Oxytocin increases after affiliative interactions in male Barbary macaques

Abstract

14Mammals living in stable social groups often mitigate the costs of group living through the 15 formation of social bonds and cooperative relationships. The neuropeptide hormone 16 oxytocin (OT) has been proposed to promote both bonding and cooperation although only 17 a limited number of studies have investigated this under natural conditions. Our aim was to 18 assess the role of OT in bonding and cooperation in male Barbary macaques (Macaca 19 sylvanus). First we tested for an effect of affiliation -grooming and triadic male-infant-male 20 interactions -with bond and non-bond partners on urinary OT levels. Secondly we aimed to 21 test whether grooming interactions (and thus increased OT levels) increase a male's 22 general propensity to cooperate in polyadic conflicts. We collected behavioral data via full-23 day focal animal protocols on 14 adult males and measured endogenous OT levels from 24 139 urine samples collected after affiliation and non-social control periods. Urinary OT 25 levels were higher after grooming with any partner. By contrast, OT levels after male-26 infant-male interactions with any partner or with bond partners were not different from 27 controls but were higher after interactions with non-bond partners. Previous grooming did 28 not increase the likelihood of males to support others in conflicts. Collectively, our results 29 support research indicating that OT is involved in the regulation of adult social bonds, 30 including in non-reproductive contexts. However, our male-infant-male interaction results 31 go against previous studies suggesting that it is affiliation with bond rather than non-bond 32 partners that trigger the release of OT. Alternatively, OT levels may have been elevated 33 prior to male-infant-male interactions thus facilitating interaction between non-bond 34 partners. The lack of an association of grooming (and by extension increased OT levels) and 35 subsequent support speaks against an OT linked increase in the general propensity to 36cooperate, yet further studies are needed for a more direct test including the possibility of 37 partner-specific contingent cooperation. 38

Oxytocin increases after affiliative interactions in male Barbary macaques

“…Overall we found a high probability that urinary OT levels are elevated following grooming interactions in adult male Barbary macaques. This is generally in line with previous studies showing a positive relationship between OT and grooming (primates: Benítez et al, 2018;Crockford et al, 2013;Snowdon et al, 2010;vampire bats, Desmodus rotundus: Carter and Wilkinson, 2015), as well as other socio-positive interactions more generally (primates: Preis et al, 2018;Benítez et al, 2018;Snowdon et al, 2010;Wittig et al, 2014;vampire bats: Carter and Wilkinson, 2015;dogs: Romero et al, 2014). Given the low number of grooming between non-bonded partners in our study, we could not test partner specific effects of grooming.…”

“…Questions still remain under which contexts OT release is partner specific. It has been suggested that in smaller social groups, all group members are bonded to a sufficient degree to elicit OT release after affiliative interactions (Benítez et al, 2018), whereas in larger groups variance in affiliation rates may be large enough that OT release may only occur after affiliations with more closely bonded partners. Such an explanation would be consistent with observed differences in partner specificity of OT release between chimpanzee populations (Crockford et al, 2013;Preis et al, 2018).…”

“…Similar to previous studies in chimpanzees and tufted capuchins (Benítez et al, 2018;Crockford et al, 2013), we tested in Barbary macaques whether urinary OT levels were influenced by grooming interactions and -given its functional relevance in Barbary macaques -also by male-infant-male interactions. We predicted that urinary OT levels would be higher after affiliative interactions (i.e., grooming, male-infant-male interactions) compared to a control period without any social interactions.…”

“…We presumed a clearance window of 15 to 60 min for excretion of OT in urine, as done in previous studies investigating urinary OT levels in other non-human primates which show biologically relevant changes in behavior during this window (Benítez et al, 2018;Crockford et al, 2013;Samuni et al, 2017). Studies in humans and marmosets have demonstrated elevated OT levels in urine 30 to 60 after administration of radio-labelled hormone (humans: Amico et al, 1987;marmosets: Seltzer and Ziegler, 2007).…”

“…Studies in humans and marmosets have demonstrated elevated OT levels in urine 30 to 60 after administration of radio-labelled hormone (humans: Amico et al, 1987;marmosets: Seltzer and Ziegler, 2007). Exogenous administration of OT in tufted capuchin monkeys also caused elevated urinary OT levels 15-60 min after administration (Benítez et al, 2018). Prior to analysis, urine samples were assigned to different behavioral conditions depending on whether at least one grooming (total time ≥ 60 sec), triadic male-infant-male interaction or no social interactions occurred in the 45 min clearance window.…”