Primate Adaptation and Evolution

By John Fleagle

Primate Adaptation and Evolution, Third Edition, is a thorough revision of the text of choice for courses in primate evolution. The book retains its grounding in the extant primate groups as the best way to understand the fossil trail and the evolution of these modern forms. However, this coverage is now streamlined, making reference to the many new and excellent books on living primate ecology and adaptation – a field that has burgeoned since the first edition of Primate Adaptation and Evolution.

By drawing out the key features of the extant families and referring to more detailed texts, the author sets the scene and also creates space for a thorough updating of the exciting developments in primate palaeontology – and the reconstruction through early hominid species – of our own human origins. This updated version covers recent developments in primate paleontology and the latest taxonomy, and includes over 200 new illustrations and revised evolutionary trees.

This text is ideal for undergraduate and post-graduate students studying the evolution and functional ecology of primates and early fossil hominids.

• Long-awaited revision of the standard student text on primate evolution
• Full coverage of newly discovered fossils and the latest taxonomy
• Over 200 new illustrations and revised evolutionary trees

• Language: English
• Publisher: Academic Press
• Release date: Mar 8, 2013
• ISBN: 9780123786333

John Fleagle

John Fleagle is a primatologist whose research combines field studies and functional morpho-logical analysis. He is interested in the adaptive radiation of primates during the last 50 million years. He has conducted paleobiological research in Egypt, Argentina, and Ethiopia and has studied living primates in Malaysia, Surinam, Brazil and Madagascar. Dr. Fleagle is a MacArthur Fellow.

Book preview

Preface

Primatology and primate evolution have changed considerably in the two and a half decades since the first edition of Primate Adaptation and Evolution was written. Like all other areas on knowledge, our knowledge of these subjects has increased dramatically, and the published literature manyfold. There are more species, more sites, more studies, more techniques, more analyses, more articles, more journals, and, hopefully, more understanding. But there is also more evidence of just how limited out current knowledge actually is, and how much it is likely to change in the future. This, like every other book, is perhaps best viewed as a progress report rather than a synthesis.

In this edition, every chapter has been revised and rewritten, some much more than others. All of the tables have been redone; there are many new figures; and most of the references are new. Some of these changes deserve further explanation.

The number of recognized primate species has risen dramatically in the past decade. There are many reasons for this. Partly it reflects an extensive increase in fieldwork in remote parts of the world that has generated a greater appreciation of the details of primate biogeography and diversity. In addition, the increasing influence of molecular systematics has generated new insights into the genetic diversity among primate populations. Finally, the widespread use of the Phylogenetic Species Concept has had a major effect on the abilities and willingness of systematists to describe and diagnose new or forgotten taxa. In general, I have used the IUCN Red List website in creating the tables of extant species in this volume. However, this increase in recognized primate species has created problems in the use of older literature for retrieving information about the behavior, ecology, body mass or limb proportions of individual taxa. For example, data that in previous decades, or previous editions of this book, were attributed to the single species of woolly lemur, Avahi laniger, may well have been derived from one of several other species now recognized as distinct in that genus. Readers should thus view the data in the tables especially as only rough estimates for the purpose of broad comparisons, not detailed analyses.

In previous editions, I tried to provide body mass estimates from most species of fossil primates derived from a single regression formula based on molar tooth dimensions. However, in the current edition I have relied more on estimates of the size of fossil species from a wide variety of sources in the literature, based on many different parameters. Thus many estimates across taxa are not methodologically comparable. They are meant to give the reader a general appreciation for the size of extinct taxa in a general sense and are not meant to be suitable for detailed analyses.

As in previous editions, I have included two types of references for each chapter. There are general references which provide broad reviews of the topics covered in that chapter. These are designed to provide more detailed documentation and discussion, and in some cases, alternative views on the material discussed in that chapter. In addition, there are numerous citations within the text of each chapter that are listed as cited references at the end of the chapter. These are not meant to provide a comprehensive or even representative documentation for the contents of the chapter. Rather they are meant to provide the readers with an entry into the literature regarding particular facts and ideas that I found interesting and/or significant. In particular, I have cited relatively recent publications that may not appear in the larger General references. However, in the early part of the twentieth century, I fully expect any reader will be able to find numerous additional references to any topic in this book through an online search.

This edition of Primate Adaptation and Evolution contains many additional illustrations. As with previous editions I have limited these to line drawings and black and white photos with an emphasis on comparisons rather than documentation and description. Nevertheless, I appreciate that these do not capture the remarkable beauty and diversity of living primates or the details of morphology that are available in various other media, including videos and 3-dimensional figures. Readers are urged to look more widely for additional illustrative materials, and I especially recommend All the World’s Primates (www.alltheworldsprimates.org).

This edition has benefitted from the generous advice, assistance and expertise of many people. The efforts and contributions of those listed in previous editions are still greatly appreciated. For help with this edition, I thank the following people, in no particular order: Alfred Rosenberger, Todd Disotell, Callum Ross, Colin Groves, Richard Kay, James Rossie, Tim Smith, Chris Kirk, Mark Coleman, Stephanie Maoilino, Doug Boyer, Steve Leigh, Andreas Koenig, Carola Borries, Charles Janson, Tim Clutton-Brock, Katie Hinde, Erin Vogel, Peter Lucas, Nate Dominy, Vivek Venkataraman, Diane Doran-Sheehy, Scott Suarez, Herman Pontzer, Patricia Wright, Chia Tan, Mireya Mayor, Shawn Lehman, Rachel Jacobs, Laurie Godfrey, Tim Ryan, Bill Jungers, Brigitte demes, Betsy Dumont, Suzanne Strait, Sara Martin, Anja Deppe, Ian Tattersall, Myron Shekelle, Dan Gebo, Marion Dagosto, Anna Nekaris, Anne Yoder, Christian Roos, Russ Mittermeier, Sharon Gursky, Peter Kappeler, Tony DiFiore, Marilyn Norconk, Alfred Rosenberger, Paul Garber, Anthony Rylands, Leila Porter, Mark Van Roosmalen, Barth Wright, Karen Wright, Scott McGraw, Joan Silk, Chris Gilbert, Eric Sargis, Alice Elder, Wendy Erb, David Fernandez, Jessica Rothman, Jessica Lodwick, Michael Steiper, Richard Wrangham, John Mitani, Dan Lieberman, Sarah Hrdy, Kristen Hawkes, Kim Hill, Kaye Reed, Jason Kamilar, Sandy Harcourt, Oliver Schulke, Julia Oster, Jon Bloch, Philip Gingerich, Frank Brown, Thure Cerling, Craig Feibel, Ian McDougall, Mary Silcox, Stephen Chester, Gregg Gunnell, Xijun Ni, Matt Cartmill, Ken Rose, Lawrence Flynn, Chris Heesy, Elwyn Simons, Nancy Stevens, Jorn Hurum, Blythe Williams, Walter Hartwig, Jonathan Perry, Marc Godinot, Chris Beard, Mark Klinger, Lauren Halenar, Siobhan Cooke, Alexa Krupp, Castor Cartelle, Ross MacPhee, Terry Harrison, Bill Sanders, Iyad Zalmout, Jay Kelley, John Kappelman, David Alba, Sergio Almecija, Salvador Moya-Sola, Isaac Casanovas-Vilar, David Pilbeam, Ellen Miller, Ari Grossman, Nina Jablonski, Rajeev Patnaik, Russ Ciochon, Brenda Benefit, Eric Delson, Martin Pickford, Mauricio Anton, Meave Leakey, The Turkana Basin Institute, Richard Leakey, Carol Ward, Michael Plavcan, Peter Ungar, The Kenya National Museum, Michel Brunet, Guy Franck, Bill Kimbel, Adam Gordon, Bernard Wood, Brian Richmond, Chris Stringer, Randall Susman, Fred Grine, Karen Baab,Philip Rightmire, David Strait, Ian Wallace, Gunter Brauer, Susan Larson, Zeray Alemseged, Tim White, John Shea, Lee Berger, and many others I may have overlooked.

As with previous editions, the heart of this book is the illustrations. Most of these are the due to the longterm efforts and unfailing patience of Stephen Nash and Luci Betti-Nash. In their talented hands even the most muddled ideas are somehow transformed into illustrations that are crisp and understandable.

Several people were especially helpful in the production of this edition. Mary Silcox provided the classification of plesiadapiforms. Stevie Carnation, Amanda Kingston, Rachel Jacobs, and Ian Wallace contributed herculean efforts in the construction and ordering of tables, figures, and references. Amanda and Ian were invaluable in correcting the proofs. Rachel wrote all of the teacher aids. Most of all, this edition owes its existence to the sustained efforts of Dr. Andrea Baden, whose scientific knowledge and judgment, editorial, graphic and photographic skills, and overall organizational abilities pulled it all together into a coherent volume.

Chapter 1

Adaptation, Evolution, and Systematics

Adaptation

Adaptation is a concept central to our understanding of evolution, but the term has proved very difficult to define in a simple phrase. One of the most succinct definitions has been offered by Vermeij (1978, p. 3): ‘An adaptation is a characteristic that allows an organism to live and reproduce in an environment where it probably could not otherwise exist.’ In the following chapters, we examine extant (living) and extinct (fossil) primates as a series of adaptive radiations – groups of closely related organisms that have evolved morphological and behavioral features enabling them to exploit different ecological niches. Adaptive radiations provide especially clear examples of evolutionary processes. The adaptive radiation of finches on the Galapagos Islands of Ecuador played an important role in guiding Darwin’s views on the origin of species.

Adaptation also refers to the process through which organisms obtain their adaptive characteristics. The primary mechanism of adaptation is natural selection. Natural selection is the process whereby any heritable features, anatomical or behavioral, that enhance the fitness of an organism relative to its peers, increase in frequency in the population in succeeding generations. Fitness, in an evolutionary sense, is reproductive success. It is important to remember that natural selection acts primarily through differential reproductive success of individuals within a population (Williams, 1966). However, there is considerable debate regarding the extent to which selection can also act at higher levels, including groups (Group Selection) and species (Species Selection).

Evolution

Evolution is modification by descent, or genetic change in a population through time. Although biologists consider most evolution to be the result of natural selection, there are other, non-Darwinian mechanisms that can and do lead to genetic change within a population. Genetic drift is change in the genetic composition of a population from generation to generation due to chance sampling events independent of selection. Founder effect is a more extreme change in the genetic makeup of a population that occurs when a new population is established by only a few individuals. This new population may sample only a small part of the variation found in the ancestral population. Thus, recessive alleles that are not expressed in the larger population may become more common or even fixed in the new population. In this way, the chance characteristics of a founder population can have dramatic effects on the subsequent evolution and adaptive diversity of a group of organisms.

The fact that the diversity of life is the result of evolution means that all organisms are related by virtue of sharing a common genetic ancestry in the distant past. However, it is also clear that living organisms are not a continuous spread of variation. The living world is composed of distinct kinds of organisms that we recognize as species. Although virtually all biologists recognize species as the natural units of life, defining exactly what a species is or how species form are more difficult problems. These are the problems that Darwin (1859) set out to explain, and they are still the subject of intense study and debate (e.g., Kimbel and Martin, 1993; Groves, 2001, 2012; DeQueiroz, 1998, 2007; Rosenberger, 2012).

Until recently, most biologists and anthropologists generally accepted the Biological Species Concept (BSC), in which species are defined as ‘groups of actually or potentially interbreeding natural populations that are reproductively isolated from other groups’ (Mayr, 1942). Although appealing, in that it emphasizes the genetic and phyletic distinctiveness of species through reproductive isolation, the Biological Species Concept is obviously impossible to apply to fossils or allopatric populations of living animals, and even difficult to apply to sympatric populations without detailed data on mating behavior and fertility (Tattersall, 1989; Groves, 2001, 2012). Moreover, as more and more ‘species’ have been sampled genetically, it has become clear that hybridization between presumed species has been very common in primate evolution (e.g., Detwiler, 2002; Zinner et al., 2011).

Many students of living organisms are more comfortable with a Mate Recognition Concept (Paterson, 1978, 1985; Masters, 1993). In this concept, species are defined as ‘the group of individuals sharing a common fertilization system’ (Paterson, 1985). A particularly important aspect of this common fertilization system is a specific mate-recognition system. Members of a species recognize one another as potential mates through such behavior or morphological features as vocalizations, mating displays, or ornamentation. Like the Biological Species Concept, the Mate Recognition Concept is virtually impossible to apply to extinct organisms.

In contrast with the Biological Species Concept and the Mate Recognition Concept, which are based on information about reproductive behavior, many paleontologists prefer a species concept based on morphological differences. The Phylogenetic Species Concept (Cracraft, 1983) is commonly adopted by students of phylogenetic systematics. In this approach, a species is ‘the smallest diagnosable cluster of individuals within which there is a parental pattern of ancestry and descent’. In this concept, a species is defined on the basis of morphological or genetic distinctions from other taxa (Cracraft, 1983). In principle, this could be based on a single feature. At present, most phylogenetic analyses, and most systematic revisions, generally follow a Phylogenetic Species Concept as species are identified by detailed morphological features or aspects of their DNA. However, the question of how many genetic differences are needed to identify a separate species is a critical, but largely unresolved, issue in primate phylogeny (Groeneveld et al., 2009).

Other researchers, using what may be called a Phenetic Fossil Species Concept, would argue that species defined morphologically should have approximately the same amount of metrical variation as extant populations (e.g., Gingerich and Schoeninger, 1979; Cope, 1993). This is often a very useful criterion when one has a continuously changing time-successive lineage in the fossil record, in which the endpoints may be very different but individual samples overlap.

Most biologists agree that a species is a distinct segment of an evolutionary lineage, and many of the differences among species concepts reflect attempts to find criteria that can be used to identify species based on different types of information, such as behavioral observations of living populations, genetic sequences, or morphological information from teeth, skull, or pelage. Some of the diversity of species concepts may be more useful in distinguishing species at different phases of their formation (de Quieroz, 1998, 2007). Paradoxically, the greatest challenge to species identification often comes not from incomplete information, but from those rare paleontological instances in which there is a continuous temporal sequence of populations undergoing directional selection (e.g., Rose and Bown, 1993). As noted above, the endpoints are clearly differentiable, but any species boundary is necessarily arbitrary (see Chapter 18).

Phylogeny

Evolutionary change within a population can take place at different rates and can yield different results. There are several terms available to describe how and why different patterns of evolutionary change occur. What is more, numerous theories exist about how common these different patterns of evolutionary change are in the history of life. The pattern in which a lineage undergoes gradual change over time is called anagenesis. Cladogenesis is the division of a single lineage into two lineages. Gradual change in the morphology of a population of organisms through time, either anagenetic or cladogenetic, is often called phyletic gradualism. This type of evolutionary pattern is very common in the fossil record, and many biologists believe that most evolutionary change has been of this type.

The rates of evolutionary change that take place in populations through time may vary considerably, theoretically over several orders of magnitude. In addition, directional selection may shift over the course of relatively short time periods due to climatic fluctuations. Some paleontologists argue that the most common type of evolutionary change is punctuated equilibrium, in which the morphology of most species is essentially stable (in equilibrium) for long periods of time, and that speciation events are the result of rapid morphological and genetic shifts (or punctuations) over brief periods of evolutionary time so that intermediate forms are rarely recovered (e.g., Gould and Eldridge, 1993). Unfortunately, the punctuated equilibrium model is very difficult to distinguish from a discontinuous fossil record and is generally defined in a way that virtually precludes the possibility of determining how often it actually takes place. Overall, it is now well-documented that evolutionary change has taken place at many different rates.

The branching pattern of successive species that results from numerous cladogenetic events is a phylogeny. Because this book deals with the adaptive radiations of primates, we are interested in reconstructing the evolutionary branching sequence, or phylogeny, of various primate groups to see how they are related to one another. Although some of us can trace our own genealogies (or those of our pets) through several generations, tracing the genealogical relationships among all primates is a much more daunting undertaking. The evolutionary radiation of primates has taken place over tens of millions of years of geological time and has involved thousands of species, millions of generations, and billions of individuals. Moreover, the records available for reconstructing primate phylogeny are meager, consisting of individuals of fewer than 300 living species and occasional bony remains of several hundred extinct species drawn from various parts of the world at various times during the past 65 million years.

The methods we use to reconstruct phylogenies are based primarily on identifying groups of related species through similarities in their morphology and in the molecular sequences of their genetic material. However, rather than just looking at overall similarity, most biologists agree that organisms should be grouped together on the basis of shared specializations (or shared derived features) that distinguish them from their ancestors. For example, body hair is a shared specialization that unites humans, apes, monkeys, and cats as mammals and distinguishes them from other types of vertebrates, whereas the common possession of a tail by many monkeys, lizards, and crocodiles is an ancestral feature that is of no particular value in assessing the evolutionary relationships among these organisms, since their common ancestor had a tail. On the other hand, the absence of a tail in apes and humans represents a derived specialization that sets us apart from our ancestors (Fig. 1.1). The common possession of a group of specializations by a cluster of species or genera is interpreted as indicating that this cluster shares a unique heritage relative to other related species. Most current studies of primate phylogeny are based on extensive analysis of morphological features and/or amino acid sequences from parts of a species’ genome, using sophisticated computer programs to determine the pattern of shared derived similarities (Kay et al., 1997; Disotell, 2011; Perelman et al., 2011).

FIGURE 1.1 Shared specializations and ancestral features.

Unfortunately, not all derived similarities among organisms are indicative of a unique heritage. Animals have frequently evolved morphological similarities independently. In addition to apes and humans, for example, a few monkey species and a few prosimians (as well as frogs) have lost all or most of their tail. The biologist’s task in reconstructing phylogeny is to distinguish those specializations that are the result of a unique heritage from those that are not. The sameness of features that results from common ancestry is called homology, and identical features that are the result of a common ancestry are homologous. In contrast, the presence of similar features in different species that is not the result of a common inheritance is described as homoplasy.

Homoplasy is a very common phenomenon in evolution (Sanderson and Hufford, 1996). Most analyses of morphological evolution find that nearly half of all similarities are the result of homoplasy rather than common ancestry. There are several types of homoplasy and many factors that cause it to be such a common phenomenon. The evolution of superficially similar features in different lineages, such as the wings of bats and the wings of birds, is often called convergence. In contrast, parallelism refers to the independent evolution of identical features in closely related organisms, such as the independent evolution of white fur in many lineages of monkey. Reversal refers to an evolutionary change in an organism that resembles the condition found in an earlier ancestor, such as the presence of hair on the fingers of humans descended from apes with hairless digits. In many cases, homoplasy is the result of natural selection for similar functional adaptations. For example, larger animals may face similar mechanical problems. In addition, homoplasy may also reflect the fact that evolutionary pathways are constrained by development and available genetic potential. In molecular evolution, the potential for homoplasy is dictated by the limited number of amino acids making up the genetic code. Although many people feel that some morphological regions, such as teeth, skulls, or postcranial elements, are more prone to homoplasy than others, most comparative assessment show that this is not the case. Moreover, features that show considerable homoplasy in one group of animals may show no homoplasy in other groups. Most significantly, homoplasy is a phenomenon that can only be identified in a retrospective analysis after a phylogeny has been constructed (Begun, 2007). Although frequently treated as an undesirable distraction in attempts to reconstruct phylogeny, homoplasy is an important evolutionary phenomenon that deserves greater study and consideration (Hall, 1999; Lockwood and Fleagle, 1999; Kay and Fleagle, 2010).

Taxonomy and Systematics

Taxonomy is a means of ordering our knowledge of biological diversity through a series of commonly accepted names for organisms. If scientists wish to communicate about animals and plants and to discuss their similarities and differences, they need a standard system of names both for individual types of organisms and for related groups of organisms. For example, the white-fronted capuchin monkey of South America, known to many people as the organ grinder monkey, goes by over a dozen different names among the different tribal and ethnic groups of South America. To scientists around the world, however, this species is known by a single name, Cebus albifrons. The practice of assigning every biological species, living or fossil, a unique name composed of two Latin words was initiated by Carolus Linnaeus, a Swedish scientist of the eighteenth century whose system of biological nomenclature is universally followed today.

Under the Linnean system, Cebus is the name of a genus (pl. genera), or group of animals; in this case several kinds of capuchin monkey (the name of a genus is always capitalized). The word albifrons, the species name, refers to a particular type of capuchin monkey, the white-fronted capuchin monkey. (A species name always begins with a lowercase letter.) Each genus name must be unique, but species names need be unique only within a particular genus, so that the combination of genus and species names is unique and refers to only one kind of organism. (The name is always written in italics, or else underlined.) Somewhere in a museum there is a preserved skeleton (or skull, or skin) that has been designated as the type specimen for this species. The type specimen provides an objective reference for this species so that any scientist who thinks he or she may have discovered a different kind of monkey can examine the individual on which Cebus albifrons is based.

The Linnean system contains a hierarchy of levels for grouping organisms into larger and larger units (Table 1.1). Within the genus Cebus, for example, there are several species: Cebus albifrons, the white-fronted capuchin; Cebus capucinus, the capped capuchin; Cebus olivaceous, the weeper capuchin; and others. Genera are grouped into families, families into orders, orders into classes, and classes into phyla. For particular lineages, these basic levels are often further subdivided or clustered into semiorders, suborders, infraorders, superfamilies, subfamilies, tribes, subgenera, or subspecies. For convenience, names at different levels of the hierarchy are often given distinctive endings. Family names usually end in dae, superfamily names in oidea, and subfamily names in inae.

TABLE 1.1

Classification of the White-fronted Capuchin monkey

∗Indicates only one of several common classifications (see Chapter 5)

In the science of classifying organisms, systematics, we attempt to apply the tidy Linnean system to the untidy, unlabeled world of animals. Fig. 1.2, the classification used in this book, is the result of one such attempt. Although biologists agree to use the Linnean framework for naming organisms, they frequently disagree about the proper classification of particular creatures. They may disagree as to whether each of the gibbon types on different islands in Southeast Asia is a distinct species or only a subspecies of a single species. Some authorities may feel that gibbons and great apes should be placed in a single family, others that they should be placed in separate families. Once they have learned the Linnean hierarchy, many students are understandably frustrated and annoyed to find that textbooks often do not agree on the classification of different species. There are, however, usually good reasons for the disagreements about primate classification, as we see in the following chapters.

FIGURE 1.2 A classification of extant primate genera. Modified from Disotell, 2008.

One reason for disagreements about primate classification is that the rules for distinguishing a genus, a family, or a superfamily are somewhat arbitrary. Scientists usually set their own standards. The only generally accepted rules are for species. However, as already discussed, many different ways have been proposed for distinguishing what a species is. Living species of mammals are remarkably consistent in their metric variability (Gingerich and Schoeninger, 1979; but see Tattersall, 1993), and we can use this standard to identify species in the fossil record. The limits for genera and families are, however, much more arbitrary.

It is generally agreed that classification should reflect phylogeny, and that taxonomic groups such as families, superfamilies, and suborders should be monophyletic groups: that is, they should have a single common ancestor that gave rise to all members of the group. Many also feel that taxonomic groups should be holophyletic groups as well: they should contain all the descendants of their common ancestor, not just some of them. But it is often not practical or possible to achieve this unambiguously, and classifications are often compromises compatible with several possible phylogenies. In addition, many biologists feel that classification should reflect not only phylogeny but also major adaptive differences, even among closely related species. For example, most biologists now agree that humans are much more closely related to chimpanzees and gorillas than to orangutans. Thus a true phyletic taxonomy would group humans with the African apes and the orangutan in a separate grouping. In spite of this, many experts still place humans in a separate family, the Hominidae, and all living great apes in a common family, the Pongidae, because they believe that humans have departed further from the common ancestor of humans and great apes than have chimpanzees and gorillas. In this arrangement, shown by the shading in Fig. 1.3, the family Pongidae is called a paraphyletic grouping because some of its members (chimpanzees and gorillas) are more closely related to a species (humans) placed in another family than they are to other members (orangutans) of their own family (Fig. 1.3). The taxonomy used in this book (Fig. 1.2) uses a more natural grouping in which all great apes and humans are placed in a single family, Hominidae, with orangutans in one subfamily, the Ponginae, and the African apes and human in a separate subfamily, Homininae. However, paraphyletic groups are commonly used when taxonomic schemes include both extant forms and fossils that may be broadly ancestral to many later groups (e.g. Cartmill, 2012).

FIGURE 1.3 A strictly phyletic classification recognizes that humans, chimpanzees, and gorillas are more closely related to each other than any of them are to orangutans; the latter are therefore grouped separately as the only pongids. A more traditional classification recognizes adaptive differences; in this case, chimpanzees and gorillas are classified with orangutans (pongids), and humans are grouped separately (hominids) because of the great degree of adaptation that distinguishes humans from even their closest primate relatives.

References

General References

1. Groves CP. Primate Taxonomy. Washington: Smithsonian Institution; 2001.

2. Rowe N, Myers M, eds. All the World’s Primates. 2011; In: http://www.alltheworldsprimates.org/; 2011.

Cited References

1. Begun DR. How to identify (as opposed to define) a homoplasy: Examples from fossil and living great apes. J Hum Evol. 2007;52:559–572.

2. Cartmill M. Primate origins, human origins, and the end of higher taxa. Evol Anthropol. 2012;21:208–220.

3. Cope D. Measures of dental variation and indicators of multiple taxa in samples of sympatric Cercopithecus species. In: Kimbel WH, Martin LB, eds. Species, Species Concepts, and Primate Evolution. New York: Plenum Press; 1993;211–238.

4. Cracraft J. Species concepts and speciation analysis. Curr Ornithol. 1983;1:159–187.

5. Darwin C. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. London: John Murray; 1859.

6. deQueiroz K. The general lineage concept of species, species criteria, and the process of speciation: A conceptual unification and terminological recommendations. In: Howard DJ, Berlocher SH, eds. Endless Forms: Species and Speciation. Oxford: Oxford University Press; 1998;57–75.

7. deQueiroz K. Species concepts and species delimitation. Syst Biol. 2007;56:879–886.

8. Detwiler KM. Hybridization between red-tailed monkeys (Cercopithecus ascanius) and blue monkeys (C. mitis) in East African forests. In: Glenn ME, Cords M, eds. The Guenons: Diversity and Adaptation in African Monkeys. New York: Kluwer Academic/Plenum Publishers; 2002;79–97.

9. Disotell TR. Primates Phylogenetics Encyclopedia of Life Sciences. Hoboken: John Wiley & Sons; 2008.

10. Gingerich PD, Schoeninger MJ. Patterns of tooth size variability in the dentition of Primates. Am J Phys Anthropol. 1979;51:457–566.

11. Gould SJ, Eldridge N. Punctuated equilibrium comes of age. Nature. 1993;366:223–227.

12. Groeneveld LF, Weisrock DW, Rasoloarison RM, Yoder AD, Kappeler PM. Species delimitation in lemurs: Multiple genetic loci reveal low levels of species diversity in the genus Cheirogaleus. Bmc Evol Biol. 2009;9:30.

13. Groves C. Primate Taxonomy. Washington DC: Smithsonian Institution Press; 2001.

14. Groves C. Why taxonomic stability is a bad idea, or why are there so few species of primates (or are there?). Evol Anthropol. 2001;10:192–198.

15. Groves C. Species concept in primates. Am J Primatol. 2012;74:687–691.

16. Hall BK, Novartis Staff, eds. Homology. Chichester: John Wiley & Sons Ltd; 1999.

17. Kay RF, Fleagle JG. Stem taxa, homoplasy, long lineages and the phylogenetic position of Dolichocebus. J Hum Evol. 2010;59:218–222.

18. Kay RF, Ross C, Williams BA. Anthropoid origins. Science. 1997;275:797–804.

19. Kimbel WH, Martin LB, eds. Species, Species Concepts, and Primate Evolution. New York: Plenum Press; 1993.

20. Lockwood CA, Fleagle JG. The recognition and evaluation of homoplasy in primate and human evolution Yrbk Phys. Anthropol. 1999;42:189–232.

21. Masters JC. Primates and paradigms: Problems with the identification of genetic species. In: Kimbel WH, Martin LB, eds. Species, Species Concepts, and Primate Evolution. New York: Plenum Press; 1993;43–64.

22. Mayr E. Systematics and the Origin of Species. New York: Columbia University Press; 1942.

23. Paterson HEH. More evidence against speciation by reinforcement. S Afr J Sci. 1978;74:369–371.

24. Paterson HEH. The recognition concept of species. In: Vrba ES, ed. Species and Speciation. Pretoria: Transvaal Museum; 1985;21–29.

25. Perelman P, Johnson WE, Roos C, Seuanez N, Horvath JE, et al. A molecular phylogeny of living primates. PLos Genetics. 2011;7:e1001342.

26. Rose KD, Bown TM. Species concepts and species recognition on Eocene primates. In: Kimbel WH, Martin LB, eds. Species, Species Concepts, and Primate Evolution. New York: Plenum Press; 1993;299–330.

27. Rosenberger AL. New World monkey nightmares: Science, art, use, and abuse (?) in platyrrhine taxonomic nomenclature. Am J Primatol. 2012;74:692–695.

28. Sanderson MJ, Hufford L. Homoplasy: The Recurrence of Similarity in Evolution. San Diego: Academic Press; 1996.

29. Tattersall I. The roles of ecological and behavioral observation in species recognition among primates. Hum Evol. 1989;4:117–124.

30. Tattersall I. Species concepts and species identification in human evolution. J Hum Evol. 1992;22:341–349.

31. Tattersall I. Speciation and morphological differentiation on the genus Lemur. In: Kimbel WH, Martin LB, eds. Species, Species Concepts, and Primate Evolution. New York: Plenum Press; 1993;163–176.

32. Vermeij GJ. Biogeography and Adaptation: Patterns of Marine Life. Cambridge, Massachusetts: Harvard University Press; 1978.

33. Williams CC. Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought. Princeton, New Jersey: Princeton University Press; 1966.

34. Zinner D, Arnold ML, Roos C. The strange blood: Natural hybridization in primates. Evol Anthropol. 2011;20:96–103.

Chapter 2

The Primate Body

Primate Anatomy

Fossil and living primates are an extraordinarily diverse array of species. Some are among the most generalized and primitive of all mammals; others show morphological and behavioral specializations unmatched in any other mammalian order. This diversity in structure, behavior, and ecology and its evolutionary history are the subjects of this book. The purpose of this chapter is to establish an anatomical frame of reference – a survey of features common to all (or almost all) primates. This chapter, then, provides pictures and descriptions of primate anatomy and preliminary indications of those anatomical features that have undergone the greatest changes in primate evolution.

Compared to most other mammals, we primates have retained relatively primitive bodies. Some of us are specialized in that we have lost our tails, and many have a relatively large brain. But no primates have departed so dramatically from the common mammalian body plan as bats, whose hands have become wings; horses, whose fingers and toes have reduced to a single digit; or baleen whales, who have lost their hindlimbs altogether, adapted their tails into flippers, and replaced their teeth with great hairlike combs. The anatomical features that distinguish the bones and teeth of primates from those of many other mammals are the result of subtle changes in the shape and proportion of homologous elements, rather than major rearrangements, losses, or additions of body parts. We generally find the same bones and teeth in all species of primates, with only minor differences reflecting different diets or locomotor habits. The fact that humans are constructed of the same bony elements as other primates (and generally other mammals) is a major piece of evidence demonstrating our evolutionary origin.

Size

Size is a basic aspect of an organism’s anatomy and plays a major role in its ecological adaptations (Jungers, 1985). It is a feature that can be readily compared, both among living species and between living and fossil primates. Adult living primates range in size from mouse lemurs and pygmy marmosets, with a mass less than 100 g, to male gorillas with a body mass of over 200 kg (Fig. 2.1). The fossil record provides evidence of a few extinct primates from early in the age of mammals that were much smaller (probably as small as 20 g) and at least one, Gigantopithecus blacki from the Pleistocene of China (see Chapter 16), that was much larger (probably over 300 kg). In their range of body sizes, primates are one of the more diverse orders of living mammals. As a group, however, primates are rather medium-sized mammals (Fig. 2.2) – larger than most insectivores and rodents and smaller than most ungulates, elephants, and marine mammals.

FIGURE 2.1 A mouse lemur (Microcebus) and a gorilla (Gorilla), the smallest and largest living primates.

FIGURE 2.2 Size ranges for various orders of mammals, including primates. The solid lines include all living species; the dotted lines include all known living and fossil primates.

Cranial Anatomy

The anatomy of the head, or cranial region, plays a particularly important role in studies of primate adaptation and evolution. Many of the anatomical features that have traditionally been used to delineate the systematic relationships among primates are cranial features, and most of our knowledge of fossil primates is based on this region.

Bones of the Skull

The adult primate skull (Figs 2.3, 2.4) consists of many different bones that together form a hollow, bony shell that houses the brain and special sense organs and also provides a base for the teeth and chewing muscles. Only the lower jaw, or mandible, and the three bones of the middle ear are separate, movable elements; the others are fused into a single unit, the cranium. This unit can be roughly divided into two regions: a more posterior braincase, or neurocranium, and a more anterior facial region, or splanchnocranium.

FIGURE 2.3 The skull of a human (Homo sapiens).

FIGURE 2.4 Skulls of a capuchin monkey (Cebus) and a lemur (Lemur) showing how differences in the size and shape of individual bones contribute to overall differences in skull form..

The braincase serves as a protective bony case for the brain, a housing for the auditory region, and an area of muscle attachment for the larger chewing muscles and the muscles that move the head on the neck. Three paired flat bones – the frontal, parietal, and temporal bones – make up the top and sides of the braincase. (The temporal bone is a relatively complicated bone with several distinct parts.) The posterior and inferior surfaces of the braincase are formed by a single bone, the occipital, which also has a number of distinct parts. A complex, butterfly-shaped bone, the sphenoid, forms the anterior surface of the braincase and joins it with the facial region.

The facial region is formed by the maxillary and premaxillary bones, which contain the upper teeth; the zygomatic bone, which forms the lateral wall of the orbit, or eye socket; the nasal bones, which form the bridge of the nose; and numerous small bones that make up the orbit and the internal nasal region. The lower jaw, or mandible, contains the lower teeth. In many mammals, and in most prosimian primates, the two halves of the mandible are loosely connected anteriorly in such a way that they can move somewhat independently of one another. This joint is called the mandibular symphysis. In higher primates, including humans, the two sides of the lower jaw are fused to form a single bony unit.

Although all primate skulls are made up of these same components, they can have very different appearances, depending on the relative size and shape of individual bones (Figs. 2.3, 2.4). The skull functions as a base and structural framework for the first part of the digestive system and as a housing for the brain and special sense organs of sight, smell, and hearing. Much of the diversity in primate skull shape reflects the need for this single bony structure to serve numerous, often conflicting functions. For example, although the size of the orbits is most directly related to the size of the eyeball and to whether a species is active during the day or the night, it influences the shape and position of the nasal cavity and the space available for chewing muscles.

Teeth and Chewing

Many parts of the head and face are important in the acquisition and initial preparation of food. The lips, cheeks, teeth, mandible, tongue, hyoid bone (a small bone suspended in the throat beneath the mandible), and muscles of the throat all participate in this complex activity; and many of these same parts also play a role in communication and sound production. The parts of the skull that can be linked most clearly to dietary habits are the teeth, the mandible, and the chewing muscles that move the lower jaw.

Teeth, more than any other single part of the body, provide the basic information underlying much of our understanding of primate evolution. Because of their extreme hardness and compact shape, teeth are the most commonly preserved identifiable remains of most fossil mammals. But teeth are more than just plentiful: they are also complex organs that provide considerable information about both the phyletic relationships and the dietary habits of their owners. Because of the importance of teeth in evolutionary studies, there is an extensive but fairly simple terminology for dental anatomy.

All primates have teeth in both the upper jaw (maxilla) and the lower jaw (mandible), and, like most features of the primate skeleton, primate teeth are bilaterally symmetrical – the teeth on one side are mirror images of those on the other. Each primate jaw normally contains four types of teeth (Fig. 2.5). These are, from front to back, incisors, canines, premolars, and molars. The number of teeth a particular species possesses is usually expressed in a dental formula. The human dental formula is 2.1.2.3./2.1.2.3., indicating that we normally have two incisors, one canine, two premolars, and three molars on each side of both the upper and the lower jaw for a total of 32 adult teeth. In most primate species, formulae for the upper and lower dentition are the same. In addition to adult (or permanent) teeth, primates have an earlier set of teeth, the milk (or deciduous) dentition, which precedes the adult incisors, canines, and premolars and occupies the same positions in the jaws. The human milk dentition, for example, contains two deciduous incisors, one deciduous canine, and two deciduous premolars (often called ‘milk molars’) in each quadrant, for a total of 20 deciduous teeth.

FIGURE 2.5 The dentition of a siamang (Symphalangus) showing two incisors (I), one canine (C), two premolars (P), and three molars (M) in each dental quadrant for a dental formula of 2.1.2.3/2.1.2.3.

The three main cusps of an upper molar (Fig. 2.6) are the paracone, the metacone, and the protocone. The triangle formed by these cusps is called the trigon. Many primates have evolved a fourth cusp distal to the protocone, called the hypocone. Small cusps adjacent and lingual to these major cusps are called conules (the paraconule and the metaconule). Accessory folds of enamel on the buccal (cheek-side) surface of the tooth are called styles, and an enamel belt around the tooth is referred to as a cingulum. Shallow areas between crests are called basins.

FIGURE 2.6 Major parts of the upper and lower teeth of a primitive primate.

The basic structure of a lower molar in a generalized mammal (Fig. 2.6) is another triangle, this one pointing toward the cheek side. The cusps have the same names as those of the upper molars, but with the suffix -id added (protoconid, paraconid, and metaconid). This basic triangle in the front of a lower molar is called the trigonid. In primates and all but the most primitive mammals there is an additional area added to the distal end of this primitive trigonid. This extra part, the talonid, is formed by two or three additional cusps: the hypoconid on the buccal side, the entoconid on the lingual (tongue) side, and, in many species, a small, distal-most cusp between these two, the hypoconulid.

Primate dentitions are involved in two different aspects of feeding. The anterior part of the dentition, the incisors and often the canines (together with the lips and often the hands), is primarily concerned with ingestion – the transfer of food from the outside world into the oral cavity in manageable pieces that can then be further prepared by the cheek teeth (the molars and premolars). The subsequent breakdown of food items by chewing is called mastication.

The molars and premolars of primates break down food mechanically in three ways: (a) by puncture-crushing or piercing the food with sharp cusps; (b) by shearing the food into small pieces, that is, by trapping particles between the blades of enamel that are formed by the crests that link cusps; and (c) by crushing or grinding food in mortar-and-pestle fashion between rounded cusps and flat basins. Different types of food require different types of dental preparation before swallowing, and it is possible to relate the various characteristics of both the anterior teeth (for obtaining and ingesting objects) and the cheek teeth (for puncturing, shearing, or grinding) to diets with different consistencies (as discussed in Chapter 9).

The movement of the lower jaw relative to the skull in both ingestion and chewing (mastication) is brought about by four major chewing muscles that originate on the skull and insert on different parts of the lower jaw (Fig. 2.7). The largest is the temporalis, which has a fan-shaped origin on the side of the skull and inserts onto the coronoid process of the mandible. The second large muscle is the masseter, which originates from the zygomatic arch and inserts on the lateral surface of the mandible. Both of these muscles close the jaw when they contract. There are two smaller muscles on the inside of the jaw: the medial and lateral pterygoids. Much of the bony development of the primate skull seems to be related to the size and shape of these muscles and to the magnitude and direction of the forces generated in the skull during chewing. These muscular differences have in turn evolved to meet mechanical demands associated with dietary differences.

FIGURE 2.7 Anterior and lateral views of a primate skull showing the major chewing muscles.

Tongue and Taste

In primates, as in all mammals, the tongue forms the floor of the oral cavity. Primate tongues vary considerably in shape (Fig. 2.8). Part of this variation reflects differences in the shape of the oral cavity itself and is determined by the relative breadth of the anterior dentition. However, part of this variation is related to differences in the function of the tongue as an organ of taste, touch, and vocalization. For example, in all strepsirrhines there is a distinctive projection from the underside of the tongue, the sublingua, which serves to clean the tooth comb (Fig. 2.9). The brown lemur, Eulemur fulvus, has a series of highly sensitive conical structures at the tip of its tongue; feathery projections have been described on the tip of the tongue of Eulemur rubriventer that seem to be associated with its habit of licking nectar from flowers (Hofer, 1981; Overdorff, 1992); and the fork-marked lemur, Phaner, has a long, muscular tongue that it uses while feeding on exudates (gums and resins). Among higher primates, humans have a very unusual tongue, in that it extends very far posteriorly and plays a major role in vocalization by changing the shape of the throat. Although all primate tongues contain the taste buds (papillae) that are responsible for the sense of taste, the size, shape, and number of different taste sensors vary considerably from species to species (Fig. 2.8; see also Hladik and Simmen, 1997; Muchlinski et al., 2011).

FIGURE 2.8 Superior view of the tongues of five primates showing differences in overall shape and in the distribution of taste papillae.

FIGURE 2.9 The tongue of a ring-tailed lemur (Lemur catta) showing the serrated sublingua that is used to clean the toothcomb.

Muscles of Facial Expression

Another aspect of cranial anatomy in primates that deserves special consideration is facial musculature (Fig. 2.10). Among primates, and especially in humans, the muscles of facial expression are more highly developed and differentiated into separate units than among any other groups of mammals (Huber, 1931). It is these muscles that make possible the range of visual expressions that characterizes and facilitates the complex social behavior of primates (Dobson 2009, 2012).

FIGURE 2.10 Muscles of facial expression in a macaque (Macaca), a young orangutan (Pongo), and a human (Homo sapiens). Note the increasing differentiation of individual muscles, which enables finer control of expressions.

The Brain and Senses

The structural shape of the skull – the development of bony buttresses and crests, as well as the relative positioning of the face and the neurocranium – seems to be greatly influenced by the size and functional requirements of the masticatory system. However, the relative sizes of many parts of the skull, such as the neurocranium and the orbits, as well as the size and position of various openings in the skull, seem more directly related to the skull’s role in housing the brain and the sense organs responsible for smell, vision, and hearing. The ways in which different primates use these senses in their daily activities is critical for understanding the variation among species in their anatomy (Dominy et al., 2001).

The Brain

The brain is the largest organ in the head, and its relative size is an important determinant of skull shape among primates. Relative to body weight, primates have the largest brains of any terrestrial mammals; only marine mammals are comparably brainy. There are, however, differences in relative brain size among primates. Lemurs, lorises, and tarsiers all have relatively small brains compared to monkeys and apes, and human brains are relatively enormous. Still, the brain is a complex organ with many parts, and although some parts of primate brains are relatively large by mammalian standards, others are relatively small. In gross morphology, a primate brain can be divided into three parts (Fig. 2.11), the brainstem, the cerebellum, and the cerebrum. Each part has very different functions, and each is made up of many different functionally distinct sections.

FIGURE 2.11 Lateral view of the brains of a lemur (Lemur), a tarsier (Tarsius), a chimpanzee (Pan), and a human (Homo sapiens), showing differences in relative size of the parts of the brain. Note especially the differences in size of the olfactory bulb and the size and development of convolutions on the cerebral hemispheres.

The brainstem forms the lower surface and base of the brain. It is an enlarged and modified continuation of the upper part of the spinal cord and is the part of the primate brain that differs least from that found among other mammals and lower vertebrates. The brainstem is concerned with basic physiological functions such as reflexes, control of heartbeat and respiration, and temperature regulation, as well as the integration of sensory input before it is relayed to ‘higher centers’ in the cerebrum. Many of the cranial nerves, which are responsible for innervation of such things as the organs of sight and hearing and the muscles of the orbit and face, arise from the brainstem. Very little of the primate brainstem is visible in either a lateral or a superior view; it is covered by two areas that have become large and specialized: the cerebellum and the cerebral hemispheres.

The cerebellum, which lies between the brainstem and the posterior part of the cerebrum, is a developmental outgrowth of the caudal region of the brainstem. It is concerned primarily with control of movement and with motor coordination. Compared to other mammals, primates have a relatively large cerebellum.

The paired cerebral hemispheres are the part of the brain that has undergone the greatest change during primate evolution. It is in this part that we find the greatest differences between primates and other mammals and the greatest differences among living primates (Fig. 2.11). Gigantic cerebral hemispheres are one of the hallmarks of human evolution. Anatomically, this part of the brain is divided into lobes named for the bones immediately overlying them – frontal, parietal, temporal, and occipital. In most primates, the surface of the cerebral hemispheres is covered with convolutions made up of characteristic folds, or gyri, which are separated by grooves, or sulci. The development of these convolutions is most apparent in larger species, and reflects the fact that the most functionally significant part of the cerebrum, the gray matter, lies at the surface. The convolutions or foldings of the brain surface provide a greater surface area for the cerebral hemispheres, relative to brain or body volume, than would be provided by a smooth surface.

Overall, the cerebral hemispheres are involved with recognition of sensations, with voluntary movements, and with mental functions such as memory, thought, and interpretation. Different regions of the cerebrum (i.e., specific gyri) can be related to particular functions (Fig. 2.12). The central sulcus, for example, separates an anterior gyrus related to voluntary movement from a more posterior gyrus concerned with sensation. Within each of these areas it is possible to identify more specific regions concerned with voluntary movement or sensation of particular parts of the body. In addition, there are other parts of the cerebral hemispheres, called association areas, which are related to the integration of input from several different senses (such as hearing and vision) and to specific tasks, such as language and speech. Two particularly well developed association areas in the human brain are those related to language: Broca’s area in the frontal lobe and Wernike’s area in the parietal and temporal lobes.

FIGURE 2.12 Important functional areas of the human brain.

Although the brain is a soft structure, primate brains often leave their mark on the bony morphology of the skull. Size (in particular, volume) is an obvious feature of a primate brain that can be determined from a skull. Furthermore, in many species, sulci and gyri also leave impressions on the internal surface of the cranium. Such impressions on fossil skulls can provide limited information about the development of different functional regions on the cerebral hemispheres of extinct primates.

The nerves that take signals to and from the brain enter and leave the cranial cavity through various holes, called foramina, in the skull bones. The largest of these holes is the foramen magnum, through which the spinal cord passes. The many smaller foramina vary considerably in size and position among living primates and are widely used in systematics. In a few cases, it seems possible to correlate the size of a foramen carrying a specific nerve to the development of a particular function or anatomical region.

Foramina also serve as passages for the arteries that supply blood to the brain and other cranial structures, and for the veins that drain those same structures. The pathway of the blood supply to the brain shows a number of distinctly different patterns among living primates, (Fig. 2.13). Although we know little about the functional significance of these differences, they have proved useful in sorting the phyletic relationships among many living and fossil primate species. The major blood supply to the head in primates comes from two branches of the common carotid artery at the base of the neck. The external carotid is responsible primarily for supplying structures in the neck and face; the internal carotid (along with the vertebral arteries) supplies the brain and the eye. The internal carotid artery enters the cranial cavity as two distinct arteries, a stapedial artery passing through the stapes bone and a promontory artery that generally lies medial to the stapedial artery and crosses the promontorium, a raised surface in the middle ear, to enter the cranial cavity further anteriorly. In most lemurs, for example, the stapedial is the larger artery; in tarsiers, New World monkeys, Old World monkeys, apes, and humans, the stapedial is generally absent in adults and the promontory provides most of the blood supply to the brain. In lorises, galagos, and cheirogaleids, a branch of the external carotid artery, the ascending pharyngeal, provides the major blood supply to the front part of the brain (Fig. 2.13).

FIGURE 2.13 Cranial external blood supply in several types of living primates. In all living primates, the vertebral arteries supply blood to the brain; however, species differ considerably in the relative contributions of the stapedial and promontory branches of the internal carotid artery, and of the ascending pharyngeal branch of the eternal carotid artery. In the lemur (Lemur), the stapedial branch provides the major arterial supply to the anterior part of the brain; in a slow loris (Nycticebus) the blood to the front of the brain comes from a large ascending pharyngeal artery; in macaques (Macaca) and all higher primates, the promontory branch of the internal carotid provides the major arterial blood supply to the anterior part of the brain.

Nasal Region and Olfaction

In many mammals, smell is the dominant sensory mode. It provides much of the information on which animals rely to find their way around, locate their food, locate potential predators, communicate with their kin and neighbors, and determine the sexual status of potential mates. Among more diurnal (active during the day) higher primates, smell seems to be less important for some of these functions than other senses such as vision, but even for these species, this most basic of senses has not been abandoned. In most primate species, it still plays an important – albeit relatively poorly understood – role in reproduction, communication, and food evaluation.

The sensation of smell is carried by the olfactory nerves, which end in paired swellings, the olfactory bulbs, which lie under the large frontal lobes of most primates (Fig. 2.11). The olfactory nerves receive their input from the special sensory membranes lining the scroll-like turbinates of the internal nasal cavity. The development of the nasal part of the olfactory system and its position with respect to the orbits show two distinctly different arrangements among primates (Fig. 2.14). In lemurs and lorises, as well as in most other mammals, the nerves responsible for olfaction pass between the orbits from the internal cavity to the brain. Within the nasal cavity, large numbers of turbinates are attached to several different bones, including several derived from the ethmoid bone that lies in the sphenoid recess, a special cul-de-sac. In tarsiers, monkeys, apes, and humans, the structure of this region is greatly simplified. The olfactory nerves pass over the interorbital septum, rather than between the orbits, and the sphenoid recess and posteriormost two turbinates are missing or greatly reduced. In apes and humans, this region is even further reduced.

FIGURE 2.14 Structure of the interior nasal region of a lemur (Lemur), a tarsier (Tarsius), and a squirrel monkey (Saimiri). Note the reduction in number and relative size of the turbinates in Tarsius and Saimiri. M, maxilloturbinate; N, nasoturbinate; E, ethmoturbinates (numbered).

Although primate noses and the tissue-lined passages that make up their internal structure are associated primarily with olfaction, they also play important roles in respiration and temperature regulation by warming and humidifying the air that passes over them.

In addition to their sense of smell, lemurs, lorises, tarsiers, and many New World monkeys (but apparently not Old World monkeys, apes, or humans) have an additional sense that seems to be particularly important in sexual communication. The vomeronasal organ (or Jacobson’s organ) is a chemical-sensing organ that lies in the anterior part of the roof of the mouth in many mammals. It is stimulated by substances found in the urine of female primates, and permits other individuals to chemically determine the reproductive status of a female.

In addition to these ‘internal’ differences in nasal structure, there is a major dichotomy among primates in the structure of the external nasal region. The strepsirrhine primates (lemurs, lorises, and galagos) have a nose with a median cleft and moist region that extends from the base of the nasal opening to the inside of the upper lip (Fig. 2.15), as in many mammals, such as dogs and cats. It has generally been argued that the strepsirrhine condition is related to the function of the Jacobson’s organ. In contrast, tarsiers and anthropoids, the haplorhines, have a dry nose, continuous upper lip and often a hairy region between the lip and the base of the nasal opening (Fig. 2.15). Associated with the presence of a moist rhinarium of strepsirrhines is a recently discovered bony feature of the nasal cavity. The nasolacrimal duct is a small tube that transmits tears from the orbit to the nasal cavity in all primates. However, the length and orientation of the duct differ in the two suborders of primates (Rossie and Smith, 2007; Fig. 2.16). In strepsirrhines the lower end of the duct extends anteriorly to direct moisture towards the external nose, but