Search

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’.

1. 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. 2. 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. 3. We used metagenomic methods to characterize viromes of individual chimpanzees while they were cycling, pregnant, and lactating. 4. 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. 5. Our results provide evidence of short-term physiological trade-offs between reproduction and infection, which is often hypothesized to constrain health in long-lived species.

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.

Old chimp friends As humans age, we prioritize established positive friendships over the new, but risky, socializing we do when we are young. It has been hypothesized that this shift may come as our own sense of mortality kicks in. Rosati et al. analyzed a rare, long-term dataset on social bonds among male chimpanzees and found a very similar focus on old and positive friendships (see the Perspective by Silk). Though there is evidence of some sense of time among nonhuman animals, it seems unlikely that they have the same impending sense of mortality that we experience; thus, these results suggest that a different, and deeper, mechanism may be at play. Science , this issue p. 473 ; see also p. 403

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.

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 four 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 non-mammalian 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 to 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 non-lethal viral infections cumulatively reflect or contribute to senescence in long-lived species such as chimpanzees.

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. Publisher PDF

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.

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 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.

We assessed the efficacy of traditional lectures versus online modules with respect to student learning in an undergraduate introductory biochemistry course in two successive years. In the first year, students had the options of attending live lectures by the course instructor and viewing online modules pre-recorded by the instructor, with the lectures and modules covering identical content; in addition, all students had a mandatory weekly application session. Utilizing pre-course and post-course tests as an instrument with which to measure learning during the course, we observed significantly increased learning (0.7 standard deviations) with attendance of traditional lectures and decreased learning with use of online modules, even after adjustment for grade point average. In the second year, the course had the same curriculum, but students were randomized to either live lectures or online modules for the first half of the course, crossing over to the other modality during the second half. With randomization, no difference in learning was observed between the two groups. Our study results suggest that although students who self-select to attend live lectures may be better primed to learn, there is no difference in learning with traditional lectures versus online modules. Furthermore, we found that students were better engaged when viewing online modules than when attending lectures in person. These findings suggest aspects of the lecture experience can be shifted to online modules in STEM courses without impacts on student learning so as to use classroom time more fully for application-based active learning interventions.

Is it possible to slow the rate of aging, or do biological constraints limit its plasticity? We test this ‘invariant rate of aging’ hypothesis with an unprecedented 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 aging 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 aging, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of aging hypothesis, implying biological constraints on how much the human rate of aging can be slowed.

Summary 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 , 4 , 5 , 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

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’.

Energy investment in reproduction is predicted to trade off against other necessary physiological functions like immunity, but it is unclear to what extent this impacts fitness in long-lived species. Among mammals, female primates, and especially apes, exhibit extensive periods of investment in each offspring. During this time, energy diverted to gestation and lactation is hypothesized to incur short and long-term deficits in maternal immunity and lead to accelerated ageing. We examined the relationship between reproduction and immunity, as measured by faecal parasite counts, in wild female chimpanzees ( Pan troglodytes schweinfurthii ) of Kibale National Park, Uganda. While we observed higher parasite shedding (counts of eggs, cysts and larvae) in pregnant chimpanzees relative to cycling females, parasites rapidly decreased during early lactation, the most energetically taxing phase of the reproductive cycle. Additionally, while our results indicate that parasite shedding increases with age, females with higher fertility for their age had lower faecal parasite counts. Such findings support the hypothesis that the relatively conservative rate of female reproduction in chimpanzees may be protective against the negative effects of reproductive effort on health. This article is part of the theme issue ‘Evolution of the primate ageing process’.

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.

Social mammals often live in groups in which a dominance hierarchy is an important determinant of access to mates. In addition to competing individually, males may form coalitions of two or more to attack or intimidate rivals. Coalition formation could be particularly advantageous for adolescent males by helping them compensate for their physical and social immaturity. However, adolescents may struggle to attract effective coalition partners because of these inadequacies. Here, we examine the behavior of maturing male chimpanzees to test whether coalitions are more frequent among more or less powerful individuals. Our longitudinal study followed 18 males (ages 5 through 25 years) and utilized 1517 coalitions across 12 years of observation of the Kanyawara chimpanzee community in Kibale National Park, Uganda. We found that rates of coalition formation increased across maturation and that this increase was independent of a rise in the overall use of aggression. Juveniles formed coalitions almost exclusively with their mothers, while adolescents partnered primarily with peers and adult males. When adolescents and adult males formed coalitions with each other, the adolescents were more likely to join the adults than vice versa. Finally, adolescents engaged in joint behavior with adult males more often in non-aggressive vocal displays than in aggressive coalitions. Taken together, our results suggest that adolescent males are largely unable to attract the most powerful coalition partners and that they “make the best of a bad job” by joining adult males in less competitive situations, when the risk of receiving aggression from opponents is lower. Adolescent males are at a disadvantage in competing for powerful allies, because they have less strength to contribute to a cooperative dyad. Even when a variety of possible coalition partners are present, the partner choices of higher-ranking males likely limit the number of remaining individuals that are available and willing to form coalitions with adolescents. Accordingly, we found that males sorted with closely ranked coalition partners down the hierarchy, leaving adolescents to form coalitions with partners of similar rank to themselves rather than high-ranking adult males. There was no evidence for rank sorting in joint vocal displays, however. Additionally, adolescents participated in more than twice as many joint vocal displays as coalitions. These data suggest that joint vocal displays represent a viable alternative to coalitions for adolescents attempting to integrate themselves into the adult male social world.

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.

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.

Facilities housing captive animals are full of staff who, every day, interact with the animals under their care. The expertise and familiarity of staff can be used to monitor animal welfare by means of questionnaires. It was the goal of our study to examine the association between chimpanzee (Pan troglodytes) welfare, happiness, and personality. To these ends we collected two waves of welfare and subjective well-being ratings of 18 chimpanzees housed at the Edinburgh Zoo and one set of ratings of 13 chimpanzees housed at Fundació Mona. Ratings were made on a welfare questionnaire that included 12 items related to stress, psychological stimulation, and behavioural indicators of negative and positive welfare states, and a 4-item subjective well-being questionnaire. In addition, ratings were made on the 54-item Hominoid Personality Questionnaire and an abbreviated version of this scale consisting of 37 antonym pairs. We used generalizability theory to test whether welfare ratings generalized across items, raters, chimpanzees, and time. We then assessed the validity of the welfare and subjective well-being questionnaires by examining their associations with behaviour. Finally, we tested whether the welfare and subjective well-being ratings were associated with personality. Welfare ratings generalized across items, raters, chimpanzees, and time. Principal components analysis and regularized exploratory factor analysis indicated that ten welfare items and all four subjective well-being items formed a single dimension (welfareSWB). LASSO regression found that lower welfareSWB was associated with regurgitation, coprophagy, urophagy, and decreased proximity to nearest neighbour. A linear model that adjusted for age, sex, and facility, indicated that higher Extraversion and lower Neuroticism were related to higher welfareSWB. Welfare ratings were reliable and associated with subjective well-being and personality, demonstrating that staff ratings are a valid and potentially valuable tool for chimpanzee welfare assessment.

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.

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. Adrenarffche 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.

Daily energy intake of adult female mammals is influenced by environmental conditions and physiological requirements, including reproduction. We examined the effects of fruit availability on macronutrient and metabolisable energy intake by adult female chimpanzees (Pan troglodytes schweinfurthii) of the Kanyawara community in Kibale National Park, Uganda from January 2014 through June 2015. Drupe fruits were abundant for four months, whereas the other fourteen months were dominated by fig fruits. The mean daily intake of food (dry matter) and metabolisable energy, did not differ between drupe-months and fig-months. However, foraging costs were higher during fig-months, as indicated by a 20% increase in feeding time. Furthermore, during drupe-months female chimpanzees ingested more water-soluble carbohydrates and lipids, and less available protein and neutral detergent fibre. Although metabolisable energy intake did not differ consistently between drupe-months and fig-months, they consumed more on days when ripe fruit dominated the diet than when leaves and pithy stems dominated the diet. Our data suggest that differences in diet quality between drupes and figs can have important effects on frugivore foraging, and that they influence net energy gain more by their effects on macronutrient composition or foraging cost than by their direct impact on energy intake.

In many group-living mammals, mothers may increase the reproductive success of their daughters even after they are nutritionally independent and fully grown [1]. However, whether such maternal effects exist for adult sons is largely unknown. Here we show that males have higher paternity success when their mother is living in the group at the time of the offspring’s conception in bonobos (N = 39 paternities from 4 groups) but not in chimpanzees (N = 263 paternities from 7 groups). These results are consistent with previous research showing a stronger role of mothers (and females more generally) in bonobo than chimpanzee societies. Postprint Postprint

Summary High-arm grooming is a form of chimpanzee grooming in which two individuals mutually groom while each raising one arm. Palm-to-palm clasping (PPC) is a distinct style of high-arm grooming in which the grooming partners clasp each other's raised palms. In wild communities, samples of at least 100 observed dyads grooming with raised hands showed PPC frequencies varying from 30% dyads grooming (Kanyawara, Kibale), and in a large free-ranging sanctuary group, the frequency reached >80% dyads (group 1, Chimfunshi) [1, 2]. Because between-community differences in frequency of PPC apparently result from social learning, are stable across generations, and last for at least 9 years, they are thought to be cultural, but the mechanism of transmission is unknown [2]. Here, we examine factors responsible for individual variation in PPC frequency within a single wild community. We found that in the Kanyawara community (Kibale, Uganda), adults of both sexes varied widely in their PPC frequency (from 50%) and did not converge on a central group tendency. However, frequencies of PPC were highly consistent within matrilines, indicating that individuals maintained lifelong fidelity to the grooming style of their mothers. Matrilineal inheritance of socially learned behaviors has previously been reported for tool use in chimpanzees [3] and in the vocal and feeding behavior of cetaceans [4, 5]. Our evidence indicates that matrilineal inheritance can be sufficiently strong in nonhuman primates to account for long-term differences in community traditions.

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.

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’.

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’.

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'.

Respiratory illnesses have caused significant mortality in African great ape populations. While much effort has been given to identifying the responsible pathogens, little is known about the factors that influence disease transmission or individual susceptibility. In the Kanyawara community of wild chimpanzees, respiratory illness has been the leading cause of mortality over 31 years, contributing to 27% of deaths. Deaths were common in all age groups except juveniles. Over 22 years of health observations, respiratory signs were rare among infants and most common among older adults of both sexes. Respiratory signs were also common among males during the transition to adulthood (ages 10–20 years), particularly among those of low rank. Respiratory signs peaked conspicuously in March, a pattern that we could not explain after modelling climatic factors, group sizes, diet or exposure to humans. Furthermore, rates of respiratory illness in the chimpanzees did not track seasonal rates of illness in the nearby village. Our data indicate that the epidemiology of chimpanzee respiratory illness warrants more investigation but clearly differs in important ways from humans. Findings on individual susceptibility patterns suggest that respiratory signs are a robust indicator for investigating immunocompetence in wild chimpanzees.

Among modern foraging societies, men hunt more than women, who mostly target relatively low-quality, reliable resources (i.e., plants and shellfish). 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.

Oxidative stress (OS) plays a central role in aging and results from a variety of stressors, making it a powerful measure of health and a way to examine phylogenetic variation in life history. However, few urinary OS markers have been examined under field conditions, particularly in primates, and their utility to non-invasively monitor acute vs. chronic conditions is poorly understood. In this study, we examined variation in 5 urinary markers of oxidative damage and protection under 5 validation paradigms in 37 wild, adult chimpanzees living in the Kibale National Park, Uganda. We used 925 urine samples to conduct both cross-sectional and within-individual analyses of responses to acute infection and variation with age. Markers of damage (8-OHdG, F-isoprostanes, MDA-TBARS, and neopterin) and total antioxidant capacity were generally positively correlated with one another. Within individuals, all markers responded to at least one if not both types of acute infection. Markers of damage also varied with age, particularly in individuals near death. Unlike in human and rodent tissues, DNA damage in urine decreased with age, both across and within individuals near death, suggesting a potential decline in DNA repair and/or metabolic rate during senescence. Our results suggest that OS can be measured using field-collected urine and may be useful for both short- and long-term indicators of health. Our results further confirm that using multiple markers and longitudinal sampling within individuals is the most productive approach for studies that seek to determine the role of OS in health and lifespan in long-lived organisms.

Unidirectional grooming is a low-cost behaviour for which the groomer is repaid via kin selection or reciprocity. Return benefits can come in the form of increased probability of being groomed or social benefits such as coalitionary support. By contrast, the reasons for mutual grooming, which occurs when two individuals simultaneously groom each other, are not understood. In this study, we test three hypotheses regarding the function of mutual grooming among wild male chimpanzees, using 16 years of data. The social bonding hypothesis posits that mutual grooming promotes a return benefit by serving to strengthen and maintain social bonds, whereas the immediate investment hypothesis states that it functions as a signal to indicate willingness to invest in (continue) the grooming bout. The switching hypothesis states that mutual grooming results from overlap created when the direction of the grooming interaction is switched. The social bonding hypothesis was not supported: measures of association were not correlated with the probability of mutual grooming. We also found no support for the switching hypothesis, as mutual grooming was equally likely to occur without a switch in the direction of grooming as when a switch occurred. The immediate investment hypothesis was supported by our finding that bouts with mutual grooming (1) were longer, (2) contained a more equitable distribution of unidirectional grooming and (3) had more unidirectional grooming switches than bouts without mutual grooming. We conclude that male chimpanzees use mutual grooming to obtain short-term benefits in the form of prolonging a grooming bout, and suggest that mutual grooming thus represents a form of overlapping parcelling.

Although male–female relationships can offer a number of advantages such as protection or social support, they are poorly studied among primates compared to same-sex relationships. We used 12 yr of data from the Kanyawara chimpanzee community to compare three independent measures of association (party association, 5m association, and grooming) among all adult dyads. Party association exhibited by male–female dyads was of intermediate strength between strong male–male and weak female–female association. Male–female dyads were less likely to be within 5m of one another and to groom as male–male dyads, but equally likely to be within 5m and more likely to groom as female–female dyads. Variation in male–female association strength was not related to male rank but was affected by female ranging patterns and female reproductive states. Females with core areas in the center of the home range were more likely to be in parties with males but did not show higher spatial proximity or grooming indices compared to females ranging in the periphery. Party association and 5m indices were higher for dyads of males and estrous females compared to those with anestrous females. These results indicate that male–female dyads are likely to associate with one another more often than female–female dyads because of overlapping ranging patterns and short-term changes in female reproductive state. We conclude that male and female chimpanzees do not exhibit proximity and grooming patterns indicative of strong affiliative bonds. This study also highlights the importance of using multiple independent measures of bond strength in studies of primate social dynamics.

Animals communicate using a vast array of different signals in different modalities. For chimpanzees, vocalizations, gestures and facial expressions are all important forms of communication, yet these signals have rarely been studied together holistically. The current study aimed to provide the first comprehensive repertoire of flexibly combined (‘free’) multimodal (MM) signals, and assess individual and contextual factors influencing production of, and responses to, unimodal (UM) and MM signals in wild chimpanzees. In total, 48 different free MM signals were produced. MM signals were produced at a significantly lower rate than UM signals, but 22 of 26 focal animals were observed to produce free MM signals. The relative production rates of different types of UM and MM signals differed significantly between the behavioural contexts investigated, showing flexible use of signals across contexts. In contrast, individual factors such as age, sex or rank of signaller did not appear to influence the type of signal produced or the likelihood of eliciting a response. Finally, we compared recipient responses to free MM grunt-gesture signals and matched UM component signals and found that these MM signals were more likely to elicit a response than a grunt alone, but were as likely to elicit a response as the gesture alone. The overall findings point to a widespread capacity for wild chimpanzees to flexibly combine signals from different modalities and highlight the importance of adopting a multimodal approach to studying communication.

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.

Uganda’s Kibale National Park contains a particularly diverse primate population, including about 1400 chimpanzees (Pan troglodytes). It is threatened by poaching and illegal deforestation, both of which are promoted by the extreme poverty, exponential population growth, and low educational achievements of local people. This poster describes a multifaceted approach to conservation taken by the Kibale Chimpanzee Project. We highlight its within-forest organization (Kibale Snare Removal Project, KSRP) and its partner NGO working with 10,000 children in the surrounding communities (The Kasiisi Project). Within the Park, KSRP rangers interact closely with the Ugandan Wildlife Authority to monitor illegal activity. In 2013 KSRP rangers reported over 1400 incidents of illegal activity in the forest and removed over 700 snares. Outside the Park, the Kasiisi Project focuses on changing attitudes and behavior through combining conservation education, community development, and higher standards in 14 primary schools. The Kasiisi Project’s philosophy is to meet people’s needs (better education, less reliance on forest resources) while providing the information, skills and motivation to reduce environmental degradation. KSRP rangers link within-forest and community activities by participating in school conservation education. Since we began, students in Kasiisi-partnered schools have achieved exceptionally high National Exam scores and show increased positive feelings towards chimpanzees and the Park. Our results suggest that because the rising human population threatens all Ugandan forests, within-forest and community activity should be combined wherever possible in order to maximize the effectiveness of conservation efforts.

The entodiniomorphid ciliate Troglodytella abrassarti is a colonic mutualist of great apes. Its host specificity makes it a suitable model for studies of primate evolution. We explored molecular diversity of T. abrassarti with regard to large geographical distribution and taxonomic diversity of its most common host, the chimpanzee. We found a very low diversification of T. abrassarti in chimpanzees across Africa. Distribution of two types of T. abrassarti supports evolutionary separation of the Western chimpanzee, P. t. verus, from populations in Central and East Africa. Type I T. abrassarti is probably a derived form, which corresponds with the Central African origin of chimpanzees and a founder event leading to P. t. verus. Exclusivity of the respective types of T. abrassarti to Western and Central/Eastern chimpanzees corroborates the difference found between an introduced population of presumed Western chimpanzees on Rubondo Island and an autochthonous population in mainland Tanzania. The identity of T. abrassarti from Nigerian P. t. ellioti and Central African chimpanzees suggests their close evolutionary relationship. Although this contrasts with published mtDNA data, it corroborates current opinion on the exclusive position of P. t. verus within the chimpanzee phylogeny. The type of T. abrassarti occurring in Central and East African common chimpanzee was confirmed also in bonobos. This may point to the presence of an ancestral Type II found throughout the Lower Guinean rainforest dating back to the common Pan ancestor. Alternatively, the molecular uniformity of T. abrassarti may imply a historical overlap of the species' distribution ranges.

Summary We thank van Leeuwen et al. [1] for their response to our finding that matrilineal relationships strongly influence the style of high-arm grooming in wild chimpanzees of the Kanyawara community. We agree with them that grooming styles could be transmitted by different mechanisms in different contexts, and we appreciate their effort to assess whether the transmission of grooming styles within two captive groups in Chimfunshi accords with our result.

Body mass is thought to influence diversification rates, but previous studies have produced ambiguous results. We investigated patterns of diversification across 100 trees obtained from a new Bayesian inference of primate phylogeny that sampled trees in proportion to their posterior probabilities. First, we used simulations to assess the validity of previous studies that used linear models to investigate the links between IUCN Red List status and body mass. These analyses support the use of linear models for ordinal ranked data on threat status, and phylogenetic generalized linear models revealed a significant positive correlation between current extinction risk and body mass across our tree block. We then investigated historical patterns of speciation and extinction rates using a recently developed maximum-likelihood method. Specifically, we predicted that body mass correlates positively with extinction rate because larger bodied organisms reproduce more slowly, and body mass correlates negatively with speciation rate because smaller bodied organisms are better able to partition niche space. We failed to find evidence that extinction rates covary with body mass across primate phylogeny. Similarly, the speciation rate was generally unrelated to body mass, except in some tests that indicated an increase in the speciation rate with increasing body mass. Importantly, we discovered that our data violated a key assumption of sample randomness with respect to body mass. After correcting for this bias, we found no association between diversification rates and mass.

Feeding systems and behaviors must evolve to satisfy the metabolic needs of organisms. This includes modifications to feeding systems as body size and metabolic needs change. Using our own data and data from the literature, we examine how size-related changes in metabolic needs are met by size-related changes in daily feeding time, chew cycle duration, volume of food processed per chew, and daily food volume intake in primates. Increases in chew cycle duration with body mass in haplorhine primates are described by a simple power function (cycle time α body mass 0.181 ). Daily feeding time increases with body mass when analyzed using raw data from the “tips” of the primate phylogenetic tree, but not when using phylogenetically independent contrasts. Whether or not daily feeding time remains constant or increases with body mass, isometry of ingested bite size and the slow rate of increase in chew cycle time with body size combine to allow daily ingested food volume to scale faster than predicted by metabolic rate. This positive allometry of daily ingested food volume may compensate for negative allometry of nutrient concentration in primate foods. Food material properties such as toughness and hardness have little impact on scaling of chew cycle durations, sequence durations, or numbers of chews in a sequence. Size-related changes in food processing abilities appear to accommodate size-related changes in food material properties, and primates may alter ingested bite sizes in order to minimize the impacts of food material properties on temporal variables such as chew cycle duration and chew sequence duration.

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 Tai 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.

If primates were capable of vocalizing to inform a receiver about an external entity, it would represent an important element of continuity with human language. We tested experimentally whether chimpanzee rough grunts, which function to refer to food, are produced selectively, indicating voluntary control, and whether they are directed at specific individuals. These are prerequisites for a system capable of actively informing others about external events. We conducted a field playback experiment in which we presented silently feeding male chimpanzees, Pan troglodytes, with arrival pant hoots of a familiar group member. We found that subjects were significantly more likely to respond with food calls to the simulated arrival of an individual with whom the caller had a high rather than low level of friendship and where there was a large rather than small positive dominance rank difference between the individuals (i.e. caller was lower ranking). We concluded that chimpanzee food calls are not simply reflexive responses to food, but can be selectively directed at socially important individuals. Our findings are thus inconsistent with traditional views of primate vocalizations as inflexibly and indiscriminately produced. Instead, our results indicate that great apes can produce semantically meaningful calls in a highly selective, recipient-directed manner. Further research is needed to test whether chimpanzees use this flexible system to inform ignorant individuals about food, but the prerequisites to support this type of communication seem to be present.

BBSRC-funded, but difficult to identify the specific grant. Determining the intentionality of primate communication is critical to understanding the evolution of human language. Although intentional signalling has been claimed for some great ape gestural signals, comparable evidence is currently lacking for their vocal signals. We presented wild chimpanzees with a python model and found that two of three alarm call types exhibited characteristics previously used to argue for intentionality in gestural communication. These alarm calls were: (i) socially directed and given to the arrival of friends, (ii) associated with visual monitoring of the audience and gaze alternations, and (iii) goal directed, as calling only stopped when recipients were safe from the predator. Our results demonstrate that certain vocalisations of our closest living relatives qualify as intentional signals, in a directly comparable way to many great ape gestures. We conclude that our results undermine a central argument of gestural theories of language evolution and instead support a multimodal origin of human language. Publisher PDF

Vocal interactions, such as call exchanges or chorusing, are common behaviours in many animal species and their function has often been attributed to social bonding. However, few studies have investigated the effectiveness of vocalizations as bonding signals in comparison to other affiliative behaviours. We tested the hypothesis that male chimpanzee, Pan troglodytes schweinfurthii, pant hoot chorusing, a common behaviour in these primates, is a reliable but also flexible signal of affiliative relationships. The results of our study, conducted on the Kanyawara community of chimpanzees in Uganda, show that males were more likely to join in with the pant hoot of preferred long-term social partners to form a chorus. This supports the hypothesis that this behaviour is a good indicator of strong or long-term social bonds between male chimpanzees. However, our results also show that pant hoot chorusing reliably reflects short-term affiliations between males. For instance, male dyads were more likely to be involved in affiliative behaviours, such as reciprocated grooming, joint nonvocal displays and coalitions, on days when they chorused together, compared to days when they did not. This pattern applied to both preferred and neutral social partners. Moreover, on a short-term basis chorusing was a better indicator of other affiliative behaviours than grooming. We suggest that in male chimpanzees pant hoot choruses are efficient signals of short-term affiliative relationships. We conclude that potentially low-cost bonding behaviours such as coordinated vocal displays might be especially adaptive in highly fluid fission–fusion societies where grouping patterns are often unpredictable.