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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

W. W. Norton & Company has been independent since its founding in 1923, when William Warder Norton and Mary D. Herter Norton first published lectures delivered at the People’s Institute, the adult education divi- sion of New York City’s Cooper Union. The firm soon expanded its program beyond the Institute, publishing books by celebrated academics from America and abroad. By mid century, the two major pillars of Norton’s publishing program— trade books and college texts— were firmly established. In the 1950s, the Norton family transferred control of the company to its employees, and today— with a staff of four hundred and a compara- ble number of trade, college, and professional titles published each year— W. W. Norton & Company stands as the largest and oldest publishing house owned wholly by its employees.

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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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1 2 3 4 5 6 7 8 9 0

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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

E T H I O P I A

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

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

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? <