Kinship shapes affiliative social networks but not aggression in ring-tailed coatis

Animal groups typically contain individuals with varying degrees of genetic relatedness, and this variation in kinship has a major influence on patterns of aggression and affiliative behaviors. This link between kinship and social behavior underlies socioecological models which have been developed to explain how and why different types of animal societies evolve. We tested if kinship and age-sex class homophily in two groups of ring-tailed coatis (Nasua nasua) predicted the network structure of three different social behaviors: 1) association, 2) grooming, and 3) aggression. Each group was studied during two consecutive years, resulting in four group-years available for analysis (total of 65 individuals). Association patterns were heavily influenced by agonistic interactions which typically occurred during feeding competition. Grooming networks were shaped by mother-offspring bonds, female-female social relationships, and a strong social attraction to adult males. Mother-offspring pairs were more likely to associate and groom each other, but relatedness had no effect on patterns of aggressive behavior. Additionally, kinship had little to no effect on coalitionary support during agonistic interactions. Adult females commonly came to the aid of juveniles during fights with other group members, but females often supported juveniles who were not their offspring (57% of coalitionary interactions). These patterns did not conform to predictions from socioecological models.     

Mate choice by lineage in three captive groups of rhesus macaques (Macaca mulatta)

The hypothesis that the matrilineal affiliation of 410 infants born in three captive groups of rhesus macaques is independent of the patrilineal affiliation of these infants was tested. Preferential mating with particular patrilines was observed for matrilineal members. We conclude that lineage affiliation does influence mate choice of rhesus macaques, at least when a large number of matrilines and relatively few patrilines which include natal males are represented in the group. Such nonrandom mating might explain high levels of genetic heterogeneity reported among matrilines within rhesus groups, despite high rates of male emigration, and is consistent with the maintenance of high levels of within-matriline kinship which might promote cooperative behavior among matriline members.     

Society, demography and genetic structure in the spotted hyena

Spotted hyenas (Crocuta crocuta) are large mammalian carnivores, but their societies, called 'clans', resemble those of such cercopithecine primates as baboons and macaques with respect to their size, hierarchical structure, and frequency of social interaction among both kin and unrelated group-mates. However, in contrast to cercopithecine primates, spotted hyenas regularly hunt antelope and compete with group-mates for access to kills, which are extremely rich food sources, but also rare and ephemeral. This unique occurrence of baboon-like sociality among top-level predators has favoured the evolution of many unusual traits in this species. We briefly review the relevant socio-ecology of spotted hyenas, document great demographic variation but little variation in social structure across the species' range, and describe the long-term fitness consequences of rank-related variation in resource access among clan-mates. We then summarize patterns of genetic relatedness within and between clans, including some from a population that had recently gone through a population bottleneck, and consider the roles of sexually dimorphic dispersal and female mate choice in the generation of these patterns. Finally, we apply social network theory under varying regimes of resource availability to analyse the effects of kinship on the stability of social relationships among members of one large hyena clan in Kenya. Although social bonds among both kin and non-kin are weakest when resource competition is most intense, hyenas sustain strong social relationships with kin year-round, despite constraints imposed by resource limitation. Our analyses suggest that selection might act on both individuals and matrilineal kin groups within clans containing multiple matrilines.     

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.     

Agonistic aiding: Kinship,rank, age,and sex influences

An analysis of 3,774 episodes of agonistic aiding collected during a two-year study of a rhesus monkey group (Macaca, mulatta) indicated the differential influence of kinship and rank relationships on the participation of different age-sex classes in both aid to victims and aid to aggressors. Most aiding favored victims rather than aggressors and was much more likely to occur when matrilineal kin were involved. Females were more likely to aid than were males, and the frequency of their participation increased with age. Females were much more influenced by kinship than were males and defended or aggressively supported kin against any third party regardless of dominance relationships. Adult males seldom aided against animals that were dominant to themselves; the rare exceptions occurred when adult males defended kin. Aiding was far more likely to occur if the victim was squealing, and noisy agonistic episodes often involved multiple aiders on both sides. Aiding patterns had some potential to insure dominance rank inheritance within families, in accordance with the Kawamura hypothesis. In aiding animals outside of their own matrilines, however, group members aided randomly with respect to this model. There was little evidence that aiding functioned to support individuals when they targeted animals to which they should be dominant as adults based on matrilineal dominance relationships. Most defensive aiding seemed to function primarily to defend victims (primarily kin) of aggression. Aggressive support of the attacker, on the other hand, seemed to function primarily to reinforce coalitions with the attacker. The identity of the victim was unimportant as long as it was neither kin to nor dominant to the aider. Aggressive support of attackers did not overturn existing dominance relationships.     

Kinship,association, and social relationships in rhesus monkeys (Macaca mulatta)

Data on social interactions with matrilineal kin were collected from two groups of rhesus monkeys for 6 years. All behavioral states, including time within one meter of another, involved kin more often than would be expected by chance. Significant associations were also found between kinship and the frequencies of various forms of agonistic as well as affiliative acts. Frequency of social interaction, however, was not a simple function of time in proximity. Although animals spent more time with kin than nonkin they had more aggressive interactions with kin. Moreover, aggression was biased toward the more serious forms of expression in interactions with kin. Time spent in association was neither predictive of the rate of aggressive interaction nor reduced by high rates of aggressive interaction. Rather than association time influencing rates of interaction, association time may be the consequence of a history of aggressive and affiliative exchanges. Preferential association and high rates of aggressive interaction with kin may be possible due to the existence of compensating social mechanisms nullifying the negative influence of specific aggressive encounters. © 1993 Wiley-Liss, Inc.     

A genetic analysis of group movement in an isolated population of tree-roosting bats

Group fission is an important dispersal mechanism for philopatric adults. In Cypress Hills Interprovincial Park, Saskatchewan, tree-roosting big brown bats (Eptesicus fuscus) exhibit fission-fusion roosting behaviour. During 2004-2007, the majority of females previously resident to roosting area 1 (RA1) moved to a new roosting area (RA4). We examined how genetic relationships, inferred from data for microsatellite loci and mitochondrial DNA, influenced new roost area (RA) selection during 2006 when colony members were split between the RAs. We found that females who moved to RA4 had higher average relatedness than those that remained in RA1. We found that nearly all females belonging to matrilines with high average relatedness moved to RA4 while females from matrilines with low average relatedness were split between the two RAs. These results suggest that closely related maternal kin preferentially move to new RAs. However, daily roosting preferences within a RA are not based on genetic relationships probably because daily roosting associations between kin and non-kin are used to ensure adequate roost group size. Studying the effects of kinship on the fission and movements of groups not only enhances our understanding of social behaviour and population genetics but also informs conservation decisions.     

A preliminary study of kinship and social organization in a semi-free-ranging group ofLemur catta

From long-term studies of a number of anthropoid species, many investigators have shown that kinship affinities affect social relationships. Factors such as proximity, social grooming, dominance rank, and mating patterns have been shown to be related to kinship. In this paper, we report the results of a preliminary study of the social organization of a group of prosimians (Lemur catta) in which individuals were identified and kinship affinities were known. We found that close matrilineal kin preferred to groom one another and to remain in close proximity more than did nonkin and distantly related animals. Furthermore, no copulations were observed within matrilines. These results are similar to those found in a number of species of anthropoids. This research was conducted on a semi-free-ranging group at the Duke University Primate Facility, Durham, North Carolina.     

Kinship Bonds Are Not Necessary for Maintaining Matrilineal Rank in Captive Japanese Macaques

Although kinship is of central importance in matrilineal (nepotistic) dominance systems, various lines of evidence indicate that its role has probably been overestimated. For example, alliances among nonkin, patterned on the basis of dominance per se, contribute to the maintenance of rank and to the remarkable stability of matrilineal rank orders. But because kin and nonkin alliances exert their stabilizing effects on the rank order simultaneously, the effect of nonkin alliances per se is unknown. We tested whether nonkin alliances are sufficient to ensure the stability of matrilineal rank relations in a laboratory-housed group of Japanese macaques (Macaca fuscata). We first created a group composed of two female subgroups: (1) a subordinate subgroup of close kin known to constitute an effective revolutionary alliance and (2) a dominant subgroup composed mostly of nonkin and distant kin known to support each other against lower-ranking females. In the course of 12 consecutive experimental manipulations, we reduced progressively the relative power of the dominant subgroup by manipulating its size and age composition. The members of the dominant subgroup maintained their rank in all experimental situations except when alone. Thus, nonkin alliances remained effective up to extremely pronounced levels of power imbalance. These results suggest that the remarkable stability of matrilineal rank orders is not conditional upon the existence of nepotistic alliances and strong matrilines of close kin.     

Kin in space: social viscosity in a spatially and genetically substructured network

Population substructuring is a fundamental aspect of animal societies. A growing number of theoretical studies recognize that who-meets-whom is not random, but rather determined by spatial relationships or illustrated by social networks. Structural properties of large highly dynamic social systems are notoriously difficult to unravel. Network approaches provide powerful ways to analyse the intricate relationships between social behaviour, dispersal strategies and genetic structure. Applying network analytical tools to a colony of the highly gregarious Galápagos sea lion (Zalophus wollebaeki), we find several genetic clusters that correspond to spatially determined 'network communities'. Overall relatedness was low, and genetic structure in the network can be interpreted as an emergent property of philopatry and seems not to be primarily driven by targeted interactions among highly related individuals in family groups. Nevertheless, social relationships between directly adjacent individuals in the network were stronger among genetically more similar individuals. Taken together, these results suggest that even small differences in the degree of relatedness can influence behavioural decisions. This raises the fascinating prospect that kin selection may also apply to low levels of relatedness within densely packed animal groups where less obvious co-operative interactions such as increased tolerance and stress reduction are important.     

Kin structure and social organization in the spotted eagle ray,Aetobatus narinari,off coastal Sarasota,FL

Observations of elasmobranchs in groups suggest sociality in sharks and rays. However we currently lack a strong understanding of social structure and the role kinship has in structuring group organization in cartilaginous fishes. The spotted eagle ray, Aetobatus narinari (Euphrasen, 1790) frequents the shallow waters near Sarasota, FL, often in pairs or groups suggesting a social component to their behavior. In the present study, eight eagle ray-specific microsatellite markers were used to investigate relatedness in A. narinari groups, and used to determine if kin structure contributed to group organization. Using regression-based and maximum-likelihood approaches, relatedness was quantified and compared within and among groups of juveniles, and adults in mixed sex and same sex groups. Results showed a lack of kin-structured sociality in A. narinari, suggesting factors apart from relatedness shape social interactions among spotted eagle rays in the near-shore waters of Sarasota, FL. Our results add to the limited amount of published literature on elasmobranch kinship, which are important for understanding implications of anthropogenic disturbance on genetic variability for coastal populations.     

Cooperative investment in public goods is kin directed in communal nests of social birds

The tragedy of the commons predicts social collapse when public goods are jointly exploited by individuals attempting to maximize their fitness at the expense of other social group members. However, animal societies have evolved many times despite this vulnerability to exploitation by selfish individuals. Kin selection offers a solution to this social dilemma, but in large social groups mean relatedness is often low. Sociable weavers (Philetairus socius) live in large colonies that share the benefits of a massive communal nest, which requires individual investment for construction and maintenance. Here, we show that despite low mean kinship within colonies, relatives are spatially and socially clustered and that nest‐building males have higher local relatedness to other colony members than do non‐building males. Alternative hypotheses received little support, so we conclude that the benefits of the public good are shared with kin and that cooperative investment is, despite the large size and low relatedness of these communities, kin directed.     

Bell miner provisioning calls are more similar among relatives and are used by helpers at the nest to bias their effort towards kin

Kin selection predicts that helpers in cooperative systems should preferentially aid relatives to maximize fitness. In family-based groups, this can be accomplished simply by assisting all group members. In more complex societies, where large numbers of kin and non-kin regularly interact, more sophisticated kin-recognition mechanisms are needed. Bell miners (Manorina melanophrys) are just such a system where individuals regularly interact with both kin and non-kin within large colonies. Despite this complexity, individual helpers of both sexes facultatively work harder when provisioning the young of closer genetic relatedness. We investigated the mechanism by which such adaptive discrimination occurs by assessing genetic kinship influences on the structure of more than 1900 provisioning vocalizations of 185 miners. These 'mew' calls showed a significant, positive linear increase in call similarity with increasing genetic relatedness, most especially in comparisons between male helpers and the breeding male. Furthermore, individual helping effort was more heavily influenced by call similarity to breeding males than to genetic relatedness, as predicted if call similarity is indeed the rule-of-thumb used to discriminate kin in this system. Individual mew call structure appeared to be inflexible and innate, providing an effective mechanism by which helpers can assess their relatedness to any individual. This provides, to our knowledge, the first example of a mechanism for fine-scale kin discrimination in a complex avian society.     

Amazonian horticulturalists live in larger,more related groups than hunter–gatherers

The relatedness of human groups has important ramifications for kin (group) selection to favor more collective action and invites the potential for more exploitation by political leaders. Endogamous marriages among kin create intensive kinship systems with high group relatedness, while exogamous marriages among nonrelatives create extensive kinship with low group relatedness. Here, a sample of 58 societies (7,565 adults living in 353 residential groups) shows that average group relatedness is higher in lowland horticulturalists than in hunter–gatherers. Higher relatedness in horticulturalists is remarkable given that village sizes are larger, harboring over twice the average number of adults than in hunter–gatherer camps. The relatedness differential between subsistence regimes increases for larger group sizes. Large and dense networks of kin may have favored an increased propensity for some forms of in-group cooperation and political inequality that emerged relatively recently in human history, after the advent of farming.     

Fitness consequences of spousal relatedness in 46 small-scale societies

Social norms that regulate reproductive and marital decisions generate impressive cross-cultural variation in the prevalence of kin marriages. In some societies, marriages among kin are the norm and this inbreeding creates intensive kinship networks concentrated within communities. In others, especially forager societies, most marriages are between more genealogically and geographically distant individuals, which generates a larger number of kin and affines of lesser relatedness in more extensive kinship networks spread out over multiple communities. Here, we investigate the fitness consequence of kin marriages across a sample of 46 small-scale societies (12 439 marriages). Results show that some non-forager societies (including horticulturalists, agriculturalists and pastoralists), but not foragers, have intensive kinship societies where fitness outcomes (measured as the number of surviving children in genealogies) peak at commonly high levels of spousal relatedness. By contrast, the extensive kinship systems of foragers have worse fitness outcomes at high levels of spousal relatedness. Overall, societies with greater levels of inbreeding showed a more positive relationship between fitness and spousal relatedness.     

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.     

Network stability is a balancing act of personality, power, and conflict dynamics in rhesus macaque societies

Stability in biological systems requires evolved mechanisms that promote robustness. Cohesive primate social groups represent one example of a stable biological system, which persist in spite of frequent conflict. Multiple sources of stability likely exist for any biological system and such robustness, or lack thereof, should be reflected and thus detectable in the group's network structure, and likely at multiple levels. Here we show how network structure and group stability are linked to the fundamental characteristics of the individual agents in groups and to the environmental and social contexts in which these individuals interact. Both internal factors (e.g., personality, sex) and external factors (e.g., rank dynamics, sex ratio) were considered from the level of the individual to that of the group to examine the effects of network structure on group stability in a nonhuman primate species. The results yielded three main findings. First, successful third-party intervention behavior is a mechanism of group stability in rhesus macaques in that successful interventions resulted in less wounding in social groups. Second, personality is the primary factor that determines which individuals perform the role of key intervener, via its effect on social power and dominance discrepancy. Finally, individuals with high social power are not only key interveners but also key players in grooming networks and receive reconciliations from a higher diversity of individuals. The results from this study provide sound evidence that individual and group characteristics such as personality and sex ratio influence network structures such as patterns of reconciliation, grooming and conflict intervention that are indicators of network robustness and consequent health and well-being in rhesus macaque societies. Utilizing this network approach has provided greater insight into how behavioral and social processes influence social stability in nonhuman primate groups.     

Strategies for determining kinship in wild populations using genetic data

Knowledge of kin relationships between members of wild animal populations has broad application in ecology and evolution research by allowing the investigation of dispersal dynamics, mating systems, inbreeding avoidance, kin recognition, and kin selection as well as aiding the management of endangered populations. However, the assessment of kinship among members of wild animal populations is difficult in the absence of detailed multigenerational pedigrees. Here, we first review the distinction between genetic relatedness and kinship derived from pedigrees and how this makes the identification of kin using genetic data inherently challenging. We then describe useful approaches to kinship classification, such as parentage analysis and sibship reconstruction, and explain how the combined use of marker systems with biparental and uniparental inheritance, demographic information, likelihood analyses, relatedness coefficients, and estimation of misclassification rates can yield reliable classifications of kinship in groups with complex kin structures. We outline alternative approaches for cases in which explicit knowledge of dyadic kinship is not necessary, but indirect inferences about kinship on a group‐ or population‐wide scale suffice, such as whether more highly related dyads are in closer spatial proximity. Although analysis of highly variable microsatellite loci is still the dominant approach for studies on wild populations, we describe how the long‐awaited use of large‐scale single‐nucleotide polymorphism and sequencing data derived from noninvasive low‐quality samples may eventually lead to highly accurate assessments of varying degrees of kinship in wild populations.     

Fine‐scale genetic structure and helping decisions in a cooperatively breeding bird

In animal societies, characteristic demographic and dispersal patterns may lead to genetic structuring of populations, generating the potential for kin selection to operate. However, even in genetically structured populations, social interactions may still require kin discrimination for cooperative behaviour to be directed towards relatives. Here, we use molecular genetics and long‐term field data to investigate genetic structure in an adult population of long‐tailed tits Aegithalos caudatus, a cooperative breeder in which helping occurs within extended kin networks, and relate this to patterns of helping with respect to kinship. Spatial autocorrelation analyses reveal fine‐scale genetic structure within our population, such that related adults of either sex are spatially clustered following natal dispersal, with relatedness among nearby males higher than that among nearby females, as predicted by observations of male‐biased philopatry. This kin structure creates opportunities for failed breeders to gain indirect fitness benefits via redirected helping, but crucially, most close neighbours of failed breeders are unrelated and help is directed towards relatives more often than expected by indiscriminate helping. These findings are consistent with the effective kin discrimination mechanism known to exist in long‐tailed tits and support models identifying kin selection as the driver of cooperation.