeleton and footprints.

FIGURE 8.3 What Is in a Fossil?: The Making of the Biological Past

sedimentary Rock formed when the deposition of sediments creates distinct layers, or strata.

taphonomy The study of the deposition of plant or animal remains and the environmental conditions affecting their preservation.

Fossils: Memories of the Biological Past | 189

time and environment. Placement of fossils in time allows us to document phylogeny, or biological change and evolutionary relationships (see chapter 6). Placement of fossils in their environmental contexts helps us understand the factors that shaped the evolution of the organisms the fossils represent.

In this chapter, you will learn about the study of fossils, or paleontology, and the vast chronology within which scientists place the fossil record. You will also learn how paleontologists— the scientists who study fossils— determine how long ago organisms lived and what their environments were like. Paleontologists are the time- keepers of the past.

Fossils: Memories of the Biological Past WHAT ARE FOSSILS? Fossils (Latin fossilis, meaning “dug up”) are the remains of once- living organisms. More specifically, they are the remains of organisms that have been wholly or partially transformed into rock through a long process of chemical replacement. In the replacement process, the minerals in bones and teeth, such as calcium and phosphorus, are very gradually replaced with rock- forming minerals like iron and silica.

TAPHONOMY AND FOSSILIZATION Fossils can derive from any body parts, but bones and teeth are by far the most common sources, providing more than 99% of the fossil record. Taphonomy— the study of what happens to an organism’s remains— describes the multiple circum- stances that must (and must not) occur for a dead organism to become a fossil (Figure 8.3). An organism will not become a fossil, for example, if its remains are left exposed for any length of time. If the remains are exposed for more than a day or so after death, scavengers such as dogs, wolves, or birds may eat the soft tissues. Maggots will quickly consume flesh. Once the flesh is gone, the bones of the skele- ton will weather, break, or disappear. Because of the unlikelihood of a quick burial not brought about by humans, very few once- living organisms end up as fossils.

If an organism is buried soon after its death, such as under soil sediments deposited by water, the remains will be at least partly protected from scavengers. To become fossilized, however, the remains must stay in an oxygen- free (anoxic) environment, where scavengers cannot access the body and where bacterial activity and decomposition are limited.

Even in this ideal burial environment, other factors can lead to the decay or alteration of the remains. For example, groundwater or acidic soils can dissolve bones and teeth, and ground pressure or geologic activity can distort the appear- ance of any potential fossils.

TYPES OF FOSSILS Fossils are found in various types of rock, but most commonly in sedimentary rock, which is produced by water and wind carrying and then dropping tiny bits

A hominin collapses and dies on shore.

After the soft-tissue remains of the hominin decay, only the skeleton is left.

The water level of the lake rises, and the lake sediments settle and cover the hominin’s bones and footprints.

A physical anthropologist examines the fossilized hominin remains. The bones provide material for study. The ancient soils (paleosols) provide material for environmental reconstruction.

TIM E

The hominin’s footprints are left in the mud.

The bones fossilize in the thick layer of sediment at the bottom of the lake, while sediments continue to be deposited as layers. The lake dries, and other geologic processes occur. A volcanic eruption, for example, spews ash over the region, providing more layers. The fossil is now embedded in a geologic stratum.

Erosion exposes deep strata in a geologic column, revealing the fossil skeleton and footprints.

FIGURE 8.3 What Is in a Fossil?: The Making of the Biological Past

sedimentary Rock formed when the deposition of sediments creates distinct layers, or strata.

taphonomy The study of the deposition of plant or animal remains and the environmental conditions affecting their preservation.

190 | CHAPTER 8 Fossils and Their Place in Time and Nature

of rock, sand, and soil over time. In South Africa, for example, sediments were washed, blown, or dropped into caves. Coincidentally, as the sediments built up, carnivores dropped the remains of animals, including early hominins, in the caves (Figure 8.4). Sediments subsequently buried the remains and filled the caves, pre- serving fossils for millions of years.

Fossilization has also occurred when volcanic activity has buried animal remains in volcanic ash. Occasionally, volcanic ash preserves footprints, such as the spectacular tracks left by three hominins around 3.5 mya at Laetoli, Tanzania (Figure 8.5).

Though fossils do not contain the original biological materials that were present in life, even fossils that are millions of years old preserve vestiges of the original

(a) 2 mya (b) Before excavation (c) During excavation

FIGURE 8.4 South African Cave Taphonomy These cutaway figures show key aspects of the taphonomy of hominin remains in South African cave sites, 2 mya and today. Through the careful study of bone accumulations, the South African paleontologist Charles Kimberlin Brain realized that the early hominin bones as well as the bones of many other kinds of animals found in the caves were likely due to carnivore activity. (a) Carnivores such as leopards often take their prey into trees to feed. If such a tree hangs over an opening of a cave, the remains of the prey may fall into it when the animal has finished its meal. As the cave fills with bones and sediment, the remains become a part of the depositional process and are fossilized over time. (b) Paleontologists discover the strata with the fossils preserved from hundreds of thousands of years of deposition. One of the most famous hominin finds, the Taung child, was found in a South African cave (discussed further in chapter 10). (c) The excavation of Swartkrans Cave in South Africa has provided important hominin fossils. The grid over the evacuation is used to map fossils and artifacts. (Photo © 1985 David L. Brill, humanoriginsphotos.com)

Fossils: Memories of the Biological Past | 191

tissue. DNA within this tissue can be used to identify genetic information. Also, chemicals within original bone tissue or tooth tissue may be used for dietary reconstruction. Chemical constituents of bone, for example, have been extracted from early hominins from South Africa and Europe. Chemical analysis shows that early hominins ate a range of foods including meat and plants.

LIMITATIONS OF THE FOSSIL RECORD: REPRESENTATION IS IMPORTANT To form a complete picture of life in the past, we need fossils that represent the full range of living things from the past to the present. Representation, then, is the crucial factor in creating a fossil record. The fuller and more representative the collection of fossils from specific animals and plants in any site or region, the richer will be our understanding of the various populations of these animals and plants within that site or region.

Some fossil species are remarkably representative. Paleontologists have found hundreds of fossils from some 55 mya, for example, representing many different kinds of early primates and animals of the period (see chapter  9). By contrast, many taxa are known from very limited fossil records, such as for the earliest apes of Africa (from around 20 mya). Key stages in the record of past life are missing because (1) paleontologists have searched for fossils in only some places— they simply have not discovered all the fossil- bearing rocks around the world, (2) fos- sils have been preserved in some places and not in others, and (3) rock sequences containing fossils are not complete in all places.

(a) (b)

FIGURE 8.5 Ancient Footprints at Laetoli (a) Fossilized footprints of our human ancestors in Laetoli, Tanzania, provide information about (b) bipedal locomotion in early hominins. What information about locomotion can anthropologists learn from footprints? (Figure 8.5b: “The Fossil Footprint Makers of Laetoli,” © 1982 by Jay H. Matternes)

192 | CHAPTER 8 Fossils and Their Place in Time and Nature

The Fayum Depression, in Egypt, helps illustrate these limitations. There, pale- ontologists have examined an unusually rich record of early primate evolution from about 37 mya to 29 mya (primate evolution is the subject of chapter 9). Hundreds of early primate fossils have been found in the Fayum geologic strata. The record ends at about 29 mya, however, when the rock stops bearing fossils. Did primates stop living there at 29 mya? Probably not. Rather, the geologic activity necessary for fossilization— the depositing of sediments— probably stopped after 29 mya. Without deposition and the burial of organisms, no new fossils were created.

Elsewhere in Africa, geologic strata dating to the same time period as the Fayum are exceedingly rare, or they do not contain fossils. Primates might have lived in those areas, but sedimentation or fossilization or both simply did not occur.

Similarly, the record of early hominin evolution in Africa is mostly restricted to the eastern and southern portions of the continent. In all likelihood, early hominins inhabited all of Africa, certainly by 4 mya, but they were not preserved as fossils throughout the continent. (Early hominin evolution is the subject of chapter 10.)

When fossil records are especially well represented over time, they help us discuss aspects of evolutionary theory, such as the timing and tempo of change. These records can indicate whether evolution is the gradual process that Charles Darwin wrote about in his Origin of Species (see chapter 2) or if its pace can speed up or slow down.

Fully interpreting the information in fossils means knowing both where the fossils were found and their ages. Without being able to place fossils in time, anthropologists cannot trace the evolution of past life.

Just How Old Is the Past? TIME IN PERSPECTIVE Most of us have limited perspectives on time. We tend to think about yesterday, today, and tomorrow or perhaps next week. Long expanses of time might extend to our earliest memories. Because most of us were born after World War  II, that conflict seems like part of the distant past. “Ancient” history might mean the beginning of the American Revolution, in 1775, or Columbus’s arrival at the Americas, in 1492.

For scientists who deal with the distant past— such as geologists, paleontolo- gists, physical anthropologists, and archaeologists— recent centuries constitute a tiny portion of time. Indeed, when put in the context of Earth’s age (4.6  billion years) or the existence of life (at least 3.5  billion years), several centuries are not even an eyeblink in time. An appreciation of the history of life and (more imme- diately for this book) of primate and human evolution must be grounded in an understanding of the deep time involved. That is, to reconstruct and interpret evolutionary changes, it is crucial to place each fossil in time, answering the ques- tion How old is it? Without an answer to that question for each and every fossil, it is not possible to order the fossils in chronological sequence. Simply, without a chronological sequence, there is no fossil record.

Throughout Part II of this book, our normally narrow perspective on time broadens to include the vast record of natural history. The following discussion is a first step toward that broader sense of time.

Just How Old Is the Past? | 193

GEOLOGIC TIME: EARTH HISTORY The evolutionary history of life on Earth involves deep time, as represented by the geologic timescale (Figure 8.6). By placing all past life forms— as represented by fossils— on that scale, paleontologists record the major changes and events in the evolution of plants and of animals (Figure  8.7). Paleontologists order the

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FIGURE 8.6 Geologic Timescale Earth history is divided into eons, eras, periods, and epochs, all of which are assigned numerical ages. As this scale approaches modern time, the divisions become more detailed numerically. According to this scale, which eon, era, period, and epoch are we in?

194 | CHAPTER 8 Fossils and Their Place in Time and Nature

evolution of major life- forms, as geologists order Earth history, in a series of three eras— the Paleozoic, the Mesozoic, and the Cenozoic— each subdivided by a series of epochs. Collectively, these eras and their epochs cover the last 545 mil- lion years. During this long expanse, an incredible amount of change— biological and geologic— has occurred.

In the upcoming chapters, we will look at some of the biological evolution during this eon, especially in the Cenozoic era. Some of the most profound geologic changes have taken place within the Mesozoic and Cenozoic eras, or within the last 200 million years. At the beginning of this time frame, the supercontinent we call Pangaea— the original continent from which our continents derive— began a pro- cess of separation, still ongoing (Figure 8.8). By the time true primates appeared, 145 million years later, the Atlantic Ocean had formed, separating North America

eras Major divisions of geologic time that are divided into periods and further subdivided into epochs.

Paleozoic The first major era of geologic time, 570–230 mya, during which fish, reptiles, and insects first appeared.

Mesozoic The second major era of geo- logic time, 230–66 mya, characterized by the emergence and extinction of dinosaurs.

Hadean

Big bang

Archean

Proterozoic

Cam- brian Ordo-

vician

Silurian Devonian

Carbon- iferous

Permian

Triassic Jurassic

Creta- ceous

Paleo- cene

Eocene Oligocene

Miocene Pliocene

Pleistocene

Holo- cene

FIGURE 8.7 Evolution of Life Earth’s geologic timescale demonstrates the evolution of major organisms. As shown in this chart, modern humans are one of the most recent organisms to have developed; our roots go much deeper, however, as our ancestors appeared millions of years ago.

Just How Old Is the Past? | 195

from Europe and South America from Africa. The gaps between North America and Europe and between South America and Africa continue to widen as the con- tinental (tectonic) plates drift apart.

RELATIVE AND NUMERICAL AGE The events described above and the idea that Earth could be hundreds of millions of years old seemed preposterous to most scholars living even a few hundred years ago. Before the eighteenth century, not many people could fathom that time stretched more than several thousand years before the present, past what geologists call “historical” time, the time since written records began. In 1654, the archbishop of Armagh, Ireland, James Ussher (1581–1656), added up all the generations of reli- gious patriarchs listed in the Old Testament of the Bible and reported that Earth was created at midday on Sunday, October 23, 4004 BC. Ussher’s pronouncement became the definitive answer to the question raised by many— How old is planet Earth?

Other scholars turned to nonhistorical sources of information, determining that a geologic past began long before the historical past. Niels Stensen (also known by his Latinized name, Nicolaus Steno; 1638–1686), a Dane serving as the court physician to the grand duke of Tuscany, studied the geologic formations around

Cenozoic The era lasting from 66 mya until the present, encompassing the radiation and proliferation of mammals such as humans and other primates.

epochs Divisions of periods (which are the major divisions of eras) in geologic time.

Pangaea A hypothetical landmass in which all the continents were joined, approximately 300–200 mya.

tectonic Refers to various structures on Earth’s surface, such as the continental plates.

(a) 200 mya (b) Late Jurassic (about 150 mya)

(c) Late Cretaceous (about 70 mya) (d) Current position

PANGAEAPANGAEA

NORTH AMERICA NORTH AMERICA

AFRICAAFRICA

INDIAINDIA

AUSTRALIAAUSTRALIA

NORTH AMERICA NORTH AMERICA

AFRICAAFRICA

INDIAINDIA

TETHYS SEA

SOUTH AMERICA

ANTARCTICA

ASIA

SOUTH AMERICA

ANTARCTICA

ASIA

AUSTRALIA

NORTH AMERICA NORTH AMERICA

AFRICAAFRICA INDIAINDIA

SOUTH AMERICA

ANTARCTICA

ASIA

AUSTRALIA

FIGURE 8.8 Movement of Continents Earth’s continents have been moving for hundreds of millions of years and continue to drift. At the end of the Paleozoic (545–245 mya), all the land on Earth formed (a) a single mass, which we call Pangaea. Beginning in the Late Triassic (245–208 mya), this supercontinent began to break up into (b) separate continents. The initial split seems to have occurred in the northern part of Pangaea, creating the North Atlantic; the southern part, including South America, Africa, the Antarctic, and Australia, remained closed. At the end of the Cretaceous (145–66 mya) (c), most of the continents were separate and the Atlantic Ocean was complete; however, the continents had yet to reach their (d) present- day positions.

196 | CHAPTER 8 Fossils and Their Place in Time and Nature

Florence, Italy, and the fossils they contained. Hypothesizing that the fossilized shark teeth that he found far under the ground were prehistoric, Stensen concluded that in a series of geologic layers— the stratigraphic sequence— higher rocks are younger than lower rocks.

Steno’s law of superposition laid the foundation for relative dating, which states the relative age of one event (such as the formation of a geologic stratum) or object (such as a fossil or an artifact) with respect to another (Figure 8.9). That is, the event recorded or object found on the bottom is the oldest, that above next oldest, and so forth. By contrast, the numerical age of an event or object is expressed in absolute years, such as 2,000 years ago, 1.3  billion years, 4004 BC, or AD 2014. Developed long before numerical aging, relative aging can be accom- plished through several methods.

RELATIVE METHODS OF DATING: WHICH IS OLDER, YOUNGER, THE SAME AGE? STRATIGRAPHIC CORRELATION Geologic correlation of strata from multiple locations— matching up strata based on physical features, chemical compositions, fossils, or other properties— in a region helps place the passage of time in a large context. This highly sophisticated method, first developed by William Smith, involves matching up physical and chemical characteristics of strata with the fossils found in those strata. Chemical characteristics make stratigraphic correlation possible across vast regions. For example, any volcanic eruption produces ash with an individual and highly specific chemical signature. The eruption’s force, together with powerful winds, can spread the ash over hundreds or even thousands of kilo- meters, as when Krakatoa, an island volcano in Indonesia that erupted in 1883, sent ash as far as 3,700 miles (6,000 km) away. When an ash layer exists above or below a fossil, that fossil can be judged younger or older than the ash, depending on their relative positions. Such correlations, from various lines of evidence, involving millions of places around the world, have resulted in the geologic timescale.

CHEMICAL DATING Soils around the world have specific chemical compositions, reflecting their local geologic histories. For example, some soils contain fluorine. Once a bone is buried in fluorine- bearing soil, the bone begins to absorb the ele- ment. A bone that has been buried for a long time will have more fluorine in it than will a bone that has been buried for a short time.

Fluorine dating, one of the first chemical dating methods, was proposed by the English chemist James Middleton in 1844 (Figure  8.10). The Croatian

Steno’s law of superposition The principle that the lower the stratum or layer, the older its age; the oldest layers are at the bottom, and the youngest are at the top.

stratigraphic correlation The process of matching up strata from several sites through the analysis of chemical, physi- cal, and other properties.

fluorine dating A relative (chemical) dating method that compares the accumulation of fluorine in animal and human bones from the same site.

chemical dating Dating methods that use predictable chemical changes that occur over time.

FIGURE 8.9 Steno’s Law of Superposition (a) This law, formulated by (b) Niels Stensen, states that the youngest strata are at the top and the oldest strata are on the bottom. In which situations would this law not apply?

(b)

TIME

This layer deposited first, parallel to the earth’s surface.

This layer deposited later, on top of the previous layer.

This layer deposited even later.

This layer must be younger than others because it cuts across.

(a)

Just How Old Is the Past? | 197

paleontologist Dragutin Gorjanović-Kramberger applied fluorine dating to human and animal remains found in Krapina, Croatia, in the late 1890s and early 1900s (Figure  8.11). Hypothesizing that the bones buried in strata at the site had absorbed fluorine, he wanted to determine if the human bones, all representing humans called Neandertals (see chapter 10), were the same age as the animal bones. The animal bones were from long- extinct, Pleistocene forms of rhinoceroses, cave bears, and cattle. Some scientists believed that the Krapina Neandertals were not ancient, however, but had been living at the site in recent times only. They con- sidered the Neandertals simply different from people living in Croatia in the late nineteenth and early twentieth centuries. If Gorjanović-Kramberger could show that the two sets of bones— human and animal— contained the same amount of fluorine, he could prove that the Neandertals were ancient and in fact had lived at the same time as the extinct animals. When the simple chemical analysis revealed that the Neandertal bones and the animal bones had very similar amounts of flu- orine, this pioneering study had shown human beings’ deep roots.

BIOSTRATIGRAPHIC (FAUNAL) DATING Gorjanović-Kramberger recognized that different strata include different kinds of fossils. He regarded these findings

Present-day surface

Strata Amount of fluorine

A

B

C

D

E

F

.001

.003

.015

.062

.32

.64

.001

.003

.015

.062

.32

.64

Fluorine dating reveals the relative ages of fossil bones at the same site. It does not provide absolute dates, and it cannot be used to compare fossils from different sites because fluorine levels in soil vary from place to place.

G

H

I

J

Recently deposited bones will have had little time to absorb fluorine.

Fossils that have been in the soil longer will have absorbed greater quantities of fluorine. The amount of fluorine in them will be much greater than in the bones near the top.

FIGURE 8.10 Fluorine Dating Bones absorb fluorine from surrounding soil.

FIGURE 8.11 Dragutin Gorjanović- Kramberger The Croatian paleontologist used fluorine dating at a site in Krapina, Croatia. The significance of this dating method was demonstrated by his results, which suggested that extinct animals and Neandertals had coexisted.

198 | CHAPTER 8 Fossils and Their Place in Time and Nature

as chronologically significant. That is, the forms of specific animals and plants change over time, so the forms discovered within individual layers can help deter- mine relative ages. Biostratigraphic dating draws on the first appearance of an organism in the fossil record, that organism’s evolutionary development over time, and the organism’s extinction. Pliocene and Pleistocene African rodents, pigs, and elephants and Eurasian mammals of all kinds have been especially useful for biostratigraphic dating because they show significant evolutionary change. By determining when certain animals lived, scientists have developed biostratigraphic markers, or index fossils, for assessing age. For example, giant deer— sometimes called Irish elk— provide useful information based on their extinction. That is, because the species appears to have died out in northern Europe around 10,600 yBP, the presence of Irish elk fossils in a northern European site indicates that the site predates 10,600 yBP.

Mammoths— relatives of modern elephants— first lived and evolved in Africa, then spread to Europe, Asia, and North America around 2.5 mya. Mammoths went extinct in Africa but continued to evolve elsewhere. After 2.5 mya, their molars became increasingly complex. Paleontologists have determined how these teeth changed from the species’ emergence to its complete extinction. Therefore, when paleontologists discover fossilized mammoth teeth, they can determine the relative age of the site simply by looking at the molars. Likewise, changes in molar shape and size have helped paleontologists develop relative ages for Pliocene– Pleistocene pigs in East Africa and South Africa (Figure 8.12).

CULTURAL DATING Material culture can provide information for cultural dat- ing. The first evidence of material culture— primitive stone tools called pebble tools— dates to about 2.6 mya. Although individually distinctive in appearance, pebble tools are not especially useful for bracketing small amounts of time, mainly because their forms changed so slowly. For example, a pebble tool from 2.5 mya is very much like one produced 1.8 mya. However, the presence of a certain kind of tool enables paleontologists to say that the site (and its hominin occupants) dates to a certain age (Figure 8.13).

Beginning in the later Pleistocene, stone tools and other components of material culture changed more rapidly. The various regional cultures in Europe collectively known as the Upper Paleolithic provide a number of “ time- specific” artifacts, such as the small sculptures known as Lion Men. The first of these artifacts was found in a cave in Germany in 1939, neglected for 30 years in part because of World War II, and only recently restored (Figure 8.14).

In the Holocene, artifacts such as ceramics became even more time- specific. In fact, ceramics were invented during this period, and their forms changed rapidly.

ABSOLUTE METHODS OF DATING: WHAT IS THE NUMERICAL AGE? THE RADIOMETRIC REVOLUTION AND THE DATING CLOCK When we say that the American Civil War took place after the American Revolution, we have provided relative ages for the two wars. That is, we have related the ages without specifying them. When we say that the American Civil War began in 1861 and the American Revolution began in 1775, we have provided numerical ages. That is, we have pinpointed the wars’ beginnings in terms of years, a measure of scaled time. We know these dates thanks to written records, individuals having recorded all

index fossils Fossils that are from spec- ified time ranges, are found in multiple locations, and can be used to determine the age of associated strata.

biostratigraphic dating A relative dating method that uses the associations of fossils in strata to determine each layer’s approximate age.

cultural dating Relative dating methods that are based on material remains’ time spans.

pebble tools The earliest stone tools, in which simple flakes were knocked off to produce an edge used for cutting and scraping.

The oldest pig molars are relatively thin and short.

Over time, the molars increased in height and length.

The youngest molars are the tallest and longest.

FIGURE 8.12 Fossil Pig Molars Changes in the size and shape of these teeth can be used for biostratigraphic dating, in a method developed by the American paleontologists Jack Harris and Tim White. Over time, the molars became taller and longer.

In addition, fossil pig molars found in conjunction with layers of volcanic ash may be used for absolute dating, if paleontologists can determine the age of the ash. (On techniques for doing this, see “The Revolution Continues: Radiopotassium Dating.”) Because the teeth and the volcanic layer are associated chronologically, the teeth can then be used as time markers when found at other sites. (“Pig Dating: Stratigraphic Correlations,” © 1985 by Jay H. Matternes)

Just How Old Is the Past? | 199

sorts of events associated with both wars (Figure 8.15). Since the time that Niels Stensen and his contemporaries began studying geologic features and fossils, sci- entists have been recording relative ages. By doing so, they have established the sequence of events in the geologic timescale— proving that the Eocene came before the Miocene, for example, and that ceramics were invented long after Neandertals lived in Europe. However, unlike historians, who often work with records con- taining dates, premodern geologists, paleontologists, and anthropologists had no means of providing numerical dates. Geologists could only group geologic events,

as chronologically significant. That is, the forms of specific animals and plants change over time, so the forms discovered within individual layers can help deter- mine relative ages. Biostratigraphic dating draws on the first appearance of an organism in the fossil record, that organism’s evolutionary development over time, and the organism’s extinction. Pliocene and Pleistocene African rodents, pigs, and elephants and Eurasian mammals of all kinds have been especially useful for biostratigraphic dating because they show significant evolutionary change. By determining when certain animals lived, scientists have developed biostratigraphic markers, or index fossils, for assessing age. For example, giant deer— sometimes called Irish elk— provide useful information based on their extinction. That is, because the species appears to have died out in northern Europe around 10,600 yBP, the presence of Irish elk fossils in a northern European site indicates that the site predates 10,600 yBP.

Mammoths— relatives of modern elephants— first lived and evolved in Africa, then spread to Europe, Asia, and North America around 2.5 mya. Mammoths went extinct in Africa but continued to evolve elsewhere. After 2.5 mya, their molars became increasingly complex. Paleontologists have determined how these teeth changed from the species’ emergence to its complete extinction. Therefore, when paleontologists discover fossilized mammoth teeth, they can determine the relative age of the site simply by looking at the molars. Likewise, changes in molar shape and size have helped paleontologists develop relative ages for Pliocene– Pleistocene pigs in East Africa and South Africa (Figure 8.12).

CULTURAL DATING Material culture can provide information for cultural dat- ing. The first evidence of material culture— primitive stone tools called pebble tools— dates to about 2.6 mya. Although individually distinctive in appearance, pebble tools are not especially useful for bracketing small amounts of time, mainly because their forms changed so slowly. For example, a pebble tool from 2.5 mya is very much like one produced 1.8 mya. However, the presence of a certain kind of tool enables paleontologists to say that the site (and its hominin occupants) dates to a certain age (Figure 8.13).

Beginning in the later Pleistocene, stone tools and other components of material culture changed more rapidly. The various regional cultures in Europe collectively known as the Upper Paleolithic provide a number of “ time- specific” artifacts, such as the small sculptures known as Lion Men. The first of these artifacts was found in a cave in Germany in 1939, neglected for 30 years in part because of World War II, and only recently restored (Figure 8.14).

In the Holocene, artifacts such as ceramics became even more time- specific. In fact, ceramics were invented during this period, and their forms changed rapidly.

ABSOLUTE METHODS OF DATING: WHAT IS THE NUMERICAL AGE? THE RADIOMETRIC REVOLUTION AND THE DATING CLOCK When we say that the American Civil War took place after the American Revolution, we have provided relative ages for the two wars. That is, we have related the ages without specifying them. When we say that the American Civil War began in 1861 and the American Revolution began in 1775, we have provided numerical ages. That is, we have pinpointed the wars’ beginnings in terms of years, a measure of scaled time. We know these dates thanks to written records, individuals having recorded all

index fossils Fossils that are from spec- ified time ranges, are found in multiple locations, and can be used to determine the age of associated strata.

biostratigraphic dating A relative dating method that uses the associations of fossils in strata to determine each layer’s approximate age.

cultural dating Relative dating methods that are based on material remains’ time spans.

pebble tools The earliest stone tools, in which simple flakes were knocked off to produce an edge used for cutting and scraping.

The oldest pig molars are relatively thin and short.

Over time, the molars increased in height and length.

The youngest molars are the tallest and longest.

FIGURE 8.12 Fossil Pig Molars Changes in the size and shape of these teeth can be used for biostratigraphic dating, in a method developed by the American paleontologists Jack Harris and Tim White. Over time, the molars became taller and longer.

In addition, fossil pig molars found in conjunction with layers of volcanic ash may be used for absolute dating, if paleontologists can determine the age of the ash. (On techniques for doing this, see “The Revolution Continues: Radiopotassium Dating.”) Because the teeth and the volcanic layer are associated chronologically, the teeth can then be used as time markers when found at other sites. (“Pig Dating: Stratigraphic Correlations,” © 1985 by Jay H. Matternes)

200 | CHAPTER 8 Fossils and Their Place in Time and Nature

FIGURE 8.13 Cultural Artifacts Among the remains of material culture that can be used to determine the time periods of archaeological sites are (a) an Oldowan chopper, (b) an Oldowan flake tool, (c) an Acheulean hand axe (France), (d) a hand axe from Ologosailie (Kenya), (e) a hand axe from Galeria (Spain), (f) a Mousterian Levallois flake tool, (g) Mousterian tools, (h) a Solutrean tool, (i) an Upper Paleolithic point, (j) a Neolithic flake tool, (k) a Neolithic axe head, (l) Neolithic scrapers, (m) a Mayan pot, (n) post- Neolithic Clovis points, (o) a post- Neolithic spade, (p) an American Indian stone maul, (q) an Inuit fishing spear, (r) a Ford Model T, and (s) an Apple iPod.

(i) (j)

(k)

(e) (f)

(g)

(h)

(a) (b)

(c)

(d)

(m)

(n) (o)

(p)

(q)

(r)

(s)

(l)

Just How Old Is the Past? | 201

paleontologists could only group species’ lives, and anthropologists could only group peoples’ lives and cultural events.

In the 1920s, the American astronomer  A.  E.  Douglass (1867–1962) devel- oped the first method for numerically dating objects and events, specifically ones including or involving wood. In studying sunspots and their impact on climate, Douglass noted that in temperate and very cold regions tree growth stopped in the winter and reactivated in the spring. This intermittence resulted in layers of growth, visible as a concentric ring pattern in the cross section of a tree. Douglass’s dendrochronology, or tree- ring method of dating, involved counting the number of rings, each of which represented one year of growth (Figure  8.16). Tree- ring dating was first used on tree sections found in archaeological sites in the Ameri- can Southwest. It works only when wood is as excellently preserved as it is in the Southwest, however, and thus can be applied in only a limited number of areas in the world.

Widely applicable numerical dating became possible in the nuclear age, fol- lowing World War  II (1939–45). In 1949, the American chemist Willard Libby (1908–1980) discovered radiocarbon dating, an accomplishment for which he won a Nobel Prize. Scientists now had a means of determining the numerical age of past life- forms via the decay of radioactive elements.

The radiocarbon method, sometimes called the carbon- 14 method, involves dat- ing carbon isotopes. Isotopes are variants of an element based on the number of neutrons in the atom’s nucleus. Some isotopes of an element are stable— in theory, they will last for an infinite amount of time, at least with respect to maintain- ing the same number of neutrons. Some isotopes are unstable— over time, they decay radioactively, transforming themselves to stable isotopes of either the same

Relative age Numerical age

Iraq War

Afghanistan War

Gulf War (Persian Gulf)

Falkland War (Argentina-England)

Six-day War (Arab-Israeli)

Vietnam War

Bay of Pigs Invasion (Cuba–United States)

Korean War

World War II

Spanish Civil War

World War I

Russian Revolution

Russo-Japanese War

Boer War (South Africa)

Iraq War Afghanistan War

Gulf War (Persian Gulf)

Falkland War (Argentina-England)

Vietnam War Six-day War (Arab-Israeli)

Bay of Pigs Invasion (Cuba–United States)

Korean War

World War II

Spanish Civil War

World War I

Russian Revolution Russo-Japanese War

Boer War

2000

1980

1960

1940

1920

1900

FIGURE 8.15 Relative vs. Numerical Wars of the twentieth and twenty- first centuries can be ordered relatively or numerically. The relative chart simply shows the order of events and does not specify when these events occurred or how long they lasted. The numerical chart provides dates and gives at least a rough sense of the wars’ starting points and durations.

FIGURE 8.14 Lion Man The discovery of another sculpture like this one, made of mammoth ivory and about 30 cm (11.8 in) high, would provide a relative date for the archaeological site. The site is at least 30,000 years old.

dendrochronology A chronometric dating method that uses a tree- ring count to determine numerical age.

radiocarbon dating The radiometric dating method in which the ratio of 14C to 12C is measured to provide an absolute date for a material younger than 50,000 years.

isotopes Two or more forms of a chemical element that have the same number of protons but vary in the number of neutrons.

202 | CHAPTER 8 Fossils and Their Place in Time and Nature

FIGURE 8.16 Dendrochronology (a) Wood from archaeological structures reveals tree- ring patterns (b) that can be used to date relatively recent archaeological sites.

Archaeological structure Dead snag Living tree

A

B

C

J

I

H

G

F

E

D

C

B

A

The thickness and spacing of tree rings create patterns. When ring patterns from older and younger samples of the same type of wood are matched up, a chronology can be extended back in time. The matching ring patterns are known as marker rings.

Different lengths of the same type of wood will necessarily reveal different ring patterns. The older part of wood segment C shows ring patterns that are older than wood segments A and B. These additional rings in C match up with other older segments of wood, such as D and E, and so forth.

(b)

(a)

Just How Old Is the Past? | 203

element or another element. Carbon has one radioisotope (unstable or radioactive isotope), identified as 14C because it has an atomic mass of 14 (six protons and eight neutrons) in its nucleus. Carbon has two non- radioisotopes (stable isotopes), 12C ( carbon- 12) and 13C ( carbon- 13), which have an atomic mass of 12 (six protons and six neutrons) and 13 (six protons and seven neutrons), respectively. The radiocar- bon method focuses on what happens to the radioisotope, 14C. Over 5,730 years, half of the 14C decays into 14N. Over the next 5,730 years, another half of the 14C decays again into 14N, and so on, until eventually most of the radioisotope will have decayed. The number representing the time it takes for half of the radioisotope to decay is called the half- life (Table 8.1).

All living plants and animals (including you) absorb about the same amount of 14C in their tissues, through the ingestion of very small amounts of atmospheric carbon dioxide (CO2). During the life of a plant or animal, the ratio of 14C to 12C remains relatively constant. Once the organism dies, it stops absorbing 14C and the 14C begins to decay, but the 12C does not decay. This means that the ratio of 14C to 12C changes over time; the longer since the death of the plant or animal, the greater the ratio (Figure 8.17).

The great advantage of the radiocarbon method is that it has a precise baseline for the start of the clock— the death of the organism. The disadvantage for dating major events in primate and human evolution is that 14C has a fairly short half- life, rendering its dates most accurate for only the last 50,000 yBP. Dates can be determined for another 25,000 years or so beyond that, but they are less precise owing to the very small amount of 14C left.

THE REVOLUTION CONTINUES: RADIOPOTASSIUM DATING All organic materials contain carbon and thus can be dated through the radiocarbon method. By contrast, nonorganic materials such as rocks contain other elements that can be dated radiometrically. Because the radioisotopes of these elements have very long half- lives, the radiometric clock is considerably longer for these nonorganic materials than for carbon- based materials. Igneous (volcanic) rock, for example, contains the radioisotope 40K ( potassium- 40). 40K decays very slowly from its unstable form to a stable gas, 40Ar ( argon- 40)—its half- life is 1.3 billion years. It is usually not possible to date rocks much younger than 200,000 yBP, but 40K’s long half- life presents no limitation on the other end of the range. Radiopotassium dating certainly accommodates all of primate evolution.

The great strength of this method is the presence of volcanic rock in many places throughout the world. During a volcanic eruption, the heat is so extreme

half- life The time it takes for half of the radioisotopes in a substance to decay; used in various radiometric dating methods.

TABLE 8.1 Isotopes Used in Radiometric Dating

Parent → Daughter Half- Life (Years) Material in Which the Isotopes Occur

14C → 14N 5,730 Anything organic (has carbon), such as wood, shell, bone

238U → 206Pb 4.5 billion Uranium- bearing minerals (zircon, uraninite)

40K → 40Ar 1.3 billion Potassium- bearing minerals (mica, feldspar, hornblende)

40Ar → 39Ar 1.3 billion Potassium- bearing minerals (mica, feldspar, hornblende)

235U → 207Pb 713 million Uranium- bearing minerals (zircon, uraninite)

igneous Rock formed from the crystalli- zation of molten magma, which contains the radioisotope 40K; used in potassium- argon dating.

radiopotassium dating The radiometric dating method in which the ratio of 40K to 40Ar is measured to provide an absolute date for a material older than 200,000 years.

204 | CHAPTER 8 Fossils and Their Place in Time and Nature

that it drives off all argon gas in the rock. The 40K solid that is in the rock sealed by lava then begins to decay to 40Ar gas, and the gas accumulates, trapped within the rock’s crystalline structure. To date that rock— which could then be millions of years old— a scientist measures, with sophisticated instruments, the amount of gas (40Ar) relative to the amount of nongas (40K) in the rock. The more gas there is, the older the rock.

The radiopotassium method was first used to date the volcanic rock associ- ated with an early hominin skull found by the British archaeologist Mary Leakey (1913–1996) in the lowest strata of Olduvai Gorge, in Tanzania, in 1959. At that time, scientists assumed that hominins had been around for perhaps a half- million years but not longer. When the associated volcanic rock at Olduvai proved to be 1.8  million years old, that dating nearly quadrupled the known time frame for human evolution. Since then, radiometric methods have helped paleontologists fine- tune the chronologies of primate evolution and human evolution.

In the 1990s, scientists developed an alternative method of radiopotassium dating, whereby they measure the ratio of 40Ar gas to 39Ar gas. In the argon– argon method, volcanic rock is bombarded with “fast” neutrons in a nuclear reactor. Like 40K, 39K is present in the volcanic rock; and the two isotopes, 40K and 39K,

14C is oxidized and forms carbon dioxide.

14CO2 is used by plants in photosynthesis. 14C is incorporated in plant tissues.

Most 14C is absorbed by the oceans.

Animals consume plants, and the plant 14C is incorporated in animal bone and other tissues through metabolic processes.

14C is produced in the atmosphere.

When animals die, their metabolism ceases, and their tissues stop incorporating 14C. 14C begins decaying to 14N. The proportion of 14C begins to decrease.

FIGURE 8.17 Radiocarbon Dating This dating method was the first generation of radioisotope methods. Such dating methods remain among the most important for the determination of numerical dates.

Just How Old Is the Past? | 205

occur in the same amounts relative to one another, no matter how old the rock may be. The neutron bombardment converts the 39K to 39Ar. Because 39Ar serves as a proxy for 40K, the ratio of 40Ar to 39Ar reveals the rock’s absolute age. This method’s advantages over the potassium– argon method are that it requires less rock and the potassium does not have to be measured. Now routinely being used by paleontologists and geologists to date early hominins (see chapter 10), the method has made it possible to date hundreds of hominin (and other) fossils from between 5 million yBP to Homo sapiens’ origin, more than 100,000 yBP. Note, though, that radiopotassium can be used to date only igneous rock, not sedimentary rock.

Fission track dating is based on the radioactive decay of naturally occurring 238U ( uranium- 238; Figure 8.18). When the isotope decays, fragments produced in the decay, or fission, process leave a line, or track, measuring just a few atoms wide on the rock crystal. Thus, the greater the number of tracks, the older the material being dated. This method can date materials from the last several million years and has been used for dating volcanic ash and obsidian (volcanic glass).

NON- RADIOMETRIC ABSOLUTE DATING METHODS Several other, non- radiometric methods provide absolute dates. Among these methods, amino acid dating is the most useful in more recent settings (Figure  8.19). This method is based on the decay of protein molecules following an organism’s death. Amino acids, the compounds that make up proteins (among the subjects of chapter  3), come in two forms, l- isomers and d- isomers, respectively known as left- handed amino acids and right- handed amino acids. Basically, this distinction means that when a protein is viewed under high- power magnification with a specialized light called polarized light, the molecules bend light to the left (and are called l- isomers) or to the right ( d- isomers). Most living organisms’ tissues are com- prised of l- isomers. Once an organism dies, these l- isomers begin to transform to d- isomers. The longer the organism has been dead, the greater the number of ds, so the fossil’s date is based on the ratio of l to d.

fission track dating An absolute dating method based on the measurement of the number of tracks left by the decay of uranium- 238.

Time

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FIGURE 8.19 Amino Acid Dating Amino acid dating is based on changes in the form of amino acid molecules (from l to d) over time.

amino acid dating An absolute dating method for organic remains such as bone or shell, in which the amount of change in the amino acid structure is measured.

polarized light A kind of light used in amino acid dating because it allows amino acid changes to be observed and measured.

FIGURE 8.18 Fission Track Dating Fission track dating employs the number of tracks left behind by isotope decay.

206 | CHAPTER 8 Fossils and Their Place in Time and Nature

The limitation of amino acid dating is that the rate of the chemical decompo- sition resulting in the shift from l to d— a process called racemization— is largely determined by the temperature of the region. That is, a region with a higher average temperature will have a faster rate of chemical decomposition than will a region with a cooler average temperature. The age range for amino acid dating is generally 40,000–100,000 yBP but has been extended to 200,000 yBP in tropical settings and to 1 mya in cooler settings. The method has provided useful dates for a variety of sites, but it is best known in human evolutionary studies for dating Border Cave, in South Africa (70,000–145,000 yBP).

racemization The chemical reaction resulting in the conversion of l amino acids to d amino acids for amino acid dating.

NMya Era Period Epoch Polarity

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The alternating layers in this schematic of a section of rock represent changes in polarity over time.

Earth’s magnetic field today

The black and white bars (N = normal, R = reversal) represent polarity changes, each of which is assigned beginning and ending dates. This chart shows the polarity changes over the past 25 mya.

0 Holocene

FIGURE 8.20 Paleomagnetic Dating Paleomagnetic dating derives from changes in Earth’s polarity.

Just How Old Is the Past? | 207

Paleomagnetic dating is based on changes in Earth’s magnetic field, which change the planet’s polarity. In essence, movement of the planet’s liquid (iron alloy) outer core creates an electric current that results in the magnetic field (Fig- ure  8.20). When the magnetic field shifts, the magnetic north and south poles shift. The poles’ shifts have been well documented. In the last 6 million years, for example, there have been four “epochs” of polar changes, or four different well- dated periods. Because certain metal grains align themselves with Earth’s magnetic field as they settle and help form sedimentary rock, geologists can examine the orientation of these fragments to determine the planet’s polarity at the time of the rock’s formation. In addition, when molten igneous rock is produced, each new layer records the polarity, which can later be determined from the hard igneous rock.

Electron spin resonance dating relies on the measurement of radioisotope concentrations (e.g., of uranium) that have accumulated in fossils over periods of time. Once buried, remains such as bones and teeth absorb radioisotopes and so record the radioactivity in the surrounding burial environment. The older the fossil, the greater the concentration; and this method can date material from a few thousand to more than a million years old.

Thermoluminescence dating is based on the amount of the sun’s energy trapped in material such as sediment, stone, or ceramic (Figure 8.21). When such an object is heated— as in an early hominin’s campfire— the energy it contains is released as light. The next time that same material is heated— as in the laboratory to derive a date— the amount of light released (measured as electrons that are from natural radiation, such as from uranium) reveals the amount of time since the mate- rial was first heated. This method can date materials back to about 800,000 yBP.

Scientists must consider various factors when choosing an absolute dating method, among them the material involved and the time range in which the fossilized organism likely lived. Some methods date the fossil, some date the context of the fossil, and others date either the fossil or the context. Radiocarbon, for example, can be used to date either the remains of the once- living organism or an associated organic substance, such as wood. To determine the age of a human skeleton, the bones can be dated directly. If, however, it can be proved that the deceased was buried at the same time a fire was lit nearby, the fire pit can be dated.

GENETIC DATING: THE MOLECULAR CLOCK The DNA in living organisms is an important source of information for retro- spectively dating key events in their species’ evolution, including divergence from closely related species and phylogenetic relationships with other organisms. In light of the well- founded assumption that a species accumulates genetic differences in general and mutations in particular over time at a more or less constant rate, it should be possible to develop a chronology showing the amount of time since two species diverged in their evolution. Simply, more closely related species should have more similar DNA than less closely related species have. The American geneticist Morris Goodman and others developed the molecular clock for dating the divergences of the major primate taxa in the 1960s. This record indicates that Old World monkeys first diverged from all other primates at about 25 mya; gibbons diverged at about 18 mya, orangutans at about 14 mya, gorillas at about 7 mya; and the split occurred between chimpanzees and hominins about 4–7 mya

paleomagnetic dating An absolute dating method based on the reversals of Earth’s magnetic field.

electron spin resonance dating An absolute dating method that uses microwave spectroscopy to measure electrons’ spins in various materials.

thermoluminescence dating A dating method in which the energy trapped in a material is measured when the object is heated.

(c)

FIGURE 8.21 Thermoluminescence Dating Thermoluminescence dating is related to the amount of light released when an object with stored energy is heated.

208 | CHAPTER 8 Fossils and Their Place in Time and Nature

(Figure  8.22). Molecular anthropologists and paleoanthropologists studying the respective genetic and fossil records find a general consistency in the dates for the origins of the major primate groups. As geneticists and anthropologists learn more about the primate genome, this method of retrospective dating is becoming increasingly refined. For example, studies of the human genome are revealing the

How Old Is It?

Fossils are the primary source of information for documenting the evolution of past life. Paleontologists have developed various means for determining a fossil’s age.

Method Basis Material Date Range

Relative Age

Law of superposition Older is lower Just about anything Just about any time

Stratigraphic correlation Like strata from different regions are related to the same event

Rocks and fossils Just about any time

Biostratigraphic (faunal) dating Evolution of animals Bones and teeth Just about any time

Chemical dating Fossils absorb chemicals, such as fluorine, in soil

Bones Less than 100,000 yBP

Cultural dating Artifacts are time- specific Technology generally Up to about 2.5 mya

Numerical Age

Dendrochronology Tree growth Specific tree types Less than 12,000 yBP

Radiocarbon dating Carbon- 14 Anything organic 50,000 yBP– AD 1950

Radiopotassium dating Potassium- 40 Volcanic rocks More than 200,000 yBP

Amino acid dating Racemization Bones, shells Less than 3 mya

Fission track dating Fission tracks on rock crystal Volcanic rock Up to 3 mya

Paleomagnetic dating Shifts in Earth’s magnetic field Sedimentary and igneous rocks

Up to 5 mya

Electron spin resonance dating Concentrations of radioisotopes Bones, teeth Several thousand to more than 1 mya

Thermoluminescence dating Trapped energy Sediment, stone, ceramics Up to 800,000 yBP

C O N C E P T C H E C K !

Reconstruction of Ancient Environments and Landscapes | 209

rate of the appearance of mutations in newborn infants. These findings suggest a slower mutation rate than previously thought, making the split between chim- panzees and the first hominins 8–10 mya. This revision of the molecular clock is also more consistent with the dates for the earliest hominins, which exceed the divergence dates provided by Goodman many years ago (see chapter 10).

In summary: anthropologists and other scientists who deal with deep time have various methods and research tools for answering questions about when past organisms were alive. Some of these methods and tools directly date fossils, and others date the fossils’ geological contexts. Relative and absolute dating have brought about a far greater understanding of the evolutionary record than was imagined when fossils were first being discovered centuries ago. Placing fossils in order creates a detailed picture of the past, of the evolutionary sequence of events for specific organisms and for groups of organisms.

In addition to determining the ages of fossils, anthropologists seek to under- stand what the habitats were like in which past plants and past animals lived. This is a new area in the study of the past, and it is becoming increasingly clear that understanding environmental contexts— reconstructing past environments to shed light on the circumstances driving evolutionary change, such as major climate change— is crucial to understanding evolution in general and local adaptations in particular. In the next section, we will explore ways in which anthropologists reconstruct environments and landscapes.

Reconstruction of Ancient Environments and Landscapes For much of the history of paleontology, the focus has been on evolutionary relationships (phylogeny). In studying the origins and morphological evolution of the various life- forms, paleontologists have asked questions such as Which (now fossilized) species gave rise to primates? To the first apes? To the first hominins? To the first modern humans? Phylogenetic questions remain central to the study of evolution, but the evolution of past organisms is not truly meaningful unless it is correlated with the circumstances under which the organisms lived and the processes that underlay their evolutionary changes. Scientists need to ask additional questions— for example, Which conditions drove natural selection and other processes that account

Million years ago

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9 FIGURE 8.22 Genetic Dating: Divergence of Higher Primates Modern primates diverged from a common ancestor millions of years ago. A “molecular clock” helps determine the time since the divergence of monkey and ape species. This system assumes that species accumulate genetic differences over time at a regular rate.

210 | CHAPTER 8 Fossils and Their Place in Time and Nature

for the appearance, evolution, radiation, and extinction of past primates and humans? This question pertains especially to the ecology of the setting the primates lived in— their habitat. Using models derived from the study of living animals, paleontol- ogists can look at the bones of extinct animals and determine how they functioned during life and in what kinds of habitats they functioned. For example, as discussed in chapter 6, the long arms and short legs of apes are now well understood to be part of the species’ adaptation to life in the trees— the apes are skilled at suspensory forms of locomotion. Therefore, when paleontologists find fossil apes with long arms, such as the Miocene ape Oreopithecus, they can infer that these primates lived in a habitat where trees were the dominant form of vegetation (Figure 8.23).

THE DRIVING FORCE IN SHAPING ENVIRONMENT: TEMPERATURE Temperature is perhaps the single most important feature of climate. Therefore, if scientists can reconstruct the temperature for a particular geologic stratum, they come very close to characterizing a past climate. Scientists cannot measure temperature in the past, but they can identify and study the impacts of different temperatures on biology and geologic chemistry. Hot climates leave very different biological and chemical signals than do cold climates.

Because of this close linkage of temperature with biology and chemistry, paleo- climatologists have reconstructed temperature changes for much of the Cenozoic (and before). Some of the best information on climate history— and especially temperature— is based on the study of foraminifera and other ocean- dwelling microorganisms (Figure  8.24). These microorganisms’ tiny shells are preserved in sediments on the ocean floor worldwide, and their chemical compositions tell important stories about temperature change over time. While the microorganisms are alive, they ingest two of the three stable isotopes of oxygen, 18O and 16O, from the ocean water. Atmospheric temperature directly affects the water’s tempera- ture, which in turn affects the amount of 18O in the water. When temperature declines, the amount of 18O in the water, and therefore in the microorganism, increases. When temperature increases, the amount of 18O decreases. Geologists have taken core samples of sediments from the ocean floor and have tracked the 18O content in the microorganisms within those sediments, producing a record of global temperature change (Figure 8.25).

Based on the isotope signatures of ancient sediments, we know that tempera- tures were high in the Paleocene, preceding the appearance of true primates, and that they peaked in the early Eocene. This warm period was followed by a gradual decline in temperature throughout the Eocene. At the boundary between the Eocene and Oligocene, about 34 mya, temperature sharply declined, then rose, then sharply declined again. Moderate ups and downs followed in the Oligocene and into the Middle Miocene. After a sharp decline about 17–15 mya, temperature leveled off for the remainder of the Miocene. Climate was drier and more seasonal about 10–5 mya, coinciding with the appearance of early hominins.

One of the most profound temperature changes, and thus dramatic alterations of climate and habitat, began at the end of the Miocene, around 6 mya (Fig- ure 8.26). Sea levels are at their highest during warm periods; during cold periods, more water is tied up in ice and glaciers than during warm periods. This cold period likely added a permanent ice sheet on the continent of Antarctica; so much water was tied up in glacial ice that the Mediterranean Sea was nearly dry. During the Pleistocene (2.6 mya– 15,000 yBP), periods of massive glaciation, or glacials, were

foraminifera Marine protozoans that have variably shaped shells with small holes.

(a)

FIGURE 8.23 Life in the Trees (a) The skeleton and body reconstruction of Oreopithecus show that the ape’s long arms were adapted to a suspensory form of locomotion. (b) Gibbons have a similar body style, adapted to life in the trees. What differences in skeletal anatomy would you expect in a primate that lived primarily on open grassland?

(b)

Reconstruction of Ancient Environments and Landscapes | 211

followed by periods of relative warmth, or interglacials. Studies of such cold- and- warm patterns indicate that the time we live in, the Holocene, is not a separate epoch but simply another interglacial. More severely cold weather might be just around the corner!

CHEMISTRY OF ANIMAL REMAINS AND ANCIENT SOILS: WINDOWS ONTO DIETS AND HABITATS Chemical analysis of the bones and teeth in fossils provides important information about past animals’ diets and habitats. The reconstruction of diets and habitats is based on the plants those animals ate. Edible plants employ either C3 photosyn- thesis or C4 photosynthesis. The type of photosynthesis determines how the plant FIGURE 8.24 Foraminifera The chemical composition of these microorganisms found

in sediments on the ocean floor provides information on past climates.

Tropical

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et er

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)

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During the Eocene, temperature increased. This change might have led to the growth of tropical forests, which were ideal habitats for the tree-dwelling ancestors of modern primates.

In the Oligocene, temperatures plunged as Earth entered a cooling period. In formerly tropical environments, forested areas would have been replaced by open grasslands. Primate ancestors would have had to adapt to the grasslands or move to other tropical environments.

At the end of the Miocene, Earth entered another cooling period. Again, dramatic changes in habitat and climate occurred. The reduced forests and increased grasslands might have accounted, in part, for the evolution of bipedal locomotion.

FIGURE 8.25 Global Temperature and Climate Changes Changes in temperature during the Cenozoic have been documented by measuring 18O in foraminifera shells. A decrease in 18O indicates an increase in temperature; conversely, an increase in 18O indicates a decrease in temperature.

FIGURE 8.26 Antarctica During the latter part of the Miocene, glaciers advanced, tying up a great deal of water that once filled the Mediterranean Sea. Antarctica was covered by a massive ice sheet, as seen in this satellite image.

212 | CHAPTER 8 Fossils and Their Place in Time and Nature

extracts and uses carbon from atmospheric carbon dioxide (CO2). In East Africa, to take one example, C3 plants include trees, bushes, and shrubs associated with a relatively wet, wooded environment; C4 plants are associated with open grasslands typical of tropical savannas. Because C3 and C4 plants extract and use carbon dif- ferently, the two stable isotopes of carbon in the plants (12C and 13C) have different ratios. C3 plants have lower ratios of 13C to 12C than do C4 plants. That is, the values for the stable isotope ratios are lower for C3 plants than for C4 plants.

When animals eat the plants, those ratios are transmitted to the body tissues (including bones and teeth) through digestion and metabolism. Thus, scientists can determine which kind of plant the animal ate based on the ratio of 13C to 12C in the animal’s remains. The amounts of 13C and 12C are determined by placing a very tiny piece of bone or of tooth in an instrument called a mass spectrometer.

Similarly, the soils in which edible plants grow express different ratios of 13C to 12C.  The plant’s residue following decay preserves the stable carbon isotopes. Worldwide, the ratios in the soils, like those in the animals, tend to be lower in forested settings than in grasslands.

Numerous remains of Miocene apes and Pliocene and Pleistocene hominins and other animals have been found in Kenya (discussed further in chapters 9 and 10). The study of these fossils’ isotopic compositions has greatly informed scientists’ environmental reconstructions. Today, the Serengeti grasslands of Kenya are dom- inated by C4 grasses (Figure 8.27). It has long been assumed that the first hominins and their immediate apelike ancestors lived in such a setting. New evidence from the study of the ancient soils (paleosols) and animal bones in Kenya and elsewhere indicates an environment with relatively low 13C to 12C ratios (C3 plant dominance). This means that if C4 grasses typical of an open grassland were present, they were quite minimal. However, sometime after 6 mya, C4 plants became dominant for a range of mammals, indicating a marked shift in ecology. Recent work at a site in Lemudong’o, Kenya, by the American anthropologist Stanley Ambrose and colleagues shows that 6 mya the animals there, unlike the ones there today, lived

FIGURE 8.27 Serengeti Plain, Kenya These grasslands are mostly composed of C4 grasses.

C3 plants Plants that take in carbon through C3 photosynthesis, which changes carbon dioxide into a compound having three carbon atoms; tending to be from more temperate regions, these plants include wheat, sugar beets, peas, and a range of hardwood trees.

C4 plants Plants that take in carbon through C4 photosynthesis, which changes carbon dioxide into a compound with four carbon atoms; these plants tend to be from warmer regions with low humidity and include corn, sugarcane, millet, and prickly pear.

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among large trees and water. In particular, birds of prey that roost in large trees (such as the strigid owl) and the large number of colobine monkeys argue for a woodland habitat. Paleosols and fauna dating to around 5.6 mya at early hominin sites in the Middle Awash Valley of Ethiopia show a similar record of open wood- land or wooded grasslands around lake margins. The combined evidence from the study of paleosols and animal fossils indicates that the earliest hominins lived in wooded settings, probably for some time after 5 mya (discussed further in chap- ter 10). This knowledge is crucial because it helps us understand the environmental context in which our humanlike ancestors rose, and that rise is fundamental to who we are as biological organisms.

This chapter presented several key concepts for understanding the past, primarily the importance of fossils as windows onto the past. Once placed in time, fossils document and enable us to interpret change over time— they become the central record of evolution. In the upcoming chapters, we will apply this knowledge about fossils and how to evaluate them as we examine nonhuman and human primate evolution. We will look at the origin and evolution of primates, from their very beginning some 55 mya to the dawn of human evolution. Primates are part of a great adaptive radiation of mammals, a radiation that continues to the present day. Understanding primate evolution provides the context for understanding who we are as biological organisms.

A N S W E R I N G T H E B I G Q U E S T I O N S

C H A P T E R   8 R E V I E W

What are fossils? • Fossils are the remains of once- living organisms,

wholly or partially transformed into rock. The most common types of fossils are bones and teeth.

What do fossils tell us about the past? • Fossils provide an essential historical record for

documenting and understanding the biological evolution of surviving and nonsurviving lineages.

• Fossils provide information on chronology and geologic time.

• Fossils and their geologic settings reveal past diets and environments, important contexts for understanding how past organisms evolved.

What methods do anthropologists and other scientists use to study fossils? • Geologic time provides the grand scale of the

evolution of life. Both relative and absolute (numerical) dates place fossils and past events in chronological sequence on that scale.

• Relative and absolute dates can be determined through various methods. Radioactive decay is central to some of the best methods of determining absolute dates.

• Past climates and habitat in general can be reconstructed via the stable isotopes of oxygen.

• Ancient animals’ diets and their habitats can be reconstructed through the stable isotopes of carbon. This record reveals the increasing dominance of open grasslands in later Miocene and Pliocene times, the period when early hominins evolved.

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K E Y T E R M S amino acid dating biostratigraphic dating C3 plants C4 plants Cenozoic chemical dating cultural dating dendrochronology electron spin resonance dating epochs eras fission track dating

fluorine dating foraminifera half- life igneous index fossils isotopes Mesozoic paleomagnetic dating Paleozoic Pangaea pebble tools polarized light

racemization radiocarbon dating radiopotassium dating sedimentary Steno’s law of superposition strata stratigraphic correlation taphonomy tectonic thermoluminescence dating

E V O L U T I O N R E V I E W The Fossil Record

Synopsis The evolution of life on Earth has occurred on a geologic timescale that is almost unfathomable, with the first single-celled organisms appearing around 3.5 billion years ago and the first multicellular organisms appearing around 1.2 billion years ago. The evolution of the order Primates is more recent, occurring over the last 50 million years, and the evolution of our own branch (i.e., hominins) more recent still, from approximately 7 mya to the present. The physical evidence, primarily bones and teeth, of these evolutionary processes constitutes the fossil record. Advances in scientific dating techniques and the ability to reconstruct ancient environments have greatly expanded paleontologists’ and physical anthropologists’ understanding of the timing of major evolutionary events, the tempo at which evolution occurs, and the environmental pressures operating on species in deep time. This knowledge sets the stage for the “big questions” regarding primate and hominin evolution that will be addressed in the subsequent chapters.

Q1. Identify the two main components around which paleontology, or the scientific study of the fossil record, is built. How does each of these components contribute to our understanding of biological evolution?

Q2. Identify the main difference between methods of relative dat- ing and methods of absolute dating. Provide one example of the use of a relative dating technique and one example of the

use of an absolute dating technique in addressing research questions about human evolution.

Q3. By definition, our knowledge of the fossil record will always be incomplete, but scientists are nonetheless able to test hypotheses regarding the evolution of our own and other spe- cies. Summarize the process by which an organism’s remains become fossilized. What are some factors that can influence fossil discoveries and our knowledge of the fossil record?

Hint Think about events that can occur before, during, and after fossilization of an organism’s remains.

Q4 . Describe the process by which genetic dating can be accom- plished via the molecular clock. How do physical anthro- pologists use both genetic dating and the fossil record to clarify evolutionary relationships and the timing of evolutionary events? How do the data sources for genetic dating and the fossil record differ from one another?

Hint Think about the kinds of organisms studied for genetic dating compared to those found in the fossil record.

Q5. Explain how gradualism and punctuated equilibrium differ with regard to the tempo, or rate, of evolutionary change. What types of environmental conditions may cause the tempo of evolution to speed up, resulting in the rapid change found in some areas of the fossil record?

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A D D I T I O N A L R E A D I N G S

Klein, R. G.  1999. The Human Career: Human Biological and Cul- tural Origins. 2nd ed. Chicago: University of Chicago Press.

Lanham, U. 1973. The Bone Hunters. New York: Columbia Univer- sity Press.

Lee- Thorp, J. A., M. Sponheimer, and N. J. van der Merwe. 2003. What do stable isotopes tell us about hominid dietary and ecolog- ical niches in the Pliocene? International Journal of Osteoarchae- ology 13: 104–113.

Marshak,  S.  2012. Earth: Portrait of a Planet. 4th  ed. New  York: Norton.

Mayor, A. 2001. The First Fossil Hunters: Paleontology in Greek and Roman Times. Princeton: Princeton University Press.

Taylor,  R.  E.  1995. Radiocarbon dating: the continuing revolution. Evolutionary Anthropology 4: 169–181.

Winchester,  S.  2001. The Map That Changed the World: William Smith and the Birth of Modern Geology. New York: HarperCollins.

Wolpoff,  M.  H.  1999. Paleoanthropology. 2nd  ed. New  York: McGraw- Hill.

ALSO KNOWN AS THE “DAWN APE,” this fossil primate was an early ancestral catarrhine. Aegyptopithecus lived approxi- mately 29–32 mya, before the divergence of hominoids (apes) and Old World monkeys. Like many catarrhines, this primate was likely an arboreal quadruped that regularly consumed leaves and fruit. (Photo © 1985 David L. Brill, humanoriginsphotos.com)

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9 Why become a primate?

What were the first primates?

What were the first higher primates?

What evolutionary developments link past primate species and living ones?

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Primate Origins and Evolution The First 50 Million Years

Remember Georges Cuvier, the Frenchman (introduced in chapter 2) who recog-nized that fossils are the remains of now- extinct animals and of plants? I bring him up again because of his central role in the study of primate evolution. The field would not have been the same had he not lived in the late eighteenth and early nineteenth centuries, when the scientific method, as we know it, began to take shape. As a child, Cuvier read the eighteenth- century biology luminaries Linnaeus and Buffon, and their works sparked in him a lifelong interest in natural history. He went on to col- lege at the University of Stuttgart, in Germany; and like many other bright college grad- uates at the time, he was recruited as a private tutor for a wealthy family, in his case in Normandy, France. While living with his host family, as luck would have it, he met France’s leading naturalist and anatomist, Étienne Geoffroy Saint- Hilaire (1772–1844). Professor Geoffroy must have been impressed with young Cuvier because he hired Cuvier as his assistant in comparative anatomy at the new National Museum of Natural History, in Paris. Cuvier became interested in the mammal fossils around Paris, and his encyclopedic knowledge of anatomy enabled him to recognize similarities between animals represented by fossils and living animals.

Among the hundreds of fossil bones and fossil teeth that he studied was a tiny skull, which he found in a gypsum quarry at nearby Montmartre. Dating to the Eocene, this specimen was unlike any skull Cuvier had ever seen. Was the animal it had come from living or extinct? When he published his description of the fossil in 1822, he did not recognize the creature he called Adapis parisiensis as a primate (Figure 9.1).

B I G Q U E S T I O N S ?

218 | CHAPTER 9 Primate Origins and Evolution: The First 50 Million Years

By the late nineteenth century, other French paleontologists had realized that Cuvier’s fossil was that of an early primate, a finding that has been substantiated time and time again during the twentieth century, making Adapis the first primate fossil described by a scientist. Cuvier, the founder of paleontology, had good reasons for not recognizing this animal as a primate. For one thing, no fossil record of pri- mates existed then— just about everything discussed in this chapter was found long after Cuvier’s time. For another, taxonomists had very little understanding of living primate variation, and they had not yet defined the order much beyond Linnaeus’s classification scheme (discussed in chapter 2).

Although Cuvier’s assessment was wrong, his meticulous description of the Ada- pis fossil was very important. Stories like this happen often in science: the original discoverer may not recognize the finding for what it is, mostly because there is no context or prior discovery. Nevertheless, the discovery provides later scientists with important evidence. In this case, Cuvier’s pioneering detailed description began the long process of documenting primate evolution, a process that continues today. Moreover, Cuvier set the bar high for future paleontologists by demonstrating the value of thorough description. Most importantly, Cuvier’s careful work planted the seeds for asking key questions about primate origins.

In the two centuries since Cuvier, many thousands of fossils of ancient primates have been discovered in Europe, Asia, Africa, North America, and South America, providing a record— relatively complete for some time periods, frustratingly incom- plete for others— of the origins and evolution of the earliest primates and their descendants. In this chapter, we address the big questions by examining the fossil record for evidence of three key developments: the first primates, the origins of higher primates (anthropoids), and the origins and evolution of the major anthropoid groups (monkeys, apes, and humans). The time frame for this chapter is expansive— 50 million years! We start in the early Paleocene, somewhere around 66 mya, and end in the late Miocene, around 6 mya, the dawn of human evolution. The record indicates that pri- mates were highly successful and, like other mammals, underwent a cycle of adaptive radiations, followed by extinctions, and then new radiations of surviving lineages. These survivors are the primates occupying Earth today, including human beings (Figure 9.2).

Why Did Primates Emerge? We know what primates are. For example, they are agile and adept at grasping, the claws have been replaced by nails, they have stereoscopic vision (the eyes are on the front of the head), they have a reduced sense of smell, and they have a big brain (Figure 9.3). Why they became what they are is far less clear. In the early 1900s, the British anatomists Sir Grafton Elliot Smith and Frederic Wood Jones proposed their arboreal hypothesis to explain primate origins. Smith and Jones hypothesized that primates’ defining characteristics were adaptations to life in the trees: grasping hands and grasping feet were crucial for holding on to tree branches, binocular vision allowed much greater depth perception for judging distance in the movement from place to place in the trees, smell was no longer necessary for finding food, and greater intelligence was important for understanding three- dimensional space in the trees. The movement from life on the ground to life in the trees, Smith and Jones surmised, put into motion a series of selective pressures that resulted in the ancestral primate.

FIGURE 9.1 Cuvier and Adapis In describing the fossil remains of an animal he mistakenly thought was an ungulate or artiodactyl (hoofed mammal), Cuvier (here seated) named the specimen Adapis, Latin for “toward sacred bull.” Later scholars realized that these remains were the first primate fossil ever recorded by a scientist.

Lyon

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arboreal hypothesis The proposition that primates’ unique suite of traits is an adaptation to living in trees.

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The arboreal hypothesis continues to profoundly influence the way anthro- pologists think about primate origins and evolution. But in the early 1970s, the American anthropologist Matt Cartmill challenged the arboreal hypothesis. He pointed out that lots of mammals are arboreal (squirrels, for example), but except for primates none have evolved the entire set of characteristics that define the order Primates. (These characteristics include generalized structure, arboreal adaptation, and care of young; see chapters 6 and 7.) To account for primate origins, Cartmill proposed his visual predation hypothesis. He hypothesized that the first primate specialized in preying on insects and other small creatures, hunting them in tree branches or in forest undergrowth. Cartmill argued that the shift to life in the trees was not the most important factor in explaining primate origins. Rather, the catching of small prey— using both a highly specialized visual appara- tus and the fine motor skills of grasping digits— set primate evolution in motion.

Although the visual predation hypothesis elegantly explains the visual adap- tations, intelligence, and grasping abilities of primates, it leaves an important question unanswered: What role do the primate characteristics play in the acquisition and consumption of fruit, which many primates eat? The American anthropologist Robert Sussman has hypothesized that the visual acuity, grasping hands, and grasping feet of primates were mostly adaptations for eating fruit and other foods made available with the radiation of modern groups of flowering plants called angiosperms. In other words, the original primate adaptation was about getting

FIGURE 9.2 Primate Family Tree The variety of primates today is the result of millions of years of primate evolution. The different lineages represented by great apes, lesser apes, Old World monkeys, New World monkeys, and prosimians reflect divergences in primate evolution. For example, New World monkeys split off around 35 mya, and Old World monkeys diverged approximately 25 mya. The lineage leading to modern humans, however, diverged from the chimpanzee lineage much more recently, somewhere between 8 and 10 mya.

visual predation hypothesis The proposition that unique primate traits arose as adap- tations to preying on insects and on small animals.

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fruit and not about preying on insects. Sussman reasoned that because there was little light in the forest, early primates required visual adaptations for seeing small objects. Moreover, their grasping toes helped the animals cling to tree branches while they picked and ate fruit, rather than having to go back to more secure and larger branches, as squirrels do when they eat nuts. Sussman’s angiosperm radi- ation hypothesis is grounded in the acquisition of a new food source available in the early Cenozoic: fruit.

In reality, elements of all three hypotheses may have provided the evolutionary opportunities that resulted in primate origins. Indeed, primates’ most special fea- ture is their adaptive versatility, especially in an arboreal setting. Primates have evolved strategies and anatomical features that enhance their ability to adapt to new and novel circumstances. That evolution constitutes primates’ story of origin.

The First True Primate: Visual, Tree- Dwelling, Agile, Smart PRIMATES IN THE PALEOCENE? We know generally when the first primates appeared— almost certainly in the early Cenozoic era. But just how early in the Cenozoic is debated by the paleontologists who study early primate evolution. They have reached no consensus as to whether the first primates appeared in the Paleocene epoch, which began 66 mya, or in the following epoch, the Eocene, which began 56 mya. The Paleocene candidate for the first primates is a highly diverse, highly successful group of primitive mammals called the plesiadapiforms, which lived in western North America, western Europe, Asia, and possibly Africa. These animals represent an adaptive radiation that flourished over a 10- million- year period, beginning at the start of the Paleocene.

Despite their amazing diversity and geographic spread, by about 56 mya most of the plesiadapiforms had gone extinct. Were they primates? Probably not. The problem with attributing them to the primate order is that they lack the key characteristics that define primates today. That is, in contrast to primates, the plesiadapiforms lacked a postorbital bar and convergent eye orbits, their digits were not especially well adapted for grasping tree branches (they lacked opposability), their digits lacked nails (they had claws), their teeth were highly specialized (some even had three cusps on their upper incisors, as opposed to the single cusp of most primates today), and their brain was tiny (Figure 9.4). Moreover, some plesiadapi- forms lacked the auditory bulla, a part of the temporal bone that contains the middle- ear bones and is present in all primates. Because of their potential relation- ship with the first true primates, the American paleontologist Philip Gingerich has called them Proprimates, a separate order from Primates.

EOCENE EUPRIMATES: THE FIRST TRUE PRIMATES Far better contenders for early primates are the euprimates (meaning “true primates”), which first appeared at the start of the Eocene, as early as 56 mya. Euprimates consisted of two closely related, highly successful groups, the adapids and the omomyids. Found in the western United States, western Europe, Africa,

FIGURE 9.3 Primate Characteristics Primates differ from other mammals thanks to a unique combination of traits, such as forward- facing eyes, a postorbital bar or fully enclosed eye orbit, a large cranial vault, a reduced snout, and a versatile dentition. In the postcranial skeleton, primates usually have divergent big toes and divergent thumbs, grasping hands and grasping feet, and nails instead of claws on their fingers and their toes.

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and Asia, they were the most common early fossil primates— accounting for about 40% of all species from that time, or about 200 species (Figure 9.5).

Were they primates? Almost certainly. Unlike the plesi- adapiforms, adapids and omomyids had clear primate charac- teristics: the postorbital bar and convergent eye orbits, long digits with opposability for grasping, digits with nails (not claws), nonspecialized teeth, and a large brain relative to body size. These features indicate that vision was essential to their adaptation, they were agile and tree- dwelling, their diet was not as special- ized as that of the plesiadapiforms, and they were smarter than the earlier animals. Their body sizes were small but highly varied. Adapids were about the same size as some modern lemurs. One of the largest, Notharctus, weighed about 7 kg (15 lb). Adapis, known from many skulls and other parts of the skeleton, weighed a little more than 1 kg (2 lb). The adapids’ incisors were flat and vertical, similar to those of many living anthropoids (Figure 9.6). In addition, like anthropoids, adapids had pronounced sexual dimorphism in body size and in canine size, some had lower jaws with two fused halves, and some had relatively short foot bones.

The omomyids differed from the adapids in having large and projecting central lower incisors, small canines, and wide variation in the other teeth. Unlike most adapids (and sometimes like living tarsiers), omomyids had a short skull, a short and narrow snout, and large eye orbits. Their large eye orbits held huge eyes adapted for night vision. Like the adapids, the omomyids consisted of widely diverse species and have left behind a great number of fossils, facts that speak to their high degree of success throughout the Eocene epoch.

From what primitive mammalian group did the adapids and omomyids evolve?  Most of the plesiadapiforms are unlikely ancestors for the euprimates

plesiadapiforms Paleocene organisms that may have been the first primates, originating from an adaptive radiation of mammals.

Proprimates A separate order of early primate ancestors from the Paleocene, such as the plesiadapiforms.

euprimates The first true primates from the Eocene: the tarsierlike omomyids and the lemurlike adapids.

adapids Euprimates of the Eocene that were likely ancestral to modern lemurs and possibly ancestral to anthropoids.

omomyids Eocene euprimates that may be ancestral to tarsiers.

Notharctus A genus of one of the largest adapids from the Eocene.

Adapis A genus of adapids from the Eocene.

1 cm

.39 in (a)

(b)

FIGURE 9.4 Plesiadapis These primatelike mammals were likely an ancestral lineage leading to true primate ancestors. (a) As this Plesiadapis skull illustrates, plesiadapiforms did not possess primates’ postorbital bar. And while primates have a versatile dentition, plesiadapiforms had very specialized anterior (front) teeth, which were separated from the posterior (rear) teeth by a large gap. In addition, Plesiadapis and other plesiadapiforms had much smaller brains than did true primate ancestors. (b) This reconstruction of Plesiadapis reflects similarities to and differences from modern primates.

angiosperm radiation hypothesis The prop- osition that certain primate traits, such as visual acuity, occurred in response to the availability of fruit and flowers following the spread of angiosperms.

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because they either went extinct before the Eocene or were too specialized to have given rise to Eocene primates. However, one plesiadapiform, Carpolestes, whose skeleton was found in Wyoming’s Bighorn Basin, had a number of characteristics that would be expected in a transitional animal leading to what were clear primates later in time. Carpolestes had a grasping foot, made possible by an opposable big toe; it had long, grasping fingers; and it had a nail on the end of the first foot digit (Figure 9.7). This animal may be the link between proprimates of the Paleocene

(a)

(b)

(c)

(d)

FIGURE 9.5 Omomyids and Adapids These two main groups of euprimates are likely related to tarsiers and lemurs, respectively. Unlike plesiadapiforms, omomyids and adapids are considered true primate ancestors because they possess many primate traits. (a, b) Omomyids, such as Shoshonius (shown here), had large eyes and large eye orbits on the front of the skull, grasping hands and grasping feet, and a reduced snout. Like tarsiers, these earliest primates were nocturnal. (c, d) Adapids, including Cuvier’s Adapis, also had forward- facing eyes. However, adapids were diurnal and had longer snouts than omomyids.

Carpolestes A plesiadapiform genus from the Paleocene, probably ancestral to the Eocene euprimates.

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(a) (b)

FIGURE 9.6 Incisor Variation (a) In modern lemur species, the lower incisors form a dental comb that projects horizontally from the mandible. (b) This feature was absent, however, in adapids, whose more vertical incisors resembled those of living monkeys and living apes.

(a) (b) (c)

FIGURE 9.7 Carpolestes simpsoni (a) Fossilized remains such as these suggest that this species of plesiadapiforms is a link between primatelike mammalian ancestors and the earliest true primate ancestors. (b) In this reconstruction of the full skeleton, the fossilized remains are highlighted. (c) This reconstruction depicts what Carpolestes might have looked like in life.

224 | CHAPTER 9 Primate Origins and Evolution: The First 50 Million Years

and euprimates of the Eocene. The extinction of the plesiadapiforms, at the end of the Paleocene, and the appearance of the euprimates, at the beginning of the Eocene, coincided with a profound period of global warming. A rapid temperature increase around 55 mya created tropical conditions virtually everywhere around the world. The resulting creation of new habitats triggered an adaptive radiation of modern- appearing primates, the euprimates. In particular, the high global temperatures and high global humidity led to an expansion of evergreen tropical forest, the environment that made possible many mammalian groups, including the primates.

THE ANTHROPOID ANCESTOR: EUPRIMATE CONTENDERS Like the Paleocene proprimates preceding them, many of the euprimates went extinct. Some of them may have provided the ancestral base for strepsirhines and haplorhines. Based on the kind of skull and tooth evidence described above, Philip Gingerich has made the case that adapids represent the ancestral group for living lemurs and anthropoids, with lemurs evolving a tooth comb (missing in adapids) and anthropoids not evolving the tooth comb. Their flat incisors, general similarity with anthropoids, and great diversity suggest that adapids had an evolutionary rela- tionship with anthropoids. However, some (or even all) of adapids’ anthropoidlike features could simply be unevolved (primitive) traits of all primates. If that is the case, then an ancestral- descendant link between adapids and later primates would be difficult to prove.

The American anthropologist Frederick Szalay sees a strong resemblance between omomyid fossils and living tarsiers and a greater similarity between

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FIGURE 9.8 Archicebus This skeleton and reconstruction of Archicebus show its combination of anthropoid and tarsier features. Its heels and ankles resemble those of monkeys, whereas its small eyes and short snout resemble those of tarsiers.

(b)(a)

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tarsiers and anthropoids than between lemurs and anthropoids. Therefore, he regards the omomyids as more likely candidates for the ancestry of anthropoids than lemurs are. However, the anatomical similarities between omomyids and tarsiers are more suggestive than definitive. No single characteristic links these Eocene primates with anthropoids. While the adapids or omomyids may be ances- tral to anthropoids, the lack of clear transitional fossils between these archaic primates and later primates makes it unclear what the anthropoid ancestor was more than 40 million years ago.

Clues to the characteristics of the early haplorhines are seen in a remarkably well- preserved skeleton of an early primate, dating to 55 mya and known as Archicebus (Figure  9.8). Discovered in an ancient lake bed in the Jingzhou area of Hubei Province, China, by a team led by the Chinese paleontologist Xijun Ni, this primate combines features of anthropoids and tarsiers. The presence of this primate in China at such an early date indicates that haplorhines originated in Asia. Although Archicebus may not have been the first haplorhine, it emerged very close to the split between haplorhines and strepsirhines. Its heel and ankle bones resemble those of monkeys. Its skull resembles that of tarsiers, with small eye orbits and a short snout. In addition, the cusps on the molars are high and pointed, similar to what is seen in tarsiers. This mosaic of features suggests that haplorhines originated at 55 mya, on the boundary between the Paleocene and the Eocene. It also suggests that the first haplorhines were diurnal (and therefore had these small eye orbits), arboreal (and therefore had these foot, hand, and limb structures), and primarily insectivorous (as tarsiers are today). And in contrast to their great evolutionary significance, the earliest- known primates appear to have been tiny. Archicebus is estimated to have been even smaller that the mouse lemur (the smallest primate today), weighing only about 28 gm (1 oz) and easily fitting into the palm of your hand.

THE FIRST ANTHROPOIDS During the Eocene, a group of primates called basal anthropoids, whose fossils have been found in Asia and Africa, had the kinds of characteristics that would be expected in an anthropoid ancestor or even the earliest anthropoid. One of the most interesting basal anthropoids is the remarkably tiny Eosimias (mean- ing “dawn monkey”), found near the village of Shanghuang, in Jiangsu Province, China, and dating to about 42 mya (Figure 9.9). It is one of a number of eosimiids found in southern and eastern Asia. Based on their observations of the teeth and the skeleton, especially of the foot bones, the American anthropologists Daniel Gebo and Christopher Beard regard Eosimias as the first true anthropoid. Espe- cially convincing about their argument is the strong similarity between the shape and overall appearance of Eosimias’s tarsal (ankle) bones and those of fossil and living anthropoids. That is, Eosimias’s short calcaneus, or heel bone, was like that of an anthropoid (Figure 9.10). It was especially similar to those of South American monkeys, revealing that this primate moved in trees like a monkey. In addition, the upper canine and upper jaw would have given it a monkeylike face.

Another, somewhat later basal anthropoid is from the Fayum Depression, in Egypt. Called Biretia by the American paleontologists Erik Seiffert and Elwyn Simons, it dates to the late Eocene, at about 37 mya. The presence of anthropoid characteristics in the teeth, such as the two- cusped (bicuspid) lower premolars, indicates that this animal, too, represents the beginnings of higher primates

FIGURE 9.9 Eosimias This basal anthropoid, first discovered in 1999, represents one of the earliest genera of catarrhines (Old World monkeys and apes). Eosimias is the smallest primate ancestor discovered to date. Its smallest species is about the size of a human thumb and about one- third the size of the smallest living primate, the mouse lemur of Madagascar, which weighs approximately 28 g (1 oz). The fossilized remains suggest they were arboreal insectivores and likely nocturnal.

basal anthropoids Eocene primates that are the earliest anthropoids.

Eosimias A genus of very small basal anthropoids from the Eocene.

Biretia An early basal anthropoid with two cusps on its lower premolars. It is one of numerous primate species recov- ered from the Fayum of northeastern Africa.

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(Figure  9.11). If it is the first higher primate, then either anthropoid ancestry began in Africa or the earlier primates from Asia emigrated to Africa and evolved into the African anthropoids. Based on the limited evidence, it is not possible to say conclusively whether Asia or Africa is the ancestral home of the higher primates, anthropoids. However, Eosimias and Biretia have the attributes that would be expected in an anthropoid ancestor. Given the earlier date for Eosimias, Asia could be the ancestral home for the higher primates. If so, then Asian basal anthropoids gave rise to all of the higher primates of Africa.

This discussion should make clear that anthropoids’ origin is murky. To under- stand the geographic (Asia versus Africa) and environmental contexts in which anthropoids arose, anthropologists are looking to the increasing fossil record of basal anthropoids and their remarkable diversity. Regardless of their geographic origins, the diversity of basal anthropoids found in both Asia and Africa suggests the beginnings of a remarkable radiation of a highly successful group of mammals.

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Tarsier foot

Tarsier Eosimias Baboon

Baboon foot

Long calcaneus

Short calcaneus

FIGURE 9.10 Calcaneal Variation Evidence for patterns of locomotion in Eosimias comes from some of the postcranial remains, especially bones of the ankle and foot. Eosimias’s calcaneus was more like that of an anthropoid (such as the baboon) than like that of a prosimian (such as the tarsier).

FIGURE 9.11 Biretia Its fossilized remains suggest that this animal was an anthropoid ancestor. For example, its lower premolars, with their two cusps, are structured like anthropoids’.

Early Anthropoids Evolve and Thrive | 227

Early Anthropoids Evolve and Thrive Beginning in the Oligocene epoch and coinciding with a period of widespread plant and animal extinctions, an episode of rapid global cooling occurred. With this shift in climate came new habitats and newly diverse primate taxa. The fossil record representing the evolution of these taxa is as remarkable in the Oligocene as the fossil record is in the Eocene. However, whereas Eocene primate fossils have been found in a wide variety of settings around the world, most of the Oligocene primate fossils have come from one primary region, the Fayum. Spanning about 8  million years of evolution, roughly 37–29 mya, the fossil record consists of a wide and abundant variety of plants and of animals. From these remains, scien- tists have constructed a detailed picture of the environment in northeast Africa (Figure 9.12). In sharp contrast to the desert landscape of the Fayum today— it is

When Were They Primates?: Anatomy through Time

Primates have a number of anatomical characteristics that reflect both an adaptation to life in the trees and related behaviors. Contenders for primate status in the Paleocene generally lack these characteristics; two groups of closely related Eocene mammals— adapids and omomyids— have these characteristics.

Characteristic Paleocene (66–56 mya)

Eocene (56–34 mya)

Present

Increased vision No Yes Yes

Partially or fully enclosed eye orbits No Yes Yes

Convergent eyes No Yes Yes

Small incisors and large canines No Yes Yes

Nails at ends of digits No Yes Yes

Mobile, grasping digits No Yes Yes

Short snout No Yes Yes

Reduced smell No Yes Yes

Increased brain size No Yes Yes

C O N C E P T C H E C K !

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among the harshest and driest places in the world— the late Eocene– early Oligo- cene landscape was much like contemporary southeast Asia— namely, wet, warm, and tropical. The Fayum’s major feature, Birket Qarun Lake, was long the focus for all organisms in the region. In addition to diverse primates, all sorts of animals lived there, including the ancestors of rodents (the earliest porcupines are from the Fayum), bats, hippopotamuses, elephants, crocodiles, and various birds. Plants are also represented by a diverse array of tropical taxa, such as mangroves, water lilies, climbing vines, figs, palms, and cinnamon. It must have been an amazing place.

The Fayum primates included various strepsirhines and at least three groups of primitive (but unmistakable) higher primates: oligopithecids, parapithecids, and propliopithecids. The oligopithecids were the earliest, dating to about 35 mya. The later parapithecids, such as their namesake genus, Parapithecus, are among these early anthropoids; and they retained some primitive characteristics. For example, parapithecids had three premolars. This condition may directly link parapithecids to platyrrhines (which also have three premolars), but having three premolars is more likely the ancestral condition that precedes the divergence of platyrrhines and catarrhines.

The propliopithecids consisted of several genera, but Propliopithecus and Aegyptopithecus, both dating to between 32 and 29 mya, are the most common of this group of primates. The propliopithecids had a more derived dental formula of 2/1/2/3, one fewer premolar than the parapithecids had. In this and other respects, they were more catarrhinelike than the parapithecids. Aegyptopithecus, the largest of the Fayum primates (it weighed 6–8 kg [13–18 lb], or about the weight of a fox) is the best- known Fayum primate (Figure 9.13). Aegyptopithecus had a sagittal crest on the top of the skull where a large temporalis muscle was attached (see Fig- ure 6.29 in chapter 6). Its brain was small compared to those of later catarrhines. The front and hind limbs were of relatively equal size, suggesting that the animal was a slow- moving, arboreal quadruped, similar to the modern howler monkey. Its overall appearance indicates that Aegyptopithecus was a primitive catarrhine— and a likely contender for the common ancestor of all later catarrhines.

While the record of early catarrhines is best and mostly richly represented at the Fayum, at least one fossil representing an ancestor of monkeys, apes, and humans has been recovered from the modern country of Saudi Arabia. During the Oligocene, before the formation of the Red Sea, the continent of Africa and the Arabian Peninsula formed a single landmass. The remarkable radiation of primates in the Fayum suggests that similar habitats in Arabia supported similar kinds of primates. In their search for Oligocene fossils, the paleontologist Iyad Zalmout and colleagues found most of a skull of an early catarrhine, now known as Saadanius. Dating to about 28 mya and postdating Aegyptopithecus, this primate

FIGURE 9.12 The Fayum Climatological and environmental reconstructions have provided a glimpse of what the Fayum was like when some of the earliest primates lived, at the end of the Eocene and the beginning of the Oligocene.

Parapithecus A genus of later parapith- ecids from the Oligocene, found in the Fayum, Egypt.

Propliopithecus Oligocene propliopithecid genus.

Aegyptopithecus A propliopithecid genus from the Oligocene, probably ancestral to catarrhines; the largest primate found in the Fayum, Egypt.

Saadanius An early catarrhine Oligocene genus from a group of primates that gave rise to later catarrhines.

FIGURE 9.13 Aegyptopithecus Shaded red in this reconstruction are the postcranial skeletal fossils of Aegyptopithecus that have been found in Fayum deposits. These recovered elements provide important information regarding the animal’s mobility and form of locomotion: arboreal quadrupedalism.

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Rukwa Rift Basin

oligopithecids The earliest anthropoid ancestors in the Oligocene, found in the Fayum, Egypt.

parapithecids Anthropoid ancestors from the Oligocene, found in the Fayum, Egypt.

propliopithecids Anthropoid ancestors from the Oligocene, found in Africa.

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The Fayum primates included various strepsirhines and at least three groups of primitive (but unmistakable) higher primates: oligopithecids, parapithecids, and propliopithecids. The oligopithecids were the earliest, dating to about 35 mya. The later parapithecids, such as their namesake genus, Parapithecus, are among these early anthropoids; and they retained some primitive characteristics. For example, parapithecids had three premolars. This condition may directly link parapithecids to platyrrhines (which also have three premolars), but having three premolars is more likely the ancestral condition that precedes the divergence of platyrrhines and catarrhines.

The propliopithecids consisted of several genera, but Propliopithecus and Aegyptopithecus, both dating to between 32 and 29 mya, are the most common of this group of primates. The propliopithecids had a more derived dental formula of 2/1/2/3, one fewer premolar than the parapithecids had. In this and other respects, they were more catarrhinelike than the parapithecids. Aegyptopithecus, the largest of the Fayum primates (it weighed 6–8 kg [13–18 lb], or about the weight of a fox) is the best- known Fayum primate (Figure 9.13). Aegyptopithecus had a sagittal crest on the top of the skull where a large temporalis muscle was attached (see Fig- ure 6.29 in chapter 6). Its brain was small compared to those of later catarrhines. The front and hind limbs were of relatively equal size, suggesting that the animal was a slow- moving, arboreal quadruped, similar to the modern howler monkey. Its overall appearance indicates that Aegyptopithecus was a primitive catarrhine— and a likely contender for the common ancestor of all later catarrhines.

While the record of early catarrhines is best and mostly richly represented at the Fayum, at least one fossil representing an ancestor of monkeys, apes, and humans has been recovered from the modern country of Saudi Arabia. During the Oligocene, before the formation of the Red Sea, the continent of Africa and the Arabian Peninsula formed a single landmass. The remarkable radiation of primates in the Fayum suggests that similar habitats in Arabia supported similar kinds of primates. In their search for Oligocene fossils, the paleontologist Iyad Zalmout and colleagues found most of a skull of an early catarrhine, now known as Saadanius. Dating to about 28 mya and postdating Aegyptopithecus, this primate

FIGURE 9.12 The Fayum Climatological and environmental reconstructions have provided a glimpse of what the Fayum was like when some of the earliest primates lived, at the end of the Eocene and the beginning of the Oligocene.

Parapithecus A genus of later parapith- ecids from the Oligocene, found in the Fayum, Egypt.

Propliopithecus Oligocene propliopithecid genus.

Aegyptopithecus A propliopithecid genus from the Oligocene, probably ancestral to catarrhines; the largest primate found in the Fayum, Egypt.

Saadanius An early catarrhine Oligocene genus from a group of primates that gave rise to later catarrhines.

FIGURE 9.13 Aegyptopithecus Shaded red in this reconstruction are the postcranial skeletal fossils of Aegyptopithecus that have been found in Fayum deposits. These recovered elements provide important information regarding the animal’s mobility and form of locomotion: arboreal quadrupedalism.

T A N Z A N I A

Rukwa Rift Basin

230 | CHAPTER 9 Primate Origins and Evolution: The First 50 Million Years

shared a number of features with the Fayum catarrhines, such as dental formula (2/1/2/3); upper molars with low, rounded cusps; and shape of the face. However, it differs from Fayum primates in having the bony auditory tube typical of later catarrhine primates.

According to the molecular evidence, the first apes and first monkeys originated in the early Miocene, likely between 25 and 30 mya (see chapter 8, “Genetic Dat- ing: The Molecular Clock”). Two fossil primates found in Tanzania illustrate the split, by 25 mya, that led to the emergence of modern apes and modern monkeys. In the Rukwa Rift Basin of eastern Tanzania, the American paleoanthropologist Nancy Stevens and her team discovered the earliest ape and earliest Old World monkey, named, respectively, Rukwapithecus fleaglei and Nsungwepithecus gunnelli. Rukwapithecus is represented by part of a mandible and teeth, and its second molar shares features with the second molars of later fossil apes. Nsungwepithecus is rep- resented by part of a mandible and just one molar. While the bilophodont cusps of that molar are not fully modern, they are clearly cercopithecoid. As a represen- tation of the split between apes and monkeys, this fossil record is modest; but it shows that ancestral apes and monkeys were present in East Africa at about the time most authorities expected.

The presence in the Arabian Peninsula and East Africa of the later Oligocene catarrhine underscores the strong likelihood that the ancestry of fossil and mod- ern catarrhines is broadly based in the African– Arabian landmass during the later Oligocene.

Coming to America: Origin of New World Higher Primates Aegyptopithecus, the earliest definitive catarrhine, clearly evolved from some anthropoid in the Old World, almost certainly in Africa. But where did the other anthropoids, the platyrrhines, come from? The first South American primate is a primitive monkey called Branisella, whose fossils were found near Salla, Bolivia, in geological deposits dating to the very late Oligocene, about 26 mya. It appears to have been a platyrrhine, given that it had three premolars and, especially, three upper molars with a four- cusp chewing surface strongly similar to that of the upper molars in living New World monkeys, such as the owl monkey. The fossil record for South America is generally sparse after the late Oligocene, but it shows the general patterns of platyrrhine evolution. The fossil platyrrhines bear a striking resemblance to living platyrrhines, represented by cebids and atelids.

HOW ANTHROPOIDS GOT TO SOUTH AMERICA One important question about the origins of platyrrhines is just how they got to South America. Four alternative hypotheses have emerged to explain primates’ presence in South America. First, platyrrhines evolved from a North American anthropoid, then migrated to South America in the late Oligocene. Second, platyr- rhines evolved from an African anthropoid and migrated across the Atlantic to South America. Third, platyrrhines evolved from an anthropoid in Africa that migrated south (mainly) on land to Antarctica and then to Patagonia, at the south- ern tip of South America. Fourth, Old World and New World anthropoids evolved independently from different lineages in Africa and South America, respectively.

FIGURE 9.14 Old World and New World Monkeys The physical resemblance of (a) Old World monkeys and (b) New World monkeys suggests that platyrrhines originated in Africa, rather than North America. Their mode of reaching South America, however, is still highly debated.

(a)

(b)

Apes Begin in Africa and Dominate the Miocene Primate World | 231

No evidence supports the first hypothesis— there were no anthropoids in North America during the Eocene or Oligocene. There were various euprimates, but none resembled the platyrrhines in South America during the late Oligocene.

Evidence supports the second hypothesis. There were early anthropoids in Africa (Fayum) beginning in the late Eocene, and they predated platyrrhines but looked remarkably similar to the earliest platyrrhines in South America (for example, they had three premolars). This resemblance indicates that platyrrhines originated in Africa before their appearance in South America. In addition, fossils indicate other similarities between animals in Africa and in South America.

The strong similarities between Old World and New World higher primates also support the third hypothesis. Migration across Antarctica would be impossible today, of course. However, migration over this major landmass would have been possible through much of the Eocene, when the climate there was much warmer and dryer.

Given the strong anatomical resemblance between African higher primates and South American higher primates, it is highly unlikely that anthropoids evolved independently in Africa and South America (Figure  9.14). DNA evidence that shows a strong relationship between Old World and New World higher primates is even stronger proof against the fourth hypothesis. In other words, these two groups did not evolve independently: they both originated in Africa.

On the face of it, it seems unlikely that primates migrated from Africa to South America via the Atlantic, especially in view of the wide and prohibitive expanse of open sea separating the west coast of Africa from the east coast of South America. At the time, however, areas of the ocean might have been shallow and dotted with series of islands. Moreover, primates might have crossed from Africa to South America via ocean currents, on natural rafts consisting of accumulated vegetation.

Apes Begin in Africa and Dominate the Miocene Primate World Following the Oligocene, the strength and completeness of the higher primate fossil record derives from rich Miocene geological deposits in East Africa, espe- cially in the present- day countries of Kenya and Uganda. Just before this time, a warming trend in the late Oligocene provided the conditions for a shift in habitats and the appearance of a new and widespread radiation of a group of catarrhine primates called the proconsulids, mostly dating to roughly 22–17 mya. Recall that the last of the Oligocene primate fossils, in Egypt and Saudi Arabia, date to about 29–28 mya. This means that about a 6- million- year gap exists between the late Oligocene catarrhines (28 mya) and the first Miocene proconsulids (22 mya). As a consequence, the immediate ancestors of proconsulids are a mystery. However, the strong anatomical similarity in skulls and in teeth between Oligocene catarrhines from the Fayum and the Arabian Peninsula and the proconsulids of the Miocene indicates a likely ancestral- descendant relationship between the earlier and later groups. For example, all of these primates have a dental formula of 2/1/2/3, and their upper incisors are broad and flat.

The proconsulids are represented by a diversity of taxa— as many as 10 genera and 15 species— from the early and middle Miocene. In fact, the diversity of pro- consulids is much greater than that of living apes today. For example, proconsulids ranged from the tiny Micropithecus, the size of a small New World monkey, to

B O L I V I A

SallaSalla

Rusinga Island

U G A N D A K E N YA

Branisella A South American genus from the Oligocene, ancestral to platyrrhines.

proconsulids Early Miocene apes found in East Africa.

Micropithecus A genus of very small proconsulids from the Miocene, found in Africa.

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the namesake genus, Proconsul, a species of which, Proconsul major, was about the size of a modern male chimpanzee, weighing about 50 kg (110 lb). Proconsul is the best- known of the early to middle Miocene apes from Africa, in part thanks to a nearly complete skeleton discovered on Rusinga Island, in western Kenya’s Lake Victoria, in the late 1940s (Figure  9.15). Reflecting the proconsulids’ biological diversity, their fossils have been found in a range of settings, representing differ- ent climates and environments, from open woodlands to tropics. Reflecting these different habitats, their diets varied considerably.

The skulls and teeth of the Miocene proconsulids were clearly like apes’ in overall appearance. The molars have the Y- 5 pattern, and the cusps are wide and rounded for eating fruit. There are well- developed honing surfaces on the backs of the upper canines and the fronts of the lower third premolars. Comparisons of tooth wear in living apes and in extinct Miocene apes suggest that some of the extinct apes ate leaves and some ate nuts and fruit but that most of them routinely ate ripe fruit.

In contrast to the skulls and teeth, the rest of the skeleton of Miocene apes is generally like monkeys’ (Figure  9.16). Unlike the living apes, these primitive apes had front and hind limbs that were equally long and that lacked specializa- tions for knuckle- walking or arm- swinging. Moreover, like Old World monkeys, Proconsul had wrist bones (carpals) that articulated directly with the ulna, one of the two forearm bones. This direct articulation, a primitive characteristic, indicates relatively limited wrist mobility, whereas living apes have highly mobile wrists for arm- swinging and arm- hanging. Proconsulids’ elbows could straighten

Proconsul A genus of early Miocene proconsulids from Africa, ancestral to catarrhines.

(a)

(b)

FIGURE 9.15 Proconsul This Miocene ape genus was first found in Kenya in 1909—it was the first fossil mammal ever discovered in that region of Africa. Proconsul literally means “before Consul”; Consul was the name given to chimpanzees that performed in European circuses. Proconsul, then, is considered an ancestor to apes, including chimpanzees. (a) The first skull of the genus was found in 1948 and was nearly complete. The cranial remains helped researchers determine that Proconsul was possibly an ancestor to apes. (b) Other fossil finds have helped researchers determine what Proconsul’s full skeleton was like. Note that it lacked a tail, like all modern apes. Here, areas shaded in red represent the parts of the skeleton that have been discovered.

Apes Begin in Africa and Dominate the Miocene Primate World | 233

Arms and legs same length

Arms longer than legs

Highly mobile shoulder joint

Shoulder joint mobility limited

Small hands

Large hands

Shallow rib cage

Deep ribcage

Limited elbow extension

High degree of elbow extension

FIGURE 9.16 Proconsulid Body Plan The body plan of primitive, Miocene apes (left) differs from that of modern apes (right). The Miocene apes had a more monkeylike body, with smaller hands, a more restricted hip joint, and a more flexible spine. Modern apes have highly mobile shoulder joints and fully extendable elbow joints, enabling them to brachiate, or swing from branch to branch; the Miocene apes, by contrast, probably were arboreal quadrupeds, not needing the great mobility in their shoulders and their wrists. For the purposes of comparison, this Miocene ape, Proconsul, and this lesser ape, the modern gibbon, have been drawn the same size. In reality, Proconsul was about half the size of a gibbon.

234 | CHAPTER 9 Primate Origins and Evolution: The First 50 Million Years

only so far, whereas living apes’ elbows can extend completely. Proconsulids’ feet combined primitive and derived features— some of the anklebones were slender, like monkeys’, but the big toes were large, like apes’. The whole package suggests that Proconsul, unlike living apes, walked on the tops of tree branches on all fours. Because these creatures lacked a number of anatomical features that living hom- inoids share, they can be used as a model of the animals that gave rise to the last common ancestor of all later hominoids.

Apes Leave Africa: On to New Habitats and New Adaptations The presence of ape fossils in Europe and Asia from about 17 mya (but not before) suggests that apes originated in Africa and then spread to Europe and Asia. The migration of primates (and other animals) from Africa to Europe and Asia was made possible by a land bridge created 23–18 mya by a drop in sea levels and the joining of the African– Arabian tectonic plate with Eurasia. Following their dispersal into Europe and Asia, apes became more diverse than ever before, thus representing an extraordinary adaptive radiation, among the most successful among higher primates.

APES IN EUROPE: THE DRYOPITHECIDS By 13 mya, the early apes had successfully adapted to a wide range of new habitats. During this time, Europe was covered by a dense, subtropical forest that provided a rich variety of foods, especially fruit. Dryopithecus, the best- known genus within a group of great apes called dryopithecids, lived in the area of Europe that is now France and Spain. Larger than earlier apes— about the size of a chimpanzee— it was first discovered and described by the eminent French paleontologist Edward Lartet (1801–1871), in 1856, in St.  Gaudens, southern France. Dryopithecus and its contemporary taxa are known from other European regions, such as Spain, Greece, and Hungary.

Dryopithecus resembled living apes in many ways: its canines were sharp and tusklike; its cheek teeth were long and had very simple chewing surfaces, well- adapted for chewing fruit (Figure 9.17); and microscopic studies of cross sections of the teeth enamel indicate that these apes grew slowly. Their brains were larger than earlier primates’, similar to the modern chimpanzee’s. Their long forelimbs, grasping feet, and long, grasping hands were powerful and adapted for arm- hanging and arm- swinging, modern apes’ main forms of locomotion.

FIGURE 9.17 Dryopithecus (a) The mandible of Dryopithecus, a Miocene ape genus from Europe, like that of (b) a modern gorilla, includes the Y- 5 molar pattern and low, rounded cusps. Both also have large canines, plus the diastema between the canine and the first premolar.

(a) (b)

FIGURE 9.18 Sivapithecus Originally found in the Siwalik Hills of modern- day India and Pakistan, this Miocene ape (center) has been proposed as ancestral to the orangutan (right). Sivapithecus’s facial features, for example, are far closer to the orangutan’s than to those of other great apes, such as the chimpanzee (left). Sivapithecus has three species, any of which may be a direct ancestor to the orangutan; however, recent finds of another Miocene ape genus have called this ancestry into question.

Dryopithecus A genus of dryopithecid apes found in southern France and north- ern Spain.

dryopithecids Early Miocene apes found in various locations in Europe.

sivapithecids Early Miocene apes found in Asia.

Sivapithecus A genus of Miocene sivapithecids, proposed as ancestral to orangutans.

Khoratpithecus A genus of Miocene apes from Asia, likely ancestral to orangutans.

Apes Leave Africa: On to New Habitats and New Adaptations | 235

APES IN ASIA: THE SIVAPITHECIDS In Asia, the sivapithecids were the counterpart of Europe’s dryopithecids. The best- known sivapithecid is Sivapithecus, an ape ancestor that thrived about 12–8 mya. Whereas chimpanzees and gorillas have thin- enameled teeth, Sivapithecus had thick- enameled teeth, adapted for eating hard, tough- textured foods such as seeds and nuts. Its robust jawbones were similarly adapted.

Because hominins also have thick- enameled teeth, primatologists once thought Sivapithecus was the ancestor of hominins. This hypothesis was rejected in 1979, when the anthropologists David Pilbeam and Ibrahim Shah discovered a partial Sivapithecus skull (Figure 9.18). Sivapithecus skulls are strikingly similar to those of living orangutans, with concave faces, narrow nasal bones, oval eye orbits from top to bottom, projecting premaxillas (the premaxilla is the area of the face below the nose), large upper central incisors, and tiny lateral incisors. Even more similar to living orangutans, however, is the newly discovered Khoratpithecus, a hominoid of the late Miocene (9–6 mya) in Thailand. Various features of this primate’s teeth and lower jaw— for example, broad front teeth, canines with a flat surface on the tongue side— indicate that this Miocene primate is living orangutans’ most likely ancestor.

Closely related to Sivapithecus, Khoratpithecus, and other Asian Miocene apes is a very interesting pongid, Gigantopithecus, also from Asia, dating to about 8–.5 mya (Figure 9.19). Appropriately named for its massive body, Gigantopithecus is the biggest primate that has ever lived, standing nearly 3 m (10 ft) tall and weighing as much as 300 kg (660 lb)! Its massiveness would have limited this fossil primate to the ground for all its activities. Like some of the other Miocene apes, it had thick- enameled teeth and large, thick- boned jaws, adapted for eating very hard foods, likely nuts and seeds.

DEAD END IN APE EVOLUTION: THE OREOPITHECIDS Around the same time Gigantopithecus emerged, a group of apes called oreopith- ecids lived in Europe. They appear in the fossil record around 8 mya and disap- pear around 7 mya. Oreopithecus, the best- known of this group, has been found mostly in coal mines in Tuscany, Italy. (Oreopithecids were also present in Africa at the same time as the proconsulids on that continent.) Its Miocene habitat was dense, tropical forests, and its teeth were highly specialized for eating leaves (Figure  9.20). Also known as the “Swamp Ape,” Oreopithecus was a medium- size

FIGURE 9.19 Gigantopithecus Bamboo was probably among the plant foods eaten by this enormous, herbivorous Miocene ape. Climate change and competition with other primate species likely brought about this ape’s extinction.

FIGURE 9.20 Oreopithecus The high, shearing crests on its molars suggest that this Miocene ape was folivorous. Like Gigantopithecus, this ancestral ape likely became extinct due to climate change.

Gigantopithecus A genus of Miocene pongids from Asia; the largest primate that ever lived.

oreopithecids Miocene apes that were found in Europe.

Oreopithecus A genus of oreopithecids found in Italy that was extinct within a million years of its appearance.

236 | CHAPTER 9 Primate Origins and Evolution: The First 50 Million Years

Primate evolution began with primitive primates in the Eocene, setting the stage for the origin of all hominoids. Euprimates of the Eocene had the basic characteristics of living primates, such as convergent eye orbits and grasping digits. In the last 20 million years, primates diversified in appearance and behavior. These changes included the shift, for some, from life in the trees to life on the ground, and eventually the beginning of bipedality in the late miocene. (Based on Fleagle, J. G. Primate Adaptation and Evolution, 2nd ed. 1999. Academic Press.)

Scenes from the late Eocene in the Paris Basin. Top: The diurnal Adapis is feeding on leaves. Bottom: Several taxa of omomyids (Pseudoloris, Necrolemur, Microchoerus). Note the large eyes, a nocturnal adaptation, typical of both ancient and modern prosimians who are active at night.

Scene from the early Miocene of Rusinga Island, Kenya. Apes first appeared during this period, and these are the first apes (two species of Proconsul, Dendropithecus, Limnopithecus). These and other taxa form the ancestry of all later apes and hominins. Note the range of habitats occupied by these primates within the forest, including some in the middle and lower canopies and some on the forest floor. These primates show a combination of monkeylike and apelike features, in the skeleton and skull, respectively.

Scenes from the early Oligocene of the Fayum, Egypt. These anthropoid ancestors include Aegyptopithecus, Propliopithecus, and Apidium. These primates were adept arborealists, using their hands and feet for climbing and feeding.

Convergent eyes and grasping hands

Large eyes for nocturnal vision

Eocene 34–56 mya

Oligocene 23–34 mya Miocene 5.3–23 mya

Quadrupedal, monkeylike primate with superb arboreal skills

Quadrupedal, apelike primate. Note the lack of a tail, an ape characteristic.

Eocene-Oligocene-Miocene Habitats and Their Primates

F I G U R E

9.21

Apes Leave Africa: On to New Habitats and New Adaptations | 237

Primate evolution began with primitive primates in the Eocene, setting the stage for the origin of all hominoids. Euprimates of the Eocene had the basic characteristics of living primates, such as convergent eye orbits and grasping digits. In the last 20 million years, primates diversified in appearance and behavior. These changes included the shift, for some, from life in the trees to life on the ground, and eventually the beginning of bipedality in the late miocene. (Based on Fleagle, J. G. Primate Adaptation and Evolution, 2nd ed. 1999. Academic Press.)

Scenes from the late Eocene in the Paris Basin. Top: The diurnal Adapis is feeding on leaves. Bottom: Several taxa of omomyids (Pseudoloris, Necrolemur, Microchoerus). Note the large eyes, a nocturnal adaptation, typical of both ancient and modern prosimians who are active at night.

Scene from the early Miocene of Rusinga Island, Kenya. Apes first appeared during this period, and these are the first apes (two species of Proconsul, Dendropithecus, Limnopithecus). These and other taxa form the ancestry of all later apes and hominins. Note the range of habitats occupied by these primates within the forest, including some in the middle and lower canopies and some on the forest floor. These primates show a combination of monkeylike and apelike features, in the skeleton and skull, respectively.

Scenes from the early Oligocene of the Fayum, Egypt. These anthropoid ancestors include Aegyptopithecus, Propliopithecus, and Apidium. These primates were adept arborealists, using their hands and feet for climbing and feeding.

Convergent eyes and grasping hands

Large eyes for nocturnal vision

Eocene 34–56 mya

Oligocene 23–34 mya Miocene 5.3–23 mya

Quadrupedal, monkeylike primate with superb arboreal skills

Quadrupedal, apelike primate. Note the lack of a tail, an ape characteristic.

238 | CHAPTER 9 Primate Origins and Evolution: The First 50 Million Years

primate, weighing an estimated 30–35 kg (66–77 lb); but it had a tiny brain. Its relatively long arms indicate that it was adept at some form of suspensory locomo- tion, similar to that of a modern gibbon. Some of its hand adaptations foreshadow developments in hominin evolution.

CLIMATE SHIFTS AND HABITAT CHANGES During the period in which Oreopithecus and other later Miocene apes disappeared, Europe, Asia, and Africa experienced dramatic changes in climate and ecology. Several factors coincided to cause these changes: a shift in tectonic plates created the Alps, the Himalayas, and the East African mountain chains; ocean currents shifted; and the polar ice caps began to reform. In Europe and then Africa, the once- lush tropical forests changed to cooler, dryer mixed woodlands and grass- lands. As a result, tropical foods disappeared, including the apes’ favored diet, fruit. In Asia, a decrease in rainfall, reduced forests, and decreased fruit availability likely contributed to the extinction of Sivapithecus.

MIOCENE APE SURVIVORS GIVE RISE TO MODERN APES A handful of ape taxa survived these dramatic disruptions in habitat. Khoratpithe- cus, for example, thrived for a time and gave rise to the orangutan of southeast Asia. The origins of the great apes of Africa and hominins are far less clear. In fact, only one small set of fossils— named Chororapithecus by their discoverer, the Japanese paleoanthropologist Gen Suwa— resembles similar parts of living great apes. These nine teeth from three individuals, found in Ethiopia and dating to about 10.5 mya, are remarkably similar to the modern gorilla’s. Their existence suggests that late Miocene African pongids may have been the common ancestor of African apes and hominins. However, the fossil record in Africa between 13 mya and 5 mya is extremely sparse, leaving an 8- million- year gap until the first hominins’ appear- ance, about 6 mya (discussed further in chapter 10). Therefore, the link between late Miocene African apes and later hominoids is unknown.

Apes Return to Africa? Ape fossils from the late Miocene might be so scarce in East Africa because apes simply were not living there, at least not in great numbers, at that time. Unless the fossil record changes, somewhere other than Africa must be the source of living African apes’ and humans’ common ancestor. The Canadian primate paleontologist David Begun suggests that late Miocene Europe might yield that ancestor. He spec- ulates that the similarities in dentition and skull between the Greek dryopithecid Ouranopithecus, on the one hand, and African apes and early hominins, on the other, indicate an ancestral- descendant relationship between European great apes and African hominins. Begun argues that the climate changes in Europe prompted late Miocene apes to move from Europe back to Africa, essentially following the tropical forests, and the foods these forests provided, as forests and foods disappeared behind them. Some of the pongids adapted to forested settings, some lived in woodlands, and eventually one group, hominins, became committed to life on the ground. To date, the fossil record for the later Miocene is too incomplete to make clear whether early hominins descended from Miocene ancestry in Europe or in Africa.

Tuscany

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Ouranopithecus A genus of Miocene dryo- pithecids found in Greece.

Monkeys on the Move | 239

Monkeys on the Move At the same time as the evolution and proliferation of ape taxa, an expansion and adaptive radiation of monkeys occurred, both in the New World and in the Old World. Primates recognizable as cercopithecoids— they have the distinctive

The First Apes: A Remarkable Radiation

The apes’ evolutionary glory days are in the Miocene epoch (23–5.3 mya), beginning in Africa and then spreading into Europe and Asia. Out of this remarkable adaptive radiation came the ancestors of living apes and of humans. All of these fossil primates had characteristics seen in living apes, especially in the teeth and the skull ( Y- 5 lower molars, 2/1/2/3 dental formula, broad incisors, large honing canines), but most were monkeylike in the postcranial skeleton (front and back limbs equally long).

Group Characteristics Age Location

Proconsulids Large range in size Tropics to open woodlands Thin enamel (e.g., Proconsul)

22–17 mya Africa (Kenya, Uganda)

Dryopithecids Some size range Tropics Thin enamel (e.g., Dryopithecus)

14–9 mya Europe (France, Spain, Germany, Greece, elsewhere)

Sivapithecids Some size range Tropics Thick enamel Skull like orangutan’s (e.g., Sivapithecus)

14–8 mya Asia (Pakistan, India, China, Thailand)

Oreopithecids Large body Tiny brain Specialized molars for eating leaves Suspensory locomotion (e.g., Oreopithecus)

9–7 mya Europe (Italy), earlier form in East Africa (Kenya)

C O N C E P T C H E C K !

240 | CHAPTER 9 Primate Origins and Evolution: The First 50 Million Years

bilophodont molars of Old World monkeys— first appeared during the early Mio- cene in North Africa and East Africa. These primitive primates are generally called victoriapithecids. Victoriapithecus, a prominent genus of the group, is just the kind of primate that would be expected for the ancestor of Old World monkeys.

Beginning in the late Miocene, especially in the Pliocene and Pleistocene, and continuing to the present day, monkey taxa have proliferated enormously. While ape species were far more prevalent and diverse during the early and mid- dle Miocene, far outnumbering the living groups, monkey species are far more diverse since the end of the Miocene. Today’s monkey taxa are for the most part the descendants of the fossil species from the Pliocene and Pleistocene. By con- trast, most of the ape and apelike taxa from the Miocene went extinct and left no descendants.

The rise in monkey species and the decline in ape species were not due to com- petition between the two groups. Rather, the origin and diversification of monkeys reflect habitat changes. The climates and environments of the early Miocene seem to have favored the adaptive radiation of apes, with most taxa then going extinct as climates and environments changed. The climates and environments of the late Miocene, and into the Pliocene and Pleistocene, seem to have favored the adaptive radiation of monkeys.

The Pliocene and Pleistocene fossil monkeys are divided into the same two subfamilies as Old World monkeys, cercopithecines and colobines. The cercopi- thecines are represented by three major groups: macaques; mangabeys, baboons, and geladas; and guenons. The fossil monkeys were widespread, as living species of monkeys are. The fossil monkeys and their living descendants are similar in many respects, such as skeletal and dental anatomy. For example, the fossil and living monkeys have virtually identical teeth (large, projecting canines) and cranial morphology.

Aegyptopithecus

Victoriapithecus

Proconsul Afropithecus

Lufengpithecus

Sivapithecus

Oreopithecus

Ouranopithecus

Australopithecus

Dryopithecus Chimpanzees

Humans Gorillas

Orangutans

Siamangs

G re

at a

pe s

Le ss

er a

pe s

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co pi

th ec

in es

C ol

ob in

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Gibbons

Asian macaques? Barbary macaques

Baboons and mangabeys Guenons

Langurs and proboscis monkeys

Colobus monkeys

Kenyapithecus

H om

in oi

ds O

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or ld

m on

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FIGURE 9.22 Catarrhine Origins This phylogeny represents catarrhine evolution. The numbers set in squares represent the estimated times of divergence. Balloons refer to approximate time ranges for fossil taxa. Old World monkeys and hominoids share a common ancestor; however, approximately 25 mya, Old World monkeys and hominoids split, each creating a separate evolutionary lineage. This last common ancestor, though, has not been discovered. Within the hominoid lineage, branching has occurred many times, including the branch leading to the lesser apes, around 18 mya, and most recently the branch leading to humans, approximately 8–9 mya. The Old World monkey lineage has also branched several times, most notably when colobines and cercopithecines split, approximately 14 mya.

victoriapithecids Miocene primates from Africa, possibly ancestral to Old World monkeys.

241

Some of the Pliocene and Pleistocene monkeys were quite large. For example, Theropithecus oswaldi, one of the best- known fossil species of Old World monkeys from East, North, and South Africa in both the Pliocene and the Pleistocene, may have weighed as much as 80 kg (176 lb), the weight of a modern female gorilla. Males had enormous canines and would have been avoided by early hominins because they were so dangerous.

The colobines included three geographic groups of species: European, Asian, and African. These species differed in many ways from their living descendants, in part reflecting their greater geographic distribution and the diverse environments they occupied. One clear evolutionary trend in many monkey species is a decrease in body size. In other words, around the world during the later Pleistocene there were widespread extinctions of large animals, including primates. These extinc- tions might have been caused by human hunting, climate change, competition with other mammals, or a combination of these factors (discussed further in chapter 13).

All of primate evolution is a dynamic story, peaking at different times and different places with key events, such as the origins of all the major groups of higher primates (Figure  9.22). The record becomes even more fascinating in the late Miocene, with the appearance of a new primate that is similar to but different from other primates. The first 50  million years of primate evolution, from the beginning of the Eocene to the last several million years of the Miocene, set the stage for the appearance of this new taxa— a primitive, humanlike primate. This ancestor’s origin begins the 7- million- year history of the appearance, rise, and dominance of humans. That story begins in the next chapter.

Theropithecus A genus of fossil and living Old World monkeys found in Africa; it was more diverse in the past than it is today and was one of the first monkey genera to appear in the evolutionary record.

A N S W E R I N G T H E B I G Q U E S T I O N S

C H A P T E R   9 R E V I E W [INSERT INQUIZITIVE LOGO/TEXT HERE]

Why become a primate? • According to the predominant theory, primate origins

represent the radiation of a primitive mammalian ancestor that adapted to life in the trees. Other theories suggest that the origins may be more closely linked to preying on insects or eating fruit.

What were the first primates? • The first radiation of primates included the

appearance of two primitive primate groups: adapids and omomyids, both at about 55 mya. These animals may have given rise to modern strepsirhines and modern haplorhines, but the exact phylogenetic

relationship between the Eocene groups and later ones is unknown.

What were the first higher primates? • In the Eocene, primate taxa possessing a combination

of strepsirhine and haplorhine characteristics appeared in Asia and Africa. These basal anthropoids may have been the first anthropoids.

• Recognizable catarrhines (e.g., Aegyptopithecus) were present 30 mya in Africa, and platyrrhines (e.g., Branisella) were present 26 mya in South America. Platyrrhines likely descended from an early African anthropoid ancestor.

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What evolutionary developments link past primate species and living ones? • The evolution of apes began in Africa and continued

in Europe and Asia. Recognizable African apes first appeared about 22 mya (e.g., Proconsul) and various Eurasian varieties (e.g., Sivapithecus) somewhat later with the opening of a land bridge connecting

these continents. Most apes went extinct in the later Miocene, although a few survived, giving rise to modern apes and humans.

• Monkeys underwent a massive adaptive radiation in the Pliocene and Pleistocene, providing the foundation for the evolution of modern species.

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K E Y T E R M S adapids Adapis Aegyptopithecus angiosperm radiation hypothesis arboreal hypothesis basal anthropoids Biretia Branisella Carpolestes dryopithecids Dryopithecus Eosimias

euprimates Gigantopithecus Khoratpithecus Micropithecus Notharctus oligopithecids omomyids oreopithecids Oreopithecus Ouranopithecus parapithecids Parapithecus

plesiadapiforms Proconsul proconsulids propliopithecids Propliopithecus Proprimates Saadanius sivapithecids Sivapithecus Theropithecus victoriapithecids visual predation hypothesis

E V O L U T I O N R E V I E W Primate Social Organization and Behavior: The Deep Roots of the Order Primates

Synopsis The origin of our own taxonomic order, the order Primates, extends over 50  million years into the past. Various hypotheses— based on characteristics seen in both living and extinct primates, such as arboreal adaptations and visual acuity— have been proposed to explain why the first true primates arose deep in the past. The evolutionary history of the order Primates can be described as somewhat tumultuous. Fluctuations in climate and other environmental pressures during the Eocene, Oligocene, and Miocene epochs affected the survival and adaptive radiations of various fossil primate taxa to differing degrees. Fossils of primate ancestors are found across Africa, Asia, and Europe in the Old World as well as North and South America in the New World. The locations and characteristics of these fossils clarify the timeline

of major evolutionary events that shaped the order Primates and illustrate that the geographic extent of primates in the past was much larger than the distribution of nonhuman primate species living today.

Q1. Describe the three hypotheses for explaining primate origins, discussed at the beginning of this chapter. Do you think the environmental pressures associated with each of these hypotheses are mutually exclusive, or could all of these factors have influenced the origins and adaptability of the earliest primates?

Q2. Identify the four alternative hypotheses for explaining the pres- ence of primates in South America. Summarize the evidence

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that supports each of these four hypotheses. Based on this evidence, assess how plausible each hypothesis is in explain- ing the origins of the New World primates.

Q3. Explain the role of climate fluctuations in the origins and evo- lution of the first true primates, the earliest anthropoids, the early Miocene “dental apes” (proconsulids), and the surviving ape species of the late Miocene.

Hint Focus on the ways that warming and cooling episodes affected habitable land areas, caused habitat changes, and affected availability of different food sources.

Q4 . There is much less diversity among living ape species than among the many fossil ape taxa of the early and mid- Miocene. In contrast, there is much greater diversity among living

monkey species than among the fossil monkey taxa of the late Miocene. Discuss the kinds of selective pressures operating in the late Miocene, Pliocene, and Pleistocene that favored an adaptive radiation of monkeys and contributed to decreased diversity among apes.

Q5. A bumper sticker reads, “If humans evolved from monkeys, then why are there still monkeys?” Using your knowledge of biological evolution in general, and the timeline of primate origins and evolution outlined in this chapter more specifically, counter the faulty logic behind this bumper sticker.

Hint See Figure 9.22 for a timeline of the key events in pri- mate evolution.

A D D I T I O N A L R E A D I N G S

Beard,  C.  2004. The Hunt for the Dawn Monkey: Unearthing the Origins of Monkeys, Apes, and Humans. Berkeley: University of California Press.

Begun, D. R. 2003. Planet of the apes. Scientific American 289(2): 74–83.

Conroy, G. C. 1990. Primate Evolution. New York: Norton.

Fleagle, J. G. 2013. Primate Adaptation and Evolution. 3rd ed. San Diego: Academic Press.

Miller, E. R., G. F. Gunnell, and R. D. Martin. 2005. Deep time and the search for anthropoid origins. Yearbook of Physical Anthropol- ogy 48: 60–95.

Rose, K. D. 1994. The earliest primates. Evolutionary Anthropology 3: 159–173.

Ross, C. F. 2000. Into the light: the origin of Anthropoidea. Annual Review of Anthropology 29: 147–194.

Walker,  A.  and  P.  Shipman. 2005. The Ape in the Tree: An Intel- lectual and Natural History of Proconsul. Cambridge, MA: Belknap Press.

OFTEN REFERRED TO AS the “cradle of humankind,” Olduvai Gorge is a ravine in East Africa’s Great Rift Valley from which many hominin fossils have been recovered, providing insight into our evolutionary roots. Geologic activ- ity and erosion have exposed some of the deepest and oldest layers of sedi- ment, enabling paleoanthropologists to find fossils from strata that are nearly 2 million years old.

TA N Z A N I A

Olduvai Gorge

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10 What is a hominin?

Why did hominins evolve from an apelike primate?

What were the first hominins?

What was the evolutionary fate of the first hominins?

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Early Hominin Origins and Evolution The Roots of Humanity

I magine yourself walking across the hot, desolate, and altogether inhospitable land-scape of East Africa’s Great Rift Valley. Imagine further that you have spent the better part of the last three decades— all your adult life— searching for early hominin fossils. Over those years, you have found evidence, such as stone tools, that early humans had lived in this place hundreds of thousands— even millions— of years ago. Still no fossils; none worth getting especially excited about. On this particular day, you see part of a bone sticking out of the ground, just like others you have seen over and over before. This one turns out to be different, though. Instead of being an animal of some sort, this fossil has human teeth— you have found a hominin, your first! In an instant, all your searching has been vindicated.

That scene describes exactly what happened to the English- born anthropologist Mary Leakey (1913–1996) one sunny morning in July  1959 (Figure 10.1). She, along with her husband, the Kenyan anthropologist Louis Leakey (1903–1972), had searched high and low for early human bones in Olduvai Gorge, a side branch of the Rift Valley, 50 km (31 mi) long. Since beginning their searches in the early 1930s, they had found ancient stone tools and ancient animal remains scattered about the landscape— lots of them. They wanted more, however. They wanted the remains of the people who had made the tools and had eaten the animals. Year after year, field season after field sea- son, disappointment after disappointment, they searched for the bones and teeth that would represent our ancestors’ roots.

What had motivated these two individuals to work so hard for so little payoff under such awful conditions? Simple. They were motivated by questions. In fact, the Leakeys

B I G Q U E S T I O N S ?

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were asking one of the fundamental questions of all time: Who were the first humans? The Leakeys demanded answers about human origins, and they were willing to do what had to be done to get those answers.

They started out with a pretty simple hunch about early hominins. Other sci- entists had found things in Olduvai Gorge— bones and tools, both in association with really old geologic strata— that strongly suggested the place would yield early hominin remains. Based on these findings, the Leakeys decided to investigate the gorge’s geologic strata (Figure 10.2). Their work took a lot of time and resources, but it paid off well, laying the essential groundwork for our present understanding of the first humans and their place in evolution. In fact, the bits of bone and the teeth found in 1959 turned out to be a crucially important hominin skull. Not only did this discovery expand the territory in which early hominins were known to have lived— at that point, they were known just from South Africa— but it added a whole new dimen- sion to their variability and geographical distribution. The Leakeys’ pioneering work in East Africa was built around questions still central to paleoanthropology.

This chapter focuses on the fossil record of early human evolution. This record sheds light on the earliest humanlike ancestors. In order of origin and evolution, they are the pre- australopithecines (before the genus Australopithecus), which lived 7–4 mya, and the australopithecines, which lived 4–1 mya.

What Is a Hominin? The morphological characteristics— and behaviors inferred from these characteristics— shared by living humans and their ancestors but not shared by apes reveal what is distinctive about hominins. For example, living humans speak, use

FIGURE 10.1 Mary and Louis Leakey This husband- and- wife team conducted some of the earliest excavations in Olduvai Gorge.

What Is a Hominin? | 247

language, depend fully on complex material culture, and have advanced cognition— living apes do not have these characteristics. Speech, advanced cognition, and complex material culture evolved in the human line long after the first hominins appeared in Africa, 7–6 mya, so these characteristics do not define a hominin. Speech likely developed only in the last 2 million years, and some authorities argue for late in that period. Evidence for material culture, in the form of primitive stone tools, dates to about 2.6 mya. As discussed in chapter 1, a hominin is much better understood as having two obligate behaviors— bipedal locomotion and nonhoning chewing— and the suite of associated physical characteristics that manifest these behaviors. The evidence is very clear: bipedal locomotion and nonhoning chewing preceded speech and material culture by several million years. Like large brains, speech and material culture help define humans today but were not attributes of the earliest hominins.

Present-day surface

Naisuisiu

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OH 13

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OH 24 OH 8

OH 10

OH 7

OH 20

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FIGURE 10.2 Geologic Strata at Olduvai One key aspect of excavations at Olduvai is the exposed strata, dating back millions of years. The strata include volcanic rock, which can be radiometrically dated to provide accurate ages for each layer. Any fossils found in these layers can then be dated according to the stratum in which they were found. The ages of fossil hominins recovered from Olduvai Gorge help anthropologists reconstruct humans’ family tree.

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BIPEDAL LOCOMOTION: GETTING AROUND ON TWO FEET In the 1800s, when the entire human fossil record was a very small fraction of what it is today, numerous authorities believed that the beginning of bipedalism was not the hallmark event distinguishing humans from apes. Rather, these scientists believed that the most important initial evolutionary change was an increase in brain size, reflecting advanced (human) intelligence. They speculated that only with advanced intelligence would language, tool use, and the other behaviors that collectively define humanness have become possible. The focus on intelligence to the exclusion of other attributes helped bring about the rapid and uncritical acceptance of some purported early hominin ancestors that later turned out to be fake.

Since then, the large early hominin fossil record has proven that bipedalism— and not human intelligence— was the foundational behavior of the Hominini, preceding most attributes associated with humans and with human behavior by millions of years. More than any other characteristic, the shift from walking with and running with four limbs (arms and legs) to walking with and running with two  limbs (legs) distinguishes hominins from the apes (and other nonhuman primates).

Seven distinguishing characteristics in the skeleton are associated with bipedal- ism (Figure 10.3; see also “What Is a Primate?” in chapter 6): the foramen magnum is positioned on the bottom of the skull, the spine is S- shaped, the ilium is short from front to back, the legs are long relative to the body trunk and arms, the knees are angled inward, the foot has a longitudinal arch, and the big toe (hallux) is not opposable. The position of the foramen magnum reflects the fact that the (bipedal) hominin carries its head atop its body, in contrast to the (quadrupedal) ape, which carries its head on the front of the body. The shortened ilium and pelvis generally reflect anatomical changes that coincided with the shift from quadrupedalism to bipedalism. Especially important is the reconfiguring of the gluteal muscles for stabilizing the hip in walking on two legs. Bipeds have distinctively long legs, which provide the ability to stride and to do so with minimal energy. The angling of the knees toward the midline of the body helps to place the feet below the body’s center of gravity, thereby helping stabilize the biped when standing, walking, or running. The loss of opposability in the big toe reflects the use of this digit in helping pro- pel the body forward during walking and running. The longitudinal arch acts as a kind of shock absorber, allowing the foot to sustain the demanding forces of body weight, especially during running and long- distance walking.

NONHONING CHEWING: NO SLICING, MAINLY GRINDING The second of the two major differences between living apes and humans (and human ancestors), a characteristic that defines the Homininae, is the way the dentition processes food (again, see “What Is a Primate?” in chapter 6). Apes and humans have evolved different dental characteristics, reflecting how each uses the canine and postcanine teeth (Figure 10.4). When apes grab on to food with their front teeth, the upper canines and lower third premolars cut and shred the food. Through evolution, apes’ upper canines have become large, pointed, and project- ing, with a sharp edge on the back. When the jaws are fully closed, each canine fits snugly in the diastema, the gap located between the canine and the third premolar

Position of the foramen magnum: In humans, the foramen magnum is on the bottom of the skull, closer to the teeth. In apes, the foramen magnum is in a posterior position. This difference reflects the fact that the human head sits on top of the body trunk, whereas the ape head sits on the front of the trunk.

Shape of the spine: In humans, the spine has an S-shape. In apes, it is straighter, almost C-shaped. The distinctive S-shape in humans is created by the concave curvature of the thoracic vertebrae, in front, and the concave curvature of the lumbar vertebrae, in the back. This arrangement, especially of the lumbar vertebrae, serves to position the body trunk’s center of gravity above the pelvis, providing more stability during walking and running.

Shape of the pelvis: The human pelvis has a very different shape from the ape pelvis. Especially distinctive is the short ilium in the bipedal human. This morphology is an essential element of the stability of the pelvis during standing, walking, and running (discussed further in chapter 6).

Length of the leg: The relatively long leg of the bipedal human provides increased efficiency during stride. In hominins, the leg is generally longer relative to the arm than it is in apes. The long arm of the ape reflects its suspensory use in trees.

Valgus knee: The knees in the biped angle inward to give it a knock-kneed appearance. The angle formed by the long axis of the femur shaft and the horizontal at the knee—called the bicondylar angle—provides an angle greater than 90 degrees. This angle is significantly greater than 90 degrees in humans than in most apes. The valgus knees place the feet together and beneath the center of gravity. By doing so, they provide stability in walking and running, especially when only one foot is on the ground during locomotion.

Longitudinal foot arch: The biped has a distinctive arch that runs from the front to the back of the bottom surface of the foot. This form gives increased leverage as the body pushes forward and serves as a shock absorber when the feet make contact with the ground during walking and running. Apes have flat feet, which reflect the adaptation of their feet for grasping.

Opposable big toe: The first digit of the foot—the big toe—is opposable in apes but not in humans. This difference reflects the function of the foot, which is solely (pun intended!) to support the body during walking and running in humans. The ape toe has a dual function, including terrestrial walking and grasping or manipulating objects. Humans have largely lost their ability to manipulate objects with their toes.

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FIGURE 10.3 Seven Steps of Bipedality This figure shows the seven key differences between a bipedal hominin and a quadrupedal pongid. The two skeletons are of a modern human and a modern gorilla. They are similar in overall form, reflecting their common ancestry. However, because the human is a biped and the gorilla is a quadruped, they have important anatomical differences. Anthropologists use these differences to identify patterns in fossils and to reconstruct their respective locomotor and related behavioral patterns.

Imagine yourself as a physical anthropologist who has just unearthed in East Africa a fossil skeleton of a hominoid dating to 4 or 5 mya. In examining your newly discovered skeleton, you would want to pay attention to these seven features. But you would need to be prepared for surprises, which you might encounter if your specimen is closer or further away from the nearest ancestor of apes and humans.

FIGURE 10.4 Nonhoning vs. Honing Chewing While humans have nonhoning chewing, primates such as gorillas (pictured here) have a honing complex, in which their very large canines cut food. The upper canines are sharpened against the lower third premolars.

BIPEDAL LOCOMOTION: GETTING AROUND ON TWO FEET In the 1800s, when the entire human fossil record was a very small fraction of what it is today, numerous authorities believed that the beginning of bipedalism was not the hallmark event distinguishing humans from apes. Rather, these scientists believed that the most important initial evolutionary change was an increase in brain size, reflecting advanced (human) intelligence. They speculated that only with advanced intelligence would language, tool use, and the other behaviors that collectively define humanness have become possible. The focus on intelligence to the exclusion of other attributes helped bring about the rapid and uncritical acceptance of some purported early hominin ancestors that later turned out to be fake.

Since then, the large early hominin fossil record has proven that bipedalism— and not human intelligence— was the foundational behavior of the Hominini, preceding most attributes associated with humans and with human behavior by millions of years. More than any other characteristic, the shift from walking with and running with four limbs (arms and legs) to walking with and running with two  limbs (legs) distinguishes hominins from the apes (and other nonhuman primates).

Seven distinguishing characteristics in the skeleton are associated with bipedal- ism (Figure 10.3; see also “What Is a Primate?” in chapter 6): the foramen magnum is positioned on the bottom of the skull, the spine is S- shaped, the ilium is short from front to back, the legs are long relative to the body trunk and arms, the knees are angled inward, the foot has a longitudinal arch, and the big toe (hallux) is not opposable. The position of the foramen magnum reflects the fact that the (bipedal) hominin carries its head atop its body, in contrast to the (quadrupedal) ape, which carries its head on the front of the body. The shortened ilium and pelvis generally reflect anatomical changes that coincided with the shift from quadrupedalism to bipedalism. Especially important is the reconfiguring of the gluteal muscles for stabilizing the hip in walking on two legs. Bipeds have distinctively long legs, which provide the ability to stride and to do so with minimal energy. The angling of the knees toward the midline of the body helps to place the feet below the body’s center of gravity, thereby helping stabilize the biped when standing, walking, or running. The loss of opposability in the big toe reflects the use of this digit in helping pro- pel the body forward during walking and running. The longitudinal arch acts as a kind of shock absorber, allowing the foot to sustain the demanding forces of body weight, especially during running and long- distance walking.

NONHONING CHEWING: NO SLICING, MAINLY GRINDING The second of the two major differences between living apes and humans (and human ancestors), a characteristic that defines the Homininae, is the way the dentition processes food (again, see “What Is a Primate?” in chapter 6). Apes and humans have evolved different dental characteristics, reflecting how each uses the canine and postcanine teeth (Figure 10.4). When apes grab on to food with their front teeth, the upper canines and lower third premolars cut and shred the food. Through evolution, apes’ upper canines have become large, pointed, and project- ing, with a sharp edge on the back. When the jaws are fully closed, each canine fits snugly in the diastema, the gap located between the canine and the third premolar

Position of the foramen magnum: In humans, the foramen magnum is on the bottom of the skull, closer to the teeth. In apes, the foramen magnum is in a posterior position. This difference reflects the fact that the human head sits on top of the body trunk, whereas the ape head sits on the front of the trunk.

Shape of the spine: In humans, the spine has an S-shape. In apes, it is straighter, almost C-shaped. The distinctive S-shape in humans is created by the concave curvature of the thoracic vertebrae, in front, and the concave curvature of the lumbar vertebrae, in the back. This arrangement, especially of the lumbar vertebrae, serves to position the body trunk’s center of gravity above the pelvis, providing more stability during walking and running.

Shape of the pelvis: The human pelvis has a very different shape from the ape pelvis. Especially distinctive is the short ilium in the bipedal human. This morphology is an essential element of the stability of the pelvis during standing, walking, and running (discussed further in chapter 6).

Length of the leg: The relatively long leg of the bipedal human provides increased efficiency during stride. In hominins, the leg is generally longer relative to the arm than it is in apes. The long arm of the ape reflects its suspensory use in trees.

Valgus knee: The knees in the biped angle inward to give it a knock-kneed appearance. The angle formed by the long axis of the femur shaft and the horizontal at the knee—called the bicondylar angle—provides an angle greater than 90 degrees. This angle is significantly greater than 90 degrees in humans than in most apes. The valgus knees place the feet together and beneath the center of gravity. By doing so, they provide stability in walking and running, especially when only one foot is on the ground during locomotion.

Longitudinal foot arch: The biped has a distinctive arch that runs from the front to the back of the bottom surface of the foot. This form gives increased leverage as the body pushes forward and serves as a shock absorber when the feet make contact with the ground during walking and running. Apes have flat feet, which reflect the adaptation of their feet for grasping.

Opposable big toe: The first digit of the foot—the big toe—is opposable in apes but not in humans. This difference reflects the function of the foot, which is solely (pun intended!) to support the body during walking and running in humans. The ape toe has a dual function, including terrestrial walking and grasping or manipulating objects. Humans have largely lost their ability to manipulate objects with their toes.

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FIGURE 10.3 Seven Steps of Bipedality This figure shows the seven key differences between a bipedal hominin and a quadrupedal pongid. The two skeletons are of a modern human and a modern gorilla. They are similar in overall form, reflecting their common ancestry. However, because the human is a biped and the gorilla is a quadruped, they have important anatomical differences. Anthropologists use these differences to identify patterns in fossils and to reconstruct their respective locomotor and related behavioral patterns.

Imagine yourself as a physical anthropologist who has just unearthed in East Africa a fossil skeleton of a hominoid dating to 4 or 5 mya. In examining your newly discovered skeleton, you would want to pay attention to these seven features. But you would need to be prepared for surprises, which you might encounter if your specimen is closer or further away from the nearest ancestor of apes and humans.

FIGURE 10.4 Nonhoning vs. Honing Chewing While humans have nonhoning chewing, primates such as gorillas (pictured here) have a honing complex, in which their very large canines cut food. The upper canines are sharpened against the lower third premolars.

250 | CHAPTER 10 Early Hominin Origins and Evolution: The Roots of Humanity

on the lower jaw and the canine and the second incisor on the upper jaw. The sharp edge on the back of the upper canine hones, or rubs against, a sharp edge on the front of the lower third premolar, or sectorial premolar. This honing action helps maintain a sharp, shearing edge on both the canine and the premolar. The shearing edge is essential for slicing up leaves and fruit before they are chewed by the back teeth and swallowed. Apes’ lower third premolar is also distinctive in having one large, dominant cusp on the cheek side of the tooth and a tiny cusp on the tongue side of the tooth.

In contrast, living and past hominins have small, blunt, and nonprojecting canines and no diastema. Hominin canines wear on the tips instead of the backs (Figure 10.5). The cusps on both sides of the lower third premolars are similar in size, or at least more similar in size than are apes’ cusps. Unlike apes, hominins do not hone their canines as they chew.

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FIGURE 10.5 Canine Wear (a) This gorilla’s dentition reveals honing wear on the back of the upper canine, caused by the tooth’s rubbing against the lower third premolar. (b) This human’s dentition reveals wear on the upper canine’s tip, which is the point of contact between the upper canine and the lower teeth when the jaws are closed.

(a) (b)

M. temporalis

M. masseter

GorillaHuman

FIGURE 10.6 Masticatory Muscles Humans and other primates have powerful chewing muscles to process food. In humans, the temporalis muscle is vertically oriented, enabling a crushing ability. In nonhuman primates, this muscle is oriented horizontally, producing slicing motions.

Why Did Hominins Emerge? | 251

Apes’ and humans’ postcanine teeth have many similar anatomical charac- teristics. The third and fourth premolars, upper and lower, have two cusps each. Apes’ and hominins’ upper molars have four cusps, and their lower molars have five cusps. Apes’ and humans’ back teeth crush and slice food, with a different emphasis: humans crush food more than apes do. Apes use their molars more for slicing than crushing, reflecting their plant- heavy diet.

In apes and humans, grinding and slicing are facilitated by powerful chewing, or masticatory, muscles, especially the temporalis, masseter, and pterygoid muscles (Figure 10.6). Hominins place more emphasis on the front portion of these mus- cles, to provide greater vertical force in crushing food. Apes place more emphasis on the back portion of the masticatory muscles because slicing requires more horizontally oriented forces. As an additional aid in powerful crushing, hominins have evolved thick enamel on their teeth (Figure 10.7). Living apes have evolved thin enamel, reflecting diets dominated by plants and soft fruit. Among the hom- inoids, the only exception is the orangutan, which has evolved thick enamel— its diet includes tough foods that require heavy crushing.

Like bipedalism, hominins’ nonhoning masticatory complex developed very early in the evolutionary record. Collectively, then, the distinguishing features of the Homininae are located in the anatomical complexes associated with acquiring and transporting food (locomotion) and chewing food (mastication).

Why Did Hominins Emerge? The fossil record and genetic information continue to fill in the story of hominins’ first appearance on the scene, in the late Miocene epoch, some 5.3–10 mya. But why did hominins evolve? Central to most arguments is bipedalism, the focal point in the study of human origins.

CHARLES DARWIN’S HUNTING HYPOTHESIS Charles Darwin offered the first serious hypothesis about the first appearance of hominins. It was a simple but elegant adaptive model for explaining human origins. Drawing on the great British naturalist Thomas Huxley’s anatomical research on

(a) (b)

Thick enamel Thin enamel

FIGURE 10.7 Enamel Thickness Enamel is the outermost layer of the exposed part of a tooth and is the hardest substance in the human body, enabling the tooth to grind and slice all types of food. Species with diets heavy in hard foods, such as seeds and nuts, have thicker enamel, allowing more of the enamel to be eroded or worn before the softer layers underneath are exposed. In these cross sections of (a) a human tooth and (b) a chimpanzee tooth, note how much thicker the human enamel is.

252 | CHAPTER 10 Early Hominin Origins and Evolution: The Roots of Humanity

the living apes of Africa (both Darwin and Huxley are discussed in chapter  2), Darwin concluded that because of the remarkable anatomical similarity between humans and African apes, Africa was hominins’ likely place of origin. The charac- teristics that distinguish living humans from living apes, Darwin reasoned, derive from one key evolutionary event in their common ancestor, namely, the shift from life in the trees to life on the ground. He observed four characteristics that set living humans and living apes apart: (1) humans are bipedal, while apes are qua- drupedal; (2) humans have tiny canines, while apes have large canines; (3) humans rely on tools in their adaptation, while apes do not; and (4) humans have big brains, while apes have small brains (Figure 10.8).

Building on these observations, Darwin asked what the advantages of biped- alism would be in a world where bipeds— early humans— ate mostly meat they acquired by killing animals with weapons. He concluded that bipedalism had freed the hands for carrying the weapons. To manufacture and use these tools, the early humans needed great intelligence. Once they had the tools, they did not need the big canines for hunting or for defense. Although he saw tool production and tool use as essential factors in the development of human intelligence, Darwin believed that humans’ large brain resulted mainly from the presence of language in humans.

Scientists now know that tool use and the increase in brain size began well after the appearance of bipedalism and the reduction in canine size. The earliest known tools date to about 2.6 mya, and evidence of brain expansion dates to sometime

What Makes a Hominin a Hominin?

Hominins have a number of anatomical characteristics that reflect two fundamental behaviors: bipedal locomotion and nonhoning chewing.

Behavior Anatomical Characteristics

Bipedalism Foramen magnum on the bottom of the skull S- shaped spine Short pelvis from front to back Long legs Knees angled toward midline of the body Double- arched foot, including a well- developed longitudinal arch Nonopposable big toe

Nonhoning chewing Blunt, nonprojecting canine Small canine relative to size of other teeth No diastema Wear on tips of canines and of third premolars Cusps on lower third premolar equal size

C O N C E P T C H E C K !

Why Did Hominins Emerge? | 253

after 2 mya. Therefore, it now seems doubtful that canine reduction began with tool use. Although Darwin’s hypothesis was refuted, it provided an essential first step toward an understanding of hominin origins.

Since Darwin, other hypotheses have emerged to answer the question of why there are hominins. After 17 mya, a massive adaptive diversification of apes occurred in Africa, resulting in many different taxa (see “Apes Begin in Africa and Dominate the Miocene Primate World” in chapter  9). At some point later,

Darwin’s Model for the Shift from Life in the Trees to Life on the Ground: Human Origins

Large canines

Bipedal

Small canines

No tool use? Tool use

Small brain

Large brain

Ancestral Ape Ancestral Human

Quadrupedal

FIGURE 10.8 Four Key Differences From Huxley’s comparative studies of apes and humans, Darwin noted four differences between these two types of primates. In Darwin’s time, there were no recorded instances of apes’ making or using tools, so tools appeared a uniquely human phenomenon. Since then, however, apes have been seen making and using tools, such as when chimpanzees “fish” for termites with a rod and crack hard nuts with a “hammer and anvil” (see “Acquiring Resources and Transmitting Knowledge: Got Culture?” in chapter 7).

254 | CHAPTER 10 Early Hominin Origins and Evolution: The Roots of Humanity

this diversity declined, perhaps due in part to competition between apes and to the rising number of monkey species that were also evolving in the late Miocene epoch. Changes in climate and in habitat also likely influenced the decline in the number of ape taxa. Most important about the evolution of Miocene apes is that somewhere out of this ancestral group of ape species arose the animal that was more human than ape.

Darwin proposed that hunting was at the basis of the divergence. However, the archaeological record suggests that hunting began much later in human evolution. Hunting, at least in the sense of cooperation among individuals to kill an animal, likely did not begin until after 2 mya, at about the same time the brain began expanding. It now seems likely that hunting played an important role in later human evolution but not in hominin origins.

PETER RODMAN AND HENRY MCHENRY’S PATCHY FOREST HYPOTHESIS The American anthropologists Peter Rodman and Henry McHenry have proposed that human origins and bipedality in particular may be related to the greater efficiency, in certain habitats, of walking on two feet rather than four feet. They suggest that bipedalism arose in areas where the forest was becoming fragmented, a process that began toward the end of the Miocene (Figure 10.9). Apes’ quadru- pedalism, they note, is not energy- efficient in Africa’s patchy forests. As the forests became patchy and food became more dispersed, early hominins would have used their energy much more efficiently once bipedalism freed their hands to pick up food. The early hominins could then have fed in trees and on the ground, depend- ing on the availability of resources.

OWEN LOVEJOY’S PROVISIONING HYPOTHESIS The American anthropologist Owen Lovejoy has offered another alternative to Darwin’s ideas about the arboreal- to- terrestrial shift and the origins of bipedal- ism. He has hypothesized that freeing the early hominins’ hands was important in initiating bipedal locomotion but not for the reasons Darwin cited. Lovejoy observes that in many species of monkeys and apes, males compete for sexual access to females. However, the young are cared for by the mother without any involvement of the father (see “What Is a Primate?” in chapter 6). Owing to the obligations of caregiving, such as the acquisition of food for her infant (and herself ), the mother theoretically is not able to care for more than one infant at a time. Moreover, she is unreceptive to mating until the infant is able to find food on its own. In apes as in humans, the time from birth to the infant’s independence can be rather long, upward of five years in chimpanzees, for example. The downside of this extended care period is that it gives apes a reproductive disadvantage since so few offspring can be born to any female. Lovejoy hypothesizes that if infants and mothers were provided with more food, they would not have to move around as much for resources. If males provisioned mothers and their offspring, each mother, again theoretically, would be able to care for two or more infants at a time. In other words, the mother could have more births— the time between births would be reduced.

Lovejoy makes the case that, for early hominins, a monogamous father enhanced the survival of the mother and offspring by providing both food and

FIGURE 10.9 East African Tree Cover Around the time that humans and bipedality arose, East Africa had large amounts of discontinuous tree cover. Rodman and McHenry propose that the areas of open grassland, interspersed with some stands of trees, such as shown here, favored bipedalism over quadrupedalism.

Why Did Hominins Emerge? | 255

protection from predators. This habitual provisioning required the male to have free hands for carrying food, so bipedalism arose. This model focuses on the selective and simultaneous advantages of monogamy and of pair- bonding, of food provisioning, of cooperation, and of bipedalism, all rolled into one distinctively human behavioral package.

SEXUAL DIMORPHISM AND HUMAN BEHAVIOR Among all the hypotheses about hominin origins, Lovejoy’s hypothesis had a unique focus, on differences in female and male body sizes and on the implications of behavior with a decidedly human bent. Through field and laboratory studies, anthropologists have observed that, in terms of body size, many living primate species are highly dimorphic sexually: males are considerably larger than females. This difference has come about because the larger the male, the more equipped it will be to outcompete other males for sexual access to females. Through natural selection, then, males in many primate species have maintained relatively large bodies. Some authorities argue that early hominins were highly dimorphic, in which case competing males were likely not involved in caring for their offspring. However, if early hominins were not especially dimorphic, then male competition for mates probably was not part of early hominin social behavior. The American anthropologist Philip Reno and his associates have studied early hominin bones to determine relative sizes of females and of males. Their analysis shows relatively little sexual dimorphism in body size, especially in comparison with apes. Such reduced sexual dimorphism suggests that males were cooperative, not compet- itive. This cooperative behavior could have included pair- bonding— one male paired with one female— a behavior pattern necessary for the kind of provisioning required in Lovejoy’s hypothesis.

BIPEDALITY HAD ITS BENEFITS AND COSTS: AN EVOLUTIONARY TRADE- OFF All the hypotheses about human origins have suggested that an apelike primate evolved into an early hominin through completely positive adaptation. Bipedal- ism’s advantages over quadrupedalism included an increased ability to see greater distances (thanks to an upright posture), greater ease of transporting both food and children, ability to run long distances, and the freeing of the hands for, eventually, such remarkable skills and activities as tool manufacture and tool use. However, the profound adaptive shift to bipedalism had its costs. Standing upright yields a better view across the landscape, but it also brings exposure to predators. Standing or walking on two feet while simultaneously lifting or carrying heavy objects over long periods of time causes back injury, such as that associated with arthritis and with slipped intervertebral disks. Bipedality also places an enormous burden on the circulatory system as it moves blood from the legs to the heart. The result of this burden is the development of varicose veins, a condition in which overwork causes the veins to bulge. Lastly, if one of a biped’s two feet is injured, then that biped’s ability to walk can be severely reduced. Unable to move about the landscape, an early hominin would have had limited chances of surviving and of reproducing. In short, bipedality is a wonderful example of the trade- offs that occur in evolution. Only rarely do adaptive shifts, including one of the most fundamental human behaviors, come without some cost.

A F R I C A

East African Rift Zone

256 | CHAPTER 10 Early Hominin Origins and Evolution: The Roots of Humanity

What Were the First Hominins? Until the 1970s, the oldest hominin fossil dated to less than 4 mya. The earliest hominins were known from one genus, Australopithecus, found mostly in two key areas of Africa: in a series of limestone caves in South Africa and in sedimentary basins and associated river drainages in the Eastern Rift Valley (part of the Great Rift Valley) in Ethiopia, Kenya, and Tanzania (Figure  10.10). As we saw in the previous chapter, the latest African Miocene apes— the group of hominoids out of which the first hominins evolved— date to about 8 mya. Thus, the crucial time period during which hominins and the last common ancestor with apes (chimpan- zees) split into separate lineages has been an unknown because of the 4- million- year gap in the fossil record (8–4 mya). Subsequently, however, hominins predating Australopithecus have been discovered in north- central and eastern Africa. These hominins have closed the gap between late Miocene ape evolution and the first hominins, the pre- australopithecines.

THE PRE- AUSTRALOPITHECINES Pre- australopithecine fossils are few in number and quite fragmentary, but they have provided critically important information about the origins and earliest

HADAR Au. afarensis

BURTELE Au. species unknown

MIDDLE AWASH Au. afarensis Au. garhi Ar. kadabba Ar. ramidus

KONSO Au. boisei

OMO Au. afarensis Au. aethiopicus Au. boisei

KOOBI FORA Au. boisei Au. afarensis

ALLIA BAY Au. anamensis

TUGEN HILLS Orrorin tugenensis

OLDUVAI GORGE Au. boisei

LAETOLI Au. afarensis

MAKAPANSGAT Au. africanus

KROMDRAAI Au. robustus

DRIMOLEN Au. robustus

SWARTKRANS Au. robustus

STERKFONTEIN Au. africanus

TAUNG Australopithecus africanus

LOMEKWI Kenyanthropus platyops

WEST TURKANA Au. aethiopicus Au. boisei

TOROS-MENALLA Sahelanthropus tchadensis

KANAPOI Au. anamensis

FIGURE 10.10 African Hominins Many hominin fossils have been found in East Africa and South Africa.

What Were the First Hominins? | 257

evolution of the Hominini. The pre- australopithecines had a number of primitive attributes, and in some respects they were more apelike than humanlike. They represent the first recognizable ancestors of the lineage leading to humans.

SAHELANTHROPUS TCHADENSIS (7–6 MYA) The earliest pre- australo pithecine is represented by most of a skull and other fossils found in central Africa, begin- ning in 2001, by the French paleontologist Michel Brunet and his colleagues (Figure  10.11). Named Sahelanthropus tchadensis (meaning “genus named for the region of the southern Sahara Desert known as the Sahel”) by its discoverers, this creature’s fossils date to 7–6 mya. The finding’s geographic location— the Toros- Menalla locality of the Djurab Desert, in Chad— surprised many because it was  2,500  km (1,553 mi) from the Eastern Rift Valley, where all other early hominins in East Africa had been found for the last three- quarters of a century. The presence of early hominins in central Africa opens a third geographic “win- dow” onto their evolution, the first two being later presences in East Africa and South Africa. In short, humans originated in Africa during the late Miocene and early Pliocene.

Cranial capacity, a rough measure of brain volume, is one important quantita- tive characteristic with which anthropologists determine the degree of humanness in individual fossil hominins. The fossil record of human evolution shows an increase in brain size, from the smallest in the oldest hominins (about 350 cubic centimeters, or cc) to the largest in Homo sapiens (about 1,450 cc). Sahelanthropus had a brain size of about 350 cc.

Its brain was primitive and like that of apes. Moreover, this hominin had a massive browridge, larger than that of modern gorillas. However, the two critical attributes that define the Hominini are present in Sahelanthropus— the primate was likely bipedal (based on the position of the foramen magnum at the base of the skull) and the canine– premolar chewing complex was nonhoning. This combina- tion of primitive (more apelike) and derived (more humanlike) features is to be expected in the oldest hominin, especially in apes’ and humans’ common ancestor. Its great age and primitive characteristics indicate that Sahelanthropus existed very close— the closest of any fossil known— to the divergence of their common ancestor into apes and hominins.

Also found at the same site were the bones and teeth of nonprimate animals, fossils that create a picture of Sahelanthropus’s habitat. These remains— of hugely diverse animal species, including fish, crocodiles, amphibious mammals associated with aquatic settings, bovids (hoofed mammals), horses, elephants, primates, and rodents associated with forests and grasslands— indicate that Sahelanthropus lived in a forest near a lake.

ORRORIN TUGENENSIS (6 MYA) Dating to around 6 mya, the fossils of at least five pre- australopithecines were found in the Tugen Hills, on the western side of Kenya’s Lake Turkana. The discoverers, paleoanthropologists Brigitte Senut and Martin Pickford, named these hominins Orrorin tugenensis (the genus means “original man” in Tugen’s local language). Among the 20 remains were several partial femurs, each missing the knee but indicating that these hominins were bipedal. For example, the femur’s neck, the area that is at the top of the bone and articulates with the hip, was relatively long (Figure 10.12). A hand phalanx found at the site was curved like a living ape’s, suggesting that Orrorin spent time in the trees. Like those of Sahelanthropus, the canines had wear on the tips and were nonhoning. The animal bones at the site indicated that Orrorin lived in a forest.

FIGURE 10.11 Sahelanthropus tchadensis Among the first and few hominin fossils uncovered in central Africa, this skull belonged to a primate with a small and primitive brain like that of apes. Note the large browridge.

C H A D

Toros-Menalla

Sahelanthropus tchadensis The earliest pre- australopithecine species found in central Africa with possible evidence of bipedalism.

Orrorin tugenensis A pre- australopithecine species found in East Africa that dis- played some of the earliest evidence of bipedalism.

258 | CHAPTER 10 Early Hominin Origins and Evolution: The Roots of Humanity

ARDIPITHECUS KADABBA AND ARDIPITHECUS RAMIDUS (5.8–4.4 MYA) At Aramis, one of a number of important paleontological sites in the fossil- rich Middle Awash Valley of Ethiopia’s expansive Afar Depression (Figure  10.13), the American physical anthropologist Tim White and his colleagues recovered the most spectacular of the pre- australopithecines (or, for that matter, any other hominin assemblage). They began exploring the Middle Awash in the early 1980s as a potential place for finding fossils. At Aramis, beginning in the early 1990s and continuing for the next 15 years, they collected fossils intensively. Their team grew to include 70 scientists from 18 countries. What drew the team back to the site, field season after field season, interrupted for years by political unrest in the region, were the very strong signals for successful recovery of key fossils that would date from the period at or just after the origins of the human lineage. The team concluded that this would be the place to look for answers to questions about the transition from ape to hominin, from a primate that walked on all fours and used its arms to move in trees to a primate that walked on the ground. Eventually, the Middle Awash region yielded the longest continuous record of hominin evolution: more than 6 million years, dating from before the australopithecines through the appearance and evolution of early Homo to the first modern  H.  sapiens (discussed in chapters 11 and 12) and after.

The scientists of the Middle Awash project predicted that fossils discovered by them from the Miocene and early Pliocene at Aramis would reveal hominin ancestors having a mosaic of apelike and humanlike characteristics. These ances- tors would have set the stage for all of later human evolution. And indeed, among their findings were two species of a new genus of hominin, Ardipithecus, including the earlier Ardipithecus kadabba and the later Ardipithecus ramidus (in the local Afar language, ardi means “ground” or “floor” and ramid means “root”), dating to

No obturator externus groove

Long neck

Location of obturator externus groove

Modern human Orrorin

Short neck

Chimpanzee

FIGURE 10.12 Orrorin tugenensis The most important skeletal remain of this pre- australopithecine is a proximal, or upper, portion of the femur, which has a long femoral neck and a groove for the obturator externus muscle. These characteristics are the same as in humans and hominin ancestors, suggesting Orrorin was bipedal. By contrast, apes (such as the chimpanzee) have a short femoral neck and no groove.

FIGURE 10.13 Middle Awash Valley, Ethiopia This hotbed of hominin fossil finds is located in the Afar Depression, an area of much geologic and tectonic activity. The Awash River flows through the depression, creating rich plant and animal life in the midst of an arid region. Because the Afar’s floor consists of volcanic rock, radiometric dating methods can be used to provide age estimates for the fossils found in the geologic strata.

K E N Y A

Lake Turkana

Tugen Hills

Ardipithecus kadabba An early pre- australopithecine species from the late Miocene to the early Pliocene; shows evidence of a perihoning complex, a primitive trait intermediate between apes and modern humans.

What Were the First Hominins? | 259

5.8–5.5 mya and 4.4 mya, respectively. The earlier Ar. kadabba is known mainly from teeth, and these fossils show that hominins’ canines wore from the tips (not the sides) but had some honing or polishing on the sides of the third lower premolar (Figure 10.14).

The later species of Ardipithecus, dubbed “Ardi” by its discoverers, is one of three or four fossil hominin discoveries of the many hundreds since the mid- nineteenth century that have transformed our understanding of the earliest period of human evolution. In 2009, Science, the leading international journal for all scientific disciplines, devoted much of an issue to the description and interpretation of this hominin, calling the finding the “Breakthrough of the Year” (Figure 10.15). Anthropologists worldwide call it the breakthrough of the century.

Ardipithecus is remarkable, first of all, because it is represented by a huge assemblage of fossils. These fossils include the most complete early hominin skel- eton found to date, along with bones and teeth of at least 35 other individuals, all bracketed to a depositional period of less than 10,000 years, an eyeblink in human evolution (Figure 10.16).

Second, the fossils provide us with a snapshot of the species: their behavior, their adaptation, and what life was like for them not long after the chimpanzee and human lineages had diverged from their common ancestor in the late Miocene. This picture includes unprecedented ecological detail derived from the study of thousands of fossilized plant and animal remains from the site in conjunction with the study of the fossil hominin remains. The ecological context shows dra- matically that these early hominins lived in a forest. This discovery provides compelling evidence that— contrary to the hypotheses of Darwin and other

E T H I O P I A

Addis Ababa

Middle Awash AramisAramis

Afar Depression

FIGURE 10.14 Ardipithecus kadabba The earlier form of this pre- australopithecine had an intermediate honing, or perihoning, complex in its dentition, while the later form lacked honing entirely. Shown here, the perihoning complex of an early form of Ardipithecus (right) is similar to chimpanzees’ honing complex (left). Together, these forms suggest that Ardipithecus was an early hominin ancestor as its dental morphology was intermediate between apes’ and humans’. (Photo © 2003 Tim D. White/David L. Brill, humanoriginsphotos.com)

FIGURE 10.15 Cover of Science Magazine The discovery of Ardipithecus was such a fundamental development that Science magazine called it the “Breakthrough of the Year.”

Ardipithecus ramidus A later pre- australopithecine species from the late Miocene to the early Pliocene; shows evidence of both bipedalism and arboreal activity but no indication of the primitive perihoning complex.

This remarkable hominin skeleton, along with the other fossils found at Aramis, provides us with a new understanding of the origins and evolution of the human and ape lineages. This new understanding is made possible by this remarkably complete fossil record and the unprecedented level and detail of multidisciplinary study, ranging from habitat reconstruction to the analysis of function and behavior of early hominins. The very primitive nature of this skeleton confirms that the divergence of the chimpanzee/human lineage was quite recent and provides insight into behavior and adaptation soon after the divergence. This fossil is the closest found yet to the common ancestor of chimpanzees and humans. Most importantly, all earlier models suggesting a chimpanzeelike ancestor for hominins are incorrect—the first hominin was not chimpanzeelike.

Almost from the beginning of the discovery of fossils in this locality some years before, it was clear that they needed a new name. Tim White called it Ardipithecus ramidus (in the local Afar language, ardi means “ground” or “floor” and ramid means “root”). The partial skeleton, nicknamed “Ardi” by the field team, required years of cleaning, preparation, and reconstruction. For example, to assemble all the skull fragments into an accurate reconstruction, casts of each of the scores of pieces were made. The resulting images were combined with digital images to produce a composite picture (see the upper left corner of the facing page). Various indicators, including the size of the body, revealed that the hominin was a female adult, weighing 50 kg (110 lbs) and standing 120 cm (4 ft) high.

Once the fossils’ locations had been recorded, it was important to remove the fossils as quickly as possible. The bones were soft and had to be treated with preservatives, and some had to be removed in plaster jackets. They were taken first to the field camp and eventually to the laboratory at the National Museum in Addis Ababa, Ethiopia, for detailed study. The 109 hominin fossils represented 36 individuals. Among them was a partial skeleton, field number ARA-VP-6/500. The oldest fossil hominin skeleton yet found, it predates Lucy’s skeleton by more than a million years. The map plotting the fossils of this hominin shows that it was widely scattered and no bones were articulated. It took the researchers three years of hard work to recover the remains of this skeleton alone.

In the early 1980s, a multidisciplinary team of geologists, paleoanthropologists, and archaeologists first visited the region near the village of Aramis, in the Middle Awash Valley, identifying it as a place where Pliocene hominins could be found. Field teams collected intensively in the region from 1995 to 2005, in geological deposits dating to 4.4 mya. During the 10-year collection period, scientists and field workers literally crawled across the landscape on their hands and knees in search of hominins and other fossils. This herculean effort had an enormous payoff, producing one of the most important fossil records of early hominins ever found and an abundant record of plants and animals. The plant and animal fossils reveal that these early hominins inhabited a cool, wet forest.

Skull and teeth: The skull is very similar to those of other pre-australopithecines, such as Sahelanthropus (see p. 257), with its tiny brain (300–350 cc) and highly projecting face. It is probably like the skull of the nearest common ancestor of apes and humans. The teeth show none of the specializations seen in living apes, such as the big incisors and canines and sectorial complex of orangutans and chimpanzees. Wear on the teeth suggests that the hominin was omnivorous, eating nonabrasive foods and some hard foods. The canine shows no functional honing, and so these hominins processed their food like later hominins. Upper limb and hand: Especially striking about the upper limb and hand are their primitiveness. Compared with those of living humans, the forearm (radius and ulna) is extraordinarily long in relation to the upper arm. The elbow joint shows no evidence that these arms were used for suspension, however. The size and morphology of the hand indicate that the hominin did not knuckle-walk. Thus, knuckle-walking evolved in later apes. The fingers are quite long and had excellent grasping capability. Ardi walked on her palms when in the trees. Pelvis: The wide pelvis indicates full hominin status: Ardi walked bipedally when on the ground. In this respect, the pelvis is quite evolved, especially compared with the upper limb/hands and lower limb/feet. The lower part of the pelvis reveals evidence of muscles used in climbing. Lower limb: The lower limb and foot are adapted for bipedality, but they also reveal characteristics that indicate significant time spent in the trees. For example, the foot has greatly elongated toes and a fully divergent big toe for grasping. No later hominin has this particular combination of features. While retaining its very primitive grasping capability, the foot also served in propelling the body forward when walking or running on the ground. Like the other parts of the skeleton, it is a mosaic of primitive and derived characteristics.

DISCOVERY 1

RECOVERY 2

LAB WORK 3

4

5 IMPLICATIONS FOR HUMAN EVOLUTION

UNDERSTANDING ARDI: HEAD TO TOE

© 2002, David L. Brill, humanoriginsphotos.com

© 1995, David L. Brill, humanoriginsphotos.com

F I G U R E

10.16 From Discovery to Understanding: Ardipithecus of Aramis

This remarkable hominin skeleton, along with the other fossils found at Aramis, provides us with a new understanding of the origins and evolution of the human and ape lineages. This new understanding is made possible by this remarkably complete fossil record and the unprecedented level and detail of multidisciplinary study, ranging from habitat reconstruction to the analysis of function and behavior of early hominins. The very primitive nature of this skeleton confirms that the divergence of the chimpanzee/human lineage was quite recent and provides insight into behavior and adaptation soon after the divergence. This fossil is the closest found yet to the common ancestor of chimpanzees and humans. Most importantly, all earlier models suggesting a chimpanzeelike ancestor for hominins are incorrect—the first hominin was not chimpanzeelike.

Almost from the beginning of the discovery of fossils in this locality some years before, it was clear that they needed a new name. Tim White called it Ardipithecus ramidus (in the local Afar language, ardi means “ground” or “floor” and ramid means “root”). The partial skeleton, nicknamed “Ardi” by the field team, required years of cleaning, preparation, and reconstruction. For example, to assemble all the skull fragments into an accurate reconstruction, casts of each of the scores of pieces were made. The resulting images were combined with digital images to produce a composite picture (see the upper left corner of the facing page). Various indicators, including the size of the body, revealed that the hominin was a female adult, weighing 50 kg (110 lbs) and standing 120 cm (4 ft) high.

Once the fossils’ locations had been recorded, it was important to remove the fossils as quickly as possible. The bones were soft and had to be treated with preservatives, and some had to be removed in plaster jackets. They were taken first to the field camp and eventually to the laboratory at the National Museum in Addis Ababa, Ethiopia, for detailed study. The 109 hominin fossils represented 36 individuals. Among them was a partial skeleton, field number ARA-VP-6/500. The oldest fossil hominin skeleton yet found, it predates Lucy’s skeleton by more than a million years. The map plotting the fossils of this hominin shows that it was widely scattered and no bones were articulated. It took the researchers three years of hard work to recover the remains of this skeleton alone.

In the early 1980s, a multidisciplinary team of geologists, paleoanthropologists, and archaeologists first visited the region near the village of Aramis, in the Middle Awash Valley, identifying it as a place where Pliocene hominins could be found. Field teams collected intensively in the region from 1995 to 2005, in geological deposits dating to 4.4 mya. During the 10-year collection period, scientists and field workers literally crawled across the landscape on their hands and knees in search of hominins and other fossils. This herculean effort had an enormous payoff, producing one of the most important fossil records of early hominins ever found and an abundant record of plants and animals. The plant and animal fossils reveal that these early hominins inhabited a cool, wet forest.

Skull and teeth: The skull is very similar to those of other pre-australopithecines, such as Sahelanthropus (see p. 257), with its tiny brain (300–350 cc) and highly projecting face. It is probably like the skull of the nearest common ancestor of apes and humans. The teeth show none of the specializations seen in living apes, such as the big incisors and canines and sectorial complex of orangutans and chimpanzees. Wear on the teeth suggests that the hominin was omnivorous, eating nonabrasive foods and some hard foods. The canine shows no functional honing, and so these hominins processed their food like later hominins. Upper limb and hand: Especially striking about the upper limb and hand are their primitiveness. Compared with those of living humans, the forearm (radius and ulna) is extraordinarily long in relation to the upper arm. The elbow joint shows no evidence that these arms were used for suspension, however. The size and morphology of the hand indicate that the hominin did not knuckle-walk. Thus, knuckle-walking evolved in later apes. The fingers are quite long and had excellent grasping capability. Ardi walked on her palms when in the trees. Pelvis: The wide pelvis indicates full hominin status: Ardi walked bipedally when on the ground. In this respect, the pelvis is quite evolved, especially compared with the upper limb/hands and lower limb/feet. The lower part of the pelvis reveals evidence of muscles used in climbing. Lower limb: The lower limb and foot are adapted for bipedality, but they also reveal characteristics that indicate significant time spent in the trees. For example, the foot has greatly elongated toes and a fully divergent big toe for grasping. No later hominin has this particular combination of features. While retaining its very primitive grasping capability, the foot also served in propelling the body forward when walking or running on the ground. Like the other parts of the skeleton, it is a mosaic of primitive and derived characteristics.

DISCOVERY 1

RECOVERY 2

LAB WORK 3

4

5 IMPLICATIONS FOR HUMAN EVOLUTION

UNDERSTANDING ARDI: HEAD TO TOE

© 2002, David L. Brill, humanoriginsphotos.com

© 1995, David L. Brill, humanoriginsphotos.com

262 | CHAPTER 10 Early Hominin Origins and Evolution: The Roots of Humanity

authorities and reaffirmed by most of the fossil record dating to the Pliocene and Pleistocene— the first hominins did not evolve in the open grasslands (Figure 10.17). The forest context for pre- australopithecines had been suggested by paleoecolog- ical analyses of the settings for Sahelanthropus and Orrorin, but the ecological records from places where these pre- australopithecine fossils were found are not nearly as extensive as the ecological record for Aramis.

Like earlier species of Ardipithecus, the Aramis fossils have a primitive yet fully hominin masticatory complex, with short, nonprojecting canines and wear on the tips of the canines. The tooth enamel is not as thin as in extant apes, but it is thinner than in all later hominins. As noted by the physical anthropologist Owen Lovejoy and his colleagues, the lower limb and foot bones reveal that the big toe was opposable, more like that of an ape today and completely unlike a human’s (Figure  10.18). Unlike an ape’s foot, however, Ardi’s foot lacked the flexibility required for grasping tree limbs and moving through trees. The musculature and construction of Ardi’s foot were rigid, a hominin adaptation for using the foot to propel itself forward when walking bipedally. The phalanges of the feet and hands were curved, indicating grasping capabilities similar to apes’. In addition, Ardi’s wrist lacked the articulations and specialized adaptations of today’s suspensory, knuckle- walking great apes. These details show that Ardi was adapted to life in the trees and to life on the ground. It was a part- time biped and a part- time quadruped. It did not evolve from an ape that was suspensory in the trees and a knuckle- walker

FIGURE 10.17 Origins of Bipedalism The earliest hominin ancestors, the pre- australopithecines, lived in a forested setting, although it might have had a discontinuous tree cover. Contrary to earlier hypotheses, bipedalism appears to have originated not in open grasslands but in an environment with trees. (© Jay. H. Matternes)

FIGURE 10.18 Foot Phalanges There is evidence that Ardipithecus was bipedal. However, its big toe (hallux) is divergent like apes’, indicating that this pre- australopithecine was arboreal at least some of the time. Like its dentition, this anatomical evidence suggests Ardipithecus was an intermediate genus. (Photo © 2003 by Tim D. White/David L. Brill, humanoriginsphotos.com)

The Pre- Australopithecines

The first hominins spanned a 3- million- year period in Africa, about 7–4 mya. They had both apelike characteristics and the features that define hominins.

Hominin Date(s) Location Hominin Date(s) Location

Sahelanthropus tchadensis

7–6 mya Djurab Desert, Chad

Ardipithecus kadabba

5.8–5.6 mya Awash River Valley, Ethiopia

Key features:

Skull and teeth found

Tiny brain (350 cc)

Skull like apes’, with massive browridge

Lived in forest setting

Key features:

Skull, teeth, postcranial bones found

Small brain

Some tooth wear on outside of third premolar (perihoning)

Thin enamel

Curved foot phalanges

Femur and pelvis indicate capable of bipedalism

Less than 1 m (3.3 ft) tall

Lived in wooded setting

Orrorin tugenensis 6 mya Tugen Hills, Kenya Ardipithecus ramidus

4.4 mya Awash River Valley, Ethiopia

Key features:

Postcranial bones found

Femurs indicate likely bipedalism

Hand phalanx like apes’ (curved)

Less than 1 m (3.3 ft) tall

Lived in forest setting

Key features:

Skull, teeth, postcranial bones found

Small brain

No perihoning

Thin enamel (only hominin with thin enamel)

Curved foot phalanges

Femur and pelvis indicate capable of bipedalism

120 cm (3.9 ft) tall

Lived in wooded setting

C O N C E P T C H E C K !

What Were the First Hominins? | 263

authorities and reaffirmed by most of the fossil record dating to the Pliocene and Pleistocene— the first hominins did not evolve in the open grasslands (Figure 10.17). The forest context for pre- australopithecines had been suggested by paleoecolog- ical analyses of the settings for Sahelanthropus and Orrorin, but the ecological records from places where these pre- australopithecine fossils were found are not nearly as extensive as the ecological record for Aramis.

Like earlier species of Ardipithecus, the Aramis fossils have a primitive yet fully hominin masticatory complex, with short, nonprojecting canines and wear on the tips of the canines. The tooth enamel is not as thin as in extant apes, but it is thinner than in all later hominins. As noted by the physical anthropologist Owen Lovejoy and his colleagues, the lower limb and foot bones reveal that the big toe was opposable, more like that of an ape today and completely unlike a human’s (Figure  10.18). Unlike an ape’s foot, however, Ardi’s foot lacked the flexibility required for grasping tree limbs and moving through trees. The musculature and construction of Ardi’s foot were rigid, a hominin adaptation for using the foot to propel itself forward when walking bipedally. The phalanges of the feet and hands were curved, indicating grasping capabilities similar to apes’. In addition, Ardi’s wrist lacked the articulations and specialized adaptations of today’s suspensory, knuckle- walking great apes. These details show that Ardi was adapted to life in the trees and to life on the ground. It was a part- time biped and a part- time quadruped. It did not evolve from an ape that was suspensory in the trees and a knuckle- walker

FIGURE 10.17 Origins of Bipedalism The earliest hominin ancestors, the pre- australopithecines, lived in a forested setting, although it might have had a discontinuous tree cover. Contrary to earlier hypotheses, bipedalism appears to have originated not in open grasslands but in an environment with trees. (© Jay. H. Matternes)

FIGURE 10.18 Foot Phalanges There is evidence that Ardipithecus was bipedal. However, its big toe (hallux) is divergent like apes’, indicating that this pre- australopithecine was arboreal at least some of the time. Like its dentition, this anatomical evidence suggests Ardipithecus was an intermediate genus. (Photo © 2003 by Tim D. White/David L. Brill, humanoriginsphotos.com)

The Pre- Australopithecines

The first hominins spanned a 3- million- year period in Africa, about 7–4 mya. They had both apelike characteristics and the features that define hominins.

Hominin Date(s) Location Hominin Date(s) Location

Sahelanthropus tchadensis

7–6 mya Djurab Desert, Chad

Ardipithecus kadabba

5.8–5.6 mya Awash River Valley, Ethiopia

Key features:

Skull and teeth found

Tiny brain (350 cc)

Skull like apes’, with massive browridge

Lived in forest setting

Key features:

Skull, teeth, postcranial bones found

Small brain

Some tooth wear on outside of third premolar (perihoning)

Thin enamel

Curved foot phalanges

Femur and pelvis indicate capable of bipedalism

Less than 1 m (3.3 ft) tall

Lived in wooded setting

Orrorin tugenensis 6 mya Tugen Hills, Kenya Ardipithecus ramidus

4.4 mya Awash River Valley, Ethiopia

Key features:

Postcranial bones found

Femurs indicate likely bipedalism

Hand phalanx like apes’ (curved)

Less than 1 m (3.3 ft) tall

Lived in forest setting

Key features:

Skull, teeth, postcranial bones found

Small brain

No perihoning

Thin enamel (only hominin with thin enamel)

Curved foot phalanges

Femur and pelvis indicate capable of bipedalism

120 cm (3.9 ft) tall

Lived in wooded setting

C O N C E P T C H E C K !

264 | CHAPTER 10 Early Hominin Origins and Evolution: The Roots of Humanity

on the ground. Instead, as suggested by reconstruction of its skeleton, Ardi moved on its palms and feet along tree branches and walked upright on the ground.

Ardi’s intermediate form of bipedality is part of the ancestry of later hominins, which became fully committed to life on the ground. Ardi evolved from some apelike ancestor, but the great apes and hominins took two entirely different behavioral and associated anatomical pathways, the former evolving suspensory locomotion and knuckle- walking and the latter evolving efficient bipedalism and losing all arboreal behavior. The extensive fossil record from Aramis clarifies the adaptive proliferation of hominin species documented in the evolution of the australopithecines and after. In short, while Ardi was clearly a primitive hominin, its array of remarkable characteristics puts it on the evolutionary pathway to the human lineage.

THE AUSTRALOPITHECINES (4–1 MYA) The australopithecines are represented by hundreds of fossils of as many as nine species from one genus, Australopithecus. Some of the species represent members of ancestral- descendant lineages (Figure  10.19). For the other species, however, anthropologists are sorting out the lineage relationships. Compared with other mammals, australopithecines did not vary greatly. Their variation was mostly in size and robusticity— from relatively small and gracile to large and robust. As a

9

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1.0 mya

3.0 mya

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2.0 mya

4.0 mya

1.5 mya

3.5 mya

4.5 mya

Ardipithecus ramidus Australopithecus anamensis Australopithecus afarensis

Australopithecus garhi Australopithecus africanus Australopithecus robustus

Australopithecus aethiopicus Australopithecus boisei Homo

1 2 3

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FIGURE 10.19 Hominin Phylogenies These four alternative phylogenies depict the possible ancestor– descendant relationships among the many australopithecine species. In each tree, Ardipithecus is at the base, leading to its descendant Australopithecus anamensis, one of the earliest australopithecines. In the second tree, 9a and 9b indicate that the Homo genus may have been the product of both ancestors.

What Were the First Hominins? | 265

group, the australopithecines had a small brain, small canines, large premolars, and large molars (Table  10.1). The later australopithecines’ face, jaws, and teeth were very large.

AUSTRALOPITHECUS ANAMENSIS (4 MYA) The oldest australopithecine species, Australopithecus anamensis (anam means “lake” in the Turkana language), was named and studied by the American paleoanthropological team of Meave Leakey, Carol Ward, and Alan Walker. Au. anamensis dates to about 4 mya and was found within Allia Bay and Kanapoi, in, respectively, the eastern and southern ends of Lake Turkana, Kenya (Figure 10.20). Other remains, found at Asa Issie, Ethiopia, have been studied by the American anthropologist Tim White and his colleagues. This creature was broadly similar in physical appearance to Ardipithe- cus, enough to indicate a probable ancestral- descendant relationship between the two genera. Reflecting its relatively early place in australopithecine evolution, Au. anamensis has a number of primitive, apelike characteristics, including very large canines, parallel tooth rows in the upper jaw, and a lower third premolar with both a very large outer cusp and a very small inner cusp (Figure 10.21). The fossils were created in woodland environments.

TABLE 10.1 The Earliest Hominins Evolve

Pre- Australopithecine Ž Australopithecine

Teeth Wear on tip of canine, but with modified honing Ž

Nonhoning

Bones Vestiges of apelike arboreal traits Ž Loss of traits

Brain Small Ž Slight increase

Australopithecus anamensis The oldest species of australopithecine from East Africa and a likely ancestor to Au. afarensis.

FIGURE 10.20 Alan Walker Walker (foreground) is seated in the bone bed at Allia Bay, where he was part of the team that recovered fragments of Australopithecus anamensis.

266 | CHAPTER 10 Early Hominin Origins and Evolution: The Roots of Humanity

AUSTRALOPITHECUS AFARENSIS (3.6–3.0 MYA) Since the early 1970s, fos- sils representing Australopithecus afarensis have been found in four main sites: Laetoli, in Tanzania, and Hadar, Korsi Dora, and Dikika, all in Ethiopia (Afar is the name of the local tribe on whose land the fossils were found in Ethiopia). Au. afarensis is the best- known australopithecine and is represented by dozens of indi- viduals from Laetoli and Hadar and single individuals from Korsi Dora and Dikika, collectively dating to 3.6–3.0 mya. The most spectacular of the Au. afarensis fossils are three partial skeletons from Hadar, Korsi Dora, and Dikika. They represent, respectively, an adult female— nicknamed “Lucy” after the Beatles’ song “Lucy in the Sky with Diamonds”—an adult male, and a three- year- old child (Figure 10.22).

The completeness of these fossil remains gives us detailed insight into the biology of Au. afarensis. Lucy stood only a little more than 1 m (about 3.5  ft) and had somewhat short legs relative to the length of the arms and body trunk. Some authorities have argued that these short legs would have limited the stride in comparison with modern people. However, the male stood about 1.5–1.7 m (about 5–5.5 ft), and the features of the skeleton and limb bones indicate that the form of walking was likely quite similar to modern humans’. This similarity suggests that Lucy’s legs were not short because it had some form of limited bipedality. Rather, Lucy simply was short. In addition to limb bones, a partial pelvis, and ribs, a scap- ula has been preserved from the adult male. This bone shows that its shoulder was similar to a modern human’s. In other words, the adult skeleton has changed little in overall plan since the time when Au. afarensis lived on the African landscape. The phalanges from Lucy’s skeleton are the same length as modern humans’, but they are curved, like the pre- australopithecines’. The curvature suggests some potential arboreal locomotion using the hands (Figure  10.23). The capability for arboreal activity may also be expressed in the morphology of the scapulae (shoulder joints) of the Dikika juvenile, especially those traits indicating suspensory locomotion.

K E N Y A

Kanapoi

T A N Z A N I A

Laetoli

Allia Bay

Chimpanzee

Au. anamensis

Modern human

FIGURE 10.21 Australopithecus anamensis Humans’ mandible widens at the rear, causing the two rows of teeth to not be parallel to each other. By contrast, this australopithecine’s mandible is like that of apes, U- shaped and with two parallel rows of teeth. Primitive features like this, combined with numerous hominin features, have led many researchers to conclude that Au. anamensis is the earliest australopithecine.

Australopithecus afarensis An early aus- tralopithecine from East Africa that had a brain size equivalent to a modern chim- panzee’s and is thought to be a direct human ancestor.

Lucy One of the most significant fossils: the 40% complete skeleton of an adult female Au. afarensis, found in East Africa.

E T H I O P I A

Asa IssieAsa Issie DikikaDikika

HadarHadar Korsi Dora

(a) (b) (c)

FIGURE 10.22 Australopithecus afarensis (a) As shown here, “Lucy” is a relatively complete skeleton, which helped researchers conclude that this species was bipedal. (b) Recently, the fossil remains of a three- year- old child were recovered and nicknamed “Lucy’s baby.” There are few children in the fossil record. (c) Skeleton from Korsi Dora. (Photo [a] © 1985, David L. Brill, humanoriginsphotos.com)

FIGURE 10.23 Finger and Toe Curvature Gorillas and other nonhuman primates have curved phalanges, which provide a better grip on tree branches and improve arboreal locomotion. In modern humans, this curvature has been lost in the hands and feet as humans are adapted to life on the ground. The phalanges of early hominins, including australopithecines, have an intermediate amount of curvature, which likely reflects an increasing adaptation to bipedalism but a retained ability to move through the trees.

Gorilla Australopithecus Modern human

What Were the First Hominins? | 267

AUSTRALOPITHECUS AFARENSIS (3.6–3.0 MYA) Since the early 1970s, fos- sils representing Australopithecus afarensis have been found in four main sites: Laetoli, in Tanzania, and Hadar, Korsi Dora, and Dikika, all in Ethiopia (Afar is the name of the local tribe on whose land the fossils were found in Ethiopia). Au. afarensis is the best- known australopithecine and is represented by dozens of indi- viduals from Laetoli and Hadar and single individuals from Korsi Dora and Dikika, collectively dating to 3.6–3.0 mya. The most spectacular of the Au. afarensis fossils are three partial skeletons from Hadar, Korsi Dora, and Dikika. They represent, respectively, an adult female— nicknamed “Lucy” after the Beatles’ song “Lucy in the Sky with Diamonds”—an adult male, and a three- year- old child (Figure 10.22).

The completeness of these fossil remains gives us detailed insight into the biology of Au. afarensis. Lucy stood only a little more than 1 m (about 3.5  ft) and had somewhat short legs relative to the length of the arms and body trunk. Some authorities have argued that these short legs would have limited the stride in comparison with modern people. However, the male stood about 1.5–1.7 m (about 5–5.5 ft), and the features of the skeleton and limb bones indicate that the form of walking was likely quite similar to modern humans’. This similarity suggests that Lucy’s legs were not short because it had some form of limited bipedality. Rather, Lucy simply was short. In addition to limb bones, a partial pelvis, and ribs, a scap- ula has been preserved from the adult male. This bone shows that its shoulder was similar to a modern human’s. In other words, the adult skeleton has changed little in overall plan since the time when Au. afarensis lived on the African landscape. The phalanges from Lucy’s skeleton are the same length as modern humans’, but they are curved, like the pre- australopithecines’. The curvature suggests some potential arboreal locomotion using the hands (Figure  10.23). The capability for arboreal activity may also be expressed in the morphology of the scapulae (shoulder joints) of the Dikika juvenile, especially those traits indicating suspensory locomotion.

K E N Y A

Kanapoi

T A N Z A N I A

Laetoli

Allia Bay

Chimpanzee

Au. anamensis

Modern human

FIGURE 10.21 Australopithecus anamensis Humans’ mandible widens at the rear, causing the two rows of teeth to not be parallel to each other. By contrast, this australopithecine’s mandible is like that of apes, U- shaped and with two parallel rows of teeth. Primitive features like this, combined with numerous hominin features, have led many researchers to conclude that Au. anamensis is the earliest australopithecine.

Australopithecus afarensis An early aus- tralopithecine from East Africa that had a brain size equivalent to a modern chim- panzee’s and is thought to be a direct human ancestor.

Lucy One of the most significant fossils: the 40% complete skeleton of an adult female Au. afarensis, found in East Africa.

E T H I O P I A

Asa IssieAsa Issie DikikaDikika

HadarHadar Korsi Dora

(a) (b) (c)

FIGURE 10.22 Australopithecus afarensis (a) As shown here, “Lucy” is a relatively complete skeleton, which helped researchers conclude that this species was bipedal. (b) Recently, the fossil remains of a three- year- old child were recovered and nicknamed “Lucy’s baby.” There are few children in the fossil record. (c) Skeleton from Korsi Dora. (Photo [a] © 1985, David L. Brill, humanoriginsphotos.com)

FIGURE 10.23 Finger and Toe Curvature Gorillas and other nonhuman primates have curved phalanges, which provide a better grip on tree branches and improve arboreal locomotion. In modern humans, this curvature has been lost in the hands and feet as humans are adapted to life on the ground. The phalanges of early hominins, including australopithecines, have an intermediate amount of curvature, which likely reflects an increasing adaptation to bipedalism but a retained ability to move through the trees.

Gorilla Australopithecus Modern human

268 | CHAPTER 10 Early Hominin Origins and Evolution: The Roots of Humanity

That is, the shoulder joints in this child are angled more like an ape’s than like a modern human’s (Figure 10.24). Thus, Au. afarensis displays an interesting mosaic of apelike and humanlike anatomical features. Regardless of how paleoanthropol- ogists interpret the shoulder joint morphology, Au. afarensis clearly was an efficient, habitual biped that spent most of its time on the ground.

Au. afarensis’s skull is known from many fragments and teeth, as well as a child’s skull and a nearly complete cranium, the latter found in the early 1990s at Hadar by Donald Johanson (Figure 10.25). The cranial capacity of this creature and others from the taxon is about 430 cc, that of a small brain, the size of an ape’s. The hyoid bone of the child’s neck is very much like an ape’s. The apelike characteristics of the bone associated with speech indicate the strong likelihood that this hominin did not have speech. The canines are large in comparison with later hominins’, the face below the nose projects like an ape’s, and overall it looks primitive.

Its many similarities with Au. anamensis indicate an ancestral- descendant link between the two. Au. afarensis is not as primitive as the earlier hominin in that the two cusps of the lower third premolars are more equal in size. Moreover, Au. afarensis’s canines are smaller than the earlier species’, and the upper tooth rows are parabolic and not parallel— in other words, more like humans’ than like apes’. Au. afarensis’s mandibles are larger, perhaps reflecting an increased use of the jaws in chewing.

Of the three key Au. afarensis sites, Laetoli is especially extraordinary because of its assemblage of fossil hominins and because of its spectacular preservation of thousands of footprints left by numerous species of animals, ranging from tiny insects to giant elephants. Geologic evidence indicates the eruption of a nearby volcano, which spewed a thin layer of very fine ash across the landscape. Soon after the eruption, a light rain fell, causing the ash to turn into a thin, gooey layer of mud. Animals then traversed the landscape, among them three hominins that left tracks indicating they had simultaneously walked across the muddy terrain around 3.6 mya (Figure 10.26). The footprints are remarkable for having been preserved for millions of years and with such clarity, a preservation made possible because the

Infraspinous fossa

Lucy

Dikika

Scapular spine

Supraspinous fossa

Glenoid fossa

(b) Juvenille

Au. afarensisf i OrangutanO t GorillaG ill ChimpanzeeChi HumanH

(a) Adult

FIGURE 10.24 Shoulder joint of Au. afarensis The glenoid fossa of the shoulder joint of Lucy, an adult, and the Dikika juvenile is oriented slightly upward, more like a modern ape than a modern human. The modern human’s glenoid faces completely laterally. The angled glenoid fossa of Au. afarensis suggests climbing abilities.

FIGURE 10.25 Australopithecus afarensis Cranium Although this species was bipedal, its brain size and canine size are more primitive and apelike. Other features of the dentition, however, are more homininlike, illustrating the creature’s intermediate position between the pre- australopithecines and other, later australopithecines.

What Were the First Hominins? | 269

volcanic ash was wet carbonatite, which dries into a rock- hard substance. Physical anthropologists’ study of these tracks reveals that the creatures were humanlike and had three key characteristics of bipedalism: round heels, double arches ( front- to- back and side- to- side), and nondivergent big toes.

In contrast to earlier hominins, which were mostly associated with some type of forested environment, Au. afarensis lived in various habitats, including forests, woodlands, and open country. These diverse environments indicate that hominins became more successful at this time, especially after 4 mya, in adapting to and exploiting new habitats. That Au. afarensis’s tooth wear is more varied than that of earlier australopithecines indicates that Au. afarensis probably had a more diverse diet than its predecessors did.

One of the most important characteristics of the Laetoli footprints is the nondi- vergent big toe. This feature indicates that the hominin had very minimal grasping ability in its toes. In this lack of ability, Au. afarensis resembles living humans and differs from living apes. The nondivergent big toe is clear evidence that Au. afarensis used its feet primarily in terrestrial locomotion, quite unlike the hominins living a million years earlier, Ar. ramidus. However, at least one other taxon of Pliocene hominin was walking around the East African landscape on considerably more primitive feet than Au. afarensis. At the Burtele site, in the Afar region of Ethiopia dating to 3.4 mya, the Ethiopian paleoanthropologist Yohannes Haile- Selassie and his team discovered the front half of a single right foot with a short but divergent opposable big toe. This foot belonged to a hominin that, at least in this one respect, was quite similar to Ardipithecus. Unlike the toe bones indicated in the Laetoli foot- prints, the second to fifth toe bones of the Burtele hominin are long and curved. This foot anatomy shows that the early hominin spent considerable time in the trees. The other characteristics of the foot bones indicate that this hominin walked bipedally. During this period of time, then, there were at least two contemporary hominins, one a climber and the other much more a biped, spending its time on the ground. Perhaps the foot bones from Burtele are from Ardipithecus, which would then have survived into the period of early Australopithecus. In any case, this fossil shows the presence of considerably more diversity in early hominin locomotion than the consensus had previously indicated.

AUSTRALOPITHECUS KENYANTHROPUS) PLATYOPS (3.5 MYA) Australo- pithecus (or Kenyanthropus) platyops is a lesser- known hominin from about the same time as Au. afarensis (Figure  10.27). It was discovered by Meave Leakey and her colleagues at Lomekwi, on the western side of Kenya’s Lake Turkana, in deposits that date to about 3.5 mya. Its habitat was mainly woodlands. Its face was unusually flat (platyops, from the Greek, means “flat face”), a derived feature in hominins, but retained some primitive characteristics.

DIVERSIFICATION OF THE HOMININAE: EMERGENCE OF MULTIPLE EVOLUTIONARY LINEAGES FROM ONE (3–1 MYA) The presence of variable hominin species— some spending considerable time on the ground and some still heavily focused on arboreal adaptation— indicates that the australopithecines were highly diverse, including in their locomotion. Beginning more than 3 mya, at least two lineages of hominin evolution emerged from this diversity. One adaptive pattern is associated with the origin and evolution of the genus Homo. The other is represented by descendants of Au. afarensis, leading to the evolution of later australopithecine lineages with multiple species of hominins

FIGURE 10.26 Laetoli Footprints These footprints, found in Tanzania, resolved any doubt as to whether Au. afarensis was bipedal. The tracks were made by three bipedal hominins, two adults and a child who walked in the footprints of one of the adults. In addition to the hominin footprints, many other prints were found at the site, including those of large animals, such as elephants and giraffes, and those of small animals, including rabbits and birds.

K E N YA

LomekwiLomekwi

Australopithecus (or Kenyanthropus) platyops An australopithecine from East Africa that had a unique flat face and was contemporaneous with Au. afarensis.

270 | CHAPTER 10 Early Hominin Origins and Evolution: The Roots of Humanity

living at the same time in East Africa and in South Africa. The lineage that led to the genus Homo survives to the present, whereas the australopithecine lineages became extinct by about 1 mya (Figure 10.28). Here, we look at the two emerging forms of early hominins.

AUSTRALOPITHECUS GARHI (2.5 MYA) Soon after discovering Au. afarensis at Hadar, Johanson and White began to suspect that Au. afarensis was the most likely ancestor of the genus Homo. However, the ancestral-descendant linkage between the two taxa was difficult to identify, owing to the virtual lack of a hominin fossil record in East Africa dating to 3–2 mya, the time during which earliest Homo likely evolved (discussed further in chapter 11). In 1999, this picture changed dramati- cally, when the Ethiopian paleoanthropologist Berhane Asfaw and his associates discovered a new Australopithecus species, which they named Australopithecus garhi (garhi means “surprise” in the Afar language). Found in Bouri, in Ethiopia’s Middle Awash region, it dated to about 2.5 mya.

Au. garhi is represented by bones, teeth, a partial skeleton, and a skull (Figure 10.29). Its teeth were larger than the earlier australopithecines’. Its third premolar’s two cusps were almost equal in size. As in Au. afarensis, beneath the nose the face had a primitive projection, and the brain was small (450 cc). For the first time in hominin evolution, the ratio of arm (humerus) length to leg (femur) length was much more humanlike than apelike, resulting from the femur’s lengthening. This more humanlike ratio indicates a decreased commitment to the arborealism of earlier australopithecines. These features combined—especially the chronolog- ical position at 2.5 mya and the cranial, dental, and postcranial features—suggest that Au. garhi was ancestral to Homo. Environmental reconstructions based on animal remains and other evidence indicate that this hominin lived on a lakeshore, as was typical of later australopithecines and early Homo.

THE FIRST TOOL MAKERS AND USERS: AUSTRALOPITHECUS OR HOMO? At least one or both early hominins made and used stone tools. Paleoan- thropologists have found very primitive stone tools from a number of sites in East Africa dating mostly to the early Pleistocene, 2.6–1.6 mya. These stone tools are part of the Oldowan Complex, the first hominin culture and the earliest culture of the Lower Paleolithic, named by Louis and Mary Leakey from their work at Olduvai Gorge. The Leakeys concluded that these early stone tools must have been produced solely by the larger-brained early Homo found at the site, rather than by the contemporary smaller-brained australopithecines. Other evidence indicates, however, that at least some australopithecines made and used stone tools. Although much of the record of early stone tool use is early Pleistocene, the discovery of ani- mal bones with cutmarks at Dikika, Ethiopia, dating to 3.3 mya, strongly suggests that the first tool-makers and users were australopithecines, probably Au. afarensis, the only hominin known from this setting (Figure 10.30). The cutmarks are char- acteristic of those made by tools when cutting meat from bone and extracting the nutritious marrow inside. Even more convincing, however, is the actual presence of stone tools dating to 3.3 mya from Lomekwi, West Turkana, Kenya. Scores of in situ artifacts, including Oldowan-like cobble tools and various other implements used for processing animals for food, document the presence of a well-established tool technology (Figure 10.31), substantially pre-dating early Homo. Because Au. (Kenyanthropus) platyops was found in the same geographic location and time, it seems likely that this hominin made and used these tools.

Australopithecus garhi A late australopith- ecine from East Africa that was contem- poraneous with Au. africanus and Au. aethiopicus and was the likely ancestor to the Homo lineage.

Oldowan Complex The stone tool culture associated with H. habilis and, possibly, Au. garhi, including primitive chopper tools.

Lower Paleolithic The oldest part of the period during which the first stone tools were created and used, beginning with the Oldowan Complex.

FIGURE 10.27 Australopithecus (Kenyanthropus) platyops A contemporary of Au. afarensis, this australopithecine was unique in having a flat face and small teeth. Its brain size, however, was similar to that of Au. afarensis.

What Were the First Hominins? | 271

Although no tools have been found at Bouri with Au. garhi, the Belgian paleo- anthropologist Jean de Heinzelin, the English anthropologist Desmond Clark, and their colleagues found mammal bones at the site having distinctive cutmarks and percussion marks that were produced by stone tools. This evidence indicates that like Au. garhi used stone tools to process animal remains for food (Figure 10.32). At the Gona River site, in the Middle Awash region, tools have been found dating to around 2.6  mya. Though still extraordinarily primitive, the tools would have been effective at cutting (Figure 10.33), butchering, and other kinds of food processing.

The dominant tools, “chopper” tools and flakes, discovered in these early homi- nin sites were used to remove the meat and process the meat from various animals, mostly herbivores. At least two activities were involved: use of flakes with sharp edges for cutting meat from bones and use of choppers and cobbles to break and smash the bones to access the protein-rich marrow. One of the sites best known for such findings is the FLK 22 site at Olduvai Gorge, where the Leakeys found the famous Australopithecus boisei cranium in the late 1950s.

Archaeologists have long assumed that such primitive tools were used for cut- ting animal tissues to obtain the meat. In some South African caves, bone tools

Ardipithecus ramidus

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Australopithecus robustus

Australopithecus sediba

FIGURE 10.28 Hominin Lineages The evolutionary relationships among the various Australopithecus species suggest two main lineages: one leading to modern Homo sapiens and the other leading to a number of australopithecines. (This second lineage is shown here as two separate lines, one from East Africa and the other from South Africa.) The ancestor to both lineages is hypothesized to be Au. afarensis, which may be a descendant of Ardipithecus and Au. anamensis.

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found by paleoanthropologists show distinctively polished patterns of microscopic wear. Through experiments, the South African paleoanthropologist Lucinda Backwell and the French paleoanthropologist Francesco d’Errico have shown this kind of wear to be produced by digging in the ground, especially digging in termite mounds. Their finding supports the idea that early hominins ate insects (in addi- tion to meat). While the idea of eating insects is revolting to our Western tastes, insects would have provided important proteins for our ancestors. Alternatively, the bone tools may have been used for digging up edible roots.

Evidence of tool use pre-dating 3.4 mya may not have been found because tools may have been made—and probably were made—out of more ephemeral materi- als, such as wood and grass. In the kinds of environments in which the earliest hominins lived, these materials would not have survived. Other evidence suggests, however, that australopithecines used tools. For example, australopithecines’ hand bones have anatomical features associated with finer manipulation than that used by living apes. The paleoanthropologist Randall Susman has found evidence of a flexor muscle in australopithecine thumbs, very similar to a muscle in living humans that is absent in apes. The flexor muscle makes possible the finer precision use of the thumb and other fingers for tool production and tool use. This evidence, combined with the presence of stone tools and/or cutmarks on animal remains in multiple settings, indicates that various species of Australopithecus incorporated

FIGURE 10.29 Australopithecus garhi This “surprise” hominin may be the link between Au. afarensis and the Homo genus. That some of its traits are similar to those of Au. afarensis while others are similar to features of Homo suggests its intermediate status. (Photo © 1999 David L. Brill, humanoriginsphotos.com)

FIGURE 10.30 Cutmarks on these animal bones from Dikika, Ethiopia indicate stone tool use at 3.3 mya.

What Were the First Hominins? | 273

material culture as a part of the process for acquiring, preparing, and consuming animal sources of protein.

EVOLUTION AND EXTINCTION OF THE AUSTRALOPITHECINES In addition to Au. garhi, other australopithecine species lived in East Africa and South Africa. In East Africa, the species included earlier and later forms of robust australopithecines called Australopithecus aethiopicus (named for Ethiopia, the country where they were first found) and Australopithecus boisei (named for a

Australopithecus aethiopicus An early robust australopithecine from East Africa, with the hallmark physical traits of large teeth, large face, and massive muscle attachments on the cranium.

FIGURE 10.31 Stone tools found in Lomekwi, Kenya date to 3.3 mya.

(a) (b) (c)

FIGURE 10.32 Tool Use and Au. garhi (a) A partial animal mandible with cutmarks, (b) a close- up of cutmarks, and (c) a scanning electron microscopic image of cutmarks showing clear signature of cuts created by stone tools held by a hominin, probably for butchering.

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benefactor who supported the discoverer’s research), respectively. Some authori- ties refer to these hyper- robust australopithecines as the genus Parathropus. The earlier hominin, Au. aethiopicus, from the west side of Lake Turkana, dates to about 2.5 mya and had a brain size of about 410 cc. The later hominin, Au. boisei, from Olduvai Gorge and around Lake Turkana, dates to 2.3–1.2 mya and had a brain size of about 510 cc. Compared with earlier australopithecines, these remarkably robust australopithecines had smaller front teeth, larger back teeth, and larger faces. Their most visually striking characteristic was a massive attachment area, on the skull, for the temporalis muscle, resulting in a well- developed sagittal crest. Both their premolars and their molars were enormous. These big teeth with large chewing surfaces, combined with large chewing muscles, made robust australopith- ecines the ultimate grinders (Figure 10.34).

Australopithecines’ greater cranial robusticity after about 2.5 mya indicates that they were increasingly focused on acquiring and eating foods that required more powerful chewing muscles than before. That is, they were eating harder foods. Robust australopithecines’ presence in East Africa ended sometime before 1 mya, indicating that they became extinct at about that time.

The earliest evidence of hominins in South Africa was described by the paleo- anthropologist and anatomist Raymond Dart. He named the species, initially found at the Taung site (Figure 10.35), Australopithecus africanus (Figure 10.36). Found also at Sterkfontein and Makapansgat, Au. africanus dates to about 3–2 mya

Australopithecus boisei Formerly known as Zinjanthropus boisei; a later robust aus- tralopithecine from East Africa that was contemporaneous with Au. robustus and Au. africanus and had the robust cranial traits, including large teeth, large face, and heavy muscle attachments.

Australopithecus africanus A gracile aus- tralopithecine from South Africa that was contemporaneous with Au. aethiopicus, Au. garhi, and Au. boisei and was likely ancestral to Au. robustus.

FIGURE 10.33 Oldowan Stone Tools A number of stone tools, known as Oldowan tools, were found at Gona, Ethiopia. Dating to 2.6 mya, these primitive tools were not found in association with hominin remains, so it is unclear which genera or species produced them. Among the remains were flaked pieces and “chopper” tools; these may have had various functions.

S O U T H A F R I C A

Taung SterkfonteinSterkfontein Makapansgat

SwartkransSwartkrans

KromdraaiKromdraai

DrimolenDrimolen Malapa

Gona

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Bouri

What Were the First Hominins? | 275

and had larger teeth than those of Au. afarensis. After about 2 mya, there were at least two descendant species of australopithecines in South Africa, Australopithe- cus robustus (sometimes called Parathropus robustus; Figure 10.37) and Australo- pithecus sediba (Figure  10.38), dating to 2.0–1.5 mya and 2.0 mya, respectively. Au. robustus is represented by fossils from the cave sites in Swartkrans, Kromdraai, and Drimolen. Au. sediba, discovered in 2008, is from the Malapa cave.

Au. robustus, probably the longest- surviving species of the australopithecine lineage in South Africa, had large premolars, a big face, and a well- developed sag- ittal crest. These hominins were similar in many respects to their contemporary East African counterparts. Australopithecines’ greater robusticity in South Africa and East Africa indicates a widespread adaptation involving an increased focus on foods that required heavy chewing. Anthropologists have long thought that this powerful masticatory complex— amply documented in later australopithecines— was well suited for chewing small, hard food items, such as nuts and seeds. Studies of microwear on tooth surfaces and stable carbon isotopes from fossils suggest, however, that while robust australopithecines in South and East Africa chewed tough foods, they were eating significant amounts of low- quality vegetation. In East Africa in particular, the evidence from stable carbon isotope ratios indi- cates that Au. boisei mostly ate savanna (C4) grasses. In this way, Au. boisei was like other contemporary grass- consuming mammals (such as horses, pigs, and hippopotamuses) but strikingly different from all other hominins. This reliance on grasses— perhaps as much as 80% of their diet was grass— would have required heavy grinding by the jaws and teeth.

The contemporary of Au. robustus, Au. sediba, is represented by the partial skeleton of a young male that was about 12 or 13 at the time of death, the partial skeleton of an adult female, and parts of at least two other individuals, including an infant. The cranial features are distinctively different from those of Au. robus- tus. The American paleoanthropologist Lee Berger, who lives and works in South Africa, and his collaborators found that the face, jaws, and teeth are relatively small. The cheekbones (zygomatics) do not flair outward, unlike those of Au. robustus. In addition, the broad pelvis and its overall shape are more Homo- like.

Australopithecus robustus A robust aus- tralopithecine from South Africa that may have descended from Au. afarensis, was contemporaneous with Au. boisei, and had the robust cranial traits of large teeth, large face, and heavy muscle attachments.

Australopithecus sediba A late species of australopithecine from South Africa that may have descended from Au. africanus, was a contemporary of Au. robustus, and expresses anatomical features found in Australopithecus and in Homo.

(a) (b)

FIGURE 10.34 Robust Australopithecines (a) Australopithecus aethiopicus and (b) Australopithecus boisei had a large sagittal crest; large, flaring zygomatic, or cheek, bones; and large teeth. The description of these australopithecines as robust, however, applies only to their crania and is likely related to a diet rich in hard foods. Neither of these bipedal species had a robust postcranial skeleton. (Photo [a] © 1995 David L. Brill, humanoriginsphotos.com; photo [b] © 1985 David L. Brill, humanoriginsphotos.com)

FIGURE 10.35 Taung, South Africa Some of the earliest evidence of hominins in South Africa was discovered in a limestone quarry in Taung.

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The Australopithecines

The australopithecines existed about 4–1 mya. Their fossils are from East Africa and South Africa. These creatures were still primitive in a number of ways, but they were more humanlike than apelike compared with the pre- australopithecines.

Hominin Date(s) Location Hominin Date(s) Location

Australopithecus anamensis

4 mya Lake Turkana, Kenya Awash River Valley, Ethiopia

Australopithecus platyops

3.5 mya Lomekwi, Kenya

Key features:

Skull fragments, teeth, postcrania found

Large outer cusp (like apes’) on third premolar

Large canines

Parallel tooth rows in upper jaw (like apes’)

Curved hand phalanx

Less than 1 m (3.3 ft) tall

Lived in wooded setting

Key features:

Skulls and teeth found

Flat face

Small brain (400–500 cc)

Contemporary with Au. afarensis, signaling split of australopithecine lineage into two

Lived in woodlands

Australopithecus afarensis

3.6–3.0 mya

Hadar, Ethiopia Australopithecus africanus

3.0–2.0 mya Taung, South Africa Sterkfontein, South Africa Makapansgat, South Africa

Key features: Skulls, teeth, postcrania (hundreds of pieces) found Partial adult skeleton (Lucy) Partial juvenile ( three- year- old) skeleton Small brain (430 cc) Hyoid like apes’ Mandible larger in earlier Laetoli than in later Hadar Smaller canines than in earlier species

Equal- size cusps on third premolar (like humans’) Curved hand phalanges Short legs Footprints indicate bipedal foot pattern with no divergent big toe Lived in wooded setting but a more open one than associated with Ardipithecus or Au. anamensis

Key features: Skulls, teeth, endocast (impression of brain), postcrania, two partial adult skeletons found Small brain (450 cc) Moderate- size teeth Equal- size cusps on third premolar Phalanges not curved Adult partial skeleton has apelike leg- to- arm ratio (short legs, long arms) Lived in open grasslands Parabolic tooth rows in upper jaw

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What Were the First Hominins? | 277

Hominin Date(s) Location Hominin Date(s) Location

Australopithecus garhi

2.5 mya Bouri, Ethiopia Australopithecus boisei

2.3–1.2 mya Olduvai, Tanzania Lake Turkana, Kenya

Key features:

Skulls, teeth, postcrania found

Small brain (450 cc)

Equal-size cusps on third premolar

Teeth larger than in earlier Au. afarensis (Photo © 1999 David L. Brill, humanoriginsphotos.com)

Ratio of upper arm length to upper leg length more humanlike than apelike

Curved foot phalanx (like Au. afarensis’s)

Lived in grasslands, on lakeshore

Tool maker/user (animal butchering)

Key features:

Skulls and teeth found

Small brain (510 cc)

Massive posterior teeth (Photo © 1985 David L. Brill, humanoriginsphotos.com)

Robust skull with sagittal crest

Lived in open grasslands

Australopithecus aethiopicus

2.5 mya Lake Turkana, Kenya Australopithecus robustus

2.0–1.5 mya Swartkrans, South Africa Kromdraai, South Africa Drimolen, South Africa

Key features:

Skull and teeth found

Small brain (410 cc)

Massive posterior teeth

Robust skull with sagittal crest (Photo © 1995 David L. Brill, humanoriginsphotos.com)

Lived in open grasslands

Key features:

Skulls and teeth found

Small brain (530 cc)

Massive posterior teeth (Photo © David L. Brill, humanoriginsphotos.com)

Robust skull with sagittal crest

Lived in open grasslands

Australopithecus sediba

2.0 mya Malapa, South Africa

Key features:

Four partial skeletons (two adults, two juveniles)

Small brain (420 cc)

Relatively small teeth

Equal-size cusps on third premolars (Photo © David L. Brill, humanoriginsphotos.com)

Gracile face and jaws

Phalanges not curved

Short fingers, long thumbs for precision grip

Long arms

Small, australopithecine-like skeleton

Homo-like pelvis

Lived in open grasslands

278 | CHAPTER 10 Early Hominin Origins and Evolution: The Roots of Humanity

FIGURE 10.36 Australopithecus africanus This Australopithecus africanus cranium was discovered in a series of limestone caves known as Sterkfontein. Located in South Africa, this site has been declared a UNESCO World Heritage Site. Unlike the robust australopithecines also discovered in South Africa, this Au. africanus cranium is gracile.

FIGURE 10.37 Australopithecus robustus Also discovered in South Africa, this robust australopithecine shares many traits with East Africa’s robust species. One of these traits, dietary specialization, might have led to the eventual extinction of both Au. robustus and the East African robust species as they were not able to adapt to vegetation changes caused by climate change. (Photo © David L. Brill, humanoriginsphotos.com)

FIGURE 10.38 Australopithecus sediba Found in a cave in South Africa, this australopithecine is quite different from its contemporary, Au. robustus, in that its face and jaws are relatively gracile, at least as represented in the juvenile skull. The gracile nature of the skull may be due to the individual’s being a child; fully mature adult characteristics are not yet present. The very small brain is an australopithecine feature.

The small body and relatively long arms, however, are more like those of australo- pithecines. Similarly, the hand has fingers with large, powerful muscles for grasping in arboreal settings yet with a long thumb for precision gripping, perhaps for tool production and use. The brain was tiny, only about 420 cc, considerably smaller than the brains in any early Homo. The presence of features associated with Homo suggests that this australopithecine might have played a part in the ancestry of our genus. For example, genetic traits in the teeth of Au. sediba show strong affinities with other australopithecines in South Africa and with early and recent Homo. However, the presence of early Homo in East Africa well before Au. sediba indicates that the transition from Australopithecus to Homo first took place in East Africa. Nevertheless, this set of fossils from Malapa provides a record of complexity that challenges some of the earlier notions of the origins of Homo. Perhaps our genus originated at various times and places on the African continent.

As in East Africa, the australopithecines in South Africa went extinct by 1 mya. The reasons for this extinction are unclear. However, the lineage leading to Homo seems to have developed an increasingly flexible and generalized diet, whereas the later robust australopithecines’ diets became less flexible and more specialized. This increasing focus on a narrower range of foods in the later robust australo- pithecines may have led to their extinction. Their brains show very little increase in size. The brains of South African Au. africanus and Au. robustus were only about 450 cc and 530 cc, respectively.

What Were the First Hominins? | 279

From the late Miocene through the Pliocene and into the Pleistocene— about 6–1  mya— the earliest hominins began to evolve. These diverse hominins had increasingly specialized diets, and their cranial morphology reflected this spe- cialization. They experienced no appreciable change in brain size or body size, however. Thus, evolution focused on mastication. A new genus of and species of hominin, Homo habilis— having a larger brain and reduced chewing complex— made its appearance (Table  10.2). At that time, australopithecines were diverse, evolving, and a significant presence on the African landscape. This gracile homi- nin likely evolved from an australopithecine, and the ancestor may have been Au. garhi. This point in human evolution is critically important because it is the earliest record of a remarkable adaptive radiation, leading to the most prolific and widespread species of primate: us.

Homo habilis The earliest Homo species, a possible descendant of Au. garhi and an ancestor to H. erectus; showed the first substantial increase in brain size and was the first species definitively associated with the production and use of stone tools.

TABLE 10.2 Trends from Late Australopithecine to Early Homo

Late Australopithecine → Early Homo

Brain Increase in size

Face Reduction in size

Teeth Reduction in size

A N S W E R I N G T H E B I G Q U E S T I O N S

C H A P T E R   1 0 R E V I E W [INSERT INQUIZITIVE LOGO/TEXT HERE]

What is a hominin? • Hominins are defined by two obligate behaviors:

bipedal locomotion and nonhoning chewing.

Why did hominins evolve from an apelike primate? • The Homininae’s origin is closely tied to the origins

of bipedal locomotion. This form of movement may have provided early hominins with a more efficient means of exploiting patchy forests, freeing the hands for feeding in trees and on the ground.

What were the first hominins? • The earliest fossil hominins were the pre-

australopithecines, dating to 7–4 mya. These hominins lived in forests.

• The pre- australopithecines gave rise to the australopithecines, dating to 4–1 mya.

• According to evidence from early stone tools of the Oldowan, stable isotopes, dental microwear, and craniofacial anatomy, early hominins underwent a wide range of diet- related adaptations. The record generally reflects increasing specialization,

with preferred foods narrowing from meat to grasses.

• The first hominins show considerable diversity in all anatomical characteristics, including both above the neck (teeth and skull) and below the neck (e.g., locomotor skeleton). Within the genus Australopithecus, some were highly terrestrial whereas others were strongly committed to an arboreal lifestyle.

What was the evolutionary fate of the first hominins? • The evolution of the australopithecine lineages

resulted in generally increased robusticity of the chewing complex, no change in brain size, and eventual extinction. The change in the chewing complex reflected an increasing focus on eating hard or tough foods, especially plants.

• By 2.5 mya, at least one australopithecine lineage gave rise to the genus Homo. Having evolved from earlier australopithecines, at least two other australopithecine lineages, one in East Africa and one in South Africa, went extinct around 1 mya.

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REVIEW THIS CHAPTER WITH PERSONALIZED, INTERACTIVE QUESTIONS THROUGH IJK, INQUIZITIVE.WWNORTON.COM q

K E Y T E R M S Ardipithecus kadabba Ardipithecus ramidus Australopithecus aethiopicus Australopithecus afarensis Australopithecus africanus Australopithecus anamensis

Australopithecus boisei Australopithecus garhi Australopithecus (or Kenyanthropus)

platyops Australopithecus robustus Australopithecus sediba

Homo habilis Lower Paleolithic Lucy Oldowan Complex Orrorin tugenensis Sahelanthropus tchadensis

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E V O L U T I O N R E V I E W The First Hominins

Synopsis The earliest hominins arose during the transition from an arboreal lifestyle to a terrestrial lifestyle. For this reason, the fossils of these first hominin species (e.g., Ardipithecus ramidus) have some anatomical features that reflect bipedality and some features that reflect arboreality. Over the course of several million years, the arboreal traits, such as a grasping foot, disappear from the fossil record. Key anatomical changes that take place in later hominins include the remarkable increase in robusticity and size of the masticatory (chewing) apparatus. These changes disap- pear with the extinction of the hyper- robust australopithecines. Throughout the fossil record, especially after 2.6 mya, evidence of tool use is present. The use of tools may or may not have been fundamental to the success of the first hominins. Most authorities regard tool use and technology in general to be especially impor- tant for the appearance and evolution of the earliest members of our own genus, Homo.

Q1. Identify the two fundamental behaviors that first emerged in the pre- australopithecines and that reflected distinctive char- acteristics of the hominin evolutionary branch. Summarize the anatomical features present in early hominin species that are indicative of each of these behaviors.

Q2. Physical anthropologists often describe bipedalism as an adaptive trade- off, a characteristic with both benefits and

costs associated with its evolution. Give two examples of the evolutionary benefits bipedalism provided to our early hominin ancestors. Also, give two examples of the evolutionary costs of bipedalism that are still encountered by humans today.

Q3. What factors explain the evolution of the robust faces and jaws of Australopithecus, especially in the early Pleistocene?

Hint Focus on the adaptive advantages of robust faces and jaws, and then consider the environmental factors that may have caused the conditions that Australopithecus was adapting to.

Q4 . Discuss the major anatomical differences between some of the earliest hominins (e.g., Ardipithecus ramidus) and some of the latest australopithecines (e.g., Australopithecus garhi and Australopithecus boisei). Also, contrast the cranial and den- tal morphology of the gracile and robust australopithecines. Which of these two groups do you think is more likely to be directly ancestral to the first members of the genus Homo?

Q5. What role might climate fluctuations have played in the appear- ance and evolution of the first hominins?

Hint Climate change in the late Miocene caused tropical forests to shift to patchy forests and open grasslands and changed the kinds of foods that were available.

A D D I T I O N A L R E A D I N G S

Cartmill, M. and F. H. Smith. 2009. The Human Lineage. Hoboken, NJ: Wiley- Blackwell.

Conroy, G. C. and H. Pontzer. 2012. Reconstructing Human Origins: A Modern Synthesis. 3rd ed. New York: Norton.

Gibbons,  A.  2006. The First Human: The Race to Discover Our Earliest Ancestors. New York: Doubleday.

Simpson,  S.  W.  2010. The earliest hominins. Pp.  314–340 in  C.  S.  Larsen, ed. A Companion to Biological Anthropology. Chichester, UK: Wiley- Blackwell.

Spencer,  F.  1990. Piltdown: A Scientific Forgery. London: Oxford University Press.

Walker,  A.  and  P.  Shipman. 1996. The Wisdom of the Bones: In Search of Human Origins. New York: Knopf.

White, T. D. 2002. Earliest hominids. Pp. 407–417 in W. C. Hartwig, ed. The Primate Fossil Record. Cambridge, UK: Cambridge Uni- versity Press.

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LOCATED AT ZHOUKOUDIAN (Dragon Bone Hill), near Beijing, People’s Republic of China, this cave was excavated in the 1920 s– 40s, revealing the remains of Homo erectus.

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11 What characteristics define the genus Homo?

What were the earliest members of the genus Homo?

What are the key evolutionary trends and other developments in early Homo?

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The Origins and Evolution of Early Homo

Charles Darwin was struck by the great anatomical similarity of living humans and African apes. In 1871, writing about human origins without having seen a human fossil, he settled on Africa as the birthplace of the earliest hominins. But he was not the only leading scientist in the nineteenth century to think about human origins and where humans first evolved. Ernst Haeckel (1834–1919), Germany’s pre- eminent anatomist and evolutionary biologist of the late nineteenth century, came up with an entirely different origins scenario. He reasoned that the Asian great ape, the orangutan, is more anatomically similar to humans than are the African great apes. Asia, not Africa, he concluded, must have been the hominins’ ancestral homeland. In his extensive scholarly work about human origins and evolution, Haeckel went to great lengths to describe what the first hominin would have looked like. He even went so far as to propose a genus name for the ancestor: Pithecanthropus, meaning “ ape- man.”

Haeckel’s books on early human evolution and its Asian origins profoundly inspired a precocious Dutch teenager, Eugène Dubois (1858–1940; Figure 11.1). Fascinated by Haeckel’s ideas about evolution, Dubois devoured Darwin’s On the Origin of Species. He enrolled in medical school at the University of Amsterdam at age 19 and received his medical degree at 26. A superb scientist, he was hired as a lecturer in the university’s anatomy department. At the same time, his interest in evolution deepened. He became convinced that to truly study human origins, he had to find human fossils. Within a year of being promoted to lecturer he quit his job, gathered his resources, got hired as a physician for the Dutch colonial government, and moved with his wife and their baby to the Dutch East Indies (the modern country of Indonesia, which includes the islands of

B I G Q U E S T I O N S

284 | CHAPTER 11 The Origins and Evolution of Early Homo

Sumatra and Borneo; Figure 11.2). His friends, neighbors, and associates thought he was reckless at best to risk his family’s well- being as he looked for something that might never be found. Soon after landing in Sumatra in December 1887, Dubois assumed his new responsibilities as a physician at a military hospital, spending his money and free time in the pursuit of fossils. After trying to juggle medicine and fossil hunting, he talked the Dutch colonial government into letting him leave his day job to work for the Dutch as a full- time paleontologist. With the help of two civil engineers and a group of 50 convicts, he searched the island but found nothing. Meanwhile, he suffered from discomfort, fatigue, illness, and depression.

Desperate to avoid returning to Holland without having found fossils, Dubois pleaded with his superiors to let him shift his focus from Sumatra to nearby Java. The authorities accepted his assurances that Java would produce fossils. Following his move to Java, Dubois heard about bones appearing out of the eroding banks of the Solo River, near the village of Trinil. Soon after commencing excavations in the late summer of 1891, he and his field crew discovered a human molar. Within a couple of months, they had found a partial skull; and later in the following year they found a complete femur (Figure 11.3). The skull was extraordinary. It was clearly not from Homo sapiens— it had a low and long braincase, no forehead to speak of, and large browridges like apes’. Was it from an ape or a human or something between an ape and a human? By measuring the braincase’s volume, he estimated that in life

FIGURE 11.1 Eugène Dubois A Dutch anatomist and anthropologist, Dubois discovered the first early hominin remains found outside Europe.

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FIGURE 11.2 Dutch East Indies On the island of Java, one of the southernmost islands of what is now Indonesia, Dubois discovered the hominin fossil later identified as Homo erectus.

Homo habilis: The First Species of the Genus Homo | 285

the brain had been about 1,000 cc, too big for a modern ape (a chimpanzee’s brain is 400 cc) and too small for a modern human (the average human brain today is about 1,450 cc). He had found what he was looking for: the human ancestor. In fact, Dubois’s anatomical study revealed that the femur was essentially identical to a mod- ern human’ s— this primitive human ancestor was fully bipedal. Convinced that he had found what Haeckel had predicted, he called his fossil hominin Pithecanthropus erectus, meaning “ upright- walking ape- man.”

Dubois’s ideas and the fossils he found met with mixed reactions, mostly nega- tive. However, as the years went by, others found more hominin fossils in Java and elsewhere in Asia. It became clear to most anthropologists that Dubois’s fossils from Java were early members of our genus but a different species, and these hominins are now called Homo erectus. Dubois’s fossil turned out to be not from the earli- est hominin or even from the earliest species of Homo (see chapter 10 and below).

Dubois was wrong in thinking that evidence of the earliest human would be found in Southeast Asia, but he was working in a scientific vacuum. Without today’s fossil record to guide him, he drew the best possible conclusion from the evidence avail- able and made crucially important discoveries about the genus Homo’s evolution. The only scientist of the time who set out a research plan to test a hypothesis about early human ancestors, he sought fossil evidence to establish evolutionary rela- tionships. In contrast to the great evolutionists of the nineteenth century— Darwin, Haeckel, Huxley, and others— he endeavored to use fossils, not living animals’ com- parative anatomy, to test his hypothesis. This revolutionary development in anthro- pology set the stage for paleoanthropology, the study of early human evolution.

This chapter focuses on the earliest members of our genus: Homo habilis and H. erectus. These were the hominins that began to develop the characteris- tic behaviors that we see in living humans, that increasingly employed intelligence and displayed adaptive flexibility, and that first depended on material culture. During early Homo’s evolution, hominins began to colonize areas of the world outside Africa. The earliest fossil evidence, from around 2.5–1.0 mya, indicates that H. habi- lis and the earliest H. erectus lived at the same time as the later australopithecines (discussed in chapter 10). Early Homo, however, adapted very differently from the other hominins, the australopithecines. These changes set the course for human evolution, the record of which is supported by abundant fossils.

Homo habilis: The First Species of the Genus Homo THE PATH TO HUMANNESS: BIGGER BRAINS, TOOL USE, AND ADAPTIVE FLEXIBILITY Modern humans are distinctive in having large brains and in depending on material culture for survival. Rather than relying on their bodies for the collection, pro- cessing, and eating of food, modern humans rely on tools and technology as part of their adaptive strategy. These attributes are what scientists looked for in the fossil record when they sought the first species of our genus. Which of the multiple hominin species in the late Pliocene and early Pleistocene show brain size expansion?

FIGURE 11.3 Java Man Dubois originally named this hominin fossil Pithecanthropus erectus, though it was nicknamed “Java Man” after the island on which it was found. Dubois recovered hominin remains, including a partial cranium.

Pithecanthropus erectus The name first proposed by Ernst Haeckel for the oldest hominin; Dubois later used this name for his first fossil discovery, which later became known as Homo erectus.

Homo erectus An early species of Homo and the likely descendant of H. habilis; the first hominin species to move out of Africa into Asia and Europe.

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Which of the hominins with brain size expansion likely depended on tools and material culture for promoting adaptive success and behavioral flexibility?

Soon after the discovery of the massively robust australopithecine Australo- pithecus boisei (its cranium is known as “OH 5”), remains of a hominin having jaws, teeth, and a face that were relatively smaller and a brain that was relatively larger were found, also in Olduvai Gorge. Its describers— Louis Leakey, Philip Tobias, and John Napier— recognized the significance of this combination of characteris- tics and named the new hominin Homo habilis (meaning “handy man”). H.  habilis is now known from Tanzania, Kenya, Ethiopia, Malawi, and South Africa— the same geographic distribution as that of the contemporary australopithecines (Figure  11.4).  H.  habilis found on the eastern side of Kenya’s Lake Turkana is sometimes called Homo rudolfensis (Figure  11.5). The major difference is that H. rudolfensis is somewhat bigger than H. habilis. Because they have the same general body plan and overall morphology (bigger brains, smaller faces), here the two species are discussed as H. habilis.

As Leakey and his associates recognized, H. habilis differs in its anatomy from the robust australopithecines dating to about the same time in East Africa and South Africa. Au. boisei had an enormous chewing complex— its back teeth, jaws, and face were very large— but it had a small brain. In sharp contrast, H. habilis had a smaller chewing complex and a larger brain. Combined, the reduced chewing complex and increased brain size gave H. habilis’s skull a more rounded, or globular, appearance. Most anthropologists agree that these attributes indicate that H. habi- lis began the lineage leading to modern humans.

Still unconfirmed is the identity of H. habilis’s immediate ancestor. The anthro- pologist Tim White’s morphological comparisons between H. habilis and the ear- lier australopithecines suggest that the ancestor was Australopithecus garhi because its face, jaws, and teeth are most similar to  H.  habilis’s. White suggests that the evolutionary transition took place sometime around 3.0–2.5 mya.

FIGURE 11.4 Homo habilis Many fossils of this hominin species have been recovered from East Africa and South Africa. (a) This specimen, known as “OH 24” or “Twiggy,” was discovered in Tanzania in 1968. Dating to 1.8 mya, Twiggy had a larger brain and a less protruding face than australopithecines. (b) Slightly younger than Twiggy, this lower jaw, known as “OH 7,” was found in Tanzania in 1960 and dates to 1.75 mya. Given its small dental size, researchers estimated that the brain size would have been smaller than in other H. habilis fossils. (c) This cranium, “ KNM- ER 1813,” was discovered in Kenya in 1973 and dates to 1.9 mya. Its brain capacity is somewhat smaller than those of other, later H. habilis specimens. (Photo [a] © 1997 David L. Brill, humanoriginsphotos.com; photo [c] © 1985 David L. Brill, )

(a) (b) (c)

HOMO HABILIS AND AUSTRALOPITHECUS: SIMILAR IN BODY PLAN For many years, H. habilis was known from just skulls and teeth. Anthropologists had no idea what the rest of the skeleton looked like. Excavations at Olduvai Gorge in the 1980s by Donald Johanson and his associates led to the discovery of a very fragmentary but important skeleton of H. habilis, known as “OH 62.” The skeleton is from an individual that was short— about 1.1 m (3.5  ft)—like the aus- tralopithecines. Also like the australopithecines, this individual had short legs in comparison with the arms. Although H. habilis walked bipedally, these short legs would not have been involved in the kind of efficient striding performed by living people. The gait would have been shorter.

HOMO HABILIS’S ADAPTATION: INTELLIGENCE AND TOOL USE BECOME IMPORTANT H. habilis’s short legs indicate that the species retained a primitive form of biped- ality, more australopithecine than human. Much more telling about  H.  habilis’s adaptation and evolution are skull and teeth morphology and evidence of the making and use of stone tools. Fossil skulls and fossil teeth reveal that this hominin ancestor had a larger brain, smaller chewing muscles, and smaller teeth than did earlier and contemporary hominins, the australopithecines. Both the brain enlargement and the masticatory changes may be linked to tools’ growing importance. Anatomical evidence from the study of hand bones, such as the pres- ence of muscles that would have provided the necessary precision grip, suggests that H. habilis and at least some of the australopithecines made and used tools. For several reasons, tool- making and tool use were likely more important in H. habilis’s adaptation. First, stone tools are more common in  H.  habilis fossil sites than in

FIGURE 11.5 Homo habilis Owing to its larger size, this fossil hominin is believed by some researchers to be a separate species from H. habilis, called Homo rudolfensis. (Photos © 1995 David L. Brill, humanoriginsphotos.com)

(a) (b)

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Lake Turkana

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Australopithecus fossil sites. Second, H. habilis’s expanding brain size indicates that it was smarter than Australopithecus, with a kind of cognitive advancement almost certainly linked to tool- making and tool use. That is, H. habilis and the lineage it founded became reliant on intelligence, tool- making, and tool use as central means of adaptation. In contrast, the australopithecines became increasingly specialized, focusing on a narrower range of foods that required heavy chewing. They may have made and used tools, but tools were not as fundamental to their survival and adaptation. H. habilis’s behavioral advances laid the foundation for later hominins’ success, including their rapid spread out of Africa and to other areas of the globe.

HABITAT CHANGES AND INCREASING ADAPTIVE FLEXIBILITY Environmental reconstruction of the East African and South African landscapes at 2.5 mya provides some insight into early Homo’s adaptive shifts. This reconstruc- tion indicates a spread of warm- season (C4) grasses, increasing habitat diversity, and increasing food resources for early hominins. Such information, along with skull and teeth morphology, suggests early Homo’s increasing dietary versatility. Tools may have played a central role in these early hominins’ ability to exploit

TA N Z A N I A

Olduvai Gorge

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Homo habilis: The First Member of Our Lineage

H. habilis was the first hominin to have anatomical and behavioral characteristics that foreshadowed the evolution of Homo sapiens: greater intelligence, reliance on tools, and dietary and behavioral flexibility.

Location/Sites Africa (Olduvai Gorge, Lake Turkana, Middle Awash, Omo, Uraha, Sterkfontein)

Chronology 2.5–1.8 mya

Biology and Culture (Compared with Australopithecines)

Feature Evidence Outcome

Tool use (Oldowan)

Skulls Teeth

Smaller face and smaller jaws Reduced size

Intelligence Brain size Increase (to 650 cc)

Diet (scavenging, plant collecting)

Plants available Body size

Perhaps more generalized No significant change

Locomotion Leg length:arm length No significant change

(Photo © 1985 David L. Brill, humanoriginsphotos.com)

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this increasingly diverse landscape. That is, stone tools were likely important for digging roots and tubers and for processing them for consumption. Such extremely primitive technology did not include the kinds of tools associated with later hominins that were clearly social, predatory hunters (discussed below, see “Evo- lution of Homo erectus: Biological Change, Adaptation, and Improved Nutrition”). Still, tools increased these early hominins’ capability of eating a greater range of food, most of it plants or small animals, the latter acquired by luck and opportunity and perhaps scavenging. This dietary shift may be what spelled adaptive success for early Homo and extinction for late Australopithecus.

Homo erectus: Early Homo Goes Global Beginning around 1.8 mya, a new hominin appeared:  H.  erectus had anatomical characteristics that distinguished it from H. habilis. As discussed above, it was the only descendant taxon of  H.  habilis and was among the earliest fossil hominins described, having been found by Eugène Dubois at Trinil, in Java.

In the century since Dubois began his work in Java, many fossils with the same general attributes as the Trinil skull— large browridges, long and low skull, and bigger brain— have been found in Europe, Asia, and Africa (Figure  11.6). These hominins collectively date to about 1.8 mya– 300,000 yBP. During this fascinating and dynamic period of human evolution, hominins first left Africa, colonized vast areas of Asia and Europe, and underwent fundamental changes in culture and adaptation that shaped human biological variation.

Daka Gona Bodo

Buia

Olorgesailie Ileret

Olduvai Gorge

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AT L A N T I C O C E A N

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Kocabaş

Mauer Gran Dolina

Boxgrove

Dmanisi

Zhoukoudian Majuangou

Gongwangling (Lantian)

Sangiran Trinil

Sambungmacan

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E U R O P E

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Homo erectus fossil finds Homo erectus archaeological sites (without hominin bones)

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FIGURE 11.6 Homo erectus Sites Fossils of H. erectus have been discovered throughout Africa, Europe, and Asia.

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HOMO ERECTUS IN AFRICA (1.8–.3 MYA) The earliest record of H. erectus comes from Africa, less than 2 mya. At that time, the last australopithecines were still around in East Africa and South Africa, and their fossils reveal great differences in anatomy and adaptation from  H.  erectus (Figure  11.7). Among the earliest and the most spectacular of these fossils is an 80% complete juvenile skeleton from Nariokotome, on the west side of Lake Tur- kana (Figure 11.8). The skeleton dates to about 1.6 mya, placing it on the bound- ary between the Pliocene and Pleistocene epochs. In contrast to Australopithecus and  H.  habilis, the Nariokotome hominin has several quintessentially modern anatomical features. One of the most striking modern characteristics is the com- bination of relatively short arms and long legs. That is, the H. erectus body plan is much more like that of a living human in its ratio of arm length to leg length. This change in limb proportions in H. erectus signals the beginning of a major alteration in the pattern of bipedal locomotion: H. erectus became completely committed to terrestrial life by adopting a fully modern stride. Life in the trees became a thing of the past.

Features of the pelvic bones and overall size indicate that the Nariokotome individual was likely a young adolescent male. He was quite tall, about 166  cm (66 in). Had he survived to adulthood, he would have grown to nearly 2 m (a little over 6.5 ft) in height. This change in height in comparison with H. habilis and the australopithecines indicates an enormous body size increase in this taxon. In addi- tion, the Nariokotome boy’s cranial capacity was about 900 cc (Figure 11.9). Even taking into account the body size increase (brain size and body size are roughly correlated), this expansion in brain size is large compared with similar changes in earlier hominins.

The Nariokotome skeleton is just one of many  H.  erectus fossils from East Africa. At Ileret, on the eastern side of Lake Turkana, the partial skull of a very small  H.  erectus— possibly a female— was found in geologic strata dating to about 1.6 mya. The skull’s diminutive size and small browridges indicate the very high  degree of variation in  H.  erectus. Some  H.  erectus individuals had very large

Homo erectusAustralopithecus boisei

The presence of a sagittal crest to anchor large chewing muscles reflects this genus’s hard diet of nuts and seeds.

The lack of a sagittal crest indicates this species had smaller chewing muscles, reflecting a much softer diet.

This genus had much smaller molars and thinner enamel, reflecting its softer diet.

The large premolars and molars enabled this genus to grind hard nuts and seeds.

(a) (b) (c) (d)

FIGURE 11.7 Australopithecus boisei vs. Homo erectus While both of these genera were contemporaneous for a period of time in Africa, there are important differences in their cranial and dental morphologies.

and  robust bones, whereas others— such as the hominin from Ileret— were quite gracile.

Just as significant as the Ileret fossil is the presence of multiple sets of footprints on an Ileret landscape dating to around 1.5 mya (Figure  11.10). Recall the foot- prints from Laetoli discussed in chapter 10, representing Australopithecus afarensis and dating to around 3.5 mya. In addition to a set of footprints dating to 1.5 mya from Koobi Fora in Kenya and the Laetoli footprints, the Ileret footprints are the first footprints of ancient hominins to be discovered by paleoanthropologists. These tracks provide a kind of fossilized picture of behavior: evidence of how early human ancestors walked. They reveal that the Ileret H. erectus walked just like a modern human. In fact, these prints provide the first solid evidence of fully modern walking. We know this because the footprints have all the fundamentals that we see in our feet, namely, the double arch (the long one extending from your heel to the base of your toes and the side- to- side one) and an adducted big toe (the big toe is close to the second toe), whereas in the Laetoli fossil the big toe and second toe are abducted (spread apart). Moreover, the prints are big, as would be expected given the great heights of H. erectus compared to earlier hominins. The pelvis and leg bones of  H.  erectus strongly indicate the modern form of walking. The Ileret

FIGURE 11.9 Nariokotome Skull The skull of the Nariokotome boy has been invaluable for relating brain size and overall body size in H. erectus. Why is that relationship important for us to know? (Photo © 1985 David L. Brill, humanoriginsphotos.com)

FIGURE 11.8 Nariokotome Researchers have debated the exact age of “Nariokotome Boy,” also known as “Turkana Boy,” but he was likely around 11 years old. Discovered in 1984, this H. erectus fossil is one of the most complete early hominin skeletons ever found.

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footprints provide proof, however, that this hominin had a foot adapted for activ- ities requiring travel, such as hunting and long- distance walking, behaviors likely first seen with H. erectus.

Other key H. erectus fossils from Africa include a partial cranium found in Oldu- vai Gorge and dating to about 1.2 mya, a partial cranium and postcrania found at Daka and dating to 1 mya (Figure 11.11), a partial cranium found at Buia and dating to about 1 mya, a pelvis found at Gona and dating to 1.2 mya, and a cranium found at Bodo and dating to about 600,000 yBP (Figure  11.12). The Daka and Bodo crania are from the Middle Awash Valley, and the Buia cranium is from Eritrea. In contrast to the Nariokotome boy’s skull and the skull from Ileret, the skulls from Olduvai Gorge, Daka, Buia, and Bodo are very robust, having thick cranial bones and very large browridges. The Olduvai cranium’s browridges are the largest of any known hominin, before or after (Figure 11.13). Only some of this greater size can be accounted for by the Nariokotome boy’s immaturity because the other three hominins were fully mature adult males.

During the process of cleaning the facial bones of the Bodo skull, Tim White found a series of barely visible linear marks on the left cheek, around the left eye

0 6 (ft)54321

2 (m)0

(b)

FIGURE 11.10 Footprints from Ileret, Kenya (a) Exposed surface showing numerous animal and hominin footprints. (b) Site drawing showing just the hominin footprints. Note the orientations of the tracks, showing different individuals walking at different times and in different directions. Can you figure out how many hominins made these tracks?

(a)

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Nariokotome

Ileret

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orbit and the nose, and elsewhere on the cranium (Figure  11.14). Microscopic analysis of the marks indicates that they were caused by a stone tool, perhaps as a contemporary hominin removed the soft tissue covering the facial bones. This activity may have been related to some ritual or to cannibalism. If so, it is the earliest evidence of body manipulation in human evolution.

HOMO ERECTUS IN ASIA (1.8–.3 MYA) The earliest evidence of H. erectus in Asia consists of five skulls, other bones, and many stone tools found, by the Georgian paleontologist David Lordkipanidze and

FIGURE 11.11 Daka Partial Cranium The Daka H. erectus fossil from the Middle Awash Valley, Ethiopia, has large browridges, a characteristic of many other H. erectus specimens in Africa and elsewhere. (Photo © 2001 David L. Brill, humanoriginsphotos.com)

FIGURE 11.12 Bodo Cranium This H. erectus fossil has different cranial features from other specimens of this species. Note the large browridges and thick cranial bones.

E T H I O P I A

Buia Bouri

Bodo

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his colleagues, in Dmanisi, Republic of Georgia (Figure 11.15). The date for this important site, 1.8 mya, indicates that H. erectus colonized western Asia very soon after it began to evolve in Africa (Figure  11.16). Compared with some members of the African  H.  erectus, these hominins’ faces and jaws were smaller and their browridges were less developed— all habilislike facial characteristics. However, in overall shape the Dmanisi hominins’ mandible and face strikingly resemble those of both the Nariokotome boy and the Ileret skull from East Africa. Also, like those of the Nariokotome skeleton, the leg bones are relatively long compared with the arm bones, at least as shown in the two partial skeletons— a child and an adult— found at the site. The oldest H. erectus from Dmanisi has a cranial capacity of only about 650 cc. The strong resemblance between the Dmanisi H. erectus and at least some of the East African H. erectus individuals indicates the relatedness of the Asian H. erectus and African H. erectus.

FIGURE 11.14 Ritual Defleshing? Viewed through a scanning electron microscope, cutmarks such as this one (arrows) indicate that stone tools were used to remove flesh from the Bodo skull. The arrows point to the groove left by the stone tool.

Thick cranial bone

Very large browridges

Large area for muscle attachment on the posterior, or rear, of the cranium

FIGURE 11.13 Olduvai Cranium This H. erectus fossil, known as “OH 9,” has the largest browridges of any hominin species.

Dmanisi

G E O R G I AG E O R G I A

In a site dating to much later, workers discovered a partial H. erectus cranium— fragments of frontal and parietal bones— of an adult male dating to about 500,000 yBP, in a rock quarry near the village of Kocabaş, in the Büyük Menderes, a large valley system in western Turkey. Like many other H. erectus specimens from Africa and from Asia, the Kocabaş specimen has massive browridges and a sagittal keel. According to the American paleoanthropologist John Kappelman and his col- leagues, the cranium’s internal surface appears to have had a bone infection very similar to that caused by tuberculosis. This hominin is doubly significant, first in being the only one found in this vast region of western Asia, second in being the first one showing signs of tuberculosis.

Since Dubois completed his fieldwork, in the 1890s, H. erectus fossils have been found in a number of sites in Indonesia, especially in Java. Some of these remains are nearly as old as the Dmanisi remains. The earlier fossils, from the Sangiran site, date to as early as 1.8–1.6 mya. This early date shows that  H.  erectus rapidly spread eastward from western Asia. Thus, once the taxon had first evolved, it colonized areas outside Africa at a rapid pace, perhaps within less than a few hundred thousand years. The emerging picture is of H. erectus’s rapid, widespread movement throughout Asia. This rapid spread illustrates the hominin’s high degree of adaptive success, a factor likely related to increasing intelligence, increasing reliance for survival on both mate- rial culture and tools, and overall greater ability at acquiring food and other resources.

Dating to 800,000 yBP, the most complete skull from eastern Asia is the Sangiran 17 cranium, from Sangiran, Indonesia. Like the African fossils, it has thick cranial bones and large browridges. Its cranial capacity is about 1,000 cc (Figure 11.17). A slight ridge, or “keel,” runs along the sagittal suture atop the skull; and this sagittal keel appears on H. erectus skulls from Asia, Africa, and Europe.

Later  H.  erectus fossils from Java, dating to between 1 mya and 500,000 yBP, include remains from Sangiran and Sambungmacan, plus the original Trinil skull

sagittal keel A slight ridge of bone found along the midline sagittal suture of the cranium, which is typically found on H. erectus skulls.

FIGURE 11.16 First Migration Homo erectus was the first hominin species to migrate out of Africa and expand into Europe and Asia. This map illustrates the movement: (1) earliest H. erectus in East Africa (Lake Turkana; ~1.8 mya); (2) early expansion of H. erectus into western Asia (Dmanisi, Georgia; ~1.7 mya); (3) rapid eastward expansion of H. erectus into southeast Asia (Sangiran, Indonesia; ~1.8–1.6 mya); (4) earliest butchered animal bones and stone tools attributed to H. erectus in northeast Asia (Majuangou, China; ~1.7 mya); (5) earliest fossil evidence of H. erectus in western Europe (Atapuerca, Spain; ~1.2 mya).

4 5

3

2

1

FIGURE 11.15 Dmanisi Extensive paleoanthropological investigations took place in the town of Dmanisi after early stone tools were discovered there in 1984. Since 1991, more than 20 hominin remains were found, including skull 5 shown here. Discovered in 2005, the remarkable completeness of the skull— the most complete of early Pleistocene Homo— helps paleoanthropologists to understand the full morphology of the cranium, mandible, and teeth of some of the earliest members of our genus. Skull 5 has the combined features typical of H.  erectus— long, low cranium and large browridges. Overall, it combines a small braincase (brain size is 546 cc) with a large face. This skull and other remains from Dmanisi provide evidence for a single evolving lineage of early Homo and having continuity of evolution from at least 1.8 mya across Africa, Europe, and Asia.

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found by Dubois. These fossils show many of the same physical characteristics as the earlier ones but also some changes, such as larger brains and smaller teeth. Some of the best information about the first hominins outside Africa comes from China. The earliest fossil is a partial skull from Gongwangling, near the village of Lantian, Shaanxi Province. The skull dates to about 1.2 mya. Like the fossils from Java, this specimen has large, well- developed browridges and thick cranial bones. Its cranial capacity is about 800 cc. The skull postdates the earliest evidence of hominins in north China, from Majuangou, by nearly 500,000 years. Both the animal bones with butchery marks and the stone artifacts found by the Chinese geologist R. X. Zhu and his collaborators date to nearly 1.7 mya, making them the earliest specimens from Asia.

The site yielding the most impressive H. erectus remains in eastern Asia is the cave in Zhoukoudian, on Dragon Bone Hill, near the modern city of Beijing. After being discovered in the 1920s, the cave was excavated into the early 1940s (Figure 11.18). Deposits dating to 400,000–780,000 yBP contained, in fragments, the bones and teeth of 40–50 individuals, as well as many stone tools and food remains. Tragically, the entire collection of priceless bones was lost during World War II, late in 1941. Fortunately, shortly before the loss, the eminent German anat- omist and anthropologist Franz Weidenreich (1873–1948) had thoroughly studied the bones and teeth, written detailed scientific reports, and made cast replicas, drawings, and photographs (Figure  11.19). This record has allowed scientists to continue studying the Zhoukoudian remains.

HOMO ERECTUS IN EUROPE (1.2 MILLION– 400,000 YBP) The earliest presence and subsequent evolution of H. erectus were somewhat later in Europe than in Africa and Asia. The earliest fossil evidence of H. erectus in western Europe is from the Sierra de Atapuerca, northern Spain— at the cave sites of Sima del Elefante, dating to about 1.2 mya, and of Gran Dolina, dating to about 900,000

FIGURE 11.17 Sangiran Homo erectus Excavations in Indonesia have uncovered many hominin fossils, including Dubois’s Java Man and, shown here, the Sangiran 17 fossil. Note the long cranium, low forehead, and large browridges.

Sambungmacan J A V A

Sangiran Trinil

Gongwangling

C H I N A

Majuangou Zhoukoudian

yBP.  The earlier site is represented by a partial mandible and some teeth, along with animal bones showing cutmarks from butchering. The later site, excavated by the Spanish paleontologist Juan Luis Arsuaga and his colleagues, is among the most important in Europe, owing to the discovery of fragmentary bones and teeth of a half- dozen hominins, along with many stone tools and animal bones. Animal bones and hominin bones had been cut with stone tools and purposely broken. This evidence indicates that hominins processed and consumed animals and other hominins (these practices are discussed further in chapter 10).

The most complete skull from Gran Dolina is Atapuerca 3, consisting of the left facial bones, upper jaw, and teeth of a child. This specimen provides a rare glimpse at what juveniles looked like at this point in human evolution (Figure  11.20). Juvenile or not, the cranium indicates that Atapuerca 3 appeared more modern than other members of H. erectus but was clearly ancestral to later hominins in the Atapuerca region and elsewhere in Europe. Indeed, its bones and teeth are similar in a number of ways to those of hominins that lived in Europe later in the Pleisto- cene, H. sapiens. For example, like the later hominins, the Gran Dolina adults have a wider nasal aperture (opening for the nose).

The only other H. erectus remains in Europe are a partial cranium from Ceprano, Italy, dating to 800,000 yBP; the Mauer jaw— a mandible and most of its teeth— from near Heidelberg, Germany, dating to 500,000 yBP; and a tibia from Box- grove, England, also dating to 500,000 yBP.

EVOLUTION OF HOMO ERECTUS: BIOLOGICAL CHANGE, ADAPTATION, AND IMPROVED NUTRITION How did H. erectus differ from earlier Homo species, such as H. habilis? One of the most obvious differences is H. erectus’s remarkable body size and height. Moreover, the increase in body size occurred rapidly, perhaps in less than a few hundred thousand years. That is, at 1.8 mya  H.  habilis was about the size of an australo- pithecine, but by 1.6 mya another hominin, H. erectus, was considerably taller and heavier. The American physical anthropologists Henry McHenry and Katherine

FIGURE 11.18 Zhoukoudian During excavations at this site in China between 1923 and 1927, H. erectus remains were discovered and called “Peking Man.” Excavations continued until the early 1940s. Today, the place is a UNESCO World Heritage Site.

Atapuerca

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Gran Dolina

FIGURE 11.19 Peking Man Although the original remains of this H. erectus fossil are lost, excellent casts, such as this reconstructed skull, enable modern anthropologists to study this important hominin. (Photo © 1996 David L. Brill, humanoriginsphotos.com)

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Coffing estimate that, from  H.  habilis to  H.  erectus, males’ heights increased by 33% (to 1.8 m, or 5.9 ft) and females’ heights by 37% (to 1.6 m, or 5.3 ft). In other words, H.  habilis— like the australopithecines— was quite short (typically less than 1.2 m, or 4 ft), but H. erectus was considerably taller (more than 1.5 m, or 5 ft). Most of this increase took place 2.0–1.7 mya (Table 11.1).

What caused the rapid increase in body size from H. habilis to H. erectus? Various factors were likely involved, such as climate change and its impact on food supply. But the fundamental reason was likely increased access to animal food sources— protein— acquired from hunting. That some primitive stone tools date to 2.5 mya indicates that early hominins were able to cut meat and process it.

Cutmarks made with stone tools have been found on bones of animal prey in Kenya and Ethiopia, at the Olduvai Gorge and Bouri sites, respectively. Indeed, the pattern of cutmarks found at Bouri indicates that even some late australopith- ecines, ones that preceded Homo, were skilled in animal butchery.

As the American anthropologist Pat Shipman’s work has shown, at Olduvai Gorge, stone- tool cutmarks overlay animal tooth marks. This finding suggests that at least some of the behavior involving butchering was scavenging— eating animals killed by other animals— and not hunting. Other evidence of meat- eating has been documented in the bone chemistry of early hominins and in wear on their teeth.

Meat- eating likely started long before H. erectus appeared, but the technology available to earlier hominins and the minimal record of hunting prior to  H.  erec- tus suggest that meat was a minor part of this hominin’s diet. Two things had to happen for early hominins to routinely acquire meat. First, to kill game hominins had to become able to manufacture the right tools, especially stone tools that could be thrown or thrust accurately, such as spears. Second, hominins had to develop the social structure whereby a group of individuals— older adolescent and adult males, primarily— could efficiently track and kill game. Both developments were part of the increase in hominin intelligence at this time, as recorded by brain size expansion and more complex technology. Once hominins had developed the technological and social means of accessing animal food sources daily, they likely had increased access to high- quality protein. This increased access to protein would in turn have produced H. erec- tus’s bump in height— these hominins were taller than their ancestors due to improved nutrition that came about by acquiring food (especially protein) through hunting.

Such increasingly sophisticated technology and increased dependence on cul- ture were important in human evolution generally. The culture associated with this period of evolution, beginning around 1.8 mya, is called the Acheulian Complex. Acheulian stone tools are more sophisticated than Oldowan tools, were produced from a wider variety of raw materials, and were fashioned into a greater range of tool types, with a greater range of functions. This diversity suggests increased familiarity with the necessary resources and with their availability. Within this diversity, the dominant tool is the handaxe (Figure 11.21). The handaxe’s sharp edge was used in cutting, scraping, and other functions.

In addition, the tools became increasingly refined— better made than before, they clearly required a great deal of both learning and skill to produce. Acheulian tools are found in association with large animals, suggesting that these tools were used to kill large animals and butcher them. In Ethiopia’s Middle Awash region, for example, tools are commonly associated with hippopotamus bones. In Olorgesailie, Kenya, the South African archaeologist Glynn Isaac recovered many baboon bones in addition to those of hippopotamuses, elephants, and other ani- mals. All these bones have cutmarks from stone tools. In addition, the tools from this and other Acheulian sites display microscopic patterns of wear that are the

FIGURE 11.20 Atapuerca 3 These remains, from Gran Dolina, are the subject of debate as some researchers believe that the juvenile they came from belonged not to H. erectus but to a new species of hominin, Homo antecessor. Others believe that despite its more modern appearance, this hominin belonged to H. erectus.

Ceprano

I TA LYI TA LY

Acheulian Complex The culture associated with H. erectus, including handaxes and other types of stone tools; more refined than the earlier Oldowan tools.

handaxe The most dominant tool in the Acheulian Complex, characterized by a sharp edge for both cutting and scraping.

TABLE 11.1 Trends from Homo habilis to Homo erectus

H. habi l is Ž H. erectus

Teeth Reduction in size

Face and jaws Reduction in size relative to size of braincase

Brain Increase in size

Browridge Increase in size

Cranial bone Increase in thickness

Body

Arms

Legs

Increase in size

Reduction in length

Increase in length

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same as those seen in experimental studies where anthropologists have butchered animals. Clearly,  H.  erectus had killed, processed, and eaten the animals at these sites, well before 1 mya (Figure 11.22). This record, from Olorgesailie and sites like it, indicates that hunting was well in place by the Middle Pleistocene. If body size increase was tied to acquisition of animal protein via hunting, it was well in place by somewhat greater than 1.5 mya.

In addition to the increase in body size, a key difference between  H.  habilis and H. erectus is the latter’s much larger brain. From H. habilis to H. erectus, brain volume increased by 33% (from 650 cc to 950 cc). Some of the enlargement in brain size was due simply to the increase in body size generally. But even when accounting for the body size increase, there was still an increase in brain size. The increase in sophistication of technology and other cultural changes seen after 2  mya or so strongly suggests that this increase in brain size reflects an increase in intelligence and cognitive abilities generally. Simply, the adaptation of H. erectus placed an emphasis on intelligence, and there was likely a selective advantage for the cognitively advanced behaviors that characterized this hominin.

Anthropologists are keenly interested in the nature of the energy intake that would have been required to grow these very brainy ancestors. That is, the brain is an energetically “expensive” tissue. What did these hominins eat that “paid” the high energetic cost of a large brain? While a number of factors are likely to have operated, improved nutritional quality is central to understanding how the cost of increasing brain size was paid. Nutrition improved as a result of meat consumption and the rich source of protein that it provided. The British primatologist Richard Wrangham contends that H. erectus was adapted to eating cooked meat and other cooked foods. These rich sources of energy would help explain the increases in brain size and body size. Cooking increases the digestibility of meat and other foods and improves the quality of the energy that it gives the eater.

Cooking would have required the ability to make and control fire. There are various claims for the early use of fire. By analyzing sediments from Wonderwerk Cave, in South Africa, the Italian archaeologist Francesco Berna and his associates have determined that H. erectus made and used fire by 1 mya (Figure 11.23). The

FIGURE 11.21 Olorgesailie (a) At this Acheulian site in Kenya, the remains of hundreds of butchered animals were found along with many handaxes and other tools. (b) This close- up shows the stone tools, with the handaxes in the middle.

(a) (b)

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researchers’ discovery of burned animal bones and plant remains in association with Acheulian tools indicates that these hominins used fire for primarily cooking. Fire may also have been used at Zhoukoudian, but the evidence from that locality is unclear and does not appear to have been made or controlled by human activity. That is, animal remains and stone tools are burned, but the type of burning is not associated with fire produced by hominins.

Fire also played a vital role in hominins’ adaptation to regions of the globe where the temperature is cold much or all of the year. The controlled use of fire made possible a major expansion in where people could live and the manner in which they prepared their food. Thus, while there is not clear evidence for the use of fire at Zhoukoudian, hominins most likely had to have made and controlled fire in order to live there, especially during cold periods of the year.

Most importantly, however, H. erectus used fire to cook food. Before using fire, hominins ate plants and animals raw. But cooking these foods made them easier to chew and, as a result, made the very powerful jaws and large teeth of H. erectus’s

FIGURE 11.22 Butchering This artist’s reconstruction shows how early Homo likely processed animals in groups, using a variety of stone tools. (© 1995 by Jay H. Matternes)

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predecessors less necessary. Indeed, the jaws and teeth of these Middle Pleistocene hominins were smaller than earlier hominins’. This size reduction was almost cer- tainly related to the cultural innovations of the Middle Pleistocene, including both controlled use of fire and more advanced tool technology. These cultural devel- opments were the harbingers of increasing environmental control and improved adaptive success, both of which form an ongoing theme of human evolution.

Another potential means of improving dietary quality and energy intake is food- sharing. In this case, males would have hunted for meat and subsequently shared it with females and dependent children. Indeed, an extensive ethnographic record for living societies shows that food- sharing happened in this manner universally. It is likely that this kind of provisioning was an essential element of increased access to high- quality nutrition. Thus, food- sharing, meat- eating, and cooking help explain the increase in brain size in human evolution, beginning especially with H. erectus.

PATTERNS OF EVOLUTION IN HOMO ERECTUS Comparisons of all the  H.  erectus fossils from Africa, Asia, and Europe reveal important information about this early Homo species, both in general similarities across these continents and in the individual forms’ evolution. H. erectus skulls are long, low, and wide at the base; and they have thick bone and large browridges. The African H. erectus tends to be the most robust, with the largest and thickest cranial bones. The Dmanisi and African forms are strongly similar— the sagittal keel, for example, is missing in Dmanisi and present only rarely in the African represen- tatives. Morphological variations are likely related to differences in time and in geography, but the degree of variability is far smaller than that in other mammals.

Some authorities have interpreted the general similarity of  H.  erectus across Africa, Asia, and Europe and through time as representing evolutionary stasis. However, various morphological attributes show significant evolution in H. erectus,

FIGURE 11.23 Wonderwerk Cave, South Africa This site may contain the earliest evidence for the controlled use of fire by early hominins.

G E R M A N Y

Mauer

K E N YA

Olorgesailie

with earlier forms having considerably smaller brains than later forms. For exam- ple, the average Dmanisi skull is 650 cc, while the average Zhoukoudian skull is 1,200 cc. Overall,  H.  erectus’s brain size increased by some 30%. The American physical anthropologist Milford Wolpoff has also documented decreases in cranial bone thickness and browridge size. These characteristics indicate a decline in skull robusticity. Accompanying these changes is a reduction in tooth size, caused by the decreased demand on the face and jaws due to the increasing importance of technology and of cooking.

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C O N C E P T C H E C K !

Homo erectus: Beginning Globalization

Homo erectus was the first hominin to inhabit territory all over the Old World. After first evolving in Africa, it spread rapidly to Asia and then to Europe. Increased intelligence, increased dependence on technology and on material culture, social hunting, and access to more protein and to better nutrition contributed to this early hominin’s remarkable adaptive success.

Location/Sites Africa (Olduvai Gorge, Lake Turkana, Ileret, Bouri, Buia, Bodo, Olorgesailie); Asia (Dmanisi, Kocabaş, Trinil, Sangiran, Sambungmacan, Gongwangling, Majuangou, Zhoukoudian); Europe (Gran Dolina, Mauer, Boxgrove)

Chronology 1.8 mya– 300,000 yBP in Africa

1.8 mya– 300,000 yBP in Asia

1.2–.4 mya in Europe

Biology and Culture (compared with Homo habilis)

Feature Evidence Outcome

Tool use (Acheulian)

Skulls Teeth

Smaller face and smaller jaws Reduced size

Fire and cooking Ash in habitation sites Smaller face and smaller jaws

Intelligence Brain size Increase (average 950 cc)

Hunting and increased meat protein

Butchered large animals

Increased body size

Possible cannibalism Cutmarks New ritual or dietary innovation

Growth Enamel perikymata Slower growth but not modern

Locomotion Leg length:arm length Fully modern striding

(Photo © 1996 David L. Brill, humanoriginsphotos.com)

304 | CHAPTER 11 The Origins and Evolution of Early Homo

Hominins’ increasing reliance on tools profoundly affected human biology. As tools began to perform the face’s and jaws’ functions in preparing food for consumption— that is, in cutting up, cooking, and processing meat and other food— there was a commensurate decline in the robusticity of these body parts, the anatomical area associated with mastication. In terms of both culture and biol- ogy,  H.  erectus evolved the contextual behavior— hunting, successful dispersal across large territory, adaptive success, and increasing dependence on and effective use of cul- ture as a means of survival. The increased dependence on culture and the dominance of behaviors requiring technology in acquiring and processing food increased the diversity of environments occupied by H. erectus. The expansion of resources acquired and habitats occupied, coupled with the high degree of mobility, laid the basis for a high level of gene flow and the presence of a limited number of species— most likely, one species. The next chapter tracks and interprets the evolution of that species, H. sapiens.

A N S W E R I N G T H E B I G Q U E S T I O N S

C H A P T E R   1 1 R E V I E W [INSERT INQUIZITIVE LOGO/TEXT HERE]

What characteristics define the genus Homo? • The genus Homo is defined on the basis of physical

(biological) and behavioral attributes, including a relatively large brain, small face and jaws, and dependence on material culture for survival.

What were the earliest members of the genus Homo? • The earliest members of the genus Homo were

Homo habilis and Homo erectus. • Fossils of H. habilis have been found in East Africa

and South Africa and date to about 2.5–1.8 mya. • H. erectus, a geographically and morphologically diverse

species, dates to about 1.8 mya– 300,000 yBP. Its fossil record is represented in Africa, Asia, and Europe.

What are the key evolutionary trends and other developments in early Homo? • Compared to the australopithecines, early H. habilis

experienced an enlargement of the brain and a general gracilization of the chewing complex. These developments were linked with an increased focus on tool production and tool use, increased dietary diversity, and increased intelligence.

• Compared with H. habilis, H. erectus experienced a continued reduction in size of the chewing complex (smaller face, jaws, and teeth), increased brain size, increased body size, and the first evidence of modern limb proportions.

• H. erectus developed an increasingly innovative and complex technology, including more elaborate tools, organized social hunting, and controlled use of fire. These developments facilitated greater access to protein and improved nutrition generally. Improved nutrition likely explains the rapid increase in body and brain size around 2.0–1.7 mya. These developments are part of the larger picture of increasing adaptive flexibility, a central theme of human evolution.

• Homo increasingly became a predator genus in the early Pleistocene, and this change at least partly explains its remarkable and rapid geographic expansion. Successful predation was largely from hunting, but early Homo likely acquired food through hunting and scavenging.

• The evolution of H.  erectus— with its increased intelligence and full commitment to material culture as an adaptive strategy— set the stage for the emergence and evolution of Homo sapiens.

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Acheulian Complex handaxe

Homo erectus Pithecanthropus erectus

sagittal keel

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E V O L U T I O N R E V I E W The Origins of Homo

Synopsis The earliest members of our genus, Homo, arose nearly 2.5 mya and were characterized by an increase in brain size and a stronger reliance on material culture for survival. Key anatomical changes in Homo habilis— such as a larger brain, a less robust jaw, and smaller teeth— highlight the growing importance of tool use and dietary diversity as adaptations in the genus Homo. Homo erectus became the first hominin species to spread out of Africa to Europe and Asia, a global dispersal made possible by anatomical and cultural adaptations, including increased brain size, larger body size, more complex tool technology, use of fire for cooking, and emergence of hunting behaviors. The first members of Homo exhibited a series of evolutionary trends that set the stage for the ongoing evolution of the genus and the eventual emergence of our own species, Homo sapiens.

Q1. Name the three features outlined in this chapter that set the earliest member of our genus,  H.  habilis, apart from the aus- tralopithecines and that are defining characteristics of the genus Homo.

Q2. In some ways, the differences between H. erectus and H. habilis are more pronounced than those between  H.  habilis and the latest australopithecines. Provide three examples of anatomical characteristics in H. erectus that differ substantially from those observed in H. habilis. What are the evolutionary trends in these characteristics that are seen between these two species?

Q3. What are some of the roles that tool use and climate change may have played in shaping the adaptive flexibility (and evolutionary success) of H. habilis relative to the species of australopithecines living at the same time?

Hint Climate change in the early Pleistocene led to the spread of a grassland environment as well as increasing habitat and resource diversity.

Q4 . H. erectus is characterized by substantial changes in body size, brain size, material culture, and dietary and behavioral flexibility compared to earlier hominin species. Rather than being unidirec- tional (e.g., increased brain size leads to complex material culture but not the other way around), how might all of these changes be part of an evolutionary feedback loop driven by biocultural adaptation?

Hint Consider the ways that certain behaviors emerging in H. erectus may have had anatomical, physiological, and nutri- tional effects, as well as the ways in which these effects may have further influenced behavioral flexibility.

Q5. H. erectus was the first hominin species to spread out of Africa to other areas of the globe. Use specific biological and cultural features and the concepts of survival, reproduction, and migration to explain why H. erectus was the first species capable of such a widespread existence.

A D D I T I O N A L R E A D I N G S

Antón,  S.  C.  2003. A natural history of Homo erectus. Yearbook of Physical Anthropology 46: 126–170.

Antón,  S.  C.  and  C.  C.  Swisher  III.  2004. Early dispersals of Homo from Africa. Annual Review of Anthropology 33: 271–296.

Dunsworth, H. and A. Walker. 2002. Early genus Homo. Pp. 419–435 in  W.  C.  Hartwig, ed. The Primate Fossil Record. Cambridge, UK: Cambridge University Press.

McHenry,  H.  M.  and  K.  Coffing. 2000. Australopithecus to Homo: transformations in body and mind. Annual Review of Anthropology 29: 125–146.

Rightmire,  G.  P.  1990. The Evolution of Homo erectus. Cambridge, UK: Cambridge University Press.

Shapiro,  H.  L.  1974. Peking Man: The Discovery, Disappearance and Mystery of a Priceless Scientific Treasure. New  York: Simon & Schuster.

Shipman, P. 2001. The Man Who Found the Missing Link. New York: Simon & Schuster.

Shipman, P. and P. Storm. 2002. Missing links: Eugène Dubois and the origins of paleoanthropology. Evolutionary Anthropology 11: 108–116.

IN THIS RECONSTRUCTION, a Neandertal child from Roc- de- Marsal, in Dordogne, France, shows a mix of modern and archaic features. Neander- tals are central to our understanding of the origins and evolution of modern humans, including key aspects of human growth and development. (© 2003 Photographer P. Plailly/E. Daynès/ Eurelios— Reconstruction Elisabeth Daynès, Paris)

Feldhofer Cave

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12 What is so modern about modern humans?

What do Homo sapiens fossils reveal about modern humans’ origins?

How has the variation in fossil H. sapiens been interpreted?

What other developments took place in H. sapiens’ evolution?

The Origins, Evolution, and Dispersal of Modern People

The Feldhofer Cave Neandertal was the first fossil hominin to receive serious attention from scientists. Prior to its (accidental) discovery in 1856, answers to questions about the physical characteristics and behaviors of human ances- tors were highly speculative. The uncovering of this skeleton signaled a change for anthropology. Feldhofer Cave is located in Neander Valley (in German, Neander Tal), near Düsseldorf, Germany. Workers happened upon the skeleton while removing clay deposits from the cave as part of a limestone quarrying operation. Sometimes acci- dental discoveries like this are reported; often, they are not. The world of anthropology got very lucky because these workers picked up the skull and bones and took them to a local schoolteacher. As luck further had it, the teacher recognized these remains as human and passed them on to the anthropologist Hermann Schaafhausen, at the University of Bonn. Schaafhausen studied the remains, quickly reported his findings to the German Natural History Society, and published a description in a leading Ger- man scientific journal. He described a skull having some archaic features, distinctive from modern humans’. In particular, the skull was long and low, different from modern people’s but with some similarities, such as in brain size (Figure 12.1). Moreover, the skeletal remains of extinct Pleistocene animals also found in the cave indicated that this human had lived at the same time as these animals. At the time these breathtaking announcements were made, many authorities believed that humans had appeared very

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recently in the history of life, certainly postdating extinct animals associated with the great Pleistocene Ice Age.1

Schaafhausen and the Neandertal skeleton caught the attention of the leaders of science in Germany and around the world. One of these leaders was the top Ger- man anthropologist of the time, Rudolf Virchow (Figure 12.2). In addition to being a leading authority on evolutionary theory, archaeology, and cultural anthropology, Virchow started the discipline of cell pathology (diseases of cells). He helped found several national scientific organizations and periodicals. He was a medical activ- ist, a political leader known across Germany, and the teacher of others who would become leaders in science and medicine. In short, his pronouncements about the Feldhofer Cave skeleton would be taken very seriously by scientists. After looking carefully at the remains, he summarily dismissed any notion that they belonged to an ancestor of living humans. He argued that their characteristics— a long, low skull and bowed, thick limb bones— were those of some modern human afflicted with rickets and arthritis. Others disagreed. Thomas Henry Huxley (see Figure 2.17) argued that this was a primitive, potentially ancestral human. But Virchow was convincing to most, setting the course for years; later, scores of remains showing the same mor- phology as the Feldhofer Cave skeleton and dating to the same period of the late Pleistocene were found. Eventually, Virchow’s pathology hypothesis was rejected, and debate centered around the role of the Feldhofer Cave skeleton and others like it— a group of hominins we call “Neandertals”—in later human evolution.

In this chapter, we will look at Homo sapiens’ evolution, from its origins in Homo erectus to its development into modern humans. Neandertals play a central role in this discussion, which is also based on rich records— of fossils, genetic variation,

1Excavations at the Feldhofer Cave in 1997 and 2000 produced more than 62 new bone fragments that are part of the original skeleton, of at least one other adult, and of a young juvenile. Radiocarbon dates on these new bones indicate that this Neandertal is about 40,000 years old.

FIGURE 12.1 Feldhofer Neandertal This Neandertal’s DNA has been used recently to test hypotheses concerning the genetic relationship between modern humans and Neandertals.

FIGURE 12.2 Rudolf Virchow Virchow made an influential but wrong pronouncement about the Feldhofer Neandertal skeleton. Among his many achievements was being the first researcher to recognize leukemia, a cancer of the blood and of bone marrow.

Modern Homo sapiens: Single Origin and Global Dispersal or Regional Continuity? | 309

culture, and behavior— from around the world. First, though, we will explore which aspects of the fossil record indicate the first appearance of modern people. Then we will examine those aspects, to understand just how anthropologists interpret the variation across the bones and teeth of H. sapiens.

What Is So Modern about Modern Humans? What do physical anthropologists mean by modern? This question is very impor­ tant because the answer to it provides us with the baseline from which to assess the origins, evolution, and geographic distribution of modern H. sapiens. Physical anthropologists define modern based on a series of distinctive anatomical char­ acteristics that contrast with archaic characteristics found in earlier hominins. Modern people— people who essentially look like us— tend to have a high and ver­ tical forehead, a round and tall skull, small browridges, a small face, small teeth, and a projecting chin (anthropologists call the latter a “mental eminence”). Below the neck, modern humans have relatively more gracile, narrower bones than their predecessors. Fossil humans having these cranial and postcranial characteristics are considered modern H. sapiens.

The immediate ancestors of modern people— archaic  H.  sapiens— differ from modern H. sapiens. Compared to modern H. sapiens, archaic H. sapiens have a lon­ ger and lower skull, a larger browridge, a bigger and more projecting face, a taller and wider nasal aperture (opening for the nose), a more projecting occipital bone (sometimes called an occipital bun when referring to Neandertals), larger teeth (especially the front teeth), and no chin. The postcranial bones of archaic H. sapiens are thicker than modern people’s.

Some hominin skeletons dating to the Upper Pleistocene have a mixture of archaic and modern features. The Skhul 5 skeleton, from Israel, is an excellent example of a hominin with archaic features, including a somewhat forward­ projecting face and pronounced browridges, and modern features, such as a dis­ tinctive chin and no occipital bun (see Figure  12.33). Similarly, the Herto skulls, from Ethiopia, have a combination of archaic and modern features, although the modern features dominate over the archaic ones. Their skulls’ modern character­ istics indicate that the Skhul and Herto hominins were on the verge of modernity or were very early modern  H.  sapiens, perhaps the earliest in western Asia and Africa, respectively.

Modern Homo sapiens: Single Origin and Global Dispersal or Regional Continuity? H. sapiens’ evolution begins with the emergence of archaic forms, some 350,000– 500,000 yBP.  These early  H.  sapiens provide the context for modern  H.  sapiens’ evolutionary development, which took place at different times in different places. The first modern H. sapiens appeared earliest in Africa, by 160,000 yBP, and latest

occipital bun A cranial feature of Nean- dertals in which the occipital bone projects substantially from the skull’s posterior.

310 | CHAPTER 12 The Origins, Evolution, and Dispersal of Modern People

in Europe. The transition to fully modern  H.  sapiens was completed globally by about 25,000 yBP.

Two main hypotheses have emerged to explain modern people’s origins (Figure  12.3). The Out- of- Africa hypothesis states that modern  H.  sapiens first evolved in Africa and then spread to Asia and Europe, replacing the indigenous archaic  H.  sapiens populations living on these two continents. The Multiregional Continuity hypothesis regards the transition to modernity as having taken place regionally and without involving replacement. From this point of view, African archaic H. sapiens gave rise to African modern H. sapiens, Asian archaic H. sapiens gave rise to Asian modern H. sapiens, and European archaic H. sapiens gave rise to European modern H. sapiens. Both models seek to explain why today human beings consist of just one genus and why that genus consists of just one species. The models differ, though, in accounting for that genus and species.

The Out­ of­ Africa model explains the single species of living humans by emphasizing a single origin of modern people and eventual replacement of archaic  H.  sapiens throughout Africa, Asia, and Europe. A simple story. The Multiregional Continuity model emphasizes the importance of gene flow across population boundaries— separate species of humanity never arose owing to the constant interbreeding of human groups throughout human evolution. Not such a simple story.

Fossil and genetic records provide a wealth of information about modern human origins. We will now consider these records and draw some conclusions from them. We will then be ready to reassess the two hypotheses and to draw further conclu­ sions about the origins of us— living people.

FIGURE 12.3 Out- of- Africa vs. Multiregional This important anthropological debate is about modern humans’ origins. (a) This chart depicts one of the two hypotheses, Out- of- Africa, according to which modern humans originated in Africa and then migrated throughout the world. (b) This chart depicts the second hypothesis, Multiregional Continuity, according to which Homo erectus evolved into modern Homo sapiens in various geographic locations. The arrows represent continuous gene flow throughout human evolution. This hypothesis considers H. ergaster and H. heidelbergensis to be H. erectus and H. neanderthalensis to be H. sapiens. (b) Multiregional Continuity(a) Out-of-Africa

H. sapiensH. sapiens

H. neanderthalensis

H. heidelbergensis

H. erectus

H. ergaster

H. erectus

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What Do Homo sapiens Fossils Tell Us about Modern Human Origins? | 311

What Do Homo sapiens Fossils Tell Us about Modern Human Origins? The fossil remains of archaic H. sapiens have been found throughout Africa, Asia, and Europe. In Africa, archaic H. sapiens evolved into modern H. sapiens at least by 160,000 yBP, perhaps as early as 200,000 yBP. In Asia and Europe, the archaics consisted of an early group and a late group, divided very roughly at about 130,000 yBP. To understand the biological changes involved in hominin groups’ evolution, we need to compare some details of a number of key fossils.

EARLY ARCHAIC HOMO SAPIENS The earliest forms of  H.  sapiens emerged around 350,000 yBP.  They have been found in Africa, Asia, and Europe (Figure 12.4). Their evolution is clearly out of

Bodo

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AragoAtapuerca

Petralona

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Kabwe

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Dali

SteinheimSwanscombe

FIGURE 12.4 Early Archaic Homo sapiens This map illustrates some of the sites in Africa, Asia, and Europe where the remains of early archaic H. sapiens have been found. (Arago skull photo © David L. Brill, humanoriginsphotos.com)

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the earlier  H.  erectus populations. Anthropologists have documented this evolu­ tionary transition in the three continental settings, noting, for example, the sim­ ilarly massive browridges in archaic  H.  sapiens and in earlier  H.  erectus. Although quite primitive in key respects, all the fossils representing archaic  H.  sapiens and earlier  H.  erectus show continued reduction in skeletal robusticity, smaller tooth size, expansion in brain size, and increasing cultural complexity.

ARCHAIC HOMO SAPIENS IN AFRICA (350,000–200,000 YBP) One of several individuals found in the Kabwe (Broken Hill) lead mine in Zambia has enormous browridges, but the facial bones and the muscle attachment areas on the back of the skull for the neck muscles are quite small compared with those of H. erectus in Africa (Figure 12.5). The cranial capacity is about 1,300 cc. The skull is similar in appearance to those of early archaic hominins from Europe. Both the Zambian and the European skulls have erectuslike characteristics: a large face, large browridges, and thick cranial bones. However, H. erectus skulls, like their Asian counterparts, are higher, reflecting a brain expansion.

EARLY ARCHAIC HOMO SAPIENS IN ASIA (350,000–130,000 YBP) Some of the best­ known fossils representing early archaic H. sapiens are from the Ngandong site, on the island of Java (Figure 12.6). The skulls are represented by the brain­ cases only— the faces are missing. Ngandong 11 has a brain size of about 1,100 cc, well within the range for early archaic H. sapiens. The skull is long and low, but com­ pared with its H. erectus ancestor, the skull is somewhat higher, reflecting its larger brain. The browridge is massive, certainly on the order of many H. erectus examples.

The Ngandong skulls share a number of features with other Asian early archaic  H.  sapiens, especially with Narmada (Madhya Pradesh, India) and Dali (Shaanxi Province, People’s Republic of China) skulls (Figure 12.7). The crania are large and robust. The browridges are quite large, although not as large as in H. erectus.

FIGURE 12.5 Kabwe This archaic H. sapiens, also known as “Broken Hill Man” or “Rhodesian Man,” was among the first early human fossils discovered in Africa. Found by miners searching for metal deposits in caves, it was originally thought to be less than 40,000 years old.

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FIGURE 12.6 Ngandong Multiple skulls were found at this site in Java in the 1930s. The brain size of this early archaic Homo sapiens falls between those of Homo erectus and of modern humans.

FIGURE 12.7 Asian Early Archaic Homo sapiens Like the Ngandong cranium, the crania of (a) Narmada and (b) Dali are robust with thick cranial bones. The cranial capacity, however, indicates the brain size was much larger than in Homo erectus but somewhat smaller than in modern humans.

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EARLY ARCHAIC HOMO SAPIENS IN EUROPE (500,000–130,000 YBP) Dating to about 430,000 yBP, one of the most significant fossils for early archaic H. sapi- ens, and for all of human evolution, is from the Sima de los Huesos cave site, in the Sierra de Atapuerca, near Burgos, Spain. Among the 28 or so individuals from the cave is a wonderfully preserved skeleton of an adult male, Atapuerca 5. This is one of the few instances ever in which a fossilized individual’s skull (including the man­ dible) was found in direct association with the postcranial skeleton. The cranial capacity is about 1,125 cc. The skull has a large browridge and a pronounced facial projection. The nasal aperture is quite tall and wide. These features foreshadow the facial characteristics of the late archaic  H.  sapiens in Europe and far western Asia, the Neandertals (discussed below). Other well­ known early archaic H. sapi- ens fossils from Europe are the skull and other remains from Arago, France; the skull from Petralona, Greece; the skull from Steinheim, Germany (Figure 12.8); and the partial skull from Swanscombe, England. Their average cranial capacity is 1,200 cc. These early archaic H. sapiens illustrate the larger brain and rounder, more gracile skulls compared with H. erectus.

EARLY ARCHAIC HOMO SAPIENS’ DIETARY ADAPTATIONS The earliest archaic  H.  sapiens had many of the same kinds of tools and material technology as the earlier H. erectus, but H. sapiens used much more diverse tools to acquire and process food. Across the group, the face, jaws, and back teeth (premolars and molars) show a general reduction in size. The American physical anthropolo­ gist  C.  Loring Brace hypothesizes that selection for large back teeth lessened as tools became more important for processing food. Simply, with reduced selection, the teeth became smaller. Alternatively, as technological innovation changed the way teeth were used, the teeth may have been under greater selection for reduced size. Anthropologists have not reached a consensus on the mechanisms behind the reduction in tooth size except to say that cultural innovation and increased dependence on material culture likely played a role in this fundamental biological change.

At the same time that the importance of the back teeth diminished, the use of the front teeth increased. That is, during this period of human evolution, the front teeth— incisors and canines— underwent heavy wear. For example, in Atapuerca 5, from Spain, the upper incisors are worn nearly to where the gums would have been

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the earlier  H.  erectus populations. Anthropologists have documented this evolu­ tionary transition in the three continental settings, noting, for example, the sim­ ilarly massive browridges in archaic  H.  sapiens and in earlier  H.  erectus. Although quite primitive in key respects, all the fossils representing archaic  H.  sapiens and earlier  H.  erectus show continued reduction in skeletal robusticity, smaller tooth size, expansion in brain size, and increasing cultural complexity.

ARCHAIC HOMO SAPIENS IN AFRICA (350,000–200,000 YBP) One of several individuals found in the Kabwe (Broken Hill) lead mine in Zambia has enormous browridges, but the facial bones and the muscle attachment areas on the back of the skull for the neck muscles are quite small compared with those of H. erectus in Africa (Figure 12.5). The cranial capacity is about 1,300 cc. The skull is similar in appearance to those of early archaic hominins from Europe. Both the Zambian and the European skulls have erectuslike characteristics: a large face, large browridges, and thick cranial bones. However, H. erectus skulls, like their Asian counterparts, are higher, reflecting a brain expansion.

EARLY ARCHAIC HOMO SAPIENS IN ASIA (350,000–130,000 YBP) Some of the best­ known fossils representing early archaic H. sapiens are from the Ngandong site, on the island of Java (Figure 12.6). The skulls are represented by the brain­ cases only— the faces are missing. Ngandong 11 has a brain size of about 1,100 cc, well within the range for early archaic H. sapiens. The skull is long and low, but com­ pared with its H. erectus ancestor, the skull is somewhat higher, reflecting its larger brain. The browridge is massive, certainly on the order of many H. erectus examples.

The Ngandong skulls share a number of features with other Asian early archaic  H.  sapiens, especially with Narmada (Madhya Pradesh, India) and Dali (Shaanxi Province, People’s Republic of China) skulls (Figure 12.7). The crania are large and robust. The browridges are quite large, although not as large as in H. erectus.

FIGURE 12.5 Kabwe This archaic H. sapiens, also known as “Broken Hill Man” or “Rhodesian Man,” was among the first early human fossils discovered in Africa. Found by miners searching for metal deposits in caves, it was originally thought to be less than 40,000 years old.

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FIGURE 12.6 Ngandong Multiple skulls were found at this site in Java in the 1930s. The brain size of this early archaic Homo sapiens falls between those of Homo erectus and of modern humans.

FIGURE 12.7 Asian Early Archaic Homo sapiens Like the Ngandong cranium, the crania of (a) Narmada and (b) Dali are robust with thick cranial bones. The cranial capacity, however, indicates the brain size was much larger than in Homo erectus but somewhat smaller than in modern humans.

)b()a(

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in life (Figure  12.9). This evidence tells us that these hominins used their front teeth as a tool, perhaps as a kind of third hand for gripping materials. In European archaic  H.  sapiens, the front teeth show a size increase. The link between heavy use of the front teeth and increase in size of these teeth suggests the likelihood of selection for large front teeth.

LATE ARCHAIC HOMO SAPIENS The hominins from this period show a continuation of trends begun with early Homo, especially increased brain size, reduced tooth size, and decreased skeletal robusticity. However, in far western Asia (the Middle East) and Europe, a new pattern of morphology emerges, reflecting both regional variation and adaptation

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FIGURE 12.10 West Asian Late Archaic Homo sapiens This map illustrates where late archaic H. sapiens’ remains have been found in western Asia, along the eastern Mediterranean Sea.

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(a) (b) (c)

FIGURE 12.8 European Early Archaic Homo sapiens Cranial remains from three prominent European sites—(a) Arago, (b) Petralona, and (c)  Steinheim— have somewhat larger cranial capacities than other early archaic H. sapiens. Although these crania reflect a more modern appearance, they retain primitive features such as larger browridges. (Photo [a] © 1985 David L. Brill, humanoriginsphotos.com)

to cold. This new pattern defines the Neandertals. Neandertal features include wide and tall nasal apertures; a projecting face; an occipital bun; a long, low skull; large front teeth (some with heavy wear); a wide, stocky body; and short limbs.

The fossil record of the late archaic H. sapiens is fascinating. For the first time in human evolution, a number of fairly complete skeletons exist, allowing new insights into the biology and behavior of these ancient humans. Moreover, the material culture includes new kinds of tools, and reflects new behaviors, that are modern in several important ways.

LATE ARCHAIC HOMO SAPIENS IN ASIA (60,000–40,000 YBP) For Asian late archaic H. sapiens, the record is fullest from sites at the far western end of the continent (Figure 12.10). Fossils from Israel form the core of discussions among

FIGURE 12.9 Atapuerca 5 One of many human skeletal remains found in Sima de los Huesos, Atapuerca 5 represents a nearly complete adult male skeleton. Its cranial capacity falls within the range of other Pleistocene humans, but its cranium is unusual in its degree of tooth wear. Notice that the front tooth is worn— that it has very little enamel left.

in life (Figure  12.9). This evidence tells us that these hominins used their front teeth as a tool, perhaps as a kind of third hand for gripping materials. In European archaic  H.  sapiens, the front teeth show a size increase. The link between heavy use of the front teeth and increase in size of these teeth suggests the likelihood of selection for large front teeth.

LATE ARCHAIC HOMO SAPIENS The hominins from this period show a continuation of trends begun with early Homo, especially increased brain size, reduced tooth size, and decreased skeletal robusticity. However, in far western Asia (the Middle East) and Europe, a new pattern of morphology emerges, reflecting both regional variation and adaptation

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FIGURE 12.10 West Asian Late Archaic Homo sapiens This map illustrates where late archaic H. sapiens’ remains have been found in western Asia, along the eastern Mediterranean Sea.

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Arago Atapuerca

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anthropologists about modern people’s emergence in western Asia. This record pertains to Neandertals from Amud, Kebara, and Tabun. The Amud Neandertals date to about 55,000–40,000 yBP and are best known from the complete skele­ ton of an adult male. He had an enormous brain, measuring some 1,740 cc, larger than earlier humans’ and the largest for any fossil hominin (Figure  12.11). The Kebara Neandertals date to about 60,000 yBP and are represented by a complete mandible  and body skeleton; the legs and cranium are missing (Figure  12.12). A  nearly complete female Neandertal skeleton from Tabun was long thought to date to about the same time, but new thermoluminescence dating indicates that the skeleton may be as old as 170,000 yBP. Like the Amud male, she had a large brain.

The Amud and Tabun skulls have a number of anatomical characteristics that are strongly similar to those of contemporary populations of late archaic H. sapiens in Europe. For example, their eye orbits tend to be small and round, their nasal openings are tall and wide, and their faces project forward. These two skulls share a number of modern characteristics, however, such as the lack of the occipital bun and the presence of relatively small teeth.

Some of the most interesting Neandertals are from the Shanidar site, in north­ ern Iraq’s Kurdistan region. These Neandertals— seven adults and three young children— have provided important insight into the lives, lifestyles, and cultural practices of late archaic H. sapiens. Shanidar 1, an older adult male dating to at least 45,000 yBP, is one of the most complete skeletons from the site (Figure  12.13). The face is that of a typical Neandertal, especially in its wide nasal aperture and forward projection. This individual’s life history is written in his bones. A frac­ ture on his upper face, well healed at the time of his death, may have been severe enough to cause blindness. Severe arthritis in his feet might have resulted from the constant stresses of traversing difficult, mountainous terrain.

Shanidar 1’s upper incisors are severely worn, probably from his use of the front teeth as a tool for grasping and holding objects in the same or a similar way as the much earlier hominin from Atapuerca. This extramasticatory wear on the front teeth is determined by culture— Neandertals used their front teeth as a part of their “tool kit.” Use of the front teeth as a tool has remained a hallmark of human behavior into recent times in a wide variety of cultures, ranging from Eskimos, who chew hides for clothing and other material culture, to Native Americans, who chew plant material to prepare it for basketry.

Shanidar 1 may have had personal reasons for using his front teeth as a tool. When he was excavated, by the American archaeologist Ralph Solecki in the late 1950s, his lower right arm was missing. The American physical anthropol­ ogist  T.  Dale Stewart suggested that the lower arm may have been either ampu­ tated or accidentally severed right above the elbow. The humerus was severely atrophied, probably owing to disuse of the arm during life. The loss of the use of the arm meant that Shanidar 1 had to use his teeth to perform some simple func­ tions, such as eating or making tools. His survival likely depended on the use of his front teeth.

LATE ARCHAIC HOMO SAPIENS IN EUROPE (130,000–30,000 YBP) The Euro­ pean late archaic H. sapiens, Neandertals, are some of the best­ known, most­ studied fossil hominins in the world (Figure  12.14). Owing to the relative completeness of the fossil record, paleoanthropologists have been able to document and debate the meaning of their physical characteristics. The Neandertal record begins in

FIGURE 12.11 Amud Neandertal The large brain size suggests that Neandertals’ intelligence was on par with modern Homo sapiens’. The exceptionally large cranial capacity of the Amud Neandertal indicates that this hominin’s brain was at least as large as a modern human’s.

FIGURE 12.12 Kebara Neandertal The almost complete skeletal torso of this hominin was discovered in Kebara Cave, Israel. Even without a cranium and legs, this is one of the most complete Neandertal skeletons found to date. (Photo © David L. Brill, humanoriginsphotos.com)

eastern Europe, at the Krapina site in Croatia, dating to 130,000 yBP. The record ends with fossils from Vindija, Croatia, dating to 32,000 yBP or somewhat later.

Like many Neandertal remains, the Krapina fossils were excavated more than a century ago. Not all such early excavations were carefully done. Fortu­ nately, the excavator of the Krapina site— the Croatian paleontologist Dragutin Gorjanović­Kramberger (see Figure  8.11)—was extraordinarily meticulous in his recording of the excavation. During the period in which he excavated the site, 1899–1905, he kept detailed notes about where his workers found fossils and stone tools. He was especially careful in recording the stratigraphic locations of the several hundred bones and teeth found at the site.

The Krapina remains were recovered from a series of strata inside a rockshelter (not quite a cave— a rock overhang provides protection from the elements). The remains are highly fragmentary, making it difficult to identify key physical char­ acteristics. The most complete cranium, Krapina 3, has the typical Neandertal features: round eye orbits, wide space between the eye orbits, wide nasal aperture, and protruding midfacial region (Figure 12.15). The Krapina front teeth are the largest of any known fossil hominin. In fact, tooth size comparisons with earlier and later humans in Europe indicate that in these Neandertals the front teeth had increased and the back teeth had decreased. The front teeth are some of the biggest in human evolution.

Anterior tooth wear indicates that the front teeth were being used as tools.

This individual has typical Neandertal characteristics, including large browridges and a large nasal aperture.

Atrophy of the right humerus (left humerus shown for comparison) may have resulted from an injury. The lower arm was likely amputated.

FIGURE 12.13 Shanidar 1 Neandertal The skeleton of this older adult Neandertal tells a life story of injury owing to accidents and violence. The majority of Neandertal skeletons have injuries.

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The Krapina bones are mostly in fragments. The Ameri­ can anthropologist Tim White has found that some of these fragments display a series of distinctive cutmarks in places where ligaments (the tissue that connects muscle to bone) were severed with stone tools. The location and pattern of cutmarks on the Krapina Neandertal bones are identical to those on animal bones found at the site. That strategically placed cutmarks appear on human and animal bones indi­ cates that these people ate animal and human tissue.

The Krapina Neandertals were not the only ones to practice cannibalism. At the Moula­ Guercy cave, in south­ eastern France, six individuals dating to about 100,000 yBP display cutmark patterns very similar to those on the animal remains at the site. At El Sidrón in northern Spain, Spanish archaeologist Antonio Rosas and his research team have documented patterns of cutmarks on cranial and postcranial bones involving removal of tissue and marrow extraction in a dozen individuals dating between 40,000 and 50,000 yBP. Unlike other settings where the human and animal bones are mixed, the Neandertal remains at El Sidrón are not asso­ ciated with animal remains, and they are located in a remote area of a complex system of caves.

FIGURE 12.14 Neandertal Sites This map illustrates the various locations of Neandertal discoveries throughout southern and middle Europe and the Middle East as well as the suggested boundaries of the Neandertal range.

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Neandertal site Boundary of Neandertal world

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FIGURE 12.15 Krapina Neandertal This Krapina cranium has many features associated with Neandertals. Can you identify the key features that characterize it as Neandertal? (Photo © David L. Brill, humanoriginsphotos.com)

Scientists cannot explain why cannibalism was practiced, but perhaps Nean­ dertals ate human flesh to survive severe food shortages during their occupation of Ice Age Europe.

Many Neandertal skeletons, including some of the best known from western Europe, are relatively late, postdating 60,000 yBP. The skeleton from La Chapelle­ aux­ Saints, France, is especially well known because anthropologists used it as the prototype for all Neandertals in the early twentieth century. It has the character­ istic Neandertal cranial morphology, including a very wide and tall nasal aperture, a projecting midface, an occipital bun, and a low, long skull (Figure 12.16).

THE NEANDERTAL BODY PLAN: ABERRANT OR ADAPTED? The La Chapelle­ aux­ Saints skeleton is also one of the most complete Neandertals. The skeleton was first described in great detail by the eminent French paleoanthropol­ ogist Marcellin Boule (1861–1942) in the early 1900s. Professor Boule’s scientific writings tremendously influenced contemporary and later scientists’ interpreta­ tions of Neandertal phylogeny, behavior, and place in human evolution generally, basically continuing the earlier opinions expressed by Virchow (discussed at the start of this chapter). Boule argued that the Neandertal cranial and postcra­ nial traits were simply too primitive and too different from modern people’s to have provided the ancestral basis for later human evolution (Figure  12.17). He concluded that the La Chapelle individual must have walked with a bent­ kneed gait— as in chimpanzees that walk bipedally— and could not have been able to speak. Simply, in his mind, Neandertals represented some side branch of human evolution— they were too primitive, too stupid, and too aberrant to have evolved into modern humans.

Boule’s interpretations led to the prevailing view at the time (still held by some authorities) that Neandertals were evolutionary dead ends, replaced by the

FIGURE 12.16 La Chapelle- aux- Saints Neandertal Like Shanidar 1, this skeleton shows evidence of healed injuries and arthritis.

(a) (b)

FIGURE 12.17 Neandertal Depictions (a) The La Chapelle- aux- Saints skeleton, here fleshed out by an illustrator in 1909, reinforced the notion that Neandertals were too stupid and too brutish to have evolved into modern humans. (b) More recent reconstructions show that Neandertals looked very similar to modern humans in many respects. In addition, estimates of brain size put them squarely within the modern human range.

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emerging modern humans and representing distant cousins of humanity that were not able to survive. In rejecting this view, we should take a closer look at some topics Boule addressed in his study of the La Chapelle skeleton.

One very distinctive feature of Neandertal faces is the enormous nasal aperture (Figure  12.18). The great size of the nasal aperture in many Neandertal fossils indicates that these people had huge noses, in both width and projection. Such massive noses were one of the cranial characteristics that led Boule to believe that Neandertals were not related to later humans in an evolutionary sense. However, nasal features are more likely part of an adaptive complex reflecting life in cold climates during the Upper Pleistocene. The shape and size of any nose is an excel­ lent example of the human face’s highly adaptable nature, especially in relation to climate. One of the nose’s important functions is to transform ambient air— the air breathed in from the atmosphere— into warm, humid air. Large noses have more internal surface area, thus providing an improved means of warming and moistening the cold, dry air that Neandertals breathed regularly. Moreover, the projecting nose typical of Neandertals placed more distance between the cold external environment and the brain, which is temperature­ sensitive. Alternatively, the large noses of Neandertals may simply be due to the fact that their faces are so large. Regardless of the circumstances resulting in Neandertals’ having large nasal apertures, many people and populations around the world today have wide, big noses, which are integral parts of their robust faces. These attributes are not uniquely Neandertal (Figure 12.19).

Other features of Neandertal skeletons are consistent with cold adaptation. For example, the infraorbital foramina— the small holes in the facial bones located beneath the eye orbits— are larger in European Neandertals than in modern peo­ ple (Figure 12.20). The foramina’s increased size is due to the blood vessels that tracked through them having been quite large. The larger blood vessels may have allowed greater blood flow to the face, preventing exposed facial surfaces from freezing.

FIGURE 12.18 Nasal Aperture The large nasal aperture of Neandertal crania, such as this cranium from Gibraltar, may have been a cold adaptation.

FIGURE 12.19 Modern Human Relatives? Some of the morphological traits associated with Neandertals can be found in modern humans, as illustrated by this photograph of the physical anthropologist Milford Wolpoff facing the reconstructed head of a European Neandertal. Might Neandertals have interbred with modern human ancestors, passing along some of these traits?

Large infraorbital foramen

Large nasal aperture

Large prominent nasal bones

Low forehead

Occipital bun

FIGURE 12.20 Cold Adaptive Traits Large infraorbital foramina are among the Neandertal traits that likely were responses to a cold environment during the later Pleistocene. Note also the distinctive Neandertal traits— low forehead and projecting occipital (occipital bun).

Most distinctive about the cold adaptation complex in Neandertals are the shape of the body trunk and the length of the arms and legs. Compared with mod­ ern humans, European Neandertals were stocky— the body was short, wide, and deep (Figure 12.21). Neandertals’ limbs were shorter than earlier or later humans’. This combination— stocky trunk and short limbs— is predicted by Bergmann’s and Allen’s rules (see “Climate Adaptation: Living on the Margins” in chapter 5). That is, animals that live in cold climates are larger than animals that live in hot cli­ mates (Bergmann’s rule). The larger body trunk reduces the amount of surface area relative to the body size. This helps promote heat retention. Moreover, animals that live in cold climates have shorter limbs than animals that live in hot climates (Allen’s rule). This, too, promotes heat retention in cold settings.

The American physical anthropologist Christopher Ruff has refined these concepts in interpreting human body shape morphology. He discovered that adaptation to heat or cold is not related to a person’s height— some heat­ adapted populations are quite tall, and some are quite short. Much more important is the width of the body trunk (usually measured at the hips), because the ratio of surface area to body mass is maintained regardless of height (Figure 12.22). This finding is borne out by a wide range of populations around the world today: populations living in the same climate all have body trunks of the same width, no matter how their heights vary. Populations living in cold climates always have wide bodies; populations living in warm climates always have narrow bodies. These dimensions are always constant in adaptation to heat or cold. In addition, the ratio of tibia (lower leg) length to femur (upper leg) length differs between people who live in hot climates and people who live in cold climates. Heat­ adapted populations have long tibias relative to their femurs (their legs are long), but cold­ adapted popula­ tions have short tibias relative to their femurs (their legs are short). Neandertals fit the predictions for cold adaptation: their body trunks are wide, and their tibias are short.

NEANDERTAL HUNTING: INEFFICIENT OR SUCCESSFUL? The French paleoanthropologists of the 1800s and early 1900s questioned Neandertals’ humanness. They suggested that Neandertals were unintelligent, could not speak,

FIGURE 12.21 Neandertal Body Proportions A further adaptation to the cold appears in Neandertals’ body proportions (left) compared with early modern humans’ (right). Neandertals’ much stockier body build reduced heat loss and increased heat retention. Early modern humans’ narrower trunk, narrower hips, and longer legs reflected the warmer environment in which these people lived.

emerging modern humans and representing distant cousins of humanity that were not able to survive. In rejecting this view, we should take a closer look at some topics Boule addressed in his study of the La Chapelle skeleton.

One very distinctive feature of Neandertal faces is the enormous nasal aperture (Figure  12.18). The great size of the nasal aperture in many Neandertal fossils indicates that these people had huge noses, in both width and projection. Such massive noses were one of the cranial characteristics that led Boule to believe that Neandertals were not related to later humans in an evolutionary sense. However, nasal features are more likely part of an adaptive complex reflecting life in cold climates during the Upper Pleistocene. The shape and size of any nose is an excel­ lent example of the human face’s highly adaptable nature, especially in relation to climate. One of the nose’s important functions is to transform ambient air— the air breathed in from the atmosphere— into warm, humid air. Large noses have more internal surface area, thus providing an improved means of warming and moistening the cold, dry air that Neandertals breathed regularly. Moreover, the projecting nose typical of Neandertals placed more distance between the cold external environment and the brain, which is temperature­ sensitive. Alternatively, the large noses of Neandertals may simply be due to the fact that their faces are so large. Regardless of the circumstances resulting in Neandertals’ having large nasal apertures, many people and populations around the world today have wide, big noses, which are integral parts of their robust faces. These attributes are not uniquely Neandertal (Figure 12.19).

Other features of Neandertal skeletons are consistent with cold adaptation. For example, the infraorbital foramina— the small holes in the facial bones located beneath the eye orbits— are larger in European Neandertals than in modern peo­ ple (Figure 12.20). The foramina’s increased size is due to the blood vessels that tracked through them having been quite large. The larger blood vessels may have allowed greater blood flow to the face, preventing exposed facial surfaces from freezing.

FIGURE 12.18 Nasal Aperture The large nasal aperture of Neandertal crania, such as this cranium from Gibraltar, may have been a cold adaptation.

FIGURE 12.19 Modern Human Relatives? Some of the morphological traits associated with Neandertals can be found in modern humans, as illustrated by this photograph of the physical anthropologist Milford Wolpoff facing the reconstructed head of a European Neandertal. Might Neandertals have interbred with modern human ancestors, passing along some of these traits?

Large infraorbital foramen

Large nasal aperture

Large prominent nasal bones

Low forehead

Occipital bun

FIGURE 12.20 Cold Adaptive Traits Large infraorbital foramina are among the Neandertal traits that likely were responses to a cold environment during the later Pleistocene. Note also the distinctive Neandertal traits— low forehead and projecting occipital (occipital bun).

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and had a simplistic culture. Put in the vernacular expression, “Their lights were on, but nobody was home.” Some paleoanthropologists continue to argue this point, viewing Neandertals as inefficient hunters and not especially well adapted to their environments. A growing body of archaeological and biological evidence demonstrates, however, that Neandertals were not clumsy mental deficients.

Neandertals were associated with the culture known as Mousterian or Middle Paleolithic. This culture’s stone tool technology, lasting about 300,000–30,000 yBP, includes a complex and distinctive type of flaking called the Levallois. This technique involves preparing a stone core and then flaking the raw materials for tools from this core (Figure 12.23). Contrary to the opinions of early anthropolo­ gists, this Neandertal technology was complex and required considerable hand– eye coordination. Moreover, anthropologists are learning that late Neandertals par­ ticipated fully in the Upper Paleolithic, the earliest cultures associated mostly with early modern H.  sapiens in Europe, producing stone tools that were modern in many respects and certainly as complex as those produced by early modern humans. Moreover, the size, shape, and articulations of the Neandertal hand reflect the kind of precise manual dexterity crucial for the fine­ crafting of tools (Figure 12.24).

If Neandertals were not effective hunters, then they might have been less successful adaptively than modern people. One way to measure hunting success is to determine how much meat Neandertals ate. Butchered animals’ bones are abundant in Neandertal habitation sites, indicating that Neandertals hunted the animals and processed the carcasses for food. Suggestive though this evidence is, the mere presence of animal remains does not reveal how important animals were in the people’s diet. To find out how important meat was in Neandertals’ diets,

FIGURE 12.22 Body Size and Body Shape The refinement of Bergmann’s and Allen’s rules regarding body size, body shape, and temperature adaptations is illustrated by these body types. The ratio of body surface area to body mass (square centimeters per kilogram) is given below each type. The greater the ratio, the more that body shape and that body size are adaptations to high temperatures. Individuals living in cold environments, such as the modern Inuit, have a lower ratio than individuals living in hot environments, such as the modern Nilotic. Because of their short stature, modern Pygmies appear to contradict Bergmann’s and Allen’s rules. However, body surface ratio reveals that Pygmies are well adapted to hot environments.

Modern Inuit (260 cm2/kg)

Modern Nilotic (301 cm2/kg)

Modern Pygmy (314 cm2/kg)

Mousterian The stone tool culture in which Neandertals produced tools using the Levallois technique.

Middle Paleolithic The middle part of the Old Stone Age, associated with Mouste- rian tools, which Neandertals produced using the Levallois technique.

Levallois A distinctive method of stone tool production used during the Middle Paleolithic, in which the core was pre- pared and flakes removed from the sur- face before the final tool was detached from the core.

Upper Paleolithic Refers to the most recent part of the Old Stone Age, associated with early modern H. sapiens and characterized by finely crafted stone and other types of tools with various functions.

This flake can now be used for scraping or cutting. Further flake removal will produce a more specialized tool.

A heavy, specific blow is directed at one end of the stone, removing a large flake. This flake is convex on one side and flat on the other.

A large stone of flint is chosen.

One side of the stone has flakes removed from the entire surface, giving it the appearance of a tortoise shell.

Small flakes are removed from the stone’s perimeter using an antler or other tool.

FIGURE 12.23 Levallois Technique To produce the Mousterian tools, Neandertals used a specific technique to remove flakes from flint cores. The use of such a technique indicates that Neandertals could visualize the shape and size of a tool from a stone core, an advanced cognitive ability.

FIGURE 12.24 Mousterian Tools Neandertals made these tools out of flint. The use of such tools would have replaced the use of front teeth as tools, reducing the amount of anterior tooth wear in some later Neandertals. (Photo © David L. Brill, humanoriginsphotos.com)

and had a simplistic culture. Put in the vernacular expression, “Their lights were on, but nobody was home.” Some paleoanthropologists continue to argue this point, viewing Neandertals as inefficient hunters and not especially well adapted to their environments. A growing body of archaeological and biological evidence demonstrates, however, that Neandertals were not clumsy mental deficients.

Neandertals were associated with the culture known as Mousterian or Middle Paleolithic. This culture’s stone tool technology, lasting about 300,000–30,000 yBP, includes a complex and distinctive type of flaking called the Levallois. This technique involves preparing a stone core and then flaking the raw materials for tools from this core (Figure 12.23). Contrary to the opinions of early anthropolo­ gists, this Neandertal technology was complex and required considerable hand– eye coordination. Moreover, anthropologists are learning that late Neandertals par­ ticipated fully in the Upper Paleolithic, the earliest cultures associated mostly with early modern H.  sapiens in Europe, producing stone tools that were modern in many respects and certainly as complex as those produced by early modern humans. Moreover, the size, shape, and articulations of the Neandertal hand reflect the kind of precise manual dexterity crucial for the fine­ crafting of tools (Figure 12.24).

If Neandertals were not effective hunters, then they might have been less successful adaptively than modern people. One way to measure hunting success is to determine how much meat Neandertals ate. Butchered animals’ bones are abundant in Neandertal habitation sites, indicating that Neandertals hunted the animals and processed the carcasses for food. Suggestive though this evidence is, the mere presence of animal remains does not reveal how important animals were in the people’s diet. To find out how important meat was in Neandertals’ diets,

FIGURE 12.22 Body Size and Body Shape The refinement of Bergmann’s and Allen’s rules regarding body size, body shape, and temperature adaptations is illustrated by these body types. The ratio of body surface area to body mass (square centimeters per kilogram) is given below each type. The greater the ratio, the more that body shape and that body size are adaptations to high temperatures. Individuals living in cold environments, such as the modern Inuit, have a lower ratio than individuals living in hot environments, such as the modern Nilotic. Because of their short stature, modern Pygmies appear to contradict Bergmann’s and Allen’s rules. However, body surface ratio reveals that Pygmies are well adapted to hot environments.

Modern Inuit (260 cm2/kg)

Modern Nilotic (301 cm2/kg)

Modern Pygmy (314 cm2/kg)

Mousterian The stone tool culture in which Neandertals produced tools using the Levallois technique.

Middle Paleolithic The middle part of the Old Stone Age, associated with Mouste- rian tools, which Neandertals produced using the Levallois technique.

Levallois A distinctive method of stone tool production used during the Middle Paleolithic, in which the core was pre- pared and flakes removed from the sur- face before the final tool was detached from the core.

Upper Paleolithic Refers to the most recent part of the Old Stone Age, associated with early modern H. sapiens and characterized by finely crafted stone and other types of tools with various functions.

This flake can now be used for scraping or cutting. Further flake removal will produce a more specialized tool.

A heavy, specific blow is directed at one end of the stone, removing a large flake. This flake is convex on one side and flat on the other.

A large stone of flint is chosen.

One side of the stone has flakes removed from the entire surface, giving it the appearance of a tortoise shell.

Small flakes are removed from the stone’s perimeter using an antler or other tool.

FIGURE 12.23 Levallois Technique To produce the Mousterian tools, Neandertals used a specific technique to remove flakes from flint cores. The use of such a technique indicates that Neandertals could visualize the shape and size of a tool from a stone core, an advanced cognitive ability.

FIGURE 12.24 Mousterian Tools Neandertals made these tools out of flint. The use of such tools would have replaced the use of front teeth as tools, reducing the amount of anterior tooth wear in some later Neandertals. (Photo © David L. Brill, humanoriginsphotos.com)

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anthropologists have applied the powerful tools of bone chemistry and stable iso­ tope analysis. Measurement of stable isotopes of both nitrogen and carbon in the bones of Neandertals— from Scladina Cave (Belgium), Vindija Cave, and Marillac (France)—indicates that Neandertals ate lots of meat, at or nearly at the level of carnivores living at the same time and place (Figure 12.25). The chemical signa­ ture of diet, then, is a powerful indicator of Neandertals’ effectiveness in acquiring and consuming animal protein. That is, it shows that Neandertals were successful hunters. This is not to say that Neandertals depended wholly on animals as sources of food. Analysis of plant residues found in Neandertal tooth calculus shows that Neandertals ate a diversity of plants, some of which were cooked. Neandertals might have consumed some of these plants for medicinal purposes. The British archaeologist Karen Hardy and her associates have documented in calculus from El Sidrón the presence of bitter­ tasting chemicals that are well­ known appetite suppressants. The presence of residues of plants that lack nutritional value indi­ cates that Neandertals might have self­ medicated, but we can never know for sure if they did.

Another indicator of their effective adaptation is the measurement of stress levels. The American physical anthropologist Debbie Guatelli­ Steinberg and her associates found that hypoplasias, the stress markers in teeth that reflect growth disruption due to poor diets or poor health, are present in Neandertals but at a frequency no different from that of modern humans. This finding, too, suggests that Neandertals dealt successfully with their environments.

NEANDERTALS BURIED THEIR DEAD In many Neandertal sites, the remains have been found scattered about, commingled and concurrent with living areas. For example, the Krapina Neandertal fossils are fragmentary and were scattered throughout the site. That is, the deceased were treated no differently from food remains or anything else being discarded. In contrast, a significant number of skeletons have been found in pits. That is, excavation of some Neandertal sites

calculus Refers to hardened plaque on teeth; the condition is caused by the minerals from saliva being continuously deposited on tooth surfaces.

FIGURE 12.25 Neandertal Diet Measures of stable isotopes of both carbon and nitrogen, here labeled 13C and 15N, respectively, can be used to determine the relative amounts of different kinds of foods consumed. This graph shows the isotope values for a variety of herbivores and of carnivores. Herbivores generally have lower isotope values than carnivores. Neandertals’ isotope levels are close to those of known carnivores, indicating that Neandertals ate plenty of meat.

δ1 5 N

δ13C

12

10

11

9

8

7

6

5

4

3

–25–26 –24 –23 –22 –21 –20 –19 –18 2

Fallow deer

Carnivores

Horses

Cave bears

Brown bears

Foxes

Neandertals

Spy B E L G I U M

F R A N C E

Scladina Cave

Marillac

in Europe and western Asia has shown that pits had been dug, corpses had been placed in the pits, and the pits had been filled in. For example, the Neandertal skel­ etons from Spy, Belgium; ones from various sites in France, such as La Chapelle­ aux­ Saints; several Shanidar individuals; and the Neandertals from Amud and Tabun, both in Israel, were found in burial pits (Figure 12.26).

Was burial of the dead a religious or ceremonial activity having significant symbolic meaning for the living, those who buried the dead? Or was burial simply a means of removing bodies from living spaces? Most of the intentionally buried skeletons were in flexed ( fetal­ oriented) postures. The hands and arms were care­ fully positioned, and the bodies were typically on their sides or backs. This vigilant treatment indicates that care was taken to place the bodies in the prepared pits. The skeletons’ postures suggest, therefore, that these burials were not just dispos­ als. They represented purposeful symbolic behavior linking those who died and those who were living.

NEANDERTALS TALKED Fundamental to human behavior is the ability to speak as part of the repertoire of communication. Conversation is a key way that we present information and exchange ideas. Because early anthropologists believed that Neandertals lacked the ability to speak, they argued that Neandertals were not related to modern people in an evolutionary sense. This idea continues to the present. The American linguist Philip Lieberman and the American anatomist Edmund Crelin, for example, have reconstructed the Neandertal vocal tract. Because their reconstruction resembles a modern newborn infant’s vocal tract, Lieberman and Crelin conclude that, like human babies, Neandertals could not express the full range of sounds necessary for articulate speech. Although inter­ esting, their reconstruction of the Neandertal vocal tract is conjectural. Based on skulls alone, it necessarily lacks the anatomical parts (soft tissues) important for determining whether Neandertals had speech.

One compelling line of evidence suggests that Neandertals were able to speak. The Kebara Neandertal skeleton includes the hyoid bone, a part of the neck that can survive from ancient settings. Various muscles and ligaments attach it to

FIGURE 12.26 Intentional Burial Like the Shanidar skeletons (among others), the La Chapelle- aux- Saints skeleton, shown here, provides evidence of intentional burial. When this individual was found in a pit, it was the first suggestion that Neandertals cared for their dead in a way similar to modern humans’ methods.

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the skull, mandible, tongue, larynx, and pharynx, collectively producing speech (Figure 12.27). The morphology of the Kebara Neandertal’s hyoid is identical to that of a living human’s. The Kebara people talked.

Even more convincing evidence that Neandertals spoke are findings from the study of microscopic wear patterns on the surfaces of incisors and canines, espe­ cially of the study of the relationship with brain laterality. The human brain is distinctive in its laterality: the clearly defined left and right sides are an anatom­ ical marker for the ability to speak. In right­ handed humans, the left side of the brain is dominant. The left brain controls right­ sided body movements, especially the use of the right hand and right arm. The left brain also controls speech and language production. In left­ handed people, these connections are reversed. The right side of the brain is dominant, controls left­ side body movements, and con­ trols areas critical for speech and language. Hand preference— right or left— can be determined by looking at the scratches on the front teeth of fossil hominins.

The American physical anthropologist David Frayer and his associates have detected microscopic parallel scratches on the surfaces of upper incisors and canines of many fossil hominins, including Neandertals from Europe. It has long been thought that Neandertals (and lots of other hominins, including modern humans) used a “ stuff­ and­ cut” method of meat processing before chewing the meat. This method consists of cutting a piece of meat by biting one end of it and holding the other end with the left hand, then holding a stone tool with the right hand to cut the meat. Often, cutting meat in this fashion inadvertently scratches the front teeth. When this happens, the scratches on the teeth have a highly dis­ tinctive pattern: they are parallel to each other, and they angle downward. When the stuff­ and­ cut method is performed experimentally, right­ handed people end up with tooth scratches that angle downward to the right and left­ handed people end up with scratches that angle downward to the left.

Frayer and his research group examined the scratch patterns on the teeth of 17 Neandertals from different sites, finding that all but two of the Neandertals had scratch patterns consistent with right­ handedness (Figure  12.28). The two exceptions had just the opposite, consistent with left­ handedness. Similarly, in the early archaic  H.  sapiens from Sima de los Huesos dating to 500,000 yBP, all

Hyoid bone Hyoid bone

FIGURE 12.27 Did Neandertals Speak? The Kebara skeleton’s hyoid is identical to a modern human hyoid, indicating that Neandertals could speak.

12 individuals studied had the scratch pattern associated with handedness. The conclusion is simple: most Neandertals and their predecessors had left­ dominant brains and were right­ handed. Therefore, they had brain laterality. Because they had brain laterality, we can conclude that Neandertals talked.

Genetic evidence also supports the notion that Neandertals spoke. The Ger­ man geneticist Johannes Krause and his team successfully identified the FOXP2 gene— a gene strongly implicated in the production of speech— from Neandertal bone samples from the El Sidrón site. Although it is not the gene for speech, it is part of a complex of genetic variation found in modern humans. Its presence in these late archaic H. sapiens indicates that Neandertals talked.

NEANDERTALS USED SYMBOLS Burial of the dead is only one of the countless contexts in which modern humans use symbolism. Think, for example, of all the signs, images, and codes you encounter every day, from the letters on this page to any jewelry you wear to your friend’s tattoo. Decorative items such as perforated shells, some stained with pigments of various colors, have been well documented in the earlier Paleolithic in Africa and the Middle East, dating to 70,000–120,000 yBP. A number of anthropologists have suggested that Neandertals differed from modern  H.  sapiens in that they lacked symbolic behavior. This lack, in turn, is seen as a feature of Neandertals’ purported cognitive inferiority to  H.  sapiens. However, the Spanish archaeologist João Zilhão and his colleagues have recently discovered clear evidence of symbolic behavior at two sites in Spain that date to 50,000 yBP. At Cueva de los Aviones and Cueva Antón, perforated marine shells similar to those in Africa and the Middle East had been painted with naturally occurring pigments, especially red, yellow, and orange. These shells were likely strung around an individual’s neck. These body ornaments are evidence that Neandertals used symbolism at least 10,000 years before the appearance of mod­ ern H. sapiens in Europe. In addition, the use of red ochre— a pigment derived from the mineral hematite— was used by hominins at least by 250,000 yBP in a range of European hominin contexts. Neandertals used symbols to communicate ideas and expressions.

The key point of this discussion of Neandertal characteristics— relating to cli­ mate adaptation, material culture, efficiency in hunting strategies, access to animal protein, treatment of the deceased, and the use of speech and symbolism— is that Neandertals likely were not weird humanlike primates, less adaptable and less intelligent than modern humans. The record shows that their behaviors, both in form and in symbol, were similar to modern humans’. The size and robusticity of their long bones show that Neandertals were highly physically active, more so than living humans. Such cultural and biological features reflect Neandertals’ success in adapting to environmental circumstances of the Upper Pleistocene, not evo­ lutionary failure. The empirical evidence disproves arguments that Neandertals were less than human.

EARLY MODERN HOMO SAPIENS Modern H. sapiens from the Upper Pleistocene are represented in the fossil record throughout Africa, Asia, and Europe. During this time, hominins moved into other areas of the world. Later in this period, they spread into regions with extreme environments, such as the arctic tundra of Siberia in northern Asia. It was a time of significant increases in population size, increased ability through cultural means of adapting to new and difficult landscapes, and the development of new

FIGURE 12.28 Handedness in Neandertals Shown here is an upper right first incisor of a Neandertal from the Vindija site, Croatia. The surface has more than 150 scratches produced by a stone tool rubbing against the tooth. Almost all the scratches are of the type shown here, angled down toward the person’s right. The red lines are the main scratches, and the different colors represent places where marks overlap. This person had a left- dominant brain, was right- handed, and possessed the ability to speak.

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Archaic Homo sapiens

Archaic H. sapiens are the first of our species, beginning some 350,000 yBP globally and evolving locally from earlier Homo erectus populations. After 150,000 yBP, regional patterns of diversity emerge, followed by simultaneous occupation of Europe by late archaic (Neandertals) and early modern H. sapiens by 40,000 yBP.

Locations (sites)1

Africa (Kabwe) Asia (Ngandong, Dali, Narmada, Amud, Kebara, Tabun,

Shanidar) Europe (Sima de los Huesos, Swanscombe, Steinheim,

Petralona, Arago, Feldhofer Cave, Atapuerca, Spy, Krapina, Vindija, Moula- Guercy, La Chapelle- aux- Saints, Scladina Cave, Marillac, Les Rochers, Engis, El Sidrón, Monte Lessini, Teshik Tash)

Chronology 350,000–30,000 yBP

Biology Mixture of H. erectus and H. sapiens characteristics 1,200 cc cranial capacity early 1,500 cc cranial capacity late Both skulls and skeletons less robust Reduced tooth size, but most of reduction in premolars and

molars (front teeth increase in size) Appearance of Neandertal morphology after 130,000 yBP

in Middle East and Europe (long, low skull; wide, large nose; large front teeth with common heavy wear; forward- projecting face; no chin; wide body trunk; short limbs)

Distinctive mtDNA structure Distinctive nuclear DNA structure but overlapping with living

humans’

Culture and behavior

Some evidence of housing structures Large- game hunting Fishing and use of aquatic resources after 100,000 yBP More advanced form of Acheulian early Mousterian late (Europe) Increased use of various raw materials besides stone after

100,000 yBP Skilled tool production Burial of deceased after 100,000 yBP Symbolic behavior Social care of sick and injured Articulate speech likely

1Sites mentioned in text; italics denote sites where Neandertal (archaic H. sapiens) remains have been found.

Sima de los Huesos

Shanidar

C O N C E P T C H E C K !

technologies and subsistence strategies. (Table  12.1 lists the four major Upper Paleolithic cultures and important events associated with each.) The cultures of the later Pleistocene, grouped in the Upper Paleolithic, are also known from their stunning imagery, including hundreds of artistic works in caves throughout Europe but concentrated especially in France and Spain (Figure  12.29). This period of human evolution also includes the universal appearance of the modern anatomical characteristics discussed at the beginning of this chapter, namely, a reduced face, small teeth, a vertical forehead, a more rounded skull, and gracile postcranial bones. Modern humans’ evolution started much earlier in Africa than in Europe and Asia.

EARLY MODERN HOMO SAPIENS IN AFRICA (200,000–6,000 YBP) The African record for early  H.  sapiens is especially important because it includes the earliest evidence of modern people’s anatomical characteristics. Crucially important fossil hominins from this time come from the Herto, Aduma, and Bouri sites, in Ethiopia’s Middle Awash River Valley, and from Omo, in southern Ethiopia. The remains from Herto— partial skulls of two adults and of a child, dating to 160,000–154,000 yBP— show a cranial capacity of about 1,450 cc, close to the average for modern humans. In addition, many of the characteristics are essentially modern, including a relatively tall cranium, a vertical forehead, smaller browridges, and a nonprojecting face. Among the archaic features are significant browridges (though the trend is toward smaller) and a relatively long face. These remains may be from the earliest modern people in Africa or at least close to the earliest. German paleoanthropologist Günter Bräuer argues that modernization in Africa first took place in East Africa. The remains’ overall appearance indicates that modern people emerged in Africa long before their arrival in Europe and western Asia. The remains from Omo may be as old as 195,000 yBP.  If so, they are the oldest evidence of anatomically modern humans. However, their dating is uncertain because the fossils were not positioned in the geological context as clearly as the Herto fossils were.

Belonging to later contexts are the partial skulls from Aduma and Bouri, dat­ ing to about 105,000–80,000 yBP.  Like the Herto skulls, these skulls have both premodern and modern characteristics. However, the most complete Aduma skull is modern in nearly every characteristic.

E T H I O P I A Herto

Bouri

Omo

Aduma

S O U T H A F R I C A

Klasies River Mouth Hofmeyr

TABLE 12.1 Timeline for Major Upper Paleolithic Cultures of Europe

The Aurignacian (45,000–30,000 yBP)  Associated with the first anatomically modern humans in Europe

The Gravettian (30,000–20,000 yBP)  The Perigordian in France  Earliest art, in the form of carved figurines  Lagar Velho burial in Portugal

The Solutrean (21,000–17,000 yBP)  France and Spain during the last glacial peak  Made very fine stone points

The Magdalenian (17,000–12,000 yBP)  Successful hunters of reindeer and horses  Spread out across Europe as conditions improved at the end of the Ice Age  Made many of the spectacular paintings and carvings

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Skulls from two key locations in southern Africa provide important informa­ tion about early modern  H.  sapiens that date to after 100,000 yBP.  Among the fragmentary remains from Klasies River Mouth Cave, anthropologists have docu­ mented the presence of a chin, a distinctively modern characteristic, that dates to at least 90,000 yBP (Figure 12.30). A nearly complete skull from Hofmeyr, dating to 36,000 yBP, bears a striking resemblance to Pleistocene modern Europeans.

Throughout the Pleistocene and well into the early Holocene, African hominins, although modern, retained some robusticity. For example, the skulls from Lothagam, Kenya, dating to the Holocene (ca. 9,000–6,000 yBP), are robust compared with living East Africans’ (Figure 12.31). During this period, a number of characteristics seen in the region’s living populations were present, such as wide noses. At Wadi Kubbaniya and Wadi Halfa, both in the Nile Valley, populations have some very robust characteristics, such as flaring cheekbones and well­ developed browridges. These features contrast sharply with the gracile facial fea­ tures seen later in the Holocene and in living people (these features are discussed further in chapter 13).

Similarly, early Holocene skulls (ca. 9,000 yBP) found at Gobero, in Niger, are long, low, and robust compared with later Holocene skulls from the same place (Figure 12.32). A later population of incipient pastoralists may have replaced the earlier hunter– gatherers. However, the reduction in robusticity more likely reflects evolution that occurred in this setting (see chapter 13).

(a) (b)

(c)

FIGURE 12.29 Chauvet Cave Art (a) Chauvet Cave is located a half- mile from the Pont d’Arc, a natural bridge in France’s Ardèche River valley. The extensive cave system contains more than 400 images of late Pleistocene animals, especially lions, mammoths, and rhinoceroses. (b) Rhinos and lions are among the animals depicted in this Ardèche cave painting, which is about 30,000 years old. (c) Upper Paleolithic tools, such as these, include some of the forms seen in earlier periods of human evolution. However, new tools reflect the procurement of additional types of food, such as the barbed harpoon for catching fish. (Tool photos [c] © 1985 David L. Brill, humanoriginsphotos.com)

K E N YA

N I G E R

Lothagam

Gobero

FIGURE 12.30 Klasies River Mouth Cave One of the most important features found on these cranial remains is a chin on the mandible of this early modern Homo sapiens from South Africa.

Chin

FIGURE 12.31 Lothagam Skull This Kenyan cranium illustrates early modern humans’ rather robust nature. Note the projection both of the lower part of the front of the skull and of the mandible.

FIGURE 12.32 Gobero Crania (a) This adult male cranium from Gobero, dating to about 9,500 yBP, is long and low and has a wide, flat face. (b) In contrast, this adult male cranium, from the same site but dating to about 6,500 yBP (the middle Holocene), is high and has a narrow, gracile face. These differences could be due to local evolutionary change or the later arrival of a new population in the region having different craniofacial characteristics.

(a) (b)

EARLY MODERN HOMO SAPIENS IN ASIA (90,000–18,000 YBP) The earliest modern H. sapiens in Asia are best represented by fossils from western Asia, in fact from the same region as the Amud and Kebara Neandertals in Israel. The 90,000­ year­ old remains from Skhul have distinctively modern characteristics, suggesting

S U D A N

Wadi Halfa

E G Y P T

Wadi Kubbaniya

Skulls from two key locations in southern Africa provide important informa­ tion about early modern  H.  sapiens that date to after 100,000 yBP.  Among the fragmentary remains from Klasies River Mouth Cave, anthropologists have docu­ mented the presence of a chin, a distinctively modern characteristic, that dates to at least 90,000 yBP (Figure 12.30). A nearly complete skull from Hofmeyr, dating to 36,000 yBP, bears a striking resemblance to Pleistocene modern Europeans.

Throughout the Pleistocene and well into the early Holocene, African hominins, although modern, retained some robusticity. For example, the skulls from Lothagam, Kenya, dating to the Holocene (ca. 9,000–6,000 yBP), are robust compared with living East Africans’ (Figure 12.31). During this period, a number of characteristics seen in the region’s living populations were present, such as wide noses. At Wadi Kubbaniya and Wadi Halfa, both in the Nile Valley, populations have some very robust characteristics, such as flaring cheekbones and well­ developed browridges. These features contrast sharply with the gracile facial fea­ tures seen later in the Holocene and in living people (these features are discussed further in chapter 13).

Similarly, early Holocene skulls (ca. 9,000 yBP) found at Gobero, in Niger, are long, low, and robust compared with later Holocene skulls from the same place (Figure 12.32). A later population of incipient pastoralists may have replaced the earlier hunter– gatherers. However, the reduction in robusticity more likely reflects evolution that occurred in this setting (see chapter 13).

(a) (b)

(c)

FIGURE 12.29 Chauvet Cave Art (a) Chauvet Cave is located a half- mile from the Pont d’Arc, a natural bridge in France’s Ardèche River valley. The extensive cave system contains more than 400 images of late Pleistocene animals, especially lions, mammoths, and rhinoceroses. (b) Rhinos and lions are among the animals depicted in this Ardèche cave painting, which is about 30,000 years old. (c) Upper Paleolithic tools, such as these, include some of the forms seen in earlier periods of human evolution. However, new tools reflect the procurement of additional types of food, such as the barbed harpoon for catching fish. (Tool photos [c] © 1985 David L. Brill, humanoriginsphotos.com)

K E N YA

N I G E R

Lothagam

Gobero

FIGURE 12.30 Klasies River Mouth Cave One of the most important features found on these cranial remains is a chin on the mandible of this early modern Homo sapiens from South Africa.

Chin

FIGURE 12.31 Lothagam Skull This Kenyan cranium illustrates early modern humans’ rather robust nature. Note the projection both of the lower part of the front of the skull and of the mandible.

FIGURE 12.32 Gobero Crania (a) This adult male cranium from Gobero, dating to about 9,500 yBP, is long and low and has a wide, flat face. (b) In contrast, this adult male cranium, from the same site but dating to about 6,500 yBP (the middle Holocene), is high and has a narrow, gracile face. These differences could be due to local evolutionary change or the later arrival of a new population in the region having different craniofacial characteristics.

(a) (b)

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that the people living there were modern H. sapiens. Among the most prominent remains from the site are several male skulls, of which Skhul 5 is the most complete. That Skhul 5 dates to before the Amud fossils indicates that modern humans lived in the region before Neandertals (Figure 12.33).

Remains of the earliest modern people from eastern Asia are very scarce. Some of these remains are purported to be older than 60,000 yBP.  At Zhiren Cave in south China, two molars and a partial mandible dating to at least 100,000 yBP show a combination of archaic and modern features. The mandible is relatively thick, like that of other archaic H. sapiens; but it has a chin, like the chin of mod­ ern H. sapiens. While not a fully modern H. sapiens, it is certainly a hominin that shows transitional characteristics leading to anatomical modernity. The earliest most complete fossil remains are a mandible and partial skeleton, dating to about 41,000 yBP, from Tianyuan Cave, China, and about 46,000 yBP from Tam Pa Ling Cave, Laos. Like the Zhiren Cave remains, these fossils have both archaic and modern features. The Tam Pa Ling skull lacks a prominent supraorbital torus, a feature that is quite modern. Better known are three skulls from the Upper Cave at Zhoukoudian, China, dating to 29,000–24,000 yBP (Figure  12.34; this site is discussed further in chapter  11). The Upper Cave skulls are robust compared with living Asians’, but the facial flatness is characteristic of native eastern Asians today. Similarly, the early modern people from Minatogawa (Okinawa), dating to about 18,000 yBP, are gracile but retain thick cranial bones and large browridges, especially compared with those of the later Holocene populations in eastern Asia.

EARLY MODERN HOMO SAPIENS IN EUROPE (35,000–15,000 YBP) Early modern people are known from various places throughout Europe. The earliest modern  H.  sapiens in Europe is from Peştera cu Oase, Romania, and dates to 35,000 yBP.  The Oase 2 skull from that site is distinctively modern, contrasting with Neandertals that lived during the same time. For example, Oase 2 has very

FIGURE 12.33 Skhul Cranium This skull possesses many characteristics associated with modern humans, including a chin, a less projecting face, small and gracile cheeks, and a high, vertical forehead. The browridges are still distinct but are much reduced compared with archaic Homo sapiens’. (Photo © 1985 David L. Brill, humanoriginsphotos.com)

(a) (b)

FIGURE 12.34 Zhoukoudian Crania (a, b) One skull recovered from Zhoukoudian shows several modern human traits, but overall these crania are more robust than their modern Asian counterparts. In the older area of this site, the famous Homo erectus fossils were found, prior to World War II.

reduced browridges and a generally gracile appearance. Almost as old are remains from Mladeč, Předmostí, and Dolní Věstonice, all in the Czech Republic, dating to 35,000–26,000 yBP. The half­ dozen Mladeč skulls (35,000 yBP) show remarkable variability, including a mix of Neandertal characteristics in some (occipital bun, low skull, large browridges, large front teeth, and thick bone) and modern char­ acteristics in others (nonprojecting face, narrow nasal opening). The Předmostí and Dolní Věstonice skulls retain a few Neandertal characteristics, but they are clearly more modern in appearance than the Mladeč people (Figure 12.35). Some Neandertal features persist well into recent times in eastern Europe, especially in the facial region (Figure 12.36).

Western Europe has virtually no fossil record for the earliest modern people, those contemporary with the populations represented by the Mladeč and Před­ mostí fossils. The skeleton of a five­ year­ old child from Lagar Velho, Portugal, dating to 24,000 yBP, has a number of archaic, Neandertal­ like cranial and post­ cranial features, such as its limb proportions and robusticity (Figure 12.37).

The best­ known western European representatives of early modern people are the remains of a half­ dozen individuals from Cro­ Magnon, in Dordogne, France, and remains from the Grimaldi Caves, in the Italian Riviera region, all of these dat­ ing to about 30,000–25,000 yBP. The Cro­ Magnon remains are often presented as the archetypical example of the earliest modern people, but in fact people varied considerably during this time. Collectively, though, both ensembles of skeletons from western Europe have distinctively modern features: vertical forehead, narrow nasal aperture, and small browridges (Figure  12.38). In addition, unlike Nean­ dertals’, their tibias are long and their body trunks are narrow. Like Neandertals, these people lived in cold climates of the late Pleistocene, but their very different body morphology suggests adaptation to warmer climates. (The implications of these skeletal features for the origins of modern  H.  sapiens are discussed later in this chapter.)

Tianyuan Cave

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Zhoukoudian

(a)

(b) FIGURE 12.35 Dolní Věstonice Skull (a, b) This cranium, from Dolní Věstonice, combines modern human and Neandertal characteristics.

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Overall, comparisons of earlier with later early modern  H.  sapiens in Europe indicate a trend toward gracilization— the faces, jaws, and teeth became smaller and the faces became less projecting. In addition, comparison of early and late Upper Paleolithic heights reconstructed from the long bones shows that the later early modern people were shorter. The decrease in the height of early modern people may have been caused, at the very end of the Pleistocene, by both a decrease in the quality of nutrition and resource stress. That is, during the last 20,000 years of the Pleistocene, food procurement intensified— more effort was put into acquiring and processing food for the same amount of caloric intake as before. This change may have occurred because human population size was increasing, placing increased pressure on food resources. An outcome of this change was a global increase in the range of foods eaten. Archaeological evidence shows that the later early modern humans hunted and collected smaller and less desirable (because not as protein­ rich) foods, such as small vertebrates, fish, shellfish, and plants. As the American anthropologist Trent Holiday has also shown, the late Upper Paleolithic people had wider body trunks and shorter legs than the early Upper Paleolithic people. The morphological shift indicates an adaptation to cold during the late Upper Paleolithic, a highly dynamic period of human adaptation and evolution.

MODERN BEHAVIORAL AND CULTURAL TRANSITIONS Anthropologists are learning that various behavioral and cultural practices devel­ oped at different places and different times in the later Pleistocene, culminating in full modernity in H. sapiens globally. In many respects, the fossil record and the cultural record show that modern behaviors and practices began, biologically and

Inward angle of the suture at the bottom of the cheek

Pinching of the bottom portion of the nasal bones

Lateral location of cheeks

High nasal angle

FIGURE 12.36 Neandertal Traits in Modern Humans The La Chapelle- aux- Saints cranium (bottom, and see Figure 12.16) and a modern Croatian cranium (top) share four major facial similarities.

FIGURE 12.37 Lagar Velho This skeleton of a child was discovered at a rockshelter site in Portugal’s Lapedo valley.

How Has the Biological Variation in Fossil Homo sapiens Been Interpreted? | 335

culturally, in Africa. For example, fishing and the use of aquatic resources as an important part of diet are first documented at Katanda, in Congo, where early modern H. sapiens were exploiting huge catfish by at least 75,000 yBP. This devel­ opment is part of a larger package of behaviors associated with modern humans, including more specialized kinds of hunting, wider employment of raw materials (such as bone) for producing tools, advanced blade technology, and trade. How­ ever, as discussed above in “Neandertals Used Symbols,” symbolic behavior and cognitive advancement were also present in Europe, albeit later than in Africa. The successful adaptation of symbolically advanced late archaic  H.  sapiens— the Neandertals— in Europe shows that the story of later evolving humans is complex. Neandertals were fundamentally no different from modern H. sapiens, especially in regard to a number of behaviors— burial of the dead, speech, and symbolism— that remain with us today.

How Has the Biological Variation in Fossil Homo sapiens Been Interpreted? At the beginning of this chapter, you read about the two key models that anthro­ pologists use to explain modern  H.  sapiens’ origins, namely, the Out­ of­ Africa model and the Multiregional Continuity model. After having learned what the fossil record reveals about the variation in late archaic  H.  sapiens, you should be starting to see what this record reveals about modern humans’ origins. Now remember the question posed at the beginning of this chapter: Which of the two models best explains modern H. sapiens’ origins?

The European fossil record from 40,000–30,000 yBP provides clues about modern H. sapiens’ origins in Europe. The earliest modern H. sapiens were present

FIGURE 12.38 Cro- Magnon (a, b) In 1868, a geologist discovered skeletons in a rockshelter in Cro- Magnon, France. These remains are anatomically modern, with a number of features distinct from Neandertals’, including a high and vertical forehead, flat browridges, a much narrower nasal aperture, and an overall gracile skull. (Photos © David L. Brill, humanoriginsphotos.com)

(a) (b)

Minatogawa

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as early as 35,000 yBP at Mladeč (Czech Republic) and at Peştera cu Oase (Roma­ nia). The latest archaic H. sapiens, the Neandertals, survived until at least 32,000 yBP or so at Vindija (Croatia). The overlap in dates between Neandertals and early modern humans indicates that the two groups coexisted in eastern Europe for at least several thousand years. This finding argues against the Multiregional Continuity model, which sees archaic  H.  sapiens as having evolved locally into modern H. sapiens. That the earliest modern H. sapiens had clear Neandertal features (such as the occipital bun) indicates interbreeding between Neandertals and early modern people. This finding argues against the Out­ of­ Africa model, which sees no gene flow between Neandertals and early modern humans. We will now see if the genetic record provides additional insight into modern H. sapiens’ origins in Europe.

ANCIENT DNA: INTERBREEDING BETWEEN NEANDERTALS AND EARLY MODERN PEOPLE?

Analysis of mitochondrial DNA (mtDNA), the DNA inherited only via the mother, offers potential clues about modern people’s origins (mtDNA is among the topics of chapter 3). Comparisons of mtDNA from more than a dozen Nean­ dertal skeletons— from Engis and Scladina in Belgium, Rochers de Villeneuve and La Chapelle­ aux­ Saints in France, Monte Lessini in Italy, El Sidrón in Spain, Feldhofer Cave in Germany, Mezmaiskaya in Russia, Teshik Tash in Uzbekistan, and Vindija Cave in Croatia— with that of early modern humans and living humans shows similarity among Neandertals and dissimilarity between Neandertals and

TABLE 12.2 Trends from Archaic Homo sapiens to Early Modern Homo sapiens

Archaic H. sapiens Early Modern H. sapiens

Brain Increase in size

Face Decrease in size and robusticity

1200 CC

Teeth and Jaws Decrease in size

1500 CC

R O M A N I A

C Z E C H R E P U B L I C

Předmostí Mladeč

Dolni Vestonice

Peştera cu Oase

Early Modern Homo sapiens

Early modern H. sapiens occurred first in Africa, later in Asia and Europe. The peopling of Europe, Asia, and Africa by only modern H. sapiens was complete by 25,000 yBP.

Locations (sites)1

Africa (Herto, Aduma, Bouri, Omo, Klasies River mouth, Lothagam, Wadi Kubbaniya, Wadi Halfa)

Asia (Skhul 5, Tianyuandong, Minatogawa) Europe (Peştera cu Oase, Mladeč, Předmostí, Dolni

Vestonice, Cro- Magnon, Grimaldi)

Chronology 160,000 yBP in Africa 90,000 yBP in western Asia 35,000 yBP in eastern Asia 32,000 yBP in Europe

Biology Vertical forehead, high skull, rounder skull, reduced facial robusticity, smaller teeth, reduced midfacial prognathism, 1,500 cc cranial capacity

Heat- adapted body morphology (small trunk, long limbs)

Culture and behavior

Upper Paleolithic Increased visible symbolic behavior (cave art) Burial of deceased with grave goods Decreased hunting, increased fishing, aquatic foods, likely

more plants, and reduced focus on big- game animals Technology changes reflect increased focus on fishing (e.g.,

bone harpoons)

1Sites mentioned in text.

C O N C E P T C H E C K !

modern humans. The German molecular geneticist Matthias Krings and his asso­ ciates found, for example, that 27 mtDNA base pairs of a sequence of 378 base pairs from the Feldhofer Cave Neandertal differ completely from living Europeans’. In contrast, living human populations have an average of just eight differences among them. These genetic differences seem to support the hypothesis that no gene flow occurred between Neandertals and modern humans during the later Pleistocene and, importantly, that Neandertals contributed none of their genetic material to the modern human gene pool. Neandertals underwent extinction, pure and simple. However, the extinction hypothesis may not be the best one. That is, mtDNA is just a tiny part of the human genome and reflects only a small fraction of the genetic code. The failure of one part of the genome to survive to the present does not mean that the entire genome became extinct. Moreover, it is possible that mtDNA lineages have been lost owing to genetic drift. Simply, much more of the genome is needed to have a more complete picture.

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Only recently has the remarkable scientific technology been available to analyze nuclear DNA to reconstruct the Neandertal genome. Such a reconstruction would make it possible to address the important question of the Neandertal contribution (if any) to the modern human genome. In a breakthrough study led by Swedish geneticist Svante Pääbo, a new technology applied to the analysis of three female Neandertal bones from Vindija Cave at last has provided the sequence of 4 billion base pairs representing the Neandertal genome. Pääbo and his team used high- throughput DNA sequencing, a technology through which much of a genome can be sequenced from a compilation of various genome fragments recovered from fossil bones. The results are breathtaking: Eurasians and Neandertals share between 1% and 4% of their nuclear DNA, an indication of a small but significant admixture. Given that Africans share no nuclear DNA with Neandertals, the admixture occurred between early modern Europeans and Neandertals after early modern people left Africa. People living today outside of Africa have DNA that likely originated from Neandertals. In that sense, the Neandertals are still with us!

But early modern  H.  sapiens may not have interbred with just Neandertals. Beginning in 2010, analysis of mitochondrial and nuclear DNA recovered from a hominin hand bone, foot bone, and a few teeth dating to 40,000 yBP from Denisova Cave, in southern Siberia, revealed a hominin genome that is neither Neandertal nor modern human. Svante Pääbo and his team, who reconstructed the Denisovan genome, expected to find a genome that was either Neandertal or modern human, but they came up with something very different from Neander­ tals or modern humans. The only similarity they could find with living people is from populations living in Melanesia (New Guinea and Bougainville Islands) and China. These findings suggest that genetic diversity in late Pleistocene Europe is more complex than previously thought. Namely, the genome came to include con­ tributions from some widespread populations that modern humans encountered as they migrated throughout Europe (the Neandertals) and from some very isolated people (the Denisovans). The Denisovans are likely archaic  H.  sapiens sharing a common origin with Neandertals. However, because paleoanthropologists have found only a few bones and teeth, we do not know what the Denisovans looked like. The genetic evidence strongly suggests that modern humans migrated from Africa and interbred with hominin species beyond just Neandertals. In fact, the European continent appears to have been inhabited by various isolated peoples. As research continues, the picture of genetic variation in humans on the evolutionary pathway toward modernity becomes increasingly complex.

LIVING PEOPLE’S GENETIC RECORD: SETTLING THE DEBATE ON MODERN HUMAN ORIGINS Living people’s genetic record helps settle the question about whether the Out­ of­ Africa model or the Multiregional Continuity model explains modern  H.  sapiens’ origins. The American geneticist and molecular biologist Rebecca Cann and her collaborators have found that sub­ Saharan African populations are more geneti­ cally diverse than populations from any other region of the world. That is, genes of people living south of the Sahara Desert today are more variable in frequency than are genes of people living in Europe, Asia, the Americas, and Australia (Figure  12.39). This pattern is also present in the phenotypic variation of ana­ tomical characteristics (e.g., cranial measurements).

Two explanations exist for Africa’s greater genetic diversity. First, a population or group of populations that has been around a long time will have accumulated

P O R T U G A L

Lagar Velho

FIGURE 12.39 Genetic Diversity Patterns of genetic diversity have been used to assess the Out- of- Africa and Multiregional Continuity models of modern humans’ origins. This graph shows genetic diversity within several major geographic groups, expressed as the average amount of genetic sequence divergence in percent. Note the much greater genetic diversity in Africans compared with other groups. (Source: Cann, R. L., M. Stoneking, and A. Wilson. 1987. Mitochondrial DNA and human evolution. Nature 325: 31–36.)

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Assimilation Model for Modern Human Variation: Neandertals Are Still with Us | 339

more mutations— hence, greater genetic variation— than a population or group of populations that has been around a short time. Therefore, Africa’s greater genetic diver­ sity may mean that modern people have existed longer there than in Asia or Europe.

Based on their assessment of mutation rates, Cann’s group came up with a figure of 200,000 yBP for the first early modern H. sapiens’ appearance, and this date is consistent with the earliest record of modern  H.  sapiens in Africa. Calculations based on other sources of genetic material, such as from the Y chromosome, pro­ vide broadly similar results.

The alternative explanation for Africa’s greater genetic diversity lies in its population structure compared with other continents’. The American anthro­ pological geneticist John Relethford observes that population size tremendously influences genetic diversity. As discussed in chapter 3, if the breeding population is small, genetic drift is a potentially powerful force for altering gene frequencies. Over time, genetic drift reduces genetic diversity in a small population (such as might have been the case in Europe and Asia). For example, if a group of 10 people splits off from a group of 1,000 people, the two resulting groups will show very different patterns of gene frequency change. The smaller population will be less variable, whereas its parent population will be more variable. Relethford argues that because in the remote past Africa had a significantly larger breeding popula­ tion size than other continents did, Africa now has greater genetic diversity.

Assimilation Model for Modern Human Variation: Neandertals Are Still with Us The more modern characteristics of East African skeletons from the Upper Pleis­ tocene (for example, Herto) provide compelling evidence that modern variation originated in Africa. The fossil record and the genetic record indicate, however, that neither the Out­ of­ Africa model nor the Multiregional Continuity model adequately explains modern humans’ origins. The Out­ of­ Africa model correctly accounts for the origin of modern human variation, but it incorrectly asserts that no gene flow occurred between Neandertals and modern H. sapiens. The Multire­ gional Continuity model is not correct about modern H. sapiens’ regional develop­ ment. However, it is correct about gene flow and the notion that Neandertals have contributed to modern H. sapiens’ gene pool.

In other words, elements of both models explain the emergence and evolution of fully modern people worldwide in the Upper Pleistocene. That is, sometime within 200,000–100,000 yBP, a population of modern heat­ adapted H. sapiens migrated from Africa to Europe and Asia. Once arriving in Europe, this population encoun­ tered members of their species— the Neandertals— who were as behaviorally and technologically complex as they. Neandertals, cold­ adapted people, had evolved from earlier  H.  sapiens populations in Europe— the early archaic  H.  sapiens— and they interbred with the newly arrived modern H. sapiens. Therefore, Neandertals’ disappearance after 30,000 yBP or so likely resulted not from their extinction but from their assimilation by much larger, more genetically diverse populations of modern humans migrating into Europe from Africa during the late Pleistocene

Grimaldi Caves

I TA LY

Cro-Magnon

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D E M O C R AT I C R E P U B L I C O F T H E C O N G O

Katanda

340 | CHAPTER 12 The Origins, Evolution, and Dispersal of Modern People

(Figure 12.40). Neandertals contributed to the gene pool of today’s European and European­ descended populations, leaving their genetic, behavioral, and adaptive legacy with modern humans in Europe and in Asia.

Modern Humans’ Other Migrations: Colonization of Australia, the Pacific, and the Americas This chapter and the preceding one have emphasized migration’s critical impor­ tance in human evolution. In the first wave out of Africa,  H.  erectus spread rapidly throughout Asia and Europe. In the second wave out of Africa, early mod­ ern H. sapiens assimilated and eventually replaced the descendants of H. erectus in Asia and Europe. The last 50,000 years of the Pleistocene saw fully modern people

FIGURE 12.40 Assimilation Model According to this model, modern Homo sapiens evolved first in Africa from Homo erectus. Groups of Homo sapiens then spread to Europe and Asia. Once in Europe and Asia, these modern H. sapiens interbred with populations they encountered, the late archaic H. sapiens (Neandertals). This admixture is the biological foundation for modern H. sapiens living outside of Africa today.

Africa

H. erectus

Late Archaic Homo sapiens

Late Archaic Homo sapiens

Late Archaic Homo sapiens

West and Central Asia

Europe East Asia

Australasia

Early Archaic Homo sapiens

M od

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H om

o sa

pie ns

Models for Explaining Modern Homo sapiens’ Origins

Charles Darwin first presented his theory of evolution in his book On the Origin of Species (1859). Based on years of personal observation and of study, this unifying biological theory drew on geology, paleontology, taxonomy and systematics, and demography.

Model Features Proponent

Out- of- Africa Modern biology, behavior, and culture originated in Africa.

Modern humans spread from Africa to Europe after 50,000 yBP.

Modern humans replaced all populations once arriving in Europe, with no gene flow.

Christopher Stringer

Multiregional Continuity Modern humans evolved from earlier archaic populations in their respective regions (Africa, Europe, Asia).

Throughout evolution, there is always significant gene flow on the borders of populations.

There is continuity of morphology in all regions of the globe.

Milford Wolpoff

Assimilation Modern humans first evolved in Africa, then spread to Europe and Asia.

Once they arrived in Europe and Asia, modern humans underwent gene flow with Neandertals.

Fred Smith, Erik Trinkaus

C O N C E P T C H E C K !

Modern Humans’ Other Migrations: Colonization of Australia, the Pacific, and the Americas | 341

spread not only into Asia and Europe but also to continents that had previously not been occupied by people. Prior to 50,000 yBP, humans occupied only three of the six inhabitable continents: Africa, Asia, and Europe. After 50,000 yBP, populations migrated from the southeastern fringes of Asia to Australia, eventually fanning out from west to east across the hundreds of islands that dot the Pacific Ocean. In the last few millennia of the Pleistocene, humans spread to the Americas (Figure 12.41). These movements, and their accompanying adaptations to unfamiliar environments, are no less a part of human evolution than are bipedalism, language use, and all the other key developments discussed in this chapter and chapter 11.

What motivated these early modern people to move? Among the multiple reasons, four are most important: population increase, disappearance of food resources, increased competition with neighbors for remaining resources, and climate deterioration. That is, a population’s resources— food especially— are available in finite quantities. As Relethford has shown through genetic studies, African populations expanded rapidly during the late Pleistocene. These increases, as populations outgrew their carrying capacities, were the prime force stimulating anatomically modern people to move into Asia and Europe. Similarly, as popula­ tion size expanded in Asia and Europe, humans continued to move and began to occupy vast regions of the globe.

I TA LY

Monte Lessini

F R A N C E

Les Rochers de Villeneuve

Engis B E L G I U M

Mezmaiskaya

R U S S I A

(Figure 12.40). Neandertals contributed to the gene pool of today’s European and European­ descended populations, leaving their genetic, behavioral, and adaptive legacy with modern humans in Europe and in Asia.

Modern Humans’ Other Migrations: Colonization of Australia, the Pacific, and the Americas This chapter and the preceding one have emphasized migration’s critical impor­ tance in human evolution. In the first wave out of Africa,  H.  erectus spread rapidly throughout Asia and Europe. In the second wave out of Africa, early mod­ ern H. sapiens assimilated and eventually replaced the descendants of H. erectus in Asia and Europe. The last 50,000 years of the Pleistocene saw fully modern people

FIGURE 12.40 Assimilation Model According to this model, modern Homo sapiens evolved first in Africa from Homo erectus. Groups of Homo sapiens then spread to Europe and Asia. Once in Europe and Asia, these modern H. sapiens interbred with populations they encountered, the late archaic H. sapiens (Neandertals). This admixture is the biological foundation for modern H. sapiens living outside of Africa today.

Africa

H. erectus

Late Archaic Homo sapiens

Late Archaic Homo sapiens

Late Archaic Homo sapiens

West and Central Asia

Europe East Asia

Australasia

Early Archaic Homo sapiens

M od

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H om

o sa

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342 | CHAPTER 12 The Origins, Evolution, and Dispersal of Modern People

Beginning in the very late Pleistocene, eastern Asia became the stepping­ off point for migrations to previously unoccupied continents. Southeast Asia served as the stepping­ off point for the movements to Australia and across the Pacific as people eventually occupied most of the 20,000–30,000 islands between Australia and the Americas. Northeast Asia served as the stepping­ off point for the spread to North America and South America.

DOWN UNDER AND BEYOND: THE AUSTRALIAN AND PACIFIC MIGRATIONS In the late Pleistocene, sea levels were considerably lower than they are today, by as much as 90 m (300  ft), exposing land surfaces now submerged by water and making them available for human occupation and movement between landmasses. Australia, New Guinea, and Tasmania constituted a single landmass, which we call Greater Australia (Figure  12.42). The islands of Sulawesi, Borneo, and Java were connected to mainland Asia. Even at the peak of the late Pleistocene’s coldest period, when sea levels were at their lowest, a considerable distance of open water separated Greater Australia from Asia. At least 70 km (43.5 mi) of open water sep­ arated Sulawesi and Borneo from Australia. To traverse open water from southeast­ ern Asia to Australia, late Pleistocene humans would have needed sophisticated boating technology and equally sophisticated navigational skills. No evidence of

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FIGURE 12.41 Modern Humans’ Migrations Another major research question in physical anthropology focuses on modern humans’ spread from Asia to Australia, the Pacific, North America, and South America. This map shows modern humans’ migration patterns from southern Asia (1 a– 6a) and eastern Asia (1 b– 3b) beginning in the late Pleistocene: (1a) earliest migration of modern Homo sapiens into Australia (Lake Mungo; ~50,000–40,000 yBP); (2a) earliest evidence of modern human occupation of New Guinea and adjacent islands (Bobongara; ~35,000 yBP); (3a) earliest evidence of modern human occupation of Tasmania (Warreen Cave; ~33,000 yBP); (4a) early expansion into Oceania (Mariana Islands; ~1500 BC); (5a) oceanic expansion into western Polynesia (Tonga and Samoa; ~1000 BC); (6a) expansion into eastern Polynesia (Cook Islands; ~AD 700); (1b) earliest evidence for expansion from northeast Asia into North America (Beringia; ~15,500 yBP— or Clovis, New Mexico; ~12,000 yBP); (3b) proposed coastal route for colonization of the New World and to South America (Monte Verde, Chile; ~14,500 yBP).

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Modern Humans’ Other Migrations: Colonization of Australia, the Pacific, and the Americas | 343

such technology and skills has been found. Modern humans seem to have had simply enough know­ how to reach Australia, which they ultimately colonized.

The earliest archaeological evidence of humans in Australia is from Lake Mungo, in western New South Wales, dating to about 40,000 yBP (Figure 12.43). The two skulls from Lake Mungo, from an adult male and an adult female, have modern characteristics: the skulls are high and have rounded foreheads with small browridges. In overall appearance, the skulls resemble ones from Kow Swamp, in Victoria’s Murray River Valley, which date to 13,000–9,000 yBP (Figure 12.44). However, the Kow Swamp skulls are more robust, with larger browridges, larger and more robust faces, and lower foreheads than the Lake Mungo skulls. These early Australians share features with  H.  erectus and later Indonesian hominins, especially in the facial skeleton, such as in the eye orbits’ shape. These anatomical similarities suggest a common genetic origin, thereby indicating regional continu­ ity of human populations and their biological evolution.

These early Australians also bear a strong similarity to native people who inhabit the continent today; the anatomical evidence indicates an ancestral­ descendant relationship. However, mtDNA from the Lake Mungo and Kow Swamp skeletons differs substantially from living native Australians’. Based on the mtDNA evidence alone, one might conclude that the ancient populations represented by the Lake Mungo and Kow Swamp skeletons were not ancestral to living native Australians; but this conclusion runs counter to a range of cultural and archaeological evidence. As with the Neandertal mtDNA lineages discussed above, a more likely explanation for the disparity between ancient and modern genes in Australia is that the mtDNA sequence in ancient anatomically modern people has not survived to the present. This Australian evidence is an important example of the very different evolutionary pathways that mtDNA and anatomical evolution can take. The fossil remains show continuity with modern native people of Australia, but the mtDNA lineage went extinct at some point after 40,000 yBP.

Southeast Asia is also the point of origin for populations that eventually dispersed throughout the Pacific Ocean. Unlike Australia, which was settled by 40,000 yBP, most of the Pacific islands extending from east of New Guinea to

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FIGURE 12.42 Land Bridge During the late Pleistocene, temperatures were much cooler and a great amount of seawater was locked in glaciers. As a result, sea levels were at their lowest, exposing shallow land, such as the Sunda shelf in Southeast Asia. On this map, the exposed land is white. Some of it connected the islands of Southeast Asia (Borneo, Java, and Sumatra) with the Asian mainland, and some of it connected Australia with New Guinea and Tasmania. Despite the increased land area, traveling to Australia would have required a sea voyage; however, there was much less distance between Southeast Asia and Australia. Modern researchers are unable to investigate evidence of the people who once inhabited the areas that are now underwater.

FIGURE 12.43 Lake Mungo This Australian site has yielded the oldest human skeleton in Australia.

344 | CHAPTER 12 The Origins, Evolution, and Dispersal of Modern People

Easter Island were not settled until well after 5,000 yBP. In fact, east of the Solo­ mon Islands, settlement across the vast Pacific did not begin until after about 1500 BC, ending with humans’ arrival on Easter Island around AD 600.

The discovery of skeletal remains dating to about 18,000 yBP may challenge long­ standing conclusions about the evolution of modern H. sapiens in far eastern Asia. In 2003, scientists found a skeleton with highly unusual characteristics in a cave on the Indonesian island of Flores (Figure  12.45). Dubbed the “hobbit” by the popular press, this hominin had an extremely tiny brain (400 cc) and stood only slightly above 1 m (about 3.5  ft). Anthropologists disagree on how to interpret these and other characteristics. The Australian anthropologists Peter Brown and Michael Morwood and colleagues regard the skeleton as evidence for the long­ term presence of an archaic species of hominin, distinctive from modern people. In fact, they consider it a newfound species of Homo, which they have called Homo floresiensis. In their interpretation of this species’ existence, a group of primitive humans became isolated early in human evolution, and their isolation led to a unique pattern of biological variation. Alternatively, the Indonesian paleo­ anthropologist Teuku Jacob and colleagues argue that this hominin was not part of a different species but a modern human who suffered from microcephaly or some other genetic or developmental abnormality. They point out that numerous cranial features of  H.  floresiensis are within the modern range of variation seen in living populations from the larger region. In addition, some of the creature’s anatomical characteristics (such as a small or absent chin and rotated premolars) resemble those of populations now living in the immediate region. This alternative hypothesis is bolstered by the apparent absence of ancestors. Without the fossils of evolutionary precursor species and more fossils from H. floresiensis, it is difficult to say whether this skeleton and other fragments recovered from the cave represent a dwarfed human species or a person with a developmental/genetic disorder. The controversy, like those surrounding Pithecanthropus and Neandertals, will remain unresolved until scientists discover and analyze more evidence.

ARRIVAL IN THE WESTERN HEMISPHERE: THE FIRST AMERICANS The American physical anthropologist Aleö Hrdlička first noted the remarkable similarity in the shapes of the upper incisors of eastern Asian and Native American peoples, past and present. He observed that Asians and Native Americans have shovel­ shaped incisors (Figure 12.46). In these incisors and many other dental features, the American anthropologists Albert Dahlberg and Christy Turner have identified a common ancestry for eastern Asians and Native Americans. Common ancestry is supported by the fact that most Native Americans today have exclu­ sively blood type  O.  Moreover, the alleles for this blood type are present with only limited variation. It is likely that the founding population, then, had these characteristics.

Additional clues about the peopling of the Americas appear in modern and ancient Native Americans’ mtDNA. For 95% of living Native Americans through­ out North America and South America, mtDNA falls into any one of four haplogroups— A, B, C, or  D. (As discussed in chapter  3, mtDNA is inherited just from the mother, so the haplogroup unit reflects the maternal line of inher­ itance.) Interestingly, the same pattern of four main haplogroups has been found in mtDNA recovered from ancient Native American skeletons. This sharing of haplogroups by modern people and ancient skeletons indicates a common

FIGURE 12.44 Kow Swamp This Australian site has yielded skeletons much more robust than those discovered at Lake Mungo. In fact, Alan Thorne, who excavated the skull, originally believed the remains to be a Homo erectus skeleton rather than a modern human skeleton.

Homo floresiensis Nicknamed “Hobbit” for its diminutive size, a possible new spe- cies of Homo found in Liang Bua Cave, on the Indonesian island of Flores.

Flores

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FIGURE 12.45 Flores Woman A recent discovery on Flores Island, Indonesia, has become the source of much debate in anthropology. Some researchers believe this “hobbit” represents a group of early hominins that evolved in isolation in the far western Pacific region. Others believe this skeleton belonged to a modern human who had some developmental or genetic abnormality. (Reconstruction photo [bottom left] © 2007 Photographer P. Plailly/E. Daynès/Eurelios/ Look at Sciences— Reconstruction Elisabeth Daynès, Paris)

The cranium is very small, especially compared with that of a modern human.

This artist’s reconstruction shows what Flores Woman may have looked like in life.

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B o r n e oS u m a t r a

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P A C I F I C O C E A NB A N D A S E AJakarta

SINGAPORE

Flores Island

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Based on measurements of the long bones, the Flores individual would have been approximately 1.0 m (3 ft) tall, considerably shorter than the average modern human.

microcephaly A condition in which the cranium is abnormally small and the brain is underdeveloped.

shovel- shaped incisors A dental trait, commonly found among Native Ameri- cans and Asians, in which the incisors’ posterior aspect has varying degrees of concavity.

Modern Humans’ Other Migrations: Colonization of Australia, the Pacific, and the Americas | 345

Easter Island were not settled until well after 5,000 yBP. In fact, east of the Solo­ mon Islands, settlement across the vast Pacific did not begin until after about 1500 BC, ending with humans’ arrival on Easter Island around AD 600.

The discovery of skeletal remains dating to about 18,000 yBP may challenge long­ standing conclusions about the evolution of modern H. sapiens in far eastern Asia. In 2003, scientists found a skeleton with highly unusual characteristics in a cave on the Indonesian island of Flores (Figure  12.45). Dubbed the “hobbit” by the popular press, this hominin had an extremely tiny brain (400 cc) and stood only slightly above 1 m (about 3.5  ft). Anthropologists disagree on how to interpret these and other characteristics. The Australian anthropologists Peter Brown and Michael Morwood and colleagues regard the skeleton as evidence for the long­ term presence of an archaic species of hominin, distinctive from modern people. In fact, they consider it a newfound species of Homo, which they have called Homo floresiensis. In their interpretation of this species’ existence, a group of primitive humans became isolated early in human evolution, and their isolation led to a unique pattern of biological variation. Alternatively, the Indonesian paleo­ anthropologist Teuku Jacob and colleagues argue that this hominin was not part of a different species but a modern human who suffered from microcephaly or some other genetic or developmental abnormality. They point out that numerous cranial features of  H.  floresiensis are within the modern range of variation seen in living populations from the larger region. In addition, some of the creature’s anatomical characteristics (such as a small or absent chin and rotated premolars) resemble those of populations now living in the immediate region. This alternative hypothesis is bolstered by the apparent absence of ancestors. Without the fossils of evolutionary precursor species and more fossils from H. floresiensis, it is difficult to say whether this skeleton and other fragments recovered from the cave represent a dwarfed human species or a person with a developmental/genetic disorder. The controversy, like those surrounding Pithecanthropus and Neandertals, will remain unresolved until scientists discover and analyze more evidence.

ARRIVAL IN THE WESTERN HEMISPHERE: THE FIRST AMERICANS The American physical anthropologist Aleö Hrdlička first noted the remarkable similarity in the shapes of the upper incisors of eastern Asian and Native American peoples, past and present. He observed that Asians and Native Americans have shovel­ shaped incisors (Figure 12.46). In these incisors and many other dental features, the American anthropologists Albert Dahlberg and Christy Turner have identified a common ancestry for eastern Asians and Native Americans. Common ancestry is supported by the fact that most Native Americans today have exclu­ sively blood type  O.  Moreover, the alleles for this blood type are present with only limited variation. It is likely that the founding population, then, had these characteristics.

Additional clues about the peopling of the Americas appear in modern and ancient Native Americans’ mtDNA. For 95% of living Native Americans through­ out North America and South America, mtDNA falls into any one of four haplogroups— A, B, C, or  D. (As discussed in chapter  3, mtDNA is inherited just from the mother, so the haplogroup unit reflects the maternal line of inher­ itance.) Interestingly, the same pattern of four main haplogroups has been found in mtDNA recovered from ancient Native American skeletons. This sharing of haplogroups by modern people and ancient skeletons indicates a common

FIGURE 12.44 Kow Swamp This Australian site has yielded skeletons much more robust than those discovered at Lake Mungo. In fact, Alan Thorne, who excavated the skull, originally believed the remains to be a Homo erectus skeleton rather than a modern human skeleton.

Homo floresiensis Nicknamed “Hobbit” for its diminutive size, a possible new spe- cies of Homo found in Liang Bua Cave, on the Indonesian island of Flores.

Flores

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FIGURE 12.45 Flores Woman A recent discovery on Flores Island, Indonesia, has become the source of much debate in anthropology. Some researchers believe this “hobbit” represents a group of early hominins that evolved in isolation in the far western Pacific region. Others believe this skeleton belonged to a modern human who had some developmental or genetic abnormality. (Reconstruction photo [bottom left] © 2007 Photographer P. Plailly/E. Daynès/Eurelios/ Look at Sciences— Reconstruction Elisabeth Daynès, Paris)

The cranium is very small, especially compared with that of a modern human.

This artist’s reconstruction shows what Flores Woman may have looked like in life.

I N D O N E S I A

B o r n e oS u m a t r a

J a v a

S u l a w e s i

M A L AY S I A

I N D I A N O C E A N

P A C I F I C O C E A NB A N D A S E AJakarta

SINGAPORE

Flores Island

500 mi0

0 500 km

Based on measurements of the long bones, the Flores individual would have been approximately 1.0 m (3 ft) tall, considerably shorter than the average modern human.

microcephaly A condition in which the cranium is abnormally small and the brain is underdeveloped.

shovel- shaped incisors A dental trait, commonly found among Native Ameri- cans and Asians, in which the incisors’ posterior aspect has varying degrees of concavity.

Clovis

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346 | CHAPTER 12 The Origins, Evolution, and Dispersal of Modern People

founding ancestry for present and past Native Americans. Moreover, Native Americans share haplogroups with north­ eastern Asians. The evidence indicates that the haplogroups were present in Asians who migrated to the Americas. The presence of all four groups throughout the Americas and the great similarity of the nucleotide sequences suggest that they share a common ancestry in a single founding population that arrived in the Americas from Asia via one migration. Consis­ tent with the mtDNA evidence from skeletal remains is the emerging record provided by the sequencing of the nuclear DNA from a Paleoindian young boy’s skeleton from Anzick, Montana, dating to the late Pleistocene (ca. 12,700 yBP). The strong similarity of the genome with native people today indicates that the person was part of the earliest wave of population giving rise to all indigenous groups in North and South America. Research by the American anthropological

geneticist Connie Mulligan and her colleagues suggests that the founding popula­ tion consisted of only about 800 people. The dental and the genetic evidence points to northeast Asia during the late Pleistocene for native New World people’s origin.

This northeastern Asian origin indicates that, in contrast to Australia’s found­ ing populations, who were adapted to tropical, wet climates, the Americas’ found­ ing populations were adapted to cold, dry climates. Both migrations indicate that these founding humans were adapted to extreme environments at the margins of human capabilities.

In contrast to the migrations to Australia and the Pacific, where the founders traveled across open seas, migrations to the Americas occurred via a land route or along the deglaciated Pacific coastline. If it was a land route, it was likely across the Bering land bridge (which we call Beringea), connecting Siberia and Alaska. Like those in the western Pacific Ocean, this land route was created when sea levels reached a low point during the later Pleistocene, exposing areas of land that are now submerged.

Genetic dating based on mutation rates of mtDNA and Y chromosomes as well as single nucleotide polymorphisms (SNPs) (see chapter 4) indicates that the migration from Asia to the Americas likely took place sometime around 15,000 yBP. The genetic findings indicate that one early migration resulted in the ances­ tral population for most Native Americans of North America and South America today. The uniform distribution of haplotypes across the Americas indicates that the migration was a rapid process and not a slow diffusion. Two other smaller and much later migrations from Asia yielded the founding populations of Na­ Dené speakers of northwestern North America and the Navajo and Apache of the southwestern United States and speakers of Eskimo­ Aleut languages. In North America, the earliest well­ documented archaeological record of habitation and material culture (especially stone artifacts) dates to around 11,500 yBP. The earliest people associated with this and other early cultures are called Paleoindians. They are well known from stone artifacts, especially large spear points associated with pre­ Clovis, Clovis, and later Folsom cultures. The Paleoindians hunted various animals, but they are best known for hunting megafauna, the large Pleistocene game such as the mammoth, steppe bison, and reindeer/caribou, and processing the meat from these animals for food (Figure 12.47).

Pleistocene megafauna became extinct by the early Holocene, and some evi­ dence suggests that in the Americas and Australia humans hunted these large animals to extinction. It seems unlikely, however, that small numbers of humans

Paleoindians The earliest hominin inhabi- tants of the Americas; they likely migrated from Asia and are associated with the Clovis and Folsom stone tool cultures in North America and comparable tools in South America.

Clovis Earliest Native American (“Paleoin- dian”) culture of North America; technol- ogy known for large, fluted, bifacial stone projectile points used as spear points for big- game hunting.

FIGURE 12.47 Paleoindians The tools the Paleoindians hunted with included a specialized, fluted projectile point, which we call a Folsom point. An extraordinary amount of skill was required to make this tool.

FIGURE 12.46 Shovel- Shaped Incisors A dental characteristic often found in East Asians is the shoveled appearance of the back, or lingual side, of the incisors. That this trait has also been found in Native Americans likely reflects their descent from East Asians.

Modern Humans’ Other Migrations: Colonization of Australia, the Pacific, and the Americas | 347

could have killed so many animals in such a short time. These extinctions were more likely due to climate change at the end of the Pleistocene and the changes in habitats frequented by large mammals. If humans’ hunting during the late Pleisto­ cene and early Holocene was involved, it played a very minor part.

The Paleoindians differed anatomically from recent Native Americans. The Paleoindians’ skulls were relatively long and narrow, and their faces were robust, with large attachment areas for the mastication muscles. In contrast, many late prehistoric and living Native Americans have short, round skulls with gracile faces. For example, the Paleoindian skull from Kennewick, Washington, dating to 8,400 yBP, is long and narrow; the face and jaws are robust (Figure 12.48). These differences between the Paleoindians and modern Native Americans have  been interpreted to mean either that the Paleoindians are not the living Native Americans’ ancestors or, alter­ natively, that the Paleoindians are the living Native Americans’ ancestors but cranial morphology has changed due to evolutionary forces and other processes over the last 10,000 years in the Americas (discussed further in chapter 13). The discovery in 2015 by Eske Willerslev and his team at the Natural History Museum of Denmark that the genetic variation—autosomal, mtDNA, and Y­chromosomal—is strongly similar between Kennewick Man and recent Native Americans makes the latter scenario more likely. That is, the ancestral­descendant genetic relationship supports the model that the cranial morphology evolved and was shaped by later processes, such as those involving use of the face and jaws in mastication.

Modern humans’ emergence and subsequent dispersal around the globe marks a remarkable period of population expansion and behavioral and biological diver­ sification. The geographic biological diversity in the world today was likely well in place by the end of the Pleistocene. The rapid expansion of human population size resulted in increased types of foods eaten. The adoption and increased use of fish and aquatic life in general during the late Pleistocene likely reflects humans’ need for alternative foods as population size expanded. Such dietary expansion set the stage for one of the most dramatic adaptive shifts in human evolution, the shift from eating plants that were gathered and animals that were hunted to eating plants and animals that were both domesticated. In the next chapter, we will look at this important transition’s biological implications for humans over the last 10,000 years of our evolution.

FIGURE 12.48 Kennewick Man (a) Discovered on the banks of the Columbia River, Kennewick Man represents the Paleoindians. (b) This artist’s reconstruction shows the Paleoindians’ likely facial appearance.(a) (b)

Folsom Early Native American (immedi- ately following Clovis) culture of North America; technology known for large, fluted, bifacial projectile points used as spear points for big- game hunting.

megafauna General term for the large game animals hunted by pre- Holocene and early Holocene humans.

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What is so modern about modern humans? • Modern humans have a number of anatomical

characteristics that distinguish them from premodern humans. These include a small face, small jaws, small teeth, a vertical and high forehead, a narrow nasal aperture, a narrow body trunk, and long legs.

What do Homo sapiens fossils reveal about modern humans’ origins? • The H. sapiens fossil record shows early

archaic H. sapiens evolving from a Homo erectus ancestor.

• There is evidence of regional diversification after 200,000 yBP. In Africa, early nearly modern people evolved 200,000–150,000 yBP. After 130,000 yBP, an archaic form of H. sapiens called Neandertals occupied much of Europe and of western Asia.

• From perhaps as long ago as 40,000–25,000 yBP, hominin groups occupied Europe— the Neandertals and modern H. sapiens. The former had various archaic features and a cold- adapted body morphology. The latter had modern characteristics and a heat- adapted body morphology. The presence of a third group— the Denisovans, with a genome distinct from those of Neandertals and modern H.  sapiens— indicates that diversity in late Pleistocene Europe was complex.

How has the variation in fossil H. sapiens been interpreted? • The Out- of- Africa model argues that

modern H. sapiens migrated from Africa to Asia and Europe. Once in Asia and Europe, they replaced indigenous late archaic H. sapiens, including the Neandertals in Europe and in western Asia.

• The Multiregional Continuity model argues that modern H. sapiens arose regionally in each of the three inhabited continents: Africa, Asia, and Europe.

• The combined presence of archaic (Neandertal) and modern anatomical characteristics in some late Pleistocene European skeletons and the overlap in DNA structure indicate that Neandertals were not replaced by modern H. sapiens. Rather, instead of disappearing through extinction, Neandertals were assimilated through admixture with early modern H. sapiens. Admixture is revealed in the fossils— from physical characteristics in bones and teeth and from the DNA. Thus, the fundamental details of modern human anatomy probably have a single place of origin (Africa), but Neandertals later contributed to the European gene pool. Neandertals are part of modern humans’ ancestry.

What other developments took place in H. sapiens’ evolution? • Modern characteristics including more advanced tool

technology, diversification of diet, and symbolism appeared first in Africa and later in Europe and Asia.

• Anthropologists do not know when spoken communication began, but at least one Neandertal had the vocal anatomy consistent with speech.

• Neandertals and contemporary humans were the first species to intentionally bury their dead.

• An important theme in human evolution is migration and expansion into regions of the globe not previously occupied. Fully modern humans migrated to Australia by 40,000 yBP and to North America and South America by 15,000 yBP. By the beginning of the Holocene, humans lived on all inhabitable continents (Antarctica is the only uninhabitable continent).

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K E Y T E R M S calculus Clovis Folsom Homo floresiensis Levallois

megafauna microcephaly Middle Paleolithic Mousterian occipital bun

Paleoindians shovel- shaped incisors Upper Paleolithic

E V O L U T I O N R E V I E W The Origins of Modern People

Synopsis Since some of the earliest discoveries of hominin fossils, such as that of the Neandertal skull found in Germany in 1856, physical anthropologists have uncovered an amazing amount of information about our evolutionary past. Fossil discoveries, as well as the application of new technologies in genetic research, have helped clarify the relationship between anatomically modern humans and our evolutionary cousins, the Neandertals. These results have also helped determine the most likely scenario for the origin and subsequent global dispersal of our own species, Homo sapiens, from approximately 200,000 yBP to the present. The remarkable discoveries made and rigorous scientific study performed by paleoanthropologists have given us a much deeper insight into the biology and behaviors that characterize the early members of our own species and continue to inform our under- standing of what it means to be human.

Q1. Provide two examples of anatomical features that physical anthropologists consider to be “modern” when defining mod- ern humans as a species (H. sapiens). Also, identify two ways in which these “modern” features contrast with the morphological characteristics present in earlier members of the genus Homo.

Q2. As discussed in chapter  5, modern human variation is highly influenced by environmental factors, including climate, latitude, and altitude. Describe three cranial and postcranial features of Neandertal skeletons that are likely adaptations to the cold climates of Upper Pleistocene Europe.

Q3. Many early descriptions and modern popular depictions por- tray Neandertals as particularly primitive in comparison to anatomically modern humans. Summarize the various aspects of Neandertal behavior and culture that strongly counter the assumption that they were simplistic, cognitively deficient evolutionary failures.

Q4 . Contrast the Out- of- Africa and Multiregional Continuity models for explaining the origins of anatomically modern H. sapiens. Using both fossil and genetic evidence, outline how neither model by itself adequately explains modern human origins but how elements of both contribute to the Assimilation model.

Hint Consider the genetic evidence from both fossil speci- mens and living human populations.

Q5. Over 1.5  million years after Homo erectus became the first hominin species to migrate out of Africa, modern H.  sapiens also spread from Africa to Europe and Asia and from there to Australia and the Americas. What kinds of environmental pressures contributed to the dispersal of modern  H.  sapiens across all regions of the globe? What do the migrations of modern humans into Australia (at least 40,000 yBP) and the Americas (at least 15,000 yBP) tell us about the range of human variation and adaptability in the past? How does this compare to the diversity we see in human populations today?

A D D I T I O N A L R E A D I N G S

Bräuer, G. 2008. The origin of modern anatomy: by speciation or intraspecific evolution. Evolutionary Anthropology 17: 22–37.

Disotell, T. R. 2012. Archaic human genomics. Yearbook of Physical Anthropology 55: 24–39.

Meltzer, D. J. 2009. First Peoples in a New World: Colonizing Ice Age America. Berkeley: University of California Press.

Nowell,  A.  2010. Defining behavioral modernity in the context of Neandertal and anatomically modern human populations. Annual Review of Anthropology 39: 437–452.

O’Connell,  J.  F.  and  J.  Allen. 1998. When did humans first arrive in greater Australia and why is it important to know? Evolutionary Anthropology 6: 132–146.

O’Rourke, D. H., M. G. Hayes, and S. W. Carlyle. 2000. Ancient DNA studies in physical anthropology. Annual Review of Anthropology 29: 217–242.

Relethford, J. H. 2001. Genetics and the Search for Modern Human Origins. New York: Wiley- Liss.

Ruff,  C.  B.  1993. Climatic adaptation and hominid evolution: the thermoregulatory imperative. Evolutionary Anthropology 2: 53–60.

Trinkaus,  E.  and  P.  Shipman. 1993. Neandertals: images of our- selves. Evolutionary Anthropology 1: 194–201.

Wolpoff, M. H. and R. Caspari. 1997. Race and Human Evolution: A Fatal Attraction. New York: Simon & Schuster.

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ONCE HUMANS BEGAN practicing agriculture, corn, wheat, and rice were three of the main crops they cultivated. The movement from procuring wild food to producing food has had many varied outcomes for modern Homo sapiens, including the decline of health.

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How did agriculture affect human living circumstances?

How did agriculture affect human biological change?

What are the most important forces shaping human biology today?

Are we still evolving?

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Our Last 10,000 Years Agriculture, Population, Biology

One of my greatest disappointments as a child was when my dentist told me my teeth were crooked and had to be fixed. My dentist was able to fix the problem by removing a lower third premolar on each side of my mandible, making room for other teeth to grow without crowding taking place. Most of my friends were not so lucky— the problems with their teeth required years of treatment, which involved painful throbbing after each orthodontic visit (in which the braces were tightened as in some kind of medieval torture); a tinny flavor no matter what was eaten; food stuck in the wiring; and, perhaps worst of all, dietary restrictions: no popcorn, no gum, no caramel, nothing sweet and sticky— in short, none of the wonderful comforts of “civilization” (Figure 13.1).

Tooth crowding and malocclusion— improper fit of the upper and lower teeth, some- times called underbite or overbite— are commonplace around much of the world today. Millions of people have crowded, misaligned teeth. This phenomenon has not always been the case, however. It has occurred mostly within the last 10,000 years— the Holo- cene. What happened?

This development, not present for most of human evolution, came about because of changes in what humans ate and how they prepared food for consumption. Namely, they switched from a diet of wild plants and wild animals to a diet partly based on domes- ticated plants and domesticated animals. In other words, in many areas of the world humans gave up hunting and gathering for agriculture (farming). Simply, they shifted from foraging for their food to producing their food. Moreover, they invented pottery, which was used for, among other functions, boiling food into soft mushes. As a result of this new technology, foods became much softer than ever before. These changes in

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what was eaten and how it was prepared reduced the stresses on humans’ chewing muscles. This reduced stress, like that on any muscle, also reduced the underlying bone. Basically, we have smaller jaws because our ancestors began eating softer foods. (Remember Wolff’s Law, discussed in chapter 5: bone develops where it is needed and recedes where it is unnecessary.)

Tooth size is under stronger genetic control than is bone size, and as a result, tooth size is less affected by the environment. And as a consequence, humans’ teeth had much less room to grow, resulting in the remarkable increase in crowded and poorly occluded teeth (Figure 13.2). The malocclusion epidemic, part of recent human evolution, is one of many consequences of our species’ dietary change and but one example of our very dynamic biology.

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(b)

FIGURE 13.1 Braces (a) Straightening teeth has become so common that in the United States orthodontics is a multibillion- dollar industry. Among the braces used are (b) the standard wires and apparatus, both stainless steel. ([a] www.CartoonStock.com)

(a) Overbite (b) Underbite

FIGURE 13.2 Malocclusion Two major forms of malocclusion can be corrected with orthodontic treatments, including braces. (a) An overbite occurs when the maxillary teeth extend farther forward than the mandibular teeth. (b) An underbite occurs when the mandibular teeth extend farther forward than the maxillary teeth.

The Agricultural Revolution: New Foods and New Adaptations | 353

The Agricultural Revolution: New Foods and New Adaptations Up until this point— to around 10,000 yBP or so— humans had acquired all their food through hunting and gathering. They hunted, trapped, fished, and otherwise collected animals big and small, terrestrial and aquatic; and they collected a huge variety of plants. During the later Pleistocene, they began to intensively exploit fish and shellfish, in oceans, lakes, streams, and so on. In the final centuries of that epoch, at the key environmental transition from the Pleistocene’s cold and dry climate to the Holocene’s warm and wet climate, people began to control animals’ and plants’ growth cycles, through a process anthropologists call domestication. Eventually, humans replaced nearly all the wild animals and wild plants in their diets with domesticated animals and domesticated plants. This dramatic change in lifeway— where people at the end of the Pleistocene and the early Holocene raised the animals and grew the plants they ate— is associated with the period called the Neolithic.

The shift from foraging to farming is among the most important adaptive transitions in hominin evolution. I rank it up there with bipedalism and speech as being fundamental to who humans are as an organism. As will be discussed in this chapter, this shift had important and long- lasting implications for Homo as an evolving organism. For example, many diseases we have today are linked in one way or another to this remarkable change in lifeway.

For 99.8% of the 7 million years of human evolution, hominins had eaten plants of all kinds, but never before had they grown them. Domesticated plants quickly became an integral part of food production across much of the globe, but that quickness is relative to the geologic timescale. Rather than happening overnight, in other words, the shift from foraging to farming took place over centuries and likely involved many successes and failures as the process unfolded for different human populations around the world (Figure 13.3). Compared with evolutionary changes that took place over thousands or hundreds of thousands of years, the transitional process of domestication— the dietary changes, biological adaptations, and resulting health changes— was quite rapid.

Authorities agree on where and when domestication took place, based on the study of plant and animal remains found in archaeological sites. In addition, breakthroughs in plant and animal genetics provide new windows on the origins of domesticated species. That is, the domesticated descendants of formerly wild plants and formerly wild animals have undergone genetic changes compared with the ancestral forms. These genetic changes have been documented via breeding experiments and by the extraction and study of DNA. The changes were brought about by humans’ selecting food products that were beneficial to them. For exam- ple, they probably selected many plants with soft outer coatings and large seed yields. In a very real sense, humans practiced artificial selection, as opposed to natural selection. The resulting changes proved very deleterious for some of the species being domesticated. In wheat, the part holding all the edible parts is called the rachis, and at some point humans selected wheat with a hard rachis for storage and later consumption. This selection, in turn, selected for plants with a hard rachis. After many generations, the wheat was unable to reproduce itself because humans had selected for plants that could not do so without human intervention (annual planting manually).

domestication The process of converting wild animals or wild plants into forms that humans can care for and cultivate.

Neolithic The late Pleistocene/early Holocene culture, during which humans domesticated plants and animals.

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The American archaeologist Melinda Zeder regards one important outcome for humans as the increased security and predictability of food access. This was a mutualistic relationship with their plant and animal “partners” in that plants and animals experienced increased reproductive fitness and range expansion.

Authorities disagree on the cause for this dramatic, worldwide change in food acquisition. They are learning, however, that the change likely did not have only one cause. At least two factors probably brought about this agricultural revolution. First, the environment changed radically, going from cooler, drier, and highly variable during the later Pleistocene to warmer, wetter, and more stable during the Holocene (Figure  13.4). This abrupt environmental change brought about new conditions— local climates and local ecologies— suited to the domestication of plants and of animals. Second, almost everywhere agriculture developed, human population increased at the same time.

POPULATION PRESSURE Changes in climate and in ecology would not have resulted in plant and animal domestication, of course, without people. Almost everywhere agriculture devel- oped, strong archaeological evidence indicates that the number and size of living sites increased. For example, on the Georgia coast (see the opening discussion in chapter 1), the beginning of agriculture coincided with an increase in the number and especially the sizes of villages. All over the world, wherever agriculture came into being, this pattern suggests that as human population size grew, people likely needed more food than hunting and gathering could provide. This population pressure model suggests that humans had to develop a new strategy for feeding the ever- growing world population. Domestication, especially of plants, produced more food per unit area of land than had hunting and gathering— more people could be fed from the same amount of land. In addition, agriculture provided

Time (yBP)

Food Procurement from Wild Plants

Food Production from Wild Plants Dominant

Crop Production Dominant

Foraging, including use of fire

Farming,with larger-scale land

clearance and systematic cultivation

Incipient farming, with small-scale

clearance of vegetation and

minimal cultivation

Full-blown agriculture, based

largely or exclusively on domestic plants, with greater labor

input into cultivation

6,0009,00011,00015,000

Decreasing dependence on wild plants for food

Plant domestication: increasing dependence on domestic plants for food

Past Present

Evolution of Food Production from Plants FIGURE 13.3 Adoption of Agriculture As this chart illustrates, humans did not simply abandon foraging and adopt agriculture. Initially, they foraged for wild plants to supplement their farming of cultivated plants. Over time, they depended less on wild plants and more on domesticated plants.

The Agricultural Revolution: New Foods and New Adaptations | 355

food that could be stored for long periods. As an adaptive solution to population increase, domestication once again shows humans’ remarkable flexibility in new and challenging circumstances.

REGIONAL VARIATION Plant and animal domestication was not just a one- time event, first occurring in  one place and then spreading globally. Rather, domestication— in particu- lar, plant domestication— started in 11 independent regions around the world

(a)

(b)

Present

yBP

(c)

Warm

Cold 100,000 50,000 25,000 12,000 10,000 8,000 6,000 4,000 2,000

Last interglacial

Last Ice Age

Time of maximum cold and glaciation

Changes in climate and first plant domestication

Postglacial

FIGURE 13.4 Temperature Changes and Plant Domestication (a) Over the last 120,000 yBP, as this timeline shows, Earth’s temperature has fluctuated substantially. Around 11,000 yBP, a rapid warming trend created new habitats favorable for plant domestication. (b) The first grains were the wild ancestors of the domesticated varieties we know today. The wild ancestor of maize (right) is teosinte (left). (c) Domestication began with humans’ harvesting of wild plants using late Paleolithic technology, such as this tool, an antler handle with stone microblades inserted into it.

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(Figure  13.5). Out of these primary centers, the idea spread through a process of diffusion in some areas and through the movement of agricultural people in others. The process evolved slowly in some areas and fast in others. Eventually, every inhabitable continent except Australia saw the change. In some regions,

(a)

Yam (D. alata) 7,000 yBP? Banana 7,000 yBP Taro 7,000 yBP?

Peanut 8,500 yBP Manioc 8,000 yBP Chili pepper 6,000 yBP

African rice 2,000 yBP Pearl millet 3,000 yBP Sorghum 4,530 yBP

Pepo squash 6,000 yBP Sunflower 6,000 yBP Chenopod 4,000 yBP Marsh elder 4,000 yBP

Moschata squash 10,000 yBP Arrowroot 9,000 yBP Yam (Dioscorea trifida) 6,000 yBP Cotton 6,000 yBP Sweet potato 4,500 yBP Lima bean 6,500 yBP Leren 10,000 yBP

Rye 11,000 yBP? Emmer wheat 10,000 yBP Einkorn wheat 10,500 yBP Barley 10,000 yBP Fig 11,400 yBP?

Mung bean 4,500 yBP Horse grain 4,500 yBP Millet 4,500 yBP

Rice 8,000 yBP Foxnut 8,000 yBP

Potato 7,000 yBP? Quinoa 5,000 yBP

Broomcorn millet 8,000 yBP Foxtail millet 8,000 yBP

Pepo squash 10,000 yBP Maize 9,000–8,000 yBP Common bean 4,000 yBP

(b)

10,00011,00012,000 9,000 8,000 7,000 6,000 5,000 4,000 3,000 2,000 1,000

yBP

Southwest Asia

Central Mexico

South China

North China

South Central Andes

Eastern United States

Sub-Saharan Africa

FIGURE 13.5 Worldwide Plant Domestication (a) This map shows the 11 separate centers of plant domestication. At each location, different types of domesticated plants were cultivated, including maize in Central America, sunflowers in eastern North America, cotton in South America, millet and sorghum in Africa, wheat in the Middle East, and banana trees in New Guinea. (b) This chart illustrates the approximate times of plant and animal domestication in the major regions of the world.

The Agricultural Revolution: New Foods and New Adaptations | 357

newly domesticated plants replaced earlier ones. For example, in the American Midwest, native seed crops— goosefoot, sumpweed, and sunflowers— were farmed about 6,000–1,000  yBP.  Later, corn replaced these crops, probably owing to its greater productivity and potential for feeding more people than before.

Archaeological evidence and genetic studies of domesticated plants indicate that prior to becoming agricultural at the end of the Pleistocene, people living in southwestern Asia began to intensively harvest the grains of wheat’s and barley’s wild ancestors. These grains provided food for the growing populations that were beginning to live in small, settled communities for at least part of the year. For the other part of the year, people were likely out and about, hunting and gathering. Within 1,000 or so years following this combined practice of exploiting wild grains and foraging, sometime around 11,500 yBP, people began to manipulate plants’ growth cycles. This manipulation was probably based on the simple observation that some seeds falling to the ground grew into new plants. People figured out what circumstances were conducive to the plants’ growth, such as adequate water and protection from animals that might eat the plants. It would have been important for the people harvesting these plants to realize that if the seeds were placed in the ground, they would sprout new plants that could grow to full maturity. These mature plants could then be harvested, just as the plants’ wild ancestors were harvested generations before.

The archaeological record suggests that farming began in southeastern Tur- key by 10,500 yBP or so. By 8,000 yBP, early agricultural communities had sprung up across a vast swath extending from the eastern side of the Mediterranean across an arch- shaped zone of grasslands and open woodlands known as the Fertile Cres- cent (Figure  13.6). Once domestication developed, within a short time villages sprang up; some of these villages developed into cities. For example, the early

Levant Fertile Crescent

A N AT O L I A

A R A B I A N P E N I N S U L A

M E S O P O TA M I A

E G Y P T

Red S ea

Çatalhöyük

Jericho I S R A E L

T U R K E Y

Vegetation zones Forest Subtropical woodland Steppe grassland Desert grassland

Mediterranean Sea

Persian Gulf

Caspian Sea

Black Sea

Ali Kosh

Tepe Guran Ganj Dareh Asiab Char-I-Khar

Zawi Chemi and Shanidar

Karim Shahir Jarmo

Gird Banahilk Assoud

Abu Hureyra

Bouqras

Aswad Labweh

Tell es-SinnQal’at el Mudiq Ras Shamra

Çatalhöyük Cafer

Gritille

Tell Judaideh Amuq

Mureybit Hayaz Hüyük Cayönü

Hallum Çemi

Ramad Ain Ghazal

Gilgal Beisamoun

Natal Oren Netiv Hagdud

Abu Gosh Ashkalon JerichoHatoula

BeidhaRosh Horesha

Sarab Tepe Siahbid

Choga Mami Sabz

FIGURE 13.6 Southwestern Asia and the Fertile Crescent Southwestern Asia, especially the region known by anthropologists as the Fertile Crescent, has numerous archaeological sites that date between 11,500 and 8,000 yBP and contain evidence of early agriculture.

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agriculture- based settlements of Jericho and Çatalhöyük, in Israel and Turkey, respectively, grew from tiny villages consisting of a few huts to the first cities, containing several or more thousands of people living in close, cramped settings (Figure 13.7).

Plant domestication was nearly as early in China (millet at 10,000 yBP and rice at 8,000 yBP) as in southwestern Asia (Figure  13.8). By this time, the form of agriculture identified by archaeologists was well along in its development, so agriculture likely developed in China earlier than that, perhaps by several thousand years. Other early domesticated plants are from Mexico (bottle gourds, 10,000 yBP; corn, 9,000 yBP), New Guinea (taro and banana trees, 7,000 yBP), eastern North America (squash, sunflowers, and goosefoot, 6,000 yBP), South America (potatoes, sweet potatoes, and manioc, 5,250 yBP), and Africa south of the Sahara Desert (sorghum and yams, 4,500 yBP).

Like most other technological innovations, agriculture spread by diffusion out of the primary centers, usually for very long distances. Corn, for example, spread from its primary center in Mexico (probably in the lowland tropics) to the Ameri- can Southwest. Eventually, corn agriculture reached North America’s Atlantic coast about 1,000 yBP. The spread occurred not through people carrying corn but through people describing their agricultural successes to neighbors, those neighbors telling their neighbors, and so forth, until the idea spread for  thousands of miles over a series of generations. For some areas of North America, the adoption and intensive use of corn occurred very rapidly, perhaps within a few generations.

Another important area of the world where anthropologists have studied the origins and diffusion of agriculture consists of both far western Asia and Europe. From southwestern Asia, the domestication of wheat and of barley spread to

(b)

FIGURE 13.7 Çatalhöyük (a) Çatalhöyük Houses, Turkey, Konya. (b) Skeletal remains of an infant adorned with stone and bone beads found at Çatalhöyük.

(a)

The Agricultural Revolution: New Foods and New Adaptations | 359

Greece by 8,000 yBP and then throughout Europe. As in North America, agricul- ture spread mostly through cultural contact and the exchange of knowledge— the idea of agriculture— rather than the movement of people. Some people moved, but (as discussed in chapter 4) the movement of early farmers was not widespread enough to account for the genetic diversity among humans in Europe today.

Animals were domesticated around the world, beginning with dogs at about 15,000 yBP.  Some 7,000–8,000 years later, goats, sheep, cattle, and pigs were domesticated. These animals were important in Asia and later Europe, but domes- ticated plants were far more fundamental to the growing human populations’ survival.

SURVIVAL AND GROWTH The importance of domestication for human evolutionary history cannot be over- estimated. Domestication fueled humans’ remarkable population growth in the Holocene, and it formed the foundation for the rise of complex societies, cities, and increasingly sophisticated technology. Archaeologists are learning that domes- ticated plants served as both a food staple and a source of drink, especially alcoholic drink. In China, for example, chemical analysis of residue inside ceramic vessels shows that perhaps as early as 8,000 yBP grapes and rice were fermented for wine.

The arrival of European explorers and colonists in the Americas had an enor- mous impact on the kinds of domesticated plants consumed by world populations. That is, beginning with Columbus’s voyages, different plants were transported and grown throughout the world. Corn, for example, was taken back to Europe by early explorers. By the middle of the 1500s, its use as a food had spread widely, and it had become an important part of diets, especially in Africa.

Today, domesticated plants are crucial for sustaining human populations. Two- thirds of calorie and protein intake comes from the key cereal grains domesticated

FIGURE 13.8 Rice There are more than 20 varieties of wild rice and two types of domesticated rice, the first of which was domesticated in southern Asia approximately 8,000 yBP. The second variety of domesticated rice was established in western Africa between 1500 BC and 800 BC.

360 | CHAPTER 13 Our Last 10,000 Years: Agriculture, Population, Biology

in the earlier Holocene, especially wheat, barley, corn, and rice. Rice has fed more people since its domestication than any other plant. It now accounts for half the food consumed by 1.7 billion people in the world whose diets include rice and more than 20% of all calories consumed by humans today. Rice and these other cereal grains are now aptly called superfoods.

Agriculture: An Adaptive Trade- Off Most people assume that the adoption of agriculture was a highly positive devel- opment in human history. Indeed, agriculture’s potential for supporting large numbers of people living in a concentrated setting and for creating surplus and, thus, wealth for some laid the foundation for the great civilizations of the past— such as in China, South America, and Mexico— and those of today. Beginning with the earliest cities in the early Holocene, no complex society, anywhere in the world, would have been possible without an agricultural economic base. Writing, art, business, technology, and just about every other feature of modern life came about because of agriculture.

POPULATION GROWTH The rise of complex societies, of civilizations, and of technologically sophisticated ways to acquire both food and other resources also brought about a number of profound, and largely negative, consequences for humankind, however. Probably the single most visible characteristic associated with the shift from foraging to farming is the increase in population size. Called the Neolithic demographic tran- sition, this shift from low birthrate to high birthrate resulted in a rapid increase in the world’s population. The greater number of births was brought about by a reduced period of weaning. The availability of grains cooked into soft mushes and fed to infants made it possible to wean infants earlier in their lives. With earlier weaning, spacing between births reduced, and mothers were able to produce more offspring.

The first major demographic transition in human evolution spurred a remark- able increase in human population around the globe. This pattern continues to the present day and continues to place increased demands on the environment.

The growth of human population in the last 10,000 years is staggering. The world population around 10,000 yBP was probably no more than 2  million or 3 million people. By 2,000 yBP, population had likely increased to 250 million or 300 million. By AD 1850, population had increased to 1 billion, and today it is over 7 billion (Figure 13.9). Increasing population leads to competition for resources. As towns and cities began to compete for increasingly limited resources (e.g., arable land for crops), organized warfare developed. Interpersonal violence has a long his- tory in human evolution, going back at least to Neandertals, in the late Pleistocene. But the level of violence in pre- Holocene hominins was nothing compared with the organized warfare of early civilizations in southwest Asia, Central America, and South America or with the medieval wars in Europe, where up to thousands of people were killed. As the study of human remains shows, organized violence has likely been present in small societies as well.

superfoods Cereal grains, such as rice, corn, and wheat, that make up a substan- tial portion of the human population’s diet today.

Agriculture: An Adaptive Trade- Off | 361

ENVIRONMENTAL DEGRADATION The consequences of environmental degradation, like those of extreme popula- tion growth, are well documented by historians and ecologists for recent human history. This degradation actually has a much more ancient origin, beginning with plant and animal domestication around 10,000 yBP. For much of the region surrounding the Mediterranean, especially the Levant, landscapes have been sub- stantially transformed and degraded. Dense settlement based on agrarian econo- mies has contributed to soil erosion, making it increasingly difficult to produce food. Around 6000 BC, a number of large towns in the eastern Mediterranean were abandoned, probably due to a period of climate drying. Contributing to the abandonment was human activity, however, such as overgrazing with goats, which resulted in damaging erosion. Moreover, the amount of fuel, especially wood, needed to support the community resulted in the destruction of native vegetation and the desiccation of landscapes.

Likewise, the recent collapse of coastal ecosystems worldwide clearly had its start in overfishing— especially in that of large vertebrates (e.g., whales) and of shellfish— beginning thousands of years ago. Simply, the dramatically altered eco- systems worldwide have caused biodiversity to crash, a development that appears to be accelerating. The American anthropologist Jeffrey McKee argues that one primary force behind the reduction in biodiversity is expanding human population size. He predicts that if left unchecked, the population will outstrip the arable land available to produce the plants and animals consumed by humans. Thus, the increased food supply that resulted from the agricultural revolution in the Holo- cene could, in the not- too- distant future, lead to a food crisis.

Po pu

la tio

n (m

illi on

s)

yBP

10,000

1,000

10

100

20,000 18,000 16,000 14,000 12,000 10,000 8,000 6,000 4,000 2,000 Present 0

At the end of the Paleolithic, population growth is minimal: .0015 percent per year.

Population growth increases rapidly: .01 percent per year

Agricultural Revolution

Modern-day rates continue to rise: Present Nineteenth century Eighteenth century

2.0% .6% .3%

FIGURE 13.9 World Population Size This graph shows the trend in population size on a global scale. Until 10,000 yBP and the advent of agriculture, population remained constant, numbering less than 10 million people. After the agricultural revolution, however, population skyrocketed.

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How Did Agriculture Affect Human Biology? A misperception shared by the public and anthropologists is that with the appear- ance of essentially modern Homo sapiens in the late Pleistocene, human biological evolution ground to a halt. That is, many think that humans stopped evolving biologically once they became modern, in the Upper Paleolithic. Unlike recent humans’ cultural evolution (for example, increasing use of technology, develop- ment of the arts), humans’ biological evolution since the closing days of the Pleis- tocene has gone largely unrecognized.

In the remainder of this chapter, we will examine the human biological changes that accompanied the agricultural revolution— changes linked directly or indirectly to the fundamental change, discussed above, in how humans have acquired resources, especially food. At the end of the chapter, we will revisit the question of why humans made this remarkable transition. Some very compelling reasons exist to believe that agriculture has contributed to H. sapiens’ evolution- ary success, at least as measured by humankind’s remarkable population increase since then.

The Good and Bad of Agriculture

Agriculture had many advantages for human adaptation. But it also had drawbacks.

Advantages

Support for larger numbers of people

Creation of surplus food

Long- term food storage, especially of grains

Disadvantages

Increased demands on the environment (land degradation)

Pollution

Conflict between populations competing for the same lands

Loss of wild species through overhunting

Decline of biodiversity

Health costs and quality- of- life implications

C O N C E P T C H E C K !

How Did Agriculture Affect Human Biology? | 363

THE CHANGING FACE OF HUMANITY As discussed at the beginning of this chapter, the foods we eat and the manner in which they are prepared tremendously influence our physical appearance. The relationship between food and morphology is well illustrated by the major anatomical changes throughout human evolution. As discussed in chapter  10, the massiveness of the late australopithecines’ face and jaws was clearly linked to the hard foods those hominins ate, such as seeds. Generating the power to chew hard foods required large masticatory muscles (and their bony support). Thus, the well- developed sagittal crests of some later australopithecines— such as Australo- pithecus aethiopicus— are adaptations related to chewing. Over the course of human evolution following the australopithecines, the face and jaws have continuously reduced in size and robusticity, reflecting a general decrease in the demand placed on  the  jaws and teeth as culture became increasingly complex and foodstuffs changed.

The reduction in size of the face and jaws is a general theme throughout human evolution, including during the Holocene and with the dietary adoption of domes- ticated plants. For example, in studying skulls from England that dated to the last couple of thousand years, Sir Arthur Keith documented a clear reduction in the size of the face and jaws. He believed that this reduction came about from eating soft foods, such as cooked cereal grains. Other physical anthropologists have noted similar changes in many other places of the world. In Sudan’s Nile valley— the region known as Nubia— hunter– gatherers living during the time immediately preceding agriculture had long and narrow skulls, whereas their descendants had short and wide skulls. My own work on the Atlantic coast of the southeastern United States shows similar trends.

TWO HYPOTHESES To explain why the human skull changed shape in Nubia during the last 10,000 yBP, anthropologists in the 1800s and most of the 1900s offered an explanation based on old concepts of race (see chapter 5 for discussion of race). In Nubia, for example, they believed that the change occurred because short- headed people invaded territory occupied by long- headed people. These ear- lier anthropologists viewed head shape as unchanging and essentially a diagnostic racial marker. They were correct that humans living in specific areas of the globe have physical characteristics in common. However, since then, anthropologists have learned that human facial and skull forms are highly plastic, as are other parts of the skeleton.

The American physical anthropologists David Carlson and Dennis Van Gerven have offered an alternative hypothesis, which explains differences in head shape in Nubia but can be applied globally. Their masticatory- functional hypothesis states that change in skull form represents a response to decreased demands on the chewing muscles— temporalis and masseter— as people shifted from eating hard- textured wild foods to eating soft- textured agricultural foods, such as mil- let. (Figure 13.10 lays out the hypothetical steps of this process.) To be sure, the millet grains eaten by ancient Nubians were not especially soft in their uncooked form. However, at that time, a critical change occurred in human technological evolution: the invention of pottery for storing food or cooking it. By cooking, I mean not a simple warm- up but cooking for hours until foods become soft mushes, rather easily chewed. The chewing of these mushes would have required far less powerful muscles. Because light use of muscle produces limited bone growth, the later Nubians, eating soft foods, had reduced faces.

masticatory- functional hypothesis The hypothesis that craniofacial shape change during the Holocene was related to the consumption of softer foods.

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Carlson and Van Gerven’s explanation for much of the change in human head shape during the Holocene is strongly supported by evidence from living species, including humans. For example, experimental research shows that primates fed soft foods have a relatively shorter skull with a smaller face and jaws than do pri- mates fed hard foods.

(a) (b) Taller

Shorter from front to back

Foraging to farming

Reduced toughness of food

Altered chewing

Reduced masticatory muscle activity

Response of cranial vault and reduced amount of bone

Shorter, wider, more globular vault with less-projecting

face and less room for teeth (increased malocclusion)

Altered craniofacial growth

Reduced size and configuration of

masticatory muscles

Reduced facial growth

Decreased stimulation of bone growth in

face and jaws

Reduced robusticity of face and jaws

Reduced face and jaws

FIGURE 13.10 Craniofacial Changes (a) The overall reduction in cranial size over the course of human evolution can be seen in Nubians’ skeletal remains. Here, the dashed line indicates the craniofacial changes that have occurred between the Mesolithic foragers and the later agriculturalists. The skull has become shorter from front to back and, simultaneously, has gotten taller. (b) As presented in this flowchart, the Nubians’ craniofacial changes resulted from alteration in diet associated with eating softer foods. In changing their diet, the Nubians were placing less demand on their chewing muscles. As a result, the associated bones changed; facial bones and jaws became smaller, and the cranial vault became rounder. The reduction in jaw size left less room for teeth, and the increased crowding resulted in malocclusion.

How Did Agriculture Affect Human Biology? | 365

IMPLICATIONS FOR TEETH These changes in skull size and skull shape had enormous implications for our teeth. Today, the high numbers of people with orthodontic problems— malocclusions ranging from simple overbite to very poorly aligned teeth— contrast sharply with the few such problems found in ancient hominins and throughout much of prehistory. The American physical anthropolo- gist James Calcagno has noted a number of exceptions, which may have influenced the size of our teeth; but malocclusions are rare prior to the modern era.

Why, then, do so many people around the globe have dental malocclusions? As with general skull shape, food plays an especially important role. Animals fed soft- textured foods develop far more occlusal abnormalities, such as crooked teeth, misaligned jaws, and chewing problems, than do animals fed hard- textured foods. The study of many thousands of skulls has shown that tooth size and jaw size have reduced in the last 10,000 yBP but at different paces. Bone is greatly subject to environmental factors, so a child fed softer foods than his or her parents ate will have appreciably reduced jaws. By contrast, teeth are controlled much more by genes, so over the course of evolution teeth have reduced far less than jaws have. Simply, the greater reduction of the bones supporting the teeth has led to greater crowding of teeth. This disharmony underscores the complex nature of our biol- ogy, which involves an interplay between intrinsic (genetic) factors and extrinsic (environmental) factors.

Malocclusion is a clearly negative result of humans’ eating soft foods. A positive result is that our teeth have very little wear since eating soft foods places less stress on the chewing surfaces.

Soft Food and Biological Change

The shift to agriculture and the eating of softer foods resulted in biological changes to the face, jaws, and teeth of modern people. Although not universal, some tendencies characterized the skulls and teeth of hunter– gatherers and of agriculturalists.

Hunter– Gatherers Agriculturalists

Long cranial vault Short skull

Large, robust mandible Small, gracile mandible

Large teeth Small teeth

Few malocclusions Many malocclusions

Much tooth wear Little tooth wear

C O N C E P T C H E C K !

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BUILDING A NEW PHYSIQUE: AGRICULTURE’S CHANGES TO WORKLOAD/ACTIVITY One major debate in anthropology concerns the extent to which the agricultural revolution improved the quality of human life, including workload. Did people have to work more or work less to acquire food through agriculture rather than through hunting and gathering? The eminent American archaeologist Robert Braidwood characterized the lifestyle of a typical hunter– gatherer as “a savage’s existence, and a very tough one . . .  following animals just to kill them to eat, or moving from one berry patch to another.” About the time Braidwood was writing this, in the 1960s, the Canadian cultural anthropologist Richard Lee and the American physical anthropologist Irven DeVore organized what turned out to be one of the most important conferences in the modern era of anthropology. They invited experts in different areas of anthropology from around the globe to determine the quality of life of hunter– gatherers, ancient and modern. A key component in assessing the quality of life was workload. If Braidwood was correct, hunter– gatherers had to work very hard, basically spending all waking hours in the food quest, getting food wherever and whenever possible. However, Lee and others reported that hunter– gatherers might not have had it all that bad when it came to workload. In fact, in his research on the Ju/’hoansi (!Kung) of southern Africa, Lee found that these hunter– gatherers had a great deal of leisure time (Figure 13.11).

Lee’s work in the 1960s set in motion the work of a whole generation of anthro- pologists, who addressed both his observations and his hypotheses. Science works this way, of course— old hypotheses are often rejected as new observations are made, and new observations generate new hypotheses. Indeed, the subsequent work showed that hunter– gatherers have quite diverse workloads. Anthropologists realized that workload depended highly on the local ecology and the kinds of foods being eaten. For example, in how they acquire plants and animals, people living in the tropics differ greatly from people living in the arctic.

FIGURE 13.11 Leisure Time While foragers, such as this band of !Kung, must spend many hours searching for and hunting for food, their work does not preclude them from relaxing for periods of time. However, studies of numerous foraging groups have shown a great deal of variation in the workloads and amounts of leisure time of hunter– gatherers.

How Did Agriculture Affect Human Biology? | 367

How do scientists know how hard or how easy a lifestyle was? Obviously, they cannot observe the behavior of dead people. Physical anthropology offers a way to reconstruct past behavior. Biomechanics, an area of great interest to physical anthropologists, provides enormous insight into the evolution of the body below the neck in relation to workload and to other activity. As with the bones of the face and of the jaws, the bones of the postcranial skeleton are highly plastic during the years of growth and of development, all the way through adulthood. The general shape and size of bones— the femur, in the leg, for example, or the humerus, in the arm— are determined by a person’s genes. However, the finer details are subject to work and activity. Highly physically active people’s bones tend to be larger and more developed than those of not so physically active people.

Borrowing from how engineers measure the strength of building materials— such as the “I” beam used in the construction of a bridge or of a house— physical anthropologists have developed a means for assessing the robusticity of bone cross sections. Based on the simple premise that material placed farther away from an axis running down the center of the bone is stronger than material placed closest to the axis (Figure  13.12), it has become possible to look at the degree of bone development and determine by empirical means how bone strength has changed over the course of human evolution to the present. Bone comparisons— from hunter– gatherers’ to later agriculturalists’ to modern peoples’—show a remarkable decline in size.

Physical anthropologists’ studies have shown that populations respond differ- ently to the adoption of an agricultural lifestyle. For example, in our research on skeletons from the Atlantic coast of Georgia and of Florida, Christopher Ruff and I have found that agricultural populations’ bones became smaller, which we inter- pret to mean that those populations worked less hard than their hunter– gatherer

FemurI-beam

FIGURE 13.12 Cross- Sectional Geometry Using engineering principles, physical anthropologists can gain insight into activity patterns by examining the cross sections of long bones, such as the femur and the humerus. The shapes of long bones, like those of I- beams (building materials used for structural support), maximize both strength and ability to resist bending, by distributing mass away from the center of the section.

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ancestors (Figure 13.13). We have also found a decrease in osteoarthritis, a dis- order of the skeletal joints that results from excessive stresses on places where the bones articulate (Figure 13.14). In contrast, the American physical anthropologist Patricia Bridges has discovered a clear increase in bone size in Alabama popula- tions. Which is correct? Did workload increase or decrease? Actually, both are cor- rect. Coastal settings involved very different means of food production compared to noncoastal settings, reflecting the regions’ differences in terrain and in other kinds of nonagricultural foods. On the Georgia coast, people collected seafood in addition to practicing agriculture. In noncoastal Alabama, people supplemented agriculture with terrestrial foods, such as deer.

In general, the reduction in human bone size represents an overall evolutionary trend in the last 20,000 yBP. Thanks to the increasing tool complexity and greater cultural sophistication, the biological changes came about as physical strength was replaced with technology. Ruff’s studies of human remains from around the world

Hunter–gatherer Bone cross sections

Agriculturalist Bone cross sections

Humerus

Femur

FIGURE 13.13 Activity Pattern Comparison Physical anthropologists compared cross sections of the femurs and humeri from prehistoric hunter– gatherers and agriculturalists living on the southeastern US Atlantic coast (modern states of Georgia and Florida; see the opening paragraphs of chapter 1) to determine whether significant changes in the native populations’ activity patterns had occurred with the shift to farming. The larger sections in the hunter– gatherers indicate greater bone strength than in their agricultural descendants. The reduced bone strength in the mission- era Indians reflects less mechanical stress in the prehistoric farmers in this setting.

osteoarthritis Degenerative changes of the joints caused by a variety of factors, especially physical activity and mechani- cal stress.

How Did Agriculture Affect Human Biology? | 369

indicate that the reduced bone mass reflects about a 10% decrease in body weight during this period.

HEALTH AND THE AGRICULTURAL REVOLUTION POPULATION CROWDING AND INFECTIOUS DISEASE The population increase during the Holocene, discussed extensively above, was linked with agri- culture and increased food production. As the population increased, communities grew more committed to raising crops and became more sedentary, living in one place the entire year. Before then, the smaller number of people had moved around at least on a seasonal basis. The increase in size and density of the population, especially when the population remained in place, had enormous, negative effects on people’s health. In short, humans began to live in conditions crowded and unsanitary enough to support pathogens.

Normal joints and bones

Cervical spine

Hand

Lumbar spine

Hip

Knee

(b)

(a)

FIGURE 13.14 Osteoarthritis (a) Degenerative joint disease, or osteoarthritis, can occur in a variety of sites throughout the body, commonly in the vertebrae, hips, knees, and hands. (b) The lumbar vertebrae, toward the base of the spine, are often among the first bones affected by osteoarthritis. This condition results from stress on the back due to lifting and carrying, and its presence on a skeleton indicates the repetition of physically demanding activity.

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Consider the overcrowded cities around the globe today. In the urban slums of Bombay, India, or Rio de Janeiro, Brazil, or La Paz, Bolivia, or even within devel- oped nations where sanitation is carefully regulated and monitored, the crowding sets up conditions for increased interpersonal contact and the spread of infectious microorganisms and of viruses.

During the Holocene, especially in agricultural settings, crowding seems to have produced illnesses and injuries. Any kind of injury to the outer surface of bone can cause a periosteal reaction, or bone buildup, which is sometimes com- bined with an abnormal expansion of a bone’s diameter. The reaction is caused by localized infection, such as from the so- called staph bacteria, Staphylococcus aureas. The infection essentially stimulates new bone growth, hence the swollen appear- ance (Figure 13.15). Most periosteal reactions are nonspecific, so anthropologists cannot tell exactly what caused them. Anthropologists find, however, a general increase in periosteal reactions on the limb bones of skeletons from crowded set- tings in the Holocene. Such reactions are practically nonexistent in human groups predating that time.

Some infections identified on bones from Holocene populations have a specific pattern that suggests the diseases that caused them. In the American Midwest and Southeast, for example, tibias are swollen and bowed, while crania have dis- tinctive cavitations (Figure 13.16). Both kinds of bone deformation are caused by a group of diseases called treponematoses, which include venereal syphilis, non- venereal (also called endemic) syphilis, and yaws. Anthropologists, historians, and others debate the origin of venereal syphilis, some blaming native populations, some blaming Christopher Columbus and his ship crews, and some arguing for the appearance of a wholly new disease sometime following the initial European explorations of the New World. However, the pattern of bone changes in the New World prior to the late 1400s suggests a nonvenereal syphilis, one passed not by sexual contact but by casual contact, such as by a mother holding her child.

Labor, Lifestyle, and Adaptation in the Skeleton

The human skeleton responds to activity, reflecting the person’s lifestyle. Hunter– gatherers’ skeletons and agriculturalists’ skeletons vary in patterns that reveal different levels of activity, including that of workload; but hunter– gatherers’ skeletons tend to show higher levels.

Hunter– Gatherers Agriculturalists

Bones with higher second moments of area

Bones with lower second moments of area

Larger, more robust bones Smaller, less robust bones

More osteoarthritis Less osteoarthritis

C O N C E P T C H E C K !

FIGURE 13.15 Periosteal Reaction The tibia is a common site of periosteal reactions. Here, the pathological tibia from St. Catherines Island, Georgia, on the left, has an irregular surface because new bone has been deposited unevenly. The normal tibia, on the right, has a smooth surface, free of any reactive bone.

periosteal reaction Inflammatory response of a bone’s outer covering due to bacte- rial infection or to trauma.

treponematoses A group of related diseases (venereal syphilis, yaws, endemic syphilis) caused by the bacteria Treponema, which causes pathological changes most often to the cranium and tibiae.

How Did Agriculture Affect Human Biology? | 371

Many other infectious diseases likely affected Holocene populations worldwide. The skeletal indicators of tuberculosis, for example, are widespread in parts of the New World, of the Old World, and of Australia, well before the time of European exploration. For much of the mid- twentieth century, many medical practitioners thought this microbial infection had been conquered; but today, 2–3 million peo- ple die annually from the disease. Other modern diseases made possible by over- crowding include, but are not limited to, measles, mumps, cholera, smallpox, and influenza. Some of these diseases have an Old World origin, but the New World was hardly a disease- free paradise before their introduction. Bioarchaeologists have documented many poor health conditions and evidence of physiological stress before the Europeans’ arrival in North America and South America.

THE CONSEQUENCES OF DECLINING NUTRITION: TOOTH DECAY All domesticated plants have nutritional drawbacks. Because they are carbohydrates, they promote dental caries, commonly known as tooth decay or “cavities” (Figure 13.17). Caries is a process in which the natural bacteria in your mouth— common culprits are Streptococcus mutans and Lactobacillus acidophilus— digest the carbohydrates there. One end product of this digestive process is lactic acid, which literally dissolves teeth’s enamel. In industrial societies today, dentists stabilize caries by removing diseased parts of teeth and filling the cavities with composite material to stop the spread of decay. In the ancient world, dentistry was mostly nonexistent, and cavities grew until the teeth fell out or, in some instances, people with cavities died from secondary infections.

Different domesticated plants promote tooth decay at varying rates. Rice does not seem to cause it to the same extent as other domesticated plants. Corn causes it considerably. Once post– AD 800 populations in eastern North America had adopted corn agriculture, the frequency of their dental caries rose dramatically (Figure 13.18).

NUTRITIONAL CONSEQUENCES DUE TO MISSING NUTRIENTS: REDUCED GROWTH AND ABNORMAL DEVELOPMENT The popular and the academic lit- eratures suggest that agriculture has improved humans’ nutrition. This conclusion

FIGURE 13.16 Treponematosis The lesions on this cranium indicate that this individual from the prehistoric southeastern United States suffered from treponematosis. The undulating surface of the skull shows active and healed lesions caused by the disease’s long, slow progression.

dental caries A disease process that creates demineralized areas in dental tis- sues, leading to cavities; demineralization is caused by acids produced by bacteria that metabolize carbohydrates in dental plaque.

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makes sense given the huge worldwide investment in agriculture, even today. How- ever, the assessment of superfoods’ nutritional content argues otherwise.

All agricultural settings have the potential to impede normal growth and devel- opment because of their nutritional limitation. Dietary reconstructions of past societies by archaeologists and studies of living agrarian populations in different settings indicate that agriculturalists’ diets tend to overemphasize one plant or a couple of them, such as rice in Asia, wheat in Europe and temperate Asia, corn in the Americas, and millet or sorghum in Africa. Thus, many groups, especially in the later Holocene, received poor nutrition from an increasingly narrow range of foods. A well- balanced diet, as your parents and teachers have told you time and again, involves variety, from all the food groups.

Domesticated plants have nutritional value, of course, but they also present a range of negative nutritional consequences. For example, corn is deficient in the amino acids lysine, isoleucine, and tryptophan; and a person who does not receive the right amount of even one amino acid will neither grow normally nor develop properly. In addition, vitamin B3 (niacin) in corn is bound chemically, and corn contains phytate, a chemical that binds with iron and hampers the body’s iron absorption. Grains such as millet and wheat contain very little iron. Rice is defi- cient in protein and thus inhibits vitamin A activity.

Numerous societies worldwide have developed strategies for improving these foods’ nutritional content. For example, corn- dependent populations commonly treat corn with alkali, a weak solution of lye. This treatment increases the ratios

(a)

(b)

(c)

FIGURE 13.17 Dental Caries (a) Cavities are more common in individuals with carbohydrate- rich diets. As a result of the digestion of carbohydrates, carious lesions form as the teeth’s enamel deteriorates. In extreme cases, the teeth’s pulp can be affected. (b) This cross section of a tooth affected by dental caries shows two common locations of cavities: the occlusal, or chewing, surface (black arrows) and between successive teeth (white arrow). (c) Lactobacillus is one of the two main bacteria that cause dental caries.

ameloblasts Cells that make tooth enamel.

iron deficiency anemia A condition in which the blood has insufficient iron; may be caused by diet, poor iron absorption, par- asitic infection, and severe blood loss.

FIGURE 13.18 Changes in Oral Health This chart shows temporal changes in dental caries in eastern North America. During the Archaic, Early Woodland, and Middle Woodland periods, which predate AD 800, the region’s native inhabitants were hunter– gatherers. During the Late Woodland, Mississippian, and Contact periods, which postdate AD 1000, the adoption of agriculture caused a large increase in dental caries.

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How Did Agriculture Affect Human Biology? | 373

of amino acids, improving the quality of the protein. Such treatments cannot, however, make up for the negative consequences of dietary overreliance on these plants.

One of the most obvious ways of assessing the impact of nutritional change in the Holocene is by looking at the growth of bones and of teeth. Like any other body tissues, bones and teeth grow to their full genetic potential only if they receive proper nutrition. Anthropologists are able to identify a few indicators of growth stress in skeletal and dental records from fossils, but these indicators are generally nonspecific— that is, they are not linked to a precise cause (for example, a particular vitamin that the person was deficient in). These stress indicators are also related to multiple factors that may or may not include nutrition. Nonnutritional factors often include infection or infectious disease. As studies of living populations have shown, nutrition and infection have a synergistic relationship: poor nutrition wors- ens the infection, and vice versa; essential nutrition is used to fight the infection and is taken away from the growth process. Despite such complications, anthro- pologists have found these indicators to be very informative about the history of stress both in individuals and in populations.

Deficiencies in dental enamel are one of the most important nonspecific stress indicators. Typically, the deficiencies appear as lines, pits, or grooves, any of which occur when the cells responsible for enamel production (called ameloblasts) are disrupted. Consequently, when the disturbance ends (the illness or the infection is over) a defect, or hypoplasia, is left (Figure  13.19). Defects of this kind are commonplace in earlier humans’ teeth— indeed, researchers have found them in australopithecines— but they are rare through most of human evolution. Some hunter– gatherer populations have high frequencies, but hypoplasias became rel- atively common in Holocene populations. The high frequency in agriculturalists around the world was caused by two factors: decline in nutritional quality and increase in infectious disease. (Other dental defects, visible in teeth only with a microscope, reflect very short- term stress episodes, lasting several hours to several days. Virtually everyone has microscopic defects in the deciduous teeth, created as a result of birth stress.)

NUTRITIONAL CONSEQUENCES OF IRON DEFICIENCY Other markers of stress and of deprivation in agricultural populations can be linked to specific causes. Iron deficiency anemia, a problem that plagues many millions of people around the globe, results when the body receives limited iron. Iron is necessary for many body functions and is an essential element in hemoglobin, serving in the transport of oxygen to the body tissues. Iron— specifically, heme iron— enters the body easily through meat- eating since meat does not require processing in the stomach and since the amino acids from the digestion of meat promote iron absorption. Iron from plants— nonheme iron— is not as readily available because various substances in plants inhibit iron absorption (see the above discussion on corn). Citric acid found in various fruits, however, may promote iron absorption.

Some authorities believe that iron deficiency is rarely caused by dietary stress and is more often related to nondietary factors. Parasitic infections, for example, are a primary cause of iron deficiency anemia in many regions of the globe. One such infection, hookworm disease, is caused when someone inhales or ingests hookworm larvae. The worm (Ancylostoma duodenale, Necator americanus) extracts blood from its human host by using the sharp teethlike structures in its head to latch itself to the intestinal wall (Figure  13.20). When several hundred or more of these worms are present, severe blood loss— and therefore anemia— can result.

FIGURE 13.19 Enamel Hypoplasias These defects reflect stress episodes that occurred during tooth development. Individuals with multiple hypoplasias on each tooth underwent several stress episodes.

FIGURE 13.20 Hookworm Parasites, such as this hookworm, can cause iron deficiency. Today, hookworms are commonly found in subtropical regions of North Africa, India, and elsewhere.

heme iron Iron— found in red meat, fish, and poultry— that the body absorbs efficiently.

nonheme iron Iron— found in lentils and beans— that is less efficiently absorbed by the body than is heme iron.

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Abundant evidence of anemia exists among skeletons in numerous settings worldwide. In response to anemia, red blood cells increase in production, poten- tially leading to porotic hyperostosis in skulls and cribra orbitalia in eye orbits (Figure 13.21). These abnormalities were quite rare before the Holocene but then suddenly appeared, especially in agricultural groups.

(a) (b)

FIGURE 13.21 Porotic Hyperostosis and Cribra Orbitalia (a) In porotic hyperostosis, which results from anemia, the cranial bones become porous as the marrow cavities expand from the increased production of red blood cells. (b) Anemia can also give the eye orbits a porous appearance, called cribra orbitalia.

Health Costs of Agriculture

Due to population increase, crowding, and poor nutrition, human populations’ health declined in many settings globally.

Health Indicator Hunter– Gatherers Agriculturalists

Infection (periosteal reactions) Low High

Dental caries Low High

Child growth and development Normal Reduced

Enamel defects (hypoplasias, microdefects)

Low High

Iron deficiency (porotic hyperostosis, cribra orbitalia)

Low High

Adult height Normal Reduced

C O N C E P T C H E C K !

porotic hyperostosis Expansion and porosity of cranial bones due to anemia caused by an iron- deficient diet, parasitic infection, or genetic disease.

cribra orbitalia Porosity in the eye orbits due to anemia caused by an iron- deficient diet, parasitic infection, or genetic disease.

The Past Is Our Future | 375

NUTRITIONAL CONSEQUENCES: HEIGHTS ON THE DECLINE In many regions where farming was adopted, adult heights declined appreciably. That peo- ple simply stopped growing as tall has been documented in western Europe, the eastern Mediterranean, Nubia, southern Asia, the Ohio River valley, and central Illinois. The Peruvian physical anthropologist Lourdes Márquez and Mexican physical anthropologist Andrés del Ángel have found a general decline in height among the Maya of the first millennium AD, a time in which this ancient civiliza- tion experienced a deterioration in environment and in living circumstances. Thus, for some groups shorter height might have been the biological result of adopting agriculture, but for other groups it might have been an adaptation to reduced resources since smaller bodies require less food. However, all the human popu- lations whose height decreased due to stress also experienced elevated infectious disease loads, anemia, malnutrition, and other factors indicating that a smaller body does not confer an adaptive advantage. These people were smaller but not healthier.

If It Is So Bad for You, Why Farm? This question brings us back to some points about evolution raised in earlier chap- ters. Namely, the key components of evolution are survival to the reproductive years and production of offspring. One documented fact about the Holocene is that during this time human fertility greatly increased. That women gave birth to more babies was likely made possible by the reduced spacing out of births in agricultural groups. Simply, because women were settled and not spending time moving about the landscape, they could bear children more frequently. Therefore, a population with a reduced quality of life might still have very high fertility. This combination, of course, is present through much of the developing world, such as in Peru, Bangladesh, Mexico, Thailand, and many African countries.

We have seen the evidence— a huge record— showing that the adoption of agri- culture resulted in the development and spread of infectious disease and a reduc- tion in health generally. Agriculture’s positive side is that it provides both more calories per unit of land and the resources for population increase. And evolution dictates that organisms, including humans, engage in behaviors that increase the potential for and outcome of reproduction.

The Past Is Our Future We can learn a lot about our future by paying attention to what has happened in the past. The global state of human health has been a driving force in our evolution and will continue to drive our future evolution.

This chapter has emphasized humans’ foraging- to- farming transition and especially the domestication of plants, changes that laid the foundation for our continued population increase (today, there are more than 7 billion humans), the concentration of populations in large urban agglomerations (more than 50% of the 7 billion live in cities), and the shift in many regions of the globe from highly varied diets to diets focused on saturated fat and carbohydrates. This dietary shift

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is resulting in an epidemic of obesity. Obesity, in turn, along with humans’ increas- ingly sedentary lifestyles, is an important factor in explaining the rising incidence of degenerative conditions including osteoporosis, cardiovascular disease, respira- tory disease, diabetes, and depression.

We also face the threat of global warming and global environmental change in general. This alarming development is the result of “greenhouse gases” (carbon dioxide and methane, especially) brought about by the burning of fossil fuels, and it has been exacerbated by the increasing lack of vegetation and natural land cover. Concentrations of elevated heat, produced from roads and rooftops and other heat- storing materials, are producing abnormally high temperatures. These circumstances, in addition to putting an unprecedented strain on food resources, are yielding what the United Nations has recently called a global “silent tsunami” of deaths due to infectious disease. For example, higher temperatures and loss of land cover increase the breeding of mosquitoes, which in turn help spread pathogens such as those associated with malaria.

How might global warming, if left unchecked, affect future generations? Experts predict that the increasingly warmer planet will see major shifts in pre- cipitation patterns, resulting in desertification in areas of the globe that are now productive. Those people most profoundly affected by the resulting decrease in the world food supply will be those already living in marginal circumstances, such as in vast areas of Africa, Asia, and Latin America. Overall, then, the ongoing envi- ronmental changes are threatening health by increased infectious disease, threats to food and water security, and population displacement as millions seek better living circumstances in especially threatened areas of the globe. Almost certainly, these circumstances will lead to biological change with long- term implications for many generations in the future.

Our Ongoing Evolution Huge changes are affecting this planet and the human (and other) populations occupying it. These changes have real meaning for our future, including our evolu- tion. But is there evidence of ongoing biological change in general and evolution in particular? In a word, plenty. Owing to technological innovations and their effects, humans are the most dominant evolutionary force on the other living organisms. Even before the Swiss chemist Paul Müller could receive the Nobel Prize in 1948 for his discovery that DDT killed insects, houseflies’ resistance to this chemical was being reported (Figure  13.22). By 1990, some 500 mosquito species had developed resistance to DDT, dashing the hopes that malaria could be eradicated. Bacteria associated with horrific infections have developed resistance to antibiot- ics, such as penicillin and tetracycline. Today, hospitals report that bacteria such as Staphylococcus aureus are almost always resistant to penicillin. The evolution of new, antibiotic- resistant strains of Mycobacterium tuberculosis is a big part of the dramatic rise in human deaths from this disease— more than 3 million people die per year. Other human- influenced evolution is also reported in a range of other organisms. For example, fish are evolving slower growth and thinner bodies owing to overfishing. Salmon males are under strong selection for smaller size, and they are returning to the sea earlier to increase their survival. These are but a few of the many examples of the pervasive evolution resulting from human presence and

global warming Warming of Earth’s tem- peratures, today largely due to the effect of burning of fossil fuels and resulting production of greenhouse gases.

Our Ongoing Evolution | 377

activity. Thus, the natural world is rapidly changing, in large part due to humans. These changes are anthropogenic.

Evolution began in the remote past, but it remains ongoing in humans and in other organisms. Few evolutionary biologists are comfortable with predicting future evolution, mainly because evolution is nonlinear and its course depends on current— that is, ever- changing— circumstances. The pioneers of evolutionary biology, in the eighteenth century, could not have predicted the dramatic changes the peppered moth underwent in the nineteenth and twentieth centuries, for example. Today, the evolutionary record makes clear that evolution, whatever its forms, will continue.

Inarguable predictions about the future world are that humans will continue to consume energy, human population size will continue to increase, and the global climate will continue to change. Left unchecked, these factors will present organ- isms with increasing challenges and perhaps new selective pressures. This chapter has painted a rather dark picture about our changing world— as we have more and more impact on the planet and its environment, we seem to be on a collision course with disaster. Just as humans have helped create these environmental changes, they will need to develop means of slowing global warming, most likely by modifying technologies and lifestyles to limit the production of greenhouse gases.

This field (and this book) is about the circumstances that create the basis for evolutionary change, such as the dramatic shifts in climate predicted in the near and far future. The warming trends have begun to melt massive ice sheets, resulting in raising sea levels and altering weather patterns in major ways. This will create positive circumstances for some organisms— e.g., for pathogens in the Arctic— and negative circumstances for others— e.g., agricultural crops, the growth of which will be adversely affected. We live in a dynamic world, resulting in nonstop bio- logical adjustments, adaptations, and declines.

Our key theme in this book is that humans adapt remarkably well to novel circumstances, and an enormous component of this resilience is culture, especially

FIGURE 13.22 DDT Resistance Many countries have used DDT, the first modern pesticide, for decades. As a result, numerous insects, such as the fruit fly (shown here), have developed a resistance to it. In 1972, the United States banned DDT because its use caused a serious decline in birds, such as the bald eagle.

anthropogenic Refers to any effect cased by humans.

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technology and material culture in general. Some technology has negatively influ- enced the world, including the technology associated with industrialization and the burning of fossil fuels. At the same time, human technology has produced a growing global economy and ways of producing more food, increasing the popu- lation, and living longer.

Scientists expect some regions of the world to be hit hard by temperature change and environmental disruption. Still, the record of human evolution of the last 5 million years suggests that humans will develop means for dealing with such problems. Time will tell if humans are able to use culture, intelligence, and innovation to thrive in this changing world. That has been the story so far, and I believe it will continue.

A N S W E R I N G T H E B I G Q U E S T I O N S

C H A P T E R   1 3 R E V I E W [INSERT INQUIZITIVE LOGO/TEXT HERE]

When, where, and why did agriculture first develop? • The Holocene epoch— the most recent 10,000

years— was not a static period in human evolution or in biological change generally. During this time, Homo sapiens dramatically altered their diets to include for the first time domesticated plants and domesticated animals.

• The earliest agriculture occurred in the eastern Mediterranean (the Levant). It arose in at least 10–11 other centers independently around the world.

• Plant and animal domestication may have arisen to feed the ever- increasing human population beginning in the Neolithic.

How did agriculture affect human living circumstances? • Agriculture (and associated population increase)

resulted in population sedentism and crowding. Accumulation of waste and increased transmission of microbes owing to crowding provided the conditions conducive to the spread and maintenance of infectious disease.

• Agricultural foods shifted nutrition from a generalized diet to one focused on carbohydrates and poorer- quality protein.

• In most settings, agriculture caused a decline in workload/activity.

How did agriculture affect human biological change? • Wherever the shift from foraging to farming

occurred, quality of diet declined owing to a decrease in the breadth of diet and a reduction in the nutritional quality of foods eaten.

• Poorer- quality diets led to a decline in health as foragers became farmers.

• The shift from hard foods to soft ones resulted in a generally shorter and rounder cranial vault, along with a smaller face and smaller jaws. The bone supporting the teeth reduced in size faster than the teeth reduced. As a result, humans now have many more orthodontic issues requiring the artificial straightening of teeth.

• Decreased workload/activity resulted in a general tendency toward increased gracilization of the skeleton.

• The decline in health did not affect human populations’ reproductive performance worldwide. For much of human evolution, population size was likely well under 1 million, but it perhaps grew to several million by the close of the Pleistocene.

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A N S W E R I N G T H E B I G Q U E S T I O N S

Today, the human population exceeds 7 billion people.

What are the most important forces shaping human biology today? • Global warming is altering the environment. If

left unchecked, it potentially will threaten food production and have continued negative impacts on health.

• Population increase is placing a burden on our resources and well- being.

• Population increase and associated crowding leads to poor sanitation and enhances the spread

of existing and newly emerging infectious diseases.

Are we still evolving? • There is abundant evidence of continued evolution in

humans and other organisms. • Little can be said about future evolution. If

environmental circumstances (global warming, for example) continue in their predicted direction, almost certainly conditions eliciting evolutionary change will occur.

4 5

K E Y T E R M S ameloblasts cribra orbitalia dental caries domestication global warming

heme iron iron deficiency anemia masticatory- functional hypothesis Neolithic nonheme iron

osteoarthritis periosteal reaction porotic hyperostosis superfoods treponematoses

E V O L U T I O N R E V I E W Setting the Stage for the Present and Future

Synopsis One of the most fundamental transitions in recent human evolution is the shift from hunting and gathering to agri- culture. For 99.8% of the 7 million years of our evolutionary past, humans and our hominin ancestors were foragers. Only within the last 10,000 years or so have humans undertaken the process of plant and animal domestication and become farmers the world over. This fundamental shift has brought significant environmental, social, and biological consequences for human health and lifestyle. In turn, these consequences have helped shape our adaptive strategies. In fact, many of the issues we face and will encounter in the future— such as environmental degradation, population growth, nutritional stress, and infectious disease— can be traced, in part, to agriculture and its influence on human biocultural evolution.

The story of what it means to be human is one of adaptation, both biological and cultural; the holistic and biocultural approaches of

physical anthropology allow this story to be told in grand detail. As this story continues on to its next chapter, the ongoing evolution of our species will be shaped by newly emerging environmental and ecological pressures. The challenges of a changing world will continue to test human adaptability and resilience.

Q1. Through the large- scale study of human skeletal remains, physical anthropologists have found that the shift from forag- ing to farming was accompanied by a number of health costs for human populations. Provide four examples of character- istics that indicate a decline in health among agriculturalists compared to their hunter– gatherer counterparts.

Q2. Explain how a combination of evolutionary and nonevolutionary factors has influenced the changes in cranial and facial form that accompanied the transition to agriculture. What kinds of

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complications have resulted from these changes? How do humans intervene to respond to these complications?

Q3. After the agricultural transition and subsequent increase in population size, what were the consequences, especially with regard to prevalence of infectious disease?

Q4 . How is the current episode of global warming distinct from other climate fluctuations over the last 50  million years that influenced the origins and evolution of nonhuman primates (see chapter  9) and fossil hominins (see chapters  10–12)? How might global warming act as an environmental pressure to shape the evolution of living organisms, including humans? How might humans adapt, both biologically and culturally, to these changing conditions?

Q5. We might consider the origin, dispersal, and growth of Homo sapiens populations— which resulted in our own species occu- pying virtually all regions of Earth— to be the earliest form of glo- balization. Today, globalization is characterized by the movement of ideas and products between the individuals and societies that make up our worldwide population. How does the process of globalization affect human biocultural variation and evolution?

Hint Think about the ways in which changes in nutrition and technology affect health and lifestyle in different population settings.

Q6. Are humans still evolving? What selective pressures will likely play the largest role in shaping the human condition 10 years, 50 years, and even 500 years from now?

A D D I T I O N A L R E A D I N G S

Bridges,  P.  S.  1996. Skeletal biology and behavior in ancient humans. Evolutionary Anthropology 4: 112–120.

Caballero, B. C. and B. M. Popkin. 2002. The Nutrition Transition: Diet and Disease in the Developing World. London: Academic Press.

Cohen, M. N. 1989. Health and the Rise of Civilization. New Haven: Yale University Press.

Epstein,  P.  R.  and  D.  Ferber. 2011. Changing Planet, Changing Health: How the Climate Crisis Threatens Our Health and What We Can Do about It. Berkeley: University of California Press.

Garrett, L. 1994. The Coming Plague: Newly Emerging Diseases in a World out of Balance. New York: Farrar, Straus & Giroux.

Larsen, C. S. 1995. Biological changes in human populations with agriculture. Annual Review of Anthropology 24: 185–213.

Myers, S. S. and J. A. Patz. 2009. Emerging threats to human health from global environmental change. Annual Review of Environment and Resources 34: 223–252.

Palumbi, S. R. 2001. Humans as the world’s greatest evolutionary force. Science 293: 1786–1790.

Ruff, C. B. 2008. Biomechanical analyses of archaeological human skeletons. Pp.  183–206 in M. A. Katzenberg and S. R. Saunders, eds. Biological Anthropology of the Human Skeleton. 2nd  ed. New York: Wiley- Liss.

Smith,  B.  D.  1995. The Emergence of Agriculture. New  York: Sci- entific American Library.

Taubes, G. 2008. The bacteria fight back. Science 321: 356–361.

E V O L U T I O N R E V I E W

A1

APPENDIX: THE SKELETON

The skeleton is an essential part of the biology of living primates, human and non­ human alike, and is discussed to one extent or another in many chapters of this book. Very likely, your instructor will want you to learn the essentials of primate osteology (that is, skeletal anatomy), including the names and parts of bones. This appendix provides a brief guide to that osteology, including the major bones and their parts. It presents a human skeleton, an ape (chimpanzee) skeleton, a monkey skeleton, a human skull, and close­ups of the foot bones, hand bones, and pelvic bones of the human and the ape to illustrate important differences between the bipedal and qua­ drupedal primates.

For more details on osteology and anatomy, see Tim White and Pieter Folkens’s The Human Bone Manual (Burlington, MA: Elsevier Academic Press, 2005) and Daris Swindler and Charles Wood’s An Atlas of Primate Gross Anatomy (Seattle: University of Washington Press, 1973).

A2 Appendix: The Skeleton

Phalanges

Metatarsals

Talus

Transverse archLongitudinal arch

Calcaneus

Tarsals

HUMAN FOOT

HUMAN FOOT (MEDIAL VIEW)

CHIMPANZEE FOOT

Talus

Calcaneus

A3Appendix: The Skeleton

Os coxae

Ilium

Sacroiliac joint

Sacrum

Acetabulum

Pubis

Ischium

Phalanges

Metacarpals

Carpals

Phalanges

Metacarpals

Carpals

HUMAN PELVIS CHIMPANZEE PELVIS

HUMAN HAND CHIMPANZEE HAND

A4 Appendix: The Skeleton

Cranium

Mandible

Cervical vertebrae (7)

Lumbar vertebrae (5)

Ilium

Sacrum

Pubis

Ischium

Femur

Patella

Tibia

Fibula

Tarsals (7)

Metatarsals (5)

Phalanges (14)

Clavicle

Scapula

Sternum

Ribs

Thoracic vertebrae (12)

Humerus

Ulna

Radius

Carpals (8)

Metacarpals (5)

Phalanges (14)

HUMAN SKELETON

A5Appendix: The Skeleton

Cervical vertebrae

Clavicle

Thoracic vertebrae

Sternum

Lumbar vertebrae

Sacrum

Pubis

Ischium

Femur

Patella

Tibia

Fibula

Tarsals

Metatarsals

Phalanges

Cranium

Mandible

Humerus

Ilium

Radius

Ulna

Carpals

Metacarpals

Phalanges

CHIMPANZEE SKELETON

A6 Appendix: The Skeleton

Lumbar vertebrae

Thoracic vertebrae

Scapula Cervical vertebrae

Cranium

Ilium

Caudal vertebrae

Pubis

Ischium

Femur

Patella

Fibula

Tibia

Tarsals

Metatarsals Phalanges

Mandible

Clavicle

Humerus

Radius

Ulna

Metacarpals

Phalanges

Carpals

MONKEY SKELETON

A7Appendix: The Skeleton

Sacrovertebral joint Pelvic curve

Lumbar curve

Thoracic curve

Cervical curve

Vertebral arch

Vertebral foramen

Transverse process

Body (centrum)

Body (centrum)

Spinous process

Transverse process

Body (centrum)

Sacrum (5 elements)

L5

L4

L3

L2

L1

T12

T11

T10

T9

T8 T7 T6

T5

T4

T3

T2 T1

C7 C6 C5 C4 C3 C2 (Axis)

C1 (Atlas)

Coccyx (3–5 elements)

Transverse foramen

Spinous process

HUMAN SPINE

A8 Appendix: The Skeleton

Nasal bonesFrontal

Temporal

Parietal

Parietal

Frontal

Sphenoid

Nasal

Zygomatic

Maxilla

Premolars

Molars

Incisors

Canine

Eye orbit

Nasal aperture

Temporal

Occipital

Mastoid process

Mandible

Zygomatic

Maxilla

Mandible

FRONTAL VIEW

HUMAN SKULL

LATERAL VIEW

A9Appendix: The Skeleton

Zygomatic bone

Palatine bone

Sphenoid

Foramen magnum

Parietal

Mastoid process

Occipital

Incisors (2)

Canine (1)

Premolars (2)

Maxilla

Molars (3)

Zygomatic bone

Temporal bone

Styloid process

Inferior nuchal line

Superior nuchal line

External occipital protuberance

Frontal

Coronal suture

Parietal

Sagittal suture

Lambdoidal suture

Occipital

Parietal

Nuchal line

Lambdoidal suture

Sagittal suture

Mastoid process POSTERIOR VIEWSUPERIOR VIEW

BASILAR VIEW

HUMAN SKULL

Occipital

A10 Appendix: The Skeleton

6 mo.

TIBIA

FEMUR

3 yrs. 6 yrs. 11 yrs. 16 yrs.

A11

GLOSSARY

abnormal hemoglobin Hemoglobin altered so that it is less efficient in binding to and carrying oxygen.

Acheulian Complex The culture associated with H. erectus, including handaxes and other types of stone tools; more refined than the earlier Oldowan tools.

adapids Euprimates of the Eocene that were likely ancestral to modern lemurs and possibly ancestral to anthropoids.

Adapis A genus of adapids from the Eocene. adaptations Changes in physical structure,

function, or behavior that allow an organ- ism or species to survive and reproduce in a given environment.

adaptive radiation The diversification of an ancestral group of organisms into new forms that are adapted to specific environ- mental niches.

adenine One of four nitrogen bases that make up DNA and RNA; it pairs with thymine in DNA molecules and uracil in RNA molecules.

adenosine triphosphate (ATP) An important cellular molecule, created by the mitochon- dria and carrying the energy necessary for cellular functions.

admixture The exchange of genetic material between two or more populations.

adult stage The third stage of life, involving the reproductive years and senescence.

Aegyptopithecus A propliopithecid genus from the Oligocene, probably ancestral to catarrhines; the largest primate found in the Fayum, Egypt.

aging The process of maturation. allele One or more alternative forms of a

gene. Allen’s rule The principle that an animal’s

limb lengths are heat- related; limbs are longer in hot environments and shorter in cold environments.

altruistic Refers to a behavior that benefits others while being a disadvantage to the individual.

ameloblasts Cells that make tooth enamel. amino acid dating An absolute dating

method for organic remains such as bone or shell, in which the amount of change in the amino acid structure is measured.

amino acids Organic molecules combined in a specific sequence by the ribosomes to form a protein.

anatomical Pertaining to an organism’s phys- ical structure.

angiosperm radiation hypothesis The prop- osition that certain primate traits, such as visual acuity, occurred in response to the availability of fruit and flowers following the spread of angiosperms.

anthropogenic Refers to any effect caused by humans.

anthropology The study of humankind, viewed from the perspectives of all people and all times.

anthropometry Measurement of the human body.

antibodies Molecules that form as part of the primary immune response to the pres- ence of foreign substances; they attach to the foreign antigens.

anticodons Sequences of three nitrogen bases carried by tRNA, they match up with the complementary mRNA codons and each designate a specific amino acid during protein synthesis.

antigens Specific proteins, on the surface of cells, that stimulate the immune system’s antibody production.

Apidium A parapithecid genus from the Oli- gocene, possibly ancestral to anthropoids.

arboreal  Tree- dwelling, adapted to living in the trees.

arboreal adaptation A suite of physical traits that enable an organism to live in trees.

arboreal hypothesis The proposition that primates’ unique suite of traits is an adap- tation to living in trees.

archaeology The study of historic of pre- historic human populations through the analysis of material remains.

Ardipithecus kadabba An early pre- australopithecine species from the late Miocene to the early Pliocene; shows evidence of a perihoning complex, a prim- itive trait intermediate between apes and modern humans.

Ardipithecus ramidus A later pre- australopithecine species from the late

Miocene to the early Pliocene; shows evidence of both bipedalism and arboreal activity but no indication of the primitive perihoning complex.

artifacts Material objects from past cultures. Australopithecus aethiopicus An early robust

australopithecine from East Africa, with the hallmark physical traits of large teeth, large face, and massive muscle attachments on the cranium.

Australopithecus afarensis An early australo- pithecine from East Africa that had a brain size equivalent to a modern chimpanzee’s and is thought to be a direct human ancestor.

Australopithecus africanus A gracile aus- tralopithecine from South Africa that was contemporaneous with Au. aethiopicus, Au. garhi, and Au. boisei and was likely ancestral to Au. robustus.

Australopithecus anamensis The oldest spe- cies of australopithecine from East Africa and a likely ancestor to Au. afarensis.

Australopithecus boisei Formerly known as Zinjanthropus boisei; a later robust aus- tralopithecine from East Africa that was contemporaneous with Au. robustus and Au. africanus and had the robust cranial traits, including large teeth, large face, and heavy muscle attachments.

Australopithecus garhi A late australopith- ecine from East Africa that was contem- poraneous with Au. africanus and Au. aethiopicus and was the likely ancestor to the Homo lineage.

Australopithecus (or Kenyanthropus) platyops  An australopithecine from East Africa that had a unique flat face and was contemporaneous with Au. afarensis.

Australopithecus robustus A robust aus- tralopithecine from South Africa that may have descended from Au. afarensis, was contemporaneous with Au. boisei, and had the robust cranial traits of large teeth, large face, and heavy muscle attachments.

Australopithecus sediba A late species of australopithecine from South Africa that may have descended from Au. africanus, was a contemporary of Au. robustus, and

A12 Glossary

expresses anatomical features found in Australopithecus and in Homo.

autosomes All chromosomes, except the sex chromosomes, that occur in pairs in all somatic cells (not the gametes).

balanced polymorphism Situation in which selection maintains two or more phenotypes for a specific gene in a population.

basal anthropoids Eocene primates that are the earliest anthropoids.

basal metabolic rate (BMR) The rate at which an organism’s body, while at rest, expends energy to maintain basic bodily functions; measured by the amount of heat given off per kilogram of body weight.

basal metabolic requirement The mini- mum amount of energy needed to keep an organism alive.

Bergmann’s rule The principle that an animal’s size is heat- related; smaller bodies are adapted to hot environments, and larger bodies are adapted to cold environments.

bilophodont Refers to lower molars, in Old World monkeys, that have two ridges.

biocultural approach The scientific study of the interrelationship between what humans have inherited genetically and culture.

biological (physical) anthropology The study of the evolution, variation, and adaptation of humans and their past and present relatives.

biostratigraphic dating A relative dating method that uses the associations of fossils in strata to determine each layer’s approximate age.

bipedalism Walking on two feet. Biretia An early basal anthropoid with

two cusps on its lower premolars. It is one of numerous primate species recov- ered from the Fayum of northeastern Africa.

blending inheritance An outdated, dis- reputed theory that the phenotype of an offspring was a uniform blend of the parents’ phenotypes.

bone mass The density of bone per unit of measure.

brachiators Organisms that move by brachi- ation, or arm- swinging.

Branisella A South American genus from the Oligocene, ancestral to platyrrhines.

C3 plants Plants that take in carbon through C3 photosynthesis, which changes carbon dioxide into a compound having three carbon atoms; tending to be from more temperate regions, these plants include wheat, sugar beets, peas, and a range of hardwood trees.

C4 plants Plants that take in carbon through C4 photosynthesis, which changes carbon dioxide into a compound with four carbon atoms; these plants

tend to be from warmer regions with low humidity and include corn, sugarcane, millet, and prickly pear.

calculus Refers to hardened plaque on teeth; the condition is caused by the minerals from saliva being continuously deposited on tooth surfaces.

canine– premolar honing complex The dental form in which the upper canines are sharpened against the lower third premolars when the jaws are opened and closed.

capillaries Small blood vessels between the terminal ends of arteries and the veins.

Carpolestes A plesiadapiform genus from the Paleocene, probably ancestral to the Eocene euprimates.

catastrophism The doctrine asserting that cataclysmic events (such as volcanoes, earthquakes, and floods), rather than evolutionary processes, are responsible for geologic changes throughout Earth’s history.

Cenozoic The era lasting from 66 mya until the present, encompassing the radiation and proliferation of mammals such as humans and other primates.

chemical dating Dating methods that use predictable chemical changes that occur over time.

chromosomes The strand of DNA found in the nucleus of eukaryotes that contains hundreds or thousands of genes.

clade Group of organisms that evolved from a common ancestor.

cline A gradual change in some phenotypic characteristic from one population to the next.

Clovis Earliest Native American (“Paleoin- dian”) culture of North America; technol- ogy known for large, fluted, bifacial stone projectile points used as spear points for big- game hunting.

coding DNA Sequences of a gene’s DNA (also known as exons) that are coded to produce a specific protein and are transcribed and translated during protein synthesis.

codominance Refers to two different alleles that are equally dominant; both are fully expressed in a heterozygote’s phenotype.

codons The sequences of three nitrogen bases carried by mRNA that are coded to produce specific amino acids in protein synthesis.

cognitive abilities Refers to the capacity of the brain to perceive, process, and judge information from the surrounding environment.

complementary bases The predictable pairing of nitrogen bases in the structure of DNA and RNA, such that adenine and thymine always pair together (adenine and uracil in RNA) and cytosine and guanine pair together.

cribra orbitalia Porosity in the eye orbits due to anemia caused by an iron- deficient diet, parasitic infection, or genetic disease.

crossing- over The process by which homologous chromosomes partially wrap around each other and exchange genetic information during meiosis.

cultural anthropology The study of modern human societies through the analysis of the origins, evolution, and variation of culture.

cultural dating Relative dating methods that are based on material remains’ time spans.

culture Learned behavior that is transmit- ted from person to person.

cytoplasm The jellylike substance inside the cell membrane that surrounds the nucleus and in which the organelles are suspended.

cytosine One of four nitrogen bases that make up DNA and RNA; it pairs with guanine.

data Evidence gathered to help answer questions, solve problems, and fill gaps in scientific knowledge.

deciduous dentition Also known as baby teeth or milk teeth, this is the first set of teeth, which forms in utero and erupts shortly after birth.

deme A local population of organisms that have similar genes, interbreed, and produce offspring.

demic diffusion A population’s movement into an area previously uninhabited by that group.

demography The study of a population’s features and vital statistics, including birth rate, death rate, population size, and population density.

dendrochronology A chronometric dating method that uses a tree- ring count to determine numerical age.

dental caries A disease process that creates demineralized areas in dental tissues, lead- ing to cavities; demineralization is caused by acids produced by bacteria that metabolize carbohydrates in dental plaque.

dental formula The numerical description of a species’ teeth, listing the number, in one quadrant of the jaws, of incisors, canines, premolars, and molars.

deoxyribonucleic acid (DNA) A double- stranded molecule that provides the genetic code for an organism, consisting of phosphate, deoxyribose sugar, and four types of nitrogen bases.

derived characteristics Characteristics present in only one or a few species of a group.

diaphyses The main midsection, or shaft, portions of long bones; each contains a medullary cavity.

diastema A space between two teeth. dietary plasticity A diet’s flexibility in

adapting to a given environment.

Glossary A13

diploid cell A cell that has a full comple- ment of paired chromosomes.

directional selection Selection for one allele over the other alleles, causing the allele frequencies to shift in one direction.

disruptive selection Selection for both extremes of the phenotypic distribution; may eventually lead to a speciation event.

diurnal Refers to those organisms that normally are awake and active during daylight hours.

domestication The process of converting wild animals or wild plants into forms that humans can care for and cultivate.

dominant Refers to an allele that is expressed in an organism’s phenotype and that simultaneously masks the effects of another allele, if another one is present.

dryopithecids Early Miocene apes found in various locations in Europe.

Dryopithecus A genus of dryopithecid apes found in southern France and northern Spain.

electron spin resonance dating An abso- lute dating method that uses microwave spectroscopy to measure electrons’ spins in various materials.

empirical Verified through observation and experiment.

endemic Refers to a characteristic or fea- ture that is natural to a given population or environment.

endogamous Refers to a population in which individuals breed only with other members of the population.

endotoxins Toxins released by bacteria when they break down or die.

Eoanthropus dawsoni The species name given to the cranium and mandible in the Piltdown hoax.

Eosimias A genus of very small basal anthropoids from the Eocene.

epigenetic Refers to heritable changes but without alteration in the genome.

epiphyses The end portions of long bones; once they fuse to the diaphyses, the bones stop growing longer.

epochs Divisions of periods (which are the major divisions of eras) in geologic time.

equilibrium A condition in which the system is stable, balanced, and unchanging.

eras Major divisions of geologic time that are divided into periods and further sub- divided into epochs.

essential amino acids Those amino acids that cannot be synthesized in the body; they must be supplied by the diet.

eukaryotes Multicelled organisms that have a membrane- bound nucleus containing both the genetic material and specialized organelles.

euprimates The first true primates from the Eocene: the tarsierlike omomyids and the lemurlike adapids.

evolutionary biology A specialty within the field of biology; the study of the process of change in organisms.

evolutionary synthesis A unified theory of evolution that combines genetics with natural selection.

exogamous Refers to a population in which individuals breed only with nonmembers of their population.

fission track dating An absolute dating method based on the measurement of the number of tracks left by the decay of uranium- 238.

fitness Average number of offspring produced by parents with a particular genotype compared to the number of off- spring produced by parents with another genotype.

fluorine dating A relative (chemical) dating method that compares the accumulation of fluorine in animal and human bones from the same site.

Folsom Early Native American (immedi- ately following Clovis) culture of North America; technology known for large, fluted, bifacial projectile points used as spear points for big- game hunting.

foraminifera Marine protozoans that have variably shaped shells with small holes.

forensic anthropology The scientific exam- ination of skeletons in hope of identifying the people whose bodies they came from.

fossil fuel Combustible material, such as oil, coal, or natural gas, composed of organ- isms’ remains preserved in rocks.

fossils Physical remains of part or all of once- living organisms, mostly bones and teeth, that have become mineralized by the replacement of organic with inorganic materials.

founder effect The accumulation of random genetic changes in a small population that has become isolated from the parent pop- ulation due to the genetic input of only a few colonizers.

frameshift mutation The change in a gene due to the insertion or deletion of one or more nitrogen bases, which causes the subsequent triplets to be rearranged and the codons to be read incorrectly during translation.

free- floating nucleotides Nucleotides (the basic building block of DNA and RNA) that are present in the nucleus and are used during DNA replication and mRNA synthesis.

functional adaptations Biological changes that occur during an individual’s lifetime, increasing the individual’s fitness in the given environment.

gametes Sexual reproductive cells, ova and sperm, that have a haploid number of chromosomes and that can unite with a gamete of the opposite type to form a new organism.

gemmules As proposed by Darwin, the units of inheritance, supposedly accu- mulated in the gametes so they could be passed on to offspring.

gene The basic unit of inheritance; a sequence of DNA on a chromosome, coded to produce a specific protein.

gene flow Admixture, or the exchange of alleles between two populations.

gene pool All the genetic information in the breeding population.

genetic drift The random change in allele frequency from one generation to the next, with greater effect in small populations.

genome The complete set of genetic information— chromosomal and mitochon- drial DNA— for an organism or species that represents all of the inheritable traits.

genomics The branch of genetics that stud- ies species’ genomes.

genotype The genetic makeup of an organ- ism; the combination of alleles for a given gene.

genus A group of related species. geology The study of Earth’s physical

history. Gigantopithecus A genus of Miocene pon-

gids from Asia; the largest primate that ever lived.

global warming Warming of Earth’s tem- peratures, today largely due to the effect of burning of fossil fuels and resulting production of greenhouse gases.

glucose- 6-phosphate dehydrogenase (G6PD) An enzyme that aids in the proper functioning of red blood cells; its deficiency, a genetic condition, leads to hemolytic anemia.

grade Group of organisms sharing the same complexity and level of evolution.

growth velocity The speed with which an organism grows in size, often measured as the amount of growth per year.

guanine One of four nitrogen bases that make up DNA and RNA; it pairs with cytosine.

habitat The specific area of the natural envi- ronment in which an organism lives.

habituate Refers to the process of ani- mals becoming accustomed to human observers.

half- life The time it takes for half of the radioisotopes in a substance to decay; used in various radiometric dating methods.

handaxe The most dominant tool in the Acheulian Complex, characterized by a sharp edge for both cutting and scraping.

haplogroups A large set of haplotypes, such as the Y chromosome or mitochon- drial DNA, that may be used to define a population.

haploid cell A cell that has a single set of unpaired chromosomes; half of the num- ber of chromosomes as a diploid cell.

A14 Glossary

haplotypes A group of alleles that tend to be inherited as a unit due to their closely spaced loci on a single chromosome.

Hardy- Weinberg law of equilibrium A math- ematical model in population genetics that reflects the relationship between frequencies of alleles and of genotypes; it can be used to determine whether a popu- lation is undergoing evolutionary changes.

heme iron  Iron— found in red meat, fish, and poultry— that the body absorbs efficiently.

hemoglobinopathies A group of related genetic blood diseases characterized by abnormal hemoglobin.

hemolytic anemias Conditions of insuf- ficient iron in the blood due to the destruction of red blood cells resulting from genetic blood diseases, toxins, or infectious pathogens.

heritability The proportion of phenotypic variation in a population that is due to genetic variation across individuals rather than variation in the environmental conditions experienced by the individuals. This proportion can vary from one pop- ulation to another, and thus it provides a sense of the contribution of genetic influence for each population.

heteroplasmic Refers to a mixture of more than one type of organellar DNA, such as mitochondrial DNA, within a cell or a single organism’s body, usually due to the mutation of the DNA in some organelles but not in others.

heterozygous Refers to the condition in which a pair of alleles at a single locus on homologous chromosomes are different.

homeostasis The maintenance of the inter- nal environment of an organism within an acceptable range.

homeothermic Refers to an organism’s ability to maintain a constant body temperature despite great variations in environmental temperature.

homeotic (Hox) genes Also known as homeobox genes, they are responsible for differentiating the specific segments of the body, such as the head, tail, and limbs, during embryological development.

hominin Humans and humanlike ancestors. Homo erectus An early species of Homo

and the likely descendant of H. habilis; the first hominin species to move out of Africa into Asia and Europe.

Homo floresiensis Nicknamed “Hobbit” for its diminutive size, a possible new species of Homo found in Liang Bua Cave, on the Indonesian island of Flores.

Homo habilis The earliest Homo species, a possible descendant of Au. garhi and an ancestor to H. erectus; showed the first sub- stantial increase in brain size and was the first species definitively associated with the production and use of stone tools.

homologous Refers to each set of paired chromosomes in the genome.

homoplasmic Refers to nuclear DNA, which is identical in the nucleus of each cell type (except red blood cells).

homozygous Refers to the condition in which a pair of alleles at a single locus on homologous chromosomes are the same.

Huntington’s chorea A rare genetic disease in which the central nervous system degenerates and the individual loses con- trol over voluntary movements, with the symptoms often appearing between ages 30 and 50.

hygiene hypothesis The proposition that increasing allergies among children are the result of decreased exposure to microbes, such as those found in dirt.

hypercholesterolemia The presence of high levels of cholesterol in an organism’s blood; this condition may result from the dietary consumption of foods that promote high cholesterol or through the inheritance of a genetic disorder.

hypothermia A condition in which an organ- ism’s body temperature falls below the normal range, which may lead to the loss of proper body functions and, eventually, death.

hypotheses Testable statements that potentially explain specific phenomena observed in the natural world.

hypoxia Less than usual sea- level amount of oxygen in the air or in the body.

igneous Rock formed from the crystalliza- tion of molten magma, which contains the radioisotope 40K; used in potassium- argon dating.

index fossils Fossils that are from specified time ranges, are found in multiple loca- tions, and can be used to determine the age of associated strata.

induced mutations Refers to those muta- tions in the DNA resulting from exposure to toxic chemicals or to radiation.

infanticide The killing of a juvenile. intrauterine Refers to the area within the

uterus. iron deficiency anemia A condition in

which the blood has insufficient iron; may be caused by diet, poor iron absorp- tion, parasitic infection, and severe blood loss.

isotopes Two or more forms of a chemi- cal element that have the same number of protons but vary in the number of neutrons.

karyotype The characteristics of the chro- mosomes for an individual organism or a species, such as number, size, and type. The karyotype is typically presented as a photograph of a person’s chromosomes that have been arranged in homologous pairs and put in numerical order by size.

Khoratpithecus A genus of Miocene apes from Asia, likely ancestral to orangutans.

kin selection Altruistic behaviors that increase the donor’s inclusive fitness, that is, the fitness of the donor’s relatives.

Klinefelter’s syndrome A chromosomal trisomy in which males have an extra X chromosome, resulting in an XXY con- dition; affected individuals typically have reduced fertility.

lactation The production and secretion of milk from a female mammal’s mammary glands, providing a food source to the female’s young.

Lamarckism First proposed by Lamarck, the theory of evolution through the inheri- tance of acquired characteristics in which an organism can pass on features acquired during its lifetime.

language A set of written or spoken sym- bols that refer to things (people, places, concepts, etc.) other than themselves.

law of independent assortment Mendel’s second law, which asserts that the inher- itance of one trait does not affect the inheritance of other traits.

law of segregation Mendel’s first law, which asserts that the two alleles for any given gene (or trait) are inherited, one from each parent; during gamete production, only one of the two alleles will be present in each ovum or sperm.

Levallois A distinctive method of stone tool production used during the Middle Paleo- lithic, in which the core was prepared and flakes removed from the surface before the final tool was detached from the core.

life history The timing and details of growth events and development events from con- ception through senescence and death.

linguistic anthropology The study of the construction, use, and form of language in human populations.

linkage Refers to the inheritance, as a unit, of individual genes closely located on a chromosome; an exception to the law of independent assortment.

locus The location on a chromosome of a specific gene.

loph An enamel ridge connecting cusps on a tooth’s surface.

Lower Paleolithic The oldest part of the period during which the first stone tools were created and used, beginning with the Oldowan Complex.

Lucy One of the most significant fossils: the 40% complete skeleton of an adult female Au. afarensis, found in East Africa.

macroevolution Large- scale evolution, such as a speciation event, that occurs after hundreds or thousands of generations.

macronutrients Essential chemical nutri- ents, including fat, carbohydrates, and protein, that a body needs to live and to function normally.

masticatory- functional hypothesis The hypothesis that craniofacial shape change during the Holocene was related to the consumption of softer foods.

material culture The part of culture that is expressed as objects that humans use to manipulate environments.

Glossary A15

matriline DNA, such as mitochondrial DNA, whose inheritance can be traced from mother to daughter or to son.

megafauna General term for the large game animals hunted by pre- Holocene and early Holocene humans.

meiosis The production of gametes through one DNA replication and two cell (and nuclear) divisions, creating four haploid gametic cells.

melanic Refers to an individual with high concentrations of melanin.

melanin A brown pigment that determines the darkness or lightness of a human’s skin color due to its concentration in the skin.

melanocytes Melanin- producing cells located in the skin’s epidermis.

menarche Refers to the onset of menstrua- tion in an adolescent female.

Mendelian inheritance The basic princi- ples associated with the transmission of genetic material, forming the basis of genetics, including the law of segregation and the law of independent assortment.

menopause The cessation of the menstrual cycle, signifying the end of a female’s ability to bear children.

Mesozoic The second major era of geo- logic time, 230–66 mya, characterized by the emergence and extinction of dinosaurs.

messenger RNA (mRNA) The molecules that are responsible for making a chem- ical copy of a gene needed for a specific protein, that is, for the transcription phase of protein synthesis.

microcephaly A condition in which the cranium is abnormally small and the brain is underdeveloped.

microevolution Small- scale evolution, such as changes in allele frequency, that occurs from one generation to the next.

micronutrients Essential substances, such as minerals or vitamins, needed in very small amounts to maintain normal body functioning.

Micropithecus A genus of very small procon- sulids from the Miocene, found in Africa.

microsatellites Also called short tandem repeats (STRs); refers to sequences of repeated base pairs of DNA, usually no more than two to six. If repeated excessively, they are often associated with neurological disorders, such as Hunting- ton’s chorea.

Middle Paleolithic The middle part of the Old Stone Age, associated with Mouste- rian tools, which Neandertals produced using the Levallois technique.

mitochondria Energy- producing (ATP) organelles in eukaryotic cells; they possess their own independent DNA.

mitosis The process of cellular and nuclear division that creates two identical diploid daughter cells.

monogamous Refers to a social group that includes an adult male, an adult female, and their offspring.

monosomy Refers to the condition in which only one of a specific pair of chromosomes is present in a cell’s nucleus.

morphology Physical shape and appearance. motor skills Refers to the performance of

complex movements and actions that require the control of nerves and muscles.

Mousterian The stone tool culture in which Neandertals produced tools using the Levallois technique.

mutagens Substances, such as toxins, chem- icals, or radiation, that may induce genetic mutations.

mutation A random change in a gene or chromosome, creating a new trait that may be advantageous, deleterious, or neu- tral in its effects on the organism.

natural selection The process by which some organisms, with features that enable them to adapt to the environment, pref- erentially survive and reproduce, thereby increasing the frequency of those features in the population.

Neolithic The late Pleistocene/early Holocene culture, during which humans domesticated plants and animals.

nocturnal Refers to those organisms that are awake and active during the night.

noncoding DNA Sequences of a gene’s DNA (also known as introns) that are not coded to produce specific proteins and are excised before protein synthesis.

nondisjunctions Refers to the failure of the chromosomes to properly segregate during meiosis, creating some gametes with abnormal numbers of chromosomes.

nonheme iron Iron— found in lentils and beans— that is less efficiently absorbed by the body than is heme iron.

nonhoning canine An upper canine that, as part of a nonhoning chewing mechanism, is not sharpened against the lower third premolar.

nonmelanic Refers to an individual with low concentrations of melanin.

nonmineralized Refers to bone reduced to its organic component.

nonsynonymous point mutation A point mutation that creates a triplet coded to produce a different amino acid from that of the original triplet.

Notharctus A genus of one of the largest adapids from the Eocene.

nucleotide The building block of DNA and RNA, comprised of a sugar, a phosphate group, and one of four nitrogen bases.

nucleus A membrane- bound structure in eukaryotic cells that contains the genetic material.

nutrition transition The shift in diet to one that is high in saturated fat and sugar; a cause of the global obesity endemic.

occipital bun A cranial feature of Neander- tals in which the occipital bone projects substantially from the skull’s posterior.

Oldowan Complex The stone tool culture associated with H. habilis and, possibly,

Au. garhi, including primitive chopper tools.

olfactory bulb The portion of the anterior brain that detects odors.

oligopithecids The earliest anthropoid ancestors in the Oligocene, found in the Fayum, Egypt.

omomyids Eocene euprimates that may be ancestral to tarsiers.

opposable Refers to primates’ thumb, in that it can touch each of the four finger- tips, enabling a grasping ability.

oreopithecids Miocene apes that were found in Europe.

Oreopithecus A genus of oreopithecids found in Italy that was extinct within a million years of its appearance.

Orrorin tugenensis A pre- australopithecine species found in East Africa that dis- played some of the earliest evidence of bipedalism.

osteoarthritis Degenerative changes of the joints caused by a variety of factors, especially physical activity and mechani- cal stress.

osteoblasts Cells responsible for bone formation.

osteoclasts Cells responsible for bone resorption.

osteoporosis The loss of bone mass, often due to age, causing the bones to become porous, brittle, and easily fractured.

Ouranopithecus A genus of Miocene dryo- pithecids found in Greece.

paleogenetics The application of genetics to the past, especially in anthropology and paleontology; the study of genetics in past organisms.

Paleoindians The earliest hominin inhabitants of the Americas; they likely migrated from Asia and are associated with the Clovis and Folsom stone tool cultures in North America and compara- ble tools in South America.

paleomagnetic dating An absolute dating method based on the reversals of Earth’s magnetic field.

paleontology The study of extinct life- forms through the analysis of fossils.

Paleozoic The first major era of geo- logic time, 570–230 mya, during which fish, reptiles, and insects first appeared.

pandemic Wide regional or global spread of infectious disease.

Pangaea A hypothetical landmass in which all the continents were joined, approxi- mately 300–200 mya.

parapithecids Anthropoid ancestors from the Oligocene, found in the Fayum, Egypt.

Parapithecus A genus of later parapithecids from the Oligocene, found in the Fayum, Egypt.

parental investment The time and energy parents expend for their offspring’s benefit.

A16 Glossary

patriline DNA whose inheritance can be traced from father to son via the Y chromosome.

pebble tools The earliest stone tools, in which simple flakes were knocked off to produce an edge used for cutting and scraping.

peptide bond Chemical bond that joins amino acids into a protein chain.

periosteal reaction Inflammatory response of a bone’s outer covering due to bacterial infection or to trauma.

personal genomics The branch of genom- ics focused on sequencing individual genomes.

phenotype The physical expression of the genotype; it may be influenced by the environment.

phylogeny The evolutionary relationships of a group of organisms.

physical anthropology The original term for biological anthropology.

Pithecanthropus erectus The name first proposed by Ernst Haeckel for the oldest hominin; Dubois later used this name for his first fossil discovery, which later became known as Homo erectus.

plesiadapiforms Paleocene organisms that may have been the first primates, originating from an adaptive radiation of mammals.

point mutations Replacements of a single nitrogen base with another base, which may or may not affect the amino acid for which the triplet codes.

polarized light A kind of light used in amino acid dating because it allows amino acid changes to be observed and measured.

polyandrous Refers to a social group that includes one reproductively active female, several adult males, and their offspring.

polygenic Refers to one phenotypic trait that is affected by two or more genes.

polygynous Refers to a social group that includes one adult male, several adult females, and their offspring.

polymerase chain reaction (PCR) A technique that amplifies a small sample of DNA into a large amount that can be used for various genetic tests.

polymorphism Refers to the presence of two or more alleles at a locus and where the frequency of the alleles is greater than 1% in the population.

polypeptide Also known as a protein, a chain of amino acids held together by multiple peptide bonds.

population genetics A specialty within the field of genetics; it focuses on the changes in gene frequencies and the effects of those changes on adaptation and evolution.

porotic hyperostosis Expansion and porosity of cranial bones due to anemia

caused by an iron- deficient diet, parasitic infection, or genetic disease.

positive selection Process in which advan- tageous genetic variants quickly increase in frequency in a population.

postnatal stage The second stage of life, beginning with birth, terminat- ing with the shift to the adult stage, and involving substantial increases in height, weight, and brain growth and development.

power grip A fistlike grip in which the fingers and thumbs wrap around an object in opposite directions.

preadaptation An organism’s use of an ana- tomical feature in a way unrelated to the feature’s original function.

precision grip A precise grip in which the tips of the fingers and thumbs come together, enabling fine manipulation.

prehensile tail A tail that acts as a kind of a hand for support in trees, common in New World monkeys.

prenatal stage The first stage of life, begin- ning with the zygote in utero, terminating with birth, and involving multiple mitotic events and the differentiation of the body into the appropriate segments and regions.

primates A group of mammals in the order Primates that have complex behavior, varied forms of locomotion, and a unique suite of traits, including large brains, forward- facing eyes, fingernails, and reduced snouts.

primitive characteristics Characteristics present in multiple species of a group.

Proconsul A genus of early Miocene proconsulids from Africa, ancestral to catarrhines.

proconsulids Early Miocene apes found in East Africa.

prokaryotes  Single- celled organisms with no nuclear membranes or organelles and with their genetic material as a single strand in the cytoplasm.

propliopithecids: Anthropoid ancestors from the Oligocene, found in Africa.

Propliopithecus Oligocene propliopithecid genus.

Proprimates A separate order of early pri- mate ancestors from the Paleocene, such as the plesiadapiforms.

racemization The chemical reaction result- ing in the conversion of l amino acids to d amino acids for amino acid dating.

radiocarbon dating The radiometric dating method in which the ratio of 14C to 12C is measured to provide an absolute date for a material younger than 50,000 years.

radiopotassium dating The radiometric dating method in which the ratio of 40K to 40Ar is measured to provide an absolute date for a material older than 200,000 years.

recessive An allele that is expressed in an organism’s phenotype if two copies are present but is masked if the dominant allele is present.

recombination The exchange of genetic material between homologous chromosomes, resulting from a cross- over event.

regulatory genes Those genes that deter- mine when structural genes and other regulatory genes are turned on and off for protein synthesis.

regulatory proteins Proteins involved in the expression of control genes.

replication The process of copying nuclear DNA prior to cell division so that each new daughter cell receives a complete complement of DNA.

reproductive isolation Any circumstance that prevents two populations from interbreeding and exchanging genetic material, such as when two populations are separated by a large body of water or a major mountain range.

rhinarium The naked surface around the nostrils, typically wet in mammals.

ribonucleic acid (RNA) A single- stranded molecule involved in protein synthesis, consisting of a phosphate, ribose sugar, and one of four nitrogen bases.

ribosomal RNA (rRNA) A fundamental structural component of a ribosome.

ribosomes The organelles attached to the surface of endoplasmic reticulum, located in the cytoplasm of a cell; they are the site of protein synthesis.

rigidity (bone) Refers to the strength of bone to resist bending and torsion.

Saadanius An early catarrhine Oligocene genus from a group of primates that gave rise to later catarrhines.

sagittal keel A slight ridge of bone found along the midline sagittal suture of the cranium, which is typically found on H. erectus skulls.

Sahelanthropus tchadensis The earliest pre- australopithecine species found in central Africa with possible evidence of bipedalism.

scientific law A statement of fact describing natural phenomena.

scientific method An empirical research method in which data are gathered from observations of phenomena, hypotheses are formulated and tested, and conclu- sions are drawn that validate or modify the original hypotheses.

sectorial (premolar) Refers to a premolar adapted for cutting.

secular trend A phenotypic change over time, due to multiple factors; such trends can be positive (e.g., increased height) or negative (e.g., decreased height).

sedimentary Rock formed when the depo- sition of sediments creates distinct layers, or strata.

Glossary A17

senescence Refers to an organism’s biologi- cal changes in later adulthood.

sex chromosomes The pair of chromo- somes that determine an organism’s biological sex.

sexual dimorphism A difference in a physical attribute between the males and females of a species.

sexual selection The frequency of traits that change due to those traits’ attractive- ness to members of the opposite sex.

shovel- shaped incisors A dental trait, commonly found among Native Amer- icans and Asians, in which the incisors’ posterior aspect has varying degrees of concavity.

sickle- cell anemia A genetic blood disease in which the red blood cells become deformed and sickle- shaped, decreasing their ability to carry oxygen to tissues.

single nucleotide polymorphisms (SNPs)  Variations in the DNA sequence due to the change of a single nitrogen base.

sivapithecids Early Miocene apes found in Asia.

Sivapithecus A genus of Miocene sivapithecids, proposed as ancestral to orangutans.

skin reflectance Refers to the amount of light reflected from the skin that can be measured and used to assess skin color.

social learning The capacity to learn from other humans, enabling the accumulation of knowledge across many generations.

sociolinguistics The science of investigating language’s social contexts.

somatic cells Diploid cells that form the organs, tissues, and other parts of an organism’s body.

species A group of related organisms that can interbreed and produce fertile, viable offspring.

spontaneous mutations Random changes in DNA that occur during cell division.

stabilizing selection Selection against the extremes of the phenotypic distribution, decreasing the genetic diversity for this trait in the population.

Steno’s law of superposition The principle that the lower the stratum or layer, the older its age; the oldest layers are at the bottom, and the youngest are at the top.

strata Layers of rock, representing various periods of deposition.

stratigraphic correlation The process of matching up strata from several sites through the analysis of chemical, physical, and other properties.

stressors Any factor that can cause stress in an organism, potentially affecting the body’s proper functioning and its homeostasis.

structural genes Genes coded to produce particular products, such as an enzyme

or hormone, rather than for regulatory proteins.

structural proteins Proteins that form an organism’s physical attributes.

sun protection factor (SPF) The rating calculated by comparing the length of time needed for protected skin to burn to the length of time needed for unprotected skin to burn.

superfoods Cereal grains, such as rice, corn, and wheat, that make up a substantial portion of the human population’s diet today.

synonymous point mutation A neutral point mutation in which the substituted nitrogen base creates a triplet coded to produce the same amino acid as that of the original triplet.

systematics The study and classification of living organisms to determine their evolu- tionary relationships with one another.

taphonomy The study of the deposition of plant or animal remains and the envi- ronmental conditions affecting their preservation.

taxonomy The classification of organisms into a system that reflects degree of relatedness.

tectonic Refers to various structures on Earth’s surface, such as the continental plates.

terrestrial  Life- forms, including humans, that live on land versus living in water or in trees.

thalassemia A genetic blood disease in which the hemoglobin is improperly synthesized, causing the red blood cells to have a much shorter life span.

theory A set of hypotheses that have been rigorously tested and validated, lead- ing to their establishment as a gener- ally accepted explanation of specific phenomena.

thermoluminescence dating A dating method in which the energy trapped in a material is measured when the object is heated.

Theropithecus A genus of fossil and liv- ing Old World monkeys found in Africa; it was more diverse in the past than it is today and was one of the first monkey genera to appear in the evolutionary record.

thymine One of four nitrogen bases that make up DNA; it pairs with adenine.

tooth comb Anterior teeth (incisors and canines) that have been tilted forward, creating a scraper.

total daily energy expenditure (TDEE) The number of calories used by an organism’s body during a 24-hour period.

transcription The first step of protein syn- thesis, involving the creation of mRNA based on the DNA template.

transfer RNA (tRNA) The molecules that are responsible for transporting amino

acids to the ribosomes during protein synthesis.

translation The second step of protein synthesis, involving the transfer of amino acids by tRNA to the ribosomes, which are then added to the protein chain.

translocations Rearrangements of chro- mosomes due to the insertion of genetic material from one chromosome to another.

transposable elements Mobile pieces of DNA that can copy themselves into entirely new areas of the chromosomes.

treponematoses A group of related diseases (venereal syphilis, yaws, endemic syphilis) caused by the bacteria Treponema, which causes pathological changes most often to the cranium and tibiae.

triplets Sequences of three nitrogen bases each in DNA, known as codons in mRNA.

trisomy Refers to the condition in which an additional chromosome exists with the homologous pair.

type 2 diabetes A disease in which the body does not produce sufficient amounts of insulin or the cells do not use available insulin, causing a buildup of glucose in the cells.

uniformitarianism The theory that processes that occurred in the geologic past are still at work today.

Upper Paleolithic Refers to the most recent part of the Old Stone Age, associated with early modern H. sapiens and characterized by finely crafted stone and other types of tools with various functions.

uracil One of four nitrogen bases that make up RNA; it pairs with adenine.

vasoconstriction The decrease in blood ves- sels’ diameter due to the action of a nerve or of a drug; it can also occur in response to cold temperatures.

vasodilation The increase in blood vessels’ diameter due to the action of a nerve or of a drug; it can also occur in response to hot temperatures.

victoriapithecids Miocene primates from Africa, possibly ancestral to Old World monkeys.

visual predation hypothesis The proposi- tion that unique primate traits arose as adaptations to preying on insects and on small animals.

weaning The process of substituting other foods for the milk produced by the mother.

Wolff’s Law The principle that bone is placed in the direction of functional demand; that is, bone develops where needed and recedes where it is not needed.

Y- 5 Hominoids’ pattern of lower molar cusps.

zygote The cell that results from a sperm’s fertilization of an ovum.

A19

GLOSSARY OF PL ACE NAMES

Primary research and/or findings are noted for each place.

Chapter 1 Baffin Island—Franz Boas research St. Catherines Island, Georgia—Clark Larsen

research

Chapter 2 Galápagos Islands—Charles Darwin trip and

observations

Chapter 6 New World (primates) Old World (primates) Taï Forest, Ivory Coast, West Africa—primate

behavior and conservation

Chapter 7 Gombe, Tanzania—Jane Goodall research

Chapter 9 Bighorn Basin, Wyoming—Carpolestes The Fayum Depression, Egypt—

Aegyptopithecus, Parapithecus, Apidium, Biretia, oligopithecids, parapithecids, propliopithecids

Jingzhou, China—Archicebus Paris Basin—Adapis Rukwa Rift Basin, Tanzania—Rukwapithecus

fleaglei, Nsungwepithecus gunnelli Rusinga Island, Lake Victoria,

Kenya—Proconsul Saudi Arabia—Saadanius Salla, Bolivia—Branisella Shanghuang, Jiangsu Province,

China—Eosimias St. Gaudens, France—Dryopithecus Tuscany, Italy—Oreopithecus

Chapter 10 Afar Depression, Ethiopia—Ardipithecus Allia Bay, Kenya—Australopithecus anamensis Aramis, Ethiopia—Ardipithecus kadabba and

Ardipithecus ramidus Asa Issie, Ethiopia—Australopithecus anamensis Awash River Valley, Ethiopia—Ardipithecus and

Australopithecus garhi Bouri, Middle Awash River Valley, Ethiopia—

Australopithecus garhi

Burtele, Ethiopia—Australopithecus species unknown

Dikika, Ethiopia—Australopithecus afarensis Djurab Desert, Chad—Sahelanthropus tchadensis Drimolen, South Africa—Australopithecus

robustus Eastern Rift Valley, Africa—Australopithecus Gona River, Ethiopia—Australopithecus garhi

tools Hadar, Ethiopia—Australopithecus afarensis Kanapoi, Kenya—Australopithecus anamensis Korsi Dora, Ethiopia—Australopithecus afarensis Kromdraai, South Africa—Australopithecus

robustus Laetoli, Tanzania—Australopithecus afarensis Lake Turkana, Kenya—Australopithecus ana-

mensis, Orrorin tugenensis, Australopithecus (Kenyanthropus) platyops, and Australopithe- cus aethiopicus

Lomekwi, Kenya—Australopithecus (Kenyanthro- pus) platyops

Makapansgat, South Africa—Australopithecus africanus

Malapa, South Africa—Australopithecus sediba Olduvai Gorge, Tanzania—various

Australopithecines Piltdown Common, East Sussex, England—

Piltdown hoax Sterkfontein, South Africa—Australopithecus

africanus Swartkrans, South Africa—Australopithecus

robustus Taung, South Africa—Australopithecus

africanus Tugen Hills, Kenya—Orrorin tugenensis

Chapter 11 Atapuerca, Spain—Homo erectus Bodo, Middle Awash River Valley, Ethiopia—

Homo erectus and evidence of cutmarks on bones

Bouri, Middle Awash River Valley, Ethio- pia—Homo erectus and evidence of animal butchery

Boxgrove, England—Homo erectus Buia, Eritrea—Homo erectus Ceprano, Italy—Homo erectus Dmanisi, Republic of Georgia—Homo erectus Gona, Ethiopia—complete pelvis of Homo

erectus

Gongwangling, China—Homo erectus Gran Dolina, Spain—Homo erectus, evidence

of animal butchery, and cutmarks on H. erectus bones

Ileret, Kenya—Homo erectus Lake Turkana, Kenya—Homo habilis Majuangou, China—Homo erectus Mauer, Germany—Homo erectus Nariokotome, Kenya—Homo erectus Olduvai Gorge, Tanzania—Homo habilis, Homo

erectus, and Homo rudolfensis Olorgesailie, Kenya—Acheulian tools Omo, Ethiopia—Homo habilis Sambungmacan, Java—Homo erectus Sangiran, Java—Homo erectus Sima del Elefanté, Spain—Homo erectus Sterkfontein, South Africa—Homo habilis Trinil, Java—Homo erectus Uraha, Malawi—Homo habilis Zhoukoudian, China—Homo erectus and evi-

dence of fire

Chapter 12 Aduma, Middle Awash River Valley, Ethio-

pia—early modern Homo sapiens Amud, Israel—Neandertal and evidence of

intentional burial Arago, France—early archaic Homo sapiens Atapuerca, Spain—early archaic Homo sapiens Bouri, Middle Awash River Valley, Ethiopia—

early modern Homo sapiens Clovis, New Mexico—Paleoindian sites Cro-Magnon, France—early modern Homo

sapiens Cueva Antón, Spain—Neandertal Cueva de los Aviones, Spain—Neandertal Dali, China—early archaic Homo sapiens Dederiyeh, Syria—Neandertal Denisova, Russia— Dolni Vestonice, Czech Republic—early

modern Homo sapiens El Sidron, Spain—Neandertal Engis, Belgium—Neandertal Feldhofer Cave, Germany—Neandertal Flores, Indonesia—early Homo sapiens

(“Hobbit”) Folsom, New Mexico—Paleoindian sites Gobero, Niger—early modern Homo sapiens Grimaldi Caves, Italy—early modern Homo

sapiens

A20 Glossary

Hayonim, Israel—Neandertal Herto, Middle Awash River Valley, Ethiopia—

early modern Homo sapiens Hofmeyr, South Africa—early modern Homo

sapiens Kabwe (Broken Hill), Zambia—early archaic

Homo sapiens Katanda, Congo—early modern Homo sapiens Kebara, Israel—Neandertal Kennewick, Washington—controversial

Paleoindian find Klasies River Mouth Cave, South Africa—early

modern Homo sapiens Kow Swamp, Victoria, Australia—early mod-

ern Homo sapiens Krapina, Croatia—Neandertal and possible

evidence of cannibalism La Chapelle-aux-Saints, France—Neandertal

and evidence of intentional burial Lagar Velho, Portugal—early modern Homo

sapiens Lake Mungo, New South Wales, Australia—

early modern Homo sapiens Les Rochers de Villeneuve,

France—Neandertal Lothagam, Kenya—early modern Homo sapiens

Marillac, France—Neandertal Mezmaiskaya, Russia—Neandertal Minatogawa, Japan—early modern Homo

sapiens Mladeč, Czech Republic—early modern Homo

sapiens Monte Lessini, Italy—Neandertal Moula-Guercy, France—Neandertal and possi-

ble evidence of cannibalism Narmada, India—early archaic Homo sapiens Ngandong, Java—early archaic Homo sapiens Omo, Ethiopia—early modern Homo sapiens Peştera cu Oase, Romania—early modern

Homo sapiens Petralona, Greece—early archaic Homo sapiens Prědmostí, Czech Republic—early modern

Homo sapiens Qafzeh, Israel—Neandertal Rochers de Villeneuve, France—Neandertal Scladina, Belgium—Neandertal Shanidar, Kurdistan, Iraq—Neandertal, evi-

dence of care of the sick, and evidence of intentional burial

Sima de los Huesos, Sierra de Atapuerca, Spain—early archaic Homo sapiens

Skhul, Israel—early modern Homo sapiens

Spy, Belgium—Neandertal Steinheim, Germany—early archaic Homo

sapiens Swanscombe, England—early archaic Homo

sapiens Tabun, Israel—Neandertal and evidence of

intentional burial Teshik Tash, Uzbekistan—Neandertal Tianyuan Cave, China—early modern Homo

sapiens Vindija Cave, Croatia—Neandertal Wadi Halfa, Egypt—early modern Homo sapiens Wadi Kubbaniya, Egypt—early modern Homo

sapiens Zhoukoudian, Upper Cave, China—early mod-

ern Homo sapiens

Chapter 13 Çatalhöyük, Turkey—evidence of early cities Cowboy Wash, Colorado—evidence of

cannibalism Fertile Crescent, Jordan Valley—early agricul-

tural communities Jericho, Israel—evidence of early cities Levant—early plant domestication

A21

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PERMISSIONS ACKNOWLEDGMENTS

ILLUSTRATION CREDITS

Chapter 2: Figure 2.15B: Greg Mercer, Figure, “Seven Pairs of Contrasting Traits.” © The Field Museum, #GN91263d. Reprinted with permission.

Chapter 4: Figure 4.7: Mark Ridley: Figure from Evolution, p. 77. Copyright © 2004 by Blackwell Science Ltd., a Blackwell Publishing Company. Reproduced with permission of Blackwell Publishing Ltd.; Figure 4.16: Jen Christiansen: Figure: Malaria Cycle, originally printed in “Tackling Malaria” by Claire P. Dunavan, Scientific American, Vol. 293, No. 6, Dec. 2005, p. 79. Reprinted by permission.

Chapter 6: Figure 6.27: Bruce Latimer: Figure: Ape and human pelvis mechanics. Reprinted by permission.

Chapter 8: Figure 8.17B: R.H. Towner: Fig- ure: Box 4. Constructing Chronologies from “Archaeological Dendrochronology in the Southwestern U.S.”, Evolutionary Anthropology, p. 73. Copyright © 2002, Wiley-Liss, Inc. Reprinted with permission of Wiley-Liss, Inc., a subsidiary of John Wiley & Sons, Inc.; Figure 8.19: BioArch: Figure: Amino Acid Dating from “Amino Acid Racemization.” Reprinted by permission.

Chapter 9: Figure 9.22: Reprinted from Current Biology, Vol. 8, No. 16, Salvador Moyà- Solá, et al., “Primate Evolution – In and Out of Africa”, pp. 582-588, Copyright © 1999 Elsevier Science Ltd., with permission from Elsevier.

Chapter 10: Figure 10.2: “Olduvai Gorge”, p. 61 from The Human Evolution Coloring Book, 2nd Edition by Adrienne Zihlman. Copyright © 1982, 2000 by Coloring Concepts, Inc. Reprinted by permission of HarperCollins Publishers; Figure 10.19: Figure from “Aus- tralopithecus garhi: A New Species of Early Hominid from Ethopia”, Berhane Asfaw, et al., Science, Vol. 284, April 23, 1999, p. 634. Copyright © 1999, The American Association for the Advancement of Science. Reprinted

with permission from AAAS; Figure 10.24: Figure from “Did australopiths climb trees?” by Susan Larson. Science Vol. 338. Pp. 478-479. Copyright © 2010, The American Association for the Advancement of Science. Reprinted with permission from Susan Larson; Figure 10.28: Figure from “Australopithecus sediba: A New Species of Homo-Like Australopith from South Africa,” Lee R. Berger, et al., Science, Vol. 328, April 1, 2010, p. 195. Copyright © 2010, The American Association for the Advancement of Science. Reprinted with permission from AAAS.

Chapter 11: Figure 11.10B: Figure S3 from “Early Hominin Foot Morphology Based on 1.5-Million-Year-Old Footprints from Ilerent, Kenya,” by Bennett, et al., Science, Vol. 323, No. 5918, February 27, 2009, p. 11. Copyright © 2009, The American Association for the Advancement of Science. Reprinted with permission from AAAS.

Chapter 12: Figure 12.25: Reprinted from Journal of Archaeological Science, Vol. 26, No. 6, June 1999, Hervé Bocherens, et al., “Palaeoen- vironmental and Palaeodietary Implications of Isotopic Biogeochemistry of Last Interglacial Neanderthal and Mammal Bones in Scladina Cave (Belgium),” pp. 599-607, Copyright © 1999 Academic Press, with permission from Elsevier.

Chapter 13: Figure 13.5B: Bruce D. Smith: Figure “The approximate time periods when plants and animals were first domesticated” from The Emergence of Agriculture, p. 13, 1998. Reprinted by permission; Figure 13.9: Colin Renfrew and Paul Bahn: Figure drawn by Annick Boothe. From Archaeology: Theories, Methods and Practice by Colin Renfrew and Paul Bahn, Thames & Hudson Inc., New York. Reprinted by permission of the publisher; Fig- ure 13.13: Roberto Osti: Figure “Bones of the Postcontact Indians” from “Reading the Bones of La Florida” by Clark S. Larsen, Scientific American, Vol. 282, No. 6, p. 84. Reprinted by permission of Roberto Osti Illustrations; Figure 13.18: Clark S. Larsen: Figure 3.2 “Percentage of teeth affected by dental caries

in eastern North America” from Bioarchaeology: Interpreting Behavior from the Human Skeleton, p. 69, Cambridge University Press, 1997.

PHOTOGRAPHS

Frontmatter: (page ii) H. Lansdown/Alamy

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Chapter 4: Page 70 (top): © Donna Proctor, Photographer- “Leafy Sea Dragons;” (left): © Warren Photographic; (right): Shuttershock; p. 73 (b): Kevin Schafer/Corbis; (c): Mark Boulton/ Science Source; p. 74 (Horseshoe Crab): Scott T. Smith/ Corbis; (Horseshoe Crab Fossil): Colin Keates/DK Limited/Corbis; (Cockroach): Somchai Som/ Shutterstock; (Cockroach Fos- sil): Jonathan Blair/ Corbis; (Opossum): Lynda Richardson/Corbis; (Opossum Fossil): Colin Keates/ DK Limited/ Corbis; p. 80 (White Alligator): W. Perry Conway/ Corbis; (White Cat): DK Limited/ Corbis; (Fruit Fly): Eye of Science/ Science Source; (Cheetah): Anthony Bannister/ Science Source; p. 82 (top): Stephen Frink Collection/ Alamy; (bottom): Michael Willmer Forbes Tweedie/ Science Source; p. 83 (both): Roger Tidman/ Corbis; p. 86: Dr. Gopal Murti/ Science Source; p. 89 (a): Reuters/ Cor- bis; (b): Paul Hilton/epa/Corbis; p. 93: Conor Caffrey/ Science Source; p. 94: Acey Harper/ Time Life Pictures/ Getty Images.

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Geographic/ Getty Images; p. 146 (bottom right): Martin Harvey/ Gallo Images/ Corbis; p. 150 (loris): Martin Harvey/Corbis; (tarsius): Cheryl Ravelo/Reuters/Corbis; (lemur): Kevin Schafer/Corbis; (indri): Wolfgang Kaehler/ Corbis; (aye-ayes): Nigel J. Dennis;/Gallo Images/Corbis; (tamarin): Charles Krebs/zefa/ Corbis; (spider monkey): Herbert Kehrer/ Corbis; p. 151 (colobus): Kevin Schafer/Corbis; (mandrill): DLILLC/Corbis; (gibbon): Anup Shah/Getty Images; (orangutan): Corbis; (man): Corbis; p. 152: Frans Lanting/ Corbis; p. 154 (both): Courtesy of the Division of Fossil Primates at Duke University, Elwyn L. Simons. (c) 2015, Division of Fossil Primates at Duke Universtiy. All Rights Reserved; p. 155 (right): Ann Kakaliouras, Whittier College; (center): AP Photo/World Conservation Union/Bill Konstant; (bottom left): Kevin Scafer/ Corbis; p. 156 (a): Art Wolfe/Science Source; (b): Theo Allofs/Corbis; (c): Gavriel Jecan/Corbis; (d): AP Photo/World Conservation Union/Bill Konstant; (e): Tim Laman / Getty Images; (f ): Art Wolfe/Science Sourc (g): Tom Brakefield/ Corbis; (h): Nevada Wier/Corbis; p. 157 (a): Roy Toft/National Geographic Image Collection; (b): Michael Nichols/National Geographic Image Collection; (c): D. Robert & Lorri Franz/Corbis; (d): Gallo Images/Corbis; (e): Adam Jones/Science Source; p. 159 (top): Keenan Ward/ Corbis; (bottom): Pascal Goet- gheluck/ Science Source.

Chapter 7: Page 164: Bettmann/Corbis; p. 171 (a): John Giustina/Corbis; (b): Tadashi Miwa/ Getty Images; p. 173: William Wallauer/ JGI www.janegoodall.org; p. 174 (top): Photo by Etsuko Nogami, provided by Primate Research Institute, Kyoto University. Matsuzawa, T., Humle, T., and Sugiyama, Y. 2011 “The chim- panzees of Bossou and Nimba”, Springer; p. 175 (left): Clark S. Larsen; (right): Dr. Paco Ber- tolani; p. 176: Dawn Kitchen; p. 177 (a): David Tipling/ Getty Images; (b): Florian Moellers; p. 178 (top): imageBroker/Alamy; (botttom): Alison Jones / DanitaDelimont.com Danita Deli- mont Photography / Newscom; p. 179: Yukiko Shimooka; p. 180: Susan Kuklin / Science Source.

Chapter 8: Page 183: Photo © 1996 David L. Brill, humanoriginsphotos.com; p. 184: © 1995 David L. Brill, humanoriginsphotos.com; p. 186 (left): Courtesy of American Philosoph- ical Society; (right): Bettmann/Corbis; p. 187 (a): Reuters/Corbis; (b): Henry Romero/ Reuters/Corbis; (c): Chris Hellier/Corbis; (d); Tom Bean/Corbis; (e): Wolfgang Kaehler/ Corbis; (f ): Naturfoto Honal/Corbis; (g): James L. Amos/Corbis; (h): Tom Bean/Corbis; (i): Philip Gould/Corbis; (j): Darwinius Masillae 2009. Jens L. Franzen, Philip D. Gingerich, Jörg Habersetzer1, Jørn H. Hurum, Wighart von Koenigswald, B. Holly Smith; http:// creativecommons.org/licenses/by-sa/2.5 /deed.en ; p. 190 (c): © 1985 David L. Brill, humanoriginsphotos.com; p. 191(a): John

Reader/ Science Source; (b): “The Fossil Footprint Makers of Laetoli” © 1982 Jay H. Matternes; p. 196: History of Medicine/ National Institute of Health; p. 197: Courtesy of the Croatian Natural History Museum; p. 199 (c) 1985 Jay H. Matternes; p. 200 (a-b): Peter A. Bostrom; (c): John Reader/ Science Source; (d): Kenneth Garrett/ Getty Images; (e): Javier Trueba/ Madrid Scientific Films/ Science Source; (f): Martin Land/ Science Source; (g): The Art Archive/ Corbis; (h): World Museum of Man, 2004; (i): Peter A. Bostrom; (j): Sheila Terry/ Science Source; (k): Martin Land/ Science Source; (l): Pascal Goetgheluck / Science Source; (m): Steven Alvarez/ National Geographic Image Collection/ Getty Images; (n): Peter A. Bostrom; (o): Asian Art & Archaeology/ Corbis; (p): Werner Forman/Corbis; (q): Werner Forman/Corbis; (r): Bettmann/Corbis; (s): Remi Benali/Corbis; p. 201: Lion Man Statuette - photo by Thomas Stephan © Ulmer Museum, Ulm, Germany; p. 202: Doug Wilson/Corbis; p. 205: Trevor Dumitry, Stanford University; p. 207: James O. Hamblen; p. 211 (top): Ron Boardman; Frank Lane Picture Agency/ Corbis; (bottom): Image Makers/Getty Images; p. 212: Hans Strand/ Corbis.

Chapter 9: Page 216: ©: 1985 David L. Brill, www.humanoriginsphotos.com; p. 218: Bett- mann/Corbis; p. 222: (both): Original art by Mark Klingler; copyright: Carnegie Museum of Natural History; p. 223 (all): William Sacco; p. 224 (left): Xijun Ni/Chinese Academy of Sciences; (right): Paul Tafforeau/ ESRF and Xijun Ni/ Chinese Academy of Sciences; p. 225: Nancy Perkins, Carnegie Museum of Natural History; p. 226: Seiffert et al. (2005). Basal anthropoids from Egypt and the antiquity of Africa’s higher primate radiation. Science 310: 300-304. Copyright © 2005, AAAS; p. 230 (both): Martin Harvey/Corbis; p. 232 (a): Alan Walker; p. 234 (a): Courtesy of and © of Eric Delson; (b): William K. Sacco; (bottom): David Pilbeam; p. 235: Courtesy of and © of Eric Delson; p. 239: (Proconsul): Alan Walker; (Dryopithecus): Courtesy of and © of Eric Del- son; (Sivapitecus): David Pilbeam; (Orepitecids): Courtesy of and © of Eric Delson.

Chapter 10: Page 244: © Adriadne Van Zand- bergen/ Africa Image Library; p. 246: Bettmann/ Corbis; p. 247: Adrienne I. Zihlman, Adapted from A. Zihlman, The Human Evolution Col- oring Book; p. 248 (top): Martin Harvey/Gallo Images/Corbis; p. 250 (bottom both): William K. Sacco; p. 254: Fridmar Amm/zefa/Corbis; p. 257: MPFT; p. 258 (top): © Nanci Kahn/ Insti- tute of Human Origins, Arizona State Univer- sity; p. 259 (left): © 2003 Tim D. White; (right): Cover Image: © 2009 Jay H. Matternes. From Science 18 December 2009: Vol. 326. no. 5960. Reprinted with permissions from AAAS; p. 260 (1): © 2002 David L. Brill, human originsphotos .com; (2): © 1994 Tim D. White; (3): Photo © 1995 David L. Brill, humanoriginsphotos.com; p. 261 (4): Image © 2009 Jay H. Matternes.

Permissions Acknowledgments

Permissions Acknowledgments A49

From: Lovejoy et al. The Great Divides: Ardip- ithecus ramidus Reveals the Postcrania of Our Last Common Ancestors with African Apes. Sci- ence 2 October 2009: Vol. 326. no. 5949, pp. 73, 100-106. Reprinted with permission from AAAS; (5): © 2009 Tim D. White; (5): Suwa et al. The Ardipithecus Ramidus Skull and Its Implications for Hominid Origins. Science 2 October 2009: Vol. 326. no. 5949, 68, 68e1-68e7. Reprinted with permission from AAAS; p. 262 (left): © 1985 Jay H. Matternes; (right): © 2009 C. O. Lovejoy et al. Ardipithecus ramidus and the Paleobiology of Early Hominids. Science 2 October 2009: Vol. 326. no. 5949, pp. 64, 75-86. Copyright © 2009 AAAS; p. 263 (top left): MPFT; (top right): © 2003 Tim White; (bottom right): © 2009 Tim D. White; p. 265: Kenneth Garrett/National Geographic Image Collection; p. 267 (a): © 1985 David L. Brill, www.humanoriginsphotos.com; (b): Zeresenay Alemseged/Science Source; (c): Yohannes Haile-Selassie, Liz Russell, Cleve- land Museum of Natural History. Used with permission from the Proceedings of the National Academy of Sciences. An early Australopithecus afarensis postcranium from Woranso-Mille, Ethiopia by Yohannes Haile-Selassie et al., PNAS, 6 July 2010: Vol. 107 no. 27, Fig. 1. Anatomically arranged elements of KSD-VP-1/1; p. 268 (top): © William Kimbel/ Institute of Human Origins, Arizona State University; p. 269: J. Reader/Science Source; p. 270: Fred Spoor; courtesy of National Museums of Kenya; p. 272 (left): © 1999 David L. Brill, www .humanoriginsphotos.com; (right all): McPherron et al. Evidence for stone-tool-assisted consump- tion of animal tissues before 3.39 million years ago at Dikika, Ethiopia, Nature (2010) Copy- right © 2010, Rights Managed by Nature Pub- lishing Group; p. 273 (top all): Harmand et al. 3.3-million-year-old stone tools from Lomekwi 3, West Turkana, Kenya. Copyright © 2015, Rights Managed by Nature Publishing Group; (bottom a-c): Photo credit (c) 1999 : © Tim D. White; (c): Photo credit: Permission of G. Richards & B. Plowman; p. 274: Stout et al. Technological variation in the earliest Oldowan from Gona, Afar, Ethiopia. Journal of Human Evolution 58 (2010) 474-491. Copyright © 2010, Elsevier; p. 275 (top both): © David L. Brill, www .humanoriginsphotos.com; (bottom): Photo by W. David Fooce; p. 276 (top right): Fred Spoor; courtesy of National Museums of Kenya; (bot- tom left): © 1985 David L. Brill, www .humanoriginsphotos.com; (bottom right): © Jeffrey Schwartz, University of Pittsburgh; p. 277 (all but bottom): © David L. Brill, www .humanoriginsphotos.com; (bottom): Photo by Brett Eloff courtesy of Lee Berger and the University of Witwatersrand; p. 278 (top left): Gallo Images /Corbis; (top right): © David L. Brill, www. Humanoriginsphotos.com; (bottom): Photo by Brett Eloff, courtesy of Lee Berger and the University of Witwatersrand.

Chapter 11: Page 282 (left): Russell L. Ciochon, University of Iowa; (right): Bettmann/Corbis;

p. 284: Nationaal Natuurhistorisch Museum, Leiden, the Netherlands; p. 285: Nationaal Natuurhistorisch Museum, Leiden, the Nether- lands; p. 286 (a): © David L. Brill, www .humanoriginsphotos.com; (b): John Reader/ Science Source; (c): © David L. Brill, www .humanoriginsphotos.com; p. 287 (both): © David L. Brill, www.humanoriginsphotos.com; p. 288: © David L. Brill, www.humanoriginsphotos .com; p. 290 (a): © 1985 David L. Brill www .humanoriginsphotos.com; (b): © Donald Johanson, Institute of Human Origins, Arizona State University; (c): Human Origins Program at the National Museum of Natural History, Smithsonian Institution, Photo by Chip Clark; (d): Human Origins Program at the National Museum of Natural History, Smithsonian Institution, Photo by Chip Clark; p. 291 (left): © 1985 David L. Brill, www .humanoriginsphotos.com; (right): National Museum of Kenya; photo by Alan Walker; p. 292: Image by Matthew Bennett, Bour- nemouth University. Bennett et al. Early Hominin Foot Morphology Based on 1.5- Million-Year-Old Footprints from Ileret, Kenya, Science 27 February 2009: vol. 323. no. 5918, pp. 1197-1201. Copyright (c) 2009, AAAS; p. 293 (top): Photo © 2001 David L. Brill, www.humanoriginsphotos.com; (bottom): Photo Credit © Tim D. White; p. 294 (top): Courtesy of an © National Museum of Tanzania & Eric Delson (photo by C. Tarka); (bottom): Photo Credit: © Tim D. White; p. 295: David Lordkipanidze, et.al. A Complete Skull from Dmanisi, Georgia, and the Evolutionary Biology of Early Homo. Science 18 October 2013: 342 (6156), 326-331. Copyright (c) 2013. AAAS; p. 296: Milford Wolpoff; p. 297 (top): Philippe Plailly/Science Source; (bottom): © David L. Brill, www .humanoriginsphotos.com; p. 298: Javier Trueba/Madrid Scientific Films/Science Source; p. 300 (both): Photo credit: © Tim D. White; p. 301: © 1995 Jay H. Matternes; p. 302: Courtesy of Michael Chazen; p. 303: © David L. Brill, www.humanoriginsphotos.com.

Chapter 12: Page 306: © 2003 Photographer P. Plailly E. Daynes Eurelios - Reconstruc- tion Elisabeth Daynes Paris; p. 308 (top): LVR- Landes Museum Bonn; (bottom): NIH/ Wikimedia; p. 311 (petralona): Milford Wol- poff; (bodo): Photo Credit: (c) Tim D. White; (steinheim): Courtesy of Staatliches Museum fur Naturkunde; (arago): © David L. Brill www.humanoriginsphotos.com; (kabwe): John Reader/Science Source; (ngandong): Milford Wolpoff; (narmada): Courtesy of Dr. K.A.R. Kennedy, Cornell University and the Univer- sity of Allahabad, India; (dali): Courtesy of Dr. Xinzhi Wu; (atapuerca): Javier Trueba, Madrid, Scientific Films/Science Source; (swanscombe): Jeffrey Schwartz, University of Pittsburgh; p. 312 (left): John Reader/ Science Source; (right): Milford Wolpoff; p. 313 (a): Courtesy of Dr. K.A.R. Kennedy, Cornell

University and the University of Allahabad, India; (b): Courtesy of and © of Eric Delson; p. 314 (a): © David L. Brill, www.humanoriginsphotos.com; (b): Milford Wolpoff; (c): Courtesy of Staatliches Museum for Naturkunde; p. 315 (bottom): Javier Trueba, Madrid, Scientific Films/Science Source; p. 316 (top): Ira Block/National Geo- graphic/Getty Images; (bottom): © 1985 David L. Brill, www.humanoriginsphotos.com; p. 317 (all): Photo credit and copyright by Dr. Erik Trinkaus; p. 318: © David L. Brill, www .humanoriginsphotos.com; p. 319 (top right): John Reader/Science Source; (bottom left): Granger Collection; (bottom right): Melanie Brigockas, Peabody Museum of Natural History, Yale University, New Haven, Connecticut; p. 320 (top): John Reader/Science Source; (bottom): Milford Wolpoff; p. 323: © David L. Brill, www.humanoriginsphotos.com; p. 325: Musée de l’Homme de Neandertal; p. 327: Photo by David W. Frayer; p. 328: (top): Javier Trueba, Madrid, Scientific Films/Science Source; (bot- tom): Photo credit and copyright by Dr. Erik Trinkaus; p. 330 (a): Roger Antrobus/Corbis; (b): AP Photo/ Jean Clottes; (c, all): © 1985, David L. Brill, www.humanoriginsphotos.com; p. 331 (top, both): Milford Wolpoff; (bottom, both): © Mike Hettwer; p. 332 (top): © David L. Brill, www.humanoriginsphotos.com; (bottom, both): Clark S. Larsen; p. 333 (both): Courtesy of and © of Eric Delson; p. 334 (left): Photo by Milford Wolpoff. Milford Wolpoff et al. 2004. Why not the Neandertals? World Archaeology 36 (4): 527-546. Copyright © 2004 Routledge; (right): Alan Thorne/epa/ Corbis; p. 335 (both): © David L. Brill, www .humanoriginsphotos.com; p. 337: Courtesy of and © of Eric Delson; p. 343 (top): Alan Thorne/epa/Corbis; p. 344: Milford Wolpoff; p. 345 (top): Reuters/Landov; (bottom left): © 2007 Photographer P. Plailly E. Daynes Eurelios/ Look At Sciences/ Reconstruction Elisabeth Daynes, Paris; (bottom right): Photo- graph courtesy of Peter Brown; p. 346(top): Ira Block/ National Geographic Image Collection; (bottom): Leland C. Bement; p. 347 (both): James C. Chatters.

Chapter 13: Page 350 (top): Corbis; (left): Scott Haddow; (right): Jim Holmes/Getty Images; p. 352 (top left): Cartoon by Ron Therien cartoonstock.com; (top right): Corbis; (bottom) Illustration Copyright © 2013 Nucleus Medical Media, All rights reserved. www.nucleusinc. com; p. 355 (both): Photo by John Doebley; p. 358 (a): blickwinkel / Alamy; (b): National Geographic Image Collection / Alamy; p. 359: Corbis; p. 366:Peter Johnson/Corbis; p. 369: Clark Larsen/ Mark Griffin; p. 370: Clark Spencer Larsen; p. 371: Tracy K. Betsinger; p. 372 (a): Clark Spencer Larsen; (b): Donald J. Ortner, Smithso- nian Institution; (c) Scimat/Science Source; p. 373 (top): Barry Stark; (bottom): David Scharf/Science Source; p. 374 (a): Clark Spencer Larsen; (b): Mark C. Griffin; p. 377: Darwin Dale/Visualphotos .com/Science Source.

INDEX

Page numbers in italics refer to figures, illustrations, and tables.

A abnormal hemoglobin, 84, 85, 85, 86, 86,

89–90, 90, 103 ABO blood group system, 62, 63, 92, 96, 96 absolute (numerical) dating, 195, 196, 198–99,

201–7, 208, 209, 213 non-radiometric dating and, 205, 205–7,

206, 207 radiometric dating and, 198–99, 201, 201,

202, 203, 203, 204 radiopotassium dating and, 203–5, 205, 208

acclimatization, 113 Acheulean hand axe, 200, 300 Acheulian Complex, 298 activity, see workload adapids, 220–21, 222, 223, 224, 225, 241 Adapis, 221, 222, 236 Adapis parisiensis, 217–18, 218 adaptation, 22, 101, 113–28, 129–30

arboreal, 132, 133, 135, 138, 138–41, 139, 140, 141, 142, 163, 210, 210, 218–19, 220, 229, 237

to climate change, 114–20, 115, 116, 117, 118, 119, 120, 238, 242, 314–15, 320, 320–21, 321, 322

developmental (ontogenic), 113 diurnal, 141 excessive activity and reproductive

ecology, 128 functional, 113, 119, 129 high altitudes and, 113, 118, 118–20, 119,

120, 129 nocturnal, 141, 236 nutritional, 120–26, 126, 129, 351,

353–55, 355 macronutrients and micronutrients in,

120–21, 121–22 overnutrition in, 123–26, 124, 126 undernutrition in, 121, 121, 123, 123,

126, 129 physiological (acclimatization), 113 of primates, 133, 134, 136–37 solar radiation and, 116, 116–18, 117, 119 workload, 126, 126–28, 127, 128, 130 see also genetic variation

adaptive advantage, 80–81, 98 adaptive radiation, 22, 239, 242

Addis Ababa, National Museum in, 260 adenine, 48 adenosine triphosphate (ATP), 47 admixture, 93–94, 348

see also gene flow adolescence, 105, 106–7, 111, 129 adult stage in human life history, 105, 108,

109–10, 110, 111, 129 Aduma site, 329 advantageous characteristics, see adaptive

advantage Aegyptopithecus, 216, 229, 229–30, 237 Aethiopis, 102 Afar Depression (Ethiopia), 258, 258 affixation in vocalizations, 178–79 Africa, 195, 195

agriculture in, 356, 358, 359 early archaic Homo sapiens in, 310, 310, 311, 311,

312, 312, 341 early modern Homo sapiens in, 327, 329,

329–30, 330, 331, 339, 340 genetic variation in, 338, 338–39 global warming and, 376 Homo erectus in, 289, 289, 290, 290–93, 291,

292, 293, 294, 294, 295, 296, 303, 304, 305, 312, 340

human evolution in, 7, 15, 118, 192, 256, 256, 334–35

malaria in, 86–87, 87, 88, 89 primate evolution in, 192, 228, 230, 231, 235,

238, 239, 242 sickle-cell anemia in, 86–87, 87, 88, 89 undernutrition in, 121 see also specific regions

aging, 109–10, 110 agriculture, 4, 350, 351–79

biocultural variation and, 362–75, 370, 378–79 climate and, 353, 354, 355 dietary change and, 351, 353–55, 359, 378 environmental degradation from, 361 health costs of, 350, 369–75, 370, 371, 372,

373, 374, 378 in Holocene, 359, 360, 370, 378 human height and, 375 infectious disease and, 353, 369–71, 370,

371, 373, 376 nutritional deficiencies and, 371–75, 372,

373, 374 population growth and, 354–55, 360, 361,

369–71, 370, 371, 378

regional variation in, 355–59, 356, 357, 358, 359 rise of, 351, 353–55, 354, 355, 365, 378, 379 and rise of villages, towns, and cities, 357–58,

358, 359 workload and, 366, 366–69, 367, 368, 369,

370, 378 Alabama, 368 Alaska, 126, 346 alcoholic beverages, 359 Aleutian Islands, 126 alkali, 372–73 alleles, 34, 35, 36, 67, 98, 99

dominant, 34, 35, 35, 64, 76, 83 evolutionary change in, 74, 75, 90 heterozygous, 64, 64, 83, 86, 89 homozygous, 63, 76, 83, 85, 86 mutation and, 77–78, 79, 80, 80 PKU, 66 recessive, 34, 35, 35, 64, 76 see also genes

Allen, Joel, 115 Allen’s Rule, 115, 116, 321, 322 Allia Bay (Kenya), 265, 265 alligators, 80 Allison, Anthony, 71–72, 86 altitudes, high, adaptation and, 113, 118,

118–20, 119, 120, 129 altruistic behavior, 170–71 Ambrose, Stanley, 212 ameloblasts, 373 American Civil War, 198 Americani Illinoici, 102 American Revolution, 198 American Sign Language, 180 Americas, European exploration and

colonization of, 2, 3, 4, 5 amino acid dating, 205, 205–6, 208 amino acids, 56, 59, 67, 372, 373 ammonites, 187 Amud Neandertals, 315, 316, 316, 325, 331 anatomical evidence, 15 Ancylostoma duodenale, 373 Andes mountains, 116, 120 androgens, 108 anemia

hemolytic, 84, 90 iron deficiency, 373, 373 sickle-cell, 36–37, 71–72, 76, 84–85, 85,

86, 86–87, 87, 88, 89, 103 thalassemia, 89

A51

Ángel, Andrés del, 375 angiosperm radiation hypothesis, 220 animal remains, chemistry of, 211–13 ankle (tarsal) bones, 225, 234 Antarctica, 211, 231 anthropogenic impact, 87, 377 anthropoids (Anthropoidea)

basal, 225, 225–26, 226, 241 characteristics of, 221, 225, 229 emergence of, 224–25, 225 evolution of, 218, 226, 227, 227–30, 228, 229 taxonomy of, 149, 149, 150–51, 155, 155–60,

156, 157, 158, 159, 160, 161, 162 teeth of, 142

anthropology branches of, 5, 6, 16, 17 definition of, 5–6, 16 see also archaeology; cultural anthropology;

linguistic anthropology; physical anthropology

antibiotics, overuse of, 376 antibodies, 56, 63, 63 anticodons, 57, 59 antigens, 63, 63 apes

chewing and, 248, 251 evolution of, 230, 231–32, 232, 233, 234,

236–37, 239, 242 in Asia (sivapithecids), 234, 234, 235, 235,

238, 239, 242 climate shifts and, 238 in Europe (dryopithecids), 234, 234, 238,

239, 242 modern apes, 238 oreopithecids, 235, 235, 238

gestural communication of, 179 great, see pongids (great apes) growth stages of, 146 hominins vs., 160, 161, 247–48, 249, 250–51,

252, 253, 254, 283 lesser, see hylobatids (lesser apes) similarities between humans and, 135 suspensory, 158, 158, 210 taxonomy of, 149, 150–51, 152, 154 teeth of, 144, 145, 145, 153, 248, 250–51, 262 see also specific species

Apidium, 237 Apple iPod, 200 aquatic resources, early modern Homo sapiens’s

use of, 334, 335 Arago (France), 313, 314 Aramis (Ethiopia), 258, 260–61, 262 arboreal, definition of, 15 arboreal adaptation, 132, 133, 135, 138, 138–41,

139, 140, 141, 142, 163, 210, 210, 218–19, 220, 229, 237

arboreal hypothesis, 218–19 archaeology, 5, 6, 16 Archean eon, 193, 194 Archicebus, 224, 225 Ardipithecus, 183, 258–59, 259, 260–61, 262,

262, 264, 264, 271 Ardipithecus kadabba, 258, 258–59, 259, 260–61,

262, 262, 263, 264 Ardipithecus ramidus, 258, 258–59, 259, 260–61,

262, 262, 263, 264, 264, 271, 281

Argentina, 6, 9, 63, 185 argon-39, 205 argon-40, 203, 204 Arsuaga, Juan Luis, 297 artifacts, 5 Asa Issie (Ethiopia), 265 Asfaw, Berhane, 270 Asia

agriculture in, 357, 358–59, 359, 372 early archaic Homo sapiens in, 310, 311, 311, 312,

312, 313, 341 early modern Homo sapiens in, 327, 331–32,

332, 340 genetic variation in, 338, 338, 339 global warming and, 376 Homo erectus in, 282, 289, 289, 293–96, 295,

296, 297, 303, 304, 305, 332, 340 human migrations in, 340–42, 341, 342 Neandertals in, 314, 315, 315–16, 316, 317,

341, 348 sivapithecids in, 234, 234, 235, 235, 239, 242 undernutrition in, 121 see also East Asians; Southeast Asia

assimilation evolutionary model, 339–40, 340, 341

assortment, independent, 54, 55 Atapuerca 5, 313–14, 315 Atapuerca, Sierra de, 296 Atapuerca 3 skull, 297, 298 atelids, 155 ATP (adenosine triphosphate), 47 Aurignacian culture, 329 Australia, 73, 371

aborigines of, 94 genetic diversity in, 338, 338 Greater, 342, 343 human migrations to, 341, 342, 342–43, 343,

344, 346, 348 australopithecines, 246, 264–79, 276–77

brain size of, 265, 265, 268, 270, 274, 278 evolution of, 264, 264–66, 265, 266, 267, 268,

268–69, 269, 270, 276–77, 280 extinction and, 273–75, 275, 278, 278–79,

279, 280 multiple evolutionary lineages, emergence

of, 269–72, 271, 272, 273, 274 face morphology of, 265, 269, 270, 363 habitat of, 269 Homo erectus vs., 290, 290, 291 Homo habilis vs., 286–88, 304 phalanges of, 266, 267 robust, 274, 275 skeletons of, 266, 267, 268, 268, 270,

275, 278 teeth of, 265, 265, 268, 270, 270, 274–75,

278, 290 tool use by, 270–72, 272, 273, 274, 288

Australopithecus, 246, 256, 264, 280, 290 Australopithecus aethiopicus, 264, 271, 273, 274,

275, 277, 363 Australopithecus afarensis, 264, 266, 267, 268,

268–69, 269, 270, 271, 272, 276, 291 Australopithecus africanus, 264, 271, 274–75, 276,

278, 278 Australopithecus anamensis, 264, 265, 265, 266,

268, 271, 276

Australopithecus boisei, 264, 271, 273–74, 275, 275, 277, 286, 290

Australopithecus garhi, 264, 270–72, 271, 272, 273, 277, 279, 286

Australopithecus platyops, 269, 270, 270, 276 Australopithecus robustus, 264, 271, 275, 275,

277, 278, 278 Australopithecus sediba, 271, 275, 277, 278, 278 axes, hand, 200, 298, 300

B baboons, 156, 158, 165, 225, 240

cooperation in, 170–71 reproductive strategies of, 169, 169 residence patterns of, 168 teeth of, 142, 145 vocalizations of, 176, 177

Bacillus permians, 187 Backwell, Lucinda, 271–72 balanced polymorphism, 86 Balkans, mass murders in, 63 Bangladesh, 375 Bantu populations, 87, 89 barley, 358 basal anthropoids, 225, 225–26, 226, 241 basal metabolic rate (BMR), 116 basal metabolic requirement, 121 base insertion, 79 base substitution, 79, 86 Beagle, HMS, 21, 22, 31 Beall, Cynthia, 120 Beard, Christopher, 225 beetles, 75 Begun, David, 238 Beijing, 282, 296 Belgium, 324, 324, 325, 336, 341 Belize, 177 Benyshek, Daniel, 125–26 Bergmann, Carl, 115 Bergmann’s Rule, 115, 115, 116, 321, 322 Bering land bridge (Beringea), 346 Berna, Francesco, 300 Big Horn Basin (Wyoming), 222 big toe, see hallux (big toe) bilophodont molars, 144, 145, 240 biocultural approach, 6 biocultural variation

agriculture and, 362–75, 370, 378–79 clines and, 103–4, 129 as evolutionary continuum, 101 in fossil Homo sapiens, interpretation of,

335–39, 336, 338 in hominins, 7, 8 race concept and, 101, 102, 102, 103, 129

biodiversity, 361 biological anthropology, see physical

anthropology biological variation, human, see biocultural

variation biology

evolutionary, 24, 29–30, 31, 74 human, 7, 8, 9

biomechanics of bones, 367–69, 368, 369

biostratigraphic dating, 197–98, 199, 208

A52 Index

bipedalism, 12 of australopithecines, 266, 267 habitat and, 15 as hominin characteristic, 8, 10, 12, 15, 15, 160,

248, 249, 252, 252, 254, 254–55 origins of, 262, 262, 264 skeletal indicators of, 159, 160

Biretia, 225, 226, 226 Birket Qarun Lake, 228 Biston betularia, 82, 82–83, 83 Biston carbonaria, 82–84, 83, 84 black-and-white colobus monkeys, 135,

136, 156 blending inheritance, 34, 35 blood, glucose levels in, 125 blood types, human, 62, 63, 344

frequencies of, 92, 92, 93, 96, 96, 103 Blumenbach, Johann Friedrich, 102, 102 BMI (body mass index), 124 BMR (basal metabolic rate), 116 Boas, Franz, 8, 103 Bodo (Ethiopia), 292, 293, 293 body hair, 114 body mass index (BMI), 124 body shape

climate adaptation and, 114–15, 115, 314–15, 321, 321, 322

of early modern Homo sapiens, 333, 334 of Neandertals, 315, 321, 321, 322

body tissues, 106 body weight, 124, 124–25 Bolivia, 230, 231, 370 Bombay, 370 bone chemistry, 324 bone mass, 127–28, 128 bones

biomechanics of, 367, 367–69, 368, 369 calcaneus (heel bone), 225 fractures, 110 growth of, 107, 107, 108 nonmineralized, 107 remodeling of, 127, 127 rigidity of, 127 tarsal (ankle), 225, 234 ulna, 107 workload and, 126, 126–27, 130, 367, 367–69,

368, 369 see also skeletons

bonobos, 151, 152, 153, 158, 180 Border Cave, South Africa, 206 Borneo, 132, 175, 284, 284, 342, 343 Botswana, 176, 176 Bougainville Islands, 338 Boule, Marcellin, 319, 320 Bouri (Ethiopia), 270, 271, 293, 298, 329 Boxgrove (England), 297, 300 Boyd, Robert, 13 Brace, C. Loring, 102, 313 braces, orthodontic, 351, 352 brachiators, 158 Braidwood, Robert, 366 brain

human, growth and development of, 105, 106, 106, 107

primate, morphology of, 147, 147, 218, 227 Brain, Charles Kimberlin, 190

brain size of Ardipithecus, 261 of australopithecines, 265, 265, 270, 274, 278 of Australopithecus afarensis, 268, 268 of early modern Homo sapiens, 336 of Homo erectus, 284–85, 289, 295, 296, 298,

299, 300, 303, 303, 304, 305 of Homo habilis, 279, 285–86, 286, 287, 288,

288, 299, 300, 304, 305 of Homo sapiens, 257, 312, 312, 313 of Neandertals, 307, 314, 316, 319 of primates, 147, 147, 155, 229, 234, 235, 238

Branisella, 230, 231 Bräuer, Günter, 329 Brazil, 108, 109, 370 Bridges, Patricia, 368 Broken Hill (Kabwe) mine (Zambia), 312, 312 Brown, Peter, 344 browridges

of early archaic Homo sapiens, 309, 312, 312, 313, 314

of early modern Homo sapiens, 329, 330, 332, 333, 335

of Homo erectus, 289, 290, 292, 293, 294, 295, 295, 296, 299, 302

of modern humans, 309, 343 of Neandertals, 317

Brunet, Michel, 257 Bryce Canyon, 24 Budongo Forest, 178 Buffon, Georges-Louis Leclerc, Comte de, 217 Buia, 292, 293 Burgos (Spain), 313 burials by Neandertals, 324–25, 325, 327, 348 butchering

by early Homo, 298, 300, 301 by Neandertals, 322

Büyük Menderes, 295

C Calcagno, James, 365 calcaneus (heel bone), 225 calculus, 324 Cambrian period, 193, 194 Campbell’s monkeys, 135, 136, 179 Candela, Pompeo, 96 canine-premolar complex

of early archaic Homo sapiens, 313 honing, 144, 145, 145 nonhoning, 250, 250–51

canine teeth of Neandertals, 326 of primates, 144, 145, 145

Cann, Rebecca, 338, 339 cannibalism, 293, 303, 319 capillaries, 85 capuchin (Cebus) monkeys, 175 carbohydrates, 371, 372, 375, 378 carbon-14 dating, see radiocarbon dating Carbon-inferous period, 193, 194 carbon isotopes, 201, 203, 203, 212 carbon-13, 212 carbon-12, 212 caries, dental, 371, 372 Carlson, David, 363, 364 Carpolestes, 222, 223

Carpolestes simpsoni, 223 Cartmill, Matt, 219 Çatalhöyük, 357, 358, 358 catarrhines (Old World higher primates), 149,

151 evolution of, 216, 229, 230, 231, 240, 241 teeth of, 155, 155

catastrophism, 26 catfish, 335 cats, domestic, 80 Caucasoid race, 101, 102, 102 cave art, 329, 330 cebids, 155 ceboids (New World monkeys), 143, 143, 149,

150, 155, 219 arboreal adaptation of, 155 reproductive strategies of, 169 residence patterns of, 169

cell membrane (wall), 44, 45 cells

cytoplasm of, 44, 45, 45 diploid, 53, 53 division of, see meiosis; mitosis haploid, 53, 54 nucleus of, 44, 45, 45 organelles of, 44 types of, 44–46, 45, 46 see also gametes; somatic cells

Cenozoic era, 194, 195 primate evolution in, 220 temperature change in, 210, 211

Central America, 121, 356 cephalic index, 103 Ceprano (Italy), 297 cercopithecines, 156, 157–58 cercopithecoids (Old World monkeys)

evolution of, 207, 216, 219, 230, 232, 239–41, 240

reproductive strategies of, 169 residence patterns of, 168 taxonomy of, 149, 151, 155–57, 156 teeth of, 143, 144, 145, 145

C4 plants, 212 chacma baboons, 176 Chad, 256, 257 Chaplin, George, 116 Chauvet cave art, 330 cheetahs, 80 chemical dating, 196–97, 197, 208 chemistry of animal remains and ancient soils,

211–13, 212 Cheney, Dorothy, 176, 179 chest size, altitudes and, 113, 120 chewing complex

of hominins, 248, 248, 250, 250–51, 251, 252, 259, 259, 279

of Homo habilis, 279, 286, 287, 304 of modern humans, 363, 365 nonhoning, 8, 10–11, 12, 248, 248, 250,

250–51, 251, 252 childhood, 105, 106, 111, 129

prolonged, 112 chimpanzees, 135, 136, 151, 152, 153, 157, 158, 159

brain morphology of, 147 cooperation in, 170, 171, 171 DNA in, 46

Index A53

chimpanzees (continued) evolution of, 207, 219 food acquisition by, 181 genetic closeness to humans of, 42 gestural communication in, 179 Goodall’s study of, 9, 164, 165–66 grooming among, 167, 171, 179, 179 growth stages of, 146 intelligence of, 166, 174 life span of, 167 material culture of, 173, 173–75, 174, 175, 180 as omnivores, 166 parental investment by, 146 polio in, 135 social organization of, 165 teeth of, 142, 144, 235, 251 tool use by, 11, 12, 13, 166, 173, 173–75, 175, 304 vocalizations of, 177, 178

chin (mental eminence), 309, 330, 331, 332 China

agriculture in, 358, 359, 359 Archicebus in, 224, 225 Dali, 312, 313 early modern Homo sapiens in, 332, 332 Homo erectus in, 282, 295, 296, 296, 297 Shanghuang, 225

cholesterol, high, 124–25 Chororapithecus, 238 chromosomes, 36, 37, 46, 47, 48, 67

homologous, 51, 51, 53, 64, 67 sex, 51, 51–52 types of, 51, 51–52

cities, agriculture and rise of, 357–58, 358, 359 cladistic classification, 148–49, 149, 152–53, 153 Clark, Desmond, 271 classification systems, see systematics;

taxonomy climate/climate change

adaptation to, 114–20, 115, 116, 117, 118, 119, 120, 235, 238, 242, 288, 314–15

agriculture and, 353, 354, 355 Holocene, 353 Miocene, 210, 211, 254 reconstruction of, 210–11, 211

clines, 103–4, 129 Clinton, Bill, 43 Clovis culture, 346 Clovis points, 200 cockroaches, 74 coding DNA, 60, 78 codominance, 65 codons, 57, 59, 78, 86 Coffing, Katherine, 297–98 cognition in hominins, advanced, 247 cognitive abilities, 106, 106 cold stress, adaptation and, 115–16, 119, 314–15,

320, 320–21, 321, 322 collagen, 65 colobines, 156, 156–57, 158, 213, 240, 240, 241 colobus monkeys, 136, 137, 138, 144, 156 Columbus, Christopher, 5, 50, 94, 192, 359, 370 competition

reproduction and, 167, 167, 169, 170, 255 vocalizations and, 177

complementary bases in DNA, 48, 49 conception, 105

Congo, 335, 339 continental drift, 195 cooking by Homo erectus, 300, 301–2, 303, 303, 304 cooperation in primates, 170–72, 171 corn, 350, 357, 358, 359, 371, 372 Correns, Carl Erich, 36 Costa, Dora, 108 cotton, 356 crabs, 187 cranial capacity, see brain size cranium, see skulls Crelin, Edmund, 325 Cretaceous period, 193, 194, 195 cribra orbitalia, 374, 374 Crick, Francis, 37, 48 Croatia, 317, 317, 324, 327, 336, 338 Crockford, Cathy, 178 Cro-Magnon site, 333, 335 cross-over, 54 C3 plants, 212 Cueva Antón (Spain), 318, 327 Cueva de los Aviones (Spain), 327 cultural anthropology, 5, 6, 16 cultural dating, 198, 200, 201, 208 culture, 5

see also material culture cutmarks, 272, 273, 297, 298, 318 Cuvier, Georges, 25–26, 26, 27, 32, 185, 217–18,

218 cytoplasm, 44, 45, 45, 58 cytosine, 48 Czech Republic, 333, 333, 336, 336

D Dahlberg, Albert, 344 Daka (Ethiopia), 292, 293 Dali site (China), 312, 313 Darwin, Charles, 19, 21, 29, 38, 72, 183, 259,

283, 285 hunting hypothesis of, 251–52, 253, 254 hypothesis on origin of human bipedalism, 15 natural selection theory of, 22, 30, 33–34, 40,

80–81 On the Origin of Species, 20, 32, 33, 34, 192, 283,

340 portrait of, 15, 20, 22 theory of evolution, 21–24, 23, 27, 31–33, 32,

39, 80, 185 Darwin, Erasmus, 27, 30 Darwinius masillae, 187 data, 14, 14 dating

absolute (numerical), 195, 196, 198–99, 201–7, 208, 209, 213

non-radiometric dating and, 205, 205–7, 206, 207

radiometric dating and, 198–99, 201, 201, 202, 203, 203, 204

radiopotassium dating and, 203–5, 205, 208 genetic, 207–9, 209 relative, 195–98, 201, 208, 209, 213

biostratigraphic dating and, 197–98, 199, 208 chemical dating, 196–97, 197, 208 cultural dating and, 198, 200, 201, 208 stratigraphic correlation and, 196, 208

thermoluminescence, 207, 207, 208

Dawn Ape, see Aegyptopithecus DDT resistance, 376, 377 De Brazza’s monkeys, 156 deciduous dentition, 106, 106, 107, 107 demes, 72 Demidoff’s galago, 135, 136 demography, 24, 29 dendrochronology, 201, 202, 208 Dendropithecus, 237 Denisova Cave, 338, 342 dental caries, 371, 372 dental comb, 223 dental formula, 142–43, 143, 229, 230, 239 dentition

deciduous, 106, 106, 107, 107 of primates, 142, 220 see also teeth

deoxyribonucleic acid (DNA), see DNA (deoxyribonucleic acid)

derived characteristics, 148 dermis, 116, 117 d’Errico, Francesco, 272 developmental (ontogenic) adaptation, 113 development in humans, 104–12, 129

postnatal, 105, 106, 106–9, 107, 108, 109, 111, 129

prenatal, 52, 52–53, 105, 111, 129 Devonian period, 193, 194 DeVore, Irven, 165, 366 diabetes, type 2, 125–26, 129 Diana monkeys, 135, 136, 177, 178, 179 diaphyses, 107, 107 diastema, 145, 145 diet

of early archaic Homo sapiens, 313–14, 315 of early modern Homo sapiens, 334 of Homo erectus, 298, 300, 302, 304 of Homo habilis, 288, 288–89 of Neandertals, 322, 324, 324 reconstruction of, 211–13 rise of agriculture and, 351, 353–55,

359, 378 see also nutrition

dietary plasticity, 135, 137, 142, 142–43, 143, 144, 145, 145–46, 161, 163

Dikika (Ethiopia), 266, 268, 270 dimorphism, sexual, 106, 155, 156, 167, 167, 169,

221, 255 diploid cells, 53, 53 directional selection, 81, 81 “Dirty War,” 6, 9 disease, infectious, 375

agriculture and, 353, 369–71, 370, 371, 373, 376

population growth and, 379 Spaniards introduction of, to Native

Americans, 4 disruptive selection, 81, 81 diurnal adaptation, 141 Djurab Desert, 257 Dmanisi (Republic of Georgia), 294, 295, 295,

302, 303 DNA (deoxyribonucleic acid), 9, 19, 39, 43,

46–68 coding, 60, 78 dating and, 207

A54 Index

discovery of, 37–38 disease and, 43 double-helix structure of, 48, 48, 49 evolution and, 37–38, 43–44, 50, 231 in fossils, 191 meiosis and, 49, 53, 54, 55, 56, 56, 64, 67 mitochondrial, see mitochondrial DNA

(mtDNA) mitosis and, 48, 49, 52, 52–53, 53, 67 mutation in, see mutations noncoding, 60, 78 nuclear, 46, 67, 338, 346 polymorphisms and, 61–65, 63, 64 protein synthesis and, 56, 56–57, 57, 58–59,

60, 60, 68 replication of, 48–49, 49, 51, 51–52, 68 sequences of, 48, 93 in structural and regulatory genes, 61,

61, 62 Dolní Věstonice skulls, 333, 333 domestication of food resources, 11, 12–13,

351, 353–60, 354, 355, 356, 357, 359, 379

see also agriculture dominant alleles, 34, 35, 35, 64, 76, 83 Dordogne, 306, 333, 335 Douglass, A. E., 201 Down House, 32 Down syndrome, 54 Dragon Bone Hill (China), 296 Drimolen (South Africa), 275 dryopithecids, 234, 234, 238, 239 Dryopithecus, 234, 234 Dubois, Eugène, 283–85, 284, 289, 296 Dunkers, 92, 92–93 Düsseldorf (Germany), 307 Dutch East Indies, 283, 284

E eagles, 136, 138, 172, 177 Earth, age of, 24, 192, 193, 195 East Africa

australopithecines in, 269–70, 271, 273, 274, 275, 278, 290

early hominins in, 254, 254 early modern Homo sapiens in, 329, 330,

331, 339 Homo erectus in, 290–91, 294, 295 Homo habilis in, 286, 286, 288, 304 see also specific sites

East Asians blood types of, 96, 96 shovel-shaped incisors of, 344, 345, 346

Easter Island, 344 Eastern Rift Valley, 256, 256, 257 ecosystems, see habitats Egypt, 192, 225, 227–29, 228, 229, 231, 237 Egyptians, ancient, 102 electron spin resonance dating, 207, 208 elements, transposable, 78 El Sidron (Spain), 318, 324, 327, 336 embryonic development, 52, 105, 111 empirical, definition of, 14 enamel, thickness of, 146, 235, 251, 251, 262,

290, 315, 373, 373 endogamous populations, 92, 94

endoplasmic reticulum, 44 Engis, 336, 341 England, see Great Britain environmental degradation, 361 environmental stress, 105, 108, 108–9, 129 environments, 8

definition of, 7 extreme, 129 temperature and, 210–11, 211, 224 variation in, 65–66, 66 see also habitats

enzyme abnormalities, 89–90 enzymes, 56, 56, 58 Eocene epoch, 193, 194, 199

primates in, 187, 217–18, 220–22, 222, 223, 224, 225, 225–26, 226, 227–28, 228, 231, 236, 241

temperature change in, 210, 211 eons, 193, 194 Eosimias, 225, 225, 226 epidermis, 116, 117 epigenetics, 65, 67, 68 epiphyses, 107, 107, 108 epochs, geologic, 193, 194, 195

see also specific epochs equilibrium, 76

Hardy-Weinberg law of, 76, 76–77, 77, 83, 84, 98, 99

eras, geologic, 193, 194, 195 see also Cenozoic era; Mesozoic era; Paleozoic

era Eritrea, 292 Escherichia coli, 45 Eskimos, see Inuit Essay on the Principle of Population, An

(Malthus), 29 essential amino acids, 56 estrogens, 108 Ethiopia, 15, 256, 298

Afar Depression, 258, 258 Aramis, 258, 260–61, 262 Asa Issie, 265 Bodo, 292, 293, 293 Bouri, 270, 271, 293, 298, 329 Daka, 292, 293 Dikika, 266, 268, 270 Gona, 273 Hadar (Ethiopia), 266, 268, 270 Middle Awash Valley, 183, 213, 258, 258–59,

260–61, 270, 271, 288, 292, 293, 298, 329

Ethiopian (Africans) race, 102 eukaryotes, 44–45, 45 euprimates, 220–22, 222, 223, 224, 236 Europe

agriculture in, 358–59, 372 early archaic Homo sapiens in, 310, 311, 311, 312,

313, 314, 341 early modern Homo sapiens in, 327, 329, 329,

332–34, 333, 334, 335, 340 early primates in, 234, 234, 238, 239, 242 evolution of modern humans in, 335 Homo erectus in, 289, 289, 295, 295, 296–97,

298, 304, 305, 340 Neandertals in, 314, 316–19, 318, 319, 320,

326, 335, 338, 339, 341, 348

Europeans, 90 American exploration and settlements of, 2, 3,

4, 5, 90, 94, 359, 370 blood types of, 103 genetic variation in, 338, 338, 339

evolution, 21–40, 194 agriculture and, 362, 363 of anthropoids, 218, 226, 227, 227–30, 228, 229 of apes, 230, 231–32, 232, 233, 234, 236–37,

239, 242 in Asia (sivapithecids), 234, 234, 235, 235,

238, 239, 242 climate shifts and, 238 in Europe (dryopithecids), 234, 234, 238,

239, 242 modern apes, 238 oreopithecids, 235, 235, 238

of catarrhines, 216, 229, 230, 231, 240, 241 Darwin and, 19, 21–24, 23, 27, 30, 31–33, 32,

39, 40, 80, 185 dating of, see dating DNA and, 37–38, 43–44, 50 of euprimates, 220–22, 222, 223, 224 fossil evidence for, 183, 186, 187, 188, 192, 213 geologic time scale and, 193, 193–95, 194, 195 habitat and, 236–37 of hominins, 7, 8, 10–11, 13, 15, 16, 192, 206,

207, 244, 245–81 australopithecines, see australopithecines pre-australopithecines, 246, 256–59,

257, 258, 259, 260–61, 262, 262, 263, 264, 280

of Homo erectus, 297–98, 299, 300, 300–304, 301, 302, 304

Lamarck and, 30, 31 macro, 74, 75 micro, 74, 75 of monkeys, 207, 237, 239–41, 240, 242 as ongoing process, 376–78, 377, 379 of platyrrhines, 229, 230, 230–31, 241 of primates, 137, 192, 194, 214, 216, 217–42,

219, 227 reproductive success in, 81 skin color and, 118, 129 see also adaptation; genetic variation; natural

selection evolutionary biology, 24, 29–30, 31, 74 evolutionary change, see genetic variation evolutionary synthesis, 36–37, 37, 38, 39, 40 excess weight, 124, 124–25 exogamous populations, 92, 94 eye orbits

cribra orbitalia in, 374, 374 of Neandertals, 316, 317, 320, 321 of primates, 141, 141, 152, 220, 221, 222, 227,

235, 236

F face morphology

of australopithecines, 265, 269, 270, 363 of early archaic Homo sapiens, 309, 312,

312, 313 of early modern Homo sapiens, 329, 330, 331,

332, 332, 334, 334, 336 of Homo habilis, 279, 299 of modern humans, 309, 363, 364, 378

Index A55

face morphology (continued) of Native Americans vs. Paleoindians, 347, 347 of Neandertals, 313, 315, 316, 320, 321

farming, see agriculture faunal (biostratigraphic) dating, 197–98, 199, 208 fava beans, 89 Fayum Depression (Egypt), 192, 225, 227–29,

228, 229, 231, 237 feet

bipedalism and, see bipedalism phalanges, 262, 266, 267 of tarsiers, 152

Feldhofer Cave (Germany), 306, 307–8, 308, 318, 336, 337

femur, 107, 368 diaphysis of, 107 epiphysis of, 107 of Homo erectus, 284, 285

ferns, 187 Fertile Crescent, 357, 357 fertility, human

as adaptive advantage, 112 in Holocene, 375

fertilization, 52, 52, 105, 111 fetus, 52, 105 fibroblasts, 117 finches, Galápagos, 22, 23 fingernails of primates, 140, 140 fire, Homo erectus’s use of, 300–301, 302, 303,

305 Fischer, Julia, 178 fish, 187, 376 Fisher, R. A., 71 fishing, 334, 335 fission track dating, 205, 205, 208 fitness, 81, 81 flagellum, 45 Flores Island, 344, 344, 345 Flores Woman, 345 Florida, 367, 368 fluorine dating, 196–97, 197 folate (folic acid), 118, 121 folic acid, 118, 121 Folsom culture, 346, 346 food acquisition

domesticated, 11, 12–13, 351, 353–60, 354, 355, 356, 357, 359, 379

by early modern Homo sapiens, 334 by primates, 171, 172–73, 180, 181 see also agriculture; hunting

food resources, availability of, 173, 298, 341 footprints of early hominins, 190, 191, 268–69,

269, 291–92, 292 foramen magnum, 160, 248, 249 foramina, infraorbital, 320, 321 foraminifera, 210, 211 Ford Model T, 200 forensic anthropology, 6, 9

Argentina’s “Dirty War” and, 6, 9 September 11, 2001, terrorist attacks and, 7, 63

fossil fuels, 376 fossil pig molars, 198, 199 fossils/fossil record, 19, 21, 24, 25–26, 32, 39,

73, 74, 183, 184, 185–214 creation of, 188, 189 definition of, 188, 213

DNA in, 191 evolution and, 183, 186, 187, 188, 192, 213 hominin, 190, 191, 246–51, 257, 257, 258,

258–59, 260–61, 262, 264, 281, 285, 286 index, 198, 199 limiatations of, 191–92 representation in, 191–92 types of, 188, 190, 190–91, 191

founder effect, 93, 93, 94 FOXP2 gene, 327 fractures, bone, 110 frameshift mutation, 78 France

early archaic Homo sapiens in, 313, 314 early modern Homo sapiens in, 329, 329, 333,

335 La Chapelle-aux-Saints, 319, 319, 325, 325,

334, 336 Neandertals in, 306, 318, 319, 319, 324, 325,

325, 334 Rochers de Villeneuve, 336, 341 St. Gaudens, 234

Franklin, Rosalind, 37 Frayer, David, 326 free-floating nucleotides, 49, 51, 51 Frisancho, Roberto, 113 fruit fly (Drosophila melanogaster), 62

mutations in, 36, 37, 80 fuel, wood as, 361 Fulbe community, 6 functional adaptations, 113, 119, 129

G Gage, Timothy, 167 galagos, 136, 143, 149, 150, 153, 154 Galápagos Islands, 22, 23 gametes, 46, 46, 51–52, 53, 54, 64 gametocytes, 88 gas transport proteins, 56 Gebo, Daniel, 225 geladas, 168, 169, 169, 240 gemmules, 33–34 gene flow, 36–37, 93–94, 95, 96, 96, 97, 98, 348 gene frequency, 72, 75, 92, 93, 96, 98, 339 gene linkage, 56, 56 gene pool, 36, 72, 94 genes, 34, 35, 36, 39

homeotic (Hox), 60, 61, 62, 67 pleiotropic, 66, 66 polymorphisms and, 61–65, 63, 64 regulatory, 60, 61, 61, 62 structural, 60, 61 see also genotypes

genetic change, see genetic variation genetic code, see DNA (deoxyribonucleic acid) genetic dating, 207–9, 209, 346 genetic drift, 37, 38, 90–93, 91, 92, 93, 94, 97,

98, 339 genetic markers, 96, 96 genetics, 36, 39, 42–68

complexity of, 65–66, 66 population, 36, 71–99

demes, reproductive isolation, and species in, 72–74, 73, 74, 75, 76

gene flow and, 93–94, 95, 96, 96, 97, 98 genetic drift and, 90–93, 91, 92, 93, 94, 98

Hardy-Weinberg law of equilibrium and, 76, 76–77, 77

mutations and, 77–78, 79, 80, 80, 97–98 natural selection and, see natural selection

genetic variation, 34–35, 66, 66, 97 gene flow and, 94, 95, 96, 96, 97 genetic drift and, 90–93, 91, 92, 93, 94 in modern humans, 338, 338–39, 340 mutations and, 78, 94 of Native Americans, 50 natural selection and, 72, 80–90, 98 see also adaptation; evolution

genome, 7, 46 human, 7, 78, 104 Neandertal, 338

genotypes, 36, 63, 63–65, 67, 68 fitness and, 81 thrifty, 125 see also genes

genus, 28, 29 Geoffroy Saint-Hilaire, Étienne, 217 geographic clines, 103–4 geologic strata, 24, 24, 186, 192, 196, 247 geologic timescale, 193, 193–95, 194, 195, 214 geology, 24, 24 Georgia, 2, 3–4, 16, 354, 367, 368, 368 Georgianae, 102 Germans, blood type of, 92, 92 Germany

early archaic Homo sapiens in, 313, 314 Feldhofer Cave, 306, 307–8, 308, 318, 336,

337 Homo erectus in, 297 Lion Men sculpture in cave in, 198, 201

giant deer, 198 gibbons, 152, 153, 158, 169, 210

evolution of, 207, 219 growth stages of, 146 life span of, 167 teeth of, 144

Gigantopithecus, 235, 235 Gingerich, Phillip, 220, 224 global warming, 224, 376, 379 glucose levels, 125 glucose-6-phosphate dehydrogenase (G6pd),

85, 89–90 Gobero, 330, 331 Gombe, 174, 179 Gombe National Park, 164, 165, 179 Gona (Ethiopia), 273 Gona River, 271 Gongwangling (China), 296, 296 Goodall, Jane, 9, 164, 165–66, 173–74 Goodman, Morris, 207 goosefoot, 357, 358 gorillas, 151, 152, 153, 157, 158, 159, 180

evolution of, 207, 219, 241 phalanges of, 267 as polygynous, 168 skeleton of, 249 skull of, 154 teeth of, 142, 235, 250

Gorjanović-Kramberger, Dragutin, 197, 197, 317

gradistic (traditional) classification, 148–49, 149, 152–53, 153

A56 Index

grandmothering, 112, 112 Gran Dolina, 296–97, 297, 298 grasp of primates, 138, 138–39, 218, 219–20,

221, 222, 227, 236 Gravettian culture, 329 gray langurs, 156 great apes, see pongids (great apes) Great Britain

early archaic Homo sapiens in, 313 Homo erectus in, 297 peppered moths in, 82, 82–84, 83, 84 Smith’s geologic map of, 186

Greater Australia, 342, 343 Great Rift Valley, 244, 245 Greece, 234, 313, 314, 359 greenhouse gases, 376 Greenland, 94, 113 Grimaldi Caves, 333 grooming, 167, 170, 170

hand clasp, 179, 179 growth

in humans, 104–12, 129 postnatal, 105, 106, 106–9, 107, 108, 109,

111, 129 prenatal, 105, 111, 129

in primates, 146, 147 growth velocity, 106, 106 G6pd (glucose-6-phosphate dehydrogenase),

85, 89–90 guanine, 48 Guatelli-Steinberg, Debbie, 324

H habitats, 22

climate shifts and, 238, 288 coastal, 368 evolution and, 236–37 reconstruction of, 211–12 see also environments

habituate, 166 Hadar (Ethiopia), 266, 268, 270 Hadean eon, 193, 194 Haeckel, Ernst, 283, 285 Haile-Selassie, Yohannes, 269 Haldane, J. B. S., 71 half-life, 203, 203 hallux (big toe)

bipedalism and, 249, 262 opposable, 139, 139–40, 269

Hamilton, William, 171 handaxes, 200, 298, 300 hand clasp grooming, 179, 179 hand preference in Neandertals, 326–27, 327 haplogroups, 50, 344, 346 haploid cells, 53, 54 haplorhines, 148, 149, 149, 150, 155, 155–60,

156, 157, 158, 159, 160, 161, 162, 225 haplotypes, 54, 56 Hardy, Godfrey, 76 Hardy, Karen, 324 Hardy-Weinberg law of equilibrium, 76, 76–77,

77, 83, 84, 98, 99 Harris, Jack, 199 health, impact of agriculture on, 350, 369–75,

370, 371, 372, 373, 374, 378 hearing in primates, 141

heat stress, 114–15, 115, 119, 321 heel bone (calcaneus), 225 Heidelberg (Germany), 297 height

of early modern Homo sapiens, 334 of Homo erectus, 291, 298, 299 of Homo habilis, 298, 299 of modern humans, 108, 108–9, 109, 375 nutrition and, 108, 108, 109, 123, 123, 126–27

Heinzelin, Jean de, 271 heme iron, 373 hemoglobinopathies, 89, 90 hemoglobins, 86

abnormal, 84, 85, 85, 86, 86, 89–90, 90, 103 in high altitudes, 119

hemolytic anemias, 84, 90 heritability, 66, 66 Herodotus, 102, 185 Herto, 329, 339 Herto skulls, 309 heteroplasmic, 48 heterozygous alleles, 64, 64, 83, 86, 89 high altitudes, adaptation and, 113, 118, 118–20,

119, 120, 129 “hobbits,” 344, 345 Hofmeyr, 329, 330 Holiday, Trent, 334 Holocene epoch, 193, 194, 198

agriculture in, 359, 360, 370, 378 climate change in, 353 early modern Homo sapiens in, 330, 331 human fertility increase in, 375 infectious disease in, 370–71, 371 nutritional change in, 373, 373

homeostasis, 109, 113, 126 homeothermic life forms, 114 homeotic (Hox) genes, 60, 61, 62, 67 hominins, 7

apes vs., 160, 161, 247–48, 249, 250–51, 252, 253, 254, 283

biocultural variation in, see biocultural variation

brain size of, 13, 147 characteristics of, 8, 10–11, 12, 16, 246–51, 252

bipedalism, 8, 10, 12, 15, 15, 160, 248, 249, 252, 252, 254, 254–55

chewing complex, 248, 248, 250, 250–51, 251, 252, 259, 259

definition of, 7, 280 domestication of food resources, 11, 12–13 evolution of, 7, 8, 10–11, 13, 15, 16, 192, 206,

207, 244, 245–81 australopithecines, see australopithecines pre-australopithecines, 246, 256–59, 257,

258, 259, 260–61, 262, 262, 263, 264, 280

fossils, 190, 191, 246–51, 257, 257, 258, 258–59, 260–61, 262, 264, 281, 285, 286

hunting by, 8, 11, 12 intelligence of, 13 material culture of, 8, 11, 12, 247 origins of, 251–55, 253, 254, 280 phylogenies of, 264 social learning and, 13 speech of, 8, 10, 12, 246–47 taxonomy of, 149, 151, 152

teeth of, 235 tool use by, 8, 11, 12, 13, 252–53 see also specific hominins

hominoids, 151, 152, 157, 158 evolution of, 216, 236–37, 240

Homo (genus), 264, 270, 304, 305 adaptive flexibility of, 285–86 tool use by, 270, 272

Homo erectus, 271, 284–85, 285, 289–304, 303, 341

in Africa, 289, 289, 290, 290–93, 291, 292, 293, 294, 294, 295, 296, 304, 305, 340

as ancestor of Homo sapiens, 310 in Asia, 282, 289, 289, 293–96, 295, 296, 297,

304, 305, 332, 340 australopithecines vs., 290, 290, 291 brain size of, 284–85, 289, 295, 296, 298, 299,

300, 303, 303, 304, 305 browridges of, 289, 290, 292, 293, 294, 295,

295, 296, 299, 302 cannibalism among, 293, 303 diet of, 298, 300, 302, 304 early archaic Homo sapiens vs., 312, 313, 313 in Europe, 289, 289, 295, 295, 296–97, 298,

303, 304, 305, 340 evolution of, 297–98, 299, 300, 300–304,

301, 302, 304 fire used by, 300–301, 302, 305 height of, 291, 298, 299 Homo habilis vs., 289, 290, 297–98, 299, 300,

302, 304 hunting by, 303, 304 migrations of, 303, 340 skeletons of, 290–91, 291 skulls of, 284, 285, 289, 290, 291, 292, 293,

293, 294, 295–96, 296, 297, 297, 298, 302, 303, 344

teeth of, 284, 290, 296, 297, 299, 301–2, 304 tool use by, 295, 296, 297, 298, 300, 301,

303, 304 Homo floresiensis, 344 Homo habilis, 271, 279, 285–89, 288, 304

australopithecines vs., 286–88, 304 brain size of, 279, 285–86, 286, 287, 288, 288,

299, 300, 304 chewing complex of, 279, 286, 287, 304 diet of, 288, 288–89 height of, 298, 299 Homo erectus vs., 289, 290, 297–98, 299, 300,

302, 304 skeletal structure of, 287 skulls of, 286, 286, 287, 287 teeth of, 279, 286, 287, 299, 305 tool use by, 287–89, 288, 304

homologous chromosomes, 51, 51, 53, 64, 67 homoplasmic, 46 Homo rudolfensis, 286, 287 Homo sapiens, 29, 271, 348

adaptive flexibility of, 101 archaic, 309, 328, 336 assimilation evolutionary model for, 339–40,

340, 341 brain size of, 257, 312, 312, 313 early archaic, 183, 311, 311–14

in Africa, 310, 310, 311, 311, 312, 312, 341 in Asia, 310, 311, 311, 312, 312, 313, 341

Index A57

Homo sapiens (continued) browridges of, 309, 312, 312, 313, 314 dietary adaptations of, 313–14, 315 in Europe, 310, 311, 311, 312, 313, 314, 341 face morphology of, 309, 312, 312, 313 Homo erectus vs., 312, 313, 313 skulls of, 309, 312, 312, 313, 313, 314, 315 teeth of, 309, 313–14, 315, 326–27 tool use and technology of, 313, 315

early modern, 322, 327–34, 337 in Africa, 327, 329, 329–30, 330, 331, 339, 340 in Asia, 327, 331–32, 332, 340 body shape of, 333, 334 browridges of, 329, 330, 332, 333, 335 in Europe, 327, 329, 329, 332–34, 333, 334,

335, 340 face morphology of, 329, 330, 331, 332, 332,

334, 334, 336 fishing and aquatic resource use by, 334, 335 gracility vs. robustness in, 334 hunting by, 329, 334 migrations of, 340 nasal apertures of, 333, 335 Neandertals’ coexistence with, 336–38 skulls of, 329–30, 331, 332, 332–33, 333,

334, 335 teeth of, 329, 332, 334, 336

late archaic, see Neandertals modern, see modern humans Multiregional Continuity evolutionary model

for, 310, 310, 335–36, 338, 338–39, 340, 348 Out-of-Africa evolutionary model for, 310,

310, 335–36, 338, 338–39, 340, 348 homozygous alleles, 63, 76, 83, 85, 86 honing complex, 145, 145 Hooke, Robert, 25, 25, 27 hookworm, 373, 373 Hooton, Earnest, 8 hormones, 56, 108 horseshoe crab, 74 howler monkeys, 155, 168, 177, 177, 229 Hox (homeotic) genes, 60, 61, 62, 67 Hrdlička, Aleš, 8, 344 Hrdy, Sarah Blaffer, 169 humans, see hominins; modern humans humerus, 107, 316, 317, 368 hunter-gatherers, 4

quality of life of, 366, 366 shift to agriculture by, 351, 353–57, 354, 355,

356, 360, 365, 379 skeletons of, 367, 368, 370

hunting Darwin’s hypothesis about, 251–52, 253, 254 by early modern Homo sapiens, 329, 334 by hominins, 8, 11, 12, 303 by Neandertals, 321–22, 323, 324, 324 by Paleoindians, 346, 346

Huntington’s chorea, 93, 93, 94 Hutton, James, 24, 24, 32 Huxley, Thomas Henry, 36, 36, 159, 251–52,

253, 285, 308 hylobatids (lesser apes), 149, 151, 152, 153, 157 hyoid bone, 10, 268, 325, 326, 326 hypercholesterolemia, 124 hypoplasias, 373 hypothermia, 115, 116

hypotheses, 14, 14, 16 hypoxia, 118–20, 120

I Ice Age, Pleistocene, 8, 319 igloos, 116 igneous rock, 203 Ileret (Kenya), 290, 292, 292 Illinois, 375 immune system, malnutrition and, 121 incisors

of early archaic Homo sapiens, 313–14, 315 of euprimates, 223 of Neandertals, 326, 327 of primates, 137, 142, 143, 144, 145, 227 shovel-shaped, 344, 345, 346

independent assortment, 54, 55 index fossils, 198, 199 India, 312, 312, 313, 370 Indonesia, 196, 283–84, 284, 295, 295, 296,

343, 344, 344, 345 induced mutations, 78 industrial melanism, 82, 82–84, 83, 84 Industrial Revolution, 82 infancy, 105, 111, 112, 129 infant care, see parental investment infanticide, 169, 170 infectious disease, see disease, infectious infertility, 54 infraorbital foramina, 320, 321 inheritance, 33–36, 39, 40 insulin, 125 intelligence

of chimpanzees, 166, 174 of hominids, 13 of primates, 147, 147, 161 see also brain size

intrauterine environment, 105 Inuit, 113, 116, 316, 322 ionizing radiation and mutations, 78 Iraq, 63, 316, 317 Irish elk, 198 iron, absorption of, 372 iron deficiency anemia, 373, 373 Isaac, Glynn, 298 isolation, reproductive, 72–73, 73 isotopes, 201

carbon, 201, 203, 203, 212 fission tracking and, 205, 205 oxygen, 210

Israel, 309, 315, 315, 316, 325, 331, 357, 358 Italy

early modern Homo sapiens in, 333 Homo erectus in, 297 Monte Lessini, 336, 341 thalassemia in, 89

Ivory Coast, 135, 136–37, 175, 177

J Jablonski, Nina, 116 Jacob, Teuku, 344 Jane Goodall Institute, 164 Java, 284, 289, 295–96, 296, 312, 312, 342, 343 Java Man (Pithecanthropus erectus), 284–85,

285, 296 see also Homo erectus

jaw, see mandible Jefferson, Thomas, 185, 186 Jericho, 357, 358 Johannsen, Wilhelm Ludvig, 36 Johanson, Donald, 268, 270, 287 Jones, Frederic Wood, 218 Ju/’hoansi (!Kung), 366, 366 Jurassic period, 193, 194, 195 juvenile period, 105, 106, 111, 129

K Kabwe (Broken Hill) mine (Zambia), 310, 312,

312 Kanapoi (Kenya), 265 Kanzi (captive bonobo), 180 Kappelman, John, 295 karyotype, 51, 51 Katanda (Congo), 335, 339 Kebara Neandertals, 315, 316, 316, 325–26,

326, 331 Keith, Arthur, 363 Kemp, Brian, 50 Kennewick Man, 347, 347 Kent, England, 32 Kenya, 165, 179, 256, 286, 298

Allia Bay, 265, 265 Ileret, 290, 292, 292 Kanapoi, 265 Lake Victoria, 232 Lemudong’o, 212–13 Lomekwi, 269, 270 Nariokotome, 290 Olorgesailie, 298, 300, 300, 302 Rusinga Island, 231, 232, 237 Serengeti grasslands of, 212, 212 sickle-cell gene in, 71–72, 86 Turkana in, 109, 265, 269, 286, 288, 290

Kenyanthropus platyops, 269, 270, 270 keratin, 57 keratinocytes, 116, 117 Khoratpithecus, 235, 238 kinkajous, 155 kin selection, 171 Kitchen, Dawn, 176, 177 Klasies River Mouth Cave, 330, 331 Klinefelter’s syndrome, 78 kneecap, 107 Kocabaş specimen, 295 Koobi Fora, 291 Korsi Dora, 266, 267 Kow Swamp, 343, 344 Krakatoa, 196 Krapina Neandertals, 197, 317, 317–18,

318, 324 Krause, Johannes, 327 Krings, Matthias, 337 Kromdraai (South Africa), 275 !Kung ( Ju/’hoansi), 366, 366 Kurdish Jews, 89

L La Chapelle-aux-Saints (France), 319, 319, 325,

325, 334, 336 lactation, 105, 109, 112 lactic acid, 371 Lactobacillus acidophilus, 371

A58 Index

Laetoli (Tanzania), 190, 191, 266, 268, 269, 269, 291

Lagar Velho skeleton, 329, 333, 334 Lamarck, Chevalier de ( Jean-Baptiste de

Monet), 27, 30, 31 lamarckism, 27, 30, 31 language, 5 langurs, 156, 168 Lantian (China), 296 Laos, 332 La Paz, 370 Lartet, Edward, 234 law, scientific, 15 law of independent assortment, 54, 55 law of segregation, 62, 64 law of superposition, Steno’s, 196, 208 leafy sea dragon, 82 Leakey, Louis, 165, 166, 245–46, 246, 265,

270, 271, 286 Leakey, Mary, 204, 245–46, 246, 269, 270, 271 Lee, P. C., 172 Lee, Richard, 366 left-handedness, 326–27 Le Gros Clark, Wilfrid E., 135 leisure time, 343, 366 Lemudong’o (Kenya), 212–13 lemurs, 140, 141, 153, 222

growth stages of, 146 life span of, 167 taxonomy of, 149, 149, 150 teeth of, 143, 143, 144, 154, 224

leopards, 177, 190 lesser apes, see hylobatids (lesser apes) lesser spot-nosed monkeys, 135, 136 leuciam, 80 Levallois tools, 200, 322, 323 Levant, 361, 378 Lewontin, R. C., 103 lexigrams, 180 Liang Bua Cave, 344 Libby, Willard, 201 Lieberman, Philip, 325 life history of humans, 104–12, 129

adult stage in, 105, 109–10, 110, 111 definition of, 104 postnatal stage in, 105, 106, 106–9, 107, 108,

109, 111, 129 prenatal stage in, 105, 111, 129

limbs of Neandertals, 315, 321 Limnopithecus, 237 Lincoln, Abraham, 61 linguistic anthropology, 5, 6, 16 linkage of genes, 56, 56 Linnaeus, Carolus (Carl von Linné), 27, 28, 29,

29, 102, 135, 217 Lion Men sculptures, 198, 201 living populations, 96, 101–30, 183 Livingstone, Frank B., 87, 104 locomotion, suspensory (arboreal), 158, 158,

238, 266 locus (plural, loci) on chromosomes, 60, 61,

76, 93 Lomekwi (Kenya), 269, 270 long bones

growth of, 107, 107 of Neandertals, 327

Loomis, William, 117 loph, 145 Lordkipanidze, David, 293 lorises, 143, 143, 144, 149, 149, 150,

153–54, 219 Lothagam, 330, 330, 331 Lovejoy, Owen, 254, 255, 262 low birth weight, 105 Lower Paleolithic, 270 Lucy (A. afarensis), 266, 267, 268, 268 lung volume, 129 Lyell, Charles, 25, 25, 27, 32

M macaques, 169, 219, 240

growth stages of, 146 life span of, 167

macroevolution, 74, 75 macronutrients, 120–21, 121–22 Madagascar, 153–54, 154 Madhya Pradesh, 312 Magdalenian culture, 329 Mahale National Park, 179 maize, see corn Majuangou (China), 295, 296, 296 Malapa (South Africa), 275, 278 malaria, 71, 72, 76, 86–87, 87, 88, 89, 103 Malawi, 286 Malay race, 102 malnutrition, 121, 121, 123, 123–26, 124, 126,

129 malocclusion, 351, 352, 352, 365, 365 Malthus, Thomas, 27, 29, 29, 30, 32 mammoths, 198 Manchester, England, 83 mandible

of early archaic Homo sapiens, 313 of early modern Homo sapiens, 331, 332, 334 of Homo erectus, 294, 297, 299, 302 of modern humans, 266, 352, 363, 364 of Neandertals, 316 see also skulls

mandrills, 156 mangabeys, 136, 240 manioc, 358 Man’s Place in Nature (Huxley), 159 Marfan syndrome, 61, 65 Mariana Islands, 342 Marillac (France), 324 Márquez, Lourdes, 375 masseter muscle, 159, 363 mastication, see chewing complex masticatory-functional hypothesis, 363 masticatory muscles, 158, 250, 251 material culture, 8, 11, 12, 247

of chimpanzee societies, 12, 13 for cultural dating, 198 primate, 173, 173–75, 174, 175, 180, 181

matriline, 48, 52 matrilocal societies, 95 maturity

sexual, 61, 106–8 social, 108

Mauer jaw, 297 Maya, 375 Mayan pot, 200

McGraw, Scott, 172 McGrew, Bill, 179 McHenry, Henry, 254, 297–98 McKee, Jeffrey, 361 Mead, Margaret, 6 meat-eating, 298, 300, 303, 324, 324, 326 megafauna, 346–47 Megaladapis, 154 Megalonyx jeffersoni, 186 meiosis, 49, 53, 54, 55, 56, 56, 64, 67 Melanesia, 338 melanic form, 82, 82–84, 83, 84 melanin, 116, 117 melanocytes, 117 menarche, 106 Mendel, Gregor, 34, 34, 36, 39, 40, 54, 72

law of independent assortment, 54, 55 law of segregation, 62, 64

Mendelian inheritance, 36 menopause, 110 mental eminence, see chin (mental eminence) merozoites, 88 Mesolimulus walchii, 74 Mesolithic, 364 Mesozoic era, 194 messenger RNA (mRNA), 57, 58, 60, 79, 86 methane, 376 Mexico, 358, 375 Mezmaiskaya (Russia), 336, 341 microcephaly, 344, 345 Microchoerus, 236 microevolution, 74, 75 Micrographia (Hooke), 25 micronutrients, 120–21 Micropithecus, 231–32 microsatellites, 62–63, 93, 104 Middle Awash Valley, 183, 213, 258, 258–59,

260–61, 270, 271, 288, 292, 293, 298, 329

Middle East, agriculture in, 356 Middle Paleolithic culture, 322, 323 Middleton, James, 196 migrations

of early modern Homo sapiens, 340 of Homo erectus, 294, 295, 303, 340 of modern humans, 339–47, 342, 348

to Australia and Pacific Islands, 342, 342–44, 343, 344, 345, 346, 348

to the Western Hemisphere (first Americans), 344, 346, 346–47, 347, 348

millet, 356, 358, 363 Minatogawa, 332 minerals, 122 Miocene epoch, 193, 194, 199

hominins in, 251, 254, 257, 259, 279 primates in, 230, 231–32, 232, 233, 234,

234, 235, 235, 236, 238, 239, 240, 241, 242, 256

temperature change in, 210, 211, 254 Mission Santa Catalina de Guale, 3–4 mitochondria, 44, 47–48 mitochondrial DNA (mtDNA), 48, 52, 95

fossil record vs., 343 human evolution and, 336–37 of Native Americans, 50, 344, 346

mitosis, 48, 49, 52, 52–53, 53, 67, 105

Index A59

Mladeč skulls, 333, 336 modern humans, 309, 348

bone strength of, 367–69 browridges of, 309, 343 chins of, 309 evolutionary lineages of, 219, 309–10,

310, 348 face morphology of, 309, 363, 364, 378 genetic variation in, 338, 338–39, 340 growth stages of, 146 height of, 108, 108–9, 109, 375 life history of, see life history of humans mandible of, 266, 352, 363, 364 migrations of, 339–47, 342, 348

to Australia and Pacific Islands, 342, 342–44, 343, 344, 345, 346, 348

to the Western Hemisphere (first Americans), 344, 346, 346–47, 347, 348

Neandertals’ genetic relationship to, 50, 306, 308, 319, 319, 320, 320, 321, 321, 322, 326, 339–40, 340, 341, 348

nutritional requirements of, 120–21, 121–22, 123, 123

racial categorization of, see race concept skeletons of, 126, 126–27, 249, 343, 344, 344,

345, 363, 364 skin color of, 100 skulls of, 309, 343, 344, 363, 364 teeth of, 309, 344, 345, 346, 363, 365, 378 see also Homo sapiens: early modern

molars of early archaic Homo sapiens, 313 of early modern Homo sapiens, 332 eruption of, 106, 107 fossil pig, 198, 199 of Homo erectus, 284, 290 of primates, 137, 142, 143, 143, 144, 145,

145, 230 Y-5, 144, 145, 152, 153, 158, 232

Mongol migrations, 96 Mongoloid race, 101, 102, 102 monkeys, 133, 135, 136–37, 168, 169, 230, 254

adaptive radiation of, 242 brain morphology of, 147 evolution of, 207, 237, 239–41, 240, 242 New World, see ceboids (New World

monkeys) Old World, see cercopithecoids (Old World

monkeys) predators of, 138 taxonomy of, 149, 150–51, 152, 154, 156,

156–58 teeth of, 144, 145, 145 vocalizations of, 176, 177, 177–78, 179

monogamous mating, 167, 169 monosomy, 54 Monte Lessini (Italy), 336, 341 Moore, Leslie, 6 Morgan, Thomas Hunt, 36 morphology, 15 Morwood, Michael, 344 mosquitoes, 86, 87, 88, 89 moth, peppered, 82, 82–84, 83, 84 motor skills, 106 Moula-Guercy cave (France), 318, 319 mountain sickness, 118–19

mouse lemur, 225 Mousterian culture, 322, 323 Mousterian tools, 200 mRNA (messenger RNA), 57, 58–59, 60,

79, 86 mtDNA, see mitochondrial DNA (mtDNA) Müller, Paul, 376 Mulligan, Connie, 346 Multiregional Continuity evolutionary model,

310, 310, 335–36, 338, 338–39, 340, 348 Mungo, Lake, 342, 343, 343, 344 Murray River Valley (Australia), 343 muscles

masseter, 159 masticatory, 158, 250, 251 temporalis, 158, 159

mutagens, 78 mutations, 36, 37, 50, 62, 76, 77–78, 79, 80, 80,

84–85, 86, 86, 89, 93, 94, 97–98 frameshift, 78 induced, 78 point, 78 spontaneous, 78, 80

Muybridge, Eadweard, 15 Mycobacterium tuberculosis, 376

N nails, 140, 140, 218, 220, 221, 227 Napier, John, 138, 286 Nariokotome (Kenya), 290 Nariokotome Boy, 290, 291, 292, 294 Narmada (India), 312, 312, 313 nasal apertures

of early archaic Homo sapiens, 309, 313 of early modern Homo sapiens, 333, 335 of Neandertals, 315, 316, 317, 317, 319, 319,

320, 320 Native Americans, 316

blood types of, 93 European contacts with, 3, 4, 90, 94, 370 evolutionary change in, 4 genetic variation in, 50 haplogroups of, 344, 346 malaria and, 90 mtDNA of, 50, 344, 346 Paleoindians vs., 347 as race, 101, 102, 102 shovel-shaped incisors of, 344, 345, 346 skin color of, 104 teeth of, 345 type 2 diabetes in, 125–26

natural selection, 20, 22, 30, 33–34, 36, 40, 70, 97

adaptive advantage and, 80–81, 98 in animals (peppered moth), 82, 82–84, 83,

84 genetic variation and, 72, 80–90, 98 in humans (abnormal hemoglobins and

malaria resistance), 84–87, 85, 86, 87, 88, 89, 89–90, 90

patterns of, 81, 81 sickle-cell anemia and, 84–85, 85 types of, 81, 81

nDNA (nuclear nDNA), 46, 67, 338, 346 Neandertals, 199, 306, 314–27

Amud, 315, 316, 316, 325, 331

in Asia, 314, 315, 315–16, 316, 317, 341, 348 body shape of, 315, 321, 321, 322 brain size of, 307, 314, 316, 319 browridges of, 317 burials by, 324–25, 325, 327, 348 cold climate adaptation of, 314–15, 320,

320–21, 321, 322 diet of, 322, 324, 324 early modern Homo sapiens’ coexistence with,

336–38 in Europe, 314, 316–19, 318, 319, 320, 326,

335, 338, 339, 341, 348 as evolutionary dead ends, 319–20 eye orbits of, 316, 317, 320, 321 face morphology of, 313, 315, 316, 320, 321 hunting by, 321–22, 323, 324, 324 incisors of, 326, 327 Kebara, 315, 316, 316, 325–26, 326, 331 Krapina, 197, 317, 317–18, 318, 324 limbs/bones of, 315 modern humans’ genetic relationship with,

50, 306, 308, 319, 319, 320, 320, 321, 321, 322, 326, 339–40, 340, 341, 348

mtDNA of, 336–37, 343 nasal aperture of, 315, 316, 317, 317, 319, 319,

320, 320 occipital bun of, 309, 315, 319, 321 robustness of, 314, 327 Shanidar, 315, 316, 317, 325, 328 skeletons of, 307, 308, 314, 315, 316, 316, 317,

319, 319, 324–25, 325, 336–37 skull of, 307, 318, 318, 319, 319, 320, 328,

334, 349 speech ability of, 321, 325–27, 326, 327, 348 symbolism used by, 327, 335 teeth of, 314, 315, 316, 317, 317, 324,

326–27, 327 tool use and technology of, 322, 323 violence of, 360

Neander Valley (Germany), 307 Necator americanus, 373 Necrolemur, 236 Neel, James V., 125 Negroid (African) race, 101 Neolithic Demographic Transition, 360 Neolithic period, 353, 378 Neolithic tools, 200 neonatal deaths, 105 neonatal period, 105, 111 Netherlands, 123 Newfoundland, 94 New Guinea, 6, 338, 338, 342, 342, 343,

343, 356, 358 New South Wales, 343 New World higher primates, see platyrrhines

(New World higher primates) New World monkeys, see ceboids

(New World monkeys) Ngandong, Java, 312, 312 Ni, Xijun, 225 niacin (vitamin B3), 372 Nile Valley, 330, 363 Nilotic, 322 nocturnal adaptation, 141, 236 noncoding DNA, 60, 78 nondisjunctions, 54

A60 Index

nonheme iron, 373 nonhoning canine teeth, 10–11, 12 nonhoning chewing, 8, 10–11, 12, 248, 248,

250, 250–51, 251, 252 nonmelanic form, 82, 82–84, 83, 84 nonmineralized bone, 107 non-radiometric dating, 205, 205–7, 206, 207 nonsynonymous point mutations, 78 North America

agriculture in, 356, 358, 359, 372 East Asian migrations to, 342, 342, 344,

346, 348 native populations of, see Native Americans

Notharctus, 221 Nsungwepithecus gunnelli, 230 Nubia, 363 Nubians, 363, 364, 375 nuchal crest, 159 nuclear DNA (nDNA), 46, 67, 338, 346 nucleoid region, 45 nucleotides, 49, 49, 51, 67, 346 nucleus, 44, 45, 45, 58 numerical (absolute) dating, see absolute

(numerical) dating nutrients, 56, 120–21, 121–22 nutrition

adaptation and, 120–26, 126, 129, 351, 353–55, 355

macronutrients and micronutrients in, 120–21, 121–22

overnutrition in, 123–26, 124, 126 undernutrition in, 121, 121, 123, 123,

126, 129 deficiencies in, 126, 129, 371–75, 372,

373, 374 height and, 108, 108, 109, 123, 123, 126–27 malnutrition, 121, 121, 123, 123–26, 124,

126, 129 prenatal, 105 see also diet

O Oase 2 skull, 332–33 obesity, 124–25, 129, 376 observation, 14, 14 occipital bun, 309, 315, 319, 321, 336 Oceania, 342 Ohio River Valley, 375 Okinawa, 332 Oldowan Complex, 270 Oldowan tools, 200, 273 Olduvai Gorge (Tanzania), 204, 244, 245–46,

246, 247, 270, 271, 274, 286, 287, 288, 292, 294, 298

Old World higher primates, see catarrhines (Old World higher primates)

Old World monkeys, see cercopithecoids (Old World monkeys)

Oligocene epoch, 193, 194 primates in, 227–30, 228, 229, 231, 236–37 temperature change in, 210, 211

oligopithecids, 228, 229 olive baboons, 156 olive colobus, 135, 136 Olorgesailie (Kenya), 298, 300, 300, 302 omnivores, 166

omomyids, 220–21, 222, 224, 225, 236, 241 On the Origin of Species (Darwin), 20, 32, 33,

34, 192, 283, 340 ontogenic (developmental) adaptation, 113 oocysts, 88 Oota, Hiroki, 95 opossums, 74, 155 opposable digits, 138, 138–40, 139, 249 orangutans, 132, 151, 152, 153, 157, 158, 175, 180

evolution of, 207, 219 fingernails of, 140 growth stages of, 146 residence patterns of, 168, 169 teeth of, 142, 144

Ordovician period, 193, 194 oreopithecids, 235, 235, 238, 239 Oreopithecus, 210, 210, 235, 235, 238 organelles, 44, 48 Orrorin tugenensis, 257, 258, 262, 263 orthodontics, 351, 352, 365, 378 osteoarthritis, 367–68, 369, 370 osteoblasts, 127 osteoclasts, 127 osteomalacia, 117 osteoporosis, 110, 110, 128, 376 Ouranopithecus, 238 Out-of-Africa evolutionary model, 310, 310,

335–36, 338, 338–39, 340, 348 overbite, 351, 352 overnutrition, 123–26, 124, 126 overweight, 124 ovum, 46, 46, 52, 105 oxygen deprivation, adaptation and, 118,

118–19, 120, 129 oxygen isotopes, 210

P Pääbo, Svante, 338 Pacific Islands, human migrations to, 342,

342, 343, 343–44, 345, 346 Pakistan, 184, 234 paleoanthropology, 9, 285 Paleocene epoch, 193, 194

primates in, 220, 221 temperatures in, 210

paleogenetics, 50, 54 Paleoindians, 346, 346, 347, 347 Paleolithic

Lower, 270 Middle, 322, 323 Upper, 198, 322, 329, 329, 330, 334

paleomagnetic dating, 206, 207, 208 paleontology, 8, 24, 25–26, 188

see also fossils/fossil record paleosols, 213 Paleozoic era, 194, 195 Pangaea, 194, 195, 195 parapithecids, 228, 229 Parapithecus, 229 parental investment, 135, 146, 146–47, 147,

148, 163 Paris Basin, 236 patella, 107 patriline, 52 patrilocal societies, 95 PCR (polymerase chain reaction), 50, 54

peas, Mendel’s experiments with, 34, 34, 36, 55, 72

pebble tools, 198, 200 Peking Man (Homo erectus), 297 pelvis, bipedalism and, 248, 249, 261, 266 penicillin, 376 Pennsylvania, Dunkers in, 92, 92–93 peppered moth, 82, 82–84, 83, 84 peptide bonds, 57, 59 periods, geologic, 193 periosteal reactions, 370, 370 Permian period, 193, 194 personal genomics, 104 Peruvian Andes, 116, 120 Peştera cu Oase, 332, 336 Petralona (Greece), 313, 314 phalanges, 262, 266, 267 Phanerozoic eon, 193 phenotypes, 36, 63, 63–99

pleiotropic genes and, 65, 66, 66, 67, 68 polygenic traits in, 65, 66, 66, 68

phenylketonuria, 66 photosynthesis, 211–12 phylogeny, 148, 152–53, 188, 209, 264 physical anthropologists, 4, 5, 7–8, 9, 16, 19 physical anthropology, 3–16, 17

definition of, 5, 6, 16 as interdisciplinary science, 8, 16 see also forensic anthropology

physiological (acclimatization) adaptation, 113 Pickford, Martin, 257 pigmentation, skin, see skin color pig molars, fossil, 198, 199 Pilbeam, David, 235 Piperata, Barbara, 108 Pithecanthropus, 283, 344 Pithecanthropus erectus “Java Man,” 284–85,

285 see also Homo erectus

PKU allele, 66 plant remains, chemistry of, 211–12, 212 plants, domestication of, see agriculture plasma membrane, see cell membrane (wall) Plasmodium falciparum, 88 platyrrhines (New World higher primates),

149, 150, 155, 155 evolution of, 229, 230, 230–31, 241

pleiotropy, 65, 66, 66, 67, 68 Pleistocene epoch, 193, 194, 197, 198

cercopithecoids in, 240–41 early modern Homo sapiens in, 329, 333,

334, 339 food acquisition in, 353 hominins in, 262, 279 human migrations in, 339–40, 342, 342–43,

343 late (Upper), 346, 353, 354, 360 Neandertals in, 337 temperature change in, 210–11 tools in, 198, 201

plesiadapiforms, 220, 221–22, 223, 224 Plesiadapis, 221 Pliocene epoch, 193, 194, 198, 212

cercopithecoids in, 240–41 hominins in, 257, 259, 262, 269, 279

point mutations, 78

Index A61

polarized light, 205 polio, 135 pollex (thumb), opposable, 138, 138–39 pollution, 82, 83, 84 Polo, Marco, 5, 102 polyandrous, 168 polygenic traits, 65, 66, 66, 68 polygynous, 168 polymerase chain reaction (PCR), 50, 54 polymorphisms, 61–65, 63, 64

balanced, 86 Polynesia, 342 polypeptides, 57 pongids (great apes), 157, 158, 180, 249

evolution of, 219, 238 taxonomy of, 151, 153

population density, 108 population genetics, 36, 71–99

definition of, 36 demes, reproductive isolation, and species in,

72–74, 73, 74, 75, 76 gene flow and, 93–94, 95, 96, 96, 97, 98 genetic drift and, 90–93, 91, 92, 93, 94, 98 Hardy-Weinberg law of equilibrium and, 76,

76–77, 77, 83 mutations and, 77–78, 79, 80, 80, 97–98 natural selection and, see natural selection

population growth, 341, 354–55, 360, 361, 369–71, 370, 371, 378, 379

populations endogamous, 92, 94 exogamous, 92, 94 living, 96, 101–30, 183

porotic hyperostosis, 374, 374 Portugal, 329, 333, 334 positive selection, 84 postmenopausal period, 112, 112 postnatal stage in human life history, 105,

106, 106–9, 107, 108, 109, 111, 129 postorbital bar, 220, 221 potassium-39, 204–5 potassium-40, 203, 204–5 potatoes, 358 pottery, 200, 351, 363 potto, 135, 136 Potwar Plateau, 184 power grip, 138, 138–39 preadaptation, 140 pre-australopithecines, 246, 256–59, 257,

258, 259, 260–61, 262, 262, 263, 264, 280

precision grip, 138, 138–39 Př edmostí skulls, 333 pregnancy, 105, 111, 125 prehensile tails, 155, 155 premolars

of early archaic Homo sapiens, 313 of primates, 137, 142, 142, 143, 143, 145, 146,

154, 155, 229 prenatal stage in human life history, 52,

52–53, 105, 111, 129 primates, 7

adaptation of, 133, 134, 136–37 arboreal, 132, 133, 135, 138, 138–41, 139,

140, 141, 142, 163, 210, 210, 218–19, 220, 229, 237

brain size of, 147, 147, 218, 227, 229, 235, 238 characteristics of, 133, 134, 135, 136–37, 162,

163, 218, 220, 227, 236 cooperation in, 170–72, 171 dental formula of, 142–43, 143 dietary plasticity of, 135, 137, 142, 142–43,

143, 144, 145, 145–46, 161, 163 diseases of, 135 distribution of, 134, 134 diversity of, 135, 138, 162, 163, 166–67 in Eocene, 187, 217–18, 220–22, 222, 223,

224, 225, 225–26, 226, 227–28, 228, 231, 236, 241

evolution of, 137, 192, 194, 214, 216, 217–42, 219, 227

eye orbits of, 141, 141, 220, 221, 222, 227, 235, 236

first true, 220–22, 222, 223, 224, 241 food acquisition by, 171, 172–73, 180, 181 grasping abilities of, 138, 138–39, 218,

219–20, 221, 222, 227, 236 grooming among, 167, 170, 170, 179, 179 growth stages of, 146, 147 hearing in, 141 intelligence of, 147, 147, 161 living, 133–63, 165–82 material culture of, 173, 173–75, 174, 175, 180,

181 in Miocene, 230, 231–32, 232, 233, 234, 234,

235, 235, 236, 238, 239, 240, 241, 242, 256

nails of, 140, 140, 218, 220, 221, 227 in Oligocene, 227–30, 228, 229, 231, 236–37 in Paleocene, 220, 221 parental investment of, 135, 146, 146–47, 147,

148, 163 reproduction strategies of, 169, 169–70, 170,

181, 182 residence patterns of, 168, 168–69, 182 skeletal structure of, 136, 138, 138–40, 139,

140, 142, 220 smell sense of, reduced, 137, 141, 153, 161,

218, 227 snout length of, 137, 141, 220, 222, 227 social organization of, 165, 166–72, 167, 168,

169, 170, 171, 181, 182 study of, 9, 134–35, 162 taxonomy of, 28, 29, 135, 148–62, 150–51, 162

cladistic vs. gradistic, 148–49, 149, 152–53, 153

haplorhines, 155, 155–60, 156, 157, 158, 159, 160, 161, 162

strepsirhines, 153–54, 154, 161 teeth of, 137, 142, 142–43, 143, 144, 145,

145–46, 220, 221, 223, 227, 235 touch in, enhanced sense of, 136, 140, 140,

142, 161 vision in, enhanced, 137, 141, 141, 142, 161,

219–20, 227 vocalizations of, 166, 175–80, 176, 177, 178,

179, 180, 181 primatologists, 133, 134 primatology, 9, 134–35, 162 primitive characteristics, 148 probability, genetic drift and, 91, 91–93 proboscis monkeys, 156

Proconsul, 232, 232, 233, 234, 237 proconsulids, 231, 232, 233, 234, 235, 239 Proconsul major, 232 prokaryotes, 44, 45, 45 prolonged childhood, 112 propliopithecids, 228, 229 Propliopithecus, 229, 237 proprimates, 220, 221, 222, 224 prosimians (Prosimii)

brain morphology of, 147 evolution of, 219, 236 taxonomy of, 149

protein gas transport, 56 mechanical, 56 regulatory, 56, 67 structural, 56, 56, 57 synthesis of, 44, 56, 56–57, 57, 58–59, 60,

60, 68 Proterozoic eon, 193, 194 provisioning hypothesis, 254–55 Pruetz, Jill, 174 Pseudoloris, 236 puberty, 105, 106, 106–7, 111 Punnett squares, 55, 76, 77 putty-nosed monkeys, 135, 136 Pygmies, 322

Q quadrupedalism, 158, 159, 160, 237, 248, 249,

254, 262 quality of life, 366, 366 Quechua Indians, 107, 113

R race concept, 96, 101

historical roots of, 101, 102, 102 as invalid, 101, 102, 102–4, 129

racemization, 206 rachis, 353 radiation, adaptive, 22, 239, 242 radiocarbon dating, 201, 203, 203, 204, 207,

208 radiometric dating, 198–99, 201, 201, 202,

203, 203, 204 radiopotassium dating, 203–5, 205, 208 radius, 107 Ray, John, 27, 27 recessive alleles, 34, 35, 35, 64, 76 recombination, 54 red colobus monkeys, 135, 136, 137, 138 regulatory genes, 60, 61, 61, 62 regulatory proteins, 56, 67 relative dating, 195–98, 201, 208, 209, 213

biostratigraphic dating and, 197–98, 199, 208 chemical dating and, 196–97, 197, 208 cultural dating and, 198, 200, 201, 208 stratigraphic correlation and, 196, 208

Relethford, John, 339, 341 remodeling, skeletal, 127, 127 replication of DNA, 48–49, 49, 51, 51–52, 68 representation, fossil record, 191–92 reproduction

competition and, 167, 167, 169, 170, 255 excessive workload and, 128 social organization and, 167

A62 Index

reproductive isolation, 72–73, 73 reproductive strategies of primates, 169,

169–70, 170, 181, 182 reproductive success, 81 reproductive system, human, 106, 106 residence patterns of primates, 168,

168–69, 182 rhinarium, 141, 148 Rhodesian Man, 312 ribonucleic acid (RNA), 56, 57 ribosomal RNA (rRNA), 57 ribosomes, 57, 58–59 rice, 350, 359, 360, 371, 372 rickets, 117, 117, 308 right-handedness, 326–27, 327 rigidity of bones, 127 ring-tailed lemurs, 153 Rio de Janiero, 370 RNA (ribonucleic acid), 56, 57 robusticity

of australopithecines, 274, 275 of early modern Homo sapiens, 330, 331,

332, 334 of Homo erectus, 302, 303, 304 of Neandertals, 314, 327

Rochers de Villeneuve (France), 336, 341 Rodman, Peter, 254 Romania, 332, 336, 336 Rosas, Antonio, 318 rRNA (ribosomal RNA), 57 Ruff, Christopher, 321, 367, 368–69 Rukwapithecus fleaglei, 230 Rukwa Rift Basin, 230 Rusinga Island (Kenya), 231, 232, 237 Russia, 336, 341, 342

S Saadanius, 229–30 sagittal crest, 159, 275, 275, 290, 363 sagittal keel, 295, 302 Sahara Desert, 257, 338 Sahelanthropus tchadensis, 257, 257, 262, 263 Salla (Bolivia), 230, 231 salmon, 376 Sambungmacan ( Java), 295, 296 Sangiran 17 fossil, 295, 296 Sangiran Homo erectus, 295, 296 Santa Catalina de Guale mission, 3–4 Saudi Arabia, 229, 231 Savage-Rumbaugh, Sue, 180 Schaafhausen, Hermann, 307, 308 Schaik, Carel van, 175 Science, 259, 259 scientific law, 15 scientific method, 14, 14–16, 15, 17 Scladina Cave (Belgium), 324, 324, 336 scratch patterns on teeth, hand preference

and, 326–27, 327 sea levels in late Pleistocene, 342, 342 Seckler, David, 123 sectorial premolar, 145, 146 secular trend, 108 sediment/sedimentary rock, 188, 190, 190 segregation, Mendel’s law of, 62, 64 Seiffert, Erik, 225 senescence, 105, 109–10, 110, 111, 129

Senut, Brigitte, 257 September 11, 2001, terrorist attacks, forensic

anthropologists and, 7, 63 Serengeti grasslands, 212, 212 sex chromosomes, 51, 51–52 sexual dimorphism, 106, 155, 156, 167, 167, 169,

221, 255 sexual maturity, 61, 106–8 sexual selection, 169 Seyfarth, Robert, 176, 179 Seysenegg, Erich Tschermak von, 36 Shaanxi Province (China), 296, 312 Shah, Ibrahim, 235 Shanghuang, 225 Shanidar Neandertals, 315, 316, 317, 325, 328 Shipman, Pat, 298 shivering, 116 shoulder joints, 268, 268 shovel-shaped incisors, 344, 345, 346 Shultz, Susanne, 171, 172 siamangs, 158, 169 Siberia, 327, 338, 346 sickle-cell anemia, 36–37, 84–85, 85, 86, 103

malaria and, 71, 72, 76, 86–87, 87, 88, 89 Sierra de Atapuerca, 296, 313 Silurian period, 193, 194 Sima de los Huesos cave (Spain), 313, 315,

326–27, 328 Simons, Elwyn, 225 single nucleotide polymorphisms (SNPs), 48,

49, 62, 346 sivapithecids, 234, 234, 235, 235, 239 Sivapithecus, 184, 234, 235, 238, 242 Siwalik Hills (India and Pakistan), 234 skeletons

of australopithecines, 266, 267, 268, 268, 270, 275, 278

of early archaic Homo sapiens, 315, 333 of Homo erectus, 290–91, 291 of Homo habilis, 287 of hunter-gatherers, 367, 368 Lagar Velho, 329, 333, 334 of modern humans, 126, 126–27, 249, 343,

344, 344, 345, 363, 364 of Neandertals, 307, 308, 314, 315, 316, 316,

317, 319, 319, 324–25, 325, 334, 336–37 of pre-australopithecines, 260 of primates, 136, 138, 138–40, 139, 140,

142, 220 of Tyrannosaurus rex, 187 see also bones

Skhul 5, 309, 331–32, 332 skin cancer, 117 skin color, 100, 102, 104

evolution and, 118, 129 solar radiation and, 113, 116, 116–17, 119

skin reflectance, 116 skulls

of Ardipithecus, 261 of Australopithecus aethiopicus, 275 of Australopithecus afarensis, 268, 268 of Australopithecus africanus, 278 of Australopithecus boisei, 275 of Australopithecus garhi, 270, 272 of Australopithecus robustus, 275, 275, 278 of Australopithecus sediba, 278

of early archaic Homo sapiens, 309, 312, 312, 313, 313, 314, 315

of early modern Homo sapiens, 329–30, 331, 332, 332–33, 333, 334, 335

of Homo erectus, 284, 285, 289, 290, 291, 292, 293, 293, 294, 295–96, 296, 297, 297, 298, 302, 303, 344

of Homo habilis, 286, 286, 287, 287 of Megaladapis, 154 of modern humans, 309, 343, 344, 363, 364 of Neandertals, 307, 318, 318, 319, 319, 320,

328, 349 porotic hyperostosis in, 374, 374 of Sivapithecus, 184, 234, 235 see also mandible

Slocombe, Katie, 178 sloth, 185 smell in primates, sense of, 137, 141, 153, 161,

218, 227 Smith, Fred, 340 Smith, Grafton Elliot, 218 Smith, William, 186 snout length, 137, 141, 220, 222, 225, 227 SNPs (single nucleotide polymorphisms), 48,

49, 62, 346 social learning, 13 social maturity, 108 social organization of primates, 165, 166–72,

167, 168, 169, 170, 171, 181, 182 sociolinguistics, 5 soft-shelled turtles, 187 soils, ancient (paleosols), 211–13, 212 solar radiation

folate protection and, 118 skin color and, 113, 116, 116–17, 119 vitamin D synthesis and, 117, 117–18

Solecki, Ralph, 316 solitary primates, 168, 169 Solomon Islands, 344 Solo River, 284 Solutrean culture, 329 Solutrean tools, 200 somatic cells, 46, 46, 48, 52, 52–53,

53, 54, 98 sooty mangabeys, 135, 136 sorghum, 356, 358 South Africa

australopithecines in, 256, 271, 273, 274–75, 278, 286, 290

Border Cave, 206 early modern Homo sapiens in, 330, 331 Homo habilis in, 286, 286, 288, 304 taphonomy of hominid remains in, 190, 190 Wonderwerk Cave, 300, 302

South America, 195, 195 agriculture in, 356, 358 civilization in, 360 human migrations to, 342, 342, 346 primates in, 230, 230–31 undernutrition in, 121

Southeast Asia land bridges in, 343 lorises in, 154

Spain American colonies of, 2, 3 Burgos, 313

Index A63

Spain (continued) early archaic Homo sapiens in, 313–14, 315,

326–27 early modern Homo sapiens in, 329, 329 El Sidron, 318, 324 Homo erectus in, 295, 296–97, 297, 298 Neandertal symbolism in, 327

species definition of, 22, 72 in taxonomy, 28, 29

speech as hominin characteristic, 8, 10, 12, 246–47 Neandertals and, 321, 325–27, 326, 327, 348

sperm, 46, 46, 52 SPF (sun protection factor), 117 spider monkeys, 155 spine, 249, 369 spontaneous mutations, 78, 80 sporozoites, 88 squash, 358 St. Catherines Island, Ga., 3–4, 16 St. Gaudens (France), 234 stabilizing selection, 81, 81 stable isotope analysis, 324, 324 Staphylococcus aureas, 370, 376 Steckel, Richard, 108 Steinheim (Germany), 313, 314 Steno’s law of superposition, 196, 208 Stensen, Niels (Steno), 195–96, 196, 199 Sterkfontein, 278 Stevens, Nancy, 230 Stewart, T. Dale, 316 strata, geologic, 24, 24, 186, 192, 196, 247 stratigraphic correlation, 196, 208 strepsirhines, 135, 138, 141, 143, 145, 148, 149,

149, 150, 153–54, 154, 161, 162, 169 Streptococcus mutans, 371 stress

environmental, 105, 108, 108–9, 129 heat, 114–15, 115, 119

stressors, 105 Strier, Karen, 172 Stringer, Christopher, 340 stromatolites, 187 structural genes, 60, 61 structural proteins, 56, 56, 57 Sudan, 363 Sulawesi, 342 Sumatra, 132, 175, 284, 284, 343 sumpweed, 357 sunburn, 117 Sunda shelf, 343 sunflowers, 356, 357, 358 sun protection factor (SPF), 117 superfoods, 360 superposition, Steno’s law of, 196, 208 survival, social organization and, 167, 167 Susman, Randall, 139, 272 suspensory locomotion, 158, 158, 238,

264, 266 Sussman, Robert, 220 Suwa, Gen, 238 Swamp Ape, see Oreopithecus Swanscombe, 313, 314 Swartkrans (South Africa), 275 Swartkrans Cave, 190

sweating, 114 sweet potatoes, 358 symbolism, 327, 335, 348 synonymous point mutations, 78 synthesis, protein, 44, 56, 56–57, 57, 58–59,

60, 60, 68 syphilis, 370 Systema Naturae (Linnaeus), 29 systematics, 24, 29 Szalay, Frederick, 224

T Tabun, 315, 316, 325 Taï Forest, 135, 136–37, 177, 179 tails, prehensile, 155, 155 Tam Pa Ling Cave, 332 Tang, Hua, 104 Tanganyika, Lake, 165 tanning, 113 Tanzania, 179, 179, 230, 256, 286

Gombe National Park in, 164, 165, 179 Laetoli, 190, 191, 266, 268, 269, 269 Olduvai Gorge in, 204, 244, 245–46,

246, 247, 270, 271, 274, 286, 287, 292, 294, 298

taphonomy, 188, 189, 190 taro, 358 tarsal (ankle) bones, 225, 234 tarsiers, 143, 143, 152, 222, 224–25, 225

taxonomy of, 149, 149, 150 Tasmania, 342, 342, 343 Taung cave (South Africa), 275 taxa, see genus; species taxonomy, 24, 26–27, 28, 29

of primates, 28, 29, 135, 148–62, 150–51, 162 cladistic vs. traditional, 148–49, 149 haplorhines, 155, 155–60, 156, 157, 158, 159,

160, 161, 162 strepsirhines, 153–54, 154, 161, 162

race and, 102, 102, 129 TDEE (total daily energy expenditure), 121 technology, 313

see also tools; tool use tectonic plates, 195, 238 teeth, 224, 235

of australopithecines, 265, 265, 268, 270, 270, 274–75, 278, 290

caries in, 371, 372 crowding of, 351, 352, 352 deciduous, 106, 106, 107, 107 of early archaic Homo sapiens, 309, 313–14,

315, 326–27 of early modern Homo sapiens, 329, 332,

334, 336 enamel thickness in, 146, 235, 251, 251,

373, 373 of Homo erectus, 284, 290, 296, 297, 299,

301–2, 304 of Homo habilis, 279, 286, 287, 299, 305 hypoplasias of, 373 malocclusion of, 351, 352, 352, 365, 365 of modern humans, 309, 344, 345, 346, 363,

365, 378 of Neandertals, 314, 315, 316, 317, 317, 324,

326–27, 327 of pre-australopithecines, 261

of primates, 137, 142, 142–43, 143, 144, 145, 145–46, 154, 155, 155, 220, 221, 223, 227, 235

see also canine-premolar complex; dental formula

temperature change, 210–11, 211, 224, 353, 354, 355, 378

temporalis muscle, 158, 159, 363 terrestrial, definition of, 15 Teshik Tash (Uzbekistan), 318, 336 tests, testing, 14 Thailand, 95, 235, 375 thalassemia, 89 theories, 14 thermoluminescence dating, 207, 207, 208 thermoregulation, 114, 115–16 Theropithecus oswaldi, 241 Thomas’s galagos, 136, 138 Thorne, Alan, 344 thumb (pollex), 138, 138–39, 272 thymine, 48 Tianyuan Cave, 332, 333 Tibetans, 120, 120 tibia, 107, 107, 297 timescale, geologic, 193, 193–95, 194, 195, 214 Tishkoff, Sarah, 89 Titanic disaster, 115 Tobias, Philip, 286 toe, big, see hallux (big toe) tools

Acheulian, 298, 300, 301 Folsom point, 346 Levallois, 322, 323 pebble, 198, 200 stone, 11, 12, 270, 271, 272, 273, 287–88,

289, 293, 295, 296, 297, 298, 300, 301, 322, 323

tool use by australopithecines, 270–72, 272,

273, 274, 288 by chimpanzees, 11, 12, 13, 166, 173,

173–75, 175 by early archaic Homo sapiens, 313, 315 by hominins, 8, 11, 12, 13, 252–53 by Homo erectus, 295, 296, 297, 298, 300, 301,

303, 304 by Homo habilis, 287–89, 288, 304 by Neandertals, 322, 323

tooth comb, 144, 145, 154, 224 Toros-Menalla (Chad), 256, 257 total daily energy expenditure (TDEE), 121 touch in primates, sense of, 136, 140, 140,

142, 161 towns, rise of, 358 traits, polygenic and pleiotropic, 66, 66, 68 transcription in protein synthesis, 56, 58,

60, 79 transfer RNA (tRNA), 57, 59 translation in protein synthesis, 56, 58–59, 60 translocations, 54 transposable elements, 78 tree-ring method of dating, see

dendrochronology treponematoses, 370, 371 Triassic period, 193, 194, 195 trilobites, 187

A64 Index

trimesters, 105, 111 Trinil ( Java), 284, 289, 295–96, 296 Trinkaus, Erik, 340 triplets, 57 trisomies, 54 tRNA (transfer RNA), 57, 59 tryptophan, 372 tuberculosis, 295, 371 Tungusae, 102 Turkana (people), 109 Turkana, Lake, 257, 265, 269, 274, 286, 288,

290 Turkana boy, see Nariokotome boy Turkey, 357, 357–58, 358 Turner, Christy, 344 turtles, 187 Twiggy, 286 type 2 diabetes, 125–26, 129 Tyrannosaurus rex skeleton, 187

U Uganda, 178, 231, 231 ulna, 107 ultraviolet (UV) radiation, 104, 116–17, 118,

119, 129 underbite, 351, 352 undernutrition, 121, 121, 123, 123, 129 UNESCO World Heritage Sites, 278, 297 uniformitarianism, 25, 32 United Nations, 376 United States, agriculture in, 357 Upper Paleolithic, 198, 322, 329, 329,

330, 334 uracil, 57 uranium-238, 205, 205 Ussher, James, 195 Utah, 24 UV (ultraviolet) radiation, 104, 116–17, 118,

119, 129 Uzbekistan, 318, 336

V Van Gerven, Dennis, 363, 364 variation

biocultural, see biocultural variation

environmental, 66, 66 see also genetic variation

vasoconstriction, 115–16 vasodilation, 114 vertebrae of primates, 140, 140 vervet monkeys, 156, 176, 179 Victoria, Lake, 232 victoriapithecids, 240 Victoriapithecus, 240 Vikings, 94 Vindija Cave (Croatia), 317, 317, 324, 327, 336,

338 violence, 360 Virchow, Rudolf, 308, 308, 319 Virginia, 185 vision in primates, 137, 141, 141, 142, 161,

219–20, 227 visual predation hypothesis, 219–20 vitamin A, 372 vitamin B3 (niacin), 372 vitamin D synthesis, 117, 117–18 vitamins, 122 vocalizations, 166, 175–80, 176, 177, 178, 179,

180, 181 affixation in, 178–79 of chimpanzees, 177, 178 food-associated, 178 predator-specific, 176, 176–78, 179

volcanic ash, 190, 191, 196, 199, 268–69 volcanic rock, 203–4, 247 Vries, Hugo de, 36

W Wadi Halfa, 330, 331 Wadi Kubbaniya, 330, 331 Walker, Alan, 265, 265 Wallace, Alfred Russel, 33, 33 Ward, Carol, 265 Washburn, Sherwood, 165 Watson, James, 37, 48 weaning, 106 Weidenreich, Franz, 296 weight

excess, 124, 124–25 low birth, 105

Weinberg, Wilhelm, 76 West Africa, 135, 136–37, 175, 177 West Africans, sickle-cell anemia in,

36–37, 76 Wexler, Nancy, 94 wheat, 350, 353, 356, 357, 358, 372 White, Tim, 199, 258, 260, 270, 286,

292, 318 Wilson, Edward O., 167 Wolff’s Law, 127, 352 Wolpoff, Milford, 303, 320, 340 Wonderwerk Cave, 300, 302 wood as fuel, 361 woolly monkeys, 155 woolly spider monkeys, 155, 155 workload

adaptation and, 126, 126–28, 127, 128, 130 agriculture and, 366, 366–69, 367, 368, 369,

370, 378 effect on bones of, 126, 126–27

World Health Organization, 124 World War II, human height and, 123, 123 Wrangham, Richard, 171, 300 Wright, Sewall, 71 Wyoming, 222

X X chromosome, 51, 51–52

Y yams, 358 Y chromosomes, 51–52, 95, 339 Y-5 molars, 144, 145, 152, 153, 158, 232

Z Zalmour, Iyad, 229 Zambia, 310, 312, 312 Zeder, Melinda, 354 Zhiren Cave, 332 Zhoukoudian (China), 282, 296, 296, 297,

301, 303, 332, 332, 333 Zhu, R. X., 296 Zilhão, João, 327 Zuberbühler, Klaus, 177, 178, 179 zygotes, 49, 52, 105

Index A65

  • Essentials of Physical Anthropology 3e
    • Half Title
    • Title Page
    • Copyright
    • Dedication
    • About the Author
    • Basic Table of Contents
    • Table of Contents
    • Two-Page Spreads
    • To the Instructor
    • To the Student���������������������
  • CHAPTER 1. What Is Physical Anthropology?
  • PART I. The Present: Foundation for the Past
    • CHAPTER 2. Evolution: Constructing a Fundamental Scientific Theory
    • CHAPTER 3. Genetics: Reproducing Life and Producing Variation
    • CHAPTER 4. Genes and Their Evolution: Population Genetics
    • CHAPTER 5. Biology in the Present: Living People
    • CHAPTER 6. Biology in the Present: The Other Living Primates
    • CHAPTER 7. Primate Sociality, Social Behavior, and Culture
  • PART II. The Past: Evidence for the Present
    • CHAPTER 8. Fossils and Their Place in Time and Nature
    • CHAPTER 9. Primate Origins and Evolution: The First 50 Million Years
    • CHAPTER 10. Early Hominin Origins and Evolution: The Roots of Humanity
    • CHAPTER 11. The Origins and Evolution of Early Homo
    • CHAPTER 12. The Origins, Evolution, and Dispersal of Modern People
    • CHAPTER 13. Our Last 10,000 Years: Agriculture, Population, Biology
  • Appendix: The Skeleton
  • Glossary
  • Glossary of Place Names
  • Bibliography
  • Permissions Acknowledgments
  • Index
    1. 2015-12-22T13:22:24+0000
    2. Preflight Ticket Signature