Social Interactions through the Eyes of Macaques and Humans

Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable resources. Observing such social interactions between group members provides individuals with essential information (e.g. on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners. This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore, the monkeys’ gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions. Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying a homologous cognitive mechanism of social attention between rhesus macaques and humans.     

Mounting Interactions between Female Japanese Macaques: Testing the Influence of Dominance and Aggression

The goal of the work reported here was to determine whether female Japanese macaques (Macaca fuscata) participated in same-sex mounting interactions during homosexual consortships to communicate about asymmetries in their dominance relationships and to reduce aggression. Focal data were collected during 21 homosexual consortships involving 14 females living in a captive, mixed-sex group of 37 individuals. We identified eight types of mounts, one solicitation used specifically to request to mount (hands-on-hindquarters solicitation), two solicitations used specifically to request to be mounted (hindquarter and back presentations), and one behavior employed to facilitate mounts-in-progress (clasping). We tested whether dominant consort partners (1) mounted more and (2) requested to mount more than their subordinate partners and whether subordinate consort partners (1) requested to be mounted more and (2) facilitated mounts-in-progress more than their dominant partners. Finally, we examined whether mounting was temporally linked to the onset of aggressive interactions between consort partners and whether it functioned to defuse incipient aggression. None of these predictions was supported. All types of mounts, mount solicitations, and clasping occurred bi-directionally within consort dyads. Mutual sexual attraction and gratification provided the proximate motivation for these mounting interactions and, in turn, for the formation and maintenance of their homosexual consortships.     

Adjustment of Temporal Call Usage During Vocal Exchange of Coo Calls in Japanese Macaques

Japanese macaques (Macaca fuscata) exchange coo calls with group members to maintain contact. I examined the relationship between the distance between group members and (1) the latency of vocal responses to spontaneous calls, and (2) the latency of spontaneous call repetition in the absence of vocal responses. After a subject monkey's spontaneous call, the latency of vocal response by another group member was longer when the subject was farther from the group members than when the subject was near the group members. Furthermore, subject repeated calls with longer intervals in the absence of vocal response, which suggests that they wait longer for the vocal responses of other group members when the expected response latency is longer. These results reveal that Japanese macaques flexibly alter the timing of their calls based on others’ vocal responses.     

Fecundity of Paternal and Maternal Non-Parental Female Relatives of Homosexual and Heterosexual Men

A variety of social, developmental, biological and genetic factors influence sexual orientation in males. Thus, several hypotheses have attempted to explain the sustenance of genetic factors that influence male homosexuality, despite decreased fecundity within the homosexuals. Kin selection, the existence of maternal effects and two forms of balancing selection, sexually antagonistic selection and overdominance, have been proposed as compensatory mechanisms for reduced homosexual fecundity. Here, we suggest that the empirical support for kin selection and maternal effects cannot account for the low universal frequency and stability of the distribution of homosexuals. To identify the responsible compensatory mechanism, we analyzed fecundity in 2,100 European female relatives, i.e., aunts and grandmothers, of either homosexual or heterosexual probands who were matched in terms of age, culture and sampling strategy. Female relatives were chosen to avoid the sampling bias of the fraternal birth order effect, which occurs when indirectly sampling mothers though their homosexual sons. We observed that the maternal aunts and grandmothers of homosexual probands were significantly more fecund compared with the maternal aunts and maternal grandmothers of the heterosexual probands. No difference in fecundity was observed in the paternal female lines (grandmothers or aunts) from either of the two proband groups. Moreover, due to the selective increase in maternal female fecundity, the total female fecundity was significantly higher in homosexual than heterosexual probands, thus compensating for the reduced fecundity of homosexuals. Altogether, these data support an X-linked multi-locus sexually antagonistic hypothesis rather than an autosomal multi-locus overdominance hypothesis.     

Male Masturbation in Free-Ranging Japanese Macaques

We studied masturbatory behavior of males over a 14-mo period in free-ranging Japanese macaques (Macaca fuscata yakui) on Yakushima island, Japan. We distinguished 2 types: (1) masturbation only and (2) masturbation with final ejaculation. Both types occurred in all 15 adult troop males. We calculated masturbation only as an index (M/h). It occurred over the whole year; however, it was more frequent during the mating than during the non-mating periods. Masturbation with ejaculation was restricted to the mating period. Male mating success correlated positively with social status. Both rate of masturbation only and masturbatory ejaculations increased as male social status and male mating success declined. Lower-ranking males had higher rates of masturbation only, i.e., they spent more time masturbating than higher-ranking males did. Lower-ranking males also had higher proportions of ejaculates for masturbation, while higher-ranking males used most of their ejaculates for mating.     

Infant Handling and Maternal Response in Japanese Macaques

We focused on the social interactions of infant Japanese macaques (Macaca fuscata) and on the protective response of their mothers to such interactions. Infant social interactions included: received allomaternal behavior (positive infant handling), hand touch and inspection (neutral handling), and aggression (negative handling) as well as social play. Maternal protective responses included aggression to the infant's interactant and restraining or retrieving the infant. All types of social interactions as well as the maternal response to such interactions showed clear developmental variations. Frequency of infant social interactions and maternal protective responses also showed large interindividual variability. Juvenile and subadult females without maternal experience were the most frequent infant handlers. Infants received positive handling primarily from their kin, while mothers were equally protective in response to positive handling received by kin and by non-kin. Conversely, kin showed higher levels of neutral handling and their interest was more easily tolerated by mothers compared to that of non-kin.     

Dominance Turnover Between an Alpha and a Beta Male and Dynamics of Social Relationships in Japanese Macaques

We report a case of turnover between an alpha (GN) and a beta male (R7) and its effects in a troop of provisioned Japanese macaques (Macaca fuscata fuscata) in Shiga-Heights, Nagano Prefecture, Japan. The aggression between the 2 males was caused by the intrusion of GN towards the consort of R7. R7 received support from his brother and mother, and consequently defeated GN. After the turnover, R7 attacked GN frequently, which may have functioned to stabilize the dominance relationship between them. Also, R7 selectively attacked females friendly to GN soon after the turnover. Although we never observed polyadic aggression among males during the stable dominance period, 20 cases of polyadic aggression occurred among the 6 highest-ranked males in the 2 days following the turnover, and one case occurred on the fourth day. R7 and GN formed stable conservative alliances for attacking subordinate males. Males that did not participate in the turnover began to form revolutionary coalitions to attack higher-ranking males, but they were thwarted by the conservative coalitions between the dominants. Mutualism was a plausible explanation for the patterns of coalition formation because most of them were conservative with little associated cost. Seven females had a high proximity index (C-score) to GN before the turnover, but a significantly lower proximity index after the turnover. On the day of the turnover, 6 non-lactating females suddenly became receptive, suggesting that the turnover induced immediate receptivity in the females.     

Male-male Interactions in Heterosexual and All-male Wild Mountain Gorilla Groups

Variation in male dispersal and behavior patterns are components of intraspecific differences in social systems. A comparison of male behavior in different social settings can be useful for determining which behavioral mechanisms contribute to variability in social systems. Two heterosexual multimale groups and one all-male group of mountain gorillas (Gorilla gorilla beringei) were observed for over 1100 h at the Karisoke Research Centre, Rwanda. Data on proximity patterns, dominance relationships, aggression, agonistic interventions, affiliation, and homosexual behavior were compared among the males in these groups to examine the influence of female presence, sex ratio, group size, and kinship on male—male interactions. Males in the all-male group stayed closer together, affiliated more, exhibited more homosexual behavior, and were more aggressive toward each other than males in heterosexual groups. However, the males in heterosexual groups showed more wounding and more consistent dominance relationships. Kinship did not influence male-male relationships in the all-male group. The males in the heterosexual groups rarely interacted with one another; they may actively avoid close proximity to reduce aggression. Results suggest that the variable social system of mountain gorillas may be more strongly influenced by demographic factors, male-female social relationships, and male-male competition for mates than by any benefits of male-male relationships.     

Effects of Environmental and Social Conditions on Homosexual Pairing in the Japanese Beetle (Popillia japonica Newman)

Homosexual pairing between males occurs under natural conditions in a wide variety of taxa, including many insect species, but few studies have investigated how environmental and social conditions affect same-sex pairing in insects. We investigated factors affecting homosexual pairing in male Japanese beetles (Popillia japonica Newman) in the field and in the laboratory. Specifically, we investigated how time of day, sex ratio, beetle density, and temperature affected the likelihood of homosexual pairing. In the field, male–male pairs constituted 1–6% of the pairs we collected. Homosexual pairs were more common in the afternoon than in the morning and the evening. Sex ratio, density, and temperature were all related to the likelihood of finding a homosexual pair, but the relationships were not linear. In the laboratory, higher male densities and relatively male-biased sex ratios were associated with an increase in the frequency of homosexual pairs. Homosexual pairs were more frequent at relatively low and relatively high temperatures. Males that mounted other males tended to be smaller than the males that they mounted. In addition, compared to males that were not homosexually paired, there was some indication that the mounting males were smaller, and the mounted males larger, than the unpaired males. Our data suggest that homosexual pairs are a result of males mistaking other males for females, and we hypothesize that the environmental and social factors cause changes in homosexual pairing through their effects on the frequency of pair formation and pair duration.     

Postconflict Behavior Among Male Japanese Macaques

Reconciliation was first described more than 20 years ago. Since then, it has been observed in many mammals (mainly primates) but data on postconflict behavior among males are still scarce because they usually aggressively compete for mating partners, rarely maintain amicable relationships with one another. Accordingly, reconciliation is expected to occur at low rates. Although this is true for Japanese macaque males, the subspecies on Yakushima Island (Macaca fuscata yakui) seems to represent an exception as grooming among males occurs often. We analyzed postconflict behavior among them and discuss the possible factors that may favor the occurrence of grooming and reconciliation. Selective attraction between former opponents—reconciliation—occurred soon after conflicts. Consolation—affiliative interactions between a focal animal and group members other than the former opponents occurring earlier in PCs than in MCs—was absent among males. Conciliatory tendency is higher for Yakushima macaque males (0.31) versus that in studies on the other subspecies Macaca fuscata. We discuss differences in the behavioral ecology of the 2 subspecies, the ecological and social factors that may favor the occurrence of reconciliation, and the possible benefits that males gain from grooming exchange and reconciliation.     

Homosexual incest avoidance among females in captive Japanese macaques

This paper reports a systematic pattern of homosexual incest avoidance among females in a captive group of Japanese macaques (Macaca fuscata) culled from the Arashiyama-West troop known for its high rates of female homosexuality. The study group included three matrilines and two generations. Between eight and 11 females were sexually active over four consecutive mating seasons, and all engaged in both heterosexual and homosexual activity. While all females performed homosexual acts with almost all possible non-kin partners, they systematically avoided homosexual interactions with their mother, daughters, and sisters. This pattern could not be explained either in terms of kin not being simultaneously in estrus, kin avoiding affiliative interactions in general, or non-kin utilizing the tension-reducing effect of estrus to affiliate exclusively with each other. In contrast to homosexual females, heterosexual pairs of relatives (brother-sister, mother-son) were sometimes incestuous. Assuming that female homosexuality expresses the reproductive strategy of females unconstrained by male influence, the present results point to the strong tendency of females to avoid incest and suggest that males are primarily responsible for the reported exceptions to incest avoidance.     

Male-Infant Interactions in Baboons and Macaques: A Critique and Reevaluation

A critical reexamination of the empirical data on male-infantinteractions among baboons and macaques reveals a number ofsignificant contrasts between them. On an absolute and relativescale, the frequency of occurrence among baboons is rare. Whenmale baboons do interact with infants, only a small proportionof all available male actors do so, and even fewer still (lessthan one-quarter) account for any substantial percentage ofall interactions. In contrast, macaque males are very frequentlyand commonly involved with infants; all males of the group interactwith infants to some degree, and a greater proportion of allthe group's males can be characterized as "heavily involved"with infants. The rejection of the role of kinship in interpretingthis phenomenon, especially as it occurs among baboons, hasrested almost exclusively on the pattern of estimated paternitybetween male and infant from behavioral (consort) criteria.These behavioralbased data are incomplete at best, possiblyincorrect in some instances, and in fact, in many studies kinshipappears to be a predominant factor. Until patrilineal data arederived from independent cytogenetic studies, these evolutionaryinterpretations must be viewed with extreme skepticism.     

短尾猴的社会行为与社会关系

群体生活的动物通过社会行为相联系,社会行为的类别和发生的频率决定了动物社会关系的性质,进而决定了社会结构的类型。本文根据作者在安徽黄山对短尾猴16年的观察研究,描述和分析了一些重要的社会行为,探讨了短尾猴社会中各种社会关系的特点和性质。雌性短尾猴之间的行为比较简单,缺乏多样性,主要通过近距及理毛等状态性行为建立和维持,是长久和稳固的关系;雄性短尾猴之间具有丰富的行为,事件性行为(如拥抱、爬跨等)占主要部分,易发生冲突但也易于和解;雄性和雌性关系与繁殖季节有关,交配期主要是性关系,产仔期主要是友好关系;成体和幼体的关系主要是照料与被照料的关系。     

Interannual Variation in Nut Abundance Is Related to Agonistic Interactions of Foraging Female Japanese Macaques (Macaca fuscata)

The importance of dominance status to foraging and ultimately survival or reproductive success in wild primates is known; however, few studies have addressed these variables simultaneously. We investigated foraging and social behavior among 17 adult female Japanese macaques (Macaca fuscata) on Kinkazan Island, northern Japan, from September to November in 2 consecutive years (2004 and 2005) to determine whether interannual variation in food availability was related to variation in agonistic interactions over food resources and the feeding behavior of individuals of different dominance rank. We compared energy obtained with daily energy requirements and also examined the effect of variation in feeding behavior on female survival and reproductive success. Fruiting conditions differed considerably between the 2 yr: of four nut-producing species, the nuts of only Torreya nucifera fruited in 2004, whereas all four species, particularly Fagus crenata, produced nuts in abundance in 2005. The abundance and average crown size of trees of Torreya nucifera were smaller than those of Fagus crenata, and there was a higher frequency of agonistic interactions during 2004, when dominant, but not subordinate, individuals were able to satisfy daily energy requirements from nut feeding alone through longer nut feeding bouts. In contrast, all macaques, regardless of their dominance rank, were able to satisfy their energy requirements by feeding on nuts in 2005. Subordinate macaques appeared to counter their disadvantage in 2004 by moving and searching for food more and maintaining larger interindividual distances. Several lower-ranking females died during the food-scarce season of 2004, and only one dominant female gave birth the following birth season. In contrast, none of the adult females died during the food-scarce season of 2005, and 12 females gave birth the following birth season. These findings suggest that an interaction between dominance rank and interannual variation in food availability are related to macaque behavior, survival, and reproduction.     

Heterosexual and Homosexual Partners Practising Unprotected Sex May Develop Allogeneic Immunity and to a Lesser Extent Tolerance

Background

Epidemiological studies suggest that allogeneic immunity may inhibit HIV-1 transmission from mother to baby and is less frequent in multiparous than uniparous women. Alloimmune responses may also be elicited during unprotected heterosexual intercourse, which is associated ex vivo with resistance to HIV infection.

Methodology/Principal Findings

The investigation was carried out in well-defined heterosexual and homosexual monogamous partners, practising unprotected sex and a heterosexual cohort practising protected sex. Allogeneic CD4⁺ and CD8⁺ T cell proliferative responses were elicited by stimulating PBMC with the partners'' irradiated monocytes and compared with 3^rd party unrelated monocytes, using the CFSE method. Significant increase in allogeneic proliferative responses was found in the CD4⁺ and CD8⁺ T cells to the partners'' irradiated monocytes, as compared with 3^rd party unrelated monocytes (p≤0.001). However, a significant decrease in proliferative responses, especially of CD8⁺ T cells to the partners'' compared with 3^rd party monocytes was consistent with tolerization, in both the heterosexual and homosexual partners (p<0.01). Examination of CD4⁺CD25⁺FoxP3⁺ regulatory T cells by flow cytometry revealed a significantly greater proportion of these cells in the homosexual than heterosexual partners practising unprotected sex (p<0.05). Ex vivo studies of infectivity of PBMC with HIV-1 showed significantly greater inhibition of infectivity of PBMC from heterosexual subjects practising unprotected compared with those practising protected sex (p = 0.02).

Conclusions/Significance

Both heterosexual and homosexual monogamous partners practising unprotected sex develop allogeneic CD4⁺ and CD8⁺ T cell proliferative responses to the partners'' unmatched cells and a minority may be tolerized. However, a greater proportion of homosexual rather than heterosexual partners developed CD4⁺CD25FoxP3⁺ regulatory T cells. These results, in addition to finding greater inhibition of HIV-1 infectivity in PBMC ex vivo in heterosexual partners practising unprotected, compared with those practising protected sex, suggest that allogeneic immunity may play a significant role in the immuno-pathogenesis of HIV-1 infection.     

Coevolution of Facial Expression and Social Tolerance in Macaques

The purpose of this study is to test the hypothesis that social tolerance drives the evolution of facial expression in macaques. Macaque species exhibit a range of social styles that reflect a continuum of social tolerance. Social interactions in more tolerant taxa tend to be less constrained by rank and kinship than in less‐tolerant macaques. I predicted that macaques that are more tolerant would exhibit a wider range of facial displays than less‐tolerant species because interactions that are open to negotiation are characterized by greater uncertainty than interactions that are constrained by rank or kinship. To test this hypothesis, I conducted a phylogenetically informed regression analysis (N = 11) using previously published data on repertoire size and two quantitative measures of social tolerance (conciliatory tendency and counter‐aggression). As predicted, macaques with more tolerant social styles tended to have larger repertoires than less‐tolerant species. These results support the hypothesis that increased social tolerance favors the elaboration of communication to mitigate uncertainty.     

Troop Extinction and Female Fusion in Wild Japanese Macaques in Yakushima

We observed three cases of troop extinction and two cases of female fusion in the wild population of Japanese macaques on Yakushima Island, Japan. Troops P and T decreased in size relatively slowly over a few years until each troop consisted of only three monkeys. Several months later, the remaining adult female of P merged with the adjacent troop S, followed by the remaining female of T. S subsequently also decreased in size and disappeared about 2 years later. In the early stage of troop decline, the mortality rate of adult females was as low as in a growing troop, but the birthrate was quite low. In the late stage of troop decline, the mortality rate increased and the birthrate remained low. An important factor leading to troop extinction may be an increase in population density and the resulting increase in intergroup competition. During the period when P and T declined and ceased to exist, the range of the adopted troop shifted to cover their previous ranges. In the fused troop, there was no severe aggression directed towards the immigrant females or harassment from residents of the adopted troop and there was affiliative social interaction between the immigrant females and resident members. These results agree with previous reports on female fusion: it occurs when the shrinking group consists of one or no adult member, and the immigrant females are not at a severe disadvantage in their adoptive group. A possible benefit for immigrant females is to avoid disadvantage of one-adult group in conflict with conspecifics. A possible cost for immigrant females is transfer to the other troop or to unfamiliar area or both. The cost to transfer to another group may not be high because the members of the adoptive troop are relatively tolerant to immigrants. The cost to transfer to unfamiliar range may be minimized by immigration to the troop whose range shifted to the immigrants' former range.     

Agonistic Support in Juvenile Japanese Macaques: Cognitive and Functional Implications

Agonistic support is generally considered a classical example of altruistic behaviour. It plays a critical role in the process of rank acquisition. This study investigates agonistic coalitions involving juvenile Japanese macaques (Macaca fuscata) living in a large captive group. Kinship was a good predictor of agonistic support received by juvenile macaques. Kinship also had a significant, though weaker, influence on agonistic support given by juvenile macaques. The latter was strongly influenced by the prospective rank of the individual against which the coalition was directed, i.e. by the rank relationship between the target of the coalition and the juvenile’s mother. Juvenile macaques intervened aggressively more against prospectively subordinate individuals than against prospectively dominant individuals. These results imply agonistic support is not necessarily altruistic, and support the hypothesis that primates may understand the rank relationship that exist among their group mates, i.e. that they are aware of third‐party social relationships. They also suggest that selective pressures associated with the process of rank acquisition may have favoured the evolution of higher cognitive abilities.     

Variation in Intergroup Encounters in Two Populations of Japanese Macaques

The nature of intergroup encounters differed between two populations of wild Japanese macaques (Macaca fuscata): the Yakushima and Kinkazan populations. In the Yakushima population, intergroup encounters were more likely to result in the displacement of one group, intergroup agonistic interaction was common, and intergroup dominance was usually distinct. When displacement occurred at Yakushima, larger groups tended to dominate smaller ones. Conversely, in the Kinkazan population, intergroup encounters rarely resulted in displacement, intergroup agonistic interaction was rare, and intergroup dominance was usually unclear. Thus, monkeys in Yakushima appear to defend resources actively during encounters, while those in Kinkazan usually did not defend resources. The frequency of encounters was significantly higher in Yakushima than in Kinkazan. The two populations had very different group densities and traveling speeds, both of which directly influence the chance of encounters. Taking these differences into account, we compared the observed frequency with those predicted by the ideal gas model. The observed frequencies in both populations were about one-third of the number expected with the model, which suggests that the differences in encounter frequency were caused by differences in group density and traveling speed. We discuss this intraspecific variation in light of economic defendability in connection to habitat differences and the evolutionary significance of resource defense behavior.     

Social and Demographic Influences on Mothering Style in Pigtail Macaques

This study represents the first investigation of variability in mothering styles in pigtail macaques, Macaca nemestrina nemestrina. Fifteen group-living mother-infant pairs were focally observed during the first 12 wk of infant life and several measures of maternal and infant behavior were recorded. Variability in mothering styles occurred along the three dimensions of maternal protectivencss, rejection, and warmth. Maternal parity and aggression received by mothers were the best predictors of variability in protectiveness and warmth, whereas variability in rejection was not predicted by any of the variables considered. This study provides clear evidence that aggression towards mothers and previous maternal experience have an important influence on mothering styles in pigtail macaques.