Primate Adaptation and Evolution Third Edition John G. Fleagle Stony Brook University, Stony Brook, NY AMSTERDAM • BOSTON • HEIDELBERG • LONDON • NEW YORK • OXFORD • PARIS SAN DIEGO • SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO Academic Press is an Imprint of Elsevier Academic Press is an imprint of Elsevier 525 B Street, Suite 1800, San Diego, CA 92101-4495, USA 225 Wyman Street, Waltham, MA 02451, USA 32 Jamestown Road, London NW1 7BY, UK Third edition 2013 Copyright © 2013 Elsevier Inc. All rights reserved. No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means electronic, mechanical, photocopying, recording or otherwise without the prior written permission of the publisher. Permissions may be sought directly from Elsevier’s Science & Technology Rights Department in Oxford, UK: phone (+44) (0) 1865 843830; fax (+44) (0) 1865 853333; email: [email protected]. 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Because of rapid advances in the medical sciences, in particular, independent verification of diagnoses and drug dosages should be made British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress ISBN: 978-0-12-378632-6 For information on all Academic Press publications visit our website at elsevierdirect.com Typeset by TNQ Books and Journals Pvt Ltd. www.tnq.co.in Printed and bound in the United States of America 13 14 15 16 17 10 9 8 7 6 5 4 3 2 Preface Primatology and primate evolution have changed consider- estimates of the size of fossil species from a wide variety ably in the two and a half decades since the first edition of sources in the literature, based on many different param- of Primate Adaptation and Evolution was written. Like all eters. Thus many estimates across taxa are not method- other areas on knowledge, our knowledge of these subjects ologically comparable. They are meant to give the reader a has increased dramatically, and the published literature general appreciation for the size of extinct taxa in a general manyfold. There are more species, more sites, more stud- sense and are not meant to be suitable for detailed analyses. ies, more techniques, more analyses, more articles, more As in previous editions, I have included two types of journals, and, hopefully, more understanding. But there is references for each chapter. There are general references also more evidence of just how limited out current knowl- which provide broad reviews of the topics covered in that edge actually is, and how much it is likely to change in the chapter. These are designed to provide more detailed docu- future. This, like every other book, is perhaps best viewed mentation and discussion, and in some cases, alternative as a progress report rather than a synthesis. views on the material discussed in that chapter. In addition, In this edition, every chapter has been revised and there are numerous citations within the text of each chapter rewritten, some much more than others. All of the tables that are listed as cited references at the end of the chapter. have been redone; there are many new figures; and most These are not meant to provide a comprehensive or even of the references are new. Some of these changes deserve representative documentation for the contents of the chap- further explanation. ter. Rather they are meant to provide the readers with an The number of recognized primate species has risen dra- entry into the literature regarding particular facts and ideas matically in the past decade. There are many reasons for that I found interesting and/or significant. In particular, I this. Partly it reflects an extensive increase in fieldwork in have cited relatively recent publications that may not appear remote parts of the world that has generated a greater appre- in the larger General references. However, in the early part ciation of the details of primate biogeography and diversity. of the twentieth century, I fully expect any reader will be In addition, the increasing influence of molecular system- able to find numerous additional references to any topic in atics has generated new insights into the genetic diversity this book through an online search. among primate populations. Finally, the widespread use of This edition of Primate Adaptation and Evolution con- the Phylogenetic Species Concept has had a major effect tains many additional illustrations. As with previous editions on the abilities and willingness of systematists to describe I have limited these to line drawings and black and white and diagnose new or forgotten taxa. In general, I have used photos with an emphasis on comparisons rather than docu- the IUCN Red List website in creating the tables of extant mentation and description. Nevertheless, I appreciate that species in this volume. However, this increase in recognized these do not capture the remarkable beauty and diversity of primate species has created problems in the use of older lit- living primates or the details of morphology that are available erature for retrieving information about the behavior, ecol- in various other media, including videos and 3-dimensional ogy, body mass or limb proportions of individual taxa. For figures. Readers are urged to look more widely for addi- example, data that in previous decades, or previous editions tional illustrative materials, and I especially recommend All of this book, were attributed to the single species of woolly the World's Primates (www.alltheworldsprimates.org). lemur, Avahi laniger, may well have been derived from one This edition has benefitted from the generous advice, of several other species now recognized as distinct in that assistance and expertise of many people. The efforts and genus. Readers should thus view the data in the tables espe- contributions of those listed in previous editions are still cially as only rough estimates for the purpose of broad com- greatly appreciated. For help with this edition, I thank parisons, not detailed analyses. the following people, in no particular order: Alfred In previous editions, I tried to provide body mass esti- Rosenberger, Todd Disotell, Callum Ross, Colin Groves, mates from most species of fossil primates derived from Richard Kay, James Rossie, Tim Smith, Chris Kirk, Mark a single regression formula based on molar tooth dimen- Coleman, Stephanie Maiolino, Doug Boyer, Steve Leigh, sions. However, in the current edition I have relied more on Andreas Koenig, Carola Borries, Charles Janson, Tim ix x Preface Clutton-Brock, Katie Hinde, Erin Vogel, Peter Lucas, Nate Brenda Benefit, Eric Delson, Martin Pickford, Mauricio Dominy, Vivek Venkataraman, Diane Doran-Sheehy, Scott Anton, Meave Leakey, The Turkana Basin Institute, Richard Suarez, Herman Pontzer, Patricia Wright, Chia Tan, Mireya Leakey, Carol Ward, Michael Plavcan, Peter Ungar, The Mayor, Shawn Lehman, Rachel Jacobs, Laurie Godfrey, Kenya National Museum, Michel Brunet, Franck Guy, Tim Ryan, Bill Jungers, Brigitte demes, Betsy Dumont, Bill Kimbel, Adam Gordon, Bernard Wood, Brian Suzanne Strait, Sara Martin, Anja Deppe, Ian Tatter- Richmond, Chris Stringer, Randall Susman, Fred Grine, sall, Myron Shekelle, Dan Gebo, Marion Dagosto, Anna Karen Baab, Philip Rightmire, David Strait, Ian Wallace, Nekaris, Anne Yoder, Christian Roos, Russ Mittermeier, Gunter Brauer, Susan Larson, Zeray Alemseged, Tim Sharon Gursky, Peter Kappeler, Tony DiFiore, Marilyn White, John Shea, Lee Berger, and many others I may have Norconk, Alfred Rosenberger, Paul Garber, Anthony Rylands, overlooked. Leila Porter, Mark Van Roosmalen, Barth Wright, Karen As with previous editions, the heart of this book is the Wright, Scott McGraw, Joan Silk, Chris Gilbert, Eric Sargis, illustrations. Most of these are the due to the longterm Alice Elder, Wendy Erb, David Fernandez, Jessica Rothman, efforts and unfailing patience of Stephen Nash and Luci Jessica Lodwick, Michael Steiper, Richard Wrangham, Betti-Nash. In their talented hands even the most muddled John Mitani, Dan Lieberman, Sarah Hrdy, Kristen Hawkes, ideas are somehow transformed into illustrations that are Kim Hill, Kaye Reed, Jason Kamilar, Sandy Harcourt, crisp and understandable. Oliver Schulke, Julia Oster, Jon Bloch, Philip Gingerich, Several people were especially helpful in the produc- Frank Brown, Thure Cerling, Craig Feibel, Ian McDougall, tion of this edition. Mary Silcox provided the classification Mary Silcox, Stephen Chester, Gregg Gunnell, Xijun Ni, Matt of plesiadapiforms. Stevie Carnation, Amanda Kingston, Cartmill, Ken Rose, Lawrence Flynn, Chris Heesy, Elwyn Rachel Jacobs, and Ian Wallace contributed herculean Simons, Nancy Stevens, Jorn Hurum, Blythe Williams, efforts in the construction and ordering of tables, figures, Walter Hartwig, Jonathan Perry, Marc Godinot, Chris Beard, and references. Amanda and Ian were invaluable in correct- Mark Klinger, Lauren Halenar, Siobhan Cooke, Alexa ing the proofs. Rachel wrote all of the teacher aids. Most of Krupp, Castor Cartelle, Ross MacPhee, Terry Harrison, all, this edition owes its existence to the sustained efforts of Bill Sanders, Iyad Zalmout, Jay Kelley, John Kappelman, Dr. Andrea Baden, whose scientific knowledge and judg- David Alba, Sergio Almecija, Salvador Moya-Sola, Isaac ment, editorial, graphic and photographic skills, and overall Casanovas-Vilar, David Pilbeam, Ellen Miller, Ari organizational abilities pulled it all together into a coherent Grossman, Nina Jablonski, Rajeev Patnaik, Russ Ciochon, volume. Chapter 1 Adaptation, Evolution, and Systematics ADAPTATION events independent of selection. Founder effect is a more Adaptation is a concept central to our understanding extreme change in the genetic makeup of a population that of evolution, but the term has proved very difficult to occurs when a new population is established by only a few define in a simple phrase. One of the most succinct def- individuals. This new population may sample only a small initions has been offered by Vermeij (1978, p. 3): ‘An part of the variation found in the ancestral population. adaptation is a characteristic that allows an organism to Thus, recessive alleles that are not expressed in the larger live and reproduce in an environment where it probably population may become more common or even fixed in could not otherwise exist.’ In the following chapters, the new population. In this way, the chance characteristics we examine extant (living) and extinct (fossil) primates of a founder population can have dramatic effects on the as a series of adaptive radiations – groups of closely subsequent evolution and adaptive diversity of a group of related organisms that have evolved morphological and organisms. behavioral features enabling them to exploit different The fact that the diversity of life is the result of evolution ecological niches. Adaptive radiations provide especially means that all organisms are related by virtue of sharing a clear examples of evolutionary processes. The adaptive common genetic ancestry in the distant past. However, it is radiation of finches on the Galapagos Islands of Ecuador also clear that living organisms are not a continuous spread played an important role in guiding Darwin’s views on of variation. The living world is composed of distinct kinds the origin of species. of organisms that we recognize as species. Although vir- Adaptation also refers to the process through which tually all biologists recognize species as the natural units organisms obtain their adaptive characteristics. The pri- of life, defining exactly what a species is or how species mary mechanism of adaptation is natural selection. Natu- form are more difficult problems. These are the problems ral selection is the process whereby any heritable features, that Darwin (1859) set out to explain, and they are still anatomical or behavioral, that enhance the fitness of an the subject of intense study and debate (e.g., Kimbel and organism relative to its peers, increase in frequency in the Martin, 1993; Groves, 2001, 2012; DeQueiroz, 1998, 2007; population in succeeding generations. Fitness, in an evo- Rosenberger, 2012). lutionary sense, is reproductive success. It is important to Until recently, most biologists and anthropolo- remember that natural selection acts primarily through dif- gists generally accepted the Biological Species Con- ferential reproductive success of individuals within a pop- cept (BSC), in which species are defined as ‘groups of ulation (Williams, 1966). However, there is considerable actually or potentially interbreeding natural populations debate regarding the extent to which selection can also act that are reproductively isolated from other groups’ (Mayr, at higher levels, including groups (Group Selection) and 1942). Although appealing, in that it emphasizes the species (Species Selection). genetic and phyletic distinctiveness of species through reproductive isolation, the Biological Species Concept is obviously impossible to apply to fossils or allopat- EVOLUTION ric populations of living animals, and even difficult to Evolution is modification by descent, or genetic change apply to sympatric populations without detailed data on in a population through time. Although biologists con- mating behavior and fertility (Tattersall, 1989; Groves, sider most evolution to be the result of natural selection, 2001, 2012). Moreover, as more and more ‘species’ have there are other, non-Darwinian mechanisms that can and been sampled genetically, it has become clear that hybrid- do lead to genetic change within a population. Genetic ization between presumed species has been very common drift is change in the genetic composition of a popula- in primate evolution (e.g., Detwiler, 2002; Zinner et al., tion from generation to generation due to chance sampling 2011). 1 Primate Adaptation and Evolution. http://dx.doi.org/10.1016/B978-0-12-378632-6.00001-X Copyright © 2013 Elsevier Inc. All rights reserved. 2 Primate Adaptation and Evolution Many students of living organisms are more comfortable PHYLOGENY with a Mate Recognition Concept (Paterson, 1978, 1985; Masters, 1993). In this concept, species are defined as ‘the Evolutionary change within a population can take place group of individuals sharing a common fertilization system’ at different rates and can yield different results. There are (Paterson, 1985). A particularly important aspect of this com- several terms available to describe how and why differ- mon fertilization system is a specific m ate-recognition sys- ent patterns of evolutionary change occur. What is more, tem. Members of a species recognize one another as potential numerous theories exist about how common these differ- mates through such behavior or morphological features as ent patterns of evolutionary change are in the history of vocalizations, mating displays, or ornamentation. Like the life. The pattern in which a lineage undergoes gradual Biological Species Concept, the Mate Recognition Concept change over time is called anagenesis. Cladogenesis is is virtually impossible to apply to extinct organisms. the division of a single lineage into two lineages. Gradual In contrast with the Biological Species Concept and change in the morphology of a population of organisms the Mate Recognition Concept, which are based on infor- through time, either anagenetic or cladogenetic, is often mation about reproductive behavior, many paleontologists called phyletic gradualism. This type of evolutionary pat- prefer a species concept based on morphological differ- tern is very common in the fossil record, and many biolo- ences. The Phylogenetic Species Concept (Cracraft, gists believe that most evolutionary change has been of 1983) is commonly adopted by students of phylogenetic this type. systematics. In this approach, a species is ‘the smallest The rates of evolutionary change that take place in diagnosable cluster of individuals within which there is a populations through time may vary considerably, theoreti- parental pattern of ancestry and descent’. In this concept, a cally over several orders of magnitude. In addition, direc- species is defined on the basis of morphological or genetic tional selection may shift over the course of relatively distinctions from other taxa (Cracraft, 1983). In principle, short time periods due to climatic fluctuations. Some this could be based on a single feature. At present, most paleontologists argue that the most common type of evo- phylogenetic analyses, and most systematic revisions, lutionary change is punctuated equilibrium, in which generally follow a Phylogenetic Species Concept as spe- the morphology of most species is essentially stable (in cies are identified by detailed morphological features or equilibrium) for long periods of time, and that speciation aspects of their DNA. However, the question of how many events are the result of rapid morphological and genetic genetic differences are needed to identify a separate spe- shifts (or punctuations) over brief periods of evolutionary cies is a critical, but largely unresolved, issue in primate time so that intermediate forms are rarely recovered (e.g., phylogeny (Groeneveld et al., 2009). Gould and Eldridge, 1993). Unfortunately, the punctuated Other researchers, using what may be called a Phenetic equilibrium model is very difficult to distinguish from a Fossil Species Concept, would argue that species defined discontinuous fossil record and is generally defined in a morphologically should have approximately the same amount way that virtually precludes the possibility of determining of metrical variation as extant populations (e.g., Gingerich how often it actually takes place. Overall, it is now well- and Schoeninger, 1979; Cope, 1993). This is often a very documented that evolutionary change has taken place at useful criterion when one has a continuously changing time- many different rates. successive lineage in the fossil record, in which the endpoints The branching pattern of successive species that results may be very different but individual samples overlap. from numerous cladogenetic events is a phylogeny. Because Most biologists agree that a species is a distinct seg- this book deals with the adaptive radiations of primates, we ment of an evolutionary lineage, and many of the differences are interested in reconstructing the evolutionary branching among species concepts reflect attempts to find criteria that sequence, or phylogeny, of various primate groups to see can be used to identify species based on different types of how they are related to one another. Although some of us information, such as behavioral observations of living popu- can trace our own genealogies (or those of our pets) through lations, genetic sequences, or morphological information several generations, tracing the genealogical relationships from teeth, skull, or pelage. Some of the diversity of species among all primates is a much more daunting undertak- concepts may be more useful in distinguishing species at dif- ing. The evolutionary radiation of primates has taken place ferent phases of their formation (de Quieroz, 1998, 2007). over tens of millions of years of geological time and has Paradoxically, the greatest challenge to species identification involved thousands of species, millions of generations, and often comes not from incomplete information, but from those billions of individuals. Moreover, the records available for rare paleontological instances in which there is a continuous reconstructing primate phylogeny are meager, consisting of temporal sequence of populations undergoing directional individuals of fewer than 300 living species and occasional selection (e.g., Rose and Bown, 1993). As noted above, the bony remains of several hundred extinct species drawn from endpoints are clearly differentiable, but any species boundary various parts of the world at various times during the past is necessarily arbitrary (see Chapter 18). 65 million years. Chapter | 1 Adaptation, Evolution, and Systematics 3 The methods we use to reconstruct phylogenies are not. The sameness of features that results from common based primarily on identifying groups of related species ancestry is called homology, and identical features that are through similarities in their morphology and in the molecu- the result of a common ancestry are homologous. In con- lar sequences of their genetic material. However, rather trast, the presence of similar features in different species than just looking at overall similarity, most biologists agree that is not the result of a common inheritance is described that organisms should be grouped together on the basis of as homoplasy. shared specializations (or shared derived features) that dis- Homoplasy is a very common phenomenon in evo- tinguish them from their ancestors. For example, body hair lution (Sanderson and Hufford, 1996). Most analyses of is a shared specialization that unites humans, apes, mon- morphological evolution find that nearly half of all sim- keys, and cats as mammals and distinguishes them from ilarities are the result of homoplasy rather than common other types of vertebrates, whereas the common posses- ancestry. There are several types of homoplasy and many sion of a tail by many monkeys, lizards, and crocodiles is factors that cause it to be such a common phenomenon. an ancestral feature that is of no particular value in assess- The evolution of superficially similar features in differ- ing the evolutionary relationships among these organisms, ent lineages, such as the wings of bats and the wings of since their common ancestor had a tail. On the other hand, birds, is often called convergence. In contrast, paral- the absence of a tail in apes and humans represents a derived lelism refers to the independent evolution of identical specialization that sets us apart from our ancestors (Fig. 1.1). features in closely related organisms, such as the indepen- The common possession of a group of specializations by a dent evolution of white fur in many lineages of monkey. cluster of species or genera is interpreted as indicating that Reversal refers to an evolutionary change in an organism this cluster shares a unique heritage relative to other related that resembles the condition found in an earlier ancestor, species. Most current studies of primate phylogeny are such as the presence of hair on the fingers of humans based on extensive analysis of morphological features and/ descended from apes with hairless digits. In many cases, or amino acid sequences from parts of a species’ genome, homoplasy is the result of natural selection for similar using sophisticated computer programs to determine the functional adaptations. For example, larger animals may pattern of shared derived similarities (Kay et al., 1997; face similar mechanical problems. In addition, homoplasy Disotell, 2011; Perelman et al., 2011). may also reflect the fact that evolutionary pathways are Unfortunately, not all derived similarities among organ- constrained by development and available genetic poten- isms are indicative of a unique heritage. Animals have fre- tial. In molecular evolution, the potential for homoplasy quently evolved morphological similarities independently. is dictated by the limited number of amino acids making In addition to apes and humans, for example, a few mon- up the genetic code. Although many people feel that some key species and a few prosimians (as well as frogs) have morphological regions, such as teeth, skulls, or postcranial lost all or most of their tail. The biologist’s task in recon- elements, are more prone to homoplasy than others, most structing phylogeny is to distinguish those specializations comparative assessment show that this is not the case. that are the result of a unique heritage from those that are Moreover, features that show considerable homoplasy in FIGURE 1.1 Shared specializations and ancestral features. 4 Primate Adaptation and Evolution one group of animals may show no homoplasy in other groups. Most significantly, homoplasy is a phenomenon TABLE 1.1 Classification of the White-fronted Capuchin that can only be identified in a retrospective analysis monkey after a phylogeny has been constructed (Begun, 2007). Kingdom Animal Although frequently treated as an undesirable distraction Phylum Chordata in attempts to reconstruct phylogeny, homoplasy is an important evolutionary phenomenon that deserves greater Class Mammalia (mammals) study and consideration (Hall, 1999; Lockwood and Order Primates (primates) Fleagle, 1999; Kay and Fleagle, 2010). Semiorder Haplorhini Suborder Anthropoidea (higher primates) TAXONOMY AND SYSTEMATICS Infraorder Platyrrhini (New World monkeys) Taxonomy is a means of ordering our knowledge of bio- logical diversity through a series of commonly accepted Superfamily Ceboidea (New World monkeys) names for organisms. If scientists wish to communicate Family Cebidae (capuchins, squirrel monkeys, owl about animals and plants and to discuss their similarities monkeys, and marmosets)* and differences, they need a standard system of names both Subfamily Cebinae (capuchins and squirrel monkeys)* for individual types of organisms and for related groups of organisms. For example, the white-fronted capuchin mon- Genus Cebus (capuchins) key of South America, known to many people as the organ Species Cebus albifrons (white-fronted capuchin) grinder monkey, goes by over a dozen different names *Indicates only one of several common classifications (see Chapter 5) among the different tribal and ethnic groups of South America. To scientists around the world, however, this spe- cies is known by a single name, Cebus albifrons. The prac- tice of assigning every biological species, living or fossil, classes, and classes into phyla. For particular lineages, a unique name composed of two Latin words was initiated these basic levels are often further subdivided or clustered by Carolus Linnaeus, a Swedish scientist of the eighteenth into semiorders, suborders, infraorders, superfamilies, century whose system of biological nomenclature is uni- subfamilies, tribes, subgenera, or subspecies. For con- versally followed today. venience, names at different levels of the hierarchy are Under the Linnean system, Cebus is the name of a often given distinctive endings. Family names usually end genus (pl. genera), or group of animals; in this case sev- in dae, superfamily names in oidea, and subfamily names eral kinds of capuchin monkey (the name of a genus is in inae. always capitalized). The word albifrons, the species name, In the science of classifying organisms, systematics, refers to a particular type of capuchin monkey, the white- we attempt to apply the tidy Linnean system to the untidy, fronted capuchin monkey. (A species name always begins unlabeled world of animals. Fig. 1.2, the classification used with a lowercase letter.) Each genus name must be unique, in this book, is the result of one such attempt. Although but species names need be unique only within a particu- biologists agree to use the Linnean framework for naming lar genus, so that the combination of genus and species organisms, they frequently disagree about the proper clas- names is unique and refers to only one kind of organism. sification of particular creatures. They may disagree as to (The name is always written in italics, or else underlined.) whether each of the gibbon types on different islands in Somewhere in a museum there is a preserved skeleton Southeast Asia is a distinct species or only a subspecies of a (or skull, or skin) that has been designated as the type single species. Some authorities may feel that gibbons and specimen for this species. The type specimen provides great apes should be placed in a single family, others that an objective reference for this species so that any scientist they should be placed in separate families. Once they have who thinks he or she may have discovered a different kind learned the Linnean hierarchy, many students are under- of monkey can examine the individual on which Cebus standably frustrated and annoyed to find that textbooks albifrons is based. often do not agree on the classification of different species. The Linnean system contains a hierarchy of levels There are, however, usually good reasons for the disagree- for grouping organisms into larger and larger units ments about primate classification, as we see in the follow- (Table 1.1). Within the genus Cebus, for example, there ing chapters. are s everal s pecies: Cebus albifrons, the white-fronted One reason for disagreements about primate classifica- capuchin; Cebus capucinus, the capped capuchin; Cebus tion is that the rules for distinguishing a genus, a family, olivaceous, the weeper capuchin; and others. Genera are or a superfamily are somewhat arbitrary. Scientists usu- grouped into families, families into orders, orders into ally set their own standards. The only generally accepted