Juveniles Outrank Higher-Born Females in Groups of Long-Tailed Macaques with Minimal Kinship

In a typical matrilineal or nepotistic hierarchy a mother's rank sets both her daughter's lowest rank (above lower-born females), and her daughter's highest rank (below the mother and higher-born females). Long-tailed macaques (Macaca fascicularis) form typical matrilineal dominance orders. We report a variant of this system that we observed in 4 groups of captive long-tailed macaques characterized by an unusual kinship structure. Each group was composed of the smallest possible matrilineages (mother-offspring pairs), the mothers being unrelated to each other. In each group, juveniles ranked above all the females subordinate to their mother, as this is the case in a typical matrilineal hierarchy, but a majority of juveniles of both sexes outranked their own mothers and/or several higher-born females and their offspring. Adult females resisted the juveniles and were 2.5 times heavier than the latter. The patterning of interventions in conflicts suggests that this unusual ranking pattern resulted from the existence of bridging alliances between the juveniles and individuals ranking above the juveniles' targets. The results indicate that the sole presence of the mother is sufficient for a daughter to outrank the females subordinate to her mother, but it is not sufficient to prevent the daughter from ascending the rank order. Our data suggest that in the absence of extensive alliances among kin, which normally stabilize the rank order, juveniles were able to benefit from infrequent, opportunistic interventions by high-ranking nonkin individuals.     

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.     

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.     

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.     

Rank relations among sisters in semi-free-ranging Barbary macaques (Macaca sylvanus)

Although semi-free-ranging Barbary macaque females are able to outrank older females from lower-ranking matrilines (matrilineal rank acquisition), they do not systematically outrank their older sisters, as is known to be the case for semi-free-ranging rhesus monkeys (Macaca mulatta) and Japanese macaques (Macaca fuscata). We test the hypothesis that differences in the support received by younger sisters against their older sisters and against older lower-ranking females might account for this interspecific difference. Thirty-one sister dyads, members of a group of 109 Barbary macaques living at La Montagne des Singes, France, were observed during 16 months. The results indicate that (1) all females were dominant to their younger sisters, and the latter were never observed to challenge their older sisters; (2) younger sisters received as much kin support against their older sisters as against older lower-ranking females; (3) only very young females received support from their kin against their older sisters; (4) younger sisters received much more support from nonkin females against lower-ranking females than against their older sisters; and (5) Barbary macaque females appear to be supported against their older sisters less frequently than rhesus macaque females are. We conclude that the lack of nonkin support is the main factor accounting for the failure of younger sisters to outrank their older sisters in Barbary macaques. Initially this might result from kin support not being sufficient to induce younger sisters to challenge and to solicit support against their older sisters.     

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.     

Kin and Child Survival in Rural Malawi

This paper investigates the impact of kin on child survival in a matrilineal society in Malawi. Women usually live in close proximity to their matrilineal kin in this agricultural community, allowing opportunities for helping behavior between matrilineal relatives. However, there is little evidence that matrilineal kin are beneficial to children. On the contrary, child mortality rates appear to be higher in the presence of maternal grandmothers and maternal aunts. These effects are modified by the sex of child and resource ownership: female children and children in households where women, rather than men, own land suffer higher mortality rates in the presence of maternal kin. These modifiers suggest the detrimental effects of matrilineal kin may result from competition between such kin for resources. There are some positive effects of kin on child survival: the presence of elder siblings of both sexes is correlated with higher survival rates, and there is some weak evidence that paternal grandmothers may be beneficial to a child’s survival chances. There is little evidence that any male kin, whether matrilineal or patrilineal, and including fathers, affect child mortality rates. This study highlights the importance of taking social and ecological context into account when investigating relationships between kin.     

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.     

Patterns of affiliation among immature rhesus monkeys (Macaca mulatta)

The affiliative interaction patterns of the immature members of a group of rhesus monkeys at the Yerkes Regional Primate Research Center reflected a strong bias toward matrilineal kin, although this effect was modified by age and sex variables. Association with kin decreased with age, particularly for males. Juvenile males showed less of a kin bias in their behavior than did juvenile females, especially for grooming. Juvenile males also exhibited a preference for interaction with other males. The diminished association with kin and the same-sex bias may be reinforced in adolescence as adult males begin to aggressively target adolescent males involved in agonistic encounters with females or immatures. Adolescent males did not decrease their levels of social interaction relative to those of adolescent females; however, these males preferentially associated with other males (predominantly their own age-sex class) and specifically avoided females and younger animals, both kin and nonkin. Avoidance may diminish conflicts with females or immatures which could result from association, thereby decreasing the potential for selective aggressive interference by adult males. Juvenile and adolescent females maintained strong ties with their kin and preferentially associated with other females and immatures. The breadth of interaction of females with other females may facilitate the establishment of dominance relationships as females mature. Familiarity and predictability may also decrease the necessity of more severe agonistic interaction.     

Age-dependent patterns of intensive observation on elders by free-ranging juvenile Japanese macaques (Macaca fuscata yakui) within foraging context on Yakushima

Early learning about edible food in the environment is a critical survival task for young nonhuman primates. Social learning and social facilitation are often cited to explain how youngsters learn to select and find their food. In this framework, we observed eight mother-youngster pairs of free-ranging Japanese macaques divided into two sets according to the age of the young (infants aged between 7 and 12 months and juveniles aged between 1.5 and 2 years) during three winter months. We systematically investigated the intensive observation directed by the youngsters toward elders by recording the target's identity (e.g. mother, subadult), the items manipulated by the elder and those items closely observed by the youngster, along with the behavior of the youngster preceding and immediately following an intensive observation period. The diet of the mothers and juveniles was estimated from time records of each feeding occurrence for each food item (identified to species level) and from the quantity of fresh matter ingested. The results show that intensive observation by both infants and juveniles were directed toward those elders engaged in plant and invertebrate foraging. Such behavior was age-dependent, being more frequent in infants than in juveniles. The majority of the intensive observations were directed toward the mother. Intensive observations also shaped a change in the behavior of infants by significantly stimulating the investigation of food items and locations otherwise not investigated by juveniles. Moreover, infants showed a particular interest in rare food items and especially invertebrates. Age differences between the two sets of young and their interest in rare foods are discussed with reference to the occurrence of intensive observation within the framework of kin relationships, social organization, and social transmission of information about food type and food location and its survival values.     

The evolution of matrilineal kinship organization

Matrilineal kinship organization is a human social system that emphasizes interactions between matrilineal kin, i.e. individuals related only through females. The ‘matrilineal puzzle’ refers to the potential for tension characteristic of this social system, owing to the conflict between the interests and responsibilities of men in their roles as brother/uncle versus husband/father. From an evolutionary perspective, matrilineal kinship organization is puzzling when it diverts investment of resources from the individuals who provide the potentially highest reproductive returns. I use a game-theoretic framework to investigate a particular form of matrilineal inheritance—the transfer of property from a maternal uncle to a sororal nephew. The analysis reveals two mechanisms that may make this strategy a stable evolutionary outcome. First, a polygynous male has multiple wives, and hence multiple brothers-in-law; with matrilineal inheritance, each additional brother-in-law may transfer resources to the male''s wife''s offspring, thus potentially contributing to the male''s inclusive fitness. Second, the husband of a polyandrous female is effectively ‘sharing’ paternity with other men; depending on the number of husbands, he may be better off investing in his sister''s offspring. I conclude by discussing how these results address the challenges posed by the occurrence of matrilineal kinship organization.     

Avoidance of close consanguineous inbreeding in captive groups of rhesus macaques

In three captive groups of rhesus macaques (Macaca mulatto) the intensity of inbreeding avoidance was directly correlated with the closeness of kinship. The incidence of inbreeding between matrilineal relatives was lower than expected were mating to occur randomly with regard to matrilineal affiliation. The avoidance of mating between sons and their mothers and between matrilineal sibs contributed about squally to this outcome. The incidence of mating between more remote matrilineal relatives was lower than, but could not be shown to differ significantly from, that expected at the 0.05 level of probability. Familiarity fostered by interactions among matriline members probably provides a focus for avoidance of matrilineal inbreeding, and might influence male dispersal. Results of this study are consistent with reports of female rhesus macaques' avoidance of sexual activity with matrilineal male relatives as predicted by parental investment theory The observed incidence of inbreeding between patrilineal relatives was not different from that expected, but significantly fewer of the patrilineally inbred matings involved father/daughter matings than expected were mating random. Recognition of phenotypic similarities might provide a focus for avoidance of inbreeding between fathers and their daughters, but is loss reliable than strategies for avoiding matrilineal inbreeding. Adaptations for avoiding matrilineal inbreeding that are more effective than those for avoiding patrilineal inbreeding might have evolved because the risk of patrilineal inbreeding, and hence the resulting loss in fitness, is marginal compared to that for matrilineal inbreeding in free-ranging groups. © 1995 Wiley-Liss, Inc.     

雌性黄山短尾猴回避近亲交配

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

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.     

Social behavior of infant and mother Japanese Macaques (Macaca fuscata): Effects of kinship,partner sex,and infant sex

The behavioral interactions of 22 infant and mother Japanese macaques with other group members were studied. Focal-animal observations were made from the time of each infant’s birth until 1 year of age. Infants and mothers both displayed exceedingly strong preferences for associating with matrilineal kin and, specifically, for female kin. The degree of genetic relatedness was positively correlated with levels of spatial proximity, contact, grooming, aggression, and play. Overall frequencies of interactions with nonkin were very low, and partner sex was not an important factor in interactions with nonkin. There were no significant differences between male and female infants in interactions with kin versus nonkin. There was only one significant difference between male and female infants in interactions with males versus females: female infants showed stronger preferences for initiating proximity with females over males than did male infants. Because mothers provide the focal point for infant interactions during the first year of life, we compared the behavior of infants and mothers. Mothers were the recipients of more social interactions than were infants, mothers engaged in more grooming than did infants, and infants engaged in more social play than did mothers. These findings are only partially consistent with kin-selection theory, and the inadequacies of studying matrilineal kin discrimination to test kin selection are reviewed. The near-absence of infant sex differences in associations with social partners suggests that although maternal kin other than the mother are important to infant socialization, they probably do not contribute to the development of behavioral sex differences until after the first year of life.     

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.     

Influence of kinship and spatial density on reconciliation and grooming in rhesus monkeys

Some cercopithecine primates direct disproportionate amounts of grooming, huddling, and agonistic support toward maternal kin. Disproportionate amounts of aggression are also directed toward maternal kin, however, suggesting that mechanisms that restore relationships damaged by aggression, such as reconciliation, might be biased toward these preferred social partners. Studies investigating kinship effects and reconciliation are inconsistent, however, perhaps because of differences in the environmental conditions under which behavior was observed. In order to test the effects of kinship and spatial density on affiliative and reconciliation behavior, we conducted focal and scan sampling on a group of rhesus monkeys (Macaca mulatta) living in an outdoor corral under low spatial density conditions. We then compared this data to previously published data on a group of the same species living under higher spatial density conditions. Neither overall grooming nor reconciliation were affected by spatial density once correction procedures were applied. Grooming was kin biased at both study sites, whereas reconciliation was kin biased only in the low-density group. Although data failed to support a Coping Model according to which grooming and reconciliation should go up under higher densities, we suggest that coping may be reflected not so much in overall rates of behavior but in strategic partner choices, such as the increased importance monkeys under crowded conditions appear to attach to nonkin partners. © 1996 Wiley-Liss, Inc.     

Aggressive interventions and matrilineal dominance relations in semifree-ranging barbary macaques (Macaca sylvanus)

Female Barbary macaques (Macaca sylvanus) form matrilineal hierarchies, i.e. they come to rank below their mother in relation to non-kin females in the course of maturation. The stability of such hierarchies and the acquisition of the matrilineal rank are achieved through dyadic aggressions and third party interventions in conflicts. This study examines the dynamics of interventions in non-kin conflicts in a semifree-ranging group of 109 Barbary macaques at “La Montagne des Singes,” Kintzheim, France. Focal sampling on 13 females aged 3 and 4 years not yet dominant over all older females from lower ranking kin groups (lower born females) was carried out during 16 months in 1987 and 1988. Results on the direction of support in non-kin female conflicts (all samples pooled) show that interventions were generally provided on behalf of the female from the higher ranking kin group (higher born female). Rates of interventions (derived from focal samples) given and received were correlated with the hierarchy; higher born females received more support and intervened more often than lower born females. A subset of interventions (based on the age of the females involved) was analyzed according to the rank distance between the opponents and the type of support provided (spontaneous or solicited). On the basis of their representation, intermediate-ranking supporters (i.e. females ranking between the opponents) intervened more often than above-ranking supporters (i.e. females dominant to both opponents), and they intervened more often spontaneously than following a solicitation. The results on interventions are discussed in the perspective of benefits to supporters. Twenty-one instances of outranking of older females (matrilineal rank acquisition) were observed. By the end of the study, the number of older lower born females not yet outranked by the focal females was negatively correlated to the rank distance between the two sets of females. However no such correlation was found between these two groups when compared according to their age difference in years.     

Patterns of fight interference in free-ranging rhesus monkeys

Rhesus monkeys occasionally break up fights among conspecifics and this phenomenon may be called “interference.” The present study describes the patterns of interference in a group of free-ranging rhesus monkeys and evaluates the effect of this behavior onMacaca mulatta social organization. Data were collected at Cayo Santiago. Strong sexual differences were found in the patterning of interference behavior. Females tended to help victims of aggression and animals from the interferer's own genealogy, especially juveniles. In addition, females were likely to interfere as subordinate to the target animal. Natal and non-natal males oriented toward unrelated adult females and generally only interfered in fights if dominant to the target animal. Further, the males helped victims of aggression significantly less often than females did. Contrary to expectation, the dominant males were noteworthy neither for the quantity nor the effect of their interference. In general, the findings reinforce the notion that females are the stable and central part of a rhesus monkey social group. The findings also suggest that interference plays a role in the maintenance of group stability and cohesion.     

Longitudinal study of dominance relations among captive patas monkeys

Eight and a half years of dominance relations within a captive group of patas monkeys were analyzed. It was found that matrilineal kinship significantly influenced individuals' ranks. In contrast, with the exception of certain intramatriline changes, increasing age had no predictable effect on overall rank, at least for females (this was untestable for males). Offspring typically challenged maternal dominance and in eight of twelve dyads, offspring either rose fully over their mothers (three cases, all daughters) or at least achieved dominance ambiguity with them. Additionally, two of the four younger sisters with an opportunity to rise in rank over an older sister did so. The group dominance hierarchy was unstable for 75% of the study due to a combination of agonistically induced and demographically induced rank changes. Concentration of the highest ranks in a single matriline showed a stronger association with group hierarchy stability than did the presence of an adult, nonnatal male. Group hierarchy stability was associated with increased affiliation (sitting close and sitting touching), but otherwise there were no behavioral correlations. Individuals' ranks within the group hierarchy were unrelated to their chances of being wounded or having diarrhea. Adult females' ranks were over twice as stable as the group hierarchy (57.1% stability), but stability/instability was not correlated with any behavioral changes. Available evidence suggests that dominance relations play only a minor role in the organization of patas monkeys' intragroup behavior. Am. J. Primatol. 42:41–51, 1997. © 1997 Wiley-Liss, Inc.