Wild Chimpanzees Research Articles

Genetic Diversity in Chimpanzee Transcriptomics Does Not Represent Wild Populations.

Chimpanzees (Pan troglodytes) are a genetically diverse species, consisting of four highly distinct subspecies. As humans’ closest living relative, they have been a key model organism in the study of human evolution, and comparisons of human and chimpanzee transcriptomes have been widely used to characterize differences in gene expression levels that could underlie the phenotypic differences between the two species. However, the subspecies from which these transcriptomic data sets have been derived is not recorded in metadata available in the public NCBI Sequence Read Archive (SRA). Furthermore, labeling of RNA sequencing (RNA-seq) samples is for the most part inconsistent across studies, and the true number of individuals from whom transcriptomic data are available is difficult to ascertain. Thus, we have evaluated genetic diversity at the subspecies and individual level in 486 public RNA-seq samples available in the SRA, spanning the vast majority of public chimpanzee transcriptomic data. Using multiple population genetics approaches, we find that nearly all samples (96.6%) have some degree of Western chimpanzee ancestry. At the individual donor level, we identify multiple samples that have been repeatedly analyzed across different studies and identify a total of 135 genetically distinct individuals within our data, a number that falls to 89 when we exclude likely first- and second-degree relatives. Altogether, our results show that current transcriptomic data from chimpanzees are capturing low levels of genetic diversity relative to what exists in wild chimpanzee populations. These findings provide important context to current comparative transcriptomics research involving chimpanzees.

Vocal communication in wild chimpanzees: a call rate study.

BackgroundPatterns of vocal communication have implications for species conservation: a change in calling behaviour can, for instance, reflect a disturbed habitat. More importantly, call rate is a parameter that allows conservation planners to convert call density into animal density, when detecting calls with a passive acoustic monitoring system (PAM).MethodsWe investigated chimpanzee (Pan troglodytes schweinfurthii) call rate during the late dry season in the Issa Valley, western Tanzania by conducting focal follows. We examined the socio-ecological factors that influence call production rate of savanna woodland chimpanzees.ResultsWe found that sex, proportion of time spent in a vegetation type, proportion of time spent travelling, time of the day, party size and swollen parous female presence had a significant effect on the call rate. Call rate differed among the different demographic classes with subadult and adult males vocalising twice as often as the subadult and adult females and three times as often as the juveniles.ApplicationsThe use of PAM and recent statistical developments to estimate animal density is promising but relies on our knowing individual call rate, often not available for many species. With the improvement in automatic call detection, we anticipate that PAM will increasingly be broadly applied to primates but also across taxa, for conservation.

Sensitivity to the communicative partner's attentional state: A developmental study on mother-infant dyads in wild chimpanzees (Pan troglodytes schweinfurthii).

Gestural communication permeates all domains of chimpanzees' social life and is intentional in use. However, we still have only limited information on how young apes develop the sociocognitive skills needed for intentional communication. In this cross-sectional study, we document the development of behavioral adjustment to the recipient's visual attention-considered a hallmark of intentional communication-in wild immature chimpanzees' gestural communication. We studied 11 immature chimpanzees (Pan troglodytes schweinfurthii): three infants, four juveniles, and four adolescents gesturing towards their mother. We quantified silent-visual, audible, and contact gestures indexed to maternal visual attention and inattention. We investigated unimodal adjustment, defined by the capacity of young chimpanzees to deploy fewer silent-visual signals when their mothers did not show full visual attention towards them as compared with when they did. We then examined cross-modal adjustment, defined as the capacity of chimpanzees to deploy more audible-or-contact gestures than silent-visual gestures in the condition where their mothers did not show full visual attention as compared to when they did. Our results show a gradual decline in the use of silent-visual gestures when the mother is not visually attentive with increasing age. The absence of silent-visual gesture production toward a visually inattentive recipient (complete unimodal adjustment) was not fully in place until adolescence. Immature chimpanzees used more audible-or-contact gestures than silent-visual ones when their mothers did not show visual attention and vice-versa when they did. This cross-modal adjustment was expressed in juveniles and adolescents but not in infants. Overall, this study shows that infant chimpanzees were limited in their sensitivity to maternal attention when gesturing, whereas adolescent chimpanzees adjusted their communication appropriately. Juveniles present an intermediate pattern with cross-modal adjustment preceding unimodal adjustment and with variability in the age of onset.

Evaluating adaptive hypotheses for female-led infanticide in wild chimpanzees

Although rare among group-living primates, infanticide by females has been reported in several chimpanzee, Pan troglodytes, populations. We examined 13 infanticidal attacks over 47 years at Gombe National Park, Tanzania to evaluate three adaptive hypotheses. (1) Exploitation of the infant as a food resource – by eating a vulnerable neonate, attackers gain calories that may be important during periods of food scarcity or energetic stress. (2) Resource competition – Gombe females concentrate their foraging in overlapping core areas and dominance rank influences foraging success. By killing the infant of a female with high core area overlap, the perpetrator removes a current and future competitor, improving her access to food. (3) Low cost – female chimpanzees mature and reproduce slowly, and longevity increases reproductive success. Physical aggression causes risk of severe injury or death, so females will only mount attacks when risks to the perpetrator are low. In support of hypothesis 1, females usually consumed the carcass. However, attacks were not more likely in times of resource or energy scarcity. In support of hypothesis 2, females attacked others with whom they shared core areas, but attacks did not cause shifts in ranging patterns. In support of hypothesis 3, one or more attackers always outranked the victim, the attacks often involved coalitions and victims usually lacked kin support. Attacks were more likely to be successful when attackers were not hindered by clinging infants and victims could not retreat. Our results provide further evidence for female competition and the adaptive value of female-led infanticide in this species.

Social bonds provide multiple pathways to reproductive success in wild male chimpanzees

SummaryIn most male mammals, fitness is strongly shaped by competitive access to mates, a non-shareable resource. How, then, did selection favor the evolution of cooperative social bonds? We used behavioral and genetic data on wild chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania, to study the mechanisms by which male-male social bonds increase reproductive success. Social bonds increased fitness in several ways: first, subordinate males that formed strong bonds with the alpha male had higher siring success. Independently, males with larger networks of strong bonds had higher siring success. In the short term, bonds predicted coalition formation and centrality in the coalition network, suggesting that males benefit from being potential allies to numerous male rivals. In the long term, male ties influenced fitness via improved dominance rank for males that attain alpha status. Together, these results suggest that male bonds evolved in chimpanzees by affording both short- and long-term pathways to reproductive success.

In vivo deciduous dental eruption in LuiKotale bonobos and Gombe chimpanzees.

Existing data on bonobo and chimpanzee dental eruption timing are derived predominantly from captive individuals or deceased wild individuals. However, recent advances in noninvasive photographic monitoring of living, wild apes have enabled researchers to characterize dental eruption in relatively healthy individuals under naturalistic conditions. At present, such data are available for only one population of wild chimpanzees. We report data for an additional population of wild chimpanzees and the first dental eruption data for wild bonobos. We collected photographs and video footage of teeth from the open mouths of wild bonobos and East African chimpanzees of known age from LuiKotale, Democratic Republic of the Congo, and Gombe National Park, Tanzania, respectively. We scored the presence and absence of deciduous teeth from photographs and video footage to characterize deciduous dental eruption timing in these two populations. Deciduous dental eruption ages in our sample fall within the range of variation previously documented for captive chimpanzees, but eruption ages are later in wild than in captive contexts. We found substantial variation in deciduous canine eruption timing, particularly among bonobos. One bonobo had a deciduous canine present by 227 days old while another did not have a deciduous canine present at 477 days old. Our data indicate that deciduous teeth erupt later in wild individuals than in captive individuals. We also found that deciduous dental eruption timing varies considerably between individuals within our study populations, a pattern that is consistent with previous studies. Future studies should consider sources of variation in deciduous canine eruption timing and relationships with other aspects of life history as additional data become available.

First observation of a chimpanzee with albinism in the wild: Social interactions and subsequent infanticide.

Albinism—the congenital absence of pigmentation—is a very rare phenomenon in animals due to the significant costs to fitness of this condition. Both humans and non‐human individuals with albinism face a number of challenges, such as reduced vision, increased exposure to ultraviolet radiation, or compromised crypticity resulting in an elevated vulnerability to predation. However, while observations of social interactions involving individuals with albinism have been observed in wild non‐primate animals, such interactions have not been described in detail in non‐human primates (hereafter, primates). Here, we report, to our knowledge, the first sighting of an infant with albinism in wild chimpanzees (Pan troglodytes schweinfurthii), including social interactions between the infant, its mother, and group members. We also describe the subsequent killing of the infant by conspecifics as well as their behavior towards the corpse following the infanticide. Finally, we discuss our observations in relation to our understanding of chimpanzee behavior or attitudes towards individuals with very conspicuous appearances.

Culture-enriched community profiling improves resolution of the vertebrate gut microbiota.

Vertebrates harbour gut microbial communities containing hundreds of bacterial species, most of which have never been cultivated or isolated in the laboratory. The lack of cultured representatives from vertebrate gut microbiotas limits the description and experimental interrogation of these communities. Here, we show that representatives from >50% of the bacterial genera detected by culture-independent sequencing in the gut microbiotas of fence lizards, house mice, chimpanzees, and humans were recovered in mixed cultures from frozen faecal samples plated on a panel of nine media under a single growth condition. In addition, culturing captured >100 rare bacterial genera overlooked by culture-independent sequencing, more than doubling the total number of bacterial sequence variants detected. Our approach recovered representatives from 23 previously uncultured candidate bacterial genera, 12 of which were not detected by culture-independent sequencing. Results identified strategies for both indiscriminate and selective culturing of the gut microbiota that were reproducible across vertebrate species. Isolation followed by whole-genome sequencing of 161 bacterial colonies from wild chimpanzees enabled the discovery of candidate novel species closely related to the opportunistic pathogens of humans Clostridium difficile and Hungatella hathewayi. This study establishes culturing methods that improve inventories and facilitate isolation of gut microbiota constituents from a wide diversity of vertebrate species.

A preliminary analysis of wound care and other-regarding behavior in wild chimpanzees at Ngogo, Kibale National Park, Uganda.

Caring for others is a key feature of human behavior. Mothers, fathers, siblings, grandparents, and other group members provide care in the form of provisioning, protection, and first aid. To what extent is other-regarding behavior present in our primate relatives? Here we describe an unusual incident of other-regarding behavior toward an injured juvenile female chimpanzee (Pan troglodytes schweinfurthii) at Ngogo in Kibale National Park, Uganda. After the juvenile received a mild head wound from an adult female, several adolescent and juvenile chimpanzees gathered to touch, lick, and peer at the wound. One adolescent male wiped a leaf across the cut. Another adolescent male later groomed the injured female and briefly carried her. Across a 5-year period, we observed only three other instances of other-directed wound care in chimpanzees, occurring in 4% (4/100) of cases in which we observed individuals with fresh wounds, and 57 other instances of allomaternal carrying. Despite the infrequency of such behaviors, our study adds another chimpanzee field site to the list of those where other-directed wound care has been observed. Observations from wild chimpanzees provide insight into empathy and may inform our understanding of the evolution of other-regarding behavior in humans.

Structure of Chimpanzee Gut Microbiomes across Tropical Africa.

ABSTRACTUnderstanding variation in host-associated microbial communities is important given the relevance of microbiomes to host physiology and health. Using 560 fecal samples collected from wild chimpanzees (Pan troglodytes) across their range, we assessed how geography, genetics, climate, vegetation, and diet relate to gut microbial community structure (prokaryotes, eukaryotic parasites) at multiple spatial scales. We observed a high degree of regional specificity in the microbiome composition, which was associated with host genetics, available plant foods, and potentially with cultural differences in tool use, which affect diet. Genetic differences drove community composition at large scales, while vegetation and potentially tool use drove within-region differences, likely due to their influence on diet. Unlike industrialized human populations in the United States, where regional differences in the gut microbiome are undetectable, chimpanzee gut microbiomes are far more variable across space, suggesting that technological developments have decoupled humans from their local environments, obscuring regional differences that could have been important during human evolution.IMPORTANCE Gut microbial communities are drivers of primate physiology and health, but the factors that influence the gut microbiome in wild primate populations remain largely undetermined. We report data from a continent-wide survey of wild chimpanzee gut microbiota and highlight the effects of genetics, vegetation, and potentially even tool use at different spatial scales on the chimpanzee gut microbiome, including bacteria, archaea, and eukaryotic parasites. Microbial community dissimilarity was strongly correlated with chimpanzee population genetic dissimilarity, and vegetation composition and consumption of algae, honey, nuts, and termites were potentially associated with additional divergence in microbial communities between sampling sites. Our results suggest that host genetics, geography, and climate play a far stronger role in structuring the gut microbiome in chimpanzees than in humans.

Early maternal loss leads to short- but not long-term effects on diurnal cortisol slopes in wild chimpanzees.

The biological embedding model (BEM) suggests that fitness costs of maternal loss arise when early-life experience embeds long-term alterations to hypothalamic-pituitary-adrenal (HPA) axis activity. Alternatively, the adaptive calibration model (ACM) regards physiological changes during ontogeny as short-term adaptations. Both models have been tested in humans but rarely in wild, long-lived animals. We assessed whether, as in humans, maternal loss had short- and long-term impacts on orphan wild chimpanzee urinary cortisol levels and diurnal urinary cortisol slopes, both indicative of HPA axis functioning. Immature chimpanzees recently orphaned and/or orphaned early in life had diurnal cortisol slopes reflecting heightened activation of the HPA axis. However, these effects appeared short-term, with no consistent differences between orphan and non-orphan cortisol profiles in mature males, suggesting stronger support for the ACM than the BEM in wild chimpanzees. Compensatory mechanisms, such as adoption, may buffer against certain physiological effects of maternal loss in this species.

<Note>Use of a novel human object as a masturbatory tool by a wild male chimpanzee at Bulindi, Uganda

<Note>Use of a novel human object as a masturbatory tool by a wild male chimpanzee at Bulindi, Uganda

Gregariousness is associated with parasite species richness in a community of wild chimpanzees.

Increased risk of pathogen transmission through proximity and contact is a well-documented cost of sociality. Affiliative social contact, however, is an integral part of primate group life and can benefit health. Despite its importance to the evolution and maintenance of sociality, the tradeoff between costs and benefits of social contact for group-living primate species remains poorly understood. To improve our understanding of this interplay, we used social network analysis to investigate whether contact via association in the same space and/or physical contact measured through grooming were associated with helminth parasite species richness in a community of wild chimpanzees (Pan troglodytes schweinfurthii). We identified parasite taxa in 381 fecal samples from 36 individuals from the Kasekela community of chimpanzees in Gombe National Park, Tanzania, from November 1, 2006 - October 31, 2012. Over the study period, eight environmentally transmitted helminth taxa were identified. We quantified three network metrics for association and grooming contact, including degree strength, betweenness, and closeness. Our findings suggest that more gregarious individuals - those who spent more time with more individuals in the same space - had higher parasite richness, while the connections in the grooming network were not related to parasite richness. The expected parasite richness in individuals increased by 1.13 taxa (CI: 1.04, 1.22; p = 0.02) per one standard deviation increase in degree strength of association contact. The results of this study add to the understanding of the role that different types of social contact plays in the parasite richness of group-living social primates.

Urinary neopterin of wild chimpanzees indicates that cell-mediated immune activity varies by age, sex, and female reproductive status

The study of free-living animal populations is necessary to understand life history trade-offs associated with immune investment. To investigate the role of life history strategies in shaping proinflammatory cell-mediated immune function, we analyzed age, sex, and reproductive status as predictors of urinary neopterin in 70 sexually mature chimpanzees (Pan troglodytes) at Ngogo, Kibale National Park, Uganda. In the absence of clinical signs of acute infectious disease, neopterin levels significantly increased with age in both male and female chimpanzees, as observed in humans and several other vertebrate species. Furthermore, males exhibited higher neopterin levels than females across adulthood. Finally, females with full sexual swellings, pregnant females, and post-reproductive females, the oldest individuals in our sample, exhibited higher neopterin levels than lactating females and cycling females without full swellings. Variation in females’ neopterin levels by reproductive status is consistent with post-ovulatory and pregnancy-related immune patterns documented in humans. Together, our results provide evidence of ample variation in chimpanzee immune activity corresponding to biodemographic and physiological variation. Future studies comparing immune activity across ecological conditions and social systems are essential for understanding the life histories of primates and other mammals.

Contest competition for fruit and space among wild chimpanzees in relation to the vertical stratification of metabolizable energy

Variance in the quality of food sites exploited by group-living animals should allow dominant individuals to gain feeding advantages. In some cases of eating in large patches, however, the amount of agonism can be puzzlingly low. We studied this problem in wild adult chimpanzees, Pan troglodytes, eating ripe fruits in large tree crowns, a context in which little aggression has previously been recorded. Observations were conducted from within the same tree crown as feeding chimpanzees, which allowed us to obtain high-quality data on food distribution, feeding behaviour and aggression. We assessed energy availability and chimpanzee behaviour in relation to their feeding depth. Deeper food sites were associated with less metabolizable food energy (kcal/m3) and lower energy intake rates (kcal/min). Energy availability also varied by tree type (higher in drupe trees than in fig trees) and fruit ripeness (higher in riper fruits). Males were dominant to females, and within both sexes aggressive interactions conformed to a linear hierarchy. Overall higher-ranking individuals used aggression and dominance to access superior feeding sites and achieve higher rates of energy intake, but the effects of dominance varied according to tree type, sex and party composition. Our study shows that covert contest competition over feeding sites gave dominant individuals an important advantage even in very large patches.

First Evidence of Chimpanzee Extractive Tool Use in Cantanhez, Guinea-Bissau: Cross-Community Variation in Honey Dipping

Wild chimpanzee tool use is highly diverse and, in many cases, exhibits cultural variation: tool-use behaviours and techniques differ between communities and are passed down generations through social learning. Honey dipping – the use of sticks or leaves to extract honey from hives – has been identified across the whole species’ range. Nonetheless, there seems to be marked variation in honey dipping at a species level, with most descriptions originating from central Africa, and involving the use of complex tool sets, or even multifunctional tools. In West Africa, while honey consumption is common, in most cases tools are not used. We document, for the first time, the use of honey dipping tools in unhabituated chimpanzee (Pan troglodytes verus) communities at Cantanhez National Park (CNP), Guinea-Bissau. Over a 23-month period we employed a combination of direct (camera traps, n = 1944 camera trap days) and indirect (1000km of reconnaissance walks, collection of abandoned tools) methods to study four neighbouring communities in central CNP. Fluid dipping tools were found in three of the four communities; here we analyse 204 individual stick tools from the 70 tool-use ateliers found. In addition to documenting individual tool dimensions and raw materials, we adopt methods from primate archaeology to describe the typology of different tools based on use-wear patterns. We describe differences in tools used for different honey types, between communities, and tools and tool kits that show an unexpected degree of complexity. Our data also suggest the use of tool sets, i.e., tools with different functions used sequentially toward the same goal; as well as possible multifunction tools (pounding and dipping), never before described for western chimpanzees. Our study fills gaps in our knowledge of the wild chimpanzee cultural repertoire and highlights how chimpanzee tool manufacture and use can vary even at local scales.

Effects of domestication on the gut microbiota parallel those of human industrialization.

Domesticated animals experienced profound changes in diet, environment, and social interactions that likely shaped their gut microbiota and were potentially analogous to ecological changes experienced by humans during industrialization. Comparing the gut microbiota of wild and domesticated mammals plus chimpanzees and humans, we found a strong signal of domestication in overall gut microbial community composition and similar changes in composition with domestication and industrialization. Reciprocal diet switches within mouse and canid dyads demonstrated the critical role of diet in shaping the domesticated gut microbiota. Notably, we succeeded in recovering wild-like microbiota in domesticated mice through experimental colonization. Although fundamentally different processes, we conclude that domestication and industrialization have impacted the gut microbiota in related ways, likely through shared ecological change. Our findings highlight the utility, and limitations, of domesticated animal models for human research and the importance of studying wild animals and non-industrialized humans for interrogating signals of host-microbial coevolution.

The function of chimpanzee greeting calls is modulated by their acoustic variation

Signalling plays an important role in mediating social interactions in many animal species. For example, during approaches certain species produce ‘greetings’, which can take the form of vocal or visual signals, which reduce the probability of aggressive interactions and/or facilitate affiliation when approaching each other. However, in species where greetings comprise both vocal and visual signals, little is known about how the vocal component relates to the visual component or, in species with fission–fusion dynamics, to the time spent together by the dyad in the same subgroup prior to the approach. Similarly, in species with several acoustic variants of greeting calls, it is unclear whether different variants have different functions. We looked at the production of two acoustically distinct greeting call variants, low-fundamental frequency pant grunts and high-fundamental frequency pant barks, during approaches between two individuals in five communities of wild chimpanzees, Pan troglodytes, in Uganda and Ivory Coast. More specifically, we explored the relationship between greeting call production and (1) aggressive and submissive interactions during the approach and (2) preceding and subsequent proximity levels between the involved individuals. Calls were more likely to be produced during aggressive interactions and were associated with postures and gestures linked to submission; these patterns were stronger when the utterance contained a pant bark rather than a pant grunt alone. The production of greeting calls was more likely soon after party fusion and was negatively related to subsequent proximity levels between the caller and receiver. These results expand our knowledge of greeting calls and imply that these calls might be used to re-establish dominance relationships after a period of separation, and that the function of these calls can be modulated by their specific acoustic variants and by visual signals that often accompany them.

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.

Discovery of Novel Herpes Simplexviruses in Wild Gorillas, Bonobos, and Chimpanzees Supports Zoonotic Origin of HSV-2

Viruses closely related to human pathogens can reveal the origins of human infectious diseases. Human herpes simplexvirus type 1 (HSV-1) and type 2 (HSV-2) are hypothesized to have arisen via host-virus codivergence and cross-species transmission. We report the discovery of novel herpes simplexviruses during a large-scale screening of fecal samples from wild gorillas, bonobos, and chimpanzees. Phylogenetic analysis indicates that, contrary to expectation, simplexviruses from these African apes are all more closely related to HSV-2 than to HSV-1. Molecular clock-based hypothesis testing suggests the divergence between HSV-1 and the African great ape simplexviruses likely represents a codivergence event between humans and gorillas. The simplexviruses infecting African great apes subsequently experienced multiple cross-species transmission events over the past 3 My, the most recent of which occurred between humans and bonobos around 1 Ma. These findings revise our understanding of the origins of human herpes simplexviruses and suggest that HSV-2 is one of the earliest zoonotic pathogens.