Early involvement in friendships predicts later plasma concentrations of oxytocin and vasopressin in juvenile rhesus macaques (Macaca mulatta)

Abstract

The neuropeptides oxytocin (OT) and arginine vasopressin (AVP) are involved in social bonding in attachment relationships, but their role in friendship is poorly understood. We investigated whether rhesus macaques’ (Macaca mulatta) friendships at age one predicted plasma OT and AVP at two later time points. Subjects were 54 rhesus macaques at the California National Primate Research Center (CNPRC). Blood was drawn during a brief capture-and-release in the home cage, and plasma assayed for OT and AVP using an enzyme immunoassay (EIA). Separate linear mixed models for each sex tested the effects of dominance rank, age, sampling time point, housing condition, parturition status, two blood draw timing measures, and five friendship types: proximity friendships, play friendships, reciprocal friendships (a preference for a peer that also preferred the subject), multiplex friendships (friendships displayed in more than one behavioral domain), and total number of friendships. Females’ number of reciprocal and play friendships at age one significantly predicted later OT; additionally, these two friendship types interacted with rank, such that high-ranking females with the fewest friendships had the highest OT concentrations. Friendship did not predict later OT levels in males, however proximity, play, reciprocal, and total number of friendships predicted males’ plasma AVP. Play and total number of friendships also tended to predict AVP in females. Our results show that peripheral measures of neuroendocrine functioning in juvenile rhesus monkeys are influenced by early involvement in friendships. Friendships have an especially strong impact on an individual’s psychosocial development, and our data suggest OT and AVP as potential underlying mechanisms. Moreover, sex differences in the functioning of the OT and AVP systems, and their relation to friendship, may have important clinical implications for the use of OT as a therapeutic, as well as informing the social context in which it is administered.

Evolving the neuroendocrine physiology of human and primate cooperation and collective action

“…Friendships involve the reciprocal exchange of various social behaviours such as grooming, food sharing and coalitionary support [2,[58][59][60], and appear to be regulated by OT. For example, a greater number and intensity in female friendships in macaques is associated with higher levels of baseline OT, though the same effect was not found among male macaques [22]. In chimpanzees, acute increases in OT occur following food sharing, leading to an intensification of reciprocal investment in the relationship [21].…”

“…The neuroendocrine physiology of OT was co-opted for numerous behaviours associated with maternal care including the regulation of the amount of care given by mothers and demanded [20,21], macaques [22], marmosets [23] [9, 13,24,25] intergroup interactions [26,27] testosterone paternal care marmosets [28], not titi monkeys [29] [16] pair bond [16] in-group [30] [31] out-group chimpanzees [32] [33] no effect [34] intrasexual competition chimpanzees [35], baboons [36], colobus monkeys [37], not bonobos [38] [ 39,40] [ 31] rstb.royalsocietypublishing.org Phil. Trans.…”

Compared to what: what can we say about nonapeptide function and social behavior without a frame of reference?

“…Indeed, advances in understanding nonapeptide function and social behavior in the lab have been made in several examples of tractable, non-traditional species. These examples include meadow voles [38], mandarin voles [39], tuco tucos [40], deer mice [41, 42], African striped mice [43, 44], guinea pigs [45], tree shrews [46•], titi monkeys [47•], rhesus macaques [48, 49], zebra finches [50, 51], anole lizards [52], tree frogs [53], butterfly fish [54], and cichlid fishes [55, 56]. …”

Oxytocin-induced coping with stressful life events in old age depends on attachment: Findings from the cross-sectional KORA Age study

“…hypothalamic-pituitary-adrenal (HPA) axis (Brune, 2012). Interestingly, it was demonstrated in macaques that not only parental relationships (essential in the formation of secure attachment style) but also friendships in early life predict oxytocin in later life (Weinstein et al, 2014). Thus, despite the fact that both oxytocin and HPA axis activity in adulthood are impacted by early life experiences (Gunnar and Quevedo, 2008;Feldman, 2012), these pathways are pliable and influenced throughout life, beginning with care-giver/parental interactions, to close friendships, to socio-cultural networks in later life.…”