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.

The evolution and changing ecology of the African hominid oral microbiome.

The oral microbiome plays key roles in human biology, health, and disease, but little is known about the global diversity, variation, or evolution of this microbial community. To better understand the evolution and changing ecology of the human oral microbiome, we analyzed 124 dental biofilm metagenomes from humans, including Neanderthals and Late Pleistocene to present-day modern humans, chimpanzees, and gorillas, as well as New World howler monkeys for comparison. We find that a core microbiome of primarily biofilm structural taxa has been maintained throughout African hominid evolution, and these microbial groups are also shared with howler monkeys, suggesting that they have been important oral members since before the catarrhine-platyrrhine split ca. 40 Mya. However, community structure and individual microbial phylogenies do not closely reflect host relationships, and the dental biofilms of Homo and chimpanzees are distinguished by major taxonomic and functional differences. Reconstructing oral metagenomes from up to 100 thousand years ago, we show that the microbial profiles of both Neanderthals and modern humans are highly similar, sharing functional adaptations in nutrient metabolism. These include an apparent Homo-specific acquisition of salivary amylase-binding capability by oral streptococci, suggesting microbial coadaptation with host diet. We additionally find evidence of shared genetic diversity in the oral bacteria of Neanderthal and Upper Paleolithic modern humans that is not observed in later modern human populations. Differences in the oral microbiomes of African hominids provide insights into human evolution, the ancestral state of the human microbiome, and a temporal framework for understanding microbial health and disease.

Language likely promoted peace before 100,000 ya.

Based on evidence of selection against alpha-male behavior in the earliest Homo sapiens, I suggest that by 300,000 ya (years ago) language would have been sufficiently sophisticated to contribute to peacemaking between groups. Language also influenced the social landscape of peace and war, and groups' ability to form coalitions.

Associations between faecal chemical pollutants and hormones in primates inhabiting Kibale National Park, Uganda.

While anthropogenic pollutants are known to be a threat to primates, our understanding of exposure to pollutants in situ and their sub-lethal effects is still limited. We used non-invasive biomonitoring to examine associations between faecal concentrations of 97 chemical pollutants and faecal hormone metabolites of cortisol and oestradiol in four primate species inhabiting Kibale National Park, Uganda (chimpanzees-Pan troglodytes, olive baboons-Papio anubis, red colobus-Piliocolobus tephrosceles and red-tailed monkeys-Cercopithecus ascanius). Across all species (n = 71 samples), results demonstrated positive associations of organochlorine pesticides (OCPs) (ß = 0.143, p = 0.020) and organophosphate esters (ß = 0.112, p = 0.003) with cortisol in adult females. Additionally, we observed positive associations of OCPs (ß = 0.192, p = 0.013) and brominated flame retardants (ß = 0.176, p = 0.004) with cortisol in juveniles. Results suggest that cumulative pesticides and flame retardants are disruptive to endocrine function in these populations, which could have implications for development, metabolism and reproduction. Our study further demonstrates that faeces can be an important, non-invasive matrix for examining pollutant-hormone associations in wild primates and other critical wildlife populations.

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.

Females undergo selection too.

Extending Campbell's (1999) staying alive theory (SAT) beyond aggression, we reviewed evidence that females are more self-protective than males. Many commentators provided additional supporting data. Sex differences in life-history adaptations, in the optimal relation between survival and reproduction, and in the mechanisms underlying trade-offs involved with self-protection remain important topics with numerous opportunities for improved understanding.

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.

Nutritional geometry of female chimpanzees (Pan troglodytes).

Primate foraging is influenced by the spatial and temporal distribution of foods, which may facilitate or constrain optimal nutrient intakes. Chimpanzees are frugivorous primates that mainly subsist on ripe fruit that is typically low in available protein (AP) and high in easily digestible carbohydrates. Because chimpanzees prefer ripe fruit and often eat it in large quantities compared with other foods, we hypothesized that protein intake would be tightly regulated while non-protein energy (NPE) would vary with fruit intake. To test this hypothesis, we conducted all-day follows on female chimpanzees, recorded all types of food consumed (i.e., drupes, figs, and non-fruit foods), estimated the nutritional contributions of these foods to daily NPE and AP intake and investigated how the ratio of NPE to AP varied due to changes in the types of foods consumed. Although the proportions of drupes, figs, and non-fruit foods varied in their diets, female chimpanzees maintained a relatively stable intake of AP while intake of NPE varied depending on the daily diet, demonstrating that like other frugivorous primates studied to date, chimpanzees prioritize protein. The mean daily ratio of NPE to AP was 7:1, which is similar to that of other frugivorous primates studied. Our results support the hypothesis that frugivorous animals may generally prioritize AP, while maximizing NPE intake within that constraint, and could shed light on aspects of human dietary evolution.

Two types of aggression in human evolution.

Two major types of aggression, proactive and reactive, are associated with contrasting expression, eliciting factors, neural pathways, development, and function. The distinction is useful for understanding the nature and evolution of human aggression. Compared with many primates, humans have a high propensity for proactive aggression, a trait shared with chimpanzees but not bonobos. By contrast, humans have a low propensity for reactive aggression compared with chimpanzees, and in this respect humans are more bonobo-like. The bimodal classification of human aggression helps solve two important puzzles. First, a long-standing debate about the significance of aggression in human nature is misconceived, because both positions are partly correct. The Hobbes-Huxley position rightly recognizes the high potential for proactive violence, while the Rousseau-Kropotkin position correctly notes the low frequency of reactive aggression. Second, the occurrence of two major types of human aggression solves the execution paradox, concerned with the hypothesized effects of capital punishment on self-domestication in the Pleistocene. The puzzle is that the propensity for aggressive behavior was supposedly reduced as a result of being selected against by capital punishment, but capital punishment is itself an aggressive behavior. Since the aggression used by executioners is proactive, the execution paradox is solved to the extent that the aggressive behavior of which victims were accused was frequently reactive, as has been reported. Both types of killing are important in humans, although proactive killing appears to be typically more frequent in war. The biology of proactive aggression is less well known and merits increased attention.

Self-protection as an adaptive female strategy.

Many male traits are well explained by sexual selection theory as adaptations to mating competition and mate choice, whereas no unifying theory explains traits expressed more in females. Anne Campbell's "staying alive" theory proposed that human females produce stronger self-protective reactions than males to aggressive threats because self-protection tends to have higher fitness value for females than males. We examined whether Campbell's theory has more general applicability by considering whether human females respond with greater self-protectiveness than males to other threats beyond aggression. We searched the literature for physiological, behavioral, and emotional responses to major physical and social threats, and found consistent support for females' responding with greater self-protectiveness than males. Females mount stronger immune responses to many pathogens; experience a lower threshold to detect, and lesser tolerance of, pain; awaken more frequently at night; express greater concern about physically dangerous stimuli; exert more effort to avoid social conflicts; exhibit a personality style more focused on life's dangers; react to threats with greater fear, disgust, and sadness; and develop more threat-based clinical conditions than males. Our findings suggest that in relation to threat, human females have relatively heightened protective reactions compared to males. The pervasiveness of this result across multiple domains suggests that general mechanisms might exist underlying females' unique adaptations. An understanding of such processes would enhance knowledge of female health and well-being.

Sexual dimorphism in chimpanzee (Pan troglodytes schweinfurthii) and human age-specific fertility.

Across vertebrates, species with intense male mating competition and high levels of sexual dimorphism in body size generally exhibit dimorphism in age-specific fertility. Compared with females, males show later ages at first reproduction and earlier reproductive senescence because they take longer to attain adult body size and musculature, and maintain peak condition for a limited time. This normally yields a shorter male duration of effective breeding, but this reduction might be attenuated in species that frequently use coalitionary aggression. Here, we present comparative genetic and demographic data on chimpanzees from three long-term study communities (Kanyawara: Kibale National Park, Uganda; Mitumba and Kasekela: Gombe National Park, Tanzania), comprising 581 male risk years and 112 infants, to characterize male age-specific fertility. For comparison, we update estimates from female chimpanzees in the same sites and append a sample of human foragers (the Tanzanian Hadza). Consistent with the idea that aggressive mating competition favors youth, chimpanzee males attained a higher maximum fertility than females, followed by a steeper decline with age. Males did not show a delay in reproduction compared with females, however, as adolescents in both sites successfully reproduced by targeting young, subfecund females, who were less attractive to adults. Gombe males showed earlier reproductive senescence and a shorter duration of effective breeding than Gombe females. By contrast, older males in Kanyawara generally continued to reproduce, apparently by forming coalitions with the alpha. Hadza foragers showed a distinct pattern of sexual dimorphism in age-specific fertility as, compared with women, men gained conceptions later but continued reproducing longer. In sum, both humans and chimpanzees showed sexual dimorphism in age-specific fertility that deviated from predictions drawn from primates with more extreme body size dimorphism, suggesting altered dynamics of male-male competition in the two lineages. In both species, coalitions appear important for extending male reproductive careers.

Feces are Effective Biological Samples for Measuring Pesticides and Flame Retardants in Primates.

The habitats of wild primates are increasingly threatened by surrounding anthropogenic pressures, but little is known about primate exposure to frequently used chemicals. We applied a novel method to simultaneously measure 21 legacy pesticides (OCPs), 29 current use pesticides (CUPs), 47 halogenated flame retardants (HFRs), and 19 organophosphate flame retardants in feces from baboons in the U.S.A., howler monkeys in Costa Rica, and baboons, chimpanzees, red-tailed monkeys, and red colobus in Uganda. The most abundant chemicals were α-hexachlorocyclohexane (α-HCH), ß-hexachlorocyclohexane (ß-HCH), and hexachlorobenzene among OCPs across all sites, chlorpyrifos among CUPs in Costa Rica and Indiana, decabromodiphenylethane (DBDPE) in Costa Rica and Indiana and 2, 2', 4, 4'-tetrabromodiphenyl ether (BDE-47) in Uganda as HFRs, and tris(2-butoxyethyl) phosphate (TBOEP) as OPFRs across all sites. The detected chemical concentrations were generally higher in red-tailed monkeys and red colobus than in chimpanzees and baboons. Our methods can be used to examine the threat of chemical pollutants to wildlife, which is critical for endangered species where only noninvasive methods can be used.

Lethal aggression in Pan is better explained by adaptive strategies than human impacts.

Observations of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) provide valuable comparative data for understanding the significance of conspecific killing. Two kinds of hypothesis have been proposed. Lethal violence is sometimes concluded to be the result of adaptive strategies, such that killers ultimately gain fitness benefits by increasing their access to resources such as food or mates. Alternatively, it could be a non-adaptive result of human impacts, such as habitat change or food provisioning. To discriminate between these hypotheses we compiled information from 18 chimpanzee communities and 4 bonobo communities studied over five decades. Our data include 152 killings (n = 58 observed, 41 inferred, and 53 suspected killings) by chimpanzees in 15 communities and one suspected killing by bonobos. We found that males were the most frequent attackers (92% of participants) and victims (73%); most killings (66%) involved intercommunity attacks; and attackers greatly outnumbered their victims (median 8:1 ratio). Variation in killing rates was unrelated to measures of human impacts. Our results are compatible with previously proposed adaptive explanations for killing by chimpanzees, whereas the human impact hypothesis is not supported.

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.