Browsing by Author "Pusey, Anne E"

In chimpanzees, most females disperse from the community in which they were born to reproduce in a new community, thereby eliminating the risk of inbreeding with close kin. However, across sites, some females breed in their natal community, raising questions about the flexibility of dispersal, the costs and benefits of different strategies and the mitigation of costs associated with dispersal and integration. In this dissertation I address these questions by combining long-term behavioral data and recent field observations on maturing and young adult females in Gombe National Park with an experimental manipulation of relationship formation in captive apes in the Congo.

To assess the risk of inbreeding for females who do and do not disperse, 129 chimpanzees were genotyped and relatedness between each dyad was calculated. Natal females were more closely related to adult community males than were immigrant females. By examining the parentage of 58 surviving offspring, I found that natal females were not more related to the sires of their offspring than were immigrant females, despite three instances of close inbreeding. The sires of all offspring were less related to the mothers than non-sires regardless of the mother’s residence status. These results suggest that chimpanzees are capable of detecting relatedness and that, even when remaining natal, females can largely avoid, though not eliminate, inbreeding.

Next, I examined whether dispersal was associated with energetic, social, physiological and/or reproductive costs by comparing immigrant (n=10) and natal (n=9) females of similar age using 2358 hours of observational data. Natal and immigrant females did not differ in any energetic metric. Immigrant females received aggression from resident females more frequently than natal females. Immigrants spent less time in social grooming and more time self-grooming than natal females. Immigrant females primarily associated with resident males, had more social partners and lacked close social allies. There was no difference in levels of fecal glucocorticoid metabolites in immigrant and natal females. Immigrant females gave birth 2.5 years later than natal females, though the survival of their first offspring did not differ. These results indicate that immigrant females in Gombe National Park do not face energetic deficits upon transfer, but they do enter a hostile social environment and have a delayed first birth.

Next, I examined whether chimpanzees use condition- and phenotype-dependent cues in making dispersal decisions. I examined the effect of social and environmental conditions present at the time females of known age matured (n=25) on the females’ dispersal decisions. Females were more likely to disperse if they had more male maternal relatives and thus, a high risk of inbreeding. Females with a high ranking mother and multiple maternal female kin tended to disperse less frequently, suggesting that a strong female kin network provides benefits to the maturing daughter. Females were also somewhat less likely to disperse when fewer unrelated males were present in the group. Habitat quality and intrasexual competition did not affect dispersal decisions. Using a larger sample of 62 females observed as adults in Gombe, I also detected an effect of phenotypic differences in personality on the female’s dispersal decisions; extraverted, agreeable and open females were less likely to disperse.

Natural observations show that apes use grooming and play as social currency, but no experimental manipulations have been carried out to measure the effects of these behaviors on relationship formation, an essential component of integration. Thirty chimpanzees and 25 bonobos were given a choice between an unfamiliar human who had recently groomed or played with them over one who did not. Both species showed a preference for the human that had interacted with them, though the effect was driven by males. These results support the idea that grooming and play act as social currency in great apes that can rapidly shape social relationships between unfamiliar individuals. Further investigation is needed to elucidate the use of social currency in female apes.

I conclude that dispersal in female chimpanzees is flexible and the balance of costs and benefits varies for each individual. Females likely take into account social cues present at maturity and their own phenotype in choosing a settlement path and are especially sensitive to the presence of maternal male kin. The primary cost associated with philopatry is inbreeding risk and the primary cost associated with dispersal is delay in the age at first birth, presumably resulting from intense social competition. Finally, apes may strategically make use of affiliative behavior in pursuing particular relationships, something that should be useful in the integration process.

Sexual conflict occurs when female and male fitness interests diverge. In a social system characterized by aggressive sexual coercion and the risk of infanticide, female chimpanzees (Pan troglodytes) respond to this conflict by exhibiting an exaggerated sexual swelling that advertises sexual receptivity while concealing the exact timing of ovulation. Sexual swellings impose significant costs, yet can persist into pregnancy. Records from long-term studies of eastern chimpanzees (P. t. schweinfurthii) in Gombe National Park, TZ, and Kibale National Park, UG, provide data on postconception swellings, while data on group composition and behaviors such as mating, grooming, and aggression are drawn from the Gombe database only. Throughout, I use linear mixed models to simultaneously test multiple effects while controlling for repeated measures of individuals. In Chapter 1, I tested whether variation in females’ vulnerability to infanticide and aggression predicted the amount of swelling during pregnancy. In Chapter 2, I examined female-male relationships across reproductive states to ask whether females can better gain benefits and avoid costs by affiliating promiscuously with all males, or by investing in relationships with preferred males. Finally, I analyzed metabolites of reproductive hormones using urine samples from pregnant females in both populations to build a hormonal profile of postconception swellings. Swellings during pregnancy increase female-male association, and are caused by the same basic hormonal mechanism as preconception swellings, though they occur in a very different hormonal milieu. Females at greater risk of infanticide and intrasexual aggression swell more during pregnancy. Females mate promiscuously before conception, but during pregnancy and lactation, preferentially groom with males that are likely to protect them from aggression and infanticide. Based on these and other findings, I conclude that postconception swellings in chimpanzees are an adaptive response to sexual conflict.

This dissertation presents three studies of the social and reproductive behavior and social structure of male chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania.

I. In many species of non-human primates, males cooperate and form friendly social bonds while simultaneously competing with each other for dominance rank and mating opportunities. While several studies reveal clear links between female bonds and correlates of fitness in female philopatric primate species, few have investigated whether bonds among males have measurable fitness benefits. Further, no studies in chimpanzees have investigated the fitness effects of cooperative exchange, or contrasted the fitness effects of bond formation and cooperative exchange. Here, I investigate whether 1) male social bonds, 2) position in affiliative and coalition networks, or 3) strategic exchange with other individuals of grooming for support or tolerance facilitate fitness benefits in one population of wild, free-ranging chimpanzees. I generated measures of social connectedness, coalition formation, and grooming effort for each male in two-year periods from 1990 to 2011, and employed mixed models to determine whether, controlling for current rank and age, these measures predicted 1) rank change (a correlate of future reproductive output) and 2) reproductive success within each period. I found that rank change was associated with betweenness in the network of coalition formation, but only weakly with social bonds and not at all with position in the network of social relationships. I further found that rank change was predicted by grooming effort, although this relationship depended on male dominance rank. Surprisingly, reproductive success was not associated with social connectedness or with betweenness in coalitionary or social relationship networks. Instead, grooming effort strongly predicted reproductive success. Thus it appears that males that occupy central positions in the coalition network, and those that groom others at a high rate, are more likely to rise in rank (if they are low-ranking to begin with). However, males that successfully sire offspring groom others at a high rate. These results suggest that, unlike in cercopithecine primates, social bonds do not enhance fitness in male chimpanzees, and instead males rely on grooming and coalition formation to improve their rank and reproductive success.

II. Animals face both costs and benefits associated with living in groups. When the costs of membership exceed the benefits, group fissions can occur. Fissions are documented in a number of animal species, but are comparatively rare in male philopatric primates. One of the few likely cases occurred in chimpanzees in 1973 in Gombe National Park, Tanzania, when the main study community split into two separate communities, Kasekela and Kahama. Over the next four years, the Kasekela community killed the adult males and one female of the Kahama community. Here we use social network analysis to explore the process of community fission in chimpanzees by examining association, grooming, and ranging patterns. We found that the two communities split from one original cohesive community, although one with incipient subgrouping patterns. Subgrouping patterns in the grooming and association networks began to increase sharply beginning in 1971, and this period closely coincided with a dominance struggle between three high-ranking males and with a peak in operational sex ratio. Finally, we found a relationship between post-split community membership and previous association, grooming and ranging patterns in most periods of analysis, a tendency that became more pronounced as the fission approached. Thus, analysis suggests that the community began to split during a time of unusual sex ratio and a protracted dominance struggle, and that individuals remained with others with whom they preferentially associated in the previous years. These results are contrasted with group fissions in other taxa, and provide clues to the costs and benefits of group membership in chimpanzees.

III. In sexually reproducing animals, male and female reproductive strategies often conflict. In some species, males use aggression to overcome female choice, but debate persists over the extent to which this strategy is successful. Previous studies of male aggression toward females among wild chimpanzees have yielded contradictory results about the relationship between aggression and mating behavior. Critically, however, copulation frequency in primates is not always predictive of reproductive success. We analyzed a 17-year sample of behavioral and genetic data from the Kasekela chimpanzee community in Gombe National Park, Tanzania, to test the hypothesis that male aggression toward females increases male reproductive success. We examined the effect of 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 aggression during a female’s swollen periods was positively correlated with copulation frequency. However, aggression toward swollen females was not predictive of paternity. Instead, aggression by high-ranking males toward females during their nonswollen periods was positively associated with likelihood of paternity. This indicates that long-term patterns of intimidation allow high-ranking males to increase their reproductive success, supporting the sexual coercion hypothesis. To our knowledge, this is the first study to present genetic evidence of sexual coercion as an adaptive strategy in a social mammal.