Melissa Emery Thompson

Aging and fertility patterns in wild chimpanzees provide insights into the evolution of menopause

Human menopause is remarkable in that reproductive senescence is markedly accelerated relative to somatic aging, leaving an extended postreproductive period for a large proportion of women. Functional explanations for this are debated, in part because comparative data from closely related species are inadequate. Existing studies of chimpanzees are based on very small samples and have not provided clear conclusions about the reproductive function of aging females. These studies have not examined whether reproductive senescence in chimpanzees exceeds the pace of general aging, as in humans, or occurs in parallel with declines in overall health, as in many other animals. In order to remedy these problems, we examined fertility and mortality patterns in six free-living chimpanzee populations. Chimpanzee and human birth rates show similar patterns of decline beginning in the fourth decade, suggesting that the physiology of reproductive senescence was relatively conserved in human evolution. However, in contrast to humans, chimpanzee fertility declines are consistent with declines in survivorship, and healthy females maintain high birth rates late into life. Thus, in contrast to recent claims, we find no evidence that menopause is a typical characteristic of chimpanzee life histories.

Male coercion and the costs of promiscuous mating for female chimpanzees

For reasons that are not yet clear, male aggression against females occurs frequently among primates with promiscuous mating systems. Here, we test the sexual coercion hypothesis that male aggression functions to constrain female mate choice. We use 10 years of behavioural and endocrine data from a community of wild chimpanzees (Pan troglodytes schweinfurthii) to show that sexual coercion is the probable primary function of male aggression against females. Specifically, we show that male aggression is targeted towards the most fecund females, is associated with high male mating success and is costly for the victims. Such aggression can be viewed as a counter-strategy to female attempts at paternity confusion, and a cost of multi-male mating.

Core area quality is associated with variance in reproductive success among female chimpanzees at Kibale National Park

Female East African chimpanzees, Pan troglodytes schweinfurthii, tend to range apart from each other in dispersed core areas, and they have dominance interactions with each other so rarely that it is difficult for observers to assess a dominance hierarchy. Nevertheless female chimpanzees can have high variance in fitness. Here, we test the hypothesis that female chimpanzee fitness variance is associated with variation in the foraging quality of their ranges. We studied range usage of 21 wild adult female chimpanzees within the Kanyawara community, Kibale National Park, Uganda. Core areas of individuals remained stable over a 9-year period and varied in their density of preferred foods. Females in neighbourhoods containing more preferred foods had elevated ovarian hormone production, shorter birth intervals and higher infant survivorship. Our results thus suggest that superior access to food may have enabled some community females to reproduce more successfully than others. Although dominance interactions are less frequent among females than among males of this species, we propose that the intensity of selection on intrasexual competition may be similar between the sexes. We discuss potential applications to other fissionefusion species.

Male Chimpanzees Prefer Mating with Old Females

Cross-cultural studies indicate that womens sexual attractiveness generally peaks before motherhood and declines with age. Cues of female youth are thought to be attractive because humans maintain long-term pair bonds, making reproductive value (i.e. future reproductive potential) particularly important to males. Menopause is believed to exaggerate this preference for youth by limiting womens future fertility. This theory predicts that in species lacking long-term pair bonds and menopause, males should not exhibit a preference for young mates. We tested this prediction by studying male preferences in our closest living relative, the chimpanzee (Pan troglodytes). We show that despite their promiscuous mating system, chimpanzee males, like humans, prefer some females over others. However, in contrast to humans, chimpanzee males prefer older, not younger, females. These data robustly discriminate patterns of male mate choice between humans and chimpanzees. Given that the human lineage evolved from a chimpanzee-like ancestor, they indicate that male preference for youth is a derived human feature, likely adapted from a tendency to form unusually long term mating bonds.

Female-led infanticide in wild chimpanzees

Document S1. Supplemental Methods, and Supplemental ReferencesxDownload (.01 MB ) Document S1. Supplemental Methods, and Supplemental ReferencesVideo illustrating adult female Zimba carrying female infant, biting its head and Zimba then receiving aggression from adult males Bwoba and Maani. Filmed by K.S. with a hand-held video camcorder (Canon MVX330i).xDownload (3.3 MB ) Video illustrating adult female Zimba carrying female infant, biting its head and Zimba then receiving aggression from adult males Bwoba and Maani. Filmed by K.S. with a hand-held video camcorder (Canon MVX330i).

Reproductive endocrinology of wild female Chimpanzees (Pan troglodytes schweinfurthii): methodological considerations and the role of hormones in sex and conception

Fecal and urine samples were collected from 81 female East African chimpanzees (Pan troglodytes schweinfurthii) in three major study populations in Gombe National Park, Tanzania, and Budongo Forest Reserve and Kibale National Park, Uganda. In this study I evaluated issues related to sample storage and assay reliability, and used these methods to investigate the significance of ovarian hormone levels in terms of conception success and sexual behavior. Drying of feces proved to be an effective technique and resulted in hormonal concentrations that were significantly correlated with concentrations in frozen feces. Estimates of ovarian steroid production based on urine and fecal sampling were significantly correlated with each other. The ovarian cycle profiles obtained, which were aligned relative to sexual swelling detumescence, corroborate previous findings in wild west African chimpanzees [Deschner et al., Animal Behaviour 66:551–560, 2003] in suggesting that the fertile period is limited to the last week of tumescence, but that ovulatory timing is not as precise as previously thought. A comparison across cycles confirmed the hypothesis that higher ovarian steroid levels are associated with an increased probability of conception. Females that did conceive with relatively low hormone levels had poor reproductive outcomes. Sexual behavior was tied to the probability of conception both within and across cycles. Copulatory activity within cycles closely followed the estrogen profile and was timed to coincide, on average, with the peak fertile period of females. Further, rates of copulation were significantly higher during the fertile periods of cycles that led to conception than those that did not. Am. J. Primatol. 67:137–158, 2005.

Female Competition over Core Areas in Pan troglodytes schweinfurthii, Kibale National Park, Uganda

Aggression is rare among wild female chimpanzees. However, in the Kanyawara chimpanzee community in Kibale National Park, Uganda, stable use of food-rich core areas is linked to increased reproductive success, suggesting that contest competition might occur over access to the highest-quality ranges. To examine this hypothesis, we studied aggression and dominance relationships among Kanyawara females during a 10-yr period that included the immigration of 5 females into the community. We tested 2 predictions: 1) that female-female aggression should intensify when immigrants enter the community because this is when core area access is determined and 2) that the quality of core areas should reflect relative female dominance relationships. In support of the first prediction, female-female aggression increased 4-fold when new immigrants were in the community, with rates peaking when there were multiple immigrants. This pattern was due primarily to aggression by resident mothers toward immigrants and featured coalitionary aggression, a rare behavior among female chimpanzees. In support of the second prediction, females occupying core areas high in foraging quality ranked high overall and higher than expected for their ages, whereas females occupying low-quality core areas were lower-ranking and ranked lower than expected for their ages. Together, the data indicate that though female aggression does not regularly occur in chimpanzees, contest competition continues to play an important role in determining long-term access to resources, an important correlate of reproductive success.

Urinary C-peptide of insulin as a non-invasive marker of energy balance in wild orangutans

Assessment of energetic condition is a critical tool for behavioral and reproductive ecologists. However, accurate quantification of energy intake and expenditure is labor-intensive, and it can be problematic for field scientists to obtain regular data on individual animals. C-peptide, a polypeptide segment of the proinsulin molecule that is secreted along with insulin in an equimolar relationship, can be measured in urine, and thus offers a potential means for the non-invasive assessment of energy balance in wild animals. Here, we validate C-peptide for the quantification of energetic condition, with specific application to wild orangutans (Pongo pygmaeus). We determined that application of urine to filter paper results in significantly lower C-peptide recoveries versus fresh samples. However, concentrations in filter paper samples were significantly correlated with fresh urine and were stable over various storage conditions and durations. We compared the C-peptide concentrations from wild orangutan urine samples with three independent measures of energetic condition: ketone bodies (urinalysis), caloric intake (nutritional biochemistry), and food availability (phenology). As expected, C-peptide concentrations were significantly lower in samples that tested positive for ketones in the field. Monthly average C-peptide concentrations of both male and female orangutans were significantly correlated with monthly determinations of energy intake and food availability. Therefore, we conclude that the collection and preservation of urine samples for C-peptide analysis are feasible under most field conditions and, in this species, presents a useful tool for assessing changes in energy balance.

Male Mating Interest Varies with Female Fecundity in Pan troglodytes schweinfurthii of Kanyawara, Kibale National Park

Female chimpanzees mate promiscuously during a period of extended receptivity marked by prominent sexual swelling. Recent studies of wild chimpanzees indicate that subtle variations in swelling size could act as a reliable cue of female fertilization potential both within and between cycles (Emery and Whitten Behavioral Ecology and Sociobiology, 54, 340–351, 2003; Deschner et al.Hormones and Behavior, 46, 204–215, 2004). Copulation rates increase during the periovulatory period and during conception cycles (Deschner et al.Hormones and Behavior, 46, 204–215, 2004; Emery Thompson American Journal of Primatology, 67, 137–158, 2005a), suggesting that males may be able to assess female fertilization potential. We asked whether facultative timing of copulation in Kanyawara chimpanzees was due to increased male mating interest or to increased female proceptivity during the most fecund days. We assessed multiple measures of male mating effort in cycles aligned relative to the day of detumescence and compared periovulatory days to other days of maximal swelling, and conception cycles to nonconception cycles. The rate and proportion of male initiative in soliciting sexual behavior increased during periods of highest fertilization potential. Males were also more likely to interrupt copulations, associate with estrous females, and compete with other males when females were most likely to conceive. Females initiated copulations more frequently during conception cycles but did not visibly shift mating behavior within cycles. Our results support the hypothesis that male chimpanzees have the ability to assess the profitability of mating attempts, a trait that may act as a counter-adaptation to female strategies to obscure paternity. We discuss potential cues and the implications for female reproductive strategies.

Demographic and Female Life History Parameters of Free-Ranging Chimpanzees at the Chimpanzee Rehabilitation Project, River Gambia National Park

We analyzed fertility and mortality records for 113 provisioned, free-ranging chimpanzees at the River Gambia National Park, The Gambia. The chimpanzees are rehabilitated orphans released by the Chimpanzee Rehabilitation Project (CRP), and their descendants born in a natural environment. Females experienced their 1st births at an average age of 14.3 yr, with average interbirth intervals of 68 mo. Despite limited provisioning, reproductive parameters in both released and 1st-generation females resembled those of wild chimpanzees and showed seasonal fluctuations. Mortality rates were low compared to those for wild chimpanzees, particularly for infants and juveniles; life expectancy at birth was 23.6 yr for females and 18 yr for males. The results have implications for our understanding of variation in reproductive parameters between captive and wild chimpanzees. We also discuss issues related to chimpanzee conservation and captive rearing.