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Abstract Proposed mechanisms of zoonotic virus spillover often posit that wildlife transmission and amplification precede human outbreaks. Between 2006 and 2012, the palm Raphia farinifera, a rich source of dietary minerals for wildlife, was nearly extirpated from Budongo Forest, Uganda. Since then, chimpanzees, black-and-white colobus, and red duiker were observed feeding on bat guano, a behavior not previously observed. Here we show that guano consumption may be a response to dietary mineral scarcity and may expose wildlife to bat-borne viruses. Videos from 2017–2019 recorded 839 instances of guano consumption by the aforementioned species. Nutritional analysis of the guano revealed high concentrations of sodium, potassium, magnesium and phosphorus. Metagenomic analyses of the guano identified 27 eukaryotic viruses, including a novel betacoronavirus. Our findings illustrate how “upstream” drivers such as socioeconomics and resource extraction can initiate elaborate chains of causation, ultimately increasing virus spillover risk.

Abstract The selection pressures that drove dramatic encephalisation processes through the mammal lineage remain elusive, as does knowledge of brain structure reorganisation through this process. In particular, considerable structural brain changes are present across the primate lineage, culminating in the complex human brain that allows for unique behaviours such as language and sophisticated tool use. To understand this evolution, a diverse sample set of humans' closest relatives with varying socio‐ecologies is needed. However, current brain banks predominantly curate brains from primates that died in zoological gardens. We try to address this gap by establishing a field pipeline mitigating the challenges associated with brain extractions of wild primates in their natural habitat. The success of our approach is demonstrated by our ability to acquire a novel brain sample of deceased primates with highly variable socio‐ecological exposure and a particular focus on wild chimpanzees. Methods in acquiring brain tissue from wild settings are comprehensively explained, highlighting the feasibility of conducting brain extraction procedures under strict biosafety measures by trained veterinarians in field sites. Brains are assessed at a fine‐structural level via high‐resolution MRI and state‐of‐the‐art histology. Analyses confirm that excellent tissue quality of primate brains sourced in the field can be achieved with a comparable tissue quality of brains acquired from zoo‐living primates. Our field methods are noninvasive, here defined as not harming living animals, and may be applied to other mammal systems than primates. In sum, the field protocol and methodological pipeline validated here pose a major advance for assessing the influence of socio‐ecology on medium to large mammal brains, at both macro‐ and microstructural levels as well as aiding with the functional annotation of brain regions and neuronal pathways via specific behaviour assessments.

To decipher the evolution of the hominoid brain and its functions, it is essential to conduct comparative studies in primates, including our closest living relatives. However, strong ethical concerns preclude in vivo neuroimaging of great apes. We propose a responsible and multidisciplinary alternative approach that links behavior to brain anatomy in non-human primates from diverse ecological backgrounds. The brains of primates observed in the wild or in captivity are extracted and fixed shortly after natural death, and then studied using advanced MRI neuroimaging and histology to reveal macro- and microstructures. By linking detailed neuroanatomy with observed behavior within and across primate species, our approach provides new perspectives on brain evolution. Combined with endocranial brain imprints extracted from computed tomographic scans of the skulls these data provide a framework for decoding evolutionary changes in hominin fossils. This approach is poised to become a key resource for investigating the evolution and functional differentiation of hominoid brains.

Abstract Mechanisms of inheritance remain poorly defined for many fitness-mediating traits, especially in long-lived animals with protracted development. Using 6,123 urinary samples from 170 wild chimpanzees, we examined the contributions of genetics, non-genetic maternal effects, and shared community effects on variation in cortisol levels, an established predictor of survival in long-lived primates. Despite evidence for consistent individual variation in cortisol levels across years, between-group effects were more influential and made an overwhelming contribution to variation in this trait. Focusing on within-group variation, non-genetic maternal effects accounted for 8% of the individual differences in average cortisol levels, significantly more than that attributable to genetic factors, which was indistinguishable from zero. These maternal effects are consistent with a primary role of a shared environment in shaping physiology. For chimpanzees, and perhaps other species with long life histories, community and maternal effects appear more relevant than genetic inheritance in shaping key physiological traits.

The social complexity hypothesis for the evolution of communication posits that complex social environments require greater communication complexity for individuals to effectively manage their relationships. We examined how different socially uncertain contexts, reflecting an increased level of social complexity, relate to variation in signalling within and between two species, which display varying levels of fission–fusion dynamics (sympatric-living chimpanzees and sooty mangabeys, Taï National Park, Ivory Coast). Combined signalling may improve message efficacy, notably when involving different perception channels, thus may increase in moments of high social uncertainty. We examined the probability of individuals to emit no signal, single or multisensory or combined (complex) signals, during social approaches which resulted in non-agonistic outcomes. In both species, individuals were more likely to use more combined and multisensory signals in post-conflict approaches with an opponent than in other contexts. The clearest impact of social uncertainty on signalling complexity was observed during chimpanzee fusions, where the likelihood of using complex signals tripled relative to other contexts. Overall, chimpanzees used more multisensory signals than mangabeys. Social uncertainty may shape detected species differences in variation in signalling complexity, thereby supporting the hypothesis that social complexity, particularly associated with high fission–fusion dynamics, promotes signalling complexity.

Summary: One universal feature of human language is its versatility in communicating about juxtapositions of everyday events. Versatile combinatorial systems of communication can be selected for if (a) several vocal units are flexibly combined into numerous and long vocal sequences and (b) vocal sequences relate to numerous daily life events. We propose (b) is more likely during simultaneous or serial (concomitant) events than single events. We analyzed 9,391 vocal utterances across the repertoire of wild chimpanzees and their events of production. Chimpanzees used vocal sequences across a range of daily life events and twice as often during concomitant than single events. Also, utterance diversity correlated positively with event diversity. Our results show the potential of chimpanzee vocal sequences to convey combined information about numerous daily life events, a step from which generalized combinatoriality could have evolved.

Uncovering brain-tissue microstructure including axonal characteristics is a major neuroimaging research focus. Within this scope, anisotropic properties of magnetic susceptibility in white matter have been successfully employed to estimate primary axonal trajectories using mono-tensorial models. However, anisotropic susceptibility has not yet been considered for modeling more complex fiber structures within a voxel, such as intersecting bundles, or an estimation of orientation distribution functions (ODFs). This information is routinely obtained by high angular resolution diffusion imaging (HARDI) techniques. In applications to fixed tissue, however, diffusion-weighted imaging suffers from an inherently low signal-to-noise ratio and limited spatial resolution, leading to high demands on the performance of the gradient system in order to mitigate these limitations. In the current work, high angular resolution susceptibility imaging (HARSI) is proposed as a novel, phase-based methodology to estimate ODFs. A multiple gradient-echo dataset was acquired in an entire fixed chimpanzee brain at 61 orientations by reorienting the specimen in the magnetic field. The constant solid angle method was adapted for estimating phase-based ODFs. HARDI data were also acquired for comparison. HARSI yielded information on whole-brain fiber architecture, including identification of peaks of multiple bundles that resembled features of the HARDI results. Distinct differences between both methods suggest that susceptibility properties may offer complementary microstructural information. These proof-of-concept results indicate a potential to study the axonal organization in post-mortem primate and human brain at high resolution.

An analysis of the structural complexity of vocal sequences in chimpanzees in the Taï National Park reveal that single vocal units are combined into numerous structured sequences with adjacency dependencies between units.

Surbeck and colleagues investigate the proximate drivers of female gregariousness in bonobos and chimpanzees across different observed communities. Their findings indicate that varied levels of sexual signalling in these two species result in different social behaviours regarding female grouping and potentially cooperation.

Summary: Early-life experiences, such as maternal care received, influence adult social integration and survival. We examine what changes to social behavior through ontogeny lead to these lifelong effects, particularly whether early-life maternal environment impacts the development of social communication. Chimpanzees experience prolonged social communication development. Focusing on a central communicative trait, the “pant-hoot” contact call used to solicit social engagement, we collected cross-sectional data on wild chimpanzees (52 immatures and 36 mothers). We assessed early-life socioecological impacts on pant-hoot rates across development, specifically: mothers’ gregariousness, age, pant-hoot rates and dominance rank, maternal loss, and food availability, controlling for current maternal effects. We found that early-life maternal gregariousness correlated positively with offspring pant-hoot rates, while maternal loss led to reduced pant-hoot rates across development. Males had steeper developmental trajectories in pant-hoot rates than females. We demonstrate the impact of maternal effects on developmental trajectories of a rarely investigated social trait, vocal production.

Summary: Primates rarely learn new vocalizations, but they can learn to use their vocalizations in different contexts. Such “vocal usage learning,” particularly in vocal sequences, is a hallmark of human language, but remains understudied in non-human primates. We assess usage learning in four wild chimpanzee communities of Taï and Budongo Forests by investigating population differences in call ordering of a greeting vocal sequence. Whilst in all groups, these sequences consisted of pant-hoots (long-distance contact call) and pant-grunts (short-distance submissive call), the order of the two calls differed across populations. Taï chimpanzees consistently commenced greetings with pant-hoots, whereas Budongo chimpanzees started with pant-grunts. We discuss different hypotheses to explain this pattern and conclude that higher intra-group aggression in Budongo may have led to a local pattern of individuals signaling submission first. This highlights how within-species variation in social dynamics may lead to flexibility in call order production, possibly acquired via usage learning.

Summary: How do animals learn to classify the world and what is the role of social learning during this process? Here, we show that young sooty mangabeys, Cercocebus atys, of Taï Forest, Côte d’Ivoire, learn to rapidly classify an unfamiliar predator by attending to others’ alarm calls and that such knowledge is retained over long periods. We experimentally exposed subjects to chimeric predator models with both snake- and leopard-like features, combined with playbacks of conspecific snake (N = 12) or leopard alarms (N = 13). Adults classified the chimeras as non-threatening but for juveniles, we found that one single alarm call exposure was sufficient to allocate the chimera to the snake or leopard category, suggesting plausibility judgments in experienced adults. We then retested N = 10 juveniles with the same models more than a year after their first experience and found that they continued to show their original response, indicating long-term retention of socially learned predator categorisation.

Mirror self-recognition (MSR) is considered an indicator of self-awareness. Standardized mirror tests reveal compelling evidence for MSR in a few non-human species, including all great apes. However, substantial inter-individual variation of MSR within species resulted in an ongoing methodological controversy, questioning the appropriateness of standard MSR tests for cross-species comparisons. Lack of motivation, in particular, is discussed as one possible cause for false negative results. Here, we compare the spontaneous behavioral response of 47 zoo-housed chimpanzees (Pan troglodytes) to (i) standard body-sized, stationary mirrors and (ii) small, portable hand mirrors. We predicted that the monopolizability and maneuverability of small mirrors increase the chances of identifying MSR across a larger proportion of individuals. Chimpanzees both revealed a substantially higher frequency of general mirror-related behaviors and engaged in significantly more and longer behaviors specifically indicating MSR when provided with small mirrors compared to a large mirror. Handheld mirrors provide a more sensitive measure for MSR within and likely between primate species than the traditional large mirrors, and thereby are a potentially valuable tool for studying self-awareness across species.

The ‘invariant rate of ageing’ hypothesis suggests that the rate of ageing tends to be constant within species. Here, Colchero et al. find support for the hypothesis across primates, including humans, suggesting biological constraints on the rate of ageing.

Strong social bonds are known to affect pairwise cooperation in primates such chimpanzees. Here, Samuni et al. show that strong social bonds also influence participation in group-level cooperation (collective action in intergroup encounters) using a long-term dataset of wild chimpanzees.

Abstract Background In animals with altricial offspring, most growth occurs after birth and may be optimized by post-natal maternal care. Maternal effects on growth may be influenced by individual characteristics of the mothers, such as social status, individual investment strategies and the length of association with offspring. The prolonged juvenile dependence seen in humans is a distinctive life history adaptation, which may have evolved to facilitate sustained somatic and brain growth. In chimpanzees, offspring are typically weaned at approximately 4 years old, yet immature individuals continue to associate with their mothers for up to 10 years beyond weaning. Whether this lengthy association or the individual characteristics of mothers influences growth patterns in this species is not clear. The relationship between urinary creatinine and specific gravity is an established non-invasive measure of muscle mass in humans and chimpanzees. We analysed the urinary creatinine and specific gravity of 1318 urine samples from 70 wild chimpanzees from the Taï Forest, Ivory Coast aged 4 to 15 years. Results We showed a clear increase in urinary creatinine levels with age in both males and females, replicating established growth curves in this species and reaffirming this measure as a reliable proxy for lean body mass. Comparing those who experience maternal loss (orphans) with non-orphan chimpanzees, maternal presence beyond weaning age and into late juvenility positively influenced offspring muscle mass throughout ontogeny such that orphans had significantly less muscle mass than age-matched non-orphans. In age-matched offspring with mothers, those with high-ranking mothers had greater muscle mass. Accounting for variation in muscle mass attributable to maternal presence, we found no effect of maternal investment (length of inter birth interval, from own birth to birth of following sibling) on offspring muscle mass. Conclusion Chimpanzee mothers have an extended and multi-faceted influence on offspring phenotypes. Our results suggest that maternal investment extends beyond lactation and into early adulthood and has clear benefits to offspring physical development. Therefore, prolonged juvenile dependence, although unique in its form in human societies, may be a trait with deeper evolutionary origins.

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.

Abstract Background Ecological immunology proposes that the optimal immune defence, and the costs coming with it, vary across environments. In environments with higher pathogen load, the immune system should experience greater challenges and, therefore, investment in maintaining it should be higher. The biomarker neopterin allows monitoring of innate immune responses, and is therefore an ideal tool to investigate the effects of ecological variables on the immune system. Here, we compared urinary neopterin levels of apparently healthy chimpanzees without acute symptoms of sickness across two environments: in captivity (22 zoos) and in the wild (two populations). Results Our results revealed that urinary neopterin levels were nearly twice as high in wild compared to captive chimpanzees, independent of chimpanzee subspecies. Conclusion We conclude that wild chimpanzees experience more frequent immune challenges in comparison to captive individuals. Therefore, wild individuals have to allocate more energy to immune function and away from reproduction and growth. Our data indicate that the generally delayed development of wild animals in comparison to captive individuals might not only be related to lower energy intake but might result from greater energy allocations to immune function. Finally, our data highlight the importance of understanding immune costs for accurate characterization of energy budgets in animals.

Predictability of social interactions can be an important measure for the social complexity of an animal group. Predictability is partially dependent on how consistent interaction patterns are over time: does the behavior on 1 day explain the behavior on another? We developed a consistency measure that serves two functions: detecting which interaction types in a dataset are so inconsistent that including them in further analyses risks introducing unexplained error; and comparatively quantifying differences in consistency within and between animal groups. We applied the consistency measure to simulated data and field data for one group of sooty mangabeys (Cercocebus atys atys) and to groups of Western chimpanzees (Pan troglodytes verus) in the Taï National Park, Côte d'Ivoire, to test its properties and compare consistency across groups. The consistency measures successfully identified interaction types whose low internal consistency would likely create analytical problems. Species-level differences in consistency were less pronounced than differences within groups: in all groups, aggression and dominance interactions were the most consistent, followed by grooming; spatial proximity at different levels was much less consistent than directed interactions. Our consistency measure can facilitate decision making of researchers wondering whether to include interaction types in their analyses or social networks and allows us to compare interaction types within and between species regarding their predictability.

Post-mortem diffusion MRI (dMRI) enables acquisitions of structural imaging data with otherwise unreachable resolutions - at the expense of longer scanning times. These data are typically acquired using highly segmented image acquisition strategies, thereby resulting in an incomplete signal decay before the MRI encoding continues. Especially in dMRI, with low signal intensities and lengthy contrast encoding, such temporal inefficiency translates into reduced image quality and longer scanning times. This study introduces Multi Echo (ME) acquisitions to dMRI on a human MRI system - a time-efficient approach, which increases SNR (Signal-to-Noise Ratio) and reduces noise bias for dMRI images. The benefit of the introduced ME-dMRI method was validated using numerical Monte Carlo simulations and showcased on a post-mortem brain of a wild chimpanzee. The proposed Maximum Likelihood Estimation echo combination results in an optimal SNR without detectable signal bias. The combined strategy comes at a small price in scanning time (here 30% additional) and leads to a substantial SNR increase (here white matter: ~ 1.6x, equivalent to 2.6 averages, grey matter: ~ 1.9x, equivalent to 3.6 averages) and a general reduction of the noise bias.

Consistent individual differences in social phenotypes have been observed in many animal species. Changes in demographics, dominance hierarchies or ecological factors, such as food availability or disease prevalence, are expected to influence decision-making processes regarding social interactions. Therefore, it should be expected that individuals show flexibility rather than stability in social behaviour over time to maximize the fitness benefits of social living. Understanding the processes that create and maintain social phenotypes requires data encompassing a range of socioecological settings and variation in intrinsic state or life-history stage or strategy. Using observational data spanning up to 19 years for some individuals, we demonstrate that multiple types of social behaviour are repeatable over the long term in wild chimpanzees, a long-lived species with complex fission–fusion societies. We controlled for temporal, ecological and demographic changes, limiting pseudo-repeatability. We conclude that chimpanzees living in natural ecological settings have relatively stable long-term social phenotypes over years that may be independent of life-history or reproductive strategies. Our results add to the growing body of the literature suggesting consistent individual differences in social tendencies are more likely the rule rather than the exception in group-living animals.

Abstract: In mammals, the excretion of cortisol can provide energy toward restoring homeostasis and is a major component of the stress response. However, chronically elevated cortisol levels also have suppressive effects on immune function. As mounting an immune response is energetically costly, sick individuals may conserve energy by exhibiting certain sickness behaviors, such as declining activity levels. Due to the complex interplay between immune function and sickness behaviors, endocrinological correlates have received growing attention in the medical community, but so far, this subject was investigated rarely. Furthermore, given the complexities of studying illnesses and immunity in natural settings, correlates of sickness behaviors have yet to be studied in non-human primates in the wild.Methods: We measured urinary cortisol levels using liquid chromatography–mass spectrometry in a group of wild habituated chimpanzees in Taï National Park, Côte d'Ivoire, before, during, and after a respiratory disease outbreak (main causative pathogen: human respiratory syncytial virus A, with coinfections of Streptococcus pneumoniae). Changes in cortisol levels were then related to urinary neopterin levels, a biomarker of immune system activation.Results: Urinary cortisol levels were found to be more than 10-fold higher during the outbreak in comparison with levels before and after the outbreak period. Increasing cortisol levels were also associated with increasing neopterin levels. Interestingly, rather atypical patterns in a diurnal decline of cortisol levels were found during infection periods, such that levels remained raised throughout the day.Conclusion: In conclusion, cortisol increase was related to cellular immune response. Our results suggest that cortisol is a mediator of infectious disease pathogenicity through its impact on the immune system and that wild chimpanzees may be facing energetic stress when sick. By monitoring immune challenges in wild-living animals, our study demonstrates that immune defenses have costs and that these costs are context-specific.

Territorial social species, including humans, compete between groups over key resources. This between-group competition has evolutionary implications on adaptations like in-group cooperation even with non-kin. An emergent property of between-group competition is group dominance. Mechanisms of group dominance in wild animal populations are difficult to study, as they require long-term data on several groups within a population. Here, using long-term data on four neighbouring groups of wild western chimpanzees, we test the hypothesis that group dominance impacts the costs and benefits of between-group competition, measured by territory size and the pressure exerted by neighbouring groups. Larger groups had larger territories and suffered less neighbour pressure compared with smaller groups. Within-group increase in the number of males led to territory increase, suggesting the role of males in territory acquisition. However, variation in territory sizes and neighbour pressure was better explained by group size. This suggests that the bisexually-bonded social system of western chimpanzees, where females participate in territorial behaviour, confers a competitive advantage to larger groups and that group dominance acts through group size in this population. Considering variation in social systems offers new insights on how group dominance acts in territorial species and its evolutionary implications on within-group cooperation.

High dominance status is associated with fitness benefits in many social mammals. Yet, attaining and maintaining a high social status often comes with elevated energetic costs. Dominance rank-related exposure to energetic and psychosocial stressors is predicted to vary depending on the type of breeding system, the means a high rank is acquired and maintained, and the stability of the dominance hierarchy. Using behavioral data and urinary cortisol levels, we investigated whether a high dominance rank is associated with elevated energetic costs in Taï male chimpanzees and whether the relationship between male dominance rank and cortisol levels varies between stable and unstable dominance periods. Additionally, we investigated potential sources of energetic and psychosocial stress linked to competition over dominance status and mating opportunities. We found that higher-ranking males gave more aggressions than lower-ranking males in stable and unstable dominance periods, but that dominance rank and urinary cortisol levels were not associated in either period. Urinary cortisol levels were higher in all males in unstable compared to stable dominance periods, whereas aggression rates showed the reversed pattern, with higher rates in stable periods. Our results indicate that dominance maintenance is not associated with elevated physiological stress for dominant Taï male chimpanzees, and that social instability exposed all males to psychosocial stress, despite lower rates of aggressive interactions. Overall, these findings suggest that male chimpanzees adjust competitive behavior to context dependent conditions, possibly by means of predictability of outcomes of social interactions, and use conflict management strategies, such as avoidance of aggression potentially diminishing the risk of escalation.

The stress-reducing effects of social bonds have been hypothesized to accrue either during stressful events or across daily affiliations. Here, Wittiget al. show that the presence of social partners reduces levels of stress hormones in wild chimpanzees beyond stressful contexts, supporting the latter hypothesis.

Investigating the repeatability of trait variation between individuals, that is the amount of individual variation in relation to overall phenotypic variation, indicates an upper level of heritability and reveals whether a given trait may be subject to selection. Labile traits are characterized by high levels of flexibility and consequently low trait repeatability is expected. Indeed, research examining glucocorticoid levels in various non-mammal species found low repeatability scores. However, mammals may be different in this respect as (i) differential maternal care early in life has the potential to prime hypothalamic-pituitary-adrenal axis functioning and (ii) allelic variation affecting hypothalamic-pituitary-adrenal axis functioning has been reported. Individuals often differ from each other in average and/or plastic labile trait expression, two aspects that can be described using a reaction norm approach. Both consistent and flexible reaction norm expression has been argued to serve adaptive purposes, depending on the stability and predictability of environmental conditions. Here, we investigated both trait and reaction norm repeatability of urinary cortisol levels in wild adult male chimpanzees. To capture the expression of the circadian urinary cortisol rhythm of individual males over time, urine samples were collected throughout the day. In total data of 30 males collected over a period of 8 years were included in the dataset. No male was sampled over the whole 8-year period however. We found minor levels of trait repeatability but considerable reaction norm repeatability. This implies a minor role of genetic or priming factors on cortisol excretion, but reveals that males differ consistently in average urinary cortisol levels and the shape of the circadian urinary cortisol rhythm. Relating these results to fitness parameters will provide answers to questions on the adaptive value of reaction norm repeatability of this labile hormonal trait in the future.

Living in permanent social groups forces animals to make decisions about when, how and with whom to interact, requiring decisions to be made that integrate multiple sources of information. Changing social environments can influence this decision-making process by constraining choice or altering the likelihood of a positive outcome. Here, we conceptualized grooming as a choice situation where an individual chooses one of a number of potential partners. Studying two wild populations of sympatric primate species, sooty mangabeys (Cercocebus atys atys) and western chimpanzees (Pan troglodytes verus), we tested what properties of potential partners influenced grooming decisions, including their relative value based on available alternatives and the social relationships of potential partners with bystanders who could observe the outcome of the decision. Across 1529 decision events, multiple partner attributes (e.g. dominance ranks, social relationship quality, reproductive state, partner sex) influenced choice. Individuals preferred to initiate grooming with partners of similar global rank, but this effect was driven by a bias towards partners with a high rank compared to other locally available options. Individuals also avoided grooming partners who had strong social relationships with at least one bystander. Results indicated flexible decision-making in grooming interactions in both species, based on a partner's value given the local social environment. Viewing partner choice as a value-based decision-making process allows researchers to compare how different species solve similar social problems.

In comparative studies of evolution of communication, the function and use of animal quiet calls have typically been understudied, despite that these signals are presumably under selection like other vocalizations, such as alarm calls. Here, we examine vocalization diversification of chimpanzee quiet ‘hoos’ produced in three contexts—travel, rest and alert—and potential pressures promoting diversification. Previous playback and observational studies have suggested that the overarching function of chimpanzee hoos is to stay in contact with others, particularly bond partners. We conducted an acoustic analysis of hoos using audio recordings from wild chimpanzees (Pan troglodytes schweinfurthii) of Budongo Forest, Uganda. We identified three acoustically distinguishable, context-specific hoo variants. Each call variant requires specific responses from receivers to avoid breaking up the social unit. We propose that callers may achieve coordination by using acoustically distinguishable calls, advertising their own behavioural intentions. We conclude that natural selection has acted towards acoustically diversifying an inconspicuous, quiet vocalization, the chimpanzee hoo. This evolutionary process may have been favoured by the fact that signallers and recipients share the same goal, to maintain social cohesion, particularly among those who regularly cooperate, suggesting that call diversification has been favoured by the demands of cooperative activities.

Grooming interactions benefit groomers, but may have negative consequences for bystanders. Grooming limits bystanders' grooming access and ensuing alliances could threaten the bystander's hierarchy rank or their previous investment in the groomers. To gain a competitive advantage, bystanders could intervene into a grooming bout to increase their own grooming access or to prevent the negative impact of others' grooming. We tested the impact of dominance rank and social relationships on grooming intervention likelihood and outcome in two sympatric primate species, Western chimpanzees (Pan troglodytes verus) and sooty mangabeys (Cercocebus atys atys). In both species, rather than increasing their own access to preferred partners, bystanders intervened mainly when an alliance between groomers could have a negative impact on them: when the lower-ranking groomer was close to the bystander in rank, when either groomer was an affiliation partner whose services they could lose, or the groomers were not yet strongly affiliated with each other. Thus, bystanders in both species appear to monitor grooming interactions and intervene based on their own dominance rank and social relationships, as well as triadic awareness of the relationship between groomers. While the motivation to intervene did not differ between species, mangabeys appeared to be more constrained by dominance rank than chimpanzees.

In several group-living species, individuals' social preferences are thought to be influenced by cooperation. For some societies with fission–fusion dynamics, sex-specific association patterns reflect sex differences in cooperation in within- and between-group contexts. In our study, we investigated this hypothesis further by comparing sex-specific association patterns in two closely related species, chimpanzees and bonobos, which differ in the level of between-group competition and in the degree to which sex and kinship influence dyadic cooperation. Here, we used long-term party composition data collected on five chimpanzee and two bonobo communities and assessed, for each individual of 10 years and older, the sex of its top associate and of all conspecifics with whom it associated more frequently than expected by chance. We found clear species differences in association patterns. While in all chimpanzee communities males and females associated more with same-sex partners, in bonobos males and females tended to associate preferentially with females, but the female association preference for other females is lower than in chimpanzees. Our results also show that, for bonobos (but not for chimpanzees), association patterns were predominantly driven by mother–offspring relationships. These species differences in association patterns reflect the high levels of male–male cooperation in chimpanzees and of mother–son cooperation in bonobos. Finally, female chimpanzees showed intense association with a few other females, and male chimpanzees showed more uniform association across males. In bonobos, the most differentiated associations were from males towards females. Chimpanzee male association patterns mirror fundamental human male social traits and, as in humans, may have evolved as a response to strong between-group competition. The lack of such a pattern in a closely related species with a lower degree of between-group competition further supports this notion.

A basic premise in behavioural ecology is the cost-benefit arithmetic, which determines both behavioural decisions and evolutionary processes. Aggressive interactions can be costly on an energetic level, demanding increased energy or causing injuries, and on a psychological level, in the form of increased anxiety and damaged relationships between opponents. Here we used urinary glucocorticoid (uGC) levels to assess the costs of aggression in wild chimpanzees of Budongo Forest, Uganda. We collected 169 urine samples from nine adult male chimpanzees following 14 aggressive interactions (test condition) and 10 resting events (control condition). Subjects showed significantly higher uGC levels after single aggressive interactions compared to control conditions, likely for aggressors as well as victims. Higher ranking males had greater increases of uGC levels after aggression than lower ranking males. In contrast, uGC levels showed no significant change in relation to aggression length or intensity, indicating that psychological factors might have played a larger role than mere energetic expenditure. We concluded that aggressive behaviour is costly for both aggressors and victims and that costs seem poorly explained by energetic demands of the interaction. Our findings are relevant for studies of post-conflict interactions, since we provide evidence that both aggressors and victims experience a stress response to conflict.