Detecting instability in animal social networks: genetic fragmentation is associated with social instability in rhesus macaques

The persistence of biological systems requires evolved mechanisms which promote stability. Cohesive primate social groups are one example of stable biological systems, which persist in spite of regular conflict. We suggest that genetic relatedness and its associated kinship structure are a potential source of stability in primate social groups as kinship structure is an important organizing principle in many animal societies. We investigated the effect of average genetic relatedness per matrilineal family on the stability of matrilineal grooming and agonistic interactions in 48 matrilines from seven captive groups of rhesus macaques. Matrilines with low average genetic relatedness show increased family-level instability such as: more sub-grouping in their matrilineal groom network, more frequent fighting with kin, and higher rates of wounding. Family-level instability in multiple matrilines within a group is further associated with group-level instability such as increased wounding. Stability appears to arise from the presence of clear matrilineal structure in the rhesus macaque group hierarchy, which is derived from cohesion among kin in their affiliative and agonistic interactions with each other. We conclude that genetic relatedness and kinship structure are an important source of group stability in animal societies, particularly when dominance and/or affilative interactions are typically governed by kinship.     

Grooming network cohesion and the role of individuals in a captive chimpanzee group

Social network analysis offers new tools to study the social structure of primate groups. We used social network analysis to investigate the cohesiveness of a grooming network in a captive chimpanzee group (N = 17) and the role that individuals may play in it. Using data from a year-long observation, we constructed an unweighted social network of preferred grooming interactions by retaining only those dyads that groomed above the group mean. This choice of criterion was validated by the finding that the properties of the unweighted network correlated with the properties of a weighted network (i.e. a network representing the frequency of grooming interactions) constructed from the same data. To investigate group cohesion, we tested the resilience of the unweighted grooming network to the removal of central individuals (i.e. individuals with high betweenness centrality). The network fragmented more after the removal of individuals with high betweenness centrality than after the removal of random individuals. Central individuals played a pivotal role in maintaining the network's cohesiveness, and we suggest that this may be a typical property of affiliative networks like grooming networks. We found that the grooming network correlated with kinship and age, and that individuals with higher social status occupied more central positions in the network. Overall, the grooming network showed a heterogeneous structure, yet did not exhibit scale-free properties similar to many other primate networks. We discuss our results in light of recent findings on animal social networks and chimpanzee grooming.     

The value of grooming to female primates

Current socioecological models suggest that the structure of female-bonded primate groups is predicated on the need for coalitionary support in competitive interactions. Social grooming is thought to be the means by which females ensure support from other individuals, either by the direct exchange of grooming for aid or by using grooming as a means of strengthening social bonds. Since these relationships are valuable, they must be regularly serviced and must be repaired if they become damaged. We question this position and show that empirical evidence to support these theoretical arguments is lacking. We then go on to present a new framework in which the inconsistencies regarding grooming and relationship negotiation are interpreted in the context of individual decision-making processes. In this framework, primate groups represent biological markets in which individuals either trade grooming in a reciprocal manner for the direct benefits that grooming itself offers, or exchange it for tolerance by more powerful animals. A number of testable predictions are derived from this hypotheses. The need for socioecological studies to focus on the dynamics of individual relationships rather than using summary measures is emphasized since only a detailed knowledge of serial interaction will provide the key to understanding the complexities of individual decision-making processes.     

The dining etiquette of desert baboons: the roles of social bonds, kinship, and dominance in co-feeding networks

To better understand how individual relationships influence patterns of social foraging in primate groups, we explored networks of co-feeding in wild desert baboons (Papio ursinus). To minimize the risk of aggression and injury associated with contest competition, we expected that individual group members would choose to co-feed with those group-mates that are most likely to show tolerance and a willingness to share food patches. We tested two alternative hypotheses about who those group-mates might be: the "social bonds hypothesis" predicts that preferred foraging partners will be those with whom individuals share strong social bonds, indexed by grooming, whereas the "kinship hypothesis" predicts that preferred foraging partners will be relatives. We also investigated and controlled for the effects of dominance rank, given that competitive ability is known to shape foraging patterns. Social network analyses of over 5,000 foraging events for 14 adults in a single troop revealed that baboon co-feeding was significantly correlated with grooming relationships but not genetic relatedness, and this finding was also true of the female-only co-feeding network. Dominant individuals were also found to be central to the co-feeding network, frequently sharing food patches with multiple group-mates. This polyadic analysis of foraging associations between individuals underlines the importance of dominance and affiliation to patterns of primate social foraging.     

Stability and Durability of Intra- and Intersex Social Bonds of Captive Rhesus Macaques (Macaca mulatta)

Many social species maintain differentiated relationships with their group members. These social bonds may reflect short-term interactions satisfying immediate needs. Alternatively, individuals of some species may entertain stable and valuable bonds that last much longer than opportunistic interactions would predict. This claim is supported by recent research that revealed clear fitness benefits for long-lasting social bonds. Here, we investigated the stability and equitability of social relationships in captive rhesus macaques, measured using their proximity and grooming patterns over a 3-yr period. We show that, in general, proximity patterns of the whole group were stable over 3 yr. More specifically, each individual’s top two nonkin within and between sex relationships based on proximity were relatively stable and some of these relationships lasted the full 3 yr. Female grooming relationships within and between sex were also stable over 3 yr. Moreover, strong social bonds in females were not based on age similarity and were not sex specific, suggesting that a general underlying mechanism of social bonding in female rhesus macaques. In contrast, patterns of male grooming of other males and of females were relatively unstable and male social bonds were less equitable than those of females. The differences in stability of the relationships between the sexes may reflect the dispersal pattern of rhesus macaques, although we have limited data on non-natal males in our study. With these data we add to a growing body of literature describing the value and durability of relationships among primates and other species.     

Sex differences in vocal communication among adult rhesus macaques

In female-bonded primate species, females invest more time in grooming than males, and the majority of this grooming occurs in intra- rather than intersexual interactions. These clear sex differences in sociability reflect females' need to forge and maintain complex networks of social relationships with other females in the group. Increasing evidence indicates that vocal signals can have a similar function to grooming in mediating social interactions and relationships, and sex differences in patterns of use of vocal communication comparable to those seen for grooming might therefore be expected to occur. In this study of free-ranging adult rhesus macaques, we tested for such patterns, focusing on the frequency of utterance of three types of vocalisations given during close-range social interactions: coos, grunts, and girneys. As predicted, we found that females gave such calls significantly more frequently than males and also directed more of these vocalisations towards other females than to males; males' rate of vocalising towards the two sexes was not significantly different. To our knowledge, these results provide the first evidence for a sex difference in the rate of production of social vocalisations among adult nonhuman primates. The finding that increased sociability is associated with increased reliance on vocal communication may have important implications for theories of language evolution.     

Sex differences in nonhuman primate grooming

In this article, sex differences in nonhuman primate social grooming are reviewed. In general, female nonhuman primates groom more than do males. This conclusion is tempered somewhat by acknowledgements of exceptions and qualifications, and by evidence for experiential control of grooming.     

Aggression, grooming and group-level cooperation in white-faced capuchins (Cebus capucinus): insights from social networks

The form of animal social systems depends on the nature of agonistic and affiliative interactions. Social network theory provides tools for characterizing social structure that go beyond simple dyadic interactions and consider the group as a whole. We show three groups of capuchin monkeys from Barro Colorado Island, Panama, where there are strong connections between key aspects of aggression, grooming, and proximity networks, and, at least among females, those who incur risk to defend their group have particular "social personalities." Although there is no significant correlation for any of the network measures between giving and receiving aggression, suggesting that dominance relationships do not follow a simple hierarchy, strong correlations emerge for many measures between the aggression and grooming networks. At the local, but not global, scale, receiving aggression and giving grooming are strongly linked in all groups. Proximity shows no correlation with aggression at either the local or the global scale, suggesting that individuals neither seek out nor avoid aggressors. Yet, grooming has a global but not local connection to proximity. Extensive groomers who tend to direct their efforts at other extensive groomers also spend time in close proximity to many other individuals. These results indicate the important role that prosociality plays in shaping female social relationships. We also show that females who receive the least aggression, and thus pay low costs for group living, are most likely to participate in group defense. No consistent "social personality" traits characterize the males who invest in group defense.     

Response of Rhesus Macaques (Macaca mulatta) to the Body of a Group Member That Died from a Fatal Attack

Among animals that form social bonds, the death of a conspecific may be a significant social event, representing the loss of an ally and resulting in disruptions to the dominance hierarchy. Despite this potential biological importance, we have only limited knowledge of animals’ reactions to the death of a group member. This is particularly true of responses to dead adults, as most reports describe the responses of mothers to dead infants. Here, we describe in detail and provide video evidence of the behavioral responses of a group of free-ranging rhesus macaques (Macaca mulatta) immediately after the death of a mid-ranking adult male as a result of a fatal attack. High-ranking male members of the group, suspected to have carried out the attack, dragged and bit the dead body, exhibiting a rate of aggression 20 times greater than baseline levels. Lower-ranking individuals approached and inspected the body by looking closely, smelling, and grooming the fur. There was inconclusive evidence that these rhesus macaques found the death of a conspecific stressful: Levels of grooming between group members after the fatal attack were significantly higher than baseline levels, and higher than levels of grooming after nonfatal attacks. However, when grooming levels were adjusted based on the assumption that individuals positioned close to the body, i.e., those visible to researchers, were more likely to be engaged in grooming than those positioned farther away, this difference from baseline was no longer significant. The rate of self-directed behaviors after the fatal attack was also not different from baseline. Many of the behaviors we observed directed toward the body (aggression, inspection) have been previously reported in chimpanzees and geladas, and are similar to reactions sometimes displayed by humans. As such, this report represents a potentially valuable contribution the nascent field of nonhuman primate thanatology.     

Network cohesion,group size and neocortex size in female-bonded Old World primates

Most primates are intensely social and spend a large amount of time servicing social relationships. In this study, we use social network analysis to examine the relationship between primate group size, total brain size, neocortex ratio and several social network metrics concerned with network cohesion. Using female grooming networks from a number of Old World monkey species, we found that neocortex size was a better predictor of network characteristics than endocranial volumes. We further found that when we controlled for group size, neocortex ratio was negatively correlated with network density, connectivity, relative clan size and proportional clan membership, while there was no effect of neocortex ratio on change in connectivity following the removal of the most central female in the network. Thus, in species with larger neocortex ratios, females generally live in more fragmented networks, belong to smaller grooming clans and are members of relatively fewer clans despite living in a closely bonded group. However, even though groups are more fragmented to begin with among species with larger neocortices, the removal of the most central individual does cause groups to fall apart, suggesting that social complexity may ultimately involve the management of highly fragmented social groups while at the same time maintaining overall social cohesion. These results emphasize a need for more detailed brain data on a wider sample of primate species.     

Sex Ratio, Conflict Dynamics, and Wounding in Rhesus Macaques (Macaca mulatta)

Rhesus macaques, like many other primates, live in stable, multi-male multi-female groups in which adult females typically outnumber adult males. The number of males in multi-male/multi-female groups is most commonly discussed in terms of mate competition, where the sex ratio is a function of an adult male's ability to monopolize a group of females. However, the relationship between sex ratio and group stability is unclear because the presence of many males may either reduce stability by increasing mate competition or may improve stability if adult males are key conflict managers. We investigated the relationship between sex ratio, male intervention behavior, and trauma in seven groups of captive rhesus macaques. Our results show that high-ranking adult males intervene twice as frequently as adult females (P<0.0001) and are about twice as successful (P<0.0001). Furthermore, the type of adult males present in the group affects the relationship between intervention behavior and rate of traumas: males must be unrelated to the highest-ranking matrilines. Groups with a lower ratio of females per male unrelated to the alpha and beta matrilines had better intervention success (P<0.04) and fewer traumas requiring veterinary care (P=0.003). We conclude that conflict management behavior by adult males, particularly those unrelated to the highest-ranking matrilines, is the mechanism by which sex ratio influences the frequency of traumas, and thus group stability. We therefore suggest that monitoring and managing the sex ratio of captive primate groups is one of many measurements to predict group stability.     

Social structure, robustness, and policing cost in a cognitively sophisticated species

Conflict management is one of the primary requirements for social complexity. Of the many forms of conflict management, one of the rarest and most interesting is third-party policing, or intervening impartially to control conflict. Third-party policing should be hard to evolve because policers personally pay a cost for intervening, while the benefits are diffused over the whole group. In this study we investigate the incidence and costs of policing in a primate society. We report quantitative evidence of non-kin policing in the nonhuman primate, the pigtailed macaque. We find that policing is effective at reducing the intensity of or terminating conflict when performed by the most powerful individuals. We define a measure, social power consensus, that predicts effective low-cost interventions by powerful individuals and ineffective, relatively costly interventions by low-power individuals. Finally, we develop a simple probabilistic model to explore whether the degree to which policing can effectively reduce the societal cost of conflict is dependent on variance in the distribution of power. Our data and simple model suggest that third-party policing effectiveness and cost are dependent on power structure and might emerge only in societies with high variance in power.     

Behavioral responses of free-ranging rhesus monkeys to food shortage

During early July 1968, a severe food shortage occurred on Cayo Santiago, an island colony of free-ranging rhesus monkeys (Macaca mulatta). The food shortage produced striking changes in the behavior of the monkeys. Within the one social group intensively studied, the total frequencies of grooming, play and fights decreased significantly; the frequency of matings also dropped; body contact, displacements by other groups, and non-displacement movements decreased, but not in statistically significant amounts. Changes in the percentage of total grooming attributable to related and unrelated monkeys reflected the stability of the rhesus matriline. Comparisons made between Cayo Santiago and other primate groups under analogous situations reveal similar responses to food shortage.     

Behavioural processes in social context: female abductions, male herding and female grooming in hamadryas baboons

The formation of bonds between strangers is an event that occurs routinely in many social animals, including humans, and, as social bonds in general, they affect the individuals' welfare and biological fitness. The present study was motivated by an interest in the behavioural processes that drive bond formation in a social context of hostility, in which the incumbent partners vary greatly in physical power and reproductive interests, a situation in which individuals of many group-living species find themselves often throughout their lives. We focused on the quantitative analysis of female abductions via male aggressive herding in a nonhuman primate, the hamadryas baboon, in which intersexual bonds are known to be strong. We tested three hypotheses informed by sexual conflict/sexual coercion theory (male herding-as-conditioning and female grooming-as-appeasement) and by socioecological theory (unit size and female competition). The results supported the predictions: males resorted to coercive tactics (aggressive herding) with abducted females, and abducted females elevated the amount of grooming directed at their new unit males; in fact, they escaped from the otherwise negative effect of unit size on female-to-male grooming. These findings reveal that conflicts of interest are natural ingredients underpinning social bonds and that resorting to coercive aggression may be an option especially when partners differ greatly in their physical power.     

Inbreeding,kin selection,and primate social evolution

In this paper I argue (a) that the study of kin selection may be facilitated by looking for influences of inbreeding, which is an important aspect of a population's genetic structure; (b) that in nonhuman primates the level of inbreeding will be largely a function of the rate of migration by individuals, usually only of one sex, between social units or troops; (c) that many primate species live in relatively outbred groups, and that their social structure reflects this; and (d) that extensive social contrasts between bonnet and pigtail macaques reflect evolution by kin selection under different levels of inbreeding.     

三种笼养灵长类活动时间分配的比较研究

采用焦点动物法和连续记录法对3种笼养灵长类活动时间分配进行比较研究。结果表明,川金丝猴Rhi-nopithecus roxellanae和熊猴Macaca assamensis用于休息的时间多于猕猴Macaca mulatta,移动时间则相反;川金丝猴和猕猴用于理毛的时间多于熊猴。不同性别年龄组之间的活动时间分配有差异,主要表现在川金丝猴母亲用于理毛的时间明显多于成年儿子,用于玩耍的时间则相反;猕猴成年雄性的移动时间和理毛时间多于成年雌性,玩耍时间则少于成年雌性;熊猴成年雌性的移动时间多于成年雄性,与成年个体相比,幼体花更多的时间用于玩耍,而相应的减少了其休息时间。     

Grooming, social bonding, and agonistic aiding in rhesus monkeys

An analysis of simultaneous grooming bouts in a captive group of rhesus monkeys (Macaca mulatta) failed to provide evidence of competition to groom high ranking partners. Not only were grooming supplantations rare, but the highest ranking individuals performing grooming did not groom the highest ranking animals receiving grooming. Lower ranking partners, however, did more grooming in nonkin dyads. Grooming partners aided one another in agonistic episodes, but the individual receiving the aid did not groom the individual providing the aid more than vice versa. Kin dyads did aid and groom one another at greater than expected rates, but the aider did not receive the greater proportion of grooming in the dyad. Males participated in more grooming than expected, but their grooming was not related to aiding either with regard to one another or female partners. Animals that were targeted in joint aggression, or aided against, received significantly less grooming from their opponents. A general social relationship expressed in partner preferences, social grooming, and agonistic aiding better explained the observed pattern than any model based on the exchange of services for favors in different currencies.     

Hormonal Correlates of Maternal Style in Captive Macaques (Macaca fuscata and M. mulatta)

Previous studies on nonhuman primate maternal styles showed that variation in infant-directed behavior falls along two dimensions, traditionally labeled as protectiveness and rejection. We investigated maternal styles in rhesus (Macaca mulatta) and Japanese (M. fuscata) macaques living in analogous captive social groups, and correlated them with the levels of estrogen metabolites excreted in female feces during the perinatal period. We focally observed mother-infant pairs 3 hours per week during the first 12 weeks of infant life. We collected fecal samples twice a week from each mother, starting 4 weeks before delivery and ending 4 weeks after delivery. Three significant components were extracted by principal component analysis from 15 different infant directed behaviors, each reflecting a different aspect of mothering style: rejection is correlated with behavioral measures of maternal opposition to contact; protectiveness is correlated with maternal solicitude; and independence is correlated with time in contact, grooming and cradling. Levels of estrogen metabolites are significantly correlated to rejection but not to protectiveness or independence, indicating that, in nonhuman primates, individual endocrine changes related to maternal behavior might specifically affect the timing of contact interruption.     

Grooming reciprocity in female tibetan macaques macaca thibetana

Grooming among nonhuman primates is widespread and may represent an important service commodity that is exchanged within a biological marketplace. In this study, using focal animal sampling methods, we recorded grooming relationships among 12 adult females in a free-ranging group of Tibetan macaques (Macaca thibetana) at Huangshan, China, to determine the influence of rank and kinship on grooming relationships, and whether females act as reciprocal traders (exchange grooming received for grooming given) or interchange traders (interchange grooming for social tolerance or other commodities). The results showed that: (1) grooming given was positively correlated with grooming received; (2) kinship did not exert a significant influence on grooming reciprocity; and (3) grooming reciprocity occurred principally between individuals of adjacent rank; however, when females of different rank groomed, females tended to groom up the hierarchy (lower ranking individuals groomed higher ranking individuals more than vice versa). Our results support the contention that both grooming reciprocity and the interchange of grooming for tolerance represent important social tactics used by female Tibetan macaques.     

Group size, grooming and fission in primates: a modeling approach based on group structure

In social animals, fission is a common mode of group proliferation and dispersion and may be affected by genetic or other social factors. Sociality implies preserving relationships between group members. An increase in group size and/or in competition for food within the group can result in decrease certain social interactions between members, and the group may split irreversibly as a consequence. One individual may try to maintain bonds with a maximum of group members in order to keep group cohesion, i.e. proximity and stable relationships. However, this strategy needs time and time is often limited. In addition, previous studies have shown that whatever the group size, an individual interacts only with certain grooming partners. There, we develop a computational model to assess how dynamics of group cohesion are related to group size and to the structure of grooming relationships. Groups’ sizes after simulated fission are compared to observed sizes of 40 groups of primates. Results showed that the relationship between grooming time and group size is dependent on how each individual attributes grooming time to its social partners, i.e. grooming a few number of preferred partners or grooming equally or not all partners. The number of partners seemed to be more important for the group cohesion than the grooming time itself. This structural constraint has important consequences on group sociality, as it gives the possibility of competition for grooming partners, attraction for high-ranking individuals as found in primates’ groups. It could, however, also have implications when considering the cognitive capacities of primates.