Primates and Their Relatives in Phylogenetic Perspective

ADVANCES IN PRIMATOLOGY

Series Editors:

JOHN G. FLEAGLE State University of New York at Stony Brook Stony Brook, New York

R. D. E. MACPHEE American Museum of Natural History New York, New York

Editorial Board:

JOHN M. ALLMAN, California Institute ofTechno\ogy, Pasadena, California

RUSSELL L. CIOCHON, University of Iowa, Iowa City, Iowa

FRAN<;:OISEJOUFFROY, Museum National d'Histoire Naturelle, Paris, France

W. PATRICK LUCKETT, University of Puerto Rico, Sanjuan, Puerto Rico

LAWRENCE B. MARTIN, State University of New York at Stony Brook, Stony Brook, New York

CAREL P. VAN SCHAlK, Duke University, Durham, North Carolina

COMPARATIVE BIOLOGY AND EVOLUTIONARY RELATIONSHIPS OF TREE SHREWS Edited by W. Patrick Luckett

EVOLUTIONARY BIOLOGY OF THE NEW WORLD MONKEYS AND CONTINENTAL DRIFT Edited by Russell L. Ciochon and A. Brunetto Chiarelli

MOLECULAR ANTHROPOLOGY: Genes and Proteins in the Evolutionary Ascent of the Primates Edited by Morris Goodman and Richard E. Tashian

NEW INTERPRETATIONS OF APE AND HUMAN ANCESTRY Edited by Russell L. Ciochon and Robert S. Corruccini

NURSERY CARE OF NONHUMAN PRIMATES Edited by Gerald C. Ruppenthal

PRIMATES AND THEIR RELATIVES IN PHYLOGENETIC PERSPECTIVE Edited by Ross D.E. MacPhee

SENSORY SYSTEMS OF PRIMATES Edited by Charles R. Noback

SIZE AND SCALING IN PRIMATE BIOLOGY Edited by William L. Jungers

SPECIES, SPECIES CONCEPTS, AND PRIMATE EVOLUTION Edited by William H. Kimbel and Lawrence B. Martin

A Continuation Order Plan is available for this series. A continuation order will bring delivery of each new volume immediately upon publication. Volumes are billed only upon actual shipment. For further information please contact the publisher.

Primates and Their Relatives in Phylogenetic Perspective

Edited by

ROSS D. E. MacPHEE American Museum of Natural History New York, New York

Springer Science+Business Media, LLC

Library of Congress Cataloging-in-Publication Data

Primates and their relatives 1n phylogenet1c perspective I ed1ted by Ross D.E. MacPhee.

p. cm. -- (Advances 1n primatology) Includes bibl iograph1cal references and index.

1. Primates--Phylogeny. 2. Cladistic analysis. 3. Anatomy. Comparative. 4. Pr1mates--Evolution. I. MacPhee, R. D. E. II. Series. QL737.P9P677 1993 599.8--dc20 93-4969

CIP

Cover: Order primates as defined by Carolus Linnaeus in the 10th edition of Systema Naturae (1758).

ISBN 978-1-4899-2390-5 ISBN 978-1-4899-2388-2 (eBook) DOI 10.1007/978-1-4899-2388-2

© 1993 Springer Science+Business Media New York

Originally published by Plenum Press, New York in 1993. Softcover reprint of the hardcover 1 st edition 1993

All rights reserved

No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher

For Veronica: Omnia praeclara rara

Contributors

Ronald M. Adkins Department of Wildlife and Fisheries Texas A&M University College Station, Texas 77843

S. K. Babcock Department of Biological

Anthropology and Anatomy Duke University Medical Center Durham, North Carolina 27710

Wendy J. Bailey Department of Anatomy and Cell

Biology Wayne State University School of

Medicine Detroit, Michigan 48201

K. Christopher Beard Section of Vertebrate Paleontology Carnegie Museum of Natural History Pittsburgh, Pennsylvania 15213

john Czelusniak Department of Anatomy and

Cell Biology Wayne State University School of

Medicine Detroit, Michigan 48201

Morris Goodman Department of Anatomy and

Cell Biology Wayne State University School of

Medicine Detroit, Michigan 48201

Rodney L. Honeycutt Department of Wildlife and Fisheries Texas A&M University College Station, Texas 77843

J. I. Johnson Anatomy Department, and

Neuroscience Program Michigan State University East Lansing, Michigan 48824

J. A. W. Kirsch Zoological Museum and Department

of Zoology University of Wisconsin-Madison Madison, Wisconsin 53706

Traute K. Kleinschmidt Max Planck Institute for Biochemistry Munich, Germany

Spencer G. Lucas

Vll

New Mexico Museum of Natural History

Albuquerque, New Mexico

W. Patrick Luckett Department of Anatomy University of Puerto Rico Medical Sciences Campus San Juan, Puerto Rico 00936 Current address: Institute des Sciences de I'Evolution Laboratoire de Paleontologie Universite Montpellier II Montpellier, France

viii CONTRIBUTORS

Ross D. E. MacPhee Department of Mammalogy American Museum of Natural History New York, New York 10024

James R. Martin Department of Anatomical Sciences

and Neurobiology School of Medicine University of Louisville Louisville, Kentucky 40292

John Nickerson Department of Ophthalmology Emory University Atlanta, Georgia 30322

Todd M. Preuss Department of Psychology Vanderbilt University Nashville, Tennessee 37240

John C. Sgouros Max Planck Institute for Biochemistry Munich, Germany

Jing-Sheng Si Department of Ophthalmology Emory University Atlanta, Georgia 30322

Nancy B. Simmons Department of Mammalogy American Museum of Natural History New York, New York 10024

Camal A. M. Singer Max Planck Institute for Biochemistry Munich, Germany

Michael J. Stanhope Department of Anatomy and

Cell Biology Wayne State University School of

Medicine Detroit, Michigan 48201

Frederick S. Szalay Department of Anthropology Hunter College, City University of

New York New York, New York 10021

J. C. M. Thewissen Department of Biological

Anthropology and Anatomy Duke University Medical Center Durham, North Carolina 27710 Present address: Department of Anatomy NEOUCOM Rootstown, Ohio 44272

John R. Wible Department of Anatomical Sciences

and Neurobiology School of Medicine University of Louisville Louisville, Kentucky 40292

Preface

This book has the modest aim of bringing together methodological, theo­retical, and empirical studies that bear on the phylogenetic placement of primates and their relatives, and continues a tradition started by Phylogeny of the Primates: A Multidisciplinary Approach (edited by W. P. Luckett and F. S. Szalay; Plenum Press, 1975) and The Comparative Biology and Evolutionary Rela­tionships of Tree Shrews (edited by W. P. Luckett, Plenum Press, 1980). Although there are several recent compendia of studies of primate relationships, most of these are exclusively concerned with the internal arrangement of clades within the order, not with the place of primates and their relatives on the eutherian cladogram.

Evolutionary theory predicts that primates must be more closely related to some non primate mammals than to others, but a continuing problem has been to find reliable procedures for recovering historical relationships among taxa. Before the 1970s, higher-level relationships among primates and euthe­rian mammals that might be closely related to them were rarely treated in detail. Outstanding exceptions, like Le Gros Clark's Antecedents of Man, were just that-exceptions. (Clark himself essentially stopped with making a case for tree shrews; he did not, for example, explore whether bats and colugos were also related to primates.) In the 1970s and 1980s, the rise of cladistic techniques and advances in molecular methods began to transform primate systematics. So did new controversies, such as the "flying primate" hypothesis, which had the salubrious effect of refocusing attention on how phylogenetic arguments ought to be justified. In April 1991, an opportunity to reflect on what to date this new knowledge has brought us came in a symposium orga­nized for the 60th annual meeting of the American Association of Physical Anthropologists, entitled "Debating the Superordinal Relationships of Pri­mates: Issues, Evidence, and Proposed Solutions." And debate there was, as is reflected in this volume, composed of papers that emerged from that meet­ing. I am grateful to all of those who participated in this undertaking.

For various forms of assistance, including help with organizing the AAPA symposium, refereeing submitted papers, discussing fine points of systematic

ix

x PREFACE

methodology, and other matters, I thank John Wible, Rob DeSalle, Chris Beard, Ward Wheeler, Darrel Frost, Fred Szalay, Pat Luckett, Matt Cartmill, Audrone Biknevicius, and Todd Preuss. My editor at Plenum, Mary Born, encouraged as well as insisted-a useful combination-and I am grateful to her for helping this project through its many stages. But most of all I thank my wife Veronica, for her invaluable assistance throughout.

Ross D.E. MacPhee

New York

Contents

1 The Importance of Methods: Archontan Phylogeny and Cladistic Analysis

of Morphological Data 1 Nancy B. Simmons

Introduction Published Data Sets: A Summary 5 Choice of Taxa for Analysis 6 Choice of Characters and Character States 15 Weighting Characters 26 Ordering Transformations 30 Finding the Shortest Tree: Algorithms and Search Techniques 34 Interpreting Results of a Cladistic Analysis 36 Discussion and Conclusions 46 Appendix 1: Character Descriptions 48 Appendix 2: Data Matrix 55 References 57

2 Origin and Evolution of Gliding in Early Cenozoic Dermoptera (Mammalia,

Primatomorpha) 63 K. Christopher Beard

Introduction 63 Dermoptera 65 Mammals 82

3

Sixty-Five Million Years of Gliding in Implications for Phylogeny of "Archontan"

References 87

The Implications of the Propatagial Muscles of Flying and Gliding Mammals for A rchontan Systematics 91

J. G. M. Thewissen and S. K. Babcock

Introduction 91 Description 94 Conclusions 106

Materials and Methods 94 Discussion 102

References 107

Xl

xii CONTENTS

4 Ontogeny of the Tympanic Floor and Roof in Archontans III

John R. Wible and James R. Martin

Introduction III Descriptions 114 Comparisons 138 References 145

5

Methods and Materials Other Recent Archontans Conclusions 144

113 134

Developmental Evidence from the Fetal Membranes for Assessing Archontan Relationships 149

W. Patrick Luckett

Introduction 149 Role of Fetal Membranes in Assessing Mammalian Phylogeny 150 Fetal Membrane Developmental Patterns of Archontans 152 Evolutionary Analysis of Archontan Fetal Membranes 169 Summary and Conclusions 179 References 182

6 Cranioskeletal Morphology of Archontans, and Diagnoses of Chiroptera, Volitantia,

and A rchonta 187 Frederick S. Szalay and Spencer G. Lucas

Introduction 187 Phylogeny 189

Cranioskeletal Evidence and Archontan Summary 222 References 223

7 A Molecular Examination of Archontan and Chiropteran Monophyly 227

Ronald M. Adkins and Rodney L. Honeycutt

Introduction 227 Discussion 230

8

Methods and Materials 229 References 245

Results and

A Molecular View of Primate Supraordinal Relationships from the Analysis of Both Nucleotide and Amino Acid Sequences 251

Michael J. Stanhope, Wendy J. Bailey, John Czelusniak, Morris Goodman, Jing-Sheng Si, John Nickerson, John G. Sgouros, Gamal A. M. Singer, and Traute K. Kleinschmidt

Introduction 251 Data Collection and Analysis 253 Sequence Results 258 Comparison and Discussion of Phylogenetic Hypotheses 265 Conclusions 277 Appendix I: IRBP Sequence Alignment 278 Appendix II: E-Globin Sequence Alignment 281 References 289

CONTENTS xiii

9 Phylogeny through Brain Traits: Interordinal Relationships among Mammals

Including Primates and Chiroptera 293 J. I. Johnson and J. A. W. Kirsch

Introduction: Value of Neural Characters 293 The 15-Character Trees, 1982 294 The 24-Character Trees, 1991 294 The 89-Character Tree, with 65 Nonneural Traits Added from Novacek et al. (1988) 303 The 29- and 94-Character Trees, with 5 Neural Traits Added from Pettigrew et al. (1989) 308 Relations of Megachiroptera, Primates, and Archonta 324 Neural Characters and Homoplasy 328 The Contribution of Neural Characters to Hypotheses about Interordinal Relationships, Including Those of Primates and Chiroptera 328 Summary 329 References 330

10 The Role of the Neurosciences in Primate Evolutionary Biology: Historical

Commentary and Prospectus 333 Todd M. Preuss

Introduction 333 The Question of Primate Neural Specializations 335 Foundations of a New Evolutionary Neurobiology 343 Summary and Conclusions 356 References 357

11 Summary 363

Ross D. E. MacPhee

Introduction 363 -Homology and Justification 363 Prospects 372 References 372

Systematic Index 375

Author and Subject Index 379