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.

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.

Wild chimpanzees exhibit humanlike aging of glucocorticoid regulation.

Cortisol, a key product of the stress response, has critical influences on degenerative aging in humans. In turn, cortisol production is affected by senescence of the hypothalamic-pituitary-adrenal (HPA) axis, leading to progressive dysregulation and increased cortisol exposure. These processes have been studied extensively in industrialized settings, but few comparative data are available from humans and closely related species living in natural environments, where stressors are very different. Here, we examine age-related changes in urinary cortisol in a 20-y longitudinal study of wild chimpanzees (n = 59 adults) in the Kanyawara community of Kibale National Park, Uganda. We tested for three key features of HPA aging identified in many human studies: increased average levels, a blunted diurnal rhythm, and enhanced response to stressors. Using linear mixed models, we found that aging was associated with a blunting of the diurnal rhythm and a significant linear increase in cortisol, even after controlling for changes in dominance rank. These effects did not differ by sex. Aging did not increase sensitivity to energetic stress or social status. Female chimpanzees experienced their highest levels of cortisol during cycling (versus lactation), and this effect increased with age. Male chimpanzees experienced their highest levels when exposed to sexually attractive females, but this effect was diminished by age. Our results indicate that chimpanzees share some key features of HPA aging with humans. These findings suggest that impairments of HPA regulation are intrinsic to the aging process in hominids and are side effects neither of extended human life span nor of atypical environments.

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.

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.

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.

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.

Wood and meat as complementary sources of sodium for Kanyawara chimpanzees (Pan troglodytes).

OBJECTIVES: Sodium, a vital micronutrient that is often in scarce supply for tropical herbivores, is sometimes found at high concentration in decaying wood. We tested two hypotheses for chimpanzees: first, that wood-eating facilitates acquisition of sodium; second, that wood-eating occurs in response to the low availability of sodium from other dietary sources. MATERIALS AND METHODS: We studied the behavior of more than 50 chimpanzees of all age-sex classes in the Kanyawara community of Kibale National Park, Uganda. We quantified the sodium content of dietary items, including wood samples from tree species that chimpanzees consumed or did not consume. To assess variation in sodium intake, we used 7 years of data on time spent feeding on plant foods, 18 months of data on rates of food intake by adult females, and 20 years of data on meat-eating. RESULTS: Major dietary sources of sodium were wood, fruits and meat. Chimpanzees consumed wood primarily from decaying trees of Neoboutonia macrocalyx (Euphorbiaceae), which had substantially higher sodium content than all other dietary items tested. Wood-eating was negatively correlated with fruit-eating. Females ate wood more often than males, while males had a greater probability of consuming meat at predation events. DISCUSSION: We propose that females ate wood more often than males because females had reduced access to meat, their preferred source of sodium. This hypothesis suggests that the need for sodium is a motivating reason for chimpanzees to consume both meat and wood.

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.

Human-like adrenal development in wild chimpanzees: A longitudinal study of urinary dehydroepiandrosterone-sulfate and cortisol.

The development of the adrenal cortex varies considerably across primates, being most conspicuous in humans, where a functional zona reticularis-the site of dehydroepiandrosterone-sulfate (DHEA/S) production-does not develop until middle childhood (5-8 years). Prior reports suggest that a human-like adrenarche, associated with a sharp prepubertal increase in DHEA/S, may only occur in the genus Pan. However, the timing and variability in adrenarche in chimpanzees remain poorly described, owing to the lack of longitudinal data, or data from wild populations. Here, we use urine samples from East African chimpanzees (Pan troglodytes schweinfurthii) collected over 20 years at Kanyawara in Kibale National Park, Uganda, to trace the developmental trajectories of DHEAS (n = 1,385 samples, 53 individuals) and cortisol (n = 12,726 samples, 68 individuals). We used generalized additive models (GAM) to investigate the relationship between age, sex, and hormone levels. Adrenarche began earlier in chimpanzees (~2-3 years) compared with what has been reported in humans (6-8 years) and, unlike humans, male and female chimpanzees did not differ significantly in the timing of adrenarche nor in DHEAS concentrations overall. Similar to what has been reported in humans, cortisol production decreased through early life, reaching a nadir around puberty (8-11 years), and a sex difference emerged with males exhibiting higher urinary cortisol levels compared with females by early adulthood (15-16 years). Our study establishes that wild chimpanzees exhibit a human-like pattern of cortisol production during development and corroborates prior reports from captive chimpanzees of a human-like adrenarche, accompanied by significant developmental increases in DHEAS. While the role of these developmental hormone shifts are as yet unclear, they have been implicated in stages of rapid behavioral development once thought unique to humans, especially in regard to explaining the divergence of female and male social behavior before pubertal increases in gonadal hormones.

Faster reproductive rates trade off against offspring growth in wild chimpanzees.

Life history theory predicts a trade-off between offspring quality and quantity. Among large-bodied mammals, prolonged lactation and infant dependence suggest particularly strong potential for a quality-quantity trade-off to exist. Humans are one of the only such species to have been examined, providing mixed evidence under a peculiar set of circumstances, including extensive nutritional provisioning by nonmothers and extrasomatic wealth transmission. Here, we examine trade-offs between reproductive rate and one aspect of offspring quality (body size) in wild chimpanzees (Pan troglodytes schweinfurthii), a species with long periods of infant dependence and little direct provisioning. Juvenile lean body mass, estimated using urinary creatinine excretion, was positively associated with the interval to the next sibling's birth. These effects persisted into adolescence and were not moderated by maternal identity. Maternal depletion could not explain poor offspring growth, as older mothers had larger offspring, and low maternal energy balance during lactation predicted larger, not smaller, juvenile size. Instead, our data suggest that offspring growth suffers when mothers wean early to invest in new reproductive efforts. These findings indicate that chimpanzee mothers with the resources to do so prioritize production of new offspring over prolonged investment in current offspring.

Lethal Respiratory Disease Associated with Human Rhinovirus C in Wild Chimpanzees, Uganda, 2013.

We describe a lethal respiratory outbreak among wild chimpanzees in Uganda in 2013 for which molecular and epidemiologic analyses implicate human rhinovirus C as the cause. Postmortem samples from an infant chimpanzee yielded near-complete genome sequences throughout the respiratory tract; other pathogens were absent. Epidemiologic modeling estimated the basic reproductive number (R0) for the epidemic as 1.83, consistent with the common cold in humans. Genotyping of 41 chimpanzees and examination of 24 published chimpanzee genomes from subspecies across Africa showed universal homozygosity for the cadherin-related family member 3 CDHR3-Y529 allele, which increases risk for rhinovirus C infection and asthma in human children. These results indicate that chimpanzees exhibit a species-wide genetic susceptibility to rhinovirus C and that this virus, heretofore considered a uniquely human pathogen, can cross primate species barriers and threatens wild apes. We advocate engineering interventions and prevention strategies for rhinovirus infections for both humans and wild apes.

The development of feeding behavior in wild chimpanzees (Pan troglodytes schweinfurthii).

OBJECTIVES: Primates have an extended period of juvenility before adulthood. Although dietary complexity plays a prominent role in hypotheses regarding the evolution of extended juvenility, the development of feeding behavior is still poorly understood. Indeed, few studies have investigated the timing and nature of feeding transitions in apes, including chimpanzees. We describe general patterns of feeding development in wild chimpanzees and evaluate predictions of the needing-to-learn hypothesis. MATERIALS AND METHODS: We analyzed 4 years of behavioral data (2010-2013) from 26 immature chimpanzees and 31 adult chimpanzees of the Kanyawara community in Kibale National Park, Uganda. Specifically, we examined milestones of nutritional independence (first consumption of solid food and cessation of suckling) as well as developmental changes in feeding time, diet composition, diet breadth, and ingestion rates. RESULTS: Chimpanzees first fed on solid food at 5.1 months and, on average, suckled until 4.8 years. Daily feeding time of immature individuals reached adult levels between 4 and 6 years, while diet composition showed minor changes with age. By juvenility (5-10 years), individuals had a complete adult diet breadth. Ingestion rates for five ripe fruit species remained below adult levels until juvenility but continued to show absolute increases into adolescence. DISCUSSION: Chimpanzees acquired adult-like patterns on all feeding measures by infancy or juvenility. These data are inconsistent with the needing-to-learn hypothesis; moreover, where delays exist, alternatives hypotheses make similar predictions but implicate physical constraints rather than learning as causal factors. We outline predictions for how future studies might distinguish between hypotheses for the evolution of extended juvenility.

Predation by female chimpanzees: Toward an understanding of sex differences in meat acquisition in the last common ancestor of Pan and Homo.

Among modern foraging societies, men hunt more than women, who mostly target relatively low-quality, reliable resources (i.e., plants). This difference has long been assumed to reflect human female reproductive constraints, particularly caring for and provisioning mates and offspring. Long-term studies of chimpanzees (Pan troglodytes) enable tests of hypotheses about the possible origins of human sex differences in hunting, prior to pair-bonding and regular provisioning. We studied two eastern chimpanzee communities (Kasekela, Mitumba) in Gombe, Tanzania and one (Kanyawara) in Kibale, Uganda. Relative to males, females had low hunting rates in all three communities, even where they encountered red colobus monkeys (the primary prey of chimpanzees) as often as males did. There was no evidence that clinging offspring hampered female hunting. Instead, consistent with the hypothesis that females should be more risk-averse than males, females at all three sites specialized in low-cost prey (terrestrial/sedentary prey at Gombe; black and white colobus monkeys at Kanyawara). Female dominance rank was positively correlated with red colobus hunting probability only at Kasekela, suggesting that those in good physical condition were less sensitive to the costs of possible failure. Finally, the potential for carcass appropriation by males deterred females at Kasekela (but not Kanyawara or Mitumba) from hunting in parties containing many adult males. Although chimpanzees are not direct analogs of the last common ancestor (LCA) of Pan and Homo, these results suggest that before the emergence of social obligations regarding sharing and provisioning, constraints on hunting by LCA females did not necessarily stem from maternal care. Instead, they suggest that a risk-averse foraging strategy and the potential for losing prey to males limited female predation on vertebrates. Sex differences in hunting behavior would likely have preceded the evolution of the sexual division of labor among modern humans.

First molar eruption, weaning, and life history in living wild chimpanzees.

Understanding dental development in chimpanzees, our closest living relatives, is of fundamental importance for reconstructing the evolution of human development. Most early hominin species are believed to show rapid ape-like patterns of development, implying that a prolonged modern human childhood evolved quite recently. However, chimpanzee developmental standards are uncertain because they have never been based on living wild individuals. Furthermore, although it is well established that first molar tooth emergence (movement into the mouth) is correlated with the scheduling of growth and reproduction across primates broadly, its precise relation to solid food consumption, nursing behavior, or maternal life history is unknown. To address these concerns we conducted a photographic study of subadult chimpanzees (Pan troglodytes schweinfurthii) in Kanyawara, Kibale National Park, Uganda. Five healthy infants emerged their lower first molars (M1s) by or before 3.3 y of age, nearly identical to captive chimpanzee mean ages (∼3.2 y, n = 53). First molar emergence in these chimpanzees does not directly or consistently predict the introduction of solid foods, resumption of maternal estrous cycling, cessation of nursing, or maternal interbirth intervals. Kanyawara chimpanzees showed adult patterns of solid food consumption by the time M1 reached functional occlusion, spent a greater amount of time on the nipple while M1 was erupting than in the preceding year, and continued to suckle during the following year. Estimates of M1 emergence age in australopiths are remarkably similar to the Kanyawara chimpanzees, and recent reconstructions of their life histories should be reconsidered in light of these findings.

Dental eruption in East African wild chimpanzees.

Knowledge of chimpanzee development has played an essential role in our understanding of the evolution of human ontogeny. However, recent studies of wild ape dentitions have cast doubt on the use of developmental standards derived from captive individuals. Others have called into question the use of deceased wild individuals to infer normative development. We conducted a high resolution photographic study of living known-age subadults in the Kanyawara community (Kibale National Park, Uganda) to generate a comprehensive three year record of dental eruption (including tooth emergence ages). These non-invasive data allow comparisons of captive and wild chimpanzees, establish accurate developmental standards for relatively healthy wild individuals, and facilitate direct assessments of primate-wide associations between dental development and life history. Emergence ages in the Kanyawara chimpanzees are very similar to living Gombe chimpanzees, and are broadly comparable to deceased Taï Forest chimpanzees. Early-emerging teeth such as the deciduous dentition and first molar (M1) appear during a time of maternal dependence, and are almost indistinguishable from captive chimpanzee emergence ages, while later forming teeth in the Kanyawara population emerge in the latter half of captive age ranges or beyond. Five juveniles whose lower M1s emerged by or before 3.3 years of age continued to nurse for a year or more beyond M1 emergence, and their mothers showed considerable variation in reproductive rates. The third molars of two adolescent females emerged several months to several years prior to the birth of their first offspring. Given that broad primate-wide relationships between molar emergence and life history do not necessarily hold within this population of chimpanzees, particularly for variables that are reported to be coincident with molar emergence, we suggest that further study is required in order to predict life history variables in hominins or hominoids.

Phylogenetic rate shifts in feeding time during the evolution of Homo.

Unique among animals, humans eat a diet rich in cooked and nonthermally processed food. The ancestors of modern humans who invented food processing (including cooking) gained critical advantages in survival and fitness through increased caloric intake. However, the time and manner in which food processing became biologically significant are uncertain. Here, we assess the inferred evolutionary consequences of food processing in the human lineage by applying a Bayesian phylogenetic outlier test to a comparative dataset of feeding time in humans and nonhuman primates. We find that modern humans spend an order of magnitude less time feeding than predicted by phylogeny and body mass (4.7% vs. predicted 48% of daily activity). This result suggests that a substantial evolutionary rate change in feeding time occurred along the human branch after the human-chimpanzee split. Along this same branch, Homo erectus shows a marked reduction in molar size that is followed by a gradual, although erratic, decline in H. sapiens. We show that reduction in molar size in early Homo (H. habilis and H. rudolfensis) is explicable by phylogeny and body size alone. By contrast, the change in molar size to H. erectus, H. neanderthalensis, and H. sapiens cannot be explained by the rate of craniodental and body size evolution. Together, our results indicate that the behaviorally driven adaptations of food processing (reduced feeding time and molar size) originated after the evolution of Homo but before or concurrent with the evolution of H. erectus, which was around 1.9 Mya.

Age-related reproductive effort in male chimpanzees: terminal investment or alternative tactics?

Because senescence impairs the ability of older males to compete successfully for mates, male reproductive strategies are expected to change with age. The terminal investment hypothesis proposes that older males, who could die soon, should take greater risks to obtain mating opportunities. Another possibility is that older males avoid such risks, adopting alternative reproductive tactics, such as increased affiliation with females, increased reliance on coalitions or sexual coercion to continue to compete with younger animals. We tested these hypotheses in wild chimpanzees, Pan troglodytes schweinfurthii, of the Kanyawara community, Kibale National Park, Uganda, where old males sire offspring at relatively high rates. Our data set included >40 000 incidents of male aggression and >5800 copulations observed between 2005 and 2017. We found that, even as their dominance status declined, old males maintained relatively high copulation rates, especially with established mothers. There was no evidence for terminal investment in response to ageing. Males became generally less aggressive as they aged. Neither did old males form affiliative bonds with females, nor use sexual coercion more frequently, as alternative reproductive tactics. Old males did, however, participate in coalitionary aggression at higher rates than young males and increased the proportion of their aggression that was coalitionary over time. Coalitions were positively associated with mating success, particularly for low- and middle-ranking males. These results support the hypothesis that ageing male chimpanzees use coalitions as an alternative reproductive tactic. The lack of evidence for terminal investment in response to ageing appears to reflect a broader mammalian pattern in which males who rely on fighting to secure mating opportunities avoid excessive risk taking as their formidability wanes.

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.

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.