Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees

Humans excel in cooperative exchanges between unrelated individuals. Although this trait is fundamental to the success of our species, its evolution and mechanisms are poorly understood. Other social mammals also build long-term cooperative relationships between non-kin, and recent evidence shows that oxytocin, a hormone involved in parent–offspring bonding, is likely to facilitate non-kin as well as kin bonds. In a population of wild chimpanzees, we measured urinary oxytocin levels following a rare cooperative event—food sharing. Subjects showed higher urinary oxytocin levels after single food-sharing events compared with other types of social feeding, irrespective of previous social bond levels. Also, urinary oxytocin levels following food sharing were higher than following grooming, another cooperative behaviour. Therefore, food sharing in chimpanzees may play a key role in social bonding under the influence of oxytocin. We propose that food-sharing events co-opt neurobiological mechanisms evolved to support mother–infant bonding during lactation bouts, and may act as facilitators of bonding and cooperation between unrelated individuals via the oxytocinergic system across social mammals.     

Variation in oxytocin is related to variation in affiliative behavior in monogamous, pairbonded tamarins

Oxytocin plays an important role in monogamous pairbonded female voles, but not in polygamous voles. Here we examined a socially monogamous cooperatively breeding primate where both sexes share in parental care and territory defense for within species variation in behavior and female and male oxytocin levels in 14 pairs of cotton-top tamarins (Saguinus oedipus). In order to obtain a stable chronic assessment of hormones and behavior, we observed behavior and collected urinary hormonal samples across the tamarins’ 3-week ovulatory cycle. We found similar levels of urinary oxytocin in both sexes. However, basal urinary oxytocin levels varied 10-fold across pairs and pair-mates displayed similar oxytocin levels. Affiliative behavior (contact, grooming, sex) also varied greatly across the sample and explained more than half the variance in pair oxytocin levels. The variables accounting for variation in oxytocin levels differed by sex. Mutual contact and grooming explained most of the variance in female oxytocin levels, whereas sexual behavior explained most of the variance in male oxytocin levels. The initiation of contact by males and solicitation of sex by females were related to increased levels of oxytocin in both. This study demonstrates within-species variation in oxytocin that is directly related to levels of affiliative and sexual behavior. However, different behavioral mechanisms influence oxytocin levels in males and females and a strong pair relationship (as indexed by high levels of oxytocin) may require the activation of appropriate mechanisms for both sexes.     

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.     

Social Grooming in Bats: Are Vampire Bats Exceptional?

Evidence for long-term cooperative relationships comes from several social birds and mammals. Vampire bats demonstrate cooperative social bonds, and like primates, they maintain these bonds through social grooming. It is unclear, however, to what extent vampires are special among bats in this regard. We compared social grooming rates of common vampire bats Desmodus rotundus and four other group-living bats, Artibeus jamaicensis, Carollia perspicillata, Eidolon helvum and Rousettus aegyptiacus, under the same captive conditions of fixed association and no ectoparasites. We conducted 13 focal sampling sessions for each combination of sex and species, for a total of 1560 presence/absence observations per species. We observed evidence for social grooming in all species, but social grooming rates were on average 14 times higher in vampire bats than in other species. Self-grooming rates did not differ. Vampire bats spent 3.7% of their awake time social grooming (95% CI = 1.5–6.3%), whereas bats of the other species spent 0.1–0.5% of their awake time social grooming. Together with past data, this result supports the hypothesis that the elevated social grooming rate in the vampire bat is an adaptive trait, linked to their social bonding and unique regurgitated food sharing behavior.     

Why preen others? Predictors of allopreening in parrots and corvids and comparisons to grooming in great apes

Allogrooming in primates serves not only a hygienic function, but also plays a crucial role in maintaining strong affiliative bonds between group members, which in turn, underpin the emergence of cooperative behavior. In contrast, although allopreening occurs in many avian species, we know little about its social functions. Our study addresses this issue by investigating allopreening in a broad comparative data set including six corvid and nine parrot species. We assessed whether rates of allopreening initiations, proportion of time spent allopreening, and the number of grooming partners in captive group-housed birds were comparable to patterns observed in captive chimpanzees and bonobos. While parrots and corvids were found to have similar rates of social grooming to bonobos and chimpanzees, Pan species dedicated significantly more time to social grooming. Animals in larger groups had more grooming partners, but when controlling for the number of potential partners, birds tended to have fewer grooming interaction partners than Pan species. We then investigated whether allopreening in parrots and corvids was predicted by behavioral markers of affiliative social bonds (close physical proximity, active feeding, and low levels of agonistic behavior). Results revealed that providing allopreening to a partner was significantly predicted by often being in close proximity, but not engagement in active feeding or agonistic behavior. We examined the region allopreened in a subset of species and found that preening a partner's head was predicted by both close physical proximity and active feeding, while body allopreening was only predicted by close physical proximity. Head preening may confer more hygienic benefits to recipients, and thus, may be more selectively provided to valued partners. Results support the hypothesis that allopreening in corvids and parrots helps maintain social bonds with an individual's most important social partners, showing some similarities to allogrooming in primates.     

Reconciliation and relationship quality in Assamese macaques (Macaca assamensis)

A consistent conclusion in reconciliation research is that animals that reconcile are likely to have strong social bonds. This has led to the hypothesis that reconciliation occurs most often between valuable social partners. We tested this hypothesis in a group of Assamese macaques (Macaca assamensis) living near a temple in Assam, India. Using focal sample and ad libitum data collection, we recorded the occurrence of reconciliation, grooming, and agonistic aiding, and the outcomes of approach. We used matrix association methods (TauKr correlation) to correlate reconciliation with grooming, aiding, and approach outcome. Females reconciled more often with females with which they had stronger grooming and aiding relationships. The correlation between reconciliation and aiding was significant for support to the aggressor and the victim. In contrast, no such correlations with reconciliation were found for males. This study provides evidence that females reconcile most often with valuable and compatible social partners. The results do not support the relationship-quality hypothesis for males, and we suggest that future studies give more consideration to the possibility that males reconcile for reasons other than to repair relationships with valuable partners.     

Allogrooming, partner choice, and dominance in male anubis baboons

This study was designed to test the hypothesis that among unrelated male baboons (Papio cynocephalus anubis) in single-gender social groups there is no significant association between dominance status and allogrooming performance. The hypothesis was tested using behavioral measures obtained by focal animal sampling techniques. The results indicate that unrelated male baboons established well-defined linear dominance hierarchies, formed allogrooming relationships with one another, and exhibited a nonrandom distribution of allogrooming; however, there were no significant relationships between dominance rank and the frequency of allogrooming. We further tested our results by grouping individuals into three dominance status classes (high, middle, and low) and comparing the classes. Analysis of variance demonstrated no significant differences in rates of allogrooming by dominance class. These results suggest that dominance did not account for the variation in observed allogrooming behavior: Dominance status did not appear to determine the frequency with which animals groomed others, the number of grooming partners, or frequency of grooming that any individual received in comparison to that performed. High-ranking animals did not have significantly more grooming partners than low-ranking animals, and there appeared to be little competition within the groups for subordinates to groom high-ranking animals. When age, kinship, and group tenure are controlled, performance and reception of allogrooming are not strongly associated with dominance in single-gender social groups of male anubis baboons.     

The Association between Oxytocin and Social Capital

Background

Oxytocin is known to be related to social behaviors, including trust. However, few studies have investigated the association between oxytocin levels and social capital. Thus, we tested the hypothesis that endogenous oxytocin levels are positively associated with social capital. We also considered whether the association differed across gender because previous studies have shown differential effects of OT on social behaviors depending on gender.

Methods

We recruited a convenience sample of 50 women and 31 men in Japan via community sampling from whom we obtained urine sample with which to measure oxytocin levels. Individual-level cognitive social capital (social trust and mutual aid) and structural social capital (community participation) were assessed using a questionnaire. We used multivariate regression, adjusted for covariates (age, number of children, self-rated health, and education), and stratified by gender to consider associations between oxytocin and social capital.

Results

Among women, oxytocin was inversely associated with social trust and mutual aid (p<0.05). However, women participating in only 1 organization in the community showed higher oxytocin than women who participated in either no organizations (p<0.05) or 2 or more organization (i.e. inverse-U shape association). Among men, no association was observed between oxytocin and either form of cognitive and structural social capital.

Conclusion

Women who perceived low cognitive social capital showed higher oxytocin levels, while structural social capital showed inverse-U shape association with oxytocin. No association between oxytocin and social capital was found among men. Further study is needed to elucidate why oxytocin was inversely associated with cognitive social capital only among women.     

Intranasal oxytocin increases social grooming and food sharing in the common vampire bat Desmodus rotundus

Intranasal oxytocin (OT) delivery has been used to non-invasively manipulate mammalian cooperative behavior. Such manipulations can potentially provide insight into both shared and species-specific mechanisms underlying cooperation. Vampire bats are remarkable for their high rates of allogrooming and the presence of regurgitated food sharing among adults. We administered intranasal OT to highly familiar captive vampire bats of varying relatedness to test for an effect on allogrooming and food sharing. We found that intranasal OT did not have a detectable effect on food-sharing occurrence, but it did increase the size of regurgitated food donations when controlling for dyad and amount of allogrooming. Intranasal OT in females increased the amount of allogrooming per partner and across all partners per trial, but not the number of partners. We also found that the peak effect of OT treatments occurred 30–50 min after administration, which is consistent with the reported latency for intranasal OT to affect relevant brain areas in rats and mice. Our results suggest that intranasal OT is a potential tool for influencing dyadic cooperative investments, but measuring prior social relationships may be necessary to interpret the results of hormonal manipulations of cooperative behavior and it may be difficult to alter partner choice in vampire bats using intranasal OT alone.     

Sex preferences in Jeju pony foals (Equus caballus) for mutual grooming and play-fighting behaviors

We investigated mutual grooming by Jeju pony (Equus caballus) foals to determine whether male foals preferentially interact with potential future sexual partners or competitors. We predicted that relative to female foals, male foals would exchange grooming more frequently with young mares and that in general, foals would mutually groom more frequently with the opposite sex rather than the same sex. Observing 53 foals between April and October 1998, we recorded 113 mutual grooming events. Male foals exchanged grooming with yearling mares more frequently than with their mother, while female foals exchanged grooming with their mother more frequently than with yearling mares. Contrary to the prediction, foals were not more likely to mutually groom with a foal of the opposite sex than with a foal of the same sex. In our study, 21 instances of play-fighting behavior followed mutual grooming between peers. Relative to intersexual grooming events, play-fighting was more likely to follow intrasexual mutual grooming, and male foals were much more likely to play fight than female foals. These results provide evidence that Jeju pony foals develop and maintain social relationships at the earliest stage of their lives. We suggest that early social experiences might influence social bonding later when the male foal begins to form a harem after separation from its mother.     

The reproductive and heterosexual behaviours of adult patas monkeys in captivity

The reproductive, agonistic, and social interactions between the adult male and adult females of a patas monkey (Erythrocebus patas) harem were investigated. The occurrence of oestrus appeared to be influenced by both social and hormonal factors. Oestrus was not limited to the peri-ovulatory period, but also occurred at other times within the menstrual cycle and after conception. Mating behaviour was correlated with seasonal decreases in daylength and temperature. The male showed no clear preference for either non-pregnant or pregnant sexual partners. Female dominance rank appeared to have little influence on intrasexual competition for copulations. Of the non-reproductive behaviours studied, only two (female-to-male grooming and heterosexual sitting-close) showed significant fluctuations in frequency with changing female reproductive state. For both behaviours, non-pregnant oestrous females showed the highest frequencies.     

Neuroendocrine control in social relationships in non-human primates: Field based evidence

Primates maintain a variety of social relationships and these can have fitness consequences. Research has established that different types of social relationships are unpinned by different or interacting hormonal systems, for example, the neuropeptide oxytocin influences social bonding, the steroid hormone testosterone influences dominance relationships, and paternal care is characterized by high oxytocin and low testosterone. Although the oxytocinergic system influences social bonding, it can support different types of social bonds in different species, whether pair bonds, parent-offspring bonds or friendships. It seems that selection processes shape social and mating systems and their interactions with neuroendocrine pathways. Within species, there are individual differences in the development of the neuroendocrine system: the social environment individuals are exposed to during ontogeny alters their neuroendocrine and socio-cognitive development, and later, their social interactions as adults. Within individuals, neuroendocrine systems can also have short-term effects, impacting on social interactions, such as those during hunting, intergroup encounters or food sharing, or the likelihood of cooperating, winning or losing. To understand these highly dynamic processes, extending research beyond animals in laboratory settings to wild animals living within their natural social and ecological setting may bring insights that are otherwise unreachable. Field endocrinology with neuropeptides is still emerging. We review the current status of this research, informed by laboratory studies, and identify questions particularly suited to future field studies. We focus on primate social relationships, specifically social bonds (mother-offspring, father-offspring, cooperative breeders, pair bonds and adult platonic friendships), dominance, cooperation and in-group/out-group relationships, and examine evidence with respect to the ‘tend and defend’ hypothesis.     

Neuropeptidergic regulation of affiliative behavior and social bonding in animals

Social relationships are essential for maintaining human mental health, yet little is known about the brain mechanisms involved in the development and maintenance of social bonds. Animal models are powerful tools for investigating the neurobiological mechanisms regulating the cognitive processes leading to the development of social relationships and for potentially extending our understanding of the human condition. In this review, we discuss the roles of the neuropeptides oxytocin and vasopressin in the regulation of social bonding as well as related social behaviors which culminate in the formation of social relationships in animal models. The formation of social bonds is a hierarchical process involving social motivation and approach, the processing of social stimuli and formation of social memories, and the social attachment itself. Oxytocin and vasopressin have been implicated in each of these processes. Specifically, these peptides facilitate social affiliation and parental nurturing behavior, are essential for social recognition in rodents, and are involved in the formation of selective mother-infant bonds in sheep and pair bonds in monogamous voles. The convergence of evidence from these animal studies makes oxytocin and vasopressin attractive candidates for the neural modulation of human social relationships as well as potential therapeutic targets for the treatment of psychiatric disorders associated with disruptions in social behavior, including autism.     

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.     

Grooming Between Male Chimpanzees at Ngogo,Kibale National Park. I. Partner Number and Diversity and Grooming Reciprocity

Allogrooming serves many social functions in primates. Grooming can help individuals to service social relationships generally, sometimes reciprocally, and may be particularly important in the development and maintenance of alliances. However, time constraints limit the number of partners with whom one individual can groom enough to maintain cooperative relationships. As a result, the size of its grooming network may reach an asymptote as the size of its group increases, and it may distribute its grooming less equally among potential partners. Chimpanzees live in multimale, fission-fusion communities; males are philopatric, and commonly associate and groom with each other. Males form within-community alliances that influence dominance rank and access to mates, and allies groom with each other regularly; males also cooperate in aggression between communities. The chimpanzee community at Ngogo, in Kibale National Park, Uganda, is unusually large and has more males than any other known community. Field data show that adult Ngogo males groomed far more with other adult males than with females or with adolescent males, in contrast to a previous report (Ghiglieri, 1984). Adolescent males groomed adults much more than the reverse; males groomed and were groomed by females about equally. Individual males groomed mostly with a small number of other males. On average, males at Ngogo had only slightly more male grooming partners overall and had the same number of important partners as those of males in a much smaller community in the Mahale National Park, Tanzania, and they distributed their grooming less equitably. These results fit those expected if limits on available grooming time cause males to have a loyalty problem as the number of potential grooming and alliance partners increases. Despite differences in the extent and equitability of their grooming networks, males at both Ngogo and Mahale showed reciprocity in grooming. Grooming reciprocity has been demonstrated for captive chimpanzee males, but the Ngogo findings are the first demonstrations of reciprocity in wild communities.     

Oxytocin and social affiliation in humans

A conceptual model detailing the process of bio-behavioral synchrony between the online physiological and behavioral responses of attachment partners during social contact is presented as a theoretical and empirical framework for the study of affiliative bonds. Guided by an ethological behavior-based approach, we suggest that micro-level social behaviors in the gaze, vocal, affective, and touch modalities are dynamically integrated with online physiological processes and hormonal response to create dyad-specific affiliations. Studies across multiple attachments throughout life are presented and demonstrate that the extended oxytocin (OT) system provides the neurohormonal substrate for parental, romantic, and filial attachment in humans; that the three prototypes of affiliation are expressed in similar constellations of social behavior; and that OT is stable over time within individuals, is mutually-influencing among partners, and that mechanisms of cross-generation and inter-couple transmission relate to coordinated social behavior. Research showing links between peripheral and genetic markers of OT with concurrent parenting and memories of parental care; between administration of OT to parent and infant's physiological readiness for social engagement; and between neuropeptides and the online synchrony of maternal and paternal brain response in social-cognitive and empathy networks support the hypothesis that human attachment develops within the matrix of biological attunement and close behavioral synchrony. The findings have conceptual implications for the study of inter-subjectivity as well as translational implications for the treatment of social disorders originating in early childhood, such as autism spectrum disorders, or those associated with disruptions to early bonding, such as postpartum depression or child abuse and neglect. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.     

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.     

Genes, brains and mammalian social bonds

Recent studies of monogamous species have revealed the role of the neuropeptides oxytocin and vasopressin in activating reward mechanisms of the brain that are involved in establishing partner recognition and selective 'bonding'. The evolutionary history of these findings resides, at a mechanistic level, in the reciprocal bonding between mother and infant that is common to all mammals. However, in Old World primates, where mother and infant alone would not survive, living in large social groups brings extended family relationships and provides for alloparenting. This has required the emancipation of parenting behaviour from the constraints of hormonal state and the evolution of large brains for decision making that was previously restricted and determined by hormonal state. How this has been achieved, what conserved mechanisms underpin social bonding, and what genetic and mechanistic changes have occurred in the evolution of social bonds are the issues addressed here.     

The role of mesotocin on social bonding in pinyon jays

The neuropeptide oxytocin influences mammalian social bonding by facilitating the building and maintenance of parental, sexual, and same-sex social relationships. However, we do not know whether the function of the avian homologue mesotocin is evolutionarily conserved across birds. While it does influence avian prosocial behavior, mesotocin's role in avian social bonding remains unclear. Here, we investigated whether mesotocin regulates the formation and maintenance of same-sex social bonding in pinyon jays (Gymnorhinus cyanocephalus), a member of the crow family. We formed squads of four individually housed birds. In the first, “pair-formation” phase of the experiment, we repeatedly placed pairs of birds from within the squad together in a cage for short periods of time. Prior to entering the cage, we intranasally administered one of three hormone solutions to both members of the pair: mesotocin, oxytocin antagonist, or saline. Pairs received repeated sessions with administration of the same hormone. In the second, “pair-maintenance” phase of the experiment, all four members of the squad were placed together in a large cage, and no hormones were administered. For both phases, we measured the physical proximity between pairs as our proxy for social bonding. We found that, compared with saline, administering mesotocin or oxytocin antagonist did not result in different proximities in either the pair-formation or pair-maintenance phase of the experiment. Therefore, at the dosages and time frames used here, exogenously introduced mesotocin did not influence same-sex social bond formation or maintenance. Like oxytocin in mammals, mesotocin regulates avian prosocial behavior; however, unlike oxytocin, we do not have evidence that mesotocin regulates social bonds in birds.     

Differential effects of kinship,dominance, and the mating season on female allogrooming in a captive group ofMacaca fuscata

An analysis of allogrooming (total times spent grooming individual partners) of 8 sexually mature females (3–12 years of age) in a captive group of 17 Japanese macaques, shows that during the nonmating season, grooming distributions were characterized by high proportions of grooming given to family members and/or higher ranking nonkin. During the mating season, all eight females showed significant shifts in their grooming distributions, and four females showed significant shifts in grooming between their nonestrous and estrous periods (defined behaviorally). Fox six of eight females, mating season grooming was characterized by either high proportions of grooming given to family members and/or heterosexual and homosexual partners. It was found that within dyadic sexual relationships, dominants gave more grooming to subordinates than the former received, in contrast to a reversal of this pattern in the majority of these same dyads during the nonmating season. This is interpreted as one short-term function of grooming: a dominant asymmetrically grooms a subordinate sexual partner to maintain proximity with (or reduce tension in) the latter. The two remaining focal females (middle ranking, nulliparous) differed from the other females in that they shifted their mating season grooming to subordinate nonkin, despite the lack of evidence that this was a result of sexual interactions, patterns of partner availability, competition, patterns of grooming reciprocity, or agonistic alliance support. From these results, it is suggested that in some contexts, grooming of subordinate nonkin may function to reduce tension in thegroomer. In the Japanese macaque, this latter possibility and the asymmetric grooming of subordinate homosexual partners may prove to be exceptions to the general rule that female cercopithecine grooming of nonkin flows up the dominance hierarchy.