Report Sexually Coercive Male Chimpanzees Sire More Offspring (2014)

School of Human Evolution and Social Change,Arizona State University, Tempe, AZ 85287-2402, USASummaryIn sexually reproducing animals, male and female reproduc-tive strategies often conﬂict [1]. In some species, males useaggression to overcome female choice [2, 3], but debatepersists over the extent to which this strategy is successful.Previous studies of male aggression toward females amongwild chimpanzees have yielded contradictory results aboutthe relationship between aggression and mating behavior[4–11]. Critically, however, copulation frequency in primatesis not always predictive of reproductive success [12].We analyzed a 17-year sample of behavioral and geneticdata from the Kasekela chimpanzee (Pan troglodytesschweinfurthii)communityinGombeNationalPark,Tanzania,to test the hypothesis that male aggression toward femalesincreasesmalereproductivesuccess.Weexaminedtheeffectof male aggression toward females during ovarian cycling,including periods when the females were sexually receptive(swollen) and periods when they were not. We found that,after controlling for confounding factors, male aggressionduring a female’s swollen periods was positively correlatedwith copulation frequency. However, aggression towardswollen females was not predictive of paternity. Instead,aggression by high-ranking males toward females duringtheir nonswollen periods was positively associated withlikelihood of paternity. This indicates that long-term patternsof intimidation allow high-ranking males to increase theirreproductive success, supporting the sexual coercion hy-pothesis. To our knowledge, this is the ﬁrst study to presentgenetic evidence of sexual coercion as an adaptive strategyin a social mammal.ResultsThe sexual coercion hypothesis predicts that male aggres-sion against females increases male ﬁtness [2, 10, 11]. Wetested this prediction using behavioral and genetic datafrom wild chimpanzees (Pan troglodytes schweinfurthii)in Gombe National Park, Tanzania. Female chimpanzeesexhibit an anogenital swelling for about 10 days within a36-day ovarian cycle [13]. During this time, a female mateswith most males in the community, although high-rankingmales attempt to prevent this by directing aggression towardcompetitors and the female herself. We consider male-female aggression during the period of maximal swelling(‘‘swollen aggression’’) as potential short-term sexual coer-cion (but not as forced copulation, as males rarely attemptintromission during or immediately following aggression[11]). We consider aggression occurring outside this period(‘‘nonswollen aggression’’) as potential long-term coercion.Results support the hypothesis that aggression towarda given female functions as an intimidation strategy thatincreases a male’s future chances of siring that female’soffspring.Aggression and PaternityWe used generalized linear mixed models (GLMMs) toanalyze the relationship between aggression and likelihoodof paternity within dyads. We included several additionalpotentially inﬂuential factors (see Experimental Procedures)and used Akaike’s information criterion (DAICc, a measureof the relative quality of a statistical model [14]) to identifythe best predictors of paternity. Nonswollen aggressionrate, male dominance rank, the interaction between thesetwo factors, and dyadic relatedness were important predic-tors of paternity (Table 1; Figure 1A). Paternity probabilitywas greater for males of higher rank (Figures 1A and 1C)but was lower if the male and female were closely related(Figures 1A and 1D). Males that were more aggressivetoward females during nonswollen periods were more likelyto conceive with those females. Although this relationshipwas positive for all males, it was particularly striking amonghigh-ranking males—a high-ranking male with the greatestrate of nonswollen aggression had a 47.9% chance ofconceiving with that female (Figure 1B). Among the subsetof dyads in which the male’s dominance rank scorewas one standard deviation above the mean (standardizedrankscore[MDS-Z]>1,n=47),therewasastrongpositive association between nonswollen aggression rateand paternity (Pearson correlation = 0.55, p < 0.00001;Figure 2).Aggression and CopulationWe used GLMMs to identify predictors of copulation rate,and again used DAICc as the selection criterion. We identiﬁedboth swollen and nonswollen aggression rates, female age,male rank, alpha male despotism ratio (see ExperimentalProcedures), relatedness, and two interaction terms as thebest predictors of copulation rate (Table 2). Overall, malesthat showed higher levels of aggression toward femalestended to copulate with those females at higher rates. How-ever, swollen aggression had the strongest association withcopulation rate. Copulation rates increased with female agebut were lower in closely related dyads and during periodswhen the alpha male was particularly dominant (high despo-