PRIMATE ORIGINS: ADAPTATIONS AND EVOLUTION DEVELOPMENTS IN PRIMATOLOGY: PROGRESS AND PROSPECTS Series Editor: Russell H. Tuttle, University of Chicago, Chicago, Illinois This peer-reviewed book series melds the facts of organic diversity with the continuity of the evolutionary process. The volumes in this series exemplify the diversity of theoretical perspectives and methodological approaches currently employed by primatologists and physical anthropologists. Specific coverage includes: primate behavior in natural habitats and captive settings; primate ecology and conservation; functional morphology and developmental biology of primates; primate systematics; genetic and phenotypic differences among living primates; and paleoprimatology. ANTHROPOID ORIGINS: NEW VISIONS Edited by Callum F. Ross and Richard F. Kay MODERN MORPHOMETRICS IN PHYSICAL ANTHROPLOGY Edited by Dennis E. Slice BEHAVIORAL FLEXIBILITY IN PRIMATES: CAUSES AND CONSEQUENCES By Clara B. Jones NURSERY REARING OF NONHUMAN PRIMATES IN THE 21ST CENTURY Edited by Gene P. Sackett, Gerald C. Ruppenthal and Kate Elias NEW PERSPECTIVES IN THE STUDY OF MESOAMERICAN PRIMATES: DISTRIBUTION, ECOLOGY, BEHAVIOR, AND CONSERVATION Edited by Paul Garber, Alejandro Estrada, Mary Pavelka and LeAndra Luecke HUMAN ORIGINS AND ENVIRONMENTAL BACKGROUNDS Edited by Hidemi Ishida, Russel H. Tuttle, Martin Pickford, Naomichi Ogihara and Masato Nakatsukasa PRIMATE BIOGEOGRAPHY Edited by Shawn M. Lehman and John Fleagle REPRODUCTION AND FITNESS IN BABOONS: BEHAVIORAL, ECOLOGICAL, AND LIFE HISTORY PERSPECTIVES Edited By Larissa Swedell and Steven R. Leigh RINGAILED LEMUR BIOLOGY: LEMUR CATTA IN MADAGASCAR 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 ADAPTATION Edited by Lisa Gould and Michelle L. Sauther PRIMATE ORIGINS: ADAPTATIONS AND EVOLUTION Edited by Matthew J. Ravosa and Marian Dagosto Department of Cell and Molecular Biology Feinberg School of Medicine, Northwestern University Chicago, Illinois Matthew J. Ravosa Marian Dagosto Department of Cell and Department of Cell and Molecular Biology Molecular Biology Feinberg School of Medicine, Feinberg School of Medicine, Northwestern University Northwestern University Chicago, Illinois Chicago, Illinois Library of Congress Control Number: 2005937517 ISBN 10: 0-387-30335-9 ISBN 13: 978-0-387-30335-2 Printed on acid-free paper. © 2007 Springer Science+Business Media, LLC All rights reserved. This work may not be translated or copied in whole or in part without the written 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 scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights. 9 8 7 6 5 4 3 2 1 springer.com CONTENTS Contributors xvii Preface xxi Introductions 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 Placental Mammals and the Phylogenetic Placement of Primates 1 Springer, 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 1 Materials and Methods 4 Results 5 Likelihood and Bayesian Analyses with the Full Data Set 5 Analyses with Outgroup Jackknifing 12 Analyses with the Nuclear Data Set 12 Analyses with Subsets of Nuclear Genes 12 Analyses with Mt rRNA Genes 13 Discussion 14 Likelihood Versus Bayesian Results 14 Early History of Placentalia 15 Major Clades of Placental Mammals 17 Relationships in Afrotheria 18 Relationships Within the Euarchontoglires Clade 18 Relationships in Laurasiatheria 19 Molecular Classification for the Living Orders of Placental Mammals 19 Conclusions 22 References 23 v vi Contents 2. New Light on the Dates of Primate Origins and Divergence 29 Soligo, C., Will, O. A., Tavaré, S., Marshall, C. R., and Martin, R. D. Introduction 29 The Fossil Record 30 The Molecular Evidence 35 Quantifying the Incompleteness of the Fossil Record 37 Preservational Bias in the Fossil Record 43 Acknowledgments 46 References 46 3. The Postcranial Morphology of Ptilocercus lowii (Scandentia, Tupaiidae) and its Implications for Primate Supraordinal Relationships 51 Sargis, E. J. Introduction 51 Taxonomy and Phylogeny of the Family Tupaiidae 52 Taxonomy 52 Supraordinal Relationships of Tupaiids 53 Significance of Ptilocercus 59 Materials and Methods 60 Results 62 Discussion 65 Conclusions 67 Acknowledgments 69 References 75 4. Primate Origins: A Reappraisal of Historical Data Favoring Tupaiid Affinities 83 Godinot, M. Introduction 83 Limits of Cladistics Confronted with Large Data Sets 86 Facing Primatomorpha 90 Are Paromomyid Dental Characters Compatible with Dermopteran Origins? 90 Dermopteran Incisors 92 Paromomyid Postcranials, Gliding, and Apatemyid Adaptations 95 Contents vii On Postcranial Characters and Archontan Phylogeny 97 Skull Characters and Conclusion 100 The Plesiadapiform Radiation and Primate Ancestry 101 Temporal and Geographical Extension 102 Plesiadapiform Dental Characters and Primate Origins 104 Other Characters and Conclusion 108 Returning to Tupaiidae 112 Important Tarsal Characters 116 Conclusion: Tupaiids as Sister-Group of Primates 120 Remarks on Scenarios of the Acquisition of Nails 122 Concluding Remarks 126 Fossils, Methods, and Primate Origins 126 Primate Morphotype Locomotor Mode 129 Summary 131 Acknowledgments 133 References 133 5. Primate Taxonomy, Plesiadapiforms, and Approaches to Primate Origins 143 Silcox, M. T. Introduction 143 Background 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 150 Previous Definitions and Diagnoses of Primates 151 The Phylogenetic Position of Plesiadapiformes 155 Background 155 A More Comprehensive Analysis 159 Taxonomic Implications of the Current Analysis 163 Primate Taxonomy and the Study of Euprimate Origins 167 Conclusions 169 Acknowledgments 170 References 171 viii Contents PART II: ADAPTATIONS AND EVOLUTION OF THE CRANIUM 6. Jaw-Muscle Function and the Origin of Primates 179 Vinyard, 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 180 Apparatus Interpretations of the Masticatory Apparatus in the First Primates 192 Tree shrew Feeding Ecology and Jaw Morphology— A Reasonable Early Primate Model? 196 Materials and Methods 197 Jaw-Muscle EMG 197 Comparative Primate EMG Data 202 Results 203 Treeshrew EMG 203 Comparison of Treeshrew and Primate EMG 206 Discussion 209 Jaw-Muscle EMG and Jaw Morphology in Treeshrews and Primates 209 Jaw-Muscle EMG and the Conservation of Primate Masticatory Behaviors 213 Mastication in the First Primates: In vivo Evidence from Treeshrews and Primates 217 Conclusions 219 Acknowledgments 219 References 220 7. Were Basal Primates Nocturnal? Evidence From Eye and Orbit Shape 233 Ross, C. F., Hall, M. I., and Heesy, C. P. Introduction 233 Orbital Convergence 235 Orbit Size and Shape 237 Reconstructions of Orbit Size and Shape in Basal Primates 240 Materials and Methods 241 Eye Shape Measures 241 Contents ix Orbit Shape Measures 241 Results 242 Eye Size and Shape 242 Orbit Size and Shape 246 Discussion 248 The Eyes of Basal Primates 248 The Eyes of Haplorhines 251 Conclusions 252 Acknowledgments 252 References 253 8. Oculomotor Stability and the Functions of the Postorbital Bar and Septum 257 Heesy, C. P., Ross, C. F., and Demes, B. Introduction 257 Neurological and Morphological Maintenance of Eye Position 260 What Are the Consequences of Disruption of Oculomotor Coordination? 263 Focus of This Study 266 Methods 267 Results 268 Discussion and Conclusions 271 Discussion of the Ocular Kinematic Results 271 Oculomotor Stability and the Function of the Postorbital Bar 272 Oculomotor Stability and the Function of the Haplorhine Septum 275 Summary 276 Acknowledgments 277 References 277 9. Primate Origins and the Function of the Circumorbital Region: What’s Load Got to Do with It? 285 Ravosa, M. J., Savakova, D. G., Johnson, K. R., and Hylander, W. L. Introduction 285 Masticatory Stress and Circumorbital Form 286 Galago Circumorbital Peak-Strain Magnitudes 289 Galago Circumorbital Principal-Strain Directions 293 Facial Torsion and the Evolution of the Primate Postorbital Bar 294 x Contents Nocturnal Visual Predation and Circumorbital Form 298 Orbital Form and Patterns of Covariation 301 Nocturnal Visual Predation and the Evolution of Orbit Orientation and the Postorbital Bar 307 Phylogenetic Evidence Regarding the NVPH and the Evolution of Circumorbital Form 316 Conclusions 317 Acknowledgments 320 References 320 PART III: ADAPTATIONS AND EVOLUTION OF THE POSTCRANIUM 10. Origins of Grasping and Locomotor Adaptations in Primates: Comparative and Experimental Approaches Using an Opossum Model 329 Lemelin, P. and Schmitt, D. Introduction 329 Models of Primate Origins: A Review 331 Convergence between Opossums and Primates: Comparative Studies 334 A Review of Didelphid and Cheirogaleid Ecology and Behavior 335 Substrate Use and Cheiridial Morphology: A Functional Model 339 Morphometric Results 341 Performance Results 346 Convergence between Opossums and Primates: Experimental Studies 351 Materials and Methods 353 Gait Patterns 356 Arm Protraction 359 Vertical Force Distribution on Limbs 362 Discussion and Conclusions 363 Acknowledgments 368 References 369 11. Evolvability, Limb Morphology, and Primate Origins 381 Hamrick, M. W. Introduction 381 Theoretical Criteria for Evolvability 383