Ecological variation in adult social play reveals a hidden cost of motherhood for wild chimpanzees.

Though common among humans, social play by adults is an uncommon occurrence in most animals, even between parents and offspring.1,2,3 The most common explanation for why adult play is so rare is that its function and benefits are largely limited to development, so that social play has little value later in life.3,4,5,6 Here, we draw from 10 years of behavioral data collected by the Kibale Chimpanzee Project to consider an alternative hypothesis: that despite its benefits, adult play in non-humans is ecologically constrained by energy shortage or time limitations. We further hypothesized that, since they may be the only available partners for their young offspring, mother chimpanzees pay greater costs of play than other adults. Our analysis of nearly 4,000 adult play bouts revealed that adult chimpanzees played both among themselves and with immature partners. Social play was infrequent when diet quality was low but increased with the proportion of high-quality fruits in the diet. This suggests that adults engage in play facultatively when they have more energy and/or time to do so. However, when diet quality was low and most adult play fell to near zero, play persisted between mothers and offspring. Increased use of play by adult chimpanzees during periods of resource abundance suggests that play retains value as a social currency beyond development but that its costs constrain its use. At the same time, when ecological conditions constrain opportunities for young to play, play by mothers fills a critical role to promote healthy offspring development.

Observational approaches to chimpanzee behavior in an African sanctuary: Implications for research, welfare, and capacity-building.

Research in African ape sanctuaries has emerged as an important context for our understanding of comparative cognition and behavior. While much of this work has focused on experimental studies of cognition, these animals semi-free-range in forest habitats and therefore can also provide important information about the behavior of primates in socioecologically-relevant naturalistic contexts. In this "New Approaches" article, we describe a project where we implemented a synthetic program of observational data collection at Ngamba Island Chimpanzee Sanctuary in Uganda, directly modeled after long-term data collection protocols at the Kibale Chimpanzee Project in Uganda, a wild chimpanzee field site. The foundation for this project was a strong partnership between sanctuary staff, field site staff, and external researchers. We describe how we developed a data-collection protocol through discussion and collaboration among these groups, and trained sanctuary caregivers to collect novel observational data using these protocols. We use these data as a case study to examine: (1) how behavioral observations in sanctuaries can inform primate welfare and care practices, such as by understanding aggression within the group; (2) how matched observational protocols across sites can inform our understanding of primate behavior across different contexts, including sex differences in social relationships; and (3) how more robust collaborations between foreign researchers and local partners can support capacity-building in primate range countries, along with mentoring and training students more broadly.

Age-related social selectivity: An adaptive lens on a later life social phenotype.

Age-related social selectivity is a process in which older humans reduce their number of social partners to a subset of positive and emotionally fulfilling relationships. Although selectivity has been attributed to humans' unique perceptions of time horizons, recent evidence demonstrates that these social patterns and processes occur in other non-human primates, suggesting an evolutionarily wider phenomenon. Here, we develop the hypothesis that selective social behavior is an adaptive strategy that allows social animals to balance the costs and benefits of navigating social environments in the face of age-related functional declines. We first aim to distinguish social selectivity from the non-adaptive social consequences of aging. We then outline multiple mechanisms by which social selectivity in old age may enhance fitness and healthspan. Our goal is to lay out a research agenda to identify selective strategies and their potential benefits. Given the importance of social support for health across primates, understanding why aging individuals lose social connections and how they can remain resilient has vital applications to public health research.

Weak, but not strong, ties support coalition formation among wild female chimpanzees.

In social species, individuals may be able to overcome competitive constraints on cooperation by leveraging relationships with familiar, tolerant partners. While strong social ties have been linked to cooperation in several social mammals, it is unclear the extent to which weak social ties can support cooperation, particularly among non-kin. We tested the hypothesis that weakly affiliative social relationships support cooperative coalition formation using 10 years of behavioural data on wild female chimpanzees. Female chimpanzees typically disperse and reside with non-kin as adults. Their social relationships are differentiated but often relatively weak, with few dyads sharing strong bonds. Females occasionally form aggressive coalitions together. Three measures of relationship quality-party association, five-metre proximity and whether a dyad groomed-positively predicted coalitions, indicating that relationship quality influenced coalition partnerships. However, dyads that groomed frequently did not form more coalitions than dyads that groomed occasionally, and kin did not cooperate more than expected given their relationship quality. Thus, strong bonds and kinship did not bolster cooperation. We conclude that cooperative coalitions among female chimpanzees depend on social tolerance but do not require strong bonds. Our findings highlight social tolerance as a distinct pathway through which females can cultivate cooperative relationships. This article is part of the theme issue 'Cooperation among women: evolutionary and cross-cultural perspectives'.

Female reproduction and viral infection in a long-lived mammal.

For energetically limited organisms, life-history theory predicts trade-offs between reproductive effort and somatic maintenance. This is especially true of female mammals, for whom reproduction presents multifarious energetic and physiological demands. Here, we examine longitudinal changes in the gut virome (viral community) with respect to reproductive status in wild mature female chimpanzees Pan troglodytes schweinfurthii from two communities, Kanyawara and Ngogo, in Kibale National Park, Uganda. We used metagenomic methods to characterize viromes of individual chimpanzees while they were cycling, pregnant and lactating. Females from Kanyawara, whose territory abuts the park's boundary, had higher viral richness and loads (relative quantity of viral sequences) than females from Ngogo, whose territory is more energetically rich and located farther from large human settlements. Viral richness (total number of distinct viruses per sample) was higher when females were lactating than when cycling or pregnant. In pregnant females, viral richness increased with estimated day of gestation. Richness did not vary with age, in contrast to prior research showing increased viral abundance in older males from these same communities. Our results provide evidence of short-term physiological trade-offs between reproduction and infection, which are often hypothesized to constrain health in long-lived species.

Vocal signals facilitate cooperative hunting in wild chimpanzees.

Cooperation and communication likely coevolved in humans. However, the evolutionary roots of this interdependence remain unclear. We address this issue by investigating the role of vocal signals in facilitating a group cooperative behavior in an ape species: hunting in wild chimpanzees. First, we show that bark vocalizations produced before hunt initiation are reliable signals of behavioral motivation, with barkers being most likely to participate in the hunt. Next, we find that barks are associated with greater hunter recruitment and more effective hunting, with shorter latencies to hunting initiation and prey capture. Our results indicate that the coevolutionary relationship between vocal communication and group-level cooperation is not unique to humans in the ape lineage and is likely to have been present in our last common ancestor with chimpanzees.

Viruses associated with ill health in wild chimpanzees.

Viral infection is a major cause of ill health in wild chimpanzees (Pan troglodytes), but most evidence to date has come from conspicuous disease outbreaks with high morbidity and mortality. To examine the relationship between viral infection and ill health during periods not associated with disease outbreaks, we conducted a longitudinal study of wild eastern chimpanzees (P. t. schweinfurthii) in the Kanyawara and Ngogo communities of Kibale National Park, Uganda. We collected standardized, observational health data for 4 years and then used metagenomics to characterize gastrointestinal viromes (i.e., all viruses recovered from fecal samples) in individual chimpanzees before and during episodes of clinical disease. We restricted our analyses to viruses thought to infect mammals or primarily associated with mammals, discarding viruses associated with nonmammalian hosts. We found 18 viruses (nine of which were previously identified in this population) from at least five viral families. Viral richness (number of viruses per sample) did not vary by health status. By contrast, total viral load (normalized proportion of sequences mapping to viruses) was significantly higher in ill individuals compared with healthy individuals. Furthermore, when ill, Kanyawara chimpanzees exhibited higher viral loads than Ngogo chimpanzees, and males, but not females, exhibited higher infection rates with certain viruses and higher total viral loads as they aged. Post-hoc analyses, including the use of a machine-learning classification method, indicated that one virus, salivirus (Picornaviridae), was the main contributor to health-related and community-level variation in viral loads. Another virus, chimpanzee stool-associated virus (chisavirus; unclassified Picornavirales), was associated with ill health at Ngogo but not at Kanyawara. Chisavirus, chimpanzee adenovirus (Adenoviridae), and bufavirus (Parvoviridae) were also associated with increased age in males. Associations with sex and age are consistent with the hypothesis that nonlethal viral infections cumulatively reflect or contribute to senescence in long-lived species such as chimpanzees.

Dominance style is a key predictor of vocal use and evolution across nonhuman primates.

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships.

The long lives of primates and the 'invariant rate of ageing' hypothesis.

Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the 'invariant rate of ageing' hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifespan equality seen in humans. We next demonstrate that variation in the rate of ageing within genera is orders of magnitude smaller than variation in pre-adult and age-independent mortality. Finally, we demonstrate that changes in the rate of ageing, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of ageing hypothesis, implying biological constraints on how much the human rate of ageing can be slowed.

Female-directed aggression by adolescent male chimpanzees primarily constitutes dominance striving, not sexual coercion.

OBJECTIVES: Chimpanzees (Pan troglodytes) are notable for exhibiting high levels of male-to-female aggression. Much of this aggression from adult males serves sexually coercive functions. Despite being smaller and lower-ranking than adult males, adolescent males also engage in regular aggression against adult females. Here, we test whether the primary function of this aggression is sexual coercion, as in adult males, or, alternatively, whether adolescent males use aggression to establish social dominance over females. MATERIALS AND METHODS: We analyzed 1771 copulations and 1812 instances of male-initiated aggression between adolescent males (aged nine through 14 years) and adult females across 21 years of observation of the Kanyawara chimpanzee community in Kibale National Park, Uganda. RESULTS: Our test of the sexual coercion hypothesis revealed that adolescent males did not selectively target cycling females for aggression, nor did aggression against cycling females predict rates of copulation with those females. Our test of the social dominance hypothesis showed that males succeeded in dominating all adult females before, or soon after, dominating their first adult male. Additionally, we found that adolescent males dominated females approximately in the order of the females' own ranks, from the bottom to the top of the female hierarchy. DISCUSSION: Our data illustrate that the establishment of social dominance was more important than sexual coercion in explaining patterns of adolescent male aggression toward females. In comparison, evidence for sexual coercion was clear and compelling in adult males. These findings highlight that the primary function of male-to-female aggression differs between adolescent and adult males.

Sex differences in early experience and the development of aggression in wild chimpanzees.

Sex differences in physical aggression occur across human cultures and are thought to be influenced by active sex role reinforcement. However, sex differences in aggression also exist in our close evolutionary relatives, chimpanzees, who do not engage in active teaching, but do exhibit long juvenile periods and complex social systems that allow differential experience to shape behavior. Here we ask whether early life exposure to aggression is sexually dimorphic in wild chimpanzees and, if so, whether other aspects of early sociality contribute to this difference. Using 13 y of all-occurrence aggression data collected from the Kanyawara community of chimpanzees (2005 to 2017), we determined that young male chimpanzees were victims of aggression more often than females by between 4 and 5 (i.e., early in juvenility). Combining long-term aggression data with data from a targeted study of social development (2015 to 2017), we found that two potential risk factors for aggression-time spent near adult males and time spent away from mothers-did not differ between young males and females. Instead, the major risk factor for receiving aggression was the amount of aggression that young chimpanzees displayed, which was higher for males than females throughout the juvenile period. In multivariate models, sex did not mediate this relationship, suggesting that other chimpanzees did not target young males specifically, but instead responded to individual behavior that differed by sex. Thus, social experience differed by sex even in the absence of explicit gender socialization, but experiential differences were shaped by early-emerging sex differences in behavior.

Aggression, glucocorticoids, and the chronic costs of status competition for wild male chimpanzees.

Across vertebrates, high social status affords preferential access to resources, and is expected to correlate positively with health and longevity. Increasing evidence, however, suggests that although dominant females generally enjoy reduced exposure to physiological and psychosocial stressors, dominant males do not. Here we test the hypothesis that costly mating competition by high-ranking males results in chronic, potentially harmful elevations in glucocorticoid production. We examined urinary glucocorticoids (n = 8029 samples) in a 20-year longitudinal study of wild male chimpanzees (n = 20 adults) in the Kanyawara community of Kibale National Park, Uganda. We tested whether glucocorticoid production was associated with dominance rank in the long term, and with mating competition and dominance instability in the short term. Using mixed models, we found that both male aggression and glucocorticoid excretion increased when the dominance hierarchy was unstable, and when parous females were sexually available. Glucocorticoid excretion was positively associated with male rank in stable and unstable hierarchies, and in mating and non-mating contexts. Glucorticoids increased with both giving and receiving aggression, but giving aggression was the primary mechanism linking elevated glucocorticoids with high rank. Glucocorticoids also increased with age. Together these results show that investment in male-male competition increases cumulative exposure to glucocorticoids, suggesting a long-term tradeoff with health that may constrain the ability to maintain high status across the life course. Our data suggest that the relationship between social rank and glucocorticoid production often differs in males and females owing to sex differences in the operation of sexual selection.

Age-related change in adult chimpanzee social network integration.

BACKGROUND: Social isolation is a key risk factor for the onset and progression of age-related disease and mortality in humans. Nevertheless, older people commonly have narrowing social networks, with influences from both cultural factors and the constraints of senescence. We evaluate evolutionarily grounded models by studying social aging in wild chimpanzees, a system where such influences are more easily separated than in humans, and where individuals are long-lived and decline physically with age. METHODOLOGY: We applied social network analysis to examine age-related changes in social integration in a 7+ year mixed-longitudinal dataset on 38 wild adult chimpanzees (22 females, 16 males). Metrics of social integration included social attractivity and overt effort (directed degree and strength), social roles (betweenness and local transitivity) and embeddedness (eigenvector centrality) in grooming networks. RESULTS: Both sexes reduced the strength of direct ties with age (males in-strength, females out-strength). However, males increased embeddedness with age, alongside cliquishness. These changes were independent of age-related changes in social and reproductive status. Both sexes maintained highly repeatable inter-individual differences in integration, particularly in mixed-sex networks. CONCLUSIONS AND IMPLICATIONS: As in humans, chimpanzees appear to experience senescence-related declines in social engagement. However, male social embeddedness and overall sex differences were patterned more similarly to humans in non-industrialized versus industrialized societies. Such comparisons suggest common evolutionary roots to ape social aging and that social isolation in older humans may hinge on novel cultural factors of many industrialized societies. Lastly, individual and sex differences are potentially important mediators of successful social aging in chimpanzees, as in humans. Lay summary: Few biological models explain why humans so commonly have narrowing social networks with age, despite the risk factor of social isolation that small networks pose. We use wild chimpanzees as a comparative system to evaluate models grounded in an evolutionary perspective, using social network analysis to examine changes in integration with age. Like humans in industrialized populations, chimpanzees had lower direct engagement with social partners as they aged. However, sex differences in integration and older males' central positions within the community network were more like patterns of sociality in several non-industrialized human populations. Our results suggest common evolutionary roots to human and chimpanzee social aging, and that the risk of social isolation with age in industrialized populations stems from novel cultural factors.

Age Patterning in Wild Chimpanzee Gut Microbiota Diversity Reveals Differences from Humans in Early Life.

Survival in primates is facilitated by commensal gut microbes that ferment otherwise indigestible plant matter, resist colonization by pathogens, and train the developing immune system.1,2 However, humans are unique among primates in that we consume highly digestible foods, wean early, mature slowly, and exhibit high lifelong investments in maintenance.3-6 These adaptations suggest that lifetime trajectories of human-microbial relationships could differ from those of our closest living relatives. Here, we profile the gut microbiota of 166 wild chimpanzees aged 8 months to 67 years in the Kibale National Park, Uganda and compare the patterns of gut microbial maturation to those previously observed in humans. We found that chimpanzee gut microbial alpha-diversity, composition, density, interindividual variation, and within-individual change over time varied significantly with age. Notably, gut microbial signatures in infants <2 years old were distinct across all five metrics. Infant chimpanzee guts were enriched in some of the same taxa prevalent in infant humans (e.g., Bifidobacterium, Streptococcus, and Bacteroides), and chimpanzee gut microbial communities, like those of humans, exhibited higher interindividual variation in infancy versus later in life. However, in direct contrast to human infants, chimpanzee infants harbored surprisingly high-diversity rather than low-diversity gut bacterial communities compared with older conspecifics. These data indicate differential trajectories of gut microbiota development in humans and chimpanzees that are consistent with interspecific differences in lactation, diet, and immune function. Probing the phenotypic consequences of differential early-life gut microbial diversity in chimpanzees and other primates will illuminate the life history impacts of the hominid-microbiome partnership.

The Kibale Chimpanzee Project: Over thirty years of research, conservation, and change.

Long-term primate field research programs contribute to the protection of endangered primate species and their vanishing habitats by informing and fostering local and international conservation programs. The Kibale Chimpanzee Project (KCP) has studied the Kanyawara community of wild chimpanzees continuously since 1987, investigating a wide range of behavioral, ecological, and physiological questions. The study area includes the northwest boundary of Kibale National Park, Uganda, and has experienced habitat change driven by multiple causes, including forest regeneration, an increasingly warmer and wetter climate, and impacts from the neighboring human population. Here, we review the history of research on Kanyawara chimpanzees and examine how their demography, diet, and social behavior have changed over the last 30+ years. While Kanyawara chimpanzees were protected from the major threats of poaching and habitat loss, respiratory diseases of human origin were a major source of mortality. Many individuals were also injured by wire hunting snares. Nevertheless, the study community has grown modestly in size, individuals have become increasingly gregarious, and birth rates have increased. These results are likely attributable to improved habitat productivity that can be traced to decades-long efforts by wildlife authorities and the associated research and conservation programs in Kibale. Overall, research has contributed both to understanding interactions among nutritional ecology, social behavior, physiology, and health of an endangered species, and also to conservation activities in the Kibale community through direct interventions, positive economic impacts, and conservation education programs.

Social selectivity in aging wild chimpanzees.

Humans prioritize close, positive relationships during aging, and socioemotional selectivity theory proposes that this shift causally depends on capacities for thinking about personal future time horizons. To examine this theory, we tested for key elements of human social aging in longitudinal data on wild chimpanzees. Aging male chimpanzees have more mutual friendships characterized by high, equitable investment, whereas younger males have more one-sided relationships. Older males are more likely to be alone, but they also socialize more with important social partners. Further, males show a relative shift from more agonistic interactions to more positive, affiliative interactions over their life span. Our findings indicate that social selectivity can emerge in the absence of complex future-oriented cognition, and they provide an evolutionary context for patterns of social aging in humans.

Evaluating the impact of physical frailty during ageing in wild chimpanzees (Pan troglodytes schweinfurthii).

While declining physical performance is an expected consequence of ageing, human clinical research has placed increasing emphasis on physical frailty as a predictor of death and disability in the elderly. We examined non-invasive measures approximating frailty in a richly sampled longitudinal dataset on wild chimpanzees. Using urinary creatinine to assess lean body mass, we found moderate but significant declines in physical condition with age in both sexes. While older chimpanzees spent less of their day in the trees and feeding, they did not alter activity budgets with respect to travel or resting. There was little evidence that declining lean body mass had negative consequences independent of age. Old chimpanzees with poor lean body mass rested more often but did not otherwise differ in activity. Males, but not females, in poor condition were more likely to exhibit respiratory illness. Poor muscle mass was associated acutely with death in males, but it did not predict future mortality in either sex. While there may be some reasons to suspect biological differences in the susceptibility to frailty in chimpanzees versus humans, our data are consistent with recent reports from humans that lean, physically active individuals can successfully combat frailty. This article is part of the theme issue 'Evolution of the primate ageing process'.

Demography, life-history trade-offs, and the gastrointestinal virome of wild chimpanzees.

In humans, senescence increases susceptibility to viral infection. However, comparative data on viral infection in free-living non-human primates-even in our closest living relatives, chimpanzees and bonobos (Pan troglodytes and P. paniscus)-are relatively scarce, thereby constraining an evolutionary understanding of age-related patterns of viral infection. We investigated a population of wild eastern chimpanzees (P. t. schweinfurthii), using metagenomics to characterize viromes (full viral communities) in the faeces of 42 sexually mature chimpanzees (22 males, 20 females) from the Kanyawara and Ngogo communities of Kibale National Park, Uganda. We identified 12 viruses from at least four viral families possessing genomes of both single-stranded RNA and single-stranded DNA. Faecal viromes of both sexes varied with chimpanzee age, but viral richness increased with age only in males. This effect was largely due to three viruses, salivirus, porprismacovirus and chimpanzee stool-associated RNA virus (chisavirus), which occurred most frequently in samples from older males. This finding is consistent with the hypothesis that selection on males for early-life reproduction compromises investment in somatic maintenance, which has delayed consequences for health later in life, in this case reflected in viral infection and/or shedding. Faecal viromes are therefore useful for studying processes related to the divergent reproductive strategies of males and females, ageing, and sex differences in longevity. This article is part of the theme issue 'Evolution of the primate ageing process'.

Shifting sociality during primate ageing.

Humans exhibit major age-related shifts in social relationships along with changes in social and emotional psychological processes that underpin these behavioural shifts. Does social ageing in non-human primates follow similar patterns, and if so, what are the ultimate evolutionary consequences of these social shifts? Here we synthesize empirical evidence for shifts in social behaviour and underlying psychological processes across species. Focusing on three elements of social behaviour and cognition that are important for humans-propensities to engage with others, the positive versus negative valence of these interactions, and capabilities to influence others, we find evidence for wide variation in the trajectories of these characteristics across primates. Based on this, we identify potential modulators of the primate social ageing process, including social organization, sex and dominance status. Finally, we discuss how comparative research can contextualize human social ageing. This article is part of the theme issue 'Evolution of the primate ageing process'.

Urinary markers of oxidative stress respond to infection and late-life in wild chimpanzees.

Oxidative stress (OS) plays a marked role in aging and results from a variety of stressors, making it a powerful measure of health and a way to examine costs associated with life history investments within and across species. However, few urinary OS markers have been examined under field conditions, particularly in primates, and their utility to non-invasively monitor the costs of acute stressors versus the long-term damage associated with aging is poorly understood. In this study, we examined variation in 5 urinary markers of oxidative damage and protection under 5 validation paradigms for 37 wild, chimpanzees living in the Kibale National Park, Uganda. We used 924 urine samples to examine responses to acute immune challenge (respiratory illness or severe wounding), as well as mixed-longitudinal and intra-individual variation with age. DNA damage (8-OHdG) correlated positively with all other markers of damage (F-isoprostanes, MDA-TBARS, and neopterin) but did not correlate with protection (total antioxidant capacity). Within individuals, all markers of damage responded to at least one if not both types of acute infection. While OS is expected to increase with age, this was not generally true in chimpanzees. However, significant changes in oxidative damage were detected within past-prime individuals and those close to death. Our results indicate that OS can be measured using field-collected urine and integrates short- and long-term aspects of health. They further suggest that more data are needed from long-lived, wild animals to illuminate if common age-related increases in inflammation and OS damage are typical or recently aberrant in humans.