Variation in the social behavior, perception, and biology of the rhesus macaque (Macaca mulatta)

Sociality evolved due to the enhanced fitness benefits associated with group living and was likely facilitated by the evolution of neural pathways that support the perception of social stimuli. Despite the adaptive benefits of proper processing of social stimuli, within-species differences in social perception abilities exist. This dissertation studies the highly social rhesus macaque in order to investigate the complex inter-relationships between individual variation in social perception, social interactions with conspecifics, and markers of oxytocin (OT) and arginine vasopressin (AVP) functioning, two neuropeptides known to modulate both social perception and social affiliation. Study 1 quantified individual differences in social perception abilities during infancy to test whether these abilities predict group differences in sociality later in life. While researchers had theorized that low social connectedness is associated with poor perception of social signals in adulthood, the relationship between early social perceptual abilities and later social functioning had not been previously tested. This study showed that monkeys with greater social recognition and social communication abilities in infancy are more likely to be categorized as high-social, whereas monkeys with impairments in these species-typical abilities in infancy are more likely to be categorized as low-social, later in life. These findings suggest that social perceptual differences at 3-4 months of age are early indicators of developmental trajectories that may ultimately influence social functioning into early adulthood. Study 2 quantified OT concentrations from concomitantly collected cerebrospinal fluid (CSF) and blood samples to test whether individual differences in social recognition during infancy are associated with markers of endogenous OT biology during juvenility. While studies had shown that administration of exogenous OT changes how primates visually process faces, whether natural variation in face processing abilities is related to differences in endogenous OT functioning was unknown. This study showed that face recognition ability in infancy positively predicts CSF OT concentration up to 5 years later, such that individuals with the greatest social recognition abilities in infancy had the highest CSF OT concentrations later in life. These findings suggest that individual social perceptual differences are associated with natural variation in OT concentrations when assessed in central, but not in peripheral, matrices. Study 3 used home corral observations of social interactions during juvenility to test whether variation in OT and AVP biology is associated with differences in social communication abilities and the quality of social relationships. While neuropeptides are known to facilitate social bonds between conspecifics, whether this relationship is mediated by variation in social communication abilities was unknown. This study showed that monkeys with higher CSF AVP concentrations use more groom solicitations, an important affiliative social signal in the species, and that this social signal, in turn, is associated with a greater number of strongly bonded social partners. These findings suggest that AVP signaling exerts an influence on the strength of social bonds through groom solicitations. These collective studies advance a nuanced perspective on how endogenous OT and AVP functioning facilitates social interactions, in part, by modulating the perception of socially relevant stimuli. Specifically, this dissertation revealed that variation in social perceptual abilities during infancy are related to both OT functioning and group differences in sociality, and that the relationship between variation in sociality and AVP functioning is mediated by an individual's social perceptual abilities. In doing so, this dissertation promotes a better understanding of how these neuropeptide systems enabled the evolution of sociality.

Advisor: Parker Karen J.
Capitanio John 
Darian-Smith Corinna 
Garner Joseph P.
Lyons David (David Michael)