Male affiliation, cooperation and kinship in wild chimpanzees

Long-term field research has revealed that male chimpanzees, Pan troglodytes, affiliate and cooperate in several contexts. Assuming close genetic relationship among males, affiliative and cooperative behaviour have been hypothesized to evolve through the indirect effects of kin selection. We tested the hypothesis that matrilineal genetic relatedness affects patterns of male social affiliation and cooperation in an unusually large community of chimpanzees at the Ngogo study site, Kibale National Park, Uganda. Field observations indicated that six behavioural measures of affiliation and cooperation among 23 adult males were significantly correlated with each other. Sequences of the first hypervariable portion of the mtDNA genome revealed that three pairs of males and one quintet shared mtDNA haplotypes. Matrix permutation tests using behavioural and genetic data showed that males that affiliated and cooperated with each other were not closely related through the maternal line. These findings add to a growing body of empirical evidence that suggest kinship plays an ancillary role in structuring patterns of wild chimpanzee behaviour within social groups. Copyright 2000 The Association for the Study of Animal Behaviour.     

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.     

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.     

Alliance membership and kinship in wild male bottlenose dolphins (Tursiops aduncus) of southeastern Australia

Bottlenose dolphins are one of only a few mammalian taxa where the males are known to cooperate within their social group in order to maintain mating access to single females against other males. Male bonds in bottlenose dolphins have been hypothesized as evolving through kinship and associated inclusive fitness effects. In this study we tested whether individually identified male bottlenose dolphins preferentially associate and form alliances with kin in a small coastal resident population of southeastern Australia using a combination of behavioural data, genetic sexing, sequences of the mitochondrial DNA control region and nuclear microsatellite markers. Males generally associated significantly more often than expected with one to three other males, with whom they jointly herded females for mating. Associations and alliance membership were not associated with either maternal kinship or genetic relatedness. The majority of male pairs within alliances were randomly related, although high relatedness values were found between males of different alliances in the resident population. These findings indicate that mechanisms other than kin selection may be foremost in the development and maintenance of cooperation between male bottlenose dolphins.     

Demographic influences on the behavior of chimpanzees

Recent research has revealed substantial diversity in the behavior of wild chimpanzees. Understanding the sources of this variation has become a central focus of investigation. While genetic, ecological, and cultural factors are often invoked to explain behavioral variation in chimpanzees, the demographic context is sometimes overlooked as a contributing factor. Observations of chimpanzees at Ngogo, Kibale National Park, Uganda, reveal that the size and structure of the unit group or community can both facilitate and constrain the manifestation of behavior. With approximately 150 individuals, the Ngogo community is much larger than others that have been studied in the wild. We have taken advantage of the unusual demographic structure of this community to document new and intriguing patterns of chimpanzee behavior with respect to hunting, territoriality, and male social relationships. Chimpanzees at Ngogo hunt often and with a considerable degree of success. In addition, male chimpanzees there frequently patrol the boundary of their territory and engage in repeated bouts of lethal intergroup aggression. By forming two distinct subgroups, male chimpanzees at Ngogo also develop social bonds above the level of dyadic pairs. While the sheer number of chimpanzees contributes to differences in hunting, patrolling, mating, and subgrouping at Ngogo, the demographic situation may also constrain behavioral interactions. At Ngogo, male chimpanzees who are closely related genetically through the maternal line do not appear to affiliate or cooperate with each other. Demographic constraints may be responsible for this finding. In this paper, I use these examples to illustrate how the demographic context affects the possible range of behavioral options open to individuals and ultimately contributes to the explanation of behavioral diversity in chimpanzees.     

Male Migration in Barbary Macaques (Macaca sylvanus) at Affenberg Salem

We analyzed male migration during a 20-year period in the free-ranging Barbary macaque population of Affenberg Salem. Most natal migrations occurred around puberty, but only one third of all males left the natal group. Secondary group transfers were rare. All males immediately transferred to other bisexual groups. Migration rates were highest during periods with high adult female/male ratios within social groups. Immigrants highly preferred groups with fewer males of their own age than in the natal group, and many males immigrated into groups that had no male their own age. These groups originated from a skewed distribution of resident males during group fissions. A comparison of emigrants with their natal peers supports the inbreeding avoidance hypothesis as cause of emigration rather than the male competition avoidance hypothesis. Emigrants had no lower individual rank position and did not come from lower-ranking matrilines. Emigrants had more female maternal relatives, especially sisters. Males without female relatives almost never emigrated. Conversely, there is virtually no indication that emigrants were evicted from the natal group. Emigrants had no increased mortality. Paternity data revealed that the reproductive success of emigrants and natal males is similar, indicating that emigration had no reproductive cost. Many similarities between emigrants and natal males that separated from female maternal kin during group fissions suggest that inner migration during fissions is an alternative way to avoid maternal inbreeding. The mating system resulted in a genetic structure within social groups that largely diminished the chances for paternal inbreeding even without recognizing paternal kin.     

Mothers matter! Maternal support,dominance status and mating success in male bonobos (Pan paniscus)

Variation in male mating success is often related to rank differences. Males who are unable to monopolize oestrous females alone may engage in coalitions, thus enhancing their mating success. While studies on chimpanzees and dolphins suggest that coalitions are independent of kinship, information from female philopatric species shows the importance of kin support, especially from mothers, on the reproductive success of females. Therefore, one might expect a similar effect on sons in male philopatric species. We evaluate mating success determinants in male bonobos using data from nine male individuals from a wild population. Results reveal a steep, linear male dominance hierarchy and a positive correlation between dominance status and mating success. In addition to rank, the presence of mothers enhances the mating success of sons and reduces the proportion of matings by the highest ranking male. Mothers and sons have high association rates and mothers provide agonistic aid to sons in conflicts with other males. As bonobos are male-philopatric and adult females occupy high dominance status, maternal support extends into adulthood and females have the leverage to intervene in male conflicts. The absence of female support to unrelated males suggests that mothers gain indirect fitness benefits by supporting their sons.     

Effects of natal male alliances on aggression and power dynamics in rhesus macaques

In the wild, male rhesus macaques disperse at sexual maturity. In captivity, however, males cannot disperse from their natal groups. Thus, the presence of natal males in captive rhesus social groups is unnatural and has the potential to negatively influence group dynamics and stability. A primary difference between natal males and non-natal (immigrant) males is that natal males have the opportunity to form long-term alliances with their maternal kin as well as nonkin. We investigated the factors associated with natal males' kin alliances and the impact of these alliances on measures of natal male behavior, group dynamics, and group stability. We found that natal males more frequently formed alliances with maternal kin when they were from high-ranking matrilines, had more siblings, and were younger. More frequent kin alliances were associated with more frequent use of intense aggression, higher individual rank, and higher degree of integration within the male displacement network. Thus, it seems that natal males use their alliances to be more active and influential in the social group, which may affect group stability. It appears that juvenile natal males from high-ranking matrilines, in particular, have the largest impact on group stability. Younger natal males from high-ranking matrilines formed alliances with kin more frequently and used intense aggression more frequently than older or lower ranking males. Furthermore, groups with a higher proportion of juvenile males from high-ranking matrilines also had higher rates of wounding. We suggest that the presence of natal males in rhesus groups may act in opposition to group stability.     

Female reproductive strategies, paternity and community structure in wild West African chimpanzees

Although the variability and complexity of chimpanzee behaviour frustrates generalization, it is widely believed that social evolution in this species occurs in the context of the recognizable social group or community. We used a combination of field observations and noninvasive genotyping to study the genetic structure of a habituated community of 55 wild chimpanzees, Pan troglodytes verus, in the Ta? Forest, C?te d'Ivoire. Pedigree relationships in that community show that female mate choice strategies are more variable than previously supposed and that the observed social groups are not the exclusive reproductive units. Genetic evidence based on nuclear microsatellite markers and behavioural obser-vations reveal that females in the Ta? forest actively seek mating partners outside their social unit; noncommunity males accounted for half the paternities over 5 years. This female mating strategy increases male gene flow between communities despite male philopatry, and negates the predicted higher relatedness among community males. Kin selection seems unlikely to explain the frequent cooperation and sharing observed among group males in this population. Similarly, inbreeding avoidance is probably not the sole cause of permanent adolescent female dispersal as a combination of extragroup mating and avoidance of incest with home group males would allow females to avoid inbreeding without the hazards associated with immigration into a new community. Extragroup mating as part of chimpanzee females' reproductive strategy may allow them to choose from a wider variety and number of males, without losing the resources and support provided by their male social group partners. Copyright 1999 The Association for the Study of Animal Behaviour.     

Age differences in social interactions of young males in a chimpanzee unit-group at the Mahale Mountains National Park,Tanzania

The behavior and social interactions of young male chimpanzees were studied in relation to their age change. The data were obtained at the Mahale Mountains National Park, during a four-month period in 1986. Early adolescent males, becoming independent of their mothers, spend a long time near adults of both sexes. Late adolescent males are not tolerated by the senior males. Although such animals do not stop traveling together with their seniors, they are separated from the other members including the males of their own age class, and each of them lives a relatively lonely life. Where seniors are not nearby, they perform charging displays in front of estrous females. Young adult males tend to remain in the proximity of the alpha male, and can associate with their seniors without pant-grunting. Although some young adult males dominate over some senior males, increasingly performing charging displays, they do not appear to be permitted to associate intimately with their seniors; they are not yet considered to have attained social maturity. Prime and senior males are strongly bonded with one another, being able to associate intimately with those of their own or senior age classes including the alpha male. A young adult male's rise in rank is not connected with joining the “adult male-cluster,” nor does a senior male's decline necessarily means his dropping out from the cluster: the social position of male chimpanzees cannot be understood solely from their agonistic dominance rank. The alpha male plays a leading part in integrating the males of the unit-group. Young adult males and their seniors tend to associate most frequently with him, and all the males of the early adolescent or senior age classes pay attention to his movements.     

Social bonds enhance reproductive success in male macaques

For animals living in mixed-sex social groups, females who form strong social bonds with other females live longer and have higher offspring survival [1-3]. These bonds are highly nepotistic, but sometimes strong bonds may also occur between unrelated females if kin are rare [2, 3] and even among postdispersal unrelated females in chimpanzees and horses [4, 5]. Because of fundamental differences between the resources that limit reproductive success in females (food and safety) and males (fertilizations), it has been predicted that bonding among males should be rare and found only for kin and among philopatric males [6] like chimpanzees [7-9]. We studied social bonds among dispersing male Assamese macaques (Macaca assamensis) to see whether males in multimale groups form differentiated social bonds and whether and how males derive fitness benefits from close bonds. We found that strong bonds were linked to coalition formation, which in turn predicted future social dominance, which influenced paternity success. The strength of males' social bonds was directly linked to the number of offspring they sired. Our results show that differentiated social relationships exert an important influence on the breeding success of both sexes that transcends contrasts in relatedness.     

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.     

Adolescent male chimpanzees do not form a dominance hierarchy with their peers

Dominance hierarchies are a prominent feature of the lives of many primate species. These hierarchies have important fitness consequences, as high rank is often positively correlated with reproduction. Although adult male chimpanzees strive for status to gain fitness benefits, the development of dominance relationships is not well understood. While two prior studies found that adolescent males do not display dominance relationships with peers, additional research at Ngogo in Kibale National Park, Uganda, indicates that adolescents there form a linear dominance hierarchy. These conflicting findings could reflect different patterns of rank acquisition across sites. An alternate possibility arises from a recent re-evaluation of age estimates at Ngogo and suggests that the report describing decided dominance relationships between adolescent males may have been due to the accidental inclusion of young adult males in the sample. To investigate these issues, we conducted a study of 23 adolescent male chimpanzees of known age during 12 months at Ngogo. Adolescent male chimpanzees exchanged pant grunts, a formal signal of submission, only 21 times. Recipients of pant grunts were late adolescent males, ranging between 14 and 16 years old. In contrast, younger adolescent males never received pant grunts from other males. Aggression between adolescent males was also rare. Analysis of pant grunts and aggressive interactions did not produce a linear dominance hierarchy among adolescent males. These data indicate that adolescent male chimpanzees do not form decided dominance relationships with their peers and are consistent with the hypothesis that the hierarchy described previously at Ngogo resulted from inaccurate age estimates of male chimpanzees. Because dominance relationships develop before adulthood in other primates, our finding that adolescent male chimpanzees do not do so is surprising. We offer possible explanations for why this is the case and suggest future studies that may help clarify the matter.     

Perseverance and food sharing among closely affiliated female chimpanzees

Chimpanzees (Pan troglodytes) have been frequently observed to share food with one another, with numerous hypotheses proposed to explain why. These often focus on reciprocity exchanges for social benefits (e.g., food for grooming, food for sex, affiliation, kinship, and dominance rank) as well as sharing based on begging and deterring harassment. Although previous studies have shown that each of these hypotheses has a viable basis, they have only examined situations in which males have preferential access to food whereby females are required to obtain the food from males. For example, studies on male chimpanzee food sharing take advantage of successful crop-raids and/or acquisitions of meat from hunting, situations that only leave females access to food controlled by male food possessors. This begs the question how and with whom might a female chimpanzee in sole possession of a high-quality food item choose to share? In two large captive groups of chimpanzees, we examined each of the hypotheses with female food possessors of a high-quality food item and compared these data to a previous study examining food transfers from male chimpanzees. Our results show that alpha females shared significantly more with closely affiliated females displaying perseverance, while kinship and dominance rank had no effect. This positive interaction between long-term affiliation and perseverance shows that individuals with whom the female possessor was significantly affiliated received more food while persevering more than those with neutral or avoidant relationships towards her. Furthermore, females with avoidant relationships persevered far less than others, suggesting that this strategy is not equally available to all individuals. In comparison to the mixed-sex trials, females chose to co-feed with other females more than was observed when the alpha male was sharing food. This research indicates that male and female chimpanzees (as possessors of a desired food item) share food in ways influenced by different factors and strategies.     

Behavioural inbreeding avoidance in wild African elephants

The costs of inbreeding depression, as well as the opportunity costs of inbreeding avoidance, determine whether and which mechanisms of inbreeding avoidance evolve. In African elephants, sex-biased dispersal does not lead to the complete separation of male and female relatives, and so individuals may experience selection to recognize kin and avoid inbreeding. However, because estrous females are rare and male-male competition for mates is intense, the opportunity costs of inbreeding avoidance may be high, particularly for males. Here we combine 28 years of behavioural and demographic data on wild elephants with genotypes from 545 adult females, adult males, and calves in Amboseli National Park, Kenya, to test the hypothesis that elephants engage in sexual behaviour and reproduction with relatives less often than expected by chance. We found support for this hypothesis: males engaged in proportionally fewer sexual behaviours and sired proportionally fewer offspring with females that were natal family members or close genetic relatives (both maternal and paternal) than they did with nonkin. We discuss the relevance of these results for understanding the evolution of inbreeding avoidance and for elephant conservation.     

Life history in male mandrills (Mandrillus sphinx): physical development, dominance rank, and group association

We assess life history from birth to death in male mandrills (Mandrillus sphinx) living in a semifree-ranging colony in Gabon, using data collected for 82 males that attained at least the age of puberty, including 33 that reached adulthood and 25 that died, yielding data for their entire lifespan. We describe patterns of mortality and injuries, dominance rank, group association, growth and stature, and secondary sexual character expression across the male lifespan. We examine relationships among these variables and investigate potential influences on male life history, including differences in the social environment (maternal rank and group demography) and early development, with the aim of identifying characteristics of successful males. Sons of higher-ranking females were more likely to survive to adulthood than sons of low-ranking females. Adolescent males varied consistently in the rate at which they developed, and this variation was related to a male's own dominance rank. Males with fewer peers and sons of higher-ranking and heavier mothers also matured faster. However, maternal variables were not significantly related to dominance rank during adolescence, the age at which males attained adult dominance rank, or whether a male became alpha male. Among adult males, behavior and morphological development were related to a male's own dominance rank, and sons of high-ranking females were larger than sons of low-ranking females. Alpha males were always the most social, and the most brightly colored males, but were not necessarily the largest males present. Finally, alpha male tenure was related to group demography, with larger numbers of rival adult males and maturing adolescent males reducing the time a male spent as alpha male. Tenure did not appear to be related to characteristics of the alpha male himself.     

Paternal kin discrimination in wild baboons.

Mammals commonly avoid mating with maternal kin, probably as a result of selection for inbreeding avoidance. Mating with paternal kin should be selected against for the same reason. However, identifying paternal kin may be more difficult than identifying maternal kin in species where the mother mates with more than one male. Selection should nonetheless favour a mechanism of paternal kin recognition that allows the same level of discrimination among paternal as among maternal kin, but the hypothesis that paternal kin avoid each other as mates is largely untested in large mammals such as primates. Here I report that among wild baboons, Papio cynocephalus, paternal siblings exhibited lower levels of affiliative and sexual behaviour during sexual consortships than non-kin, although paternal siblings were not significantly less likely to consort than non-kin. I also examined age proximity as a possible social cue of paternal relatedness, because age cohorts are likely to be paternal sibships. Pairs born within two years of each other were less likely to engage in sexual consortships than pairs born at greater intervals, and were less affiliative and sexual when they did consort. Age proximity may thus be an important social cue for paternal relatedness, and phenotype matching based on shared paternal traits may play a role as well.     

Why Do African Elephants (Loxodonta africana) Simulate Oestrus? An Analysis of Longitudinal Data

Female African elephants signal oestrus via chemicals in their urine, but they also exhibit characteristic changes to their posture, gait and behaviour when sexually receptive. Free-ranging females visually signal receptivity by holding their heads and tails high, walking with an exaggerated gait, and displaying increased tactile behaviour towards males. Parous females occasionally exhibit these visual signals at times when they are thought not to be cycling and without attracting interest from musth males. Using demographic and behavioural records spanning a continuous 28-year period, we investigated the occurrence of this “simulated” oestrus behaviour. We show that parous females in the Amboseli elephant population do simulate receptive oestrus behaviours, and this false oestrus occurs disproportionately in the presence of naïve female kin who are observed coming into oestrus for the first time. We compare several alternative hypotheses for the occurrence of this simulation: 1) false oestrus has no functional purpose (e.g., it merely results from abnormal hormonal changes); 2) false oestrus increases the reproductive success of the simulating female, by inducing sexual receptivity; and 3) false oestrus increases the inclusive fitness of the simulating female, either by increasing the access of related females to suitable males, or by encouraging appropriate oestrus behaviours from female relatives who are not responding correctly to males. Although the observed data do not fully conform to the predictions of any of these hypotheses, we rule out the first two, and tentatively suggest that parous females most likely exhibit false oestrus behaviours in order to demonstrate to naïve relatives at whom to direct their behaviour.     

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.     

Rank relations of juvenile and subadult natal males of Barbary macaques (Macaca sylvanus) at Affenberg Salem

Rank relations of more than 100 juvenile and subadult natal Barbary macaque males were analyzed. Hierarchical relations among individuals of the same age were established early during the first year of life. With few exceptions concerning infants from very high-ranking genealogies, males dominated female peers regardless of maternal rank. Males started to outrank females from older cohorts during the second year of life and completed the process of rank reversal with adult females at 5-6 years of age. An age-graded dominance pattern existed among males from different birth cohorts. Only 3 rank reversals between males from different cohorts were observed. Rank reversals among males of the same birth cohort occurred more frequently. Rank position of a male among his male peers was influenced by birth order, by maternal rank, and by the presence of juvenile brothers. Most males without juvenile brothers had low positions, regardless of maternal rank. Males born late in the birth season were also low-ranking, even when juvenile brothers were present. There was no cohort where ranking among males was determined by maternal rank alone, as is the case in rhesus monkeys and Japanese macaques. Adult/subadult male carriers had no noticeable effect on rank positions of 'their' infants. It is suggested that a weaker influence of Barbary macaque mothers on rank of their sons is related to very early integration of male infants in male social/play groups.