Reproductive inequality among males in the genus Pan.

Reproductive inequality, or reproductive skew, drives natural selection, but has been difficult to assess, particularly for males in species with promiscuous mating and slow life histories, such as bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Although bonobos are often portrayed as more egalitarian than chimpanzees, genetic studies have found high male reproductive skew in bonobos. Here, we discuss mechanisms likely to affect male reproductive skew in Pan, then re-examine skew patterns using paternity data from published work and new data from the Kokolopori Bonobo Reserve, Democratic Republic of Congo and Gombe National Park, Tanzania. Using the multinomial index (M), we found considerable overlap in skew between the species, but the highest skew occurred among bonobos. Additionally, for two of three bonobo communities, but no chimpanzee communities, the highest ranking male had greater siring success than predicted by priority-of-access. Thus, an expanded dataset covering a broader demographic range confirms that bonobos have high male reproductive skew. Detailed comparison of data from Pan highlights that reproductive skew models should consider male-male dynamics including the effect of between-group competition on incentives for reproductive concessions, but also female grouping patterns and factors related to male-female dynamics including the expression of female choice. This article is part of the theme issue 'Evolutionary ecology of inequality'.

Personality traits, rank attainment, and siring success throughout the lives of male chimpanzees of Gombe National Park.

Personality traits in many taxa correlate with fitness. Several models have been developed to try to explain how variation in these traits is maintained. One model proposes that variation persists because it is linked to trade-offs between current and future adaptive benefits. Tests of this model's predictions, however, are scant in long-lived species. To test this model, we studied male chimpanzees living in Gombe National Park, Tanzania. We operationalized six personality traits using ratings on 19 items. We used 37 years of behavioral and genetic data to assemble (1) daily rank scores generated from submissive vocalizations and (2) records of male siring success. We tested whether the association between two personality traits, Dominance and Conscientiousness, and either rank or reproductive success, varied over the life course. Higher Dominance and lower Conscientiousness were associated with higher rank, but the size and direction of these relationships did not vary over the life course. In addition, independent of rank at the time of siring, higher Dominance and lower Conscientiousness were related to higher siring success. Again, the size and direction of these relationships did not vary over the life course. The trade-off model, therefore, may not hold in long-lived and/or slowly reproducing species. These findings also demonstrate that ratings are a valid way to measure animal personality; they are related to rank and reproductive success. These traits could therefore be used to test alternative models, including one that posits that personality variation is maintained by environmental heterogeneity, in studies of multiple chimpanzee communities.

Vocal signals facilitate cooperative hunting in wild chimpanzees.

Cooperation and communication likely coevolved in humans. However, the evolutionary roots of this interdependence remain unclear. We address this issue by investigating the role of vocal signals in facilitating a group cooperative behavior in an ape species: hunting in wild chimpanzees. First, we show that bark vocalizations produced before hunt initiation are reliable signals of behavioral motivation, with barkers being most likely to participate in the hunt. Next, we find that barks are associated with greater hunter recruitment and more effective hunting, with shorter latencies to hunting initiation and prey capture. Our results indicate that the coevolutionary relationship between vocal communication and group-level cooperation is not unique to humans in the ape lineage and is likely to have been present in our last common ancestor with chimpanzees.

Correlates of individual participation in boundary patrols by male chimpanzees.

Group territory defence poses a collective action problem: individuals can free-ride, benefiting without paying the costs. Individual heterogeneity has been proposed to solve such problems, as individuals high in reproductive success, rank, fighting ability or motivation may benefit from defending territories even if others free-ride. To test this hypothesis, we analysed 30 years of data from chimpanzees (Pan troglodytes) in the Kasekela community, Gombe National Park, Tanzania (1978-2007). We examined the extent to which individual participation in patrols varied according to correlates of reproductive success (mating rate, rank, age), fighting ability (hunting), motivation (scores from personality ratings), costs of defecting (the number of adult males in the community) and gregariousness (sighting frequency). By contrast to expectations from collective action theory, males participated in patrols at consistently high rates (mean ± s.d. = 74.5 ± 11.1% of patrols, n = 23 males). The best predictors of patrol participation were sighting frequency, age and hunting participation. Current and former alpha males did not participate at a higher rate than males that never achieved alpha status. These findings suggest that the temptation to free-ride is low, and that a mutualistic mechanism such as group augmentation may better explain individual participation in group territorial behaviour. This article is part of the theme issue 'Intergroup conflict across taxa'.

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

In 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.

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.

Urine as a high-quality source of host genomic DNA from wild populations.

The ability to generate genomic data from wild animal populations has the potential to give unprecedented insight into the population history and dynamics of species in their natural habitats. However, for many species, it is impossible legally, ethically or logistically to obtain tissue samples of quality sufficient for genomic analyses. In this study we evaluate the success of multiple sources of genetic material (faeces, urine, dentin and dental calculus) and several capture methods (shotgun, whole-genome, exome) in generating genome-scale data in wild eastern chimpanzees (Pan troglodytes schweinfurthii) from Gombe National Park, Tanzania. We found that urine harbours significantly more host DNA than other sources, leading to broader and deeper coverage across the genome. Urine also exhibited a lower rate of allelic dropout. We found exome sequencing to be far more successful than both shotgun sequencing and whole-genome capture at generating usable data from low-quality samples such as faeces and dental calculus. These results highlight urine as a promising and untapped source of DNA that can be noninvasively collected from wild populations of many species.

Optimizing syndromic health surveillance in free ranging great apes: the case of Gombe National Park.

1. Syndromic surveillance is an incipient approach to early wildlife disease detection. Consequently, systematic assessments are needed for methodology validation in wildlife populations. 2. We evaluated the sensitivity of a syndromic surveillance protocol for respiratory disease detection among chimpanzees in Gombe National Park, Tanzania. Empirical health, behavioural and demographic data were integrated with an agent-based, network model to simulate disease transmission and surveillance. 3. Surveillance sensitivity was estimated as 66% (95% Confidence Interval: 63.1, 68.8%) and 59.5% (95% Confidence Interval: 56.5%, 62.4%) for two monitoring methods (weekly count and prevalence thresholds, respectively), but differences among calendar quarters in outbreak size and surveillance sensitivity suggest seasonal effects. 4. We determined that a weekly detection threshold of ≥2 chimpanzees with clinical respiratory disease leading to outbreak response protocols (enhanced observation and biological sampling) is an optimal algorithm for outbreak detection in this population. 5. Synthesis and applications. This is the first quantitative assessment of syndromic surveillance in wildlife, providing a model approach to detecting disease emergence. Coupling syndromic surveillance with targeted diagnostic sampling in the midst of suspected outbreaks will provide a powerful system for detecting disease transmission and understanding population impacts.

Social tipping points in animal societies.

Animal social groups are complex systems that are likely to exhibit tipping points-which are defined as drastic shifts in the dynamics of systems that arise from small changes in environmental conditions-yet this concept has not been carefully applied to these systems. Here, we summarize the concepts behind tipping points and describe instances in which they are likely to occur in animal societies. We also offer ways in which the study of social tipping points can open up new lines of inquiry in behavioural ecology and generate novel questions, methods, and approaches in animal behaviour and other fields, including community and ecosystem ecology. While some behaviours of living systems are hard to predict, we argue that probing tipping points across animal societies and across tiers of biological organization-populations, communities, ecosystems-may help to reveal principles that transcend traditional disciplinary boundaries.

The timing and causes of a unique chimpanzee community fission preceding Gombe's "Four-Year War".

OBJECTIVES: While permanent group fissions are documented in humans and other primate species, they are relatively rare in male philopatric primates. One of the few apparent cases occurred in 1973 in Gombe National Park, Tanzania, when a community of chimpanzees split into two separate groups, preceding the famous "Four-Year War." We tested the hypothesis that the original group was a single cohesive community that experienced permanent fission, and investigated several potential catalysts. MATERIALS AND METHODS: We calculated association, grooming, and ranging metrics from historical data and used community detection algorithms and matrix permutation tests to determine the timing, dynamics, and causes of changes in social network subgrouping structure. RESULTS: We found that the two communities indeed split from one cohesive community, albeit one with incipient subgrouping. The degree of subgrouping in grooming and association networks increased sharply in 1971 and 1972, a period characterized by a dominance struggle between three high-ranking males and unusually high male:female sex ratios. Finally, we found a relationship between post-split community membership and previous association, grooming and ranging patterns in most periods of analysis, one that became more pronounced as the fission approached. DISCUSSION: Our analysis suggests that the community began to split during a time of an unusually male-biased sex ratio and a protracted dominance struggle, and that adult males remained with those with whom they had preferentially associated prior to the split. We discuss the costs and benefits of group membership in chimpanzees and contrast these results with group fissions in humans and other taxa.

Socioecological correlates of clinical signs in two communities of wild chimpanzees (Pan troglodytes) at Gombe National Park, Tanzania.

Disease and other health hazards pose serious threats to the persistence of wild ape populations. The total chimpanzee population at Gombe National Park, Tanzania, has declined from an estimated 120 to 150 individuals in the 1960's to around 100 individuals by the end of 2013, with death associated with observable signs of disease as the leading cause of mortality. In 2004, we began a non-invasive health-monitoring program in the two habituated communities in the park (Kasekela and Mitumba) with the aim of understanding the prevalence of health issues in the population, and identifying the presence and impacts of various pathogens. Here we present prospectively collected data on clinical signs (observable changes in health) in the chimpanzees of the Kasekela (n = 81) and Mitumba (n = 32) communities over an 8-year period (2005-2012). First, we take a population approach and analyze prevalence of clinical signs in five different categories: gastrointestinal system (diarrhea), body condition (estimated weight loss), respiratory system (coughing, sneezing etc.), wounds/lameness, and dermatologic issues by year, month, and community membership. Mean monthly prevalence of each clinical sign per community varied, but typically affected <10% of observed individuals. Secondly, we analyze the presence of clinical signs in these categories as they relate to individual demographic and social factors (age, sex, and dominance rank) and simian immunodeficiency virus (SIVcpz) infection status. Adults have higher odds of being observed with diarrhea, loss of body condition, and wounds or lameness when compared to immatures, while males have a higher probability of being observed with wounds or lameness than females. In contrast, signs of respiratory illness appear not to be related to chimpanzee-specific factors and skin abnormalities are very rare. For a subset of known-rank individuals, dominance rank predicts the probability of wounding/lameness in adult males, but does not predict any adverse clinical signs in adult females. Instead, adult females with SIVcpz infection are more likely to be observed with diarrhea, a finding that warrants further investigation. Comparable data are needed from other sites to determine whether the prevalence of clinical signs we observe are relatively high or low, as well as to more fully understand the factors influencing health of wild apes at both the population and individual level. Am. J. Primatol. 80:e22562, 2018. © 2016 Wiley Periodicals, Inc.

Predation by female chimpanzees: Toward an understanding of sex differences in meat acquisition in the last common ancestor of Pan and Homo.

Among modern foraging societies, men hunt more than women, who mostly target relatively low-quality, reliable resources (i.e., plants). This difference has long been assumed to reflect human female reproductive constraints, particularly caring for and provisioning mates and offspring. Long-term studies of chimpanzees (Pan troglodytes) enable tests of hypotheses about the possible origins of human sex differences in hunting, prior to pair-bonding and regular provisioning. We studied two eastern chimpanzee communities (Kasekela, Mitumba) in Gombe, Tanzania and one (Kanyawara) in Kibale, Uganda. Relative to males, females had low hunting rates in all three communities, even where they encountered red colobus monkeys (the primary prey of chimpanzees) as often as males did. There was no evidence that clinging offspring hampered female hunting. Instead, consistent with the hypothesis that females should be more risk-averse than males, females at all three sites specialized in low-cost prey (terrestrial/sedentary prey at Gombe; black and white colobus monkeys at Kanyawara). Female dominance rank was positively correlated with red colobus hunting probability only at Kasekela, suggesting that those in good physical condition were less sensitive to the costs of possible failure. Finally, the potential for carcass appropriation by males deterred females at Kasekela (but not Kanyawara or Mitumba) from hunting in parties containing many adult males. Although chimpanzees are not direct analogs of the last common ancestor (LCA) of Pan and Homo, these results suggest that before the emergence of social obligations regarding sharing and provisioning, constraints on hunting by LCA females did not necessarily stem from maternal care. Instead, they suggest that a risk-averse foraging strategy and the potential for losing prey to males limited female predation on vertebrates. Sex differences in hunting behavior would likely have preceded the evolution of the sexual division of labor among modern humans.

Reflections of the social environment in chimpanzee memory: applying rational analysis beyond humans.

In cognitive science, the rational analysis framework allows modelling of how physical and social environments impose information-processing demands onto cognitive systems. In humans, for example, past social contact among individuals predicts their future contact with linear and power functions. These features of the human environment constrain the optimal way to remember information and probably shape how memory records are retained and retrieved. We offer a primer on how biologists can apply rational analysis to study animal behaviour. Using chimpanzees (Pan troglodytes) as a case study, we modelled 19 years of observational data on their social contact patterns. Much like humans, the frequency of past encounters in chimpanzees linearly predicted future encounters, and the recency of past encounters predicted future encounters with a power function. Consistent with the rational analyses carried out for human memory, these findings suggest that chimpanzee memory performance should reflect those environmental regularities. In re-analysing existing chimpanzee memory data, we found that chimpanzee memory patterns mirrored their social contact patterns. Our findings hint that human and chimpanzee memory systems may have evolved to solve similar information-processing problems. Overall, rational analysis offers novel theoretical and methodological avenues for the comparative study of cognition.

Transparency, usability, and reproducibility: Guiding principles for improving comparative databases using primates as examples.

Recent decades have seen rapid development of new analytical methods to investigate patterns of interspecific variation. Yet these cutting-edge statistical analyses often rely on data of questionable origin, varying accuracy, and weak comparability, which seem to have reduced the reproducibility of studies. It is time to improve the transparency of comparative data while also making these improved data more widely available. We, the authors, met to discuss how transparency, usability, and reproducibility of comparative data can best be achieved. We propose four guiding principles: 1) data identification with explicit operational definitions and complete descriptions of methods; 2) inclusion of metadata that capture key characteristics of the data, such as sample size, geographic coordinates, and nutrient availability (for example, captive versus wild animals); 3) documentation of the original reference for each datum; and 4) facilitation of effective interactions with the data via user friendly and transparent interfaces. We urge reviewers, editors, publishers, database developers and users, funding agencies, researchers publishing their primary data, and those performing comparative analyses to embrace these standards to increase the transparency, usability, and reproducibility of comparative studies.

Chimpanzee females queue but males compete for social status.

Dominance hierarchies are widespread in animal social groups and often have measureable effects on individual health and reproductive success. Dominance ranks are not static individual attributes, however, but instead are influenced by two independent processes: 1) changes in hierarchy membership and 2) successful challenges of higher-ranking individuals. Understanding which of these processes dominates the dynamics of rank trajectories can provide insights into fitness benefits of within-sex competition. This question has yet to be examined systematically in a wide range of taxa due to the scarcity of long-term data and a lack of appropriate methodologies for distinguishing between alternative causes of rank changes over time. Here, we expand on recent work and develop a new likelihood-based Elo rating method that facilitates the systematic assessment of rank dynamics in animal social groups, even when interaction data are sparse. We apply this method to characterize long-term rank trajectories in wild eastern chimpanzees (Pan troglodytes schweinfurthii) and find remarkable sex differences in rank dynamics, indicating that females queue for social status while males actively challenge each other to rise in rank. Further, our results suggest that natal females obtain a head start in the rank queue if they avoid dispersal, with potential fitness benefits.

Reproductive state and rank influence patterns of meat consumption in wild female chimpanzees (Pan troglodytes schweinfurthii).

An increase in faunivory is a consistent component of human evolutionary models. Animal matter is energy- and nutrient-dense and can provide macronutrients, minerals, and vitamins that are limited or absent in plant foods. For female humans and other omnivorous primates, faunivory may be of particular importance during the costly periods of pregnancy and early lactation. Yet, because animal prey is often monopolizable, access to fauna among group-living primates may be mediated by social factors such as rank. Wild chimpanzees (Pan troglodytes) across Africa habitually consume insects and/or vertebrates. However, no published studies have examined patterns of female chimpanzee faunivory during pregnancy and early lactation relative to non-reproductive periods, or by females of different rank. In this study, we assessed the influence of reproductive state and dominance rank on the consumption of fauna (meat and insects) by female chimpanzees of Gombe National Park, Tanzania. Using observational data collected over 38 years, we tested (a) whether faunivory varied by reproductive state, and (b) if high-ranking females spent more time consuming fauna than lower-ranking females. In single-factor models, pregnant females consumed more meat than lactating and baseline (meaning not pregnant and not in early lactation) females, and high-ranking females consumed more meat than lower-ranking females. A two-factor analysis of a subset of well-sampled females identified an interaction between rank and reproductive state: lower-ranking females consumed more meat during pregnancy than lower-ranking lactating and baseline females did. High-ranking females did not significantly differ in meat consumption between reproductive states. We found no relationships between rank or reproductive state with insectivory. We conclude that, unlike insectivory, meat consumption by female chimpanzees is mediated by both reproductive state and social rank. We outline possible mechanisms for these patterns, relate our findings to meat-eating patterns in women from well-studied hunter-gatherer societies, and discuss potential avenues for future research.

Incomplete control and concessions explain mating skew in male chimpanzees.

Sexual selection theory predicts that because male reproductive success in mammals is limited by access to females, males will attempt to defend access to mates and exclude rivals from mating. In mammals, dominance rank is correlated with male reproductive success; however, the highest-ranking (alpha) male rarely monopolizes reproduction completely. To explain why, incomplete control models propose that alpha males simply cannot control other males' access to mates. If true, then dominance rank should be a key factor influencing subordinate (non-alpha) male mating success. Alternatively, the concession model states that alpha males can prevent other males from gaining access to mates but posits that they concede matings to subordinates in exchange for social favours. This predicts that a male's grooming interactions with the alpha should mediate his access to females. We test these predictions using 36 years of data, encompassing the tenures of eight alpha male chimpanzees at Gombe National Park, Tanzania. Incomplete control models were most strongly supported. At a given copulation event, the probability that the alpha was the male that mated was negatively associated with the number of males and sexually receptive females in the party. Additionally, as the number of males increased, high dominance rank was associated with an increased likelihood that a particular non-alpha male mated. The concession model, however, was also supported. The amount of time a male spent grooming with the alpha was positively associated with his likelihood of mating when the alpha was present in the party. As grooming is a major affiliative component of male social relationships, our results suggest that social bonds with dominant individuals are leveraged for mating access, particularly in species in which males form coalitions.

'Impact hunters' catalyse cooperative hunting in two wild chimpanzee communities.

Even when hunting in groups is mutually beneficial, it is unclear how communal hunts are initiated. If it is costly to be the only hunter, individuals should be reluctant to hunt unless others already are. We used 70 years of data from three communities to examine how male chimpanzees 'solve' this apparent collective action problem. The 'impact hunter' hypothesis proposes that group hunts are sometimes catalysed by certain individuals that hunt more readily than others. In two communities (Kasekela and Kanyawara), we identified a total of five males that exhibited high hunt participation rates for their age, and whose presence at an encounter with red colobus monkeys increased group hunting probability. Critically, these impact hunters were observed to hunt first more often than expected by chance. We argue that by hunting first, these males dilute prey defences and create opportunities for previously reluctant participants. This by-product mutualism can explain variation in group hunting rates within and between social groups. Hunting rates declined after the death of impact hunter FG in Kasekela and after impact hunter MS stopped hunting frequently in Kanyawara. There were no impact hunters in the third, smaller community (Mitumba), where, unlike the others, hunting probability increased with the number of females present at an encounter with prey.

Social bonds in the dispersing sex: partner preferences among adult female chimpanzees.

In most primate societies, strong and enduring social bonds form preferentially among kin, who benefit from cooperation through direct and indirect fitness gains. Chimpanzees, Pan troglodytes, differ from most species by showing consistent female-biased dispersal and strict male philopatry. In most East African populations, females tend to forage alone in small core areas and were long thought to have weak social bonds of little biological significance. Recent work in some populations is challenging this view. However, challenges remain in quantifying the influence of shared space use on association patterns, and in identifying the drivers of partner preferences and social bonds. Here, we use the largest data set on wild chimpanzee behaviour currently available to assess potential determinants of female association patterns. We quantify pairwise similarities in ranging, dyadic association and grooming for 624 unique dyads over 38 years, including 17 adult female kin dyads. To search for social preferences that could not be explained by spatial overlap alone, we controlled for expected association based on pairwise kernel volume intersections of core areas. We found that association frequencies among females with above-average overlap correlated positively with grooming rates, suggesting that associations reflected social preferences in these dyads. Furthermore, when available, females preferred kin over nonkin partners for association and grooming, and variability was high among nonkin dyads. While variability in association above and below expected values was high, on average, nonkin associated more frequently if they had immature male offspring, while having female offspring had the opposite effect. Dominance rank, an important determinant of reproductive success at Gombe, influenced associations primarily for low-ranking females, who associated preferentially with each other. Our findings support the hypothesis that female chimpanzees form well-differentiated social relationships that are of potential adaptive value to females and their offspring.

Sexually coercive male chimpanzees sire more offspring.

In sexually reproducing animals, male and female reproductive strategies often conflict. In some species, males use aggression to overcome female choice, but debate persists over the extent to which this strategy is successful. Previous studies of male aggression toward females among wild chimpanzees have yielded contradictory results about the relationship between aggression and mating behavior. Critically, however, copulation frequency in primates is not always predictive of reproductive success. We analyzed a 17-year sample of behavioral and genetic data from the Kasekela chimpanzee (Pan troglodytes schweinfurthii) community in Gombe National Park, Tanzania, to test the hypothesis that male aggression toward females increases male reproductive success. We examined the effect of male aggression toward females during ovarian cycling, including periods when the females were sexually receptive (swollen) and periods when they were not. We found that, after controlling for confounding factors, male aggression during a female's swollen periods was positively correlated with copulation frequency. However, aggression toward swollen females was not predictive of paternity. Instead, aggression by high-ranking males toward females during their nonswollen periods was positively associated with likelihood of paternity. This indicates that long-term patterns of intimidation allow high-ranking males to increase their reproductive success, supporting the sexual coercion hypothesis. To our knowledge, this is the first study to present genetic evidence of sexual coercion as an adaptive strategy in a social mammal.