Social and sexual behaviors predict immune system activation, but not adrenocortical activation, in male rhesus macaques

Social interactions are well known to influence fitness in social animals, but the physiological processes that connect the two remain largely unknown. This study aimed to explore how variation in sociality influences the adrenocortical and/or immune system in the rhesus macaque, a seasonally breeding species engaging in indirect male-male mating competition. We collected data on 18 adult male rhesus macaques living on Cayo Santiago over 4 months during the mating season. We assessed fecal glucocorticoids (fGCs), a marker of the physiological stress response, and urinary neopterin (uNEO), a marker of immune system activation. We predicted that males who spent more time affiliated with groupmates would have decreased fGCs due to the physiological buffering potential of positive social interaction and increased uNEO associated with increased exposure to disease. Additionally, we predicted that uNEO would increase in response to copulation, consortship, and as the mating season progressed due to infection associated with sexual behavior. Although none of our sociosexual behaviors of interest predicted fGCs, the proportion of time males spent grooming, and specifically the proportion of time males spent receiving grooming from juveniles, was positively associated with concurrent uNEO concentrations. Copulation was negatively correlated with concurrent uNEO, and uNEO, but not fGCs, increased as the mating season progressed. These results indicate that certain social behaviors are associated with immune system activation and provide a putative physiological link between the physical demands of endurance rivalry and mortality commonly observed in males of this species. Significance statement Social interactions can strongly influence health in social animals, possibly mediated through the endocrine and/or immune system. We investigated how affiliative social and sexual interactions influence these systems in male rhesus macaques by non-invasively measuring hormones associated with energy allocation and responses to stressors (glucocorticoids) and a marker of immune system activation (neopterin). The sociosexual behaviors measured here did not appear to covary with glucocorticoid concentrations; however, higher neopterin concentrations were observed when males spent more time grooming. We also found that males spent less time copulating when their neopterin concentrations were high and that there is a general increase in neopterin concentrations as the mating season progresses. Our results show that variation in social and sexual behavior is associated with neopterin production in the rhesus macaque, suggesting that social investment by groupmates and disease transmission may be important factors mediating the relationship between sociality and fitness in social species.