Urinary neopterin of wild chimpanzees indicates that cell-mediated immune activity varies by age, sex, and female reproductive status

The study of free-living animal populations is necessary to understand life history trade-offs associated with immune investment. To investigate the role of life history strategies in shaping proinflammatory cell-mediated immune function, we analyzed age, sex, and reproductive status as predictors of urinary neopterin in 70 sexually mature chimpanzees (Pan troglodytes) at Ngogo, Kibale National Park, Uganda. In the absence of clinical signs of acute infectious disease, neopterin levels significantly increased with age in both male and female chimpanzees, as observed in humans and several other vertebrate species. Furthermore, males exhibited higher neopterin levels than females across adulthood. Finally, females with full sexual swellings, pregnant females, and post-reproductive females, the oldest individuals in our sample, exhibited higher neopterin levels than lactating females and cycling females without full swellings. Variation in females’ neopterin levels by reproductive status is consistent with post-ovulatory and pregnancy-related immune patterns documented in humans. Together, our results provide evidence of ample variation in chimpanzee immune activity corresponding to biodemographic and physiological variation. Future studies comparing immune activity across ecological conditions and social systems are essential for understanding the life histories of primates and other mammals.

The cost of associating with males for Bornean and Sumatran female orangutans: a hidden form of sexual conflict?

Sexual coercion, in the form of forced copulations, is relatively frequently observed in orangutans and generally attributed to their semi-solitary lifestyle. High ecological costs of association for females may be responsible for this lifestyle and may have prevented the evolution of morphological fertility indicators (e.g., sexual swellings), which would attract (male) associates. Therefore, sexual conflict may arise not only about mating per se but also about associations, because males may benefit from associations with females to monitor their reproductive state and attempt to monopolize their sexual activities. Here, we evaluate association patterns and costs for females when associating with both males and females of two different orangutan species at two study sites: Suaq, Sumatra (Pongo abelii), and Tuanan, Borneo (Pongo pygmaeus wurmbii). Female association frequency with both males and females was higher in the Sumatran population, living in more productive habitat. Accordingly, we found that the cost of association, in terms of reduced feeding to moving ratio and increased time being active, is higher in the less sociable Bornean population. Males generally initiated and maintained such costly associations with females, and prolonged associations with males led to increased female fecal cortisol metabolite (FCM) levels at Tuanan, the Bornean population. We conclude that male-maintained associations are an expression of sexual conflict in orangutans, at least at Tuanan. For females, this cost of association may be responsible for the lack of sexual signaling, while needing to confuse paternity. Significance statement Socioecological theory predicts a trade-off between the benefits of sociality and the ecological costs of increased feeding competition. Orangutans’ semi-solitary lifestyle has been attributed to the combination of high association costs and low predation risk. Previous work revealed a positive correlation between association frequencies and habitat productivity, but did not measure the costs of association. In this comparative study, we show that females likely incur costs from involuntary, male-maintained associations, especially when they last for several days and particularly in the population characterized by lower association frequencies. Association maintenance therefore qualifies as another expression of sexual conflict in orangutans, and especially prolonged, male-maintained associations may qualify as an indirect form of sexual coercion.

Foraging postures are a potential communicative signal in female bonobos

Body postures are essential in animal behavioural repertoires and their communicative role has been assessed in a wide array of taxa and contexts. Some body postures function as amplifiers, a class of signals that increase the detection likelihood of other signals. While foraging on the ground, bonobos (Pan paniscus) can adopt different crouching postures exposing more or less of their genital area. To our knowledge, their potential functional role in the sociosexual life of bonobos has not been assessed yet. Here we show, by analysing more than 2,400 foraging events in 21 captive bonobos, that mature females adopt a rear-exposing posture (forelimb-crouch) and do so significantly more often when their anogenital region is swollen than during the non-swollen phase. In contrast, mature males almost completely avoid this posture. Moreover, this strong difference results from a diverging ontogeny between males and females since immature males and females adopt the forelimb-crouch at similar frequencies. Our findings suggest that the forelimb-crouch posture may play a communicative role of amplification by enhancing the visibility of female sexual swellings, a conspicuous signal that is very attractive for both males and females. Given the high social relevance of this sexual signal, our study emphasizes that postural signalling in primates probably deserves more attention, even outside of reproductive contexts.

On the evolution of visual female sexual signalling

A long-standing evolutionary puzzle surrounds female sexual signals visible around the time of ovulation. Even among just primates, why do some species have substantial sexual swellings and/or bright colorations visible around females' genital regions, while other species are like humans, with no signs of ovulation visible? What is the evolutionary purpose behind not just these signs, but also this great variation seen among species? Here, we examine the evolutionary trade-offs associated with visual ovulation signalling using agent-based modelling. Our model predicts how various factors, including male genetic heterogeneity and reproductive inequality, female physiological costs, group size, and the weighting of genetic versus non-genetic benefits coming from males, each influence the strength of ovulation signalling. Our model also predicts that increasing the impacts of infanticide will increase ovulation signalling. We use comparative primate data to show that, as predicted by our model, larger group size and higher risk of infanticide each correlate with having stronger visual ovulation signs. Overall, our work resolves some old controversies and sheds new light on the evolution of visual female sexual signalling.