Social bonds provide multiple pathways to reproductive success in wild male chimpanzees.
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ABSTRACT:
SUBMITTER: Feldblum JT
PROVIDER: S-EPMC8390850 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Between-group competition in social animals appears to be a prominent selective pressure shaping the evolution of territoriality and cooperation [1-4]. Evidence for an effect of between-group competition on fitness in territorial species, however, is mostly lacking because of difficulty in measuring between-group competition and its long-term impact [5]. Between-group competition corresponds to a complex set of interactions between neighboring groups, and its intensity seems to depend on the competitive abilities of each interacting group [6, 7]. We tested whether the competitive ability of groups and the pressure exerted by neighboring groups affected the reproductive success of wild female chimpanzees (Pan troglodytes verus). Using long-term data on four neighboring groups in the Taï National Park, Côte d'Ivoire, collected over the course of 54 observation years, we measured the competitive ability of habituated groups using the number of mature males and the pressure exerted by non-habituated neighbors with an index of neighbor pressure that combined the frequency of neighboring encounters and related spatial information. Importantly, we found that experiencing low neighbor pressure provides fitness benefits through increased offspring survival and shorter inter-birth intervals. Also, many males in a group are associated with shorter inter-birth intervals. We conclude that high between-group competition hampers fast reproduction and offspring survival when exposure is during the prenatal period. Our findings suggest that having many males in a group results in fitness benefits and that between-group competition should be considered as a potential selective pressure that shaped key social adaptations in the hominoid lineage.
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Project description:Why share when access to benefits is uncertain is crucial to our understanding of the evolution of humans' extensive cooperation. Here, we investigated some of the different human sharing hypotheses and potential neuroendocrine mechanisms, in one of our closest living relatives, chimpanzees. The strongest predictor of sharing across food types was the presence of enduring and mutually preferred grooming partners, more than harassment, direct signalling, or trade. Moreover, urinary oxytocin levels were higher after the sharing of both individually and jointly acquired resources compared with controls. We conclude that the emotional connection inherent in social bonds was a key factor determining sharing patterns, with the oxytocinergic system potentially facilitating long-term cooperative exchanges. Testing for the role of social bonds in increasing predictability of sharing behaviour, a feature frequently overlooked, may help us to identify the evolutionary drivers of resource sharing and mechanisms that sustain delayed reciprocity between non-kin.
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Project description:Primates form strong and enduring social bonds with others and these bonds have important fitness consequences. However, how different types of communication are associated with different types of social bonds is poorly understood. Wild chimpanzees have a large repertoire of gestures, from visual gestures to tactile and auditory gestures. We used social network analysis to examine the association between proximity bonds (time spent in close proximity) and rates of gestural communication in pairs of chimpanzees when the intended recipient was within 10 m of the signaller. Pairs of chimpanzees with strong proximity bonds had higher rates of visual gestures, but lower rates of auditory long-range and tactile gestures. However, individual chimpanzees that had a larger number of proximity bonds had higher rates of auditory and tactile gestures and lower rates of visual gestures. These results suggest that visual gestures may be an efficient way to communicate with a small number of regular interaction partners, but that tactile and auditory gestures may be more effective at communicating with larger numbers of weaker bonds. Increasing flexibility of communication may have played an important role in managing differentiated social relationships in groups of increasing size and complexity in both primate and human evolution.
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Project description:While individual variation in social behaviour is ubiquitous and causes social groups to differ in structure, how these structural differences affect fitness remains largely unknown. We used social network analysis of replicate bluebanded goby (Lythrypnus dalli) harems to identify the reproductive correlates of social network structure. In stable groups, we quantified agonistic behaviour, reproduction and steroid hormones, which can both affect and respond to social/reproductive cues. We identified distinct, optimal social structures associated with different reproductive measures. Male hatching success (HS) was negatively associated with agonistic reciprocity, a network structure that describes whether subordinates 'reciprocated' agonism received from dominants. Egg laying was associated with the individual network positions of the male and dominant female. Thus, males face a trade-off between promoting structures that facilitate egg laying versus HS. Whether this reproductive conflict is avoidable remains to be determined. We also identified different social and/or reproductive roles for 11-ketotestosterone, 17β-oestradiol and cortisol, suggesting that specific neuroendocrine mechanisms may underlie connections between network structure and fitness. This is one of the first investigations of the reproductive and neuroendocrine correlates of social behaviour and network structure in replicate, naturalistic social groups and supports network structure as an important target for natural selection.
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Project description:Cooperative hunting and meat sharing are hypothesized as fundamental to human life history adaptations and biological success. Wild chimpanzees also hunt in groups, and despite the potential of inferring ancestral hominid adaptations, it remains unclear whether chimpanzee hunting is a cooperative act. Here we show support for cooperative acquisition in wild chimpanzees since hunters are more likely to receive meat than bystanders, independent of begging effort. Engagement in prey searches and higher hunt participation independently increase hunting success, suggesting that coordination may improve motivation in joint tasks. We also find higher levels of urinary oxytocin after hunts and prey searches compared with controls. We conclude that chimpanzee hunting is cooperative, likely facilitated by behavioral and neuroendocrine mechanisms of coordination and reward. If group hunting has shaped humans' life history traits, perhaps similar pressures acted upon life history patterns in the last common ancestor of human and chimpanzee.
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Project description:Social relationships play an important role in animal behavior. Bonds with kin provide indirect fitness benefits, and those with nonkin may furnish direct benefits. Adult male chimpanzees (Pan troglodytes) exhibit social bonds with maternal brothers as well as unrelated adult males, facilitating cooperative behavior, but it is unclear when these bonds develop. Prior studies suggest that social bonds emerge during adolescence. Alternatively, bonds may develop during adulthood when male chimpanzees can gain fitness benefits through alliances used to compete for dominance status. To investigate these possibilities and to determine who formed bonds, we studied the social relationships of adolescent and young adult male chimpanzees (N = 18) at Ngogo in Kibale National Park, Uganda. Adolescent male chimpanzees displayed social bonds with other males, and they did so as often as did young adult males. Adolescent and young adult males frequently joined subgroups with old males. They spent time in proximity to and grooming with old males, although they also did so with their age peers. Controlling for age and age difference, males formed strong association and proximity relationships with their maternal brothers and grooming relationships with their fathers. Grooming bonds between chimpanzee fathers and their adolescent and young adult sons have not been documented before and are unexpected because female chimpanzees mate with multiple males. How fathers recognize their sons and vice versa remains unclear but may be due to familiarity created by relationships earlier in development.
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Project description:Infrared thermal imaging has emerged as a valuable tool in veterinary medicine, in particular for evaluating reproductive processes. Here, we explored differences in skin temperature of twenty female chimpanzees in Budongo Forest, Uganda, four of which were pregnant during data collection. Based on previous literature in other mammals, we predicted increased skin temperature of maximally swollen reproductive organs of non-pregnant females when approaching peak fertility. For pregnant females, we made the same prediction because it has been argued that female chimpanzees have evolved mechanisms to conceal pregnancy, including swellings of the reproductive organs, conspicuous copulation calling, and solicitation of male mating behaviour, to decrease the infanticidal tendencies of resident males by confusing paternity. For non-pregnant females, we found slight temperature increases towards the end of the swelling cycles but no significant change between the fertile and non-fertile phases. Despite their different reproductive state, pregnant females had very similar skin temperature patterns compared to non-pregnant females, suggesting little potential for males to use skin temperature to recognise pregnancies, especially during maximal swelling, when ovulation is most likely to occur in non-pregnant females. We discuss this pattern in light of the concealment hypothesis, i.e., that female chimpanzees have evolved physiological means to conceal their reproductive state during pregnancy.
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Project description:The two closest living relatives of humans, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes), share many traits that are common in humans but rare in other mammals, including societies with high fission-fusion dynamics, male philopatry, female dispersal and extensive social bonding among unrelated individuals [1]. The major difference between these two species is that male aggression is more frequent and intense in male-dominated chimpanzees than in bonobos, where the highest-ranking individuals are female [1]. One potential explanation is that because periods of female sexual receptivity and attractiveness are more extended in bonobos [2], males compete less intensely for each mating opportunity. This would reduce the strength of selection for traits that lead to success in direct contest competition between males and in sexual coercion of females, thus increasing the potential for female choice [3]. Accordingly, it has been predicted that the influence of male dominance rank on reproductive success and the extent of male reproductive skew should be lower in bonobos than in chimpanzees [1]. Although relevant for understanding the evolution of the unusual levels of egalitarianism and cooperation found in human hunter-gatherers [4], comparative analyses in the genus Pan have been limited by the scanty paternity data available for wild bonobos [5]. Here, we show using the largest sample of paternity data available that, contrary to expectation, male bonobos have a higher reproductive skew and a stronger relationship between dominance rank and reproductive success than chimpanzees.
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