Rhesus monkey sociality is stable across time and linked to variation in the initiation but not receipt of prosocial behavior

• Published in: American journal of primatology Vol. 84; no. 12; pp. e23442 - n/a
• Main Authors: Talbot, Catherine F., Madrid, Jesus E., Del Rosso, Laura A., Capitanio, John P., Garner, Joseph P., Parker, Karen J.
• Format: Journal Article
• Language: English
• Published: United States Wiley Subscription Services, Inc 01-12-2022
• Subjects: Altruism; Animals; Assessments; Autism; Autism Spectrum Disorder; Classification; Cognition; Communication; Humans; Macaca mulatta; Male; Monkeys; Monkeys & apes; Motivation; Primates; Prosocial behavior; rhesus macaque; Social Behavior; Social classes; social communication; Social functioning; Social motivation; Stability analysis; threat behavior; Threats; Variation; social functioning; threat behavior; rhesus macaque; autism spectrum disorder; social communication; social motivation
• ISSN: 0275-2565; 1098-2345
• DOI: 10.1002/ajp.23442

Rhesus monkeys and humans are highly social primates, yet both species exhibit pronounced variation in social functioning, spanning a spectrum of sociality. Naturally occurring low sociality in rhesus monkeys may be a promising construct by which to model social impairments relevant to human autism spectrum disorder (ASD), particularly if low sociality is found to be stable across time and associated with diminished social motivation. Thus, to better characterize variation in sociality and social communication profiles, we performed quantitative social behavior assessments on N = 95 male rhesus macaques (Macaca mulatta) housed in large, outdoor groups. In Study 1, we determined the social classification of our subjects by rank‐ordering their total frequency of nonsocial behavior. Monkeys with the greatest frequency of nonsocial behavior were classified as low‐social (n = 20) and monkeys with the lowest frequency of nonsocial behavior were classified as high‐social (n = 21). To assess group differences in social communication profiles, in Study 2, we quantified the rates of transient social communication signals, and whether these social signals were initiated by or directed towards the focal subject. Finally, in Study 3, we assessed the within‐individual stability of sociality in a subset of monkeys (n = 11 low‐social, n = 11 high‐social) two years following our initial observations. Nonsocial behavior frequency significantly correlated across the two timepoints (Studies 1 and 3). Likewise, low‐social versus high‐social classification accurately predicted classification two years later. Low‐social monkeys initiated less prosocial behavior than high‐social monkeys, but groups did not differ in receipt of prosocial behavior, nor did they differ in threat behavior. These findings indicate that sociality is a stable, trait‐like characteristic and that low sociality is linked to diminished initiation of prosocial behavior in rhesus macaques. This evidence also suggests that low sociality may be a useful construct for gaining mechanistic insight into the social motivational deficits often observed in people with ASD.
Naturally low‐social (n = 20) and high‐social (n = 21) male rhesus monkeys (Macaca mulatta) differed in their social communication profiles as studied in large outdoor field corrals. Specifically, low‐social monkeys initiated significantly less prosocial behavior than high‐social monkeys but did not differ from high‐social monkeys in receipt of prosocial behavior. This motivated behavior effect was specific to the prosocial behavior domain, as low‐social and high‐social monkeys did not differ in threat behavior, either initiated or received. Data were square‐root transformed for analysis. LSM ± SEM is plotted.
HIGHLIGHTS
Quantitative social behavior assessments conducted over a 2‐year period demonstrate that sociality is a stable, trait‐like characteristic in rhesus macaques.
Naturally low‐social rhesus macaques exhibit diminished initiation of prosocial behavior compared to their high‐social peers, but no group differences were observed for receipt of prosocial behavior or threat behavior.
Naturally occurring low sociality in rhesus monkeys thus may be a useful construct for gaining mechanistic insight into the social motivational deficits often observed in people with autism spectrum disorder.