PRIMATE ORIGINS: ADAPTATIONSAND EVOLUTION

DEVELOPMENTS IN PRIMATOLOGY: PROGRESS AND PROSPECTSSeries Editor: Russell H. Tuttle, University of Chicago, Chicago, Illinois

This peer-reviewed book series melds the facts of organic diversity with the continuity ofthe evolutionary process. The volumes in this series exemplify the diversity of theoreticalperspectives and methodological approaches currently employed by primatologists andphysical anthropologists. Specific coverage includes: primate behavior in natural habitatsand captive settings; primate ecology and conservation; functional morphology anddevelopmental biology of primates; primate systematics; genetic and phenotypicdifferences among living primates; and paleoprimatology.

ANTHROPOID ORIGINS: NEW VISIONSEdited by Callum F. Ross and Richard F. Kay

MODERN MORPHOMETRICS IN PHYSICAL ANTHROPLOGYEdited by Dennis E. Slice

BEHAVIORAL FLEXIBILITY IN PRIMATES: CAUSES ANDCONSEQUENCESBy Clara B. Jones

NURSERY REARING OF NONHUMAN PRIMATES IN THE 21ST CENTURYEdited by Gene P. Sackett, Gerald C. Ruppenthal and Kate Elias

NEW PERSPECTIVES IN THE STUDY OF MESOAMERICANPRIMATES: DISTRIBUTION, ECOLOGY, BEHAVIOR, ANDCONSERVATIONEdited by Paul Garber, Alejandro Estrada, Mary Pavelka and LeAndra Luecke

HUMAN ORIGINS AND ENVIRONMENTAL BACKGROUNDSEdited by Hidemi Ishida, Russel H. Tuttle, Martin Pickford, Naomichi Ogiharaand Masato Nakatsukasa

PRIMATE BIOGEOGRAPHYEdited by Shawn M. Lehman and John Fleagle

REPRODUCTION AND FITNESS IN BABOONS: BEHAVIORAL,ECOLOGICAL, AND LIFE HISTORY PERSPECTIVESEdited By Larissa Swedell and Steven R. Leigh

RINGAILED LEMUR BIOLOGY: LEMUR CATTA INMADAGASCAR Edited by Alison Jolly, Robert W. Sussman, Naoki Koyama and Hantanirina Rasamimanana

PRIMATE ORIGINS: ADAPTATIONS AND EVOLUTION Edited by Matthew J. Ravosa and Marian Dagosto

LEMURS: ECOLOGY AND ADAPTATIONEdited by Lisa Gould and Michelle L. Sauther

PRIMATE ORIGINS:ADAPTATIONS ANDEVOLUTION

Edited by

Matthew J. Ravosa and Marian DagostoDepartment of Cell and Molecular BiologyFeinberg School of Medicine, Northwestern UniversityChicago, Illinois

Matthew J. Ravosa Marian DagostoDepartment of Cell and Department of Cell and Molecular Biology Molecular BiologyFeinberg School of Medicine, Feinberg School of Medicine,

Northwestern University Northwestern UniversityChicago, Illinois Chicago, Illinois

Library of Congress Control Number: 2005937517

ISBN 10: 0-387-30335-9ISBN 13: 978-0-387-30335-2

Printed on acid-free paper.

© 2007 Springer Science+Business Media, LLCAll rights reserved. This work may not be translated or copied in whole or in part without thewritten permission of the publisher (Springer Science+Business Media, LLC, 233 Spring Street,New York, NY 10013, USA), except for brief excerpts in connection with reviews or scholarlyanalysis. Use in connection with any form of information storage and retrieval, electronicadaptation, computer software, or by similar or dissimilar methodology now known or hereafterdeveloped is forbidden.The use in this publication of trade names, trademarks, service marks, and similar terms, even ifthey are not identified as such, is not to be taken as an expression of opinion as to whether ornot they are subject to proprietary rights.

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CONTENTS

Contributors xviiPreface xxiIntroductions for Sections I-IV xxv

PART I: SUPRAORDINAL RELATIONSHIPS OF PRIMATES AND THEIR TIME OF ORIGIN

1. A Molecular Classification for the Living Orders of PlacentalMammals and the Phylogenetic Placement of Primates 1Springer, M. S., Murphy, W. J., Eizirik, E., Madsen, O., Scally, M.,Douady, C. J., Teeling, E. C., Stanhope, M. J., de Jong, W. W., and O’Brien, S. J.Introduction 1Materials and Methods 4Results 5

Likelihood and Bayesian Analyses with the Full Data Set 5Analyses with Outgroup Jackknifing 12Analyses with the Nuclear Data Set 12Analyses with Subsets of Nuclear Genes 12Analyses with Mt rRNA Genes 13

Discussion 14Likelihood Versus Bayesian Results 14Early History of Placentalia 15Major Clades of Placental Mammals 17

Relationships in Afrotheria 18Relationships Within the Euarchontoglires Clade 18Relationships in Laurasiatheria 19

Molecular Classification for the Living Orders of Placental Mammals 19

Conclusions 22References 23

v

2. New Light on the Dates of Primate Origins and Divergence 29Soligo, C., Will, O. A., Tavaré, S., Marshall, C. R., and Martin, R. D. Introduction 29The Fossil Record 30The Molecular Evidence 35Quantifying the Incompleteness of the Fossil Record 37Preservational Bias in the Fossil Record 43Acknowledgments 46References 46

3. The Postcranial Morphology of Ptilocercus lowii(Scandentia, Tupaiidae) and its Implications for Primate Supraordinal Relationships 51Sargis, E. J.Introduction 51Taxonomy and Phylogeny of the Family Tupaiidae 52

Taxonomy 52Supraordinal Relationships of Tupaiids 53Significance of Ptilocercus 59

Materials and Methods 60Results 62Discussion 65Conclusions 67Acknowledgments 69References 75

4. Primate Origins: A Reappraisal of Historical Data Favoring Tupaiid Affinities 83Godinot, M.Introduction 83Limits of Cladistics Confronted with Large Data Sets 86Facing Primatomorpha 90

Are Paromomyid Dental Characters Compatible with Dermopteran Origins? 90

Dermopteran Incisors 92Paromomyid Postcranials, Gliding, and Apatemyid

Adaptations 95

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On Postcranial Characters and Archontan Phylogeny 97Skull Characters and Conclusion 100

The Plesiadapiform Radiation and Primate Ancestry 101Temporal and Geographical Extension 102

Plesiadapiform Dental Characters and Primate Origins 104Other Characters and Conclusion 108

Returning to Tupaiidae 112Important Tarsal Characters 116Conclusion: Tupaiids as Sister-Group of Primates 120

Remarks on Scenarios of the Acquisition of Nails 122Concluding Remarks 126

Fossils, Methods, and Primate Origins 126Primate Morphotype Locomotor Mode 129

Summary 131Acknowledgments 133References 133

5. Primate Taxonomy, Plesiadapiforms, and Approaches to Primate Origins 143Silcox, M. T. Introduction 143Background on Taxonomic Debates 145

Problems with Combining Cladistics and Linnean Taxonomy 145

Phylogenetic Taxonomy’s Solutions to the Problems Posed by Linnean Taxonomy 146

Other Taxonomic Priorities 150Previous Definitions and Diagnoses of Primates 151The Phylogenetic Position of Plesiadapiformes 155

Background 155A More Comprehensive Analysis 159Taxonomic Implications of the Current Analysis 163

Primate Taxonomy and the Study of Euprimate Origins 167Conclusions 169Acknowledgments 170References 171

Contents vii

PART II: ADAPTATIONS AND EVOLUTION OF THECRANIUM

6. Jaw-Muscle Function and the Origin of Primates 179Vinyard, C. J., Ravosa, M. J., Williams, S. H., Wall, C. E., Johnson, K. R., and Hylander, W. L. Introduction 179

Functional Morphology of the Primate Masticatory 180ApparatusInterpretations of the Masticatory Apparatus in the

First Primates 192Tree shrew Feeding Ecology and Jaw Morphology—

A Reasonable Early Primate Model? 196Materials and Methods 197

Jaw-Muscle EMG 197Comparative Primate EMG Data 202

Results 203Treeshrew EMG 203Comparison of Treeshrew and Primate EMG 206

Discussion 209Jaw-Muscle EMG and Jaw Morphology in Treeshrews

and Primates 209Jaw-Muscle EMG and the Conservation of Primate

Masticatory Behaviors 213Mastication in the First Primates: In vivo Evidence

from Treeshrews and Primates 217Conclusions 219Acknowledgments 219References 220

7. Were Basal Primates Nocturnal? Evidence From Eye and Orbit Shape 233Ross, C. F., Hall, M. I., and Heesy, C. P. Introduction 233Orbital Convergence 235Orbit Size and Shape 237Reconstructions of Orbit Size and Shape in Basal Primates 240Materials and Methods 241

Eye Shape Measures 241

viii Contents

Orbit Shape Measures 241Results 242

Eye Size and Shape 242Orbit Size and Shape 246

Discussion 248The Eyes of Basal Primates 248The Eyes of Haplorhines 251

Conclusions 252Acknowledgments 252References 253

8. Oculomotor Stability and the Functions of the Postorbital Bar and Septum 257Heesy, C. P., Ross, C. F., and Demes, B.Introduction 257

Neurological and Morphological Maintenance of Eye Position 260What Are the Consequences of Disruption of Oculomotor

Coordination? 263Focus of This Study 266

Methods 267Results 268Discussion and Conclusions 271

Discussion of the Ocular Kinematic Results 271Oculomotor Stability and the Function of the Postorbital Bar 272Oculomotor Stability and the Function of the Haplorhine

Septum 275Summary 276Acknowledgments 277References 277

9. Primate Origins and the Function of the Circumorbital Region: What’s Load Got to Do with It? 285Ravosa, M. J., Savakova, D. G., Johnson, K. R., and Hylander, W. L.Introduction 285Masticatory Stress and Circumorbital Form 286

Galago Circumorbital Peak-Strain Magnitudes 289Galago Circumorbital Principal-Strain Directions 293Facial Torsion and the Evolution of the Primate Postorbital Bar 294

Contents ix

Nocturnal Visual Predation and Circumorbital Form 298Orbital Form and Patterns of Covariation 301Nocturnal Visual Predation and the Evolution of Orbit

Orientation and the Postorbital Bar 307Phylogenetic Evidence Regarding the NVPH and the

Evolution of Circumorbital Form 316Conclusions 317Acknowledgments 320References 320

PART III: ADAPTATIONS AND EVOLUTION OF THEPOSTCRANIUM

10. Origins of Grasping and Locomotor Adaptations in Primates: Comparative and Experimental Approaches Using an Opossum Model 329Lemelin, P. and Schmitt, D. Introduction 329Models of Primate Origins: A Review 331Convergence between Opossums and Primates: Comparative

Studies 334A Review of Didelphid and Cheirogaleid Ecology and Behavior 335

Substrate Use and Cheiridial Morphology: A Functional Model 339Morphometric Results 341Performance Results 346

Convergence between Opossums and Primates: Experimental Studies 351

Materials and Methods 353Gait Patterns 356Arm Protraction 359Vertical Force Distribution on Limbs 362

Discussion and Conclusions 363Acknowledgments 368References 369

11. Evolvability, Limb Morphology, and Primate Origins 381Hamrick, M. W.Introduction 381Theoretical Criteria for Evolvability 383

x Contents

Evidence for Evolvability in the Autopod 385Primate Origins: Role of Autopod Evolution 389Discussion 393Acknowledgments 396References 396

12. Primate Gaits and Primate Origins 403Cartmill, M., Lemelin, P., and Schmitt, D. Peculiarities of Primate Gaits 403Problems of DS Walks 406DS Walking and Arboreal Locomotion 415Duty-Factor Ratios and Diagonality 420DS Gaits: Fine Branches vs. Flat Surfaces 421Locomotion and the Ancestral Primates 422Conclusions 427Acknowledgments 430References 430

13. Morphological Correlates of Forelimb Protraction in Quadrupedal Primates 437Larson, S. G.Introduction 437Methods 438Results 442Discussion 448Acknowledgments 452References 452

14. Ancestral Locomotor Modes, Placental Mammals, and the Origin of Euprimates: Lessons From History 457Szalay, F. S.Introduction 457Glimpses of History of Researches Regarding Archontan,

Plesiadapiform, and Euprimate Morphotype Locomotor Strategies, and their Influence 459

Arboreality as a Novel Strategy for the Stem of Archonta 461Visual Predation as the Strategy for the Stem Lineage

of Euprimates 461

Contents xi

The Role of Leaping in the Ancestral Euprimate 466Models and the Locomotor Strategies of Extinct Taxa 473Homology in Evolutionary Morphology 478Transitions Leading up to the Archontan and Euprimate

Locomotor Strategies and Substrate Preference 481Locomotion, and the Origins of Euprimates 482Acknowledgments 483References 483

15. The Postcranial Morphotype of Primates 489Dagosto, M.Introduction 489Reconstructing Function and Biological Roles 495Derived Features of the MRCA 499

Features Related to Grasping 500Beyond Grasping and “Small Branches” 503Features Related to Leaping 506

Do the Functional/Biological Role Attributes of the Traits as a Whole Constitute a Cohesive Story? 517

Are the Biological Roles of Features Misidentified? 518Are these Features Part of the Primate Morphotype? 521Origin of Primates as a Process Not an Event 522

Acknowledgments 525References 525

16. New Skeletons of Paleocene-Eocene Plesiadapiformes: A Diversity of Arboreal Positional Behaviors in Early Primates 535Bloch, J. I. and Boyer, D. M. Introduction 535Clarks Fork Basin Fossiliferous Freshwater Limestones 537

Documenting Postcranial-Dental Associations 538Micromomyid Skeleton: An Example from a Late Paleocene

Limestone 539Newly Discovered Plesiadapiform Skeletons 541

Postcranial Morphology and Inferred Positional Behaviors 541Plesiadapifoms as Claw-Climbing Arborealists 541Plesiadapiform Specializations: A Diversity of Arboreal

Behaviors 553

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Paromomyidae 553Carpolestidae 557Plesiadapidae 562Micromomyidae 563

Phylogenetic Implications: Primate Origins and Adaptations 566

Acknowledgments 572References 573

PART IV: ADAPTATIONS AND EVOLUTION OF THE BRAIN, BEHAVIOR, PHYSIOLOGY, AND ECOLOGY

17. Start Small and Live Slow: Encephalization, Body Size, and Life History Strategies in Primate Origins and Evolution 583Shea, B. T.Introduction 583Relative Brain Size in Primates 585

Encephalization in Extant Primates 588Encephalization in Extinct Primates 590

Precociality and Encephalization in Primate Evolution 593Reproductive Strategies and Primate Evolution 593Encephalization and Precociality 600

Precociality, Encephalization and Small Body Size in Early Primate Evolution 601

Selection for Precociality in Early Primates 604Scaling Principles and Subsequent Primate Evolution 608Primates and Other Mammals 611Summary 614Acknowledgments 617References 617

18. Evolutionary Specializations of Primate Brain Systems 625Preuss, T. M.Introduction 625Specializations of The Visual System 627

Overview 627Retinotectal Organization 632

Contents xiii

Blobs 636The Critical Role of V1 in Primate Vision 639Dorsal and Ventral Visual Processing Streams and

Their Termini in Higher-Order Parietal and Temporal Cortex 640

Specializations of Frontal Cortex 645Dorsolateral Prefrontal Cortex 645Premotor Cortex 650

Specializations of Limbic Cortex 652Dorsal Pulvinar and Related Cortical Networks 653

Specializations of Corticotectal Organization 656Primate Superior Colliculus in Attention and Action 657Conclusions 658Acknowledgment 664References 664

19. New Views on the Origin of Primate Social Organization 667Müller, A. E., Soligo, C., and Thalmann, U. Introduction 667Definition of Social Organization and Sociality 679Origin and Evolution of Primate Social Organization 680

Inferences from Strepsirrhine Primates 681Inferences from “primitive” Mammals 684Reconstruction of the Ancestral Pattern of Primate Social

Organization 685Causes for Sociality in Primates 686

Ecological Factors and Sociality in Rodents 687Body Size 691Diet 691

Conclusions 692Acknowledgments 693References 693

20. Primate Bioenergetics: An Evolutionary Perspective 703Snodgrass, J. J., Leonard, W. R., and Robertson, M. L. Introduction 703Sample and Methods 704

xiv Contents

Results 710Metabolic Variation in Strepsirrhines and Haplorhines 710Ecological Correlates of Strepsirrhine Hypometabolism 711Metabolic Variation and Body Composition 712Phylogenetic Influences on Strepsirrhine Hypometabolism:

Comparative Metabolic Data 713Phylogenetic Influences on Strepsirrhine Hypometabolism:

Implications for Subfossil Lemurs 715Discussion 718

Ecological Correlates of Primate Metabolic Variation 718Phylogenetic Influence on Primate Metabolic Variation 721Body Composition and Primate Metabolic Variation 724Implications for Models of Primate Origins 725

Acknowledgments 730References 730

21. Episodic Molecular Evolution of Some Protein Hormones in Primates and Its Implications for Primate Adaptation 739Yi, S. and Li, W.-H. Introduction 739Molecular Evolution of Lysozyme: An Example of Adaptive

Evolution 742Evolution of Lysozymes in Colobine Monkeys 742Statistical Analyses to Detect Positive Selection in Lysozyme

Sequences 743Evolution of Growth Hormone and its Receptor 746

GH and GHR as a Model System of Coevolution 746Biology of GH and GHR and their Interactions 747Gene Duplications Leading to Multiple GH-Related Loci in

Primates 748Episodic Molecular Evolution of GH in Mammals 749Test of Positive Selection in DNA Sequences of Primate GHs

and GHRs 750A Case Study of Functional Evolution—the Emergence of

Species Specificity 753Evolution of Chorionic Gonadotropin in Primates 755

Hormonal Regulation of Primate Reproduction and Role of CG 755Molecular Structure and Origin of CG 756

Contents xv

Evolution of Placental Expression of the CGα-Subunit Gene in Primates 757

Number of Gene Copies and Episodic Molecular Evolution of CGβ-Subunit Genes in Primates 759

Summary of Molecular Evolutionary Events in the Evolution of CG in Primates 761

Episodic Evolution of Other Protein Hormones 762Conclusions 767References 768

22. Parallelisms Among Primates and Possums 775Rasmussen, D. T. and Sussman, R. W. Introduction 775Overview of Phalangeroid Phylogeny 777Miniature Flower Specialists 780Small-Bodied Omnivores 786Larger-Bodied Folivores 789Critical Primate Adaptations 793Parallelism and Primitiveness 795References 798

23. Perspectives on Primate Color Vision 805Lucas, P. W., Dominy, N. J., Osorio, D., Peterson-Pereira, W., Riba-Hernandez, P., Solis-Madrigal, S., Stoner, K. E., and Yamashita, N. Introduction 805Vision 806

In Color 806In Black and White 808

Texture 809Taste 812Early Primate Evolution 813Future Research 815References 816

Taxon Index 821

xvi Contents

CONTRIBUTORS

Jonathan I. Bloch, Florida Museum of Natural History, University ofFlorida, Gainesville, FL 32611-7800

Douglas M. Boyer, Department of Anatomical Sciences, Stony BrookUniversity, Stony Brook, NY 11794-8081

Matt Cartmill, Department of Biological Anthropology and Anatomy,Duke University Medical Center, Durham, NC 27710

Marian Dagosto, Department of Cell and Molecular Biology,Northwestern University Feinberg School of Medicine, Chicago, IL60611-3008, and Department of Zoology/Mammals Division, FieldMuseum of Natural History, Chicago, IL 60605-2496

Wilfried W. deJong, Department of Biochemistry, University of Nijmegen,Netherlands

Brigitte Demes, Department of Anatomical Sciences, Health SciencesCenter, Stony Brook University, Stony Brook, NY 11794-8081

Nathaniel J. Dominy, Department of Anthropology, University ofCalifornia, Santa Cruz, CA 95064

Christophe J. Douady, Department of Biology, University of California,Riverside, CA 92521, and Department of Biochemistry and MolecularBiology, Dalhousie University, Halifax B3H 4H7, Canada

Eduardo Eizirik, Laboratory of Genomic Diversity, National CancerInstitute, Frederick, MD 21702

Marc Godinot, Ecole Pratique des Hautes Etudes, and Paléontologie,Muséum National d’Histoire Naturelle, Paris, France 61801

Margaret I. Hall, Department of Anatomical Sciences, Stony BrookUniversity, Stony Brook, NY 11794-8081

Mark W. Hamrick, Department of Cellular Biology and Anatomy, MedicalCollege of Georgia, Augusta, GA 30912

xvii

Christopher P. Heesy, Department of Anatomy, New York College ofOsteopathic Medicine, Old Westbury, NY 11568

William L. Hylander, Department of Biological Anthropology and Anatomy,Duke University Medical Center, and Duke Primate Center, Durham, NC27710

Kirk R. Johnson, Department of Biological Anthropology and Anatomy,Duke University Medical Center, Durham, NC 27710

Susan G. Larson, Department of Anatomical Sciences, Health SciencesCenter, Stony Brook University, Stony Brook, NY 11794-8081

Pierre Lemelin, Division of Anatomy, Faculty of Medicine and Dentistry,University of Alberta, Edmonton T6G 2H7, Canada

William R. Leonard, Department of Anthropology, NorthwesternUniversity, Evanston, IL 60208

Wen-Hsiung Li, Department of Ecology and Evolution, University ofChicago, Chicago, IL 60637

Peter W. Lucas, Department of Anthropology, George WashingtonUniversity, Washington DC 20037

Ole Madsen, Department of Biochemistry, University of Nijmegen,Netherlands

Charles R. Marshall, Department of Earth and Planetary Sciences,Harvard University, Cambridge, MA 02138

Robert D. Martin, Department of Anthropology and Office of AcademicAffairs, Field Museum of Natural History, Chicago, IL 60605-2496

Alexandra E. Mueller, Anthropologisches Institüt und Museum,University of Zurich, 8057 Zurich, Switzerland

William J. Murphy, Laboratory of Genomic Diversity, National CancerInstitute, Frederick, MD 21702

Stephen J. O’Brien, Laboratory of Genomic Diversity, National CancerInstitute, Frederick, MD 21702

Daniel Osorio, School of Biological Sciences, University of Sussex,Brighton BN1 9QG, UK

Wanda Peterson-Pereira, Escuela de Biologia, Universidad de Costa Rica,San Pedro, San José, Costa Rica

xviii Contributors

Todd M. Preuss, Yerkes Primate Research Center, Emory University,Atlanta, GA 30329

D. Tab Rasmussen, Department of Anthropology, Washington University,Saint Louis, MO 63130

Matthew J. Ravosa, Department of Cell and Molecular Biology,Northwestern University Feinberg School of Medicine, Chicago, IL60611-3008, and Department of Zoology/Mammals Division, FieldMuseum of Natural History, Chicago, IL 60605-2496

Pablo Riba-Hernandez, Escuela de Biologia, Universidad de Costa Rica,San Pedro, San José, Costa Rica

Marcia L. Robertson, Department of Anthropology, NorthwesternUniversity, Evanston, IL 60208

Callum F. Ross, Department of Organismal Biology and Anatomy,University of Chicago, Chicago, IL 60637

Eric J. Sargis, Department of Anthropology, Yale University, New Haven,CT 06520

Denitsa G. Savakova, Department of Cell and Molecular Biology,Northwestern University Feinberg School of Medicine, Chicago, IL60611-3008

Mark Scally, Department of Biology, University of California, Riverside,CA 92521, and Queen’s University of Belfast, Department of Biology andBiochemistry, Belfast, UK

Daniel Schmitt, Department of Biological Anthropology and Anatomy,Duke University Medical Center, Durham, NC 27710

Brian T. Shea, Department of Cell and Molecular Biology, NorthwesternUniversity Feinberg School of Medicine, Chicago, IL 60611-3008

Mary T. Silcox, Department of Anthropology, University of Winnipeg,Winnipeg, MB R3B 2E9, Canada

J. Josh Snodgrass, Department of Anthropology, University of Oregon,Eugene, OR 97403

Christophe Soligo, Human Origins Programme, Department ofPalaeontology, Natural History Museum, London SW7 5BD, UK

Silvia Solis-Madrigal, Escuela de Biologia, Universidad de Costa Rica, SanPedro, San José, Costa Rica

Contributors xix

Mark S. Springer, Department of Biology, University of California,Riverside, CA 92521

Michael J. Stanhope, Queen’s University of Belfast, Department ofBiology and Biochemistry, Belfast, UK, and Bioinformatics,GlaxoSmithKline, Collegeville, PA 19426

Kathryn E. Stoner, Centro de Investigaciones en Ecosistemas, UniversidadNacional Autónoma de México, Morelia, Michoacán 58089, México

Robert W. Sussman, Department of Anthropology, Washington University,Saint Louis, MO 63130

Frederick S. Szalay, Departments of Anthropology, and Ecology andEvolutionary Biology, City University of New York, New York, NY 10021

Simon Tavaré, Program in Molecular and Computational Biology,University of Southern California, Los Angeles, CA 90089-1340

Emma C. Teeling, Department of Biology, University of California,Riverside, CA 92521, and Laboratory of Genomic Diversity, NationalCancer Institute, Frederick, MD 21702

Urs Thalmann, Anthropologisches Institüt und Museum, University ofZurich, 8057 Zurich, Switzerland

Christopher J. Vinyard, Department of Anatomy, Northeastern OhioUniversities College of Medicine, Rootstown, OH 44272

Christine E. Wall, Department of Biological Anthropology and Anatomy,Duke University Medical Center, Durham, NC 27710

Oliver A. Will, Department of Statistics, University of Washington, Seattle,WA 98195-4322

Susan H. Williams, Department of Biomedical Sciences, Ohio University,Athens, OH 45701

Nayuta Yamashita, Department of Cell and Neurobiology, Keck School ofMedicine, University of Southern California, Los Angeles, CA 90089-9112

Soojin Yi, Department of Ecology and Evolution, University of Chicago,Chicago, IL 60637

xx Contributors

PREFACE

Primates of modern aspect are characterized by several traits of the skull andpostcranium, most notably increased encephalization, olfactory reduction,postorbital bars, larger and more convergent orbits, an opposable hallux, andnails instead of claws on the digits. When, where, how, and why a group ofmammals with this distinctive morphology emerged continues to capture theinterest of biologists. The past 15 years have witnessed the discovery of numer-ous well-preserved basal forms and sister taxa from the Paleocene and Eoceneof Asia, Africa, North America, and Europe. These new findings are particu-larly fascinating because they extend the antiquity of several higher-levelclades, greatly increase our understanding of the taxonomic diversity of thefirst Primates, and document a far greater spectrum of variation in skeletalform and body size than noted previously. Not surprisingly, the past decadealso has witnessed molecular and paleontological attempts to resolve primatesupraordinal relationships. Many of our current notions about the adapta-tions of the first primates, however, are based on research performed 20–35years ago—a period when the fossil record was much less complete. Forinstance, there remains considerable debate over the leaping versusquadrupedal component of early primate locomotion, as well as differingviews regarding the function of certain mandibular and circumorbital featuresin basal primates. Indeed, the absence of a forum for the integration of past,recent, and ongoing research on the origin of primates has greatly hindereda better understanding of the significance of marked anatomical and behav-ioral transformations during this important and interesting stage of primateevolution. Accordingly, our December 2001 conference and this accompany-ing edited volume on Primate Origins and Adaptations capitalize on anincreasing amount of independent museum, field and laboratory-basedresearch on many important outstanding problems surrounding the adaptivesynapomorphies of the earliest primates. Moreover, it couples the emergingviews of junior researchers with those who have made significant contribu-tions to the study of early primate phylogeny over the past three decades.

xxi

Due to the evident need for a reassessment of primate origins and adapta-tions, there were two principal goals of our conference and volume. First, weaim to provide a broad focus on adaptive explanations for locomotor and pos-tural patterns, craniofacial form, neuro-visual specializations, life history pat-terns, socioecology, metabolism, and biogeography in basal primates. Second,to offer an explicit evolutionary context for the analysis of major adaptivetransformations, we aim to provide a detailed morphological and molecularreview of the phylogenetic affinities of basal primates relative to later primateclades, as well as other mammalian orders. As Plesiadapiformes have figuredso heavily in discussions of primate origins, this, and the focus of our volumeon adaptive scenarios, helps to explain the overt emphasis on the evolution ofanatomical features. Therefore, in addition to strictly systematic or paleonto-logical questions regarding primate origins, we concentrate primarily on theadaptive importance of unique primate characters via a comprehensive con-sideration of anatomical, behavioral, experimental, and ecological investiga-tions of primate and nonprimate mammals. In this regard, a phylogeneticframework is critical for detailing the functional and evolutionary significanceof specific character states and morphological complexes. Given ongoingdebate regarding the appropriate content of the taxon Primates, we havedecided to let authors use the terms Primates and Euprimates as they see fit.The meaning is usually obvious from the context. Likewise, for the tooth-combed lemurs, we have let authors use the spelling Strepsirrhini orStrepsirhini as they choose.

Since an increasingly evident fact about the earliest primates is their verydiminutive body size, another important related goal is to characterize thoseadaptive trends, morphological features, and behaviors which vary and covaryallometrically. Obviously, this has figured heavily in certain explanations for theevolution of grasping appendages in small-bodied basal primates. In addition,the negative allometry of neural and orbital size, coupled with relatively largerconvergent orbits, has important structural consequences for explainingincreased orbital frontation and the correlated evolution of a postorbital bar atsmall skull sizes. Perhaps the most important contribution of our volume tobioanthropology and paleontology is that it develops a forum for evaluating pastand current research on primate origins. In doing so, we directly address a seriesof competing long-standing scenarios regarding the adaptive significance ofimportant primate synapomorphies. By examining hypotheses that have domi-nated our notions regarding early primate evolution and coupling this with an

xxii Preface

emergent body of novel evidence due to fossil discoveries, as well as technolog-ical and methodological advances, our edited volume will provide a long over-due multidisciplinary reanalysis of a suite of derived life history, socioecological,neural, visual, circumorbital, locomotor, postural, and masticatory specializa-tions of the first primates. This integrative neontological and paleontologicalperspective is critical for understanding major behavioral and morphologicaltransformations during the later evolution of higher primate clades.

This volume collects a wide-ranging series of contributions by expertsactively performing novel research relevant to the adaptive synapomorphies ofthe Order Primates. The authors and original conference participants areidentical due to the enthusiastic response of each. For this reason, we gathertogether virtually every researcher, or one of their former graduate students,currently performing important research relevant to primate origins andadaptations. The series of chapters are divided into the following sections:The Supraordinal Relationships of Primates and Their Time of Origin;Adaptations and Evolution of the Cranium; Adaptations and Evolution of thePostcranium; Adaptations and Evolution of the Brain, Behavior, Physiology,and Ecology. The contents of each chapter are briefly as follows:

Springer et al. address the molecular data regarding primate supra- andinfraordinal affinities. Soligo et al. reassess the antiquity and biogeography ofprimates and related mammals. Sargis considers the implications of tree shrewpostcranial morphology for understanding early primate phylogeny. Godinotsimilarly stresses the importance of tree shrews for understanding primate ori-gins. Silcox reexamines the fossil evidence regarding primate–plesiadapiformaffinities. Ross et al. examine the evidence for activity patterns of earlyPrimates. Ravosa et al. and Heesy et al. discuss comparative and experimentaldata regarding circumorbital form and function in primates and other verte-brates. Vinyard et al. integrate novel in vivo and morphological evidenceregarding masticatory form and function in archontans and primates. Lemelinand Schmitt provide novel information about cheiridial morphology and per-formance in a series of primate and nonprimate mammals. Hamrick discussesthe basis of evolvability of the mammalian autopod with special reference to theevolution of digital proportions in primates. Cartmill et al. consider the nov-elty and significance of primate diagonal gaits among mammals. Larson exam-ines kinematic and skeletal evidence regarding forelimb adaptations unique toprimates. Bloch and Boyer discuss the important implications of previouslyunknown North American plesiadapiform postcrania for understanding the

Preface xxiii

evolution of basal primate locomotor adaptations. Szalay reviews the philos-ophy of model construction in primate locomotor evolution. Dagosto con-siders the evidence regarding locomotor adaptations of ancestral primates.Shea investigates the evolution of encephalization in archontans vis-à-vis lifehistory, ecological, and allometric factors. Preuss employs neuroanatomicaldata to provide insight into neural specializations of the primate visual system.Mueller et al. employ a systematic analysis of extant primates to consider theevolution of basal primate social systems. Snodgrass et al. review the evolu-tionary and adaptive significance of variation in metabolic rate in the evolu-tion of brain size. Yi and Li evaluate examples of protein evolution duringprimate evolution. Sussman and Rasmussen review the ecological underpin-nings of early primate adaptations in marsupial analogs. Lucas et al. analyzethe relation between dietary evolution and color vision. Apart from a consid-eration of new fossil discoveries and their direct relevance to outstandingissues regarding the evolution of the locomotor apparatus in early primates,these presentations represent a significant increase in the wealth of kinematicand developmental data aimed at the question of primate origins.

Numerous individuals and institutions have contributed greatly to the suc-cess of our conference and this accompanying edited volume. On the publish-ing end, the following at Springer/Kluwer are thanked for their support,diligence, and patience—Andrea Macaluso, Krista Zimmer, Joanne Tracey, aswell as the series editor Russ Tuttle (University of Chicago). Our internationalconference benefited significantly from the financial support of the Wenner-Gren Foundation for Anthropological Research, Physical AnthropologyProgram of the National Science Foundation, Field Museum of NaturalHistory (especially the Mammals Division), and Department of Cell andMolecular Biology at Northwestern University Feinberg School of Medicine.The following individuals are singled out for providing unique assistance withthe organization and implementation of our conference—Bill Stanley, BrucePatterson, Larry Heaney, Bob Martin, Bob Goldman, and Gail Rosenbloom.The following graduate students offered technical and logistical help thatensured the symposium went off without a hitch—Aaron Hogue, KristinWright, Barth Wright, and Kellie Heckman. Lastly, and most importantly, wethank our spouses—Sharon Stack and Dan Gebo—for their continued supportand our respective children—Nico and Luca, and Anne Marie—for inspiration.

Matthew J. RavosaMarian Dagosto

xxiv Preface

INTRODUCTIONS FOR SECTIONS I–IV

Section I: Supraordinal Relationships of Primates and Their Time of Origin

Despite new fossil discoveries, new sources of data, and new methods ofanalysis, several important issues concerning the origin and phylogenyof Primates remain unresolved. One currently controversial issue is the time oforigin of the Order Primates. Both the analysis of molecular data (Springeret al.) and mathematical modeling (Soligo et al.) suggest a time of origin inthe middle of the Cretaceous period (80–90 MYA), while the earliest fossilrecord of primates is only 55 MYA. The fossil record can only provide a min-imum age for the origin of any taxon, while these other approaches may bemeasuring the initial divergence between a taxon and its sister group—anevent that may be not marked by any morphological differentiation. Soligoet al. discount this latter possibility, since the molecular estimate for theStrepsirhine–Haplorhine split is 80 MYA. They calculate, therefore, that thereis a 25-MY gap between the origin of identifiable primates and their firstappearance in the fossil record.

The supraordinal relationships among mammals have been an area ofintense interest among paleontologists, and primates are no exception.Although primatologists have reached some consensus about the content ofthe Order, there is still little agreement as to which living or fossil group isthe sister taxon of Primates. The molecular analysis of nuclear and mito-chondrial genes by Springer et al. provides support for the cladeEuarchontoglires, consisting of Primates, Dermopterans, Scandentia,Rodentia, and Lagomorpha. Within this clade, Primates are most closelyrelated to Dermoptera and Scandentia (=clade Euarchonta). Neither treeshrews nor flying lemurs are the exclusive sister group of Primates, but forma clade with each other. Unfortunately, this analysis does not includePtilocercus, a tree shrew that may be the most primitive of its clade and thusmay have particular relevance to primate origins (Sargis, Godinot). Nor can

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the relationships of fossil taxa be addressed. The morphological analysis of thepostcranium by Sargis, which does include Ptilocercus, finds, like the molec-ular analyses, that Scandentia and Dermoptera form a group (but only ifChiroptera is excluded). On the other hand, Godinot’s analysis, whichincludes cranial, dental, and postcranial characters, makes a strong case for aspecial relationship between tree shrews, particularly Ptilocercus, and primates.Plesiadapiformes, the Paleogene fossil group that has been traditionally mostclosely linked to Primates, were too incomplete to be analyzed effectivelyin these analyses. Silcox, by using the more ubiquitous dental characters (aswell as cranial and postcranial features) supports a sister-group relationshipbetween Plesiadapiformes and Primates to the exclusion of tree shrews or fly-ing lemurs. Therefore she, like Bloch and Boyer (Section III), supportsthe assignment of this fossil group within the Order Primates following theconventional paleontological interpretation.

Section II: Adaptations and Evolution of the Cranium

Vinyard et al. inquire if primates have unique aspects of jaw mechanics ormorphology that might indicate a role for dietary change in primate origins.Although certain jaw-adductor muscles (e.g., temporalis) show similar pat-terns of firing during chewing, others (e.g., deep masseter) are quite variable,thus primates are not homogeneous in jaw-muscle activity patterns. There arefew differences between tree shrews and strepsirhine primates in jaw mor-phology or the timing and relative activity levels of the jaw adductors, sug-gesting that the Origin of Primates may not have been accompanied by anymajor dietary shift.

Compared to any likely sister group, primates evidence a reorganization ofthe skull characterized by relatively large convergent orbits and a postorbitalbar. The adaptational significance of these features is still debated today. Onequestion concerns the activity pattern of ancestral primate. Based on an analy-sis of eye and orbit shape in mammals and birds Ross et al. are able to showthat nocturnality is the best explanation for the increased orbital convergence,large eyes, and large corneas that were likely present in primitive primates,although only the first two features are primate apomorphies. These featuresimprove image brightness and visual acuity.

The postorbital bar, one of the hallmark features of Primates, also has beenhypothesized to play a role in visual acuity by functioning as a barrier between

xxvi Introductions for Sections I–IV

the eyeball and the masticatory muscles to prevent distortion of the visualimage during chewing. Heesy et al., however, provide experimental evidencethat the anterior temporalis and medial pterygoid can cause deformation ofthe eye even in animals with postorbital bars (Otolemur, Felis), and thus spec-ulate that other compensatory mechanisms for maintaining visual acuity mustbe present. The action of the extraocular muscles is one such mechanism, anda postorbital bar would help maintain the integrity of the lateral orbit, givinga stable substrate from which these muscles could act.

Ravosa et al. marshal comparative and experimental comparative evi-dence to support a modified version of the NVP’s “rigidity” argument whereincreased orbital convergence and orbital frontation (due to increasedencephalization) both play a role in postorbital bar formation. They stress theindependent and interactive roles of asymmetrical jaw-adductor recruit-ment patterns (characteristic of insectivores and frugivores), nocturnality,encephalization and small body size on the evolution and function of thecircumorbital region and skull in basal primates.

Section III: Adaptations and Evolution of the Postcranium

Definitions of the Order Primates always have made reference to traits of thepostcranial skeleton, most notably the opposable hallux and the presence ofnails instead of claws on the digits, and it always has been the received wis-dom that something about an arboreal lifestyle has influenced the diagnosticlimb features of primates. Several workers, especially Matt Cartmill, refinedthese early, vague ideas. As part of the Nocturnal Visual Predation (NVP)model he proposed a more specific relationship between hindlimb oppositionand one aspect of primate-style arborealism, namely the need to balance andmove slowly on small supports when stalking and capturing prey. By compar-ing primates with marsupials of similar habitus, Lemelin and Schmitt areable to demonstrate that additional prehensility enhancing features (pha-langeal proportions, metapoodial/phalangeal proportions) are correlatedwith superior ability to deal with a fine-branch substrate. Hamrick discussesthe experimental and morphological evidence for the evolvability of the dis-tal limb, explaining why the origin and adaptive radiation of primates isaccompanied by high diversity in digit proportions.

There are also many behavioral aspects of primate locomotor behaviorthat distinguish them from most other arboreal mammals. The use of the

Introductions for Sections I–IV xxvii

diagonal sequence/diagonal couplets gait, emphasis on the hindlimb for sup-port and propulsion, low stride frequencies but longer stride lengths, largeangular excursions of the limbs, and the compliant gait are among them.Cartmill et al. and Lemelin and Schmitt address these behavioral differ-ences concluding that the diagonal sequence gait is a solution to moving onsmall branches with a prehensile extremity. They stress that this would onlybe a successful strategy for an animal with relatively deliberate locomotorhabits. Lemelin and Schmitt also show that Caluromys (a marsupial small-branch specialist) differs from terrestrial marsupials in sharing many of thesebehavioral traits, strongly suggesting that all of them are related to movingquadrupedally on small branches. Larson examines the morphological corre-lates of the highly protracted forelimb that results in the large angular excur-sion of the forelimb during quadrupedal walking. These are: a more obtusespinoglenoid angle, a reduction in the anterior and superior projection of thegreater tubercle possibly produced by an anterior shift of the humeral head.Smilodectes, the only early prosimian included in the study, appears moreprimitive in the humeral features than any extant primate.

In contrast to the slow moving ancestor envisioned by Cartmill and col-leagues, Szalay and Dagosto, in their grasp-leaping model, propose a muchmore agile creature. In their view, leaping is a component of locomotor behav-ior equal in importance to grasping in defining the postcranial morphotype ofPrimates. Szalay offers a sharply critical account of previous reconstructions ofthe locomotor abilities of early primates and the philosophies underlying thelogic of these reconstructions. Dagosto echoes these ideas, citing a number ofderived leaping related features of the limb skeleton shared by all primates,including the presumably paraphyletic adapids and omomyids. She also pointsout the difficulty in attempting to explain all of the derived characters of ahigher-level clade with a single adaptive hypothesis. A staged model for theacquisition of key locomotor related adaptations is proposed.

Bloch and Boyer describe the variation in postcranial bones and inferredlocomotor adaptations present among plesiadapiform primates, identifying avariety of arboreal behavioral adaptations in this group. They find no evidenceof gliding or phylogenetic links to Dermoptera among micromomyids, refutingBeard’s Eudermoptera hypothesis. Believing the similarities of the hallucal-grasping complex in Carpolestes to be a synapomorphy with true primates, theyposit that grasping was in place before anatomical adaptations for visual preda-tion or leaping, thus contesting both the NVP and grasp-leaping hypotheses.

xxviii Introductions for Sections I–IV

Section IV: Adaptations and Evolution of the Brain, Behavior, Physiology, and Ecology

As evidenced by the first three sections, features of the skull and skeleton havefigured prominently in evaluations of primate origins. But primates differfrom other mammals in many other features including size and structure ofthe brain, social organization, life history, physiology, and biochemistry. Thepapers in this section discuss some of these attributes and the relationshipsamong them.

Primates are among the “brainiest” mammals. Shea argues that theunusual combination of a precocial life history strategy at small size by earlyprimates, possibly allowed by a stable resource base, set the stage for a grade-shift in encephalization that was preserved as they diversified into larger sizes.In addition to greater size, the structure and organization of the brain distin-guish primates from other mammals. In an extensive review, Preuss demon-strates how primates have developed new cortical areas, reorganized existingstructures, changed the way existing structures connect, and established newkinds of connections. Many of these changes reflect the integration of infor-mation from the eyes and forelimb, contributing to a distinct kind of “look-ing and reaching” in primates, which fits nicely with models of primate originsthat stress the role of visual foraging.

Mueller et al. review aspects of the social organization of primates andmammals in order to reconstruct the ancestral pattern of primate socialorganization. They argue that a “dispersed” system (solitary foraging withsocial networks formed by a core of related females) was present in early pri-mates. The presence of social networks and contacts that are maintainedthroughout the year, rather than being restricted to the breeding season,are derived features compared to primitive mammals. Factors that mayexplain the development of sociality in primates are frugivory, prolongedmother-infant relationships, and large body size.

Snodgrass et al. show that ecological factors (diet quality, habitus, activ-ity pattern) are only partially successful in explaining the difference in basalmetabolic rates between lower and higher primates. The shared hypometab-olism of strepsirhines, tarsiers, and tree shrews indicates that the ancestralprimate inherited this physiology, small body size, and dependence on insectsas a food source from an archontan ancestor. Hypometabolism is possibly anadaptation to environments with low productivity and/or marked seasonality.

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Thus, the Shea, Mueller et al., and Snodgrass et al. models sometimes con-trast with each other in their reconstruction of ancestral diet (insectivory ver-sus frugivory), environment (stable versus unstable resource base), and bodysize (small versus large). In addition to metabolic rates, other aspects of phys-iology and biochemistry distinguish lower and higher primates. Yi and Li dis-cuss the evidence for adaptive evolution of the physiologically importantproteins growth hormone (GH), growth hormone receptor (GHR), andchorionic gonadotropin (CR). Each shows evidence of rapid change some-times associated with gene duplication and changes in site of expression.

We close the volume with two papers that address ecological aspects of pri-mate evolution and tie in themes from several of the previous sections. Mostcontributors use the comparative method to elucidate the adaptational signif-icance of primate apomorphies. As shown by the extensive review of pha-langeroid marsupial biology and ecology provided by Rasmussen andSussman, this radiation provides many interesting opportunities for under-standing the origin of primate diet, locomotion, foraging strategies, orbitalconvergence, life history, and physiology. While noting how much stillneeds to be learned about these mammals, they use what is known to critiquecurrent hypotheses of primate origins.

Lucas et al. manage to tie in almost every primate apomorphy in a modelof foraging evolution based, like Sussman’s, on the coevolution of primatesand angiosperms. In this model, early Primates were small, nocturnal, anddichromatic, living in angiosperms, but subsisting primarily on insects. Asangiosperms developed spines and thorns to protect themselves againstdinosaurs, primates developed nails and pads to protect themselves againstspines and thorns. The trichromatic color vision typical of catarrhines, andindependently developed in some platyrrhines and lemurs, thus is a morerecent evolutionary development.

xxx Introductions for Sections I–IV