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Sexual Conflict in Primates Evolutionary Anthropology 20:62–75 (2011) ARTICLES Sexual Conflict in Primates REBECCA M. STUMPF, RODOLFO MARTINEZ-MOTA, KRISTA M. MILICH, NICOLETTA RIGHINI, AND MILENA R. SHATTUCK Sexual conflict is increasingly recognized as a major force for evolutionary into primate behavior and evolution. change and holds great potential for delineating variation in primate behavior We propose that primate social com- and morphology. The goals of this review are to highlight the rapidly rising field plexity and the high diversity of mat- of sexual conflict and the ongoing shift in our understanding of interactions ing systems makes the Order Prima- between the sexes. We discuss the evidence for sexual conflict within the Order tes particularly fertile ground for sex- Primates, and assess how studies of primates have illuminated and can continue ual conflict research. to increase our understanding of sexual conflict and sexual selection. Finally, we introduce a framework for understanding the behavioral, anatomical, and genetic expression of sexual conflict across primate mating systems and suggest direc- HISTORICAL BACKGROUND AND tions for future research. SHIFTING PERSPECTIVES Darwin15:256 defined sexual selec- tion as being dependent on ‘‘the advantage which certain individuals Sexual conflict is defined as ‘‘a con- have over others of the same sex and flict between the evolutionary inter- species, in exclusive relation to ests of individuals of the two sexes.’’1 reproduction.’’ He also recognized This conflict may increase fitness in Rebecca M. Stumpf is an Associate Pro- two fundamental processes that fessor of Biological Anthropology at the one sex while reducing or constrain- influence sexual selection, mate com- University of Illinois, Urbana Champaign. ing fitness in the opposite sex.2 It Her research focuses on sexual conflict petition and mate choice. Darwin’s and sexual selection, more broadly. She can be manifested in myriad behav- definition emphasized intrasexual incorporates behavioral, morphological, ioral, anatomical, and physiological endocrinological and microbial analyses, levels of competition, or competition field observations of wild primates, and traits related to reproduction, includ- and conflict occurring between mem- comparative strategies (e.g., male vs. ing penile spinosity, vaginal plugs, bers of the same sex. Though inter- female, geographic, ontogenetic, and mating frequency, timing of fertiliza- inter-specific comparisons) to better sexual conflict may or may not have understand sexual selection in primates. tion, cryptic choice, infanticide, and been nascent in Darwin’s original 3 E-mail: [email protected] relative parental effort. Because formulation of sexual selection Rodolfo Martinez-Mota, Nicoletta Righini, Krista M. Milich and Milena Shattuck are these characteristics favor the repro- theory, more than a century passed PhD candidates in the Department of An- ductive interests of one sex while before the conflicting reproductive thropology at the University of Illinois, decreasing fitness in the other, coun- Urbana- Champaign. Martinez-Mota is interests between males and females interested in the relationship between hor- terstrategies can evolve, triggering an were explicitly recognized as a fun- mones and behavior, and infectious dis- evolutionary ‘‘arms race’’ between the damental evolutionary force.1,16 In eases in non-human primates. Righini is interested in studying dietary selectivity sexes. At an extreme, sexual conflict 1979, Parker emphasized that as a and the strategies employed by non- can lead to speciation through repro- consequence of the divergent evolu- human primates to cope with the exploita- ductive isolation.2,4 tionary interests of the two sexes, all tion of difficult to digest resources by inte- grating nutritional, energetic, ecological, Interest in sexual conflict is grow- reproductive interactions between and behavioral data. Milich is interested in ing across multiple fields, including the sexes, including mate choice, understanding the variation in primate evolutionary anthropology and pri- reproductive behaviors, hormones, and mating rates, and parental invest- 5–14 1 ecology. Shattuck’s research centers on matology. While no single review ment, imply a conflict. In historical understanding the evolution of the primate can thoroughly examine all aspects context, the slow recognition of sex- neuroendocrine system and its relationship to behavior. of this rapidly expanding field, our ual conflict as an important evolu- first aim here is to examine behav- tionary force is perhaps not surpris- ioral, anatomical, and genetic exam- ing. For one, reproduction was Key words: sexual conflict; sexual selection; sex- ples of sexual conflict in primates. viewed as a cooperative effort ually antagonistic selection; coercion; primates We highlight how integrating sexual between the sexes,8 particularly in conflict theory into primate studies our own species, whereby fitness VC 2011 Wiley-Liss, Inc. can advance theoretical develop- depends on both maternal and pater- DOI 10.1002/evan.20297 ments in our understanding of sexual Published online in Wiley Online Library nal cooperation and is negatively (wileyonlinelibrary.com). selection and lead to new insights affected by lack of one or the ARTICLES Sexual Conflict in Primates 63 other.17,18 In addition, female sexual still overwhelmingly ascribed to which sexual conflict is expressed reserve and passivity were expected. intrasexual mechanisms (for exam- within and across species. To date, Theoretical and empirical research ple, male-male competition), with lit- the majority of the theoretical models, by key evolutionary anthropologists tle attention is given to the potential hypotheses, predictions, and empiri- and primatologists, notably Robert influence of intersexual mechanisms cal research on sexual conflict are Trivers, Sarah Blaffer Hrdy, and Bar- (Fig. 1b, c). Specifically, female strat- based on insects, especially Drosophila bara Smuts, contributed greatly to egies such as multi-male mating and, to a lesser extent, on birds and both the understanding of sexual counter male reproductive control fish.31,33–40 These studies have been selection and development of the and provide selective pressure for fundamental for providing strong study of sexual conflict. Trivers, male co-evolution. The slow emer- evidence of conflict between the sexes building on Bateman’s19 experiments gence of sexual conflict in traditional leading to selection and counter-selec- with fruit flies, emphasized the diver- sexual selection theory may be due tion (sexually antagonistic selection). gent reproductive interests of males While such studies of sexual con- and females, including sex differen- flict have proliferated, the models, ces in parental investment.20 This assumptions, and conclusions work set the stage for future focus The slow emergence of derived from insect-focused studies on differing sexual roles and strat- may be largely inapplicable to prima- egies between the sexes. Hrdy’s em- sexual conflict in tes for several reasons. First, prima- pirical studies of wild langurs led to traditional sexual tes are highly social animals; their her then-controversial hypothesis mating strategies are flexible, com- that infanticide by males was a sexu- selection theory may be plex, polyadic, and can change over ally selected evolutionary tactic as due to the many time. Second, traditional sexual con- opposed to simply aberrant behav- flict models assume differences in ior.21 Notably, Hrdy also challenged unresolved optimal mating rates between the the notion of the ‘‘coy’’ female by discrepancies about sexes. Specifically, assumptions highlighting the prevalence of female include low mating costs for males promiscuity among primates and what constitutes sexual and high mating costs for females so proffering it as a female counterstrat- conflict, how to assess that females evolve resistance to egy to infanticide.22 More recently, males who may ‘‘manipulate’’ them Smuts and Smuts16 expanded on and model it, and the into mating more than is necessary Darwin’s traditional components of theoretical relationships to ensure fertilization.41,42 However, sexual selection, mate choice and among sexual conflict, many female primates are promiscu- male competition, by identifying ous and sexual behavior often serves coercion as a third component. This sexual selection, and the female reproductive interests in more work brought new theoretical atten- forces shaping male and ways than simply fertilization.9,43–45 tion to conflict between the sexes. Because infanticide is a considerable Despite considerable potential for female reproductive risk in many primate species,46 addi- sexual conflict to explain intersexual strategies. tional benefits gained from confusing dynamics and evolutionary pres- paternity through promiscuity may sures, further theoretical develop- counter or outweigh costs incurred ment and experimental research on from mating. Therefore, the costs sexual conflict and its consequences to the many unresolved discrepan- and benefits of mating among prima- has been slow to emerge. The cies about what constitutes sexual tes do not fit a traditional ‘‘sex as dynamic of intersexual conflict still conflict, how to assess and model it, reproduction’’ framework. Moreover, has a relatively limited role in tradi- and the theoretical relationships male primates incur considerable tional sexual selection theory.4,23,24 among sexual conflict, sexual selec- mating costs as well (including ener- Moreover, the explanatory
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