Edited by Clara B. Jones American Society of Primatologists, 2003 FOREWORD As we tell our graduate students from the moment they begin thinking about a dissertation topic, the best way to produce valuable research is to choose an interesting theory-driven question, and then to choose the study species in which it can be most effectively and feasibly addressed. Taken literally, this advice could easily cause students interested in sexual selection to forego primatology altogether. Small sample sizes, animals that live too long for us easily to measure lifetime reproductive success, and ethical constraints on experimental manipulations prevent primatologists from decisively answering many of the questions about mate choice and mating competition routinely addressed by ornithologists and ichthyologists. Yet in some respects, the study of sexual selection in nonhuman primates is particularly rewarding, as the contributors to this volume show us. First, because of the rather strange history of primatology as a discipline (reviewed in Shahnoor & Jones' chapter), the field is still wide open and many basic questioned (such as whether sexual dichromatism results from sexual selection - Gerald's chapter) remain unanswered for most or all taxa. As recently as the late 1980s, when I began research on female mate choice in rhesus macaques, many primatologists believed that it was both possible and desirable to study primate sexuality without considering sexual selection at all. The slow spread of behavioral ecological theory through primatology has left many niches available. This volume contains pioneering efforts in some of these domains, including the study of alternate male morphs and cryptic female mate choice. Sperm competition, long since well-documented in primates at the level of comparative morphology [Harcourt et al., 1981], is viewed from a peculiarly primatological angle by Thomsen, Soltis, and Teltscher. Primate courtship and mate competition are embedded in multifaceted social relationships that affect individuals' fitness through many causal pathways. A female monkey's suitors may also be her protectors against other males, recipients of her coalitional support in struggles against rival males, her own rivals in feeding competition, occasional caregivers to her offspring sired by other males, her sisters' and mother's suitors, etc. A male's rivals may also be his valuable allies in intergroup competition. Similar complications apply to female-female competition and male mate choice. Some of these considerations characterize other social animals as well, as Hager's chapter on skew theory reminds us, but they are particularly salient in primates and other large-brained, group-living mammals. Furthermore, long-term social relationships permit the operation of subtle forms of sexual coercion [Smuts and Smuts, 1993]: males can use aggression, perhaps including mild forms of aggression, to influence females' future mating decisions, a topic addressed in some of this volume's chapters. Indeed, the development by a primatologist of the concept of sexual coercion as a third form of sexual selection illustrates that our subspecialty of animal behavior can be a source of theory rather than merely a belated recipient of it. Throughout the late 1970s and 1980s, the study of primate sexual selection at the behavioral level was dominated by two debates, both of which produced a wealth of important data: Does male dominance rank correlate with reproductive success, and is infanticide by males really a reproductive strategy to which females have evolved counter-strategies? Today's discussions have become much more complex, with the realization that observed mating patterns result from interactions among female choice, male-male competition, male choice, female-female competition and sexual coercion. In studies of free-living, unmanipulated animals, untangling the effects of these forces can be daunting, to say the least. Some of the papers in this volume, most notably Bergman & Beehner's, make a valiant attempt to do so, with intriguing results. Most behavioral primatologists have chosen to study this particular order of mammals because of its phylogenetic closeness, and many behavioral similarities, to Homo sapiens. The study of sexual selection in nonhuman primates holds special importance because it can help illuminate how sexual selection operated in early hominids. It is no coincidence that Darwin's second most famous book is about both sexual selection and human evolution (though a modern publisher would probably not allow the two works to lie between the same covers!). Darwin suspected that sexual selection played a prominent role in the emergence of many peculiarly human traits. Some recent authors have taken this idea and run with it, even to the point of proposing that the human mind is almost entirely a product of sexual selection by mate choice [Miller, 2000] - a provocative argument with all the attractions and pitfalls of every "Theory of Everything." In any case, the fact that neocortex size is negatively related to the correlation between male rank and mating success in polygamous primates [Pawlowski et al., 1998] is consistent with the observation that nonhuman primates often bring sophisticated cognitive abilities to bear when solving the problems posed by sexual selection. For example, in the chacma baboons described in Palombit's chapter, males and females manipulate friendships in ways that maximize protection from sexually selected infanticidal attacks. Robbins recounts an anecdote of a female mountain gorilla patiently seeking a mating with a subordinate male while the alpha male follows her (a scenario very familiar to observers of rhesus macaques and other multi-male group-living species), and Vervaecke et al. report that subordinate bonobos often copulated surreptitiously. Successfully completing clandestine copulations requires that the participants accurately predict the behavior of (usually high-ranking) would-be harassers. And for some male primates, most notably chimpanzees, high dominance rank itself accrues as much to the brainy as to the brawny. By showing us how mate choice, mating competition and sexual coercion operate in animals that navigate a complex social landscape using mental tools evolved specifically for this purpose, studies of nonhuman primates, unlike studies of more tractable taxa, can give us deep insights into the operation of sexual selection among our hominid ancestors. For many, this is more than sufficient compensation for the methodological and analytical problems posed by species in which data points are scarce and confounding variables plentiful. Joseph H. Manson, Ph.D. Max Planck Institute for Evolutionary Anthropology & Department of Anthropology University of California, Los Angeles REEFERENCES Harcourt AH, Harvey PH, Larson SG, Short RV. 1981. Testis weight, body weight and breeding system in primates. Nature 293:55-57. Miller GF. 2000. The mating mind: how sexual choice shaped the evolution of human nature. New York: Doubleday. Pawlowski B, Lowen CB, Dunbar RIM. 1998. Neocortex size, social skills and mating success in primates. Behaviour 1 35:357-368. Smuts BB, Smuts RW.1993. Male aggression and sexual coercion of females in nonhuman primates and othermammals: evidence and theoretical implications. Adv Stud Behav 22:1 -63. TABLE OF CONTENTS Contributors x Foreword Joseph H. Manson xiii Preface Clara B. Jones xvii I. History and Theory of Sexual Selection and Reproductive Competition in Primates A Brief History of the Study of Sexual Selection and Reproductive Competition in Primatology Nazima Shahnoor and Clara B. Jones 1 Demography and the Temporal Scale of Sexual Selection Karen B.Strier 45 Models of Reproductive Skew Applied to Primates Reirmar Hager 65 Alternative Reproductive Behaviors in Primates: Towards General Principles Clara B. Jones & Govindasamy Agoramoorthy 103 How Color May Guide the Primate World: Possible Relationships Between Sexual Selection and Sexual Dichromatism Melissa S. Gerald 141 II. Sexual Selection, Reproductive Competition, and Female Primates Sex Ratio Bias from the Effects of Parity on the Reproductive Characteristics of Garnett's Bushbaby: Implications for Sexual Selection Sheree Watson, Willie Bingham, Ronda Stavisky, Aarion Gray, and M. Babette Fontenot 173 Reproductive Competition Among Female Common Marmosets (Callithrix jacchus): Proximate and Ultimate Causes Wendy Saltzman 197 Interfering With Others: Female-Female Reproductive Competition in Pan paniscus Hilde Vervaecke, Jeroen Stevens, & Linda Van Elsacke 231 The Potential for Cryptic Female Choice in Primates: Behavioral, Anatomical, and Physiological Considerations DeeAnn M. Reeder 255 III. Sexual Selection, Reproductive Competition, and Male Primates Scent Marking, Paternal Care, and Sexual Selection in Callitrichines Eckhard W. Heymann 305 Re-evaluating the Sexual Selection Hypothesis for Infanticide by Alouatta Males Carolyn M. Crockett 327 Male Infanticide in Wild Savanna Baboons: Adaptive Significance and Intraspecific Variation Ryne A. Palombit 367 The Evolution of Alternative Reproductive Morphs in Male Primates Joanna M. Setchell 413 Sperm Competition and the Function of Male Masturbation in Nonhuman Primates Ruth Thomsen, Joseph Soltis, & Christian Teltscher 437 IV. Sexual Selection on Male and Female Primates: Individuals, Populations, and Species Sexual Selection and Foraging Behavior in Male and Female Tamarins and Marmosets Julio CesarBicca-Marques 455 Behavioral Aspects of Sexual Selection in Mountain Gorillas Martha M. Robbins 477 Hybrid Zones and Sexual Selection: Insights from the Awash Baboon Hybrid Zone (Papio hamadryas anubis x P. h. hamadryas) Thore J. Bergman & Jacinta C. Beehner 503 Testing Some Theoretical Expectations of Sexual Selection versus the Recognition Species Concept in the Speciose Macaques of Sulawesi, Indonesia Jeffery W. Froehlich 539 V. Conclusions and Prospects Comparative and Theoretical Approaches to Studying Sexual Selection in Primates Charles L. Nunn 593 Taxonomic Index 615 Author Index 621 Subject Index 643 LIST OF CONTRIBUTORS Govindasamy Agoramoorthy, Ph.D. Department of Biological Sciences National Sun Yat-sen University Kaohsiung, Taiwan Research & Conservation Department Wildlife Reserves Singapore 80 Mandai Lake Road, Singapore [103] Jacinta C. Beehner Department of Anthropology Washington University One Brookings Drive St. Louis, MO 63130, USA [503] Thore J. Bergman, Ph.D. Department of Biology University of Pennsylvania 415 South University Avenue Philadelphia, PA 19104-6018, USA [503] Julio Cesar Bicca-Marques, Ph.D. Faculdade de Biociencias Pontificia Universidade Catolica do Rio Grande do Sul Av. Ipiranga, 6681 Predio 12A Caixa Postal 1429 Porto Alegre, RS 90619-900, Brazil [455] Willie Bingham, D.V.M. Mississippi State University Veterinary Diagnostic Laboratory 2531 North West Street Jackson, MS 39216, USA [173] Carolyn M. Crockett, Ph.D. National Primate Research Center RO. Box 357330 University of Washington Seattle, Washington 98195-7330, USA [327] M. Babette Fontenot, Ph.D., D.V.M. Division of Behavioral Sciences University of Louisiana at Lafayette New Iberia Research Center 4401 W. Admiral Doyle Drive New Iberia, LA 70560, USA [173] Jeffery W. Froehlich, Ph.D. Department of Anthropology University of New Mexico Albuquerque, New Mexico 87131, U.S.A. [539] Melissa S. Gerald, Ph.D. Cayo Santiago Caribbean Primate Research Center RO. Box 906 Punta Santiago, Puerto Rico 00741 [141] Aarion Gray Department of Education Guidance and Counseling Program Jackson State University Jackson, MS 39217, USA [173] Reinmar Hager Departtnent of Zoology University of Cambridge Cambridge CB2 3EJ, UK [65] Eckhard W. Heymann, Ph.D. Abteilung Verhaltensforschung & Oekologie Deutsches Primatenzentrum Kellnerweg 4 D-37077 Gottingen, Germany [305] Clara B. Jones, Ph.D. Department of Psychology Livingstone College School of Liberal Arts 701 W Monroe Street Salisbury, NC 28144, USA [xvii, 1, 103] Joseph H. Manson, Ph.D. Cultural Phylogeny Group Max Planck Institute for Evolutionary Anthropology Inselstr 22 D-04103 Leipzig, Germany [xiii] Charles L. Nunn, Ph.D. Section of Evolution and Ecology University of California One Shields Avenue Davis, CA 95616, USA [593] Ryne A. Palombit, Ph.D. Department of Anthropology/Center for Human Evolutionary Studies 131 George Street Rutgers University New Brunswick, NJ 08901-1414, USA [367] DeeAnn M. Reeder, Ph.D. Department of Biology Boston University 5 Cunnington Street Boston, MA 02215, USA [255] Martha Robbins, Ph.D. Max Planck Institute for Evolutionary Anthropology Inselstrasse 22 04103 Leipzig, Germany [477] Wendy Saltzman, Ph.D. Department of Biology University of California Riverside, CA 92521, USA [197] Joanna M. Setchell, Ph.D. School of Life Sciences University of Surrey Roehampton, West Hill London, SW15 3SN, UK [413] Nazima Shahnoor Department of Anthropology RO Box 413 University of Wisconsin-Milwaukee Milwaukee, WI 53201, USA [1] Joseph Soltis, Ph.D. Laboratory of Comparative Ethology National Institute of Child Health and Human Development National Institutes of Health RO Box 529 Poolesville, MD 20837, USA [437] Ronda Stavisky, Ph.D. University of Texas, Austin Section of Neurobiology University Station C0920 Austin, TX 70712-0248, USA [173] Karen B. Strier, Ph.D. Department of Anthropology 5203 Social Science Building University of Wisconsin-Madison 1180 Observatory Drive Madison, WI 53706, USA [45] Jeroen Stevens, Ph.D. Centre for Research and Conservation (CRC) Royal Zoological Society of Antwerp (RZSA) K Astridplein 26 2018 Antwerp, Belgium University of Antwerp (UIA) Universiteitsplein I 2610 Antwerp, Belgium [231] Christian Teltscher Max-Planck Institute for Behavioral Physiology Seewiesen PO Box 1564 82305 Starnburg, Germany [437] Ruth Thomsen, Ph.D. Institute for Zoo & Wildlife Research RG I Evolutionary Ecology Alfred-Kowalke-Str. 17 10315 Berlin, Germany [437] Linda van Elsacker, Ph.D. Centre for Research and Conservation (CRC) Royal Zoological Society of Antwerp (RZSA) K. Astridplein 26 2018 Antwerp, Belgium [231] Hilde Vervaecke, Ph.D. Centre for Research and Conservation (CRC) Royal Zoological Society of Antwerp (RZSA) K. Astridplein 26 2018 Antwerp, Belgium University of Antwerp (UIA) Universiteitsplein I 2610 Antwerp, Belgium [231] Sheree L. Watson, Ph.D. Department of Psychology University of Southern Mississippi RO Box 5026 Hattiesburg, MS 39406, USA [173] ISBN: 0965830128 $60.00 USD ($45.OO FOR ASP MEMBERS) WHERE TO ORDER: Evan L. Zucker, Treasurer, ASP Department of Psychology, Box 194 Loyola University 6363 St. Charles Ave. New Orleans, LA 70118 U.S.A. Phone: (504) 865-3255 Fax: (504) 865-3970 Email: zucker@loyno.edu Website: www.asp.org/research/aspbook/Volume3.html Checks should be made out to the American Society of Primatologists. Posted Date: 7/8/2003
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