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 power of tion, and the forces shaping male getic costs, injuries, sperm depletion, sexual conflict has only recently been and female reproductive strat- and sexually transmitted diseases emphasized, partly due to improved egies.3,4,8,25–32 (STDs)47,48 which are not considered methodologies that facilitated the in traditional models. Third, whereas understanding of reproductive mech- immediate behaviors are the focus of anisms.8 Indirectly, this emerging HOW PRIMATES CAN INFORM insect studies of sexual conflict, lon- shift in our field can be seen in pub- EXISTING SEXUAL CONFLICT gitudinal behaviors such as coercion lication records. Few primate papers (for example, conditioning aggres- MODELS referenced sexual conflict or intersex- sion49) may be more important ual selection until this decade, but a Currently, the predominant chal- among primates because of their marked increase has occurred just in lenge within the field of sexual stable social networks, individual the last few years (Fig. 1a). Concepts conflict is to develop a unified recognition, long-term memory, and such as sperm competition and the theoretical framework8 that will higher cognitive function, thus lead- evolution of sexual dimorphism are enable predictions of the ways in ing to different predictions and 64 Stumpf et al. ARTICLES

assumptions related to sexual con- flict. Finally because raising off- spring is so costly, sexual conflict over parental investment is an im- portant consideration in primates, in contrast to other orders that are characterized by little to no parental investment. The diversity of primate mating sys- tems provides an ideal system for refining our understanding of sexual conflict and challenges the assump- tions of traditional models. Specifi- cally, different primate mating sys- tems, such as polyandry and monog- amy, are expected to produce different manifestations and inten- sities of sexual conflict, including sex- ual role reversals. Thus, incorporating primate studies of sexual conflict into traditional models has the potential to contribute to a more unified frame- work of sexual conflict.

Sexual Conflict in Primate Behavior Insight into the evolutionary dy- namics of the sexual arms race between primate males and females provided important early advances in understanding sexual conflict. Hrdy and Smuts were among the first to use a sexual conflict framework for understanding sexual selection and sexual dialectics, due in large part to their focus on females. Moreover, where primates have figured promi- nently in sexual conflict theory, the emphasis has largely been on behav- ior.7,16,49,50 Because behavioral sex- ual conflict has received more detailed treatment elsewhere,7,16,49,50 here we briefly describe some of the main examples that highlight how sexual conflict theory has enriched our understanding of male and female Figure 1. a) Simple count of articles referring to sexual conflict in primates. A search was coevolution and sexual selection. conducted in PubMed, PrimateLit, and Google Scholar using the key words ‘‘sexual con- Perhaps the most compelling evi- flict,’’ ‘‘intersexual conflict’’ or ‘‘intersexual selection’’ and ‘‘primates.’’ Articles were screened to ensure that they discussed intersexual conflict and that there were no dence of sexual conflict in primates repeats between different search terms. Figures 1b and 1c depict the number of articles is infanticide. Originally viewed as found using PubMed that discuss sexual conflict and either b) sperm competition or c) simply an aberrant behavior, Hrdy21 sexual dimorphism in primates. A PubMed search was conducted using the term ‘‘sperm proposed that infanticide by males is competition’’ or ‘‘sexual dimorphism’’ paired with the terms ‘‘conflict,’’ ‘‘antagonistic,’’ a sexually selected strategy. By elimi- or ‘‘antagonism.’’ The number of articles found discussing sexual conflict was subtracted nating rival males’ offspring and from the total number of articles found when using only the term ‘‘sperm competition’’ or ‘‘sexual dimorphism’’ to calculate the number of articles on these subjects that do not shortening lactational amenorrhea in discuss sexual conflict. Articles were separated into those that discuss sexual conflict the victim’s mother, an infanticidal (black portion) and those that did not (white portion). male increases his mating opportuni- ties and reproductive potential rela- ARTICLES Sexual Conflict in Primates 65

extends to pregnancy, especially when new males appear after the female has conceived. For example, female long-tailed macaques (Macaca fascicularis) maintain swelling size, frequency of proceptive behaviors, and copulations throughout the first two-thirds of pregnancy.71 Similarly, orangutan females are particularly proceptive during early pregnancy.72 It is argued that these multi-male matings are a female counterstrategy to infanticide and coercion, manipu- lating ‘‘paternity assessment’’73 and decreasing selection for persistent or aggressive males.74 Female mate selectivity, which includes any behavior or trait that biases male mating success toward certain male phenotypes,8,73,75,76 is Figure 2. This diagram illustrates a hypothetical example of the behavioral strategies and another sexually selected trait that cre- counter-strategies in sexually antagonistic coevolution. For example, in polygynandrous ates selective pressure on male repro- mating systems, males may evolve infanticidal behavior because of the benefits gained ductive interests and constitutes a by reducing the time until a female can conceive again. Because loss of an infant is so 77–80 costly, females counter by mating with multiple males, thereby confusing paternity. Males form of conflict. Strategies of respond to multiple matings by increasing sperm competition and attempting to prevent multi-male mating and female mate multiple matings through behavioral strategies such as mate guarding. Females then selectivity are not mutually exclusive. evolve further strategies, such as concealed ovulation, which lengthens the mating pe- Indeed, evidence suggests that they riod and makes behaviors like mate guarding more difficult for the male. It also can be applied in tandem through a decreases some of the effectiveness of sperm competition, as a male is likely to mate mixed strategy of paternity confusion with a female when she is nonconceptive. Again, males attempt to overcome this by 9,80,81 evolving further strategies, such as kin recognition. The ability to differentiate his own off- and mate selectivity. spring from a rival male’s offspring decreases the costs associated with infanticide for a Females can also employ social male, leading to selection for behavior strategies and counter strategies in the continu- strategies in response to sexual con- ous ‘‘arms race’’ that is sexual conflict. flict. Among orangutans, associating with a dominant male is argued to be a female behavioral counterstrat- 80,82 tive to that of other males. For pri- could take the form of forced copula- egy to forced mating. Among mate females with heavy offspring tion, harassment, intimidation, pun- chacma baboons (Papio hamadryas investment and limited reproductive ishment and, in its extreme form, in- ursinus), both ‘‘friendships’’, a term potential, the loss of an infant is fanticide),16 as an important selective referring to close associations between extremely costly. force. Males are thought to benefit lactating females and specific adult Infanticide has been documented from sexual aggression through males, as well as female defensive coa- extensively among catarrhines in increased mating opportunities, but litions against males, are suggested to both one-male groups when a new females suffer costs, including loss of be anti-infanticide strategies, provid- male takes over the group (for mate choice, decreased foraging, ing protection to females and their off- 16,51 example, guenons and gorillas) and injury, increased stress, and sponta- spring. Male friends respond to multi-male groups (for example, red neous abortion.63–68 infanticidal attacks in different ways colobus, chacma baboons, and chim- Females have co-evolved several than do other males; these responses panzees).51 Although infanticide has counterstrategies in response to male include physically fighting the been less commonly observed among coercion and infanticide (Fig. 2).9,22 attacker, initiating chases, and issuing strepsirrhine and platyrrhine taxa, it Multi-male mating benefits female direct threats and vocalizations.83 Sec- has nonetheless been reported in primates especially at risk of infanti- ondary transfer, which is associated several of them.52–62 Because this cide by confusing paternity and thus with weak within-group social rela- behavior is rare and not easily observed, inhibiting males from killing the tionships and increased coercion by it may be more prevalent in these infants of former mates.21,45 Evi- extra-group males at the end of the taxonomic groups than currently is dence from diverse primate taxa breeding male’s tenure,84 may also be recognized. indicates that females actively solicit a female defensive strategy. Teichroeb Through long-term, detailed obser- matings from multiple males,69,70 and colleagues,85 observing six groups vations of wild baboons, Smuts and particularly when conception is of Colobus vellerosus over seven years, Smuts identified coercion (which unlikely,9 and that this behavior recorded that 90% of voluntary female 66 Stumpf et al. ARTICLES emigrations occurred when new adult For example, primate seminal fluid is nize the precise time of ovulation, males immigrated and the social envi- rich in biochemical compounds that paternity confusion ensues. Sexual ronment destabilized due to frequent aid in sperm motility and fertiliza- swellings and mating during preg- male-male aggression and evictions. tion. However, hormones and prosta- nancy71,101,102 enhance the effect. By Similar findings have been reported glandins found in seminal fluid also confusing and concentrating pater- among Thomas’s langurs (Presbytis affect females through immunosup- nity, sexual swellings manipulate thomasi) and gorillas (Gorilla sp.), pression, induction of ovulation, in- male behavior.81,103 Other taxa, such with emigrations generally occurring citation of uterine muscle contrac- as prosimians and platyrrhines, may when a female’s present offspring tions to aid sperm transport, and conceal ovulation and manipulate reach independence or die.84 These decreased female sexual receptiv- males through olfactory cues from examples illustrate that primate ity,92–95 all of which limit female pheromones or scent gland secre- behavior is a dynamic process involv- control over paternity and reproduc- tions.70 ing strategies and counterstrategies tive health. In another example, pen- Cryptic choice is another counter- between males and females, enlivening ile spines are argued to enhance con- adaptation to increase control over theoretical development and testable ception likelihood13,34,96 yet may paternity. Eberhard86:7 defines cryp- hypotheses to explain patterns of pri- damage the female reproductive tic choice as ‘‘a female-controlled mate behavior and evolution. tract,34 decrease a female’s willing- process or structure that selectively ness to mate with other partners, favors paternity by conspecific males and increase female susceptibility to with a particular trait over that of 97 Sexual Conflict in Primate STDs, arguably advantageous to others that lack the trait when the males in species where additional female has copulated with both Anatomy and Physiology mating opportunities with the same types.’’ Thus, within the female In addition to behavior, evaluating female are unlikely. reproductive tract, diverse anatomi- primate anatomy and physiology in Selective pressure resulting from cal or physiological processes may light of sexual conflict theory also these male adaptations to influence favor gametes of particular males contributes to a greater understand- paternity are high for females. Costs and/or counteract damaging effects ing of primate evolution. In particu- include fertilization by non- of male seminal substances.86,93 Ovi- lar, sexual conflict is likely to have a preferred males, fertilization by duct length in mammals, including significant effect on the reproductive more than one sperm (polyspermy) primates, correlates positively with organs,86 since there is strong selec- causing zygote mortality, and reduc- testes size, ejaculate size, and sperm tion to enhance insemination and tion of female fertility.8,98 One coun- midpiece volume,104,105 suggesting fertilization, even if those adapta- ter-strategy of female primates to that females have evolved in tions impose a cost to a sexual part- increase control over paternity is to response to sperm competition. ner. Traits that enhance one sex’s manipulate male mating behavior, Inside the vagina, sperm are exposed opportunities for mating and fertil- including infanticide and male coer- to a hostile acidic environment and ization, but impinge on the other cion, by modifying ovulatory timing phagocytotic attacks.93,106 Although sex’s opportunities, lead to adapta- and signals. For example, by syn- seminal fluid buffers the pH of the tion and counter-adaptation between chronizing ovulatory cycles, females vagina and helps with sperm trans- the sexes. limit control of multiple fertile port, it is effective only for a few One driving force of sexual conflict females by a single male.99 Alterna- hours.107 Therefore, only sperm ca- is the competition between the sexes tively, females are argued to conceal pable of surviving the vaginal tract for control over paternity. In males, ovulation to decrease male repro- can fertilize an egg.93 The vaginal this conflict manifests in physiologi- ductive control and increase pater- environment may demonstrate post cal adaptations related to rates of nity uncertainty.87,100 Specifically, copulatory sexual selection by differ- sperm production, as well as sperm concealed ovulation in the form of ential selection among male sperm. length and speed, testes size, and vol- long ovarian cycles, follicular Biochemical properties of the cervi- umes of the sperm midpiece (where phases, and extended periods of sex- cal mucus and vaginal secretions mitochondria associated with sperm ual swellings in several Old World released during orgasm affect sperm motility reside).87,88 These features primates counteract the cost of male survival.107 Moreover, uterine con- all correlate positively with levels of coercion and infanticide.70 Nunn81 tractions occurring during orgasm female promiscuity across prima- proposed the graded-signal hypothe- may facilitate transport of the sperm tes87,89–91 and increase a male’s con- sis to explain the evolution of exag- of particular males.108 The Bruce trol over paternity. While these fea- gerated sexual swellings in primates. Effect109 (that is, reabsorption of an tures are traditionally viewed in the This hypothesis states that gradual embryo after exposure to a new context of male-male competition, it increases in swelling size are general male) is argued to be a female strat- is important to emphasize that they indicators to males of the likelihood egy to avoid investment in an infant evolve in response to female behavior of conception, so that the signal and that would most likely be killed.21,73 and physiology and, in many cases, extended duration of receptivity Although it is best known in rodents, enhance male reproductive success attracts males and encourages mat- cases of abortions related to the ar- while imposing a cost on females. ing. Because males may not recog- rival of a new male have been ARTICLES Sexual Conflict in Primates 67 reported in baboons, langurs, and This conflict can be resolved increase in body size negatively gibbons.73 These various anatomical through the evolution of sex-limited affects female reproductive rates,119 and biochemical mechanisms in gene expression, or sexual dimor- demonstrating a conflict over ideal males and females affect individual phism.111 An extension of this pro- body size in primates that may not fitness and are argued to have cess likely played a role in the for- be entirely resolved through sexual evolved not only in response to intra- mation of sex chromosomes.112 dimorphism. sexual competition, but also in Indeed, the presence of sexual Genomic imprinting, perhaps the response to sexual conflict. dimorphism across a large number most persuasive genetic evidence for of primate taxa provides support in intralocus sexual conflict, exempli- itself for sexual conflict, as dimor- fies the insight to be gained from understanding this phenomenon Sexual Conflict in Primate Genes from the perspective of sexual con- While most evidence of primate flict. Imprinting is traditionally sexual conflict has come from ... viewed as a form of parent-offspring behavior studies and, to a lesser because males and conflict,120,121 with offspring maxi- extent, morphological studies, evo- females largely share the mizing maternal investment at a lution is ultimately a genetic pro- same genes, selection cost to the mother’s future repro- cess. It is therefore important to duction. However, this wording min- examine how a sexual-conflict per- on a trait in one sex imizes the conflict between maternal 122,123 spective can inform our under- leads to a correlated and paternal DNA. Genomic standing of genetic outcomes. imprinting occurs when two alleles Because genetic technology has response in the other have different expression levels only recently become accessible to sex, so that both sexes depending on which parent provided a large range of researchers, the the allele. The most common expla- field of primate genetics in general, express the trait even if nation for genomic imprinting is let alone primate genetics in rela- that it is the result of conflict over only one sex benefits 124,125 tion to sexual conflict, remains maternal investment. In a largely unexplored. To date, most from its presence. The given primate genome, an estimated studies looking at primate genetics 100–200 genes are likely to be result is intralocus 126,127 have come from fields outside of ... imprinted. In mammals, most anthropology and have taken a conflict imprinted genes are associated with very broad approach, looking at embryonic growth and development, mammals in general. Therefore, with the majority involved with de- evidence of genetic sexual conflict phism is not likely to evolve if, for velopment of the placenta as well as in primates is rare. Most of the example, the presence of large can- post natal development, such as 128,129 studies cited here reference several ines is beneficial for both sexes.113 suckling. Conflict occurs mammalian species. Nevertheless, However, several factors can allow because paternal alleles maximize because the rapidly growing field for the persistence of intralocus con- maternal investment and growth, of genetics is likely to have a large flict. Due to the constraints whereas maternal alleles inhibit impact on primatological studies imposed, dimorphism can evolve growth, presumably to balance and theories, we feel it is impor- very slowly.110 There may also be a investment between current and 121,124,125,130,131 tant to highlight how sexual con- limit to the degree of dimorphism future offspring. In flictcanenrichinterpretationof that can evolve, so that one or both support of a link to sexual conflict, genetic variation. sexes cannot obtain the ideal pheno- genomic imprinting has been found type. As well, it may be that not all across placental mammals, but not Intralocus Conflict. A beneficial trait genes are exclusively expressed in in oviparous birds and monotremes, 111 with their considerably reduced in one sex, such as the bright colora- one sex. Although most exten- 132 tion of peacocks or the large canines sively studied in Drosophila,114,115 a maternal fetal investment. Even of several primate males, may not be handful of studies have demon- the mechanisms behind imprinting have been argued to demonstrate beneficial, or may even be detrimen- strated intralocus conflict in wild 133,134 tal, in the other sex. However, animals, including mammals.116,117 sexual conflict. because males and females largely In haplorrhine primates, Lindenfors Interlocus Conflict. Interlocus con- share the same genes, selection on a and Tullberg118 demonstrated that flict, predicted to be a driving force trait in one sex leads to a correlated where there is strong male intrasex- of speciation,2,41 is another realm response in the other sex,110 so that ual selection, there is a general in which the sexual-conflict perspec- both sexes express the trait even if trend to increase the body size of tive can aid our understanding of only one sex benefits from its pres- males and, to a lesser degree, primate evolution. Interlocus con- ence. The result is intralocus conflict; females (but see Brockman, Cobo- flict, which refers to competition that is, selection on these loci is sex- len, and Whitten60). However, fur- between traits encoded by different ually antagonistic. ther analysis showed that the genes in different individuals,31,36 68 Stumpf et al. ARTICLES

A NEW FRAMEWORK FOR UNDERSTANDING THE EXPRESSION OF SEXUAL CONFLICT ACROSS PRIMATES Much variability in morphology and behavior across primates cannot be explained by either phylogeny or socioecology. Individual reproductive success depends on multiple factors, including ecology, spatial and tempo- ral distribution of mates, and opera- tional sex ratio (OSR); that is, the ratio of sexually active males to sexually receptive females at any one time. Just as these factors drive the evolution of mating and social systems,151 these factors should also influence the expression of sexual conflict, such as Figure 3. A diagram showing the interactions among sexual conflict, mating systems, and patterns of ornamentation, coercion, ecology. The evolution of sexual conflict will take place within the conditions set by both and female choice. Moreover, while ecology and the species’ mating system (which is also affected by ecology). However, ecology and mating systems are there is a two-way interaction between sexual conflict and mating systems so that the expected to drive the expression of sex- coevolution of males and females may result in shifting behavioral strategies that change the dynamics of a mating system (modified from Arnqvist and Rowe, 2005). ual conflict, mating systems are also predicted to have evolved in response to sexual conflict (Fig. 3).152 allows for continual evolution of tion theory, such as sperm competi- Variation in primate morphology traits in both sexes that manipulate tion, without invoking sexual conflict. and behavior permits hypothesis test- the outcome of male-female sexual To identify sexual conflict, it is ing and predictions for the way in interactions. Because any feature necessary to include consideration of which sexual conflict is expressed in involved in some sort of ‘‘arms male-female interactions to demon- this Order. Recently, attempts have race’’ will tend to evolve at a high strate that males, rather than evolv- been made to explain the presence of rates, evidence of these processes ing in response to other males, particular examples of sexual selection can be found by looking at base evolve in response to particular and conflict such as infanticide73 and pair substitution rates within and aspects of the female reproductive penile spines.87 Here we introduce an between species. Conflict between system and vice-versa. The evolution overall framework for understanding the sexes should result in a high ra- of the mammalian egg provides a the expression of sexual conflict and tio of nonsynonymous to synony- persuasive example. In primates and selection more broadly across pri- mous substitutions (dN/dS) in loci other mammals, the proteins of the 36 mate mating systems. For one, the involved with reproduction. Fur- zona pellucida, the coating of the thermore, sexual conflict should egg, evolve very rapidly,140 particu- manifestation and intensity of sexual also lead to the rapid evolution of larly in areas that directly interact conflict is predicted to differ mark- gene expression differences related with sperm and are associated with edly across primate mating systems to reproduction. If sexual conflict sperm reception and species recogni- in response to differing selective leads to speciation, we should see a tion.141,142,149 Sexual conflict over pressures (Fig. 4). This is predicated high level of divergence between sperm penetration rate through the on two assumptions. First, individu- species in reproductive gene sequen- zona pellucida provides a compelling als of each sex are expected to maxi- ces and expression levels.135 explanation for this rapid evolu- mize their fitness, leading to inter- In fact, across a variety of taxa tion.150 Male sperm are selected to sexual interactions that are competi- including chimpanzees and humans, penetrate the zona pellucida as tive and beset by conflict. Second, male and female reproductive traits quickly as possible, particularly in the selection pressures on male and such as proteins involved in sperm promiscuous mating systems. How- females ultimately determine the in- competition and gamete recognition ever, females have evolved polymor- tensity and manifestation of sexual are found to evolve more rapidly phic responses to enhance discrimi- conflict. Specifically, as a conse- through positive selection than do nation and minimize the possibility quence of differences in mating sys- nonsexual traits,136–139 a pattern that of polyspermy, or multiple sperm tem parameters, such as the number is consistent with intersexual entering the egg at once. This tug of of mates acquired, the manner of conflict.27,136,140–148 Although these war between males and females leads mate acquisition, the presence and studies clearly demonstrate positive to a runaway process resulting in the characteristics of pair bonds, and the selection in relation to reproduction, rapid evolution of both sexes’ game- patterns of parental care provided by this pattern can also be explained in tes as they evolve in response to each each sex,151 optimal strategies are terms of more traditional sexual selec- other.141,142 expected to vary, resulting in the ARTICLES Sexual Conflict in Primates 69

Figure 4. A model for sexual conflict and selection across different primate mating systems. Primate mating systems include monogamy (for example, Indri indri, Aotus spp., Hylobates spp., Symphalangus sp.), polyandry (for example, Callithrix spp., Saguinus spp.); polygyny (for example, Papio hamadryas, Theropithecus gelada, Gorilla gorilla gorilla); dispersed (for example, Pongo pygmaeus, Microcebus murinus); multimale-multifemale egalitarian (for example, Alouatta caraya, A. pigra, Brachyteles arachnoides, Pan paniscus); and multi- male-multifemale dominance-based (for example, Macaca fascicularis, Papio cynocephalus ursinus, Pan troglodytes). Across mating systems, the intensity and manifestation of sexual conflict are expected to vary. For each mating system, we show the expected level of sexual conflict (SC) (one arrow : ¼ low; two arrows :: ¼ intermediate; three arrows ::: ¼ high), highlight areas where sexual conflict will most likely manifest, and list examples of male and female strategies and traits known or expected to occur in these mating sys- tems. These mating systems differ in the number of mates acquired, the manner of mate acquisition, the presence and characteristics of pair bonds, and patterns of parental care provided by each sex. As a consequence of differences in these mating system parame- ters, optimal strategies shift, resulting in the molding of adaptive mechanisms of sexual conflict to mating system constraints. molding of adaptive mechanisms of with reduced or reversed sexual as mate guarding, punishment, copu- sexual conflict to mating system con- dimorphism and OSRs. lation interference, herding, seques- straints. Figure 4 presents a framework out- tering, and infanticide)14 are pre- Thus, while sexual conflict is pre- lining predictions for the differing dicted to be more prevalent. Because dicted to be ubiquitous across prima- expression of sexual conflict across the overt expression of female choice tes, mating systems with highly five primate mating systems: multi- is challenging in male-dominant poly- divergent male and female reproduc- male, multi-female (polygynandry), gynandrous mating systems, females tive interests (for example, polygy- polygyny, polyandry, monogamy, and are predicted to manifest attempts to nandry) are expected to exhibit more dispersed. For example, among influence paternity through more extensive and elaborate mechanisms multi-male multi-female mating sys- subtle means, such as variation in of sexual conflict. Specifically, sexual tems characterized by male domi- sexual receptivity, and graded signals conflict should be more intense in nance to females, both direct coer- which both confuse and concentrate primate species characterized by cion (for example, behaviors to paternity. In addition, due to high high OSRs, high mating competition, increase a male’s mating opportuni- male contest competition and the strong hierarchies, and extensive sex- ties, such as forced copulation, har- challenges of expressing overt female ual dimorphism. For example, sexual assment, and intimidation) and indi- choice, post-copulatory mechanisms conflict is predicted to be greater in rect coercion (for example, behaviors such as sperm competition and cryp- many catarrhine species than it is that attempt to prevent females from tic choice are expected to be more among platyrrhines or strepsirrhines reproducing with other males, such prevalent here than in other mating 70 Stumpf et al. ARTICLES systems. Because females have less attract females and influence female matings, while female resistance to influence over precopulatory mate choice by exploiting this mecha- mating is predicted to be minimal. choice than in they do other mating nism.153 Another mechanism found However, because the largest repro- systems, postcopulatory mechanisms, in this mating system, genetic chi- ductive threat to males in polygy- such as sperm competition and cryp- merism, may induce paternal invest- nous mating systems is female tic female choice, are expected to be ment. Chimerism occurs when high abandonment in favor of another more prevalent in these species. rates of placental fusion and delayed male, indirect coercion is predicted In multi-male, multi-female mating embryonic development during pla- to be intense, often expressed in a systems characterized by egalitarian cental fusion increase the possibility nonsexual context, and is the most male-female relationships, such as for stem cell exchange between sib- prominent form of coercion. several lemuroids, bonobos and many lings before advanced differentiation Polygynous mating systems can be New World monkeys, we predict lim- of embryonic tissues.154,155 Thus, fra- divided into two main types: one ited direct or indirect coercion from ternal twins share alleles in multiple characterized by female dispersal males. Because males do not benefit cells, possibly including germ lines, into a new unit or group and the sec- from much sexual dimorphism in size, leading to a greater than average ond by male takeovers of existing thus making coercion less tenable, coefficient of relatedness as com- groups. In polygnous species charac- male postcopulatory mechanisms pared to full siblings.156 Ross, terized by female or bisexual disper- including sperm competition, are pre- French, and Orti156 argue that mar- sal, such as gorillas and mandrills, dicted to be more extensive than pre- moset chimerism may result in intersexual selection in the form of copulatory ones such as coercion. In female-imposed costs to males in the female choice of mates is predicted these less sexually dimorphic or form of high investment in paternal to be predominantly expressed at dis- female-dominant species, females are care through kin recognition mecha- persal (that is, during female immi- predicted to exhibit more precopula- nisms such as phenotypic matching. gration into a group). Thus, we pre- tory mechanisms, (including mate This effect may be even more impor- dict that these polygynous species choice, resistance, proceptivity, and tant in groups of unrelated males. will exhibit a high prevalence of male female coalitions) and fewer postcopu- We predict that similar mechanisms persuasive signaling tactics in the latory mechanisms (for example, cryp- to induce alloparenting will be found form of elaborate male ornaments to tic choice) than in male-dominant poly- in other polyandrous species. attract females. Such ornaments gynandry. Another mechanism characteristic include the bright coloration of drills Finally, multi-male, multi-female of polyandrous primates is female and mandrills, as well as the silver- mating systems (dominant or egalitar- reproductive suppression, which is back of gorillas, which do not directly ian) are predicted to demonstrate a traditionally considered an example increase fighting ability.157 Previously, greater prevalence of genomic imprint- of female-female competition. How- ornamentation has been explained by ing than other mating systems, perhaps ever, when considered through the the coercion defense model, in which with the exception of dispersed. lens of sexual conflict, reproductive species characterized by females that Genomic imprinting is thought to max- suppression of the ovulatory function are able to avoid coercion exhibit the imize maternal investment on the cur- of other females permits dominant development of male ornaments rent sire’s offspring at a cost to the females to limit male mating opportu- instead of weapons.157 Alternatively, female and her investment in future nities, thereby raising male costs. we propose that coercion (particularly offspring, and females in these mating Males sometimes succeed at obtain- indirect) is still an important selective systems are less likely to reproduce ing additional mates, yet dominant pressure on females. Rather, selection again with the same male. In addition, females often kill the offspring of for male ornamentation is primarily the rapid evolution of genes related to these matings. Infanticide by domi- an outcome of female choice at disper- reproduction should be most prevalent nant polyandrous females may be sal. We therefore expect that orna- in polygynandrous species, where the considered yet another mechanism ments evolve in species where female reproductive interests of males and for sexual conflict because females choice of mate is manifest before pro- females are most at odds. constrain male fitness by substantially longed association with a male, Among polyandrous species, we increasing the costs of expending thereby leading to exaggerated male predict that most sexual conflict will male mating effort in exchange for signals to attract females. be expressed as conflict over paternal parental care relative to the benefits. In contrast, in polygynous species care. We expect multiple mecha- In polygynous mating systems, characterized by male takeovers, nisms to induce paternal care direct coercion is expected to be rare such as langurs, male ornamentation because, by persuading males to because mechanisms for female mate is not expected to be under strong increase parental care, females can choice and male persuasion should selection because females do not produce multiple offspring and rap- be most active before group forma- actively choose males. Rather, males idly invest energetic resources in tion and not during sexual activity. take over a group and eject resident future offspring shortly after birth. Thus, sexual interactions are pre- males. Intersexual conflict in these Females may induce paternal care by dicted to be relatively free of conflict. polygynous species should select for basing future mate choice decisions Specifically, females are predicted enhanced female fighting ability to on male parental care; males may to initiate a large proportion of prevent the resultant decrease in fit- ARTICLES Sexual Conflict in Primates 71 ness through infanticide, and mani- predicted to be high in multi-male MOVING RESEARCH ON PRIMATE fest as female resistance to incoming multi-female mating systems, and to SEXUAL CONFLICT FORWARD males, such as physical resistance, vary by male identity. Higher ranking reduced sexual dimorphism, female- males are predicted to use indirect The developing field of sexual con- female alliances, and support for res- coercion to attempt to prevent females flict is inducing a paradigm shift in ident males. from mating with other males and sexual selection theory by emphasiz- In monogamous species such as titi decrease the relative reproductive suc- ing the conflicting dynamics in monkeys and gibbons, sexual conflict cess of other males, whereas lower reproductive interactions, as well as in parental care is predicted to be ranking or nonpreferred males are pre- adaptation and counter-adaptation moderate since fitness for both sexes between the sexes. As sexual interac- depends on biparental care and is of- tions are increasingly viewed less as a cooperative undertaking and more ten maximized by shared parental ... as grounds for conflict, this shift in effort. Sexual and social relationships an individual’s focus is dramatically altering our generally endure; thus, the expres- reproductive success is understanding of the evolution of sion of male coercion is also pre- affected by the anatomical, physiological, genomic, dicted to differ from that in other and behavioral traits across species. mating systems. Indirect coercion, competing strategies of Darwin’s original conceptualization such as mate guarding, to secure and both the opposite and of sexual selection as being largely protect long-term access to females is the same sex, while also precopulatory has expanded to predicted to be more common, include copulatory and postcopula- whereas direct coercion should be driving selection on both tory mechanisms, as well as inter- relatively rare. Similar manifestations the same and opposite genomic interactions.1,22,121 This to maintain the pairbond are also shifting perception is also arguably a expected for females. Thus, mutual sex. Ultimately, however, consequence of a greater research mate guarding, territorial defense, how well an individual focus on females, resulting in new reduced canine and body dimor- competes reproductively discoveries and changing perceptions phism, and concealed ovulation or of female agency in sexual interac- frequent mating are expected. relative to others of the tions.69,86,163,164 While data on pri- In a dispersed mating system, indi- same sex is what mate sexual conflict largely come viduals occupy separate but overlap- from catarrhines, making this, in ping ranges. Mating opportunities are determines the strength itself, an area for hypothesis testing, relatively rare, of short duration, and of selection. the increasing reports of sexual con- fleeting. Thus, sexual selection on flict in other suborders165–170 suggest males is expected to drive mecha- that sexual conflict is more prevalent nisms to ensure conception and limit across noncatarrhine primates than remating by other males, such as dicted to use direct coercion more fre- currently recognized. forced copulation, genital locks, pen- quently to increase their immediate Progress toward understanding the ile spines, and ovulation induc- mating opportunities.14 Similarly, in evolutionary impact of sexual con- tion,13,87,158,159 as well as mechanisms monogamous species, paired males flict and selection among primates to increase maternal investment such are more likely to exhibit indirect coer- requires clearer definitions, concepts, as genomic imprinting. Because cion, in contrast to more direct coer- and operational measures.3,25,171 females are isolated and vulnerable to cion by nonpaired males. Currently, multiple definitions exist coercion, selection for female influ- While we have attempted to for sexual conflict,31 along with at ence on paternity is predicted to be explain and predict patterns of least nine for sexual selection.29 Sim- manifest through association patterns behaviors and morphologies through ilarly, the word ‘‘mate’’ is applied to (such as temporary consortships) and a framework of sexual conflict across both the copulatory and the repro- postcopulatory mechanisms. Male mating systems, we recognize that ductive partner,172 yet the distinction mechanisms to attract females and these are incomplete. We view this is great. Importantly, most descrip- female mechanisms to signal recep- framework as a stimulus for further tions of sexual selection invoke the tivity are predicted to emphasize research and expect that these pre- false dichotomy between intersexual acoustic or olfactory tactics in dis- dictions will be applicable on a and intrasexual selection. Both of persed compared to more aggregated broader scale to other mammalian these modes of selection clearly mating systems.160–162 orders. In a forthcoming paper, we impact both sexes. For example, Of course, plasticity in mating sys- elaborate on and test this frame- while features of male primate anat- tems and sexual conflict is expected. work, in which different mating omy and physiology are traditionally Sexual conflict strategies may vary systems and ecological conditions viewed in the context of male-male within mating systems and within spe- correspond to differences in the competition (for example, sperm cies based on such factors as age or manifestations of sex conflict across competition), they also evolved in rank. For example, male coercion is primates. response to intersexual conflict and 72 Stumpf et al. ARTICLES female-mediated selection.157,173 change resulting from sexual con- dynamics in primatology and evolu- Similarly, coercion and female flict.8,176 More refined methods for tionary anthropology. What is most choice are often categorized as distinguishing between these include interesting are the myriad ways that examples of intersexual selection examining the behavioral, ontoge- sexual conflict is expressed across because the conflicting interests of netic, and temporal plasticity of different primate mating systems. males and females drive evolution in male and female strategies (for Further research across primates will both sexes. However, these behaviors example, across the menstrual cycle) enable testing of the framework and also evolve in response to intrasexual and their effectiveness.9,14,67,74,177,178 predictions introduced in this paper. conflict. Thus, an individual’s repro- More broadly, the coupling of behav- Integrating clearer operational defini- ductive success is affected by com- ioral and genetic (for example, pater- tions, new methodologies, long-term peting strategies of both the opposite nity) data is paramount to assessing observations, and new models for and the same sex, while also driving the effectiveness of different sexual exploring male and female interac- selection on both the same and strategies and the costs and benefits tions will offer a richer understand- opposite sex. Ultimately, however, of sexually antagonistic selection on ing of sexual conflict in this order, how well an individual competes individual fitness. Parental care is and opens up new comparative reproductively relative to others of the another fruitful area for examining directions where primate research same sex is what determines the sexual conflict, as this characteristic can certainly play an important role. strength of selection.174 is of particular relevance to primates, There is much work to be done. Genetic studies of primates, with carries a heavy cost, and is under ACKNOWLEDGEMENTS such a diversity of mating systems, substantial selective pressure. Exam- provide tremendous potential for ining the interaction between male This paper arose from a graduate understanding intersexual conflict. and female neurological, hormonal, seminar on sexual selection at the Evidence of rapid evolution in genes and behavioral mechanisms influenc- University of Illinois at Urbana Cham- related to reproduction highlights ing paternal care179 within a sexual paign. We thank John Polk, Paul potential sexual conflict. Further conflict framework holds enormous Garber, Steve Leigh, Mark Grabowski, studies that identify the functional potential to shed light on the evolu- and Scott Williams for helpful feed- consequences of these molecular tion of this important, yet rare and back on the manuscript. John Fleagle changes will help to clarify how poorly understood behavior. and three anonymous reviewers pro- intersexual and intrasexual selection Studies of primate morphology vided constructive comments. drive molecular evolution.135,175 and physiology are also critical to Quantitative genetics is another com- evaluate sexual conflict. In particu- pelling tool for examining sexual lar, female traits affecting postcopu- REFERENCES conflict in primates. Recently, latory sexual selection may be under 1 Foerster and coworkers117 applied strong selection, but these mecha- Parker GA. 1979. Sexual selection and sex- 180 ual conflict. 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