Our study provides insight into the genetic factors underpinning complex behaviors via comparative study of wild primates differing in social system. This research is among the first investigations of social behavior through population genomic scans for adaptive divergence in wild primate groups using an unparalleled sample set that spans decades. Our main conclusion, that a dopamine pathway underlies the social behavioral differences seen, offers comparative insight into the evolution of human behavioral and psychiatric phenotypes. We suggest that variation in impulsivity or boldness has played a major role in the evolution of socially complex species such as primates.

Abstract

In the endeavor to associate genetic variation with complex traits, closely related taxa are particularly fruitful for understanding the neurophysiological and genetic underpinnings of species-specific attributes. Similarity to humans has motivated research into nonhuman primate models, yet few studies of wild primates have investigated immediate causal factors of evolutionarily diverged social behaviors. Neurotransmitter differences have been invoked to explain the distinct behavioral suites of two baboon species in Awash, Ethiopia, which differ markedly in social behavior despite evolutionary propinquity. With this natural experiment, we test the hypothesis that genomic regions associated with monoamine neurotransmitters would be highly differentiated, and we identify a dopamine pathway as an outlier, highlighting the system as a potential cause of species-specific social behaviors. Dopamine levels and resultant variation in impulsivity were likely under differential selection in the species due to social system structure differences, with either brash or circumspect social behavior advantageous to secure mating opportunities depending on the social backdrop. Such comparative studies into the causes of the behavioral agendas that create and interact with social systems are of particular interest, and differences in temperament related to boldness and associated with dopamine variation likely played important roles in the evolution of all social, behaviorally complex animals, including baboons and humans.