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Maternal conflict intervention is more frequent in chimpanzee compared to bonobo development
... For example, chimpanzee juveniles 87 begin facing threats from adult males soon after weaning around the age of 4 to 5 years, 88 whereas bonobos experience such threats closer to puberty around the age of 8 (Hohmann et 89 al., 2019; Kuroda, 1989). Furthermore, chimpanzee mothers in Ngogo, Uganda, have been 90 observed to actively support their offspring, intervening more frequently during infant attacks compared to bonobo mothers in Kokolopori, Democratic Republic of Congo (DRC), who 92 intervene less often (Reddy et al., 2024). This difference may reflect lower aggression levels in 93 bonobo societies and a reduced need for maternal protection. ...
Human development is marked by extended immaturity, necessitating extended care throughout infancy and childhood, facilitating advanced cognitive, social, and cultural skill acquisition. Parallels of extended development are also present in our closest living relatives, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). The Self-Domestication Hypothesis (SDH) suggests that human uniqueness stems from selection against aggression. Bonobos are also considered self-domesticated, exhibiting lower aggression and greater social tolerance, which are linked to delayed development and prolonged maternal dependence compared to chimpanzees. However, systematic, quantitative comparisons of the two species developmental patterns are limited and conflicting. This study addressed this gap by examining behavioural development in bonobo and chimpanzee infants aged 0-5.5 years living in two populations (Kokolopori community, Kokolopori Bonobo Reserve, DRC, N=21; Ngogo community, Kibale National Park, Uganda, N=22) in their natural environments. We specifically focused on (i) general behaviours (travel, feeding, grooming), and (ii) spatial independence. By systematically comparing developmental data and using consistent methods, we tested whether bonobo development aligns with SDH predictions. Our results showed similar developmental trajectories, with no species differences concerning ventral riding, nipple contact, or grooming. However, we found species differences regarding travel and proximity patterns, with chimpanzees exhibiting prolonged dorsal riding, bonobos travelling independently more often and maintaining greater distances from their mothers. Age, sibling presence, and maternal parity influenced behavioural patterns, but no sex differences were observed. These findings challenge assumptions of slower bonobo maturation, and highlight the importance of systematic, collaborative research on primate behavioural diversity in natural environments.
Biological anthropology seeks to understand humans from an evolutionary perspective. Namely, what makes humans different from other animals, and how did we get this way? Many relevant traits are physical, but many others are behavioral. For example , when and why did our species develop complex cognition, enduring bonds, and intense cooperation? Given the importance of behavior, biological anthropologists have a long history of turning to our primate relatives to generate hypotheses about the evolutionary processes shaping humans. Indeed, primate behavior is foundational to our field. But not all biological anthropologists appreciate the value of primate behavior for understanding human evolution. Beyond lip service in introductory paragraphs and grant proposals, many primatologists do not make explicit how their work is relevant to human evolution. In this review, we have three main goals: (1) emphasize how comparative studies of primate behavior are crucial to biological anthropology; (2) outline how primatologists and biological anthropologists can improve their work by avoiding common problems that arise when making such comparisons; and (3) provide a primer on the concepts and methods underlying comparative analyses of traits. We provide examples to highlight these points related to cognition, sociality, and diet. We conclude with several recommendations including (1) detailed, high-quality studies of behavior that allow for appropriate comparisons within and across species; (2) using primates as a "gateway clade" and expanding our research to any relevant taxa; and (3) careful attention to the ethical implications of making comparisons to other primates given racist tropes and a history of eugenics.
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’.
In humans, puberty initiates a period of rapid and formative neurobehavioral development. Brain and behavior changes during this maturational window contribute to opportunities for social learning. Here we provide new insights into adolescence as a unique period of social learning and development by describing field studies of our closest living relatives, chimpanzees. Like humans, chimpanzees have a multiyear juvenile life stage between weaning and puberty onset followed by a multiyear adolescent life stage after pubertal onset but prior to socially-recognized adulthood. As they develop increasing autonomy from caregivers, adolescent chimpanzees explore and develop many different types of social relationships with a wide range of individuals in a highly flexible social environment. We describe how adolescent social motivations and experiences differ from those of juveniles and adults and expose adolescents to high levels of uncertainty, risk, and vulnerability, as well as opportunities for adaptive social learning. We discuss how these adolescent learning experiences may be shaped by early life and in turn shape varied adult social outcomes. We outline how future chimpanzee field research can contribute in new ways to a more integrative interdisciplinary understanding of adolescence as a developmental window of adaptive social learning and resilience.
In many animal societies, individuals differ consistently in their ability to win agonistic interactions, resulting in dominance hierarchies. These differences arise due to a range of factors that can influence individuals’ abilities to win agonistic interactions, spanning from genetically driven traits through to individuals’ recent interaction history. Yet, despite a century of study since Schjelderup‐Ebbe's seminal paper on social dominance, we still lack a general understanding of how these different factors work together to determine individuals’ positions in hierarchies. Here, we first outline five widely studied factors that can influence interaction outcomes: intrinsic attributes, resource value asymmetry, winner–loser effects, dyadic interaction‐outcome history and third‐party support. A review of the evidence shows that a variety of factors are likely important to interaction outcomes, and thereby individuals’ positions in dominance hierarchies, in diverse species. We propose that such factors are unlikely to determine dominance outcomes independently, but rather form part of feedback loops whereby the outcomes of previous agonistic interactions (e.g. access to food) impact factors that might be important in subsequent interactions (e.g. body condition). We provide a conceptual framework that illustrates the multitude potential routes through which such feedbacks can occur, and how the factors that determine the outcomes of dominance interactions are highly intertwined and thus rarely act independently of one another. Further, we generalise our framework to include multi‐generational feed‐forward mechanisms: how interaction outcomes in one generation can influence the factors determining interaction outcomes in the next generation via a range of parental effects. This general framework describes how interaction outcomes and the factors determining them are linked within generations via feedback loops, and between generations via feed‐forward mechanisms. We then highlight methodological approaches that will facilitate the study of feedback loops and dominance dynamics. Lastly, we discuss how our framework could shape future research, including: how feedbacks generate variation in the factors discussed, and how this might be studied experimentally; how the relative importance of different feedback mechanisms varies across timescales; the role of social structure in modulating the effect of feedbacks on hierarchy structure and stability; and the routes of parental influence on the dominance status of offspring. Ultimately, by considering dominance interactions as part of a dynamic feedback system that also feeds forward into subsequent generations, we will understand better the factors that structure dominance hierarchies in animal groups.
Animal groups are often organized hierarchically, with dominant individuals gaining priority access to resources and reproduction over subordinate individuals. Initial dominance hierarchy formation may be influenced by multiple interacting factors, including an animal's individual attributes, conventions and self-organizing social dynamics. After establishment, hierarchies are typically maintained over the long-term because individuals save time, energy and reduce the risk of injury by recognizing and abiding by established dominance relationships. A separate set of behaviours are used to maintain dominance relationships within groups, including behaviours that stabilize ranks (punishment, threats, behavioural asymmetry), as well as signals that provide information about dominance rank (individual identity signals, signals of dominance). In this review, we describe the behaviours used to establish and maintain dominance hierarchies across different taxa and types of societies. We also review opportunities for future research including: testing how self-organizing behavioural dynamics interact with other factors to mediate dominance hierarchy formation, measuring the long-term stability of social hierarchies and the factors that disrupt hierarchy stability, incorporating phenotypic plasticity into our understanding of the behavioural dynamics of hierarchies and considering how cognition coevolves with the behaviours used to establish and maintain hierarchies.
This article is part of the theme issue ‘The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies’.
Comparative studies on tool technologies in extant primates, especially in our closest living relatives, offer a window into the evolutionary foundations of tool use in hominins. Whereas chimpanzee tool technology is well studied across populations, the scarcity of described tool technology in wild populations of our other closest living relative, the bonobo, is a mystery. Here we provide a first report of the tool use repertoire of the Kokolopori bonobos and describe in detail the use of leaf-umbrellas during rainfall, with the aim to improve our knowledge of bonobo tool use capacity in the wild. The tool use repertoire of the Kokolopori bonobos was most similar to that of the nearby population of Wamba and comprised eight behaviors, none in a foraging context. Further, over a 6-month period we documented 44 instances of leaf-umbrella use by 22 individuals from three communities, suggesting that this behavior is habitual. Most leaf-umbrella tool users were adult females, and we observed a nonadult using a leaf-umbrella on only a single occasion. While the study and theory of tool technologies is often based on the use of tools in foraging tasks, tool use in bonobos typically occurs in nonforaging contexts across populations. Therefore, incorporating both foraging and nonforaging contexts into our theoretical framework is essential if we wish to advance our understanding of the evolutionary trajectories of tool technology in humans.
Humans maintain extensive social ties of varying preferences, providing a range of opportunities for beneficial cooperative exchange that may promote collective action and our unique capacity for large-scale cooperation. Similarly, non-human animals maintain differentiated social relationships that promote dyadic cooperative exchange, but their link to cooperative collective action is little known. Here, we investigate the influence of social relationship properties on male and female chimpanzee participations in a costly form of group action, intergroup encounters. We find that intergroup encounter participation increases with a greater number of other participants as well as when participants are maternal kin or social bond partners, and that these effects are independent from one another and from the likelihood to associate with certain partners. Together, strong social relationships between kin and non-kin facilitate group-level cooperation in one of our closest living relatives, suggesting that social bonds may be integral to the evolution of cooperation in our own species. 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.
Many animals engage in aggression, but chimpanzees stand out in terms of fatal attacks against adults of their own species. Most lethal aggression occurs between groups, where coalitions of male chimpanzees occasionally kill members of neighboring communities that are strangers. However, the first observed cases of lethal violence in chimpanzees, which occurred at Gombe, Tanzania in the 1970s, involved chimpanzees that once knew each other. They followed the only observed case of a permanent community fission in chimpanzees. A second permanent fission recently transpired at Ngogo, Kibale National Park, Uganda. Members of a large western subgroup gradually ceased associating peacefully with the rest of the community and started behaving antagonistically toward them. Affiliation effectively ended by 2017. Here, we describe two subsequent lethal coalitionary attacks by chimpanzees of the new western community on males of the now separate central community, one in 2018 and the second in 2019. The first victim was a young adult male that never had strong social ties with his attackers. The second was a high-ranking male that had often associated with the western subgroup before 2017; he groomed regularly with males there and formed coalitions with several. Other central males present at the start of the second attack fled, and others nearby did not come to the scene. Several western females joined in the second attack; we suggest that female–female competition contributed to the fission. This event highlighted the limits on protection afforded by long-term familiarity and the constraints on costly cooperation among male chimpanzees.
Mothers provide indispensable care for infants in many mammalian species. In some long-lived species, the maternal-offspring bond persists after infancy with mothers continuing to provide resources and social support to their adult progeny. Maternal presence is associated with fitness benefits through adolescence for male chimpanzees despite the fact that mature males dominate females and form their strongest bonds with other males. How mothers support grown sons is unknown, because few studies have examined developmental shifts in mother-son relationships during adolescence and adulthood. We investigated social interactions between 29 adolescent (9–15 years) and young adult male (16–20 years) chimpanzees and their mothers at Ngogo in Kibale National Park, Uganda, over 3 years. All males under 12 years old had their mother as their top grooming and proximity partner, as did one-third of the young adult males. As males grew older, the amount of time they associated with, maintained proximity to, groomed with, and kept track of their mothers while traveling decreased. When males were together in the same party as their mothers, however, young adult males affiliated with their mothers as frequently as did adolescent males, with sons initiating the majority of these interactions. In contrast to adult sons, however, adolescent sons became distressed when separated from mothers and relied on their mothers for agonistic support and reassurance after conflicts. These findings indicate that the chimpanzee maternal-offspring bond continues but changes through adolescence and adulthood, with mothers remaining occasional social companions for most adult sons and frequent companions for some.
Significance statement
Mammalian mothers protect and provision their infants, and in some species, mothers provide social support for their adult offspring. The importance of mothers in the lives of adult sons is clear in humans and in one of our closest relatives, bonobos. Here we show mothers are also important social partners for sons throughout adolescence and into young adulthood in chimpanzees. Despite prevailing knowledge that adult males are key alliance partners for male chimpanzees, we demonstrate that male chimpanzees maintain social bonds with their mothers into adulthood. We also suggest that social bonds reflect not only the total time spent together, but what animals do during those times, as many young adults rarely groomed their mothers, but at times when they were in the same subgroup with her, they did so frequently. Future research will assess the physiological, psychological, and reproductive benefits of such mother-son bonds.
Humans are unusual among animals for continuing to provision and care for their offspring until adulthood. This "prolonged dependency" is considered key for the evolution of other notable human traits, such as large brains, complex societies, and extended postreproductive lifespans. Prolonged dependency must therefore have evolved under conditions in which reproductive success is gained with parental investment and diminished with early parental loss. We tested this idea using data from wild chimpanzees, which have similarly extended immature years as humans and prolonged mother-offspring associations. Males who lost their mothers after weaning but before maturity began reproducing later and had lower average reproductive success. Thus, persistent mother-immature son associations seem vital for enhancing male reproductive success, although mothers barely provision sons after weaning. We posit that these associations lead to social gains, crucial for successful reproduction in complex social societies, and offer insights into the evolution of prolonged dependency.
Large brains and behavioural innovation are positively correlated, species-specific traits, associated with the behavioural flexibility animals need for adapting to seasonal and unpredictable habitats. Similar ecological challenges would have been important drivers throughout human evolution. However, studies examining the influence of environmental variability on within-species behavioural diversity are lacking despite the critical assumption that population diversification precedes genetic divergence and speciation. Here, using a dataset of 144 wild chimpanzee (Pan troglodytes) communities, we show that chimpanzees exhibit greater behavioural diversity in environments with more variability - in both recent and historical timescales. Notably, distance from Pleistocene forest refugia is associated with the presence of a larger number of behavioural traits, including both tool and non-tool use behaviours. Since more than half of the behaviours investigated are also likely to be cultural, we suggest that environmental variability was a critical evolutionary force promoting the behavioural, as well as cultural diversification of great apes.
Social mammals often live in groups in which a dominance hierarchy is an important determinant of access to mates. In addition to competing individually, males may form coalitions of two or more to attack or intimidate rivals. Coalition formation could be particularly advantageous for adolescent males by helping them compensate for their physical and social immaturity. However, adolescents may struggle to attract effective coalition partners because of these inadequacies. Here, we examine the behavior of maturing male chimpanzees to test whether coalitions are more frequent among more or less powerful individuals. Our longitudinal study followed 18 males (ages 5 through 25 years) and utilized 1517 coalitions across 12 years of observation of the Kanyawara chimpanzee community in Kibale National Park, Uganda. We found that rates of coalition formation increased across maturation and that this increase was independent of a rise in the overall use of aggression. Juveniles formed coalitions almost exclusively with their mothers, while adolescents partnered primarily with peers and adult males. When adolescents and adult males formed coalitions with each other, the adolescents were more likely to join the adults than vice versa. Finally, adolescents engaged in joint behavior with adult males more often in non-aggressive vocal displays than in aggressive coalitions. Taken together, our results suggest that adolescent males are largely unable to attract the most powerful coalition partners and that they "make the best of a bad job" by joining adult males in less competitive situations, when the risk of receiving aggression from opponents is lower.
The mother-offspring relationship is paramount in most mammals and infant survival often depends on maternal investment. In species with prolonged periods of development or co-residence, mothers may continue to influence their offspring’s outcomes beyond nutritional independence with benefits biased towards the philopatric sex. Chimpanzees (Pan troglodytes) are long-lived mammals with a protracted period of immaturity during which offspring continue to travel with their mothers. In contrast to most mammals, chimpanzees are also typically male philopatric. Here, we use over 50 years of demographic data from two communities in Gombe National Park, Tanzania, to examine the survival and longevity of both male and female chimpanzees that experienced maternal loss during three different age categories. Males who were orphaned between the ages of 0–4.99 years, 5–9.99 years, and 10–14.99 years all faced significantly lower survival than non-orphans and died earlier than expected. Females faced similarly reduced survival probabilities when orphaned between 0–4.99 and 5–9.99 years of age; however, females who experienced maternal loss between 10 and 14.99 years of age were no more likely to die than non-orphans. Females orphaned in this later age class also lived significantly longer beyond maternal loss than their male counterparts. As observed in other mammals, philopatric male chimpanzees may continue to benefit from their mother’s ecological knowledge, whereas maternal influence on female offspring likely fades as they prepare to emigrate. These results emphasize how maternal influence on offspring outcomes can extend well beyond weaning, particularly for the philopatric sex.
Significance statement
Mammalian mothers are crucial to their infant’s survival and in species where offspring continue to live with their mothers after weaning, maternal influence may extend beyond dependence on mother’s milk. While in most group-living mammals females remain in their natal group, chimpanzees typically display the opposite pattern with males residing alongside their mothers into adulthood. Using over 50 years of data on wild chimpanzees, we investigated the consequences of maternal loss both before and after weaning. We found that both males and females orphaned up to 10 years of age were less likely to survive than non-orphans; however, only males orphaned between 10 and 15 years also faced lower survival. These results emphasize how chimpanzee mothers continue to matter for offspring beyond infancy and provide novel data on reduced maternal influence on survival for daughters compared to sons.
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.
In-group cohesion is an essential component of successful intergroup competition in both human and nonhuman animals, likely facilitating group members access to potential benefits. However, when benefits are equally shared among group members, group defense becomes a collective action problem, which might subvert cohesive participation during intergroup competition. There is a lack of consensus across studies and species with regard to the link between in-group cohesion and intergroup competition, likely as a result of species differences in managing the collective action problem. Here, we examine this link in a species with a striking example of collective action during intergroup competition, chimpanzees (Pan troglodytes verus). Using two years of focal-follow data on males and females in two groups at the Taï Forest, Côte d’Ivoire, we investigated the immediate and long-term effects of intergroup competition (border patrols and intergroup encounters) on measures of in-group cohesion, namely modularity, party size, and intergroup aggression. We found that groups’ association patterns were less modular (more cohesive) in months in which they engaged in more border patrols and intergroup encounters. We found that current and greater prior engagement in intergroup competition predicted larger party sizes. Furthermore, current, but not prior engagement in intergroup competition, predicted reduced intragroup aggression by males but not by females. Increased in-group cohesion in chimpanzees likely reduces potential costs of intergroup competition engagement, by facilitating joint participation in current and future intergroup conflicts, overcoming the collective action problem.
In some species habitual same-sex sexual behavior co-occurs with high levels of intra-sexual alliance formation, suggesting that these behaviors may be linked. We tested for such a link by comparing behavioral and physiological outcomes of sex with unrelated same-and opposite-sex partners in female bonobos (Pan paniscus). We analyzed behavioral outcomes following 971 sexual events involving n = 19 female and n = 8 male adult and sub-adult members of a wild, habituated bonobo community. We additionally collected n = 143 urine samples before and after sexual interactions to non-invasively measure oxytocin (OT), which modulates female sexual behavior and facilitates cooperation in other species. The majority of sexual events (65%) consisted of female same-sex genito-genital rubbing (or GG-rubbing). Female dyads engaged in significantly more sexual interactions than did inter-sexual dyads, and females were more likely to remain within close proximity to their partners following GG-rubbing. Females also exhibited greater increases in urinary OT following GG-rubbing compared with copulations, indicating a physiological basis for increased motivation to cooperate among females. The frequency of coalitionary support among non-kin was positively predicted by the frequency of sexual interactions for female as well opposite-sex dyads, although coalitionary support tended to be more frequent among females. The emergence of habitual same-sex sexual behavior may have been an important step in the evolution of cooperation outside of kinship and pair-bonds in one of our closest phylogenetic relatives.
Infanticide is well documented in chimpanzees and various hypotheses have been proposed to explain this behavior. However, since infanticide by chimpanzees is relatively rare, it has thus far not been possible to thoroughly test these hypotheses. Here we present an analysis of the largest dataset of infanticides from a single community of chimpanzees, a full record of all intra-community infanticides and failed attempts at infanticide over a 24-year period for the Sonso community of chimpanzees in the Budongo Forest, Uganda. We use these data to test four hypotheses for this behavior: the sexual selection hypothesis, male mating competition, resource competition, and meat acquisition. Our dataset consisted of 33 attacks on 30 victims, 11 of which were ‘definite’ infanticides, four of which ‘almost certain’, and nine were ‘suspected’, while nine were ‘attempted’ infanticides. The majority of attacks where the perpetrators were known (23) had only male attackers and victims were disproportionately young (two-thirds of victims with known ages were under 1 week old). Our data best support the sexual selection hypothesis for infanticide. Cannibalism was infrequent and partial, suggesting meat acquisition was a by-product of infanticide, and there was no evidence to suggest that infanticide was part of a male strategy to eliminate future competitors. Infanticide by females was rare, but we suggest sexual selection, operating through intra-sexual competition, may also be responsible for infanticide by females.
Significance
What forces produce and maintain social inequality, and why do society members tolerate this inequality? The “One Percent” clearly benefit from having high status, but low-status individuals have strong incentive to challenge the established pecking order and try to improve their position. This conundrum is particularly striking in the societies of many primates and spotted hyenas, where females who are born to low-status mothers rarely manage to improve their position. Here we find that females who are strongly allied with their group-mates are more likely to improve their status, and that upward social mobility is often achieved with support from their closest allies. This suggests that, much like some animals compete physically for status, these species compete through social alliances.
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 betweengroup 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 speciesdifferences 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.
Lethal coalitionary aggression is of significant interest to primatologists and anthropologists given its pervasiveness in human, but not nonhuman, animal societies. Chimpanzees (Pan troglodytes) provide the largest sample of recorded lethal coalitionary aggression in nonhuman primates, and most long-term chimpanzee study sites have recorded coalitionary killing of conspecifics. We report an inferred lethal attack by resident males on a former alpha male chimpanzee (P. t. verus) at Fongoli in Senegal. We describe the male’s presence in the community, his overthrow, social peripheralization for >5 yr, and his attempt to rejoin the group as well as circumstances surrounding his death. We report attacks by multiple chimpanzees on his dead body, most frequently by a young adult male and an older female. The latter also cannibalized the body. Coalitionary killing is rare among West African chimpanzees compared to the East African chimpanzee (P. t. schweinfurthii). This pattern may relate to differences in population densities, research effort, and subspecies differences in biology and behavior.
Patterns of coalitionary aggression among female animals are generally explained by kin selection theory. Frequent female coalitions are almost exclusively observed in female-philopatric species, where females stay in their natal group, and females typically form coalitions with their kin. Bonobos, Pan paniscus, in contrast, are male-philopatric, with females emigrating to new groups at adolescence, but female bonobos frequently form coalitions even though they are generally with nonrelatives. Here we investigated the patterns of female coalitions in a group of wild bonobos at Wamba, Democratic Republic of the Congo, in order to explore alternative mechanisms to kin selection for cooperation among females. We found that all female coalitions (defined as coalitions in which two or more females participated) were formed to attack males, usually after the male(s) behaved aggressively towards one or more females. There was no evidence that female bonobos used proximity, grooming or genito-genital rubbing (GG-rubbing) to develop coalition partnerships, although higher association provided females with more opportunity to form coalitions. Instead of reciprocal agonistic support, we found a unidirectional pattern in which older females supported younger females. Females defeated males more easily when they formed coalitions than when they confronted males alone. Unlike female coalitions in other species that use coalitions to cope with competition among females, our results suggest that coalitions in female bonobos might have evolved as a counterstrategy against male harassment. Females might choose their coalition partners based not on affiliative relationship or reciprocity but on mutualism. In contrast to the hypothesis that affiliative behaviour leads to coalition formation, coalitions might in fact increase gregariousness among females, leading females to develop affiliative interactions that promote tolerance.
Humans’ closest living relatives are bonobos (Pan paniscus) and chimpanzees (Pan troglodytes), yet these great ape species differ considerably from each other in terms of social behavior. Bonobos are more tolerant
of conspecifics in competitive contexts and often use sexual behavior to mediate social interactions. Chimpanzees more frequently
employ aggression during conflicts and actively patrol territories between communities. Regulation of emotional responses
is facilitated by the amygdala, which also modulates social decision-making, memory and attention. Amygdala responsiveness
is further regulated by the neurotransmitter serotonin. We hypothesized that the amygdala of bonobos and chimpanzees would
differ in its neuroanatomical organization and serotonergic innervation. We measured volumes of regions and the length density
of serotonin transporter-containing axons in the whole amygdala and its lateral, basal, accessory basal and central nuclei.
Results showed that accessory basal nucleus volume was larger in chimpanzees than in bonobos. Of particular note, the amygdala
of bonobos had more than twice the density of serotonergic axons than chimpanzees, with the most pronounced differences in
the basal and central nuclei. These findings suggest that variation in serotonergic innervation of the amygdala may contribute
to mediating the remarkable differences in social behavior exhibited by bonobos and chimpanzees.
Description Fit linear and generalized linear mixed-effects models. The models and their components are represented using S4 classes and methods. The core computational algorithms are implemented using the 'Eigen' C++ library for numerical linear algebra and 'RcppEigen' ``glue''.
Classic life-history theory predicts that menopause should not occur because there should be no selection for survival after the cessation of reproduction [1]. Yet, human females routinely live 30 years after they have stopped reproducing [2]. Only two other species-killer whales (Orcinus orca) and short-finned pilot whales (Globicephala macrorhynchus) [3, 4]-have comparable postreproductive lifespans. In theory, menopause can evolve via inclusive fitness benefits [5, 6], but the mechanisms by which postreproductive females help their kin remain enigmatic. One hypothesis is that postreproductive females act as repositories of ecological knowledge and thereby buffer kin against environmental hardships [7, 8]. We provide the first test of this hypothesis using a unique long-term dataset on wild resident killer whales. We show three key results. First, postreproductively aged females lead groups during collective movement in salmon foraging grounds. Second, leadership by postreproductively aged females is especially prominent in difficult years when salmon abundance is low. This finding is critical because salmon abundance drives both mortality and reproductive success in resident killer whales [9, 10]. Third, females are more likely to lead their sons than they are to lead their daughters, supporting predictions of recent models [5] of the evolution of menopause based on kinship dynamics. Our results show that postreproductive females may boost the fitness of kin through the transfer of ecological knowledge. The value gained from the wisdom of elders can help explain why female resident killer whales and humans continue to live long after they have stopped reproducing.
Copyright © 2015 The Authors. Published by Elsevier Ltd.. All rights reserved.
For many long-lived mammalian species, extended maternal investment has a profound effect on offspring integration in complex social environments. One component of this investment may be aiding young in aggressive interactions, which can set the stage for offspring social position later in life. Here we examined maternal effects on dyadic aggressive interactions between immature (<12 years) chimpanzees. Specifically, we tested whether relative maternal rank predicted the probability of winning an aggressive interaction. We also examined maternal responses to aggressive interactions to determine whether maternal interventions explain interaction outcomes. Using a 12-year behavioural data set (2000-2011) from Gombe National Park, Tanzania, we found that relative maternal rank predicted the probability of winning aggressive interactions in male-male and male-female aggressive interactions: offspring were more likely to win if their mother outranked their opponent's mother. Female-female aggressive interactions occurred infrequently (two interactions), so could not be analysed. The probability of winning was also higher for relatively older individuals in male-male interactions, and for males in male-female interactions. Maternal interventions were rare (7.3% of 137 interactions), suggesting that direct involvement does not explain the outcome for the vast majority of aggressive interactions. These findings provide important insight into the ontogeny of aggressive behaviour and early dominance relationships in wild apes and highlight a potential social advantage for offspring of higher-ranking mothers. This advantage may be particularly pronounced for sons, given male philopatry in chimpanzees and the potential for social status early in life to translate more directly to adult rank.
Observations of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) provide valuable comparative data for understanding the significance of conspecific killing. Two kinds of hypothesis have been proposed. Lethal violence is sometimes concluded to be the result of adaptive strategies, such that killers ultimately gain fit-ness benefits by increasing their access to resources such as food or mates 1–5 . Alternatively, it could be a non-adaptive result of human impacts, such as habitat change or food provisioning 6–9 . To discri-minate between these hypotheses we compiled information from 18 chimpanzee communities and 4 bonobo communities studied over five decades. Our data include 152 killings (n 5 58 observed, 41 inferred, and 53 suspected killings) by chimpanzees in 15 com-munities and one suspected killing by bonobos. We found that males were the most frequent attackers (92% of participants) and victims (73%); most killings (66%) involved intercommunity attacks; and attackers greatly outnumbered their victims (median 8:1 ratio). Variation in killing rates was unrelated to measures of human impacts. Our results are compatible with previously proposed adaptive expla-nations for killing by chimpanzees, whereas the human impact hypo-thesis is not supported. Substantial variation exists in rates of killing across chimpanzee study sites 2–5,10–12
In this review, we reorganize the concept and highlight the importance of prestige in humans and non-human animals by introducing key characteristics of dominance and prestige and related theories. Previous studies with non-human animals have mainly focused on dominance, presuming prestige as a human-unique social trait. However, to deepen our understanding of the evolution of prestige, comparative studies with non-human animals, especially our evolutionary closest relatives, chimpanzees and bonobos, are essential. We propose the direction of future studies to investigate how prestige has emerged as a viable strategy for gaining social rank while diverging from dominance, which will establish a foundation for investigating the impact of prestige on propensities towards large-scale cooperation and cumulative culture which are still considered unique to humans. Such comparative viewpoints on prestige, along with some hypotheses of species differences, will provide powerful guidance for understanding the evolution of social hierarchies.
Human between-group interactions are highly variable, ranging from violent to tolerant and affiliative. Tolerance between groups is linked to our unique capacity for large-scale cooperation and cumulative culture, but its evolutionary origins are understudied. In chimpanzees, one of our closest living relatives, predominantly hostile between-group interactions impede cooperation and information flow across groups. In contrast, in our other closest living relative, the bonobo, tolerant between-group associations are observed. However, as these associations can be frequent and prolonged and involve social interactions that mirror those within groups, it is unclear whether these bonobos really do belong to separate groups. Alternatively, the bonobo grouping patterns may be homologous to observations from the large Ngogo chimpanzee community, where individuals form within-group neighborhoods despite sharing the same membership in the larger group. To characterize bonobo grouping patterns, we compare the social structure of the Kokolopori bonobos with the chimpanzee group of Ngogo. Using cluster analysis, we find temporally stable clusters only in bonobos. Despite the large spatial overlap and frequent interactions between the bonobo clusters, we identified significant association preference within but not between clusters and a unique space use of each cluster. Although bonobo associations are flexible (i.e., fission–fusion dynamics), cluster membership predicted the bonobo fission compositions and the spatial cohesion of individuals during encounters. These findings suggest the presence of a social system that combines clear in-group/out-group distinction and out-group tolerance in bonobos, offering a unique referential model for the evolution of tolerant between-group interactions in humans.
In some species, individuals form well-differentiated and affiliative social relationships that facilitate cooperation and confer adaptive benefits, but few studies of males have addressed the benefits of same-sex social bonds. Among mammals, adult male chimpanzees, Pan troglodytes, form some of the strongest and most stable social bonds, and several studies have found that higher-ranking males attain short- and long-term benefits. No study in chimpanzees, however, has demonstrated a link between social bonds and dominance trajectories. To fill this gap, we used 37 years of data from Gombe National Park, Tanzania, to test the hypothesis that social bonds in adult male chimpanzees predict changes in dominance strength, which were measured by annual changes in mean Elo scores. Across 24 adult males, we found that social bonds, which were identified using both association in small groups and grooming activity, showed positive relationships with changes in dominance strength. From previous studies, the most likely mechanism for the observed relationship between adult male bond strength and dominance trajectories is the formation of cooperative coalitions, by which males with stronger bonds leverage established relationships to maintain or increase their position in the dominance hierarchy. Given the fission–fusion social structure of chimpanzees, both party-level associations and grooming relationships are essential components of male social bonding, and these results, in combination with prior studies, suggest that having strong social bonds is a valuable strategy for achieving higher rank.
Significance
Chimpanzees, human’s close evolutionary relatives, are a tractable model system for understanding how physical aggression can develop in the absence of gender socialization. Here we used 13 y of behavioral data and a targeted 3-y social development study to document clear sex differences in chimpanzees’ early aggressive experiences, supporting the possibility for social experience to shape sex-typed behavior in the absence of explicitly taught gender norms. However, as young males’ own aggressive behavior provoked aggressive responses from others, experiential differences were influenced by early-emerging behavioral differences that already resembled adult patterns. By demonstrating interactions between exposure to aggression and developing behavior, our results add an important perspective to long-standing debates over the origins of gender differences in human aggression.
Mothers are the most fundamental individuals for the survival and development of their immature offspring. Sex-biased dispersal has an effect on strong and long-lasting social bonding between mothers and their philopatric offspring. Nepotistic relationships are often seen in species with male-biased dispersal but less frequently in species with female-biased dispersal. Bonobos are unique among female-biased dispersal primates in that the females are codominant with males, exert influence on the mating opportunities of their mature sons, and tolerate each other regardless of relatedness. Few studies on bonobos have examined sex differences in social relationships between juveniles and their mothers, and how this relates to mother–son and female–female cooperative relationships amongst adults. We investigated whether the association index of juveniles with their mothers changed with age depending on the sex of the juveniles in parties of bonobos at Wamba, the Democratic Republic of the Congo. We found that female bonobos had decreased party associations with their mothers prior to their emigration from the natal group, while male bonobos maintained relatively high party associations with their mothers. These results indicate that sex differences that emerge during the juvenile period in bonobos in their spatial relationships with their mothers differ from previous findings on chimpanzees, spider monkeys, and muriquis, in which philopatric sons tend to spend less time in proximity to their mothers and disperse earlier than, or at a similar age to, daughters. The contrasts between bonobos and other primate species suggest that the high social status of female bonobos relative to that of males may facilitate the extension of maternal support for their philopatric sons, and that high tolerance among unrelated females may enable the spatial independence of daughters from their mothers at an earlier stage.
I have spent over 40 years studying the behavior of our closest living relatives, the apes. In this paper, I review my research on the spacing, mating, and vocal behavior of gibbons and orangutans (Pongo pygmaeus) and the vocal and social behavior of chimpanzees (Pan troglodytes). I devote special attention to results derived from a 25‐year‐long study of a remarkable and extraordinarily large group of chimpanzees that has recently fissioned at Ngogo in Kibale National Park, Uganda. I conclude with some advice for the next generation of field primatologists.
Research Highlights
• I review the results of my field research on gibbons, orangutans, and chimpanzees.
• My findings provide insights into the spacing, mating, and vocal behavior of gibbons and orangutans and the vocal and social behavior of chimpanzees.
In many group-living mammals, mothers may increase the reproductive success of their daughters even after they are nutritionally independent and fully grown [1]. However, whether such maternal effects exist for adult sons is largely unknown. Here we show that males have higher paternity success when their mother is living in the group at the time of the offspring's conception in bonobos (N = 39 paternities from 4 groups) but not in chimpanzees (N = 263 paternities from 7 groups). These results are consistent with previous research showing a stronger role of mothers (and females more generally) in bonobo than chimpanzee societies. Surbeck et al. show direct maternal effects for adult sons in a species with male philopatry/female dispersal and co-dominance between the sexes. Males have higher paternity success when their mother is living in the group in bonobos but not in the closely related chimpanzees, where females are subordinate and intervene less in male conflict.
The selective advantage of male infanticide is enhancement of reproductive success of the aggressor. This implies that aggression is directed at individuals sired by others, infant loss shortens the mother's inter‐birth interval, and the aggressor has a greater likelihood of siring the next offspring of the victims’ mother. As these conditions are not always met, the occurrence of male infanticide is expected to vary, and hominoid primates offer an interesting example of variation in male infanticide. Infanticide has been reported in gorillas and chimpanzees but appears to be absent in orangutans and bonobos. One argument for the absence of infanticide in bonobos is reduction of male aggression. However, given that male aggression against immature individuals occurs and that females engage in behavior that is considered to be counterstrategy against male infanticide, the risk of male infanticide may pose a potential threat. Here, we explored whether aggression by male bonobos fits predictions of male infanticide. Male aggression toward immature individuals was rare and did not have lethal consequences, but the majority of observed cases exposed targets to risks of injury. Males did not target their own offspring less frequently than unrelated immatures, and the risk of being the target of male aggression increased with the targets’ age. Overall, these results do not match the predictions of the adaptive male infanticide hypothesis. Instead, aggression by males may promote the emigration of the targets and older males may reinforce their superior status toward individuals that will soon compete for the same resources.
Two major types of aggression, proactive and reactive, are associated with contrasting expression, eliciting factors, neural pathways, development, and function. The distinction is useful for understanding the nature and evolution of human aggression. Compared with many primates, humans have a high propensity for proactive aggression, a trait shared with chimpanzees but not bonobos. By contrast, humans have a low propensity for reactive aggression compared with chimpanzees, and in this respect humans are more bonobo-like. The bimodal classification of human aggression helps solve two important puzzles. First, a long-standing debate about the significance of aggression in human nature is misconceived, because both positions are partly correct. The Hobbes-Huxley position rightly recognizes the high potential for proactive violence, while the Rousseau-Kropotkin position correctly notes the low frequency of reactive aggression. Second, the occurrence of two major types of human aggression solves the execution paradox, concerned with the hypothesized effects of capital punishment on self-domestication in the Pleistocene. The puzzle is that the propensity for aggressive behavior was supposedly reduced as a result of being selected against by capital punishment, but capital punishment is itself an aggressive behavior. Since the aggression used by executioners is proactive, the execution paradox is solved to the extent that the aggressive behavior of which victims were accused was frequently reactive, as has been reported. Both types of killing are important in humans, although proactive killing appears to be typically more frequent in war. The biology of proactive aggression is less well known and merits increased attention.
Demographic data on wild chimpanzees are crucial for understanding the evolution of chimpanzee and hominin life histories, but most data come from populations affected by disease outbreaks and anthropogenic disturbance. We present survivorship data from a relatively undisturbed and exceptionally large community of eastern chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. We monitored births, deaths, immigrations, and emigrations in the community between 1995 and 2016. Using known and estimated ages, we calculated survivorship curves for the whole community, for males and females separately, and for individuals ≤2 years old when identified. We used a novel method to address age estimation error by calculating stochastic survivorship curves. We compared Ngogo life expectancy, survivorship, and mortality rates to those from other chimpanzee communities and human hunter-gatherers. Life expectancy at birth for both sexes combined was 32.8 years, far exceeding estimates of chimpanzee life expectancy in other communities, and falling within the range of human hunter-gatherers (i.e., 27–37 years). Overall, the pattern of survivorship at Ngogo was more similar to that of human hunter-gatherers than to other chimpanzee communities. Maximum lifespan for the Ngogo chimpanzees, however, was similar to that reported at other chimpanzee research sites and was less than that of human-hunter gatherers. The absence of predation by large carnivores may contribute to some of the higher survivorship at Ngogo, but this cannot explain the much higher survivorship at Ngogo than at Kanyawara, another chimpanzee community in the same forest, which also lacks large carnivores. Higher survivorship at Ngogo appears to be an adaptive response to a food supply that is more abundant and varies less than that of Kanyawara. Future analyses of hominin life history evolution should take these results into account.
Objectives:
Female bonobos (Pan paniscus) are characterized as highly affiliative and cooperative, but few studies have quantified the strength and stability of female intra-sexual relationships or explored how variation in social relationships influences cooperation. We measure female social preferences, identify causes of variation in preferences, and test whether variation in social preferences predicts food sharing or coalitionary support.
Methods:
Data were collected over 3 years from females in the Bompusa community at LuiKotale, DRC. We measured genetic relatedness and constructed social preference indices for party association, proximity, grooming, GG-rubbing and aggression. We identified preferred social partners based on permutation tests and measured stability using Mantel tests. We used factor analysis to identify inter-relationships between preference indices and used LMMs to test whether variation in social preferences was explained by relatedness, rank differences, having dependent young or co-residency time. We used GLMMs to test whether variation in social preferences predicted food sharing or coalitionary support.
Results:
All females had preferred non-kin partners for proximity, grooming or GG-rubbing, but only grooming preferences were stable across years. Association indices were higher among lactating females, and aggression was lower among females with longer co-residency times. The factor analysis identified one factor, representing proximity and GG-rubbing preferences, labeled behavioral coordination. Dyads with higher levels of behavioral coordination were more likely to share food.
Conclusions:
Female bonobos exhibit stable, differentiated grooming relationships outside of kinship and philopatry. Females also exhibit flexible proximity and GG-rubbing preferences that may facilitate cooperation with a wider range of social partners.
The author summarizes 20 years of research in the Kibale forest in Uganda. The main body of the book demonstrates the adverse effects of logging on community structure and other aspects of forest ecology. The author provides evidence that future logging must be done at far lower intensities than is currently the norm, if intact ecosystems are to be maintained. Detailed recommendations for harvest plans compatible with the conservation of biodiversity and ecological integrity are outlined. Struhsaker addresses the underlying causes of tropical deforestation and concludes that although there are numerous proximate factors, the ultimate causes are rapidly increasing human populations and rates of consumption per capita. Comparisons with relevant studies elsewhere in the tropics are drawn and specific recommendations to address the problems are offered.
Focuses on side-directed communication (behaviour that agonistically involved apes show towards non-opponents) in Pan troglodytes. A multi-variate analysis of the contexts of this highly variable behaviour indicates that it can be divided into several functional categories: taking refuge; seeking reassurance; enlisting support; begging for support and taking courage. In general, side-directed behaviour facilitates intervention by third parties, but sometimes its function may be to appease potential supporters of the opponent, and thus keep them from interfering. -from Author
Juveniles in a natural troop of 70 yellow baboons were ranked in dominance hierarchies according to the direction of supplanting interactions. Relative rank between juvenile male was dependent on size/age, but relative rank between juvenile males and adult females was dependent on mother's rank. Juvenile females ranked according to their mother's rank both with same-sex peers and with adult females. Correlations between individual rank in these hierarchies and rates of supplanting interactions and proximity to others were examined to assess possible competitive advantage. Solicitations and supportive behaviour between kin were assessed as possible mechanisms for transmission of maternal rank. The functional consequences of these different hierarchies were discussed.
Male Pan troglodytes experience puberty when they are about 9 yr old and just over half adult weight. They reach adult weight at 14-15 yr. Females start small sexual swellings at about 8 yr, mate with adult males when they are about 10.5 yr and have their first infants when they are c12 yr. Males reduce their constant association with their mothers when they reach puberty and associate more with adult males and cycling females. Some males form strong, long-lasting associations with particular adult males. Females remain with their mothers until first oestrus, then associate with adult males either in their natal community or a new community during oestrus. Immatures of all ages spend 3-13% of their time in social grooming, but grooming partners change during adolescence. Rates of interference in copulations by males decline during adolescence and males become more cautious of copulating in the presence of adult males. Females show little sexual behaviour until they start getting large oestrus swellings. Males receive increased aggression from adult males during adolescence. -from Author