LAUSR

The biological mechanisms that underpin primate social evolution remain poorly understood. Asian colobines display a range of social organizations, which makes them good models for investigating social evolution. By integrating ecological, geological, fossil, behavioral, and genomic analyses, we found that colobine primates that inhabit colder environments tend to live in larger, more complex groups. Specifically, glacial periods during the past 6 million years promoted the selection of genes involved in cold-related energy metabolism and neurohormonal regulation. More-efficient dopamine and oxytocin pathways developed in odd-nosed monkeys, which may have favored the prolongation of maternal care and lactation, increasing infant survival in cold environments. These adaptive changes appear to have strengthened interindividual affiliation, increased male-male tolerance, and facilitated the stepwise aggregation from independent one-male groups to large multilevel societies. Description INTRODUCTION Primates have evolved a diverse set of social systems, from solitary living to large multilevel societies. The traditional socioecological model explains this diversity as a response to changing environments, which shaped patterns of cooperation and competition for resources and predator defense. However, the socioecological model does not explain why sympatric species living in the same environment exhibit different social systems. There is a growing consensus that primate social organization shows a strong phylogenetic signal as a result of shared inheritance from a common ancestor and evolved stepwise along with species differentiation. This implies a genetic basis for the evolution of animal social systems. However, the genomic mechanisms that underlie the expression of primate social systems remain poorly understood. RATIONALE Asian colobines, a subfamily of Old World monkeys, are represented by seven genera and 55 species that are distributed from tropical rainforests to snow-covered mountains. They exhibit four distinct types of social organization and provide a good model for examining the mechanisms that drive social evolution from a common ancestral state to the diverse systems present today. By integrating new genomic data across all seven colobine genera with paleoenvironmental information, the fossil record, social organization characteristics, social behavioral characteristics, and ecological niche modeling, we constructed a socioecological-genomic framework to identify selective pressures that form the genetic basis for social evolution in Asian colobines. RESULTS To understand the evolutionary process of social systems in Asian colobines, we first reconstructed their phylogenetic relationships using whole-genome data. In contrast to the previous hypothesis of three major clades, our study reveals that Asian colobines split into two clades: the odd-nosed monkeys and the classical langurs. Our phylogenetic analyses detected a strong signal in colobine social evolution, suggesting that these social systems evolved in a stepwise manner, with ancestral one-male, multifemale groups fusing into semimultilevel societies characterized by fission-fusion and then merging into complex multilevel societies. Consistent with our ecological results indicating that extant colobine primates that inhabit colder environments tend to live in larger groups, we found that adaptations driven by ancient cold events, including the late Miocene cooling and Pleistocene glacial periods, played an important role in promoting these changes in social evolution. Furthermore, our genomic analyses revealed that these cold events promoted the selection of genes involved in energy metabolism and neurohormonal regulation. In particular, more-efficient dopamine and oxytocin pathways developed in odd-nosed monkeys, which might have resulted in the prolongation of maternal care and lactation, favoring infant survival in cold environments. These adaptive changes also appear to have strengthened interindividual affiliation, increased male-male tolerance, and facilitated the stepwise social aggregation from independent one-male, multifemale groups to large multilevel societies in Asian colobines. CONCLUSION Our results reveal a stepwise evolutionary scenario of social organization in Asian colobines. We show that ancient glacial events selected for neurohormonal regulation, including dopamine and oxytocin pathways that promoted aggregation from one-male, multifemale groups into large multilevel societies. Our study demonstrates a direct link between a genomically regulated adaptation and social evolution in primates and offers new insights into the mechanisms that underpin behavioral evolution across animal taxa. Adaptation for survival in cold climates facilitated evolution of social behavior in colobine monkeys. Cold environments promoted the social evolution of Asian colobines in a stepwise manner. Genomic changes in neurohormonal regulation, including in the dopamine and oxytocin pathways, improved social affiliation in odd-nosed monkeys and thus promoted social aggregations from independent one-male, multifemale groups into large multilevel societies. Ma, million years ago.