Oxytocin increases after affiliative interactions in male Barbary macaques

Abstract

Mammals living in stable social groups often mitigate the costs of group living through the formation of social bonds and cooperative relationships. The neuropeptide hormone oxytocin (OT) has been proposed to promote both bonding and cooperation although only a limited number of studies have investigated this under natural conditions. Our aim was to assess the role of OT in bonding and cooperation in male Barbary macaques (Macaca sylvanus). First we tested for an effect of affiliation -grooming and triadic male-infant-male interactions -with bond and non-bond partners on urinary OT levels. Secondly we aimed to test whether grooming interactions (and thus increased OT levels) increase a male's general propensity to cooperate in polyadic conflicts. We collected behavioral data via fullday focal animal protocols on 14 adult males and measured endogenous OT levels from 139 urine samples collected after affiliation and non-social control periods. Urinary OT levels were higher after grooming with any partner. By contrast, OT levels after maleinfant-male interactions with any partner or with bond partners were not different from controls but were higher after interactions with non-bond partners. Previous grooming did not increase the likelihood of males to support others in conflicts. Collectively, our results support research indicating that OT is involved in the regulation of adult social bonds, including in non-reproductive contexts. However, our male-infant-male interaction results go against previous studies suggesting that it is affiliation with bond rather than non-bond partners that trigger the release of OT. Alternatively, OT levels may have been elevated prior to male-infant-male interactions thus facilitating interaction between non-bond partners. The lack of an association of grooming (and by extension increased OT levels) and subsequent support speaks against an OT linked increase in the general propensity to cooperate, yet further studies are needed for a more direct test including the possibility of partner-specific contingent cooperation.

Testosterone and cortisol are negatively associated with ritualized bonding behavior in male macaques

“…CC-BY-ND 4.0 International license a certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under The copyright holder for this preprint (which was not this version posted March 18, 2020. ; https://doi.org/10.1101/765123 doi: bioRxiv preprint previous study on the same group of Barbary macaques we did not find an increase in oxytocin levels following triadic interactions in general but found that oxytocin levels were only higher after triadic interactions with non-bond partners (Rincon et al, 2020). If the combination of low testosterone and high oxytocin is responsible for bonding, then triadic interactions may function to form bonds selectively between non-bonded partners while physiologically not affecting existing bonds between strongly bonded partners.…”

Effects of Stroking on Salivary Oxytocin and Cortisol in Guide Dogs: Preliminary Results

“…Regarding social behavior, OXT secretion after positive social interaction is widely observed in primates [12][13][14][15], but the impact of relationship strength on OXT release is not yet well known. In one study on chimpanzees, urinary OXT concentration increased after grooming with a bonded partner, but not after the same interaction with a nonbonded partner [13]; on the contrary, two studies suggest that OXT secretion is independent of affiliative relationship strength [14,16].…”

Social correlates of variation in urinary oxytocin concentrations of mantled howler monkeys Alouatta palliata (Gray, 1849) (Primates: Atelidae): A preliminary assessment

“…Urinary oxytocin concentrations of mantled howler monkeys were higher when individuals participated in affiliative interactions, a pattern also observed in capuchin monkeys, chimpanzees, common marmosets, Barbary macaques, and humans (Seltzer & Ziegler, 2007;Morhenn et al, 2008;Witting et al, 2014;Benítez et al, 2018;Rincon et al, 2020). However, whereas the relationship between oxytocin concentrations following affiliation and the quality of social relationships is positive in chimpanzees (Crockford et al, 2013), it was negative in mantled howler monkeys.…”

“…Thus, oxytocin may be part of a positive feedback mechanism underlying socialization. This mechanism is both associated with positive interactions with peers (i.e., affiliation) and agonistic behavior (De Dreu, 2012;Anacker & Beery, 2013;Fujii et al, 2016;Samuni et al, 2016;Benítez et al, 2018;Cavanaugh et al, 2018;Rincon et al, 2020). In the latter, oxytocin facilitates the categorization of individuals as belonging to the same or another group, promoting cooperation and trust toward ingroup peers, but fear and distrust towards outgroup individuals (De Dreu, 2012;Fujii et al, 2016).…”