Kinship and social bonds in female chimpanzees (Pan troglodytes)

A large body of theoretical and empirical research suggests that kinship influences the development and maintenance of social bonds among group‐living female mammals, and that human females may be unusual in the extent to which individuals form differentiated social relationships with nonrelatives. Here we combine behavioral observations of party association, spatial proximity, grooming, and space use with extensive molecular genetic analyses to determine whether female chimpanzees form strong social bonds with unrelated individuals of the same sex. We compare our results with those obtained from male chimpanzees who live in the same community and have been shown to form strong social bonds with each other. We demonstrate that party association is as good a predictor of spatial proximity and grooming in females as it is in males, that the highest party association indices are consistently found between female dyads, that the sexes do not differ in the long‐term stability of their party association patterns, and that these results cannot be explained as a by‐product of the tendency of females to selectively range in particular areas of the territory. We also show that close kin (i.e. mother–daughter and sibling dyads) are very rare, indicating that the vast majority of female dyads that form strong social bonds are not closely related. Additional analyses reveal that “subgroups” of females, consisting of individuals who frequently associate with one another in similar areas of the territory, do not consist of relatives. This suggests that a passive form of kin‐biased dispersal, involving the differential migration of females from neighboring communities into subgroups, was also unlikely to be occurring. These results show that, as in males, kinship plays a limited role in structuring the intrasexual social relationships of female chimpanzees. Am. J. Primatol. 71:840–851, 2009. © 2009 Wiley‐Liss, Inc.     

The benefits of social capital: close social bonds among female baboons enhance offspring survival

Sociality has evolved in many animal taxa, but primates are unusual because they establish highly differentiated bonds with other group members. Such bonds are particularly pronounced among females in species like baboons, with female philopatry and male dispersal. These relationships seem to confer a number of short-term benefits on females, and sociality enhances infant survival in some populations. However, the long-term consequences of social bonds among adult females have not been well established. Here we provide the first direct evidence that social relationships among female baboons convey fitness benefits. In a group of free-ranging baboons, Papio cynocephalus ursinus, the offspring of females who formed strong social bonds with other females lived significantly longer than the offspring of females who formed weaker social bonds. These survival benefits were independent of maternal dominance rank and number of kin and extended into offspring adulthood. In particular, females who formed stronger bonds with their mothers and adult daughters experienced higher offspring survival rates than females who formed weaker bonds. For females lacking mothers or adult daughters, offspring survival was closely linked to bonds between maternal sisters. These results parallel those from human studies, which show that greater social integration is generally associated with reduced mortality and better physical and mental health, particularly for women.     

No evidence that within‐group male relatedness reduces harm to females in Drosophila

Conflict between males and females over whether, when, and how often to mate often leads to the evolution of sexually antagonistic interactions that reduce female reproductive success. Because the offspring of relatives contribute to inclusive fitness, high relatedness between rival males might be expected to reduce competition and result in the evolution of reduced harm to females. A recent study investigated this possibility in Drosophila melanogaster and concluded that groups of brothers cause less harm to females than groups of unrelated males, attributing the effect to kin selection. That study did not control for the rearing environment of males, rendering the results impossible to interpret in the context of kin selection. Here, we conducted a similar experiment while manipulating whether males developed with kin prior to being placed with females. We found no difference between related and unrelated males in the harm caused to females when males were reared separately. In contrast, when related males developed and emerged together before the experiment, female reproductive output was higher. Our results show that relatedness among males is insufficient to reduce harm to females, while a shared rearing environment – resulting in males similar to or familiar with one another – is necessary to generate this pattern.     

Mating system, philopatry and patterns of kinship in the cooperatively breeding subdesert mesite Monias benschi

In the first molecular study of a member of the threatened avian family, Mesitornithidae, we used nine polymorphic microsatellite loci to elucidate parentage, patterns of within-group kinship and occurrence of extra-group paternity in the subdesert mesite Monias benschi, of southwest Madagascar. We found this cooperatively breeding species to have a very fluid mating system. There was evidence of genetic monogamy and polygynandry: of the nine groups with multiple offspring, six contained one breeding pair with unrelated helpers and three contained multiple male and female breeders with related helpers. Although patterns of within-group kinship varied, there was a strong positive relationship between group size and relatedness, suggesting that groups form by natal philopatry. There was also a strong positive correlation between within-sex and between-sex relatedness, indicating that unlike most cooperatively breeding birds, philopatry involved both sexes. In contrast to predictions of kin selection and reproductive skew models, all monogamous groups contained unrelated individuals, while two of the three polygynandrous groups were families. Moreover, although between-group variation in seasonal reproductive success was related to within-group female relatedness, relatedness among males and between the sexes had no bearing on a group's reproductive output. While kin selection may underlie helping behaviour in females, factors such as direct long-term fitness benefits of group living probably determine helping in males. Of the 14 offspring produced by fully sampled groups, at least two were sired by males from neighbouring groups: one by a breeding male and one by a nonbreeding male, suggesting that males may augment their reproductive success through extra-group paternity.     

Relatedness in wild chimpanzees: influence of paternity, male philopatry, and demographic factors

In chimpanzees (Pan troglodytes), high-ranking males are expected to have high reproductive success and females typically emigrate upon reaching maturity. Although high average relatedness among males in the same social groups has been assumed, previous reports have indicated that relatedness among males is not necessarily significantly higher than that among females. The paternity of 11 offspring and the relatedness of 50 individuals in the M group of chimpanzees at Mahale Mountains National Park, Tanzania, were investigated using DNA analyses. We determined the fathers of 10 offspring. Two different alpha males sired a total of five offspring, whereas the other males had low reproductive success. The proportion of paternal half-sibling pairs among the 10 offspring was 15.6%. The average relatedness among mature males was significantly higher than that among mature females. The existence of an old male and the long tenure of one alpha male may have contributed to this significant difference. The average dyadic relatedness among mature natal individuals was significantly higher than that in natal-immigrant pairs in which the individuals came from different groups. The average relatedness among immigrant females was similar to that in pairs of natal and immigrant females, suggesting that the immigrants came from various groups. Thus, female transfer acts to maintain low average relatedness within the group. A comparison of our results to those from other study sites suggests that although the average relatedness among adult males does not reach the level of half-siblings, under some circumstances it can exceed the relatedness of females.     

Paternal Relatedness Predicts the Strength of Social Bonds among Female Rhesus Macaques

Forming strong, equitable, and enduring social bonds with a few individuals in a group carries adaptive benefits in terms of increased longevity, offspring survival and paternity success in birds and mammals, including humans. These recent insights generated a new interest in the factors creating variation in the strength of social relationships. Whether and how animals discriminate paternal kin from non-kin and bias their social behavior accordingly is being debated. This study explores the relative importance of dominance rank, age, maternal and paternal relatedness in shaping dyadic affiliative relationships in a group of 30 captive rhesus macaque females. The strength of social relationships, measured by the composite sociality index from observational data, was independently predicted in GLMMs by both maternal and paternal relatedness as well as rank similarity. In addition, social bonds between paternal half-sisters were stronger than between distantly related kin suggesting that females biased their affiliative effort towards paternal relatives. Despite identical relatedness coefficients bonds between mothers and their daughters were three times as strong as those between full sisters. Together these results add to the growing body of evidence for paternal kin biases in affiliative behavior and highlight that females prefer descendent over lateral kin.     

Effects of Paternal Reproductive Tactic on Juvenile Behaviour and Kin Recognition in Chinook Salmon (Oncorhynchus tshawytscha)

Salmonids are characterized by alternative reproductive tactics, which can lead to an asymmetry in relatedness among offspring within nests and consequently the benefit of discriminating among nestmates. In this study, we examined the effect of paternal reproductive tactic on juvenile behaviour and kin discrimination in Chinook salmon. We created maternal half‐sibling families by collecting eggs from mature females and fertilizing one‐half with the milt of a precocious 2‐yr‐old male and the other half with the milt of a non‐precocious 4‐yr‐old male. These families were reared in full‐sibling groups for approximately 9 mo, and social interactions were then observed in groups of six fish of mixed relatedness. We found evidence for kin discrimination, as significantly less aggression was directed towards related fish than unrelated fish, and the same trends were observed regardless of whether social interactions included full‐siblings or half‐siblings. These results show that familiarity is not required to recognize kin and thereby implicate phenotype matching as the mechanism of kin recognition. We also found that the offspring of 2‐yr‐old males were larger and more aggressive than the offspring of 4‐yr‐old males, which is consistent with other studies showing that precocious males are the fastest‐growing members of their cohort. However, kin‐directed behaviours did not differ between the offspring of 2‐ and 4‐yr‐old males.     

The development of affiliative and coercive reproductive tactics in male chimpanzees

Like many animals, adult male chimpanzees often compete for a limited number of mates. They fight other males as they strive for status that confers reproductive benefits and use aggression to coerce females to mate with them. Nevertheless, small-bodied, socially immature adolescent male chimpanzees, who cannot compete with older males for status nor intimidate females, father offspring. We investigated how they do so through a study of adolescent and young adult males at Ngogo in Kibale National Park, Uganda. Adolescent males mated with nulliparous females and reproduced primarily with these first-time mothers, who are not preferred as mating partners by older males. Two other factors, affiliation and aggression, also influenced mating success. Specifically, the strength of affiliative bonds that males formed with females and the amount of aggression males directed toward females predicted male mating success. The effect of male aggression toward females on mating success increased as males aged, especially when they directed it toward females with whom they shared affiliative bonds. These results mirror sexual coercion in humans, which occurs most often between males and females involved in close, affiliative relationships.     

Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees

Humans excel in cooperative exchanges between unrelated individuals. Although this trait is fundamental to the success of our species, its evolution and mechanisms are poorly understood. Other social mammals also build long-term cooperative relationships between non-kin, and recent evidence shows that oxytocin, a hormone involved in parent–offspring bonding, is likely to facilitate non-kin as well as kin bonds. In a population of wild chimpanzees, we measured urinary oxytocin levels following a rare cooperative event—food sharing. Subjects showed higher urinary oxytocin levels after single food-sharing events compared with other types of social feeding, irrespective of previous social bond levels. Also, urinary oxytocin levels following food sharing were higher than following grooming, another cooperative behaviour. Therefore, food sharing in chimpanzees may play a key role in social bonding under the influence of oxytocin. We propose that food-sharing events co-opt neurobiological mechanisms evolved to support mother–infant bonding during lactation bouts, and may act as facilitators of bonding and cooperation between unrelated individuals via the oxytocinergic system across social mammals.     

Sexual Differences in Chimpanzee Sociality

Scientists usually attribute sexual differences in sociality to sex-specific dispersal patterns and the availability of kin within the social group. In most primates, the dispersing sex, which has fewer kin around, is the less social sex. Chimpanzees fit well into the pattern, with highly social philopatric males and generally solitary dispersing females. However, researchers in West Africa have long suggested that female chimpanzees can be highly social. We investigated whether chimpanzees in the Taï Forest (Côte d’Ivoire) exhibit the expected sexual differences in 3 social parameters: dyadic association, party composition, and grooming interactions. Though we found a significant sexual difference in each of the 3 parameters, with males being more social than females, the actual values do not reveal striking differences between the sexes and do not support the notion of female chimpanzees as asocial: females had dyadic association indices comparable to mixed-sex dyads, spent ca. 82% of their time together with other adult chimpanzees, and had a comparable number of grooming partners. Further, female associations can be among the strongest bonds within the community, indicating that both sexes can have strongly favored association partners. The findings are in contrast to reports on East African chimpanzees, the females of which are mainly solitary and rarely interact with other females. Our results suggest that researchers cannot generally regard chimpanzee females as asocial and need to redefine models deriving patterns of sociality from dispersal patterns to integrate the possibility of high female sociality in male philopatric systems.     

Inbreeding avoidance in rhesus macaques: Whose choice?

Whether nonhuman primates avoid copulating with close kin living in their social group is controversial. If sexual aversion to relatives occurs, it should be stronger in females than in males because of females' greater investment in each offspring and hence greater costs resulting from less viable offspring. Data presented here show that adult male rhesus macaques breeding in their natal groups at Cayo Santiago experienced high copulatory success, but copulated less with females of their own matrilineages than with females of other matrilineages. Adult females were never observed to copulate with males of their own matrilineage during their fertile periods. Although natal males sometimes courted their relatives, examination of two measures of female mate choice showed that females chose unrelated natal males over male kin. Female aversion to male kin was specific to the sexual context; during the birth season, females did not discriminate against their male relatives in distributing grooming. Evolved inbreeding avoidance mechanisms probably produce different outcomes at Cayo Santiago than in wild rhesus macaque populations. Gender differences in sexual aversion to relatives may be partly responsible for differences between studies in reported frequency of copulations by related pairs. © 1993 Wiley-Liss, Inc.     

Group unity of chimpanzees elucidated by comparison of sex differences in short-range interactions in Mahale Mountains National Park,Tanzania

Chimpanzees (Pan troglodytes) form multi-male and multi-female unit groups with fission–fusion grouping patterns. Short-range interaction (SRI) plays an important role in the unity of these groups and in maintaining social bonds among members. This study evaluated three models of chimpanzee social structure that differed according to the emphasis each placed on social bonds between the sexes, i.e., the male-only, the bisexual, and the male-bonded unit-group model. I investigated differences in SRI between the sexes among group members in well-habituated wild chimpanzees in Mahale Mountains National Park, Tanzania. I followed six focal adult males and six females, and quantified their respective SRI with other chimpanzees. Except between subordinate males and adult females, adults in general engaged in SRI with about 60–90% of the individuals with whom they made visual contact each day, whether in large or small parties. Although the number of social grooming (SGR) partners was limited, male–male SGR networks were wider than were either male–female or female–female SGR networks among adults. The number of contact-seeking behavior (CSB) partners was also limited, but dominant males had more CSB partners. Adult females mainly interacted by pant-grunt greeting (PGG) with adult males, but tended to do so mainly with the highest-ranking male(s) within visual contact. These results indicated that the social bonds among adult males were essential to group unity. Because of clear male dominance, adult females established peaceful coexistence with all group members despite less frequent SRI with subordinate males by maintaining affiliative social bonds with dominant males, thereby supporting the male-bonded unit-group model. Adult females had many female SRI partners, but these interactions did not involve performing conspicuous behaviors, suggesting that females maintain social bonds with other females in ways that differ from how such bonds are maintained with and between adult males.     

Co–Residence between Males and Their Mothers and Grandmothers Is More Frequent in Bonobos Than Chimpanzees

In long–lived social mammals such as primates, individuals can benefit from social bonds with close kin, including their mothers. In the patrilocal chimpanzee (Pan troglodytes spp.) and bonobo (Pan paniscus), sexually mature males reside and reproduce in their natal groups and can retain post-dependency bonds with their mothers, while immatures of both sexes might also have their paternal grandmothers available. However, quantitative information on the proportion of males and immatures that co-reside with both types of these close female relatives is limited for both species. Combining genetic parentage determination and group composition data from five communities of wild chimpanzees and three communities of wild bonobos, we estimated the frequency of co-residence between (1) mature males and their mothers, and (2) immature males and females and their paternal grandmothers. We found that adult males resided twice as frequently with their mothers in bonobos than in chimpanzees, and that immature bonobos were three times more likely to possess a living paternal grandmother than were immature chimpanzees. Patterns of female and male survivorship from studbook records of captive individuals of both species suggest that mature bonobo females survive longer than their chimpanzee counterparts, possibly contributing to the differences observed in mother–son and grandmother–immature co-residency levels. Taking into account reports of bonobo mothers supporting their sons'' mating efforts and females sharing food with immatures other than their own offspring, our findings suggest that life history traits may facilitate maternal and grandmaternal support more in bonobos than in chimpanzees.     

Adolescent male chimpanzees (Pan troglodytes) form social bonds with their brothers and others during the transition to adulthood

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.     

Male chimpanzees exchange political support for mating opportunities

Male chimpanzees, Pan troglodytes, differ from males in most other mammalian taxa because they remain in their natal communities throughout their lives, form close bonds with one another, and cooperate in a range of activities [1]. However, males also compete fiercely for status within their groups [2,3], and high rank enhances male reproductive success [4,5]. Males rely partly on coalitions to achieve and maintain status [2,3,6-9], and shifts in male alliances can have dramatic political effects [2,3,6]. It is not known what benefits are obtained by low-ranking coalition partners. Here we report that the highest-ranking (alpha) male in one well-studied community of chimpanzees rewarded his allies by allowing them preferential access to mates.     

Female relationships in bonobos(Pan paniscus)

The popular belief that women are not naturally able to bond with each other is often supported by theoretical and empirical evidence that unrelated females do not bond in nonhuman primate species. Bonobos (rare and endangered African apes, also known as pygmy chimpanzees) are (with their congener, chimpanzees) the closest living relatives of humans and appear to be an exception to this characterization. Data collected on individuals representing half of the world’s captive population reveal that bonobo females are remarkably skillful in establishing and maintaining strong affiliative bonds with each other despite being unrelated. Moreover, they control access to highly desirable food, share it with each other more often than with males, engage in same-sex sexual interactions in order to reduce tension, and form alliances in which they cooperatively attack males and inflict injuries. Their power does not stem from a size equality with or advantage over males (in fact, females average 82.5% of male size), but rather from cooperation and coalition formation. The immediate advantage to female alliances is increased control over food, the main resource on which their reproductive success depends, as well as a reduction in other costs typically associated with a female-biased dispersal system, such as male agonism in the contexts of feeding competition and sexual coercion. The ultimate advantage of friendly relationships among females is an earlier age at first reproduction, which results in a large increase in lifetime reproductive success. Analysis of this bonding phenomenon sheds light on when, where, and how we should expect unrelated human females to bond with one another by demonstrating that bonding is not dependent on access to one’s relatives but rather on an environmental situation in which female aggregation is possible, coupled with an incentive for cooperation.     

Bonds of bros and brothers: Kinship and social bonding in postdispersal male macaques

Group‐living animals often maintain a few very close affiliative relationships—social bonds—that can buffer them against many of the inevitable costs of gregariousness. Kinship plays a central role in the development of such social bonds. The bulk of research on kin biases in sociality has focused on philopatric females, who typically live in deeply kin‐structured systems, with matrilineal dominance rank inheritance and life‐long familiarity between kin. Closely related males, in contrast, are usually not close in rank or familiar, which offers the opportunity to test the importance of kinship per se in the formation of social bonds. So far, however, kin biases in male social bonding have only been tested in philopatric males, where familiarity remains a confounding factor. Here, we studied bonds between male Assamese macaques, a species in which males disperse from their natal groups and in which male bonds are known to affect fitness. Combining extensive behavioural data on 43 adult males over a 10‐year period with DNA microsatellite relatedness analyses, we find that postdispersal males form stronger relationships with the few close kin available in the group than with the average nonkin. However, males form the majority of their bonds with nonkin and may choose nonkin over available close kin to bond with. Our results show that kinship facilitates bond formation, but is not a prerequisite for it, which suggests that strong bonds are not restricted to kin in male mammals and that animals cooperate for both direct and indirect fitness benefits.     

Distribution of Affiliative Behavior Across Kin Classes and Their Fitness Consequences in Mandrills

Multimale–multifemale primate groups are ideal models to study the impact of kinship on the evolution of sociality. Indeed, the frequent combination of female philopatry and male reproductive skew produces social systems where both maternal and paternal kin are co‐resident. Several primates are known to bias their behavior toward both maternal and paternal kin. Moreover, allocation of affiliation toward paternal kin has been shown to depend on the availability in maternal kin: Female baboons invest more in paternal kin after the loss of preferred maternal kin. Here, we examined how affiliation co‐varies across kin classes in juvenile mandrills (Mandrillus sphinx), an Old World primate living in a multimale–multifemale society. While affiliation levels observed with the mother and with maternal half‐sibs co‐varied positively, especially in young females, we found that levels of affiliation among paternal half‐sibs correlated negatively with levels of affiliation among individuals from the same matriline (distant kin), possibly as a result of kin availability. In addition, in social species, social bonds between individuals have been linked to differentiated fitness consequences: More socially integrated individuals generally enjoy higher fitness. We therefore also tested whether affiliation during early life impacts fitness. We showed that the global amount of affiliation during juvenescence translated into possible reproductive benefits: Females who were more socially integrated gave birth on average a year before females that were less socially integrated. However, age at first reproduction was not predicted by the amount of affiliation exchanged with any particular kin class. These results add to the growing body of evidence demonstrating differential investment in bonding and possible social adjustments among different kin categories and emphasizing once more the adaptive value of sociality.     

雌性黄山短尾猴回避近亲交配

本研究分别在交配期(2006年9月-2006年12月)和产仔期(2007年1月-2007年4月)对黄山短尾猴鱼鳞坑YA1群中5只雄猴和5只雌猴成年个体采用目标动物法、随机取样法和连续记录法记录行为参数。研究期间记录交配行为336例:母子交配0例;母系兄妹交配7例(占2.1%),其中强行交配4例;非亲缘关系交配329例(占97.9%),非亲缘关系交配频次显著高于亲缘关系。在交配期,雄猴对亲缘雌猴跟随、性检查频次均低于非亲缘雌猴,接近指数(PMI)在亲缘和非亲缘雌猴间无显著性差异;雌猴对亲缘雄猴交配拒绝率显著高于非亲缘雄猴,接近指数在交配期显著低于非亲缘雄猴,产仔期接近指数在亲缘和非亲缘雄猴间无显著性差异。尽管雄猴在交配选择上趋于避免与亲缘雌猴交配,但某些雄猴仍会主动对有亲缘关系的雌猴邀配或强行交配,雌猴则主动回避。这些结果表明:黄山短尾猴母系亲属间可以通过行为倾向抑制近亲交配发生,且雌猴更主动回避交配,支持了近交回避的双亲投资理论。     

Relatedness and social organization of coypus in the Argentinean pampas

Behavioural and trapping studies of the social organization of coypus have suggested the occurrence of kin groups and a polygynous mating system. We used 16 microsatellite markers to analyse parentage and relatedness relationships in two populations (Jáuregui and Villa Ruiz) in the Argentinean Pampas. At Jáuregui, a dominant male monopolized most paternities, leading to a high variance in reproductive success between males and a high level of polygyny. At Villa Ruiz, variance in reproductive success was low among resident males and males were the fathers of zero to four offspring each. For females, no significant differences were found. Two different social groups in each study site were used to assess genetic relatedness within and between groups. These groups were neighbouring at Jáuregui but not at Villa Ruiz. At Villa Ruiz, coypus were significantly more related within than between groups, suggesting that behavioural groups were also genetic ones, and adult females were more related within than between groups, as should be expected for kin groups. This relationship was not found at Jáuregui. Our results provide support to previous studies based on behavioural and trapping data, which indicate that coypus form social groups and have a polygynous mating system. However, we found differences in social organization between the two populations. This is the first study to determine parentage and/or relatedness in coypus.