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.     

Long-Term Trends in Matrilineal Inbreeding Among the Japanese Macaques of Arashiyama B Troop

In a long-term study of sexual behavior in Japanese macaques, we found that matrilineal inbreeding accounted for 2.9% of the copulations recorded for the Arashiyama B troop during 7 mating seasons between 1968 and 1984. Of the 906 copulatory dyads, 46 (5.1%) occurred among kin. Close matrilineal kin dyads (r = 1/2–1/8, 1.1% of the total of copulatory dyads) strongly avoided matrilineal inbreeding, but for remote kin dyads (r > 1/8, 4.0% of the total) the tendency was weaker in some years. Among the possible determinants of matrilineal inbreeding, we found that it tended to occur among younger and lower-ranking males as an effect of troop demographic changes. There is no significant association between female rank and matrilineal inbreeding. Our results are consistent with the hypothesis that different degrees of kin relatedness are discriminated by individuals with respect to mate choice.     

The Genetic Relatedness in Groups of Joint-Nesting Taiwan Yuhinas: Low Genetic Relatedness with Preferences for Male Kin

The relative importance of direct and indirect fitness and, thus, the role of kinship in the evolution of social behavior is much debated. Studying the genetic relatedness of interacting individuals is crucial to improving our understanding of these issues. Here, we used a seven-year data set to study the genetic structure of the Taiwan yuhina (Yuhina brunneciceps), a joint-nesting passerine. Ten microsatellite loci were used to investigate the pair-wised relatedness among yuhina breeding group members. We found that the average genetic relatedness between same-sex group members was very low (0.069 for male dyads and 0.016 for female dyads). There was also a low ratio of closely-related kin (r>0.25) in the cooperative breeding groups of yuhinas (21.59% and 9.68% for male and female dyads, respectively). However, the relatedness of male dyads within breeding groups was significantly higher than female dyads. Our results suggest that yuhina cooperation is maintained primarily by direct fitness benefits to individuals; however, kin selection might play a role in partner choice for male yuhinas. Our study also highlights an important, but often neglected, question: Why do animals form non-kin groups, if kin are available? We use biological market theory to propose an explanation for group formation of unrelated Taiwan yuhinas.     

Social relations between adult males and females of Japanese monkeys in the arashiyama B troop

Some dyads of Japanese monkey adult males and females show remarkable spatial proximity and frequent exchanges of social behaviors. It is suggested that some kind of “affinity” exists between them. Females obtain much unilateral benefit from “proximity effects”; even lowranking females can dominate high-ranking females as long as they stay nearby their “affinitive” males. Males acquire female followers in return. Mating relations and female mother-daughter relations play important roles in forming new “affinitive relations.” Once monkeys have formed “affinitive relations,” however, they seldom mate with each other, as if they were kin-related. Therefore, the acquisition of female followers appears inconsistent with a male's strategy for reproducing many genes in the next generation. This study was financed partly by the Cooperative Research Fund of the Primate Research Institute, Kyoto University. The outline of this paper has already been published inTakahata (1980b).     

Components of Relationship Quality in Chimpanzees

A novel approach to studying social relationships in captive adult chimpanzees ( Pan troglodytes ) was taken by using principal components analysis (PCA) to extract three key components of relationship quality from nine behavioural variables. Based on the loadings of the behavioural variables, the components appeared to match previously hypothesized critical aspects of social relationships and were therefore labelled Value, Compatibility and Security. The effects of kinship, sex combination, age difference and time spent together on each of the relationship quality components were analysed. As expected, kin were found to have more valuable, compatible and secure relationships than non-kin. Female–female dyads were found to be more compatible than male–male or mixed-sex dyads, whereas the latter were found to be most secure. Partners of a similar age were found to have more secure and more valuable relationships than those with a larger age gap. Individuals that were together in the group for longer were more valuable and more compatible, but their relationships were found to be less secure than individuals that were together in the group for a shorter time. Although some of the results may be unexpected based on chimpanzee socio-ecology, they fit well overall with the history and social dynamics of the study group. The methods used confer a significant advantage in producing quantitative composite measures of each component of relationship quality, obtained in an objective manner. These findings therefore promote the use of such measures in future studies requiring an assessment of the qualities of dyadic social relationships.     

Huddling relationships in night sleeping groups among wild Japanese macaques in Kinkazan Island during winter

Huddling groups at sleeping sites, and allogrooming and proximity in the daytime during winter, were examined in a wild Japanese macaque (Macaca fuscata) troop on Kinkazan Island in the non-snowy district of northern Japan. All sleeping groups, defined as a cluster in which individuals huddle at sleeping sites, were formed on the ground. Their sizes tended to increase when the temperature was lower. The number of adults with mutual physical contact in sleeping groups increased when the size of sleeping groups increased. These results suggest that the physiological function of huddling is protection from low temperatures, and that macaques select the ground as sleeping sites to form large sized groups. Huddling was performed most frequently among kin dyads. Non-related dyads which appeared to be affiliative in the daytime also huddled frequently at sleeping sites. Even non-related dyads which showed affiliative behavior less frequently in the daytime exhibited huddling, at night, however, they did so less often than those of kin dyads and affiliated dyads. It appears that huddling at night by pairs that did not normally affiliate in the daytime was made possible by the increased tolerance of individuals responding to colder temperatures at night in winter. Furthermore, huddling, grooming, and proximity were exhibited at greater frequency between kin dyads, and between high-ranking males and specific females of kin groups, although the dyads of individuals older than 15 years often were involved only in huddling. These results suggest that two types of social bonds exist at sleeping sites in winter. One is the social bond common to both the daytime and nighttime, the other is peculiar to nighttime. Consequently, the social function of huddling is that, troop integration might increase at sleeping sites in winter as close social relationships among adults are extended more widely than those in daytime.     

Population Genetics,Dispersal, and Kinship Among Wild Squirrel Monkeys (Saimiri sciureus macrodon): Preferential Association Between Closely Related Females and Its Implications for Insect Prey Capture Success

Little genetic information is available to evaluate hypotheses concerning the parameters that affect population genetic structure in primate taxa that exhibit interspecific variation in social systems, such as squirrel monkeys (Saimiri). Here, we used genetic data to assess dispersal patterns, kin structure, and preferential association with same-sex kin in a wild population of Saimiri sciureus macrodon. We also analyzed behavioral data to assess whether individuals that maintain shorter interindividual distances show increased insect foraging success. If there was greater male than female dispersal, then we expected mean pairwise relatedness, F _ST values, and intragroup mean corrected assignment indices to be greater among adult females than among adult males. We also expected matrices of pairwise affinity indices (PAIs) for “association” (time spent ≤5 m) and “proximity” (time spent ≤10 m) among female dyads to positively correlate with a matrix of female pairwise relatedness. Not only did we find support for female philopatry, but we also found significant positive relationships between the relatedness matrix and each of the PAI matrices: females were more likely to be associated with (and proximal to) close female relatives than more distant relatives or unrelated individuals. Foraging analyses revealed that females had higher insect capture rates than males, and this sex difference may be related to a smaller mean interindividual distance among closely related female group members. Our result shows how estimates of genetic relatedness are useful for testing predictions regarding the evolution of sex-biased dispersal patterns, as well as potential relationships between kin-biased social behaviors and foraging success.     

Association patterns and kinship in female reindeer (Rangifer tarandus) during rut

Non-random association of females has been reported in many social species, with kinship being the main mechanism in shaping these associations. Understanding the patterns of association during rut is particularly important in polygynous animals, as this may have implications for inbreeding vulnerability and genetic structuring of populations. However, these patterns are highly dynamic and may be influenced by the population sex ratio and male age structure. We examined females' association in reindeer (Rangifer tarandus), a highly polygynous ungulate, to determine whether genetically related females associate more often than non-kin during rut and whether this association was influenced by the aforementioned factors. During three rutting seasons the male age structure and the sex ratio of the herd was manipulated: two extremely female biased sex ratios, one with only adult males and one with only young males, whereas the third being closer to a more even sex ratio and male age structure. We found that genetic relatedness influenced female association in the mixed male age group, but not in the adult and young male age groups. Highly related females (relatedness ??0.5) associated more closely than unrelated females. Further, period of the rut as well as male age structure and sex ratio had a significant effect on female association. Our study suggests that the female reindeer association during rut is not only influenced by preference for kin but also by male?Cmale competition and male age as well.     

Between-Group Variation in Female Dispersal,Kin Composition of Groups,and Proximity Patterns in a Black-and-White Colobus Monkey (Colobus vellerosus)

A growing body of evidence shows within-population variation in natal dispersal, but the effects of such variation on social relationships and the kin composition of groups remain poorly understood. We investigate the link between dispersal, the kin composition of groups, and proximity patterns in a population of black-and-white colobus (Colobus vellerosus) that shows variation in female dispersal. From 2006 to 2011, we collected behavioral data, demographic data, and fecal samples of 77 males and 92 females residing in eight groups at Boabeng-Fiema, Ghana. A combination of demographic data and a genetic network analysis showed that although philopatry was female-biased, only about half of the females resided in their natal groups. Only one group contained female-female dyads with higher average relatedness than randomly drawn animals of both sexes from the same group. Despite between-group variation in female dispersal and kin composition, female-female dyads in most of the study groups had higher proximity scores than randomly drawn dyads from the same group. We conclude that groups fall along a continuum from female dispersed, not kin-based, and not bonded to female philopatric, kin-based, and bonded. We found only partial support for the predicted link between dispersal, kin composition, and social relationships. In contrast to most mammals where the kin composition of groups is a good predictor of the quality of female-female relationships, this study provides further support for the notion that kinship is not necessary for the development and maintenance of social bonds in some gregarious species.     

Smelling right: the scent of male lemurs advertises genetic quality and relatedness

Sexual selection theory predicts that competitors or potential mates signal their quality or relatedness to conspecifics. Researchers have focused on visual or auditory modes of signal transmission; however, the importance of olfactory indicators is gaining recognition. Using a primate model and a new integrative analytical approach, we provide the first evidence relating male olfactory cues to individual genome-wide heterozygosity and to the genetic distance between individuals. The relationships between male semiochemical profiles and genetic characteristics are apparent only during the highly competitive and stressful breeding season. As heterozygosity accurately predicts health and survivorship in this population, we identify scrotal olfactory cues as honest indicators of male quality, with relevance possibly to both sexes. Beyond showing that semiochemicals could underlie kin recognition and nepotism, we provide a putative olfactory mechanism to guide male–male competition and female mate choice.     

Interindividual interactions of Molina’s hog-nosed skunksConepatus chinga in the Pampas grassland of Argentina

During one year, we radiotracked two female and two male Molina’s hog-nosed skunksConepatus chinga (Molina, 1782), a little studied mephitid, in the Pampas of central Argentina, to analyze the static and dynamic interactions between individuals. Mean home range overlap was large (44.5%), but males shared a smaller proportion of their home ranges than females. The average percentage of localizations in the overlap area (39.3%) indicates that these areas were not marginal sections of individual home ranges, but this value was greater for individuals of different genders than intrasexual dyads. The Coefficient of Spatial Association confirmed that the distances between individuals of different sexes were smaller than between animals of the same sex. During simultaneous locations, females were closer than males, but reciprocal distances between individuals varied over the time. These patterns are congruent with those described as typical for mustelids and mephitids. Our results confirm that an analysis of home range overlap should not be considered complete without the study of dynamic interactions among individuals and their temporal variations, which are necessary to overcome the limitations of spatial overlap analysis.     

Risk is a Component of Social Relationships in Spider Monkeys

In group‐living animals, social relationships are the result of the interactions between two individuals over time and can provide fitness benefits to both the participants. Recently, components of social relationships were identified in Old World primates and ravens through the use of principal component analysis (PCA). We employed PCA to identify components that define the social relationships in two communities of wild spider monkeys in the Yucatán Peninsula, Mexico and investigated whether characteristics of the dyads, such as age combination, sex combination and kinship, had an effect on the components obtained. We found two components. Component 1 had high positive loadings of proximity, grooming and subgroup index, which may reflect value or compatibility. Embrace and aggression rates loaded highly on Component 2, which was labelled risk. Component 1 was affected by kinship: kin had higher scores than non‐kin. Both the components were affected by sex combination of the dyad. Male–male dyads had higher scores than female–male and female–female dyads. The results are in accordance with what is currently known about spider monkeys’ social relationships, but provide an additional perspective with the novel component of risk. In this respect, the two components are effective in capturing the ambiguous nature of male–male relationships in spider monkeys. Overall, this study offers further insight into the social patterns underlying the relationship quality in group‐living animals and the usefulness of PCA in providing an objective assessment that reflects the animals′ perspective of their social interactions.     

Fine-Scale Spatial Organization Reflects Genetic Structure in Sheep

Preferential spatial associations between related animals have been reported in several species, but whether these relationships extend to fine resolution is largely unknown. Using a novel approach that combined pedigrees and precise geographic locations, we tested the relationship between extremely fine-scale (<3 m) spatial structure and relatedness within a captive flock of domestic female Dorset sheep ( Ovis aries ). Using GPS, we recorded the spatial distribution of individuals while foraging on summer pasture; we compared this to pair-wise coefficients of relatedness (r) and assessed significance of the patterns using Mantel and partial Mantel tests. Population organization was discernible even at this fine spatial resolution. Closely related ewes, especially full- and half-siblings (r ≥ 0.25), formed closer spatial associations than lesser-related and unrelated pairs. The genetic structuring of the flock provides a potential platform for kin selection and suggests that random population organization may not exist even at the finest spatial scales.     

Relatedness and genetic structure in a socially polymorphic population of the spider Anelosimus studiosus

The evolution of sociality remains a challenge in evolutionary biology and a central question is whether association between kin is a critical factor favouring the evolution of cooperation. This study examines genetic structure of Anelosimus studiosus, a spider exhibiting polymorphic social behaviour. Two phenotypes have been identified: an ‘asocial’ phenotype with solitary female nests and a ‘social’ phenotype with multi‐female/communal nests. To address the questions of whether these phenotypes are differentiated populations and whether cooperative individuals are closely related, we used microsatellites to analyse individuals from both communal and solitary nests. We found no evidence of differentiation between social and solitary samples, implying high rates of interbreeding. This is consistent with the hypothesis that these phenotypes coexist as a behavioural polymorphism within populations. Pairwise relatedness coefficients were used to test whether cooperating individuals are more closely related than expected by chance. Pairwise relatedness of females sharing communal webs averaged 0.25, the level expected for half‐siblings and significantly more closely related than random pairs from the population. Solitary females collected at similar distances to the communal spider pairs were also more closely related than expected by chance (mean relatedness = 0.18), but less related than social pairs. These results imply that low dispersal contributes to increase likelihood of interaction between kin, but relatedness between social pairs is not explained by spatial structure alone. We propose that these phenotypes represent stages in the evolution of sociality, where viscous population structure creates opportunities for kin selection and cooperation is favoured under certain environmental conditions.     

Male–Female Association Patterns Among Free-ranging Chimpanzees (Pan troglodytes schweinfurthii)

Although male–female relationships can offer a number of advantages such as protection or social support, they are poorly studied among primates compared to same-sex relationships. We used 12 yr of data from the Kanyawara chimpanzee community to compare three independent measures of association (party association, 5m association, and grooming) among all adult dyads. Party association exhibited by male–female dyads was of intermediate strength between strong male–male and weak female–female association. Male–female dyads were less likely to be within 5m of one another and to groom as male–male dyads, but equally likely to be within 5m and more likely to groom as female–female dyads. Variation in male–female association strength was not related to male rank but was affected by female ranging patterns and female reproductive states. Females with core areas in the center of the home range were more likely to be in parties with males but did not show higher spatial proximity or grooming indices compared to females ranging in the periphery. Party association and 5m indices were higher for dyads of males and estrous females compared to those with anestrous females. These results indicate that male–female dyads are likely to associate with one another more often than female–female dyads because of overlapping ranging patterns and short-term changes in female reproductive state. We conclude that male and female chimpanzees do not exhibit proximity and grooming patterns indicative of strong affiliative bonds. This study also highlights the importance of using multiple independent measures of bond strength in studies of primate social dynamics.     

Kin assortment in juvenile shoals in wild guppy populations

Grouping provides many potential benefits to individuals in terms of foraging and anti-predator protection. However, it has been suggested that individuals could gain additional benefits in terms of indirect fitness by grouping with kin. Surprisingly, the genetic composition of wild fish shoals and the importance of kin-associated shoaling remain poorly understood. The Trinidadian guppy (Poecilia reticulata) has life history traits that might promote kin structure of shoals such as internal fertilisation and small brood size in contrast to many other fish species. Even though previous studies did not find any indication of kin structure in shoals of adult guppies, it is possible that related juveniles remain together in shoals, partly because of lower mobility and because the advantages of kin association may change with age. Using 10 microsatellite markers, we conducted a genetic analysis on 40 shoals from four populations. Pair-wise relatedness was inferred using a modified version of the software package COLONY and permutation tests were conducted to test the hypothesis that kin occur together in juvenile shoals more often than expected by chance. The frequency of sib dyads among juveniles within shoals was significantly larger than that between shoals in two high predation populations but not in two low predation populations. This finding contributes to the understanding of factors underlying shoal composition and highlights the potential of recent methodological advances for detecting such relationships.     

The Influence of Kinship on Familiar Natal Migrant Rhesus Macaques (Macaca mulatta)

In most primate species, females remain in the natal group with kin while males disperse away from kin around the time of puberty. Philopatric females bias their social behavior toward familiar maternal and paternal kin in several species, but little is known about kin bias in the dispersing sex. Male dispersal is likely to be costly because males encounter an increased risk of predation and death, which might be reduced by dispersing together with kin and/or familiar males (individuals that were born and grew up in same natal group) or into a group containing kin and/or familiar males. Here we studied the influence of kinship on familiar natal migrant rhesus macaques (Macaca mulatta) on Cayo Santiago, Puerto Rico, by combining demographic, behavioral, and genetic data. Our data suggest that kinship influences spatial proximity between recent natal immigrants and males familiar to them. Immigrants were significantly nearer to more closely related familiar males than to more distantly related individuals. Within a familiar subgroup, natal migrants were significantly closer to maternal kin, followed by paternal kin, then non-kin, and finally to males related via both the maternal and paternal line. Spatial proximity between natal immigrants and familiar males did not decrease over time in the new group, suggesting that there is no decline in associations between these individuals within the first months of immigration. Overall, our results might indicate that kinship is important for the dispersing sex, at least during natal dispersal when kin are still available.     

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.     

MHC-mediated spatial distribution in brown trout (Salmo trutta) fry

Major histocompatibility complex (MHC) class I-linked microsatellite data and parental assignment data for a group of wild brown trout (Salmo trutta L.) provide evidence of closer spatial aggregation among fry sharing greater numbers of MHC class I alleles under natural conditions. This result confirms predictions from laboratory experiments demonstrating a hierarchical preference for association of fry sharing MHC alleles. Full-siblings emerge from the same nest (redd), and a passive kin association pattern arising from limited dispersal from the nest (redd effect) would predict that all such pairs would have a similar distribution. However, this study demonstrates a strong, significant trend for reduced distance between pairs of full-sibling fry sharing more MHC class I alleles reflecting their closer aggregation (no alleles shared, 311.5 ± (s.e.)21.03 m; one allele shared, 222.2 ± 14.49 m; two alleles shared, 124.9 ± 23.88 m; P<0.0001). A significant trend for closer aggregation among fry sharing more MHC class I alleles was also observed in fry pairs, which were known to have different mothers and were otherwise unrelated (ML-r = 0) (no alleles: 457.6 ± 3.58 m; one allele (422.4 ± 3.86 m); two alleles (381.7 ± 10.72 m); P<0.0001). These pairs are expected to have emerged from different redds and a passive association would then be unlikely. These data suggest that sharing MHC class I alleles has a role in maintaining kin association among full-siblings after emergence. This study demonstrates a pattern consistent with MHC-mediated kin association in the wild for the first time.     

Social Relationships among Males in Multimale Siamang Groups

I quantified social and spatial interactions among adults in 4 multimale siamang (Symphalangus syndactylus) groups to evaluate the importance of aggression and avoidance in mediating male-male relationships. Actual genetic relationships among adults are unknown, but available mitochondrial data suggest that in 3 of 4 groups, neither male was the offspring or maternal sibling of the female, whereas in the fourth group, a matrilineal relationship between the female and 1 adult male was not excluded. Rates of aggression involving male-male dyads were very low. One male-female dyad maintained closer spatial cohesion than those of other adult dyads in 3 of 4 groups. Nonetheless, all adult males spent substantial percentages of their time ≤20 m from other adults in their groups. The percentages of time that male-male dyads spent in social grooming interactions did not differ from those of male-female dyads. In 3 groups, both males copulated with the group female. While previous studies have reported high rates of aggression between adult males and subadult male group members in siamangs, my results suggest that male-male relationships in multimale groups at Way Canguk were relatively harmonious. Acceptance of multimale grouping (and in some cases sexual polyandry) suggests that the benefits outweigh the costs under some circumstances. If there was a genetic relationship between males, then tolerance of delayed dispersal and copulation with the adult female may function as a form of parental investment. Males may also benefit from multimale grouping via enhanced territorial defense or reduced costs of mate defense.