Invasion and defense of the basic social unit in a nonhuman primate society leads to sexual differences in the gut microbiome

Multilevel society is one of the most complex social systems in natural ecosystems and is a typical feature among some primates.Given the potential connection between social behavior and gut microbiome composition,the multilevel social system could affect the primate gut microbiome.Here,based on long-term observation(e.g.social unit dynamics,transfer,and behavior),we investigated this potential integrating 16S rRNA gene amplicon sequencing and behavior data in Yunnan snub-nosed monkeys(Rhinopithecus bieti),which possess a multilevel social group based on one male units(OMUs,each unit with several breeding females and their offspring)and all-male unit(AMU,several bachelor males residing together).We found that the mean unweighted Unifrac distance between adult males from different OMUs was significantly lower than that between adult females from different OMUs(paired Wilcoxon test,P=0.007).There was no significant difference in the mean unweighted Unifrac distance between females within the same OMU or between females from different OMUs.These findings indicated the potential connection between the defense and invasion of social units and the gut microbiome community in wild Yunnan snub-nosed monkeys.We speculated that the resident males of OMUs displaying a significantly higher similarity in the gut microbial community than that of adult females in separate OMUs might be associated with the sexual differences in their interactions and from previously having cohabitated together in the AMU.Therefore,this study suggested that multilevel societies might have an effect on the gut microbial community in this wild nonhuman primate species.