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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. [ABSTRACT FROM AUTHOR]

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. Research Highlights: Some viruses of wild primates are relatively benign but may be useful as biomarkers of physiology and health.We used metagenomic methods to characterize viral communities in feces of wild chimpanzees in two long‐term study communities (Kanyawara and Ngogo) in Kibale National Park, Uganda.Chimpanzees exhibited higher viral loads (normalized abundances of viral genetic sequences) when they were ill than when those same individuals were previously healthy.When ill, Kanyawara chimpanzees exhibited higher viral loads than Ngogo chimpanzees, and males, but not females, exhibited higher viral loads as they aged. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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'. [ABSTRACT FROM AUTHOR]

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. Am. J. Primatol. 75:342-349, 2013. © 2013 Wiley Periodicals, Inc. [ABSTRACT FROM AUTHOR]

Controversy exists regarding the nature of primate social relationships. While individual primates are frequently hypothesized to form enduring social bonds with conspecifics, recent studies suggest that relationships are labile, with animals interacting only over short periods to satisfy their immediate needs. Here I use data collected over 10 years on a community of chimpanzees, Pan troglodytes, at Ngogo, Kibale National Park, Uganda, to investigate whether male chimpanzees establish long-term social relationships and to determine the factors that affect variation in relationship quality and the stability of social bonds. Kinship and dominance rank influenced the quality of relationships. Maternal brothers and males of the same dominance rank class groomed each other more equitably than did unrelated males and males that were dissimilar in rank. In addition, males that formed strong social bonds groomed more equitably than did males that displayed weaker bonds. Social bonds were stable over time, with relationships in one year predicting those in subsequent years. Kinship and the quality of social relationships affected bond stability. Maternal half siblings and males that groomed each other equitably maintained longer-lasting bonds than did nonkin and males that groomed each other unevenly. Virtually all of the males established at least one enduring relationship with another individual. The most enduring bonds formed between a few pairs of maternal brothers and dyads that maintained balanced grooming interactions. These results indicate that male chimpanzees maintain long-lasting and equitable social bonds whose formation is affected by maternal kinship and the quality of social relationships. [Copyright &y& Elsevier]

Demography provides critical data to increase our understanding of the evolution, ecology, and conservation of primate populations. The chimpanzees of the Mahale Mountains National Park, Tanzania, have been studied for more than 34 yr on the basis of individual identification and standardized attendance records. From this long-term study, we derived the following demographic data: The major cause of death was disease (48%), followed by senescence (24%) and within-species aggression (16%). Fifty percent of Mahale chimpanzees died before weaning. The median ages of female life history variables were: first maximal swelling, 10.0 yr (n=5); emigration, 11.0 yr (n=11); and first birth, 13.1 yr (n=5). The median period of adolescent infertility was 2.8 yr (n=4) when calculated from the age at immigration to that at first birth. Female fecundity was highest between 20 and 35 yr of age, with an annual birth rate of 0.2. Twenty-six females that were observed from a young age (10–13 yr) to death at various ages (15–40 yr) gave birth to an average of 3.9 and weaned an average of 1.4 offspring. Twenty-five females that were observed from middle age (18–33 yr) to death in older age (31–48) gave birth to an average of 2.7 and weaned an average of 2.0 offspring. The post-reproductive lifespan for female chimpanzees was defined as the number of years that passed from the year when the last offspring was born to the year when the female died, minus 5. Twenty-five percent of old females had a post-reproductive lifespan. The interbirth interval after the birth of a son (&xmacr; = 72 mo) tended to be longer than that after the birth of a daughter (&xmacr; = 66 mo). The extent of female transfer, which is a rule in chimpanzees, is influenced by the size and composition of the unit group and size of the overall local community. Am. J. Primatol. 59:99–121, 2003. © 2003 Wiley-Liss, Inc. [ABSTRACT FROM AUTHOR]

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. • Adolescent and young adult male chimpanzees form affiliative relationships with females similar to, yet different from, bonds adult male chimpanzees form with other males and maternal kin. • As males enter adulthood, they form stronger relationships with more females than males do during adolescence. • Adolescent and young adult males direct aggression selectively to females with whom they form affiliative social bonds. [ABSTRACT FROM AUTHOR]

Although testosterone (T) has well known organizational and activational effects on aggression, the relationship between the two is not always clear. The challenge hypothesis addresses this problem by proposing that T will affect aggression only in fitness-enhancing situations. One way to test the challenge hypothesis is to examine the relationship between T and different types of aggression. Chimpanzees, Pan troglodytes, show aggressive behaviours in several contexts and provide an opportunity for such a test. Here we show that urinary T influences a form of male chimpanzee reproductive aggression, territorial boundary patrols. In contrast, T does not affect predatory behaviour, a form of aggression that has no immediate link to male reproduction. While these results are consistent with the challenge hypothesis, our results indicate that male chimpanzees experience a significant drop in urinary T during hunts. Additional analyses reveal that males who share meat with others display this decrease. The reason for this decrement is unclear, but we hypothesize that the relative lack of aggression that results from voluntary sharing episodes and the tolerance engendered by such acts may be contributory factors. [Copyright &y& Elsevier]

Survival in primates is facilitated by commensal gut microbes that ferment otherwise indigestible plant matter, resist colonization by pathogens, and train the developing immune system. 1,2 However, humans are unique among primates in that we consume highly digestible foods, wean early, mature slowly, and exhibit high lifelong investments in maintenance. 3–6 These adaptations suggest that lifetime trajectories of human-microbial relationships could differ from those of our closest living relatives. Here, we profile the gut microbiota of 166 wild chimpanzees aged 8 months to 67 years in the Kibale National Park, Uganda and compare the patterns of gut microbial maturation to those previously observed in humans. We found that chimpanzee gut microbial alpha-diversity, composition, density, interindividual variation, and within-individual change over time varied significantly with age. Notably, gut microbial signatures in infants <2 years old were distinct across all five metrics. Infant chimpanzee guts were enriched in some of the same taxa prevalent in infant humans (e.g., Bifidobacterium, Streptococcus , and Bacteroides), and chimpanzee gut microbial communities, like those of humans, exhibited higher interindividual variation in infancy versus later in life. However, in direct contrast to human infants, chimpanzee infants harbored surprisingly high-diversity rather than low-diversity gut bacterial communities compared with older conspecifics. These data indicate differential trajectories of gut microbiota development in humans and chimpanzees that are consistent with interspecific differences in lactation, diet, and immune function. Probing the phenotypic consequences of differential early-life gut microbial diversity in chimpanzees and other primates will illuminate the life history impacts of the hominid-microbiome partnership. • We profiled changes in the wild chimpanzee gut microbiota over the life course • 600+ samples collected over 3 years from 166 individuals aged 8 months to 67 years • Unlike humans, gut microbial diversity in chimpanzees is highest in infancy (<2 years old) • Divergent patterns may reflect interspecific differences in lactation, diet, and immunity Reese et al. profile the gut microbiota of wild chimpanzees over the life course. High gut microbial diversity among infants <2 years old contrasts sharply with the low diversity observed in human infants. This divergence could relate to interspecific differences in lactation, diet, and immunity and may contribute to lifelong differences in physiology. [ABSTRACT FROM AUTHOR]