Urinary oxytocin and social bonding in related and unrelated wild chimpanzees

Abstract

Animals that maintain cooperative relationships show gains in longevity and offspring survival. However, little is known about the cognitive or hormonal mechanisms involved in cooperation. Indeed, there is little support for a main hypothesis that non-human animals have the cognitive capacities required for bookkeeping of cooperative exchanges. We tested an alternative hypothesis that cooperative relationships are facilitated by an endocrinological mechanism involving oxytocin, a hormone required for bonding in parental and sexual relationships across mammals. We measured urinary oxytocin after single bouts of grooming in wild chimpanzees. Oxytocin levels were higher after grooming with bond partners compared with non-bond partners or after no grooming, regardless of genetic relatedness or sexual interest. We ruled out other possible confounds, such as grooming duration, grooming direction or sampling regime issues, indicating that changes in oxytocin levels were mediated by social bond strength. Oxytocin, which is thought to act directly on neural reward and social memory systems, is likely to play a key role in keeping track of social interactions with multiple individuals over time. The evolutionary linkage of an ancestral hormonal system with complex social cognition may be the primary mechanism through which long-term cooperative relationships develop between both kin and non-kin in mammals.

Figure 1.

The influence of relationship quality and recent grooming on urinary oxytocin levels (n = 33 subjects, n = 137 samples). Urinary oxytocin levels following a single bout of grooming (more than 10 min) with a genetically related bond partner, an unrelated bond partner, a non-bond partner or following resting or feeding (control). Box plots show median and quartiles, whiskers show the 95% CI, and circles indicate values >95% CI. Differences across behavioural conditions: *p < 0.05 (table 1b).

Figure 2.

The distribution of grooming-related predictor variables with respect to grooming condition and urinary oxytocin levels (n = 31 subjects, n = 78 samples). Predictor variables: (a) sex combination of dyad (number of urine samples per condition: female–female dyads: n = 22 [non-bond = 4, non-kin bond = 6, kin = 12]; male–female dyads: n = 26 [non-bond = 11, non-kin bond = 6, kin = 9]; male–male dyads: n = 30 [non-bond = 19, non-kin bond = 9, kin = 2]; (ii) direction of grooming (bidirectional: subject gives and receives grooming: n = 50 [non-bond = 16, non-kin bond = 14, kin = 20]; groomee (subject receives grooming): n = 13 [non-bond = 8, non-kin bond = 4, kin = 1]; groomer (subject gives grooming): n = 15 [non-bond = 10, non-kin bond = 3, kin = 2]. Box plots contain data from all subjects, show median and quartiles, and whiskers show 95% CI. Circles and asterisk show values > 95% CI (see table 1b).

Figure 3.

Grooming duration relative to urinary oxytocin levels across three grooming conditions. Urine samples from kin bond partner grooming, non-kin bond partner grooming and non-bond partner grooming conditions included.