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.

The development of affiliative and coercive reproductive tactics in male chimpanzees.

Like many animals, adult male chimpanzees often compete for a limited number of mates. They fight other males as they strive for status that confers reproductive benefits and use aggression to coerce females to mate with them. Nevertheless, small-bodied, socially immature adolescent male chimpanzees, who cannot compete with older males for status nor intimidate females, father offspring. We investigated how they do so through a study of adolescent and young adult males at Ngogo in Kibale National Park, Uganda. Adolescent males mated with nulliparous females and reproduced primarily with these first-time mothers, who are not preferred as mating partners by older males. Two other factors, affiliation and aggression, also influenced mating success. Specifically, the strength of affiliative bonds that males formed with females and the amount of aggression males directed toward females predicted male mating success. The effect of male aggression toward females on mating success increased as males aged, especially when they directed it toward females with whom they shared affiliative bonds. These results mirror sexual coercion in humans, which occurs most often between males and females involved in close, affiliative relationships.

A chimpanzee enamel-diet δ13C enrichment factor and a refined enamel sampling strategy: Implications for dietary reconstructions.

Reconstructing diets from stable carbon isotopic signals in enamel bioapatite requires the application of a δ13C enamel-diet enrichment factor, or the isotopic offset between diet and enamel, which has not been empirically determined for any primate. In this study, an enamel-diet enrichment factor (ε∗enamel-diet) of 11.8 ± 0.3‰ is calculated for chimpanzees (Pan troglodytes) at Ngogo in Kibale National Park, Uganda, based on a comprehensive isotopic assessment of previously analyzed dietary plant data and new isotopic analyses of enamel apatite. Different enamel sampling methods are evaluated to determine the potential influence of weaning on isotopic enamel values and dietary interpretations. The new chimpanzee enrichment factor and a sampling strategy that excludes teeth that formed before weaning completion are applied to all known chimpanzee δ13Cenamel data, either previously published or newly derived in this study, resulting in a dietary range of almost 6‰ across all chimpanzees sampled. This new chimpanzee enamel-diet enrichment factor is then used to reassess dietary reconstructions of 12 fossil hominin species whose isotopic enamel signatures have been determined. Results reveal hominin diets that are isotopically more positive than previously reconstructed, highlighting the widespread contribution of 13C-enriched C4/crassulacean acid metabolism (CAM) resources in fossil hominin diets and emphasizing the broad use of these resources during human evolution. These findings stress the importance of ascertaining and employing an appropriate enrichment factor for dietary reconstructions of specific taxa as well as standardizing the sampling protocol for tooth enamel in isotopic paleodietary reconstructions.

My life among the apes.

I have spent over 40 years studying the behavior of our closest living relatives, the apes. In this paper, I review my research on the spacing, mating, and vocal behavior of gibbons and orangutans (Pongo pygmaeus) and the vocal and social behavior of chimpanzees (Pan troglodytes). I devote special attention to results derived from a 25-year-long study of a remarkable and extraordinarily large group of chimpanzees that has recently fissioned at Ngogo in Kibale National Park, Uganda. I conclude with some advice for the next generation of field primatologists.

Adolescent and young adult male chimpanzees form affiliative, yet aggressive, relationships with females.

Primates frequently form affiliative relationships that have important fitness consequences. Affiliative relationships between unrelated males and females are ubiquitous in humans but are not widely reported in humans' closest living relatives, chimpanzees (Pan troglodytes). Instead, adult male chimpanzees are extremely aggressive to females, using the aggression to coerce females to mate with them. Adolescent male chimpanzees are physically and socially immature and unable to use aggression toward females in the same way as adult males. Instead, adolescent males might build affiliative relationships with females as an alternative tactic to increase their chances of mating and reproducing. To investigate this possibility, we recorded social interactions between 20 adolescent and 10 young adult males and 78 adult female chimpanzees over 2 years at Ngogo in Kibale National Park, Uganda. Analyses using grooming and proximity as assays revealed that adolescent and young adult males formed differentiated, affiliative relationships with females. These relationships were as strong as the bonds young males formed with maternal kin and unrelated males and increased in strength and number as males aged and started to dominate females. Male-female relationships extended outside the immediate context of mating. Although males affiliated slightly more often with females when they were cycling, they also did so when females were pregnant and nursing young infants. Males and females who formed bonds reassured each other, looked back and waited for each other while traveling, and groomed more equitably than other male-female pairs, even after the time they spent together in association and the female's reproductive state were taken into account. Despite the affiliative nature of these relationships, adolescent and young adult males selectively targeted their female partners for aggression. These findings provide new insights into the evolution of social bonds between human females and males, which can involve both affiliation and coercive violence.

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.

Long-term trends in fruit production in a tropical forest at Ngogo, Kibale National Park, Uganda.

Fruit production in tropical forests varies considerably in space and time, with important implications for frugivorous consumers. Characterizing temporal variation in forest productivity is thus critical for understanding adaptations of tropical forest frugivores, yet long-term phenology data from the tropics, in particular from African forests, are still scarce. Similarly, as the abiotic factors driving phenology in the tropics are predicted to change with a warming climate, studies documenting the relationship between climatic variables and fruit production are increasingly important. Here we present data from 19 years of monitoring the phenology of 20 tree species at Ngogo in Kibale National Park, Uganda. Our aims were to characterize short- and long-term trends in productivity and to understand the abiotic factors driving temporal variability in fruit production. Short-term (month-to-month) variability in fruiting was relatively low at Ngogo, and overall fruit production increased significantly through the first half of the study. Among the abiotic variables we expected to influence phenology patterns (including rainfall, solar irradiance, and average temperature), only average temperature was a significant predictor of monthly fruit production. We discuss these findings as they relate to the resource base of the frugivorous vertebrate community inhabiting Ngogo.

Adolescent male chimpanzees (Pan troglodytes) form social bonds with their brothers and others during the transition to adulthood.

Social relationships play an important role in animal behavior. Bonds with kin provide indirect fitness benefits, and those with nonkin may furnish direct benefits. Adult male chimpanzees (Pan troglodytes) exhibit social bonds with maternal brothers as well as unrelated adult males, facilitating cooperative behavior, but it is unclear when these bonds develop. Prior studies suggest that social bonds emerge during adolescence. Alternatively, bonds may develop during adulthood when male chimpanzees can gain fitness benefits through alliances used to compete for dominance status. To investigate these possibilities and to determine who formed bonds, we studied the social relationships of adolescent and young adult male chimpanzees (N = 18) at Ngogo in Kibale National Park, Uganda. Adolescent male chimpanzees displayed social bonds with other males, and they did so as often as did young adult males. Adolescent and young adult males frequently joined subgroups with old males. They spent time in proximity to and grooming with old males, although they also did so with their age peers. Controlling for age and age difference, males formed strong association and proximity relationships with their maternal brothers and grooming relationships with their fathers. Grooming bonds between chimpanzee fathers and their adolescent and young adult sons have not been documented before and are unexpected because female chimpanzees mate with multiple males. How fathers recognize their sons and vice versa remains unclear but may be due to familiarity created by relationships earlier in development.

Group augmentation, collective action, and territorial boundary patrols by male chimpanzees.

How can collective action evolve when individuals benefit from cooperation regardless of whether they pay its participation costs? According to one influential perspective, collective action problems are common, especially when groups are large, but may be solved when individuals who have more to gain from the collective good or can produce it at low costs provide it to others as a byproduct. Several results from a 20-y study of one of the most striking examples of collective action in nonhuman animals, territorial boundary patrolling by male chimpanzees, are consistent with these ideas. Individuals were more likely to patrol when (i) they had more to gain because they had many offspring in the group; (ii) they incurred relatively low costs because of their high dominance rank and superior physical condition; and (iii) the group size was relatively small. However, several other findings were better explained by group augmentation theory, which proposes that individuals should bear the short-term costs of collective action even when they have little to gain immediately if such action leads to increases in group size and long-term increases in reproductive success. In support of this theory, (i) individual patrolling effort was higher and less variable than participation in intergroup aggression in other primate species; (ii) males often patrolled when they had no offspring or maternal relatives in the group; and (iii) the aggregate patrolling effort of the group did not decrease with group size. We propose that group augmentation theory deserves more consideration in research on collective action.

Wild Chimpanzees Show a Decrease in Pant Grunting over Their First 6 Years of Life.

Data from a large cross-sectional sample of wild chimpanzee mother-infant dyads yield evidence that young chimpanzees' pant grunting unfolds nonlinearly over the early developmental period. Though infants begin pant grunting early, and mothers' rates did not decrease, infant pant grunting declined as infants aged through infancy. Mother-infant dyadic pant grunting discordance therefore increased over infancy, with some discordance observed at even the earliest ages. In half of 90 observed instances involving infants ranging in age from 2 weeks to 69 months, only one member of the mother-infant dyad pant grunted; infants' pant grunting was not influenced by their mother's age, their position on their mother's body at the time of the greeting, or the dominance status of the male greeted. Male infants were more likely to pant grunt than female infants. We discuss the developmental trend in the context of infants' increasing independence, changing social motivations, and male-dominated social hierarchy.

Favorable ecological circumstances promote life expectancy in chimpanzees similar to that of human hunter-gatherers.

Demographic data on wild chimpanzees are crucial for understanding the evolution of chimpanzee and hominin life histories, but most data come from populations affected by disease outbreaks and anthropogenic disturbance. We present survivorship data from a relatively undisturbed and exceptionally large community of eastern chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. We monitored births, deaths, immigrations, and emigrations in the community between 1995 and 2016. Using known and estimated ages, we calculated survivorship curves for the whole community, for males and females separately, and for individuals ≤2 years old when identified. We used a novel method to address age estimation error by calculating stochastic survivorship curves. We compared Ngogo life expectancy, survivorship, and mortality rates to those from other chimpanzee communities and human hunter-gatherers. Life expectancy at birth for both sexes combined was 32.8 years, far exceeding estimates of chimpanzee life expectancy in other communities, and falling within the range of human hunter-gatherers (i.e., 27-37 years). Overall, the pattern of survivorship at Ngogo was more similar to that of human hunter-gatherers than to other chimpanzee communities. Maximum lifespan for the Ngogo chimpanzees, however, was similar to that reported at other chimpanzee research sites and was less than that of human-hunter gatherers. The absence of predation by large carnivores may contribute to some of the higher survivorship at Ngogo, but this cannot explain the much higher survivorship at Ngogo than at Kanyawara, another chimpanzee community in the same forest, which also lacks large carnivores. Higher survivorship at Ngogo appears to be an adaptive response to a food supply that is more abundant and varies less than that of Kanyawara. Future analyses of hominin life history evolution should take these results into account.

Assessing sources of error in comparative analyses of primate behavior: Intraspecific variation in group size and the social brain hypothesis.

Phylogenetic comparative methods have become standard for investigating evolutionary hypotheses, including in studies of human evolution. While these methods account for the non-independence of trait data due to phylogeny, they often fail to consider intraspecific variation, which may lead to biased or erroneous results. We assessed the degree to which intraspecific variation impacts the results of comparative analyses by investigating the "social brain" hypothesis, which has provided a framework for explaining complex cognition and large brains in humans. This hypothesis suggests that group life imposes a cognitive challenge, with species living in larger social groups having comparably larger neocortex ratios than those living in smaller groups. Primates, however, vary considerably in group size within species, a fact that has been ignored in previous analyses. When within-species variation in group size is high, the common practice of using a mean value to represent the species may be inappropriate. We conducted regression and resampling analyses to ascertain whether the relationship between neocortex ratio and group size across primate species persists after controlling for within-species variation in group size. We found that in a sample of 23 primates, 70% of the variation in group size was due to between-species variation. Controlling for within-species variation in group size did not affect the results of phylogenetic analyses, which continued to show a positive relationship between neocortex ratio and group size. Analyses restricted to non-monogamous primates revealed considerable intraspecific variation in group size, but the positive association between neocortex ratio and group size remained even after controlling for within-species variation in group size. Our findings suggest that the relationship between neocortex size and group size in primates is robust. In addition, our methods and associated computer code provide a way to assess and account for intraspecific variation in other comparative analyses of primate evolution.

Long bone cross-sectional properties reflect changes in locomotor behavior in developing chimpanzees.

OBJECTIVES: Recent studies indicate that the locomotor behavior of wild chimpanzees changes during development. Before transitioning to quadrupedal knuckle-walking in adulthood, young chimpanzees engage in a significant amount of upper limb loading suspensory behavior. We investigated whether these dramatic changes in locomotion influence the strength and shape of chimpanzee long bones. MATERIALS AND METHODS: We examined changes in chimpanzee arboreal locomotion over the course of development using behavioral data collected on wild chimpanzees. We measured the midshaft geometric properties of femora and humeri of wild-caught individuals housed in museum collections using micro computed tomographic scans. RESULTS: Chimpanzees spent less time moving arboreally as they aged. Femoral/humeral strength ratios also increased with age, as predicted by the changing loading environment during development. Additional analyses revealed that femoral shape, but not humeral shape, varied across chimpanzee age classes. Adult femora were more elliptical compared with those of infants. This change in adult femora is consistent with the observation that adult chimpanzees spend most of their time moving terrestrially and consequently experience a less variable loading environment than do infants. DISCUSSION: Taken together, these findings contribute to our understanding of how ontogenetic changes in function affect form. As similar changes may have characterized the behavioral and skeletal ontogeny of extinct hominoids including hominins, these findings furnish a potential means to make inferences about the behavior of fossil taxa based on the structural properties of their bones.

Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution.

Fossils and molecular data are two independent sources of information that should in principle provide consistent inferences of when evolutionary lineages diverged. Here we use an alternative approach to genetic inference of species split times in recent human and ape evolution that is independent of the fossil record. We first use genetic parentage information on a large number of wild chimpanzees and mountain gorillas to directly infer their average generation times. We then compare these generation time estimates with those of humans and apply recent estimates of the human mutation rate per generation to derive estimates of split times of great apes and humans that are independent of fossil calibration. We date the human-chimpanzee split to at least 7-8 million years and the population split between Neanderthals and modern humans to 400,000-800,000 y ago. This suggests that molecular divergence dates may not be in conflict with the attribution of 6- to 7-million-y-old fossils to the human lineage and 400,000-y-old fossils to the Neanderthal lineage.

Two Cases of Cleft Lip and Other Congenital Anomalies in Wild Chimpanzees Living in Kibale National Park, Uganda.

DESIGN: Observations of wild chimpanzees ( Pan troglodytes schweinfurthii) were conducted in Kibale National Park, Uganda, at the sites of Sebitoli and Ngogo. RESULTS: We report the first two cases of cleft lip in wild chimpanzees. Additionally, some other chimpanzees in the Sebitoli community show facial dysplasia and congenital anomalies, such as patches of depigmented hairs and limb defects. CONCLUSIONS: Cleft lip has been documented in several species of nonhuman primates, but much remains unknown about the occurrence of cleft lip and cleft palate in great apes, probably because such malformations are rare, wild apes are difficult to monitor and observe, and severe cases associated with cleft palates render suckling impossible and lead to early death of infants. The genetic basis of such defects in great apes warrants investigation, as does the possibility that environmental toxins contribute to their etiology in Kibale in ways that could affect humans as well.

Removing snares is an effective conservation intervention: a case study involving chimpanzees.

Wild chimpanzees (Pan troglodytes) are caught in snares set for other animals and sometimes injure or lose body parts. Snaring can compromise the health, growth, survival, and behavior of chimpanzees and, thus, represents a threat for the conservation of this endangered species. During a long-term study of chimpanzees at Ngogo in Kibale National Park, Uganda, we started a project to remove snares in and around their territory. We compared the number of times chimpanzees were snared during the 12.75 years after the start of this project with the number of times individuals were snared during the previous 14 years. Only one chimpanzee was snared after we began removing snares compared with 12 individuals caught during the period before. This represents a clear reduction in the risk created by snaring at this site and suggests that removing snares can be employed to protect chimpanzees.

Future coexistence with great apes will require major changes to policy and practice.

The great apes-bonobos, chimpanzees, gorillas and orangutans-are critically threatened by human activities. We have destroyed their habitats, hunted them and transmitted fatal diseases to them. Yet we also conduct research on them, try to protect them and live alongside them. They are endangered, and time is running out. Here we outline what must be done to ensure that future generations continue to share this planet with great apes. We urge dialogue with those who live with great apes and interact with them often. We advocate conservation plans that acknowledge the realities of climate change, economic drivers and population growth. We encourage researchers to use technology to minimize risks to great apes. Our proposals will require substantial investment, and we identify ways to generate these funds. We conclude with a discussion of how field researchers might alter their work to protect our closest living relatives more effectively.

Diurnal variation in nutrients and chimpanzee foraging behavior.

Primate feeding behavior varies over long (e.g., weekly, seasonally, yearly) and short (e.g., hourly) scales of time due to changes in resource availability and the nutritional composition of foods. While the factors that affect long-term changes in feeding behavior have received considerable attention, few data exist regarding what drives variability in feeding behavior over the course of a single day. To address this problem, we investigated diurnal variation in chimpanzee feeding on the leaves of two species of saplings, Pterygota mildbraedii and Celtis africana, at Ngogo, Kibale National Park, Uganda. Specifically, we related short-term changes in chimpanzee feeding behavior on these leaves to diurnal variation in their nutritional composition. Results showed that chimpanzees fed on the leaves of both saplings more in the evening than they did in the morning. The nutritional quality of leaves also improved over the course of the day. Concentrations of cellulose and lignin were lower and total nonstructural carbohydrates (including sugars and starch) were higher in the evening for P. mildbraedii, and sugars were higher in the evening for C. africana. These data suggest that chimpanzees consume these resources when their quality is highest, and consequently, may track the nutrient composition of their foods over very short periods that span only a few hours. In the future, foods collected for analyses must control for time of sampling to ensure biologically meaningful assays of nutrient composition.