Evolution of the olfactory genome and its consequences for the social behavior of wild mice

Social behaviors are an essential component of animal’s life, yet the mechanisms underlying their evolution remain largely unknown, especially in mammals. The transition from promiscuity to monogamy represents an exciting opportunity to deepen our understanding of social behavior as it comprises multiple facets such as pair bonding, biparental care, and female-female aggression. Wild mice -specifically the deer mouse Peromyscus maniculatus and its sister species the oldf ield mouse P. polionotus- have become a model for linking genes to behavior. As with most mammals, P. maniculatus is highly promiscuous, whereas P. polionotus provides a rare example of both social and genetic monogamy. To further integrate behavioral and genomic information, we generated high quality reference genomes for these two species and combine comparative-genomic analyses with RNA sequencing to identify the DNA changes that contribute to behavioral evolution. Here, we focus on variation in the olfactory system, as changes affecting the sense of smell are known to lead marked modifications of mammalian behavior. First, genome-wide scans show that a significant portion of Fst outlier regions contain chemosensory genes, consistent with olfaction being an important driver of behavioral divergence. Second, our phylogenetic reconstructions of olfactory receptor genes indicate that several receptor clades show Peromyscus-specific expansion or contraction, revealing the extremely dynamic evolutionary history of these gene families and deviation from a random birth-death model. Finally, these mice show a high degree of differential transcriptome regulation in the olfactory sensory organs. By contrast, the olfactory transcriptomes differ only minimally between males and females in both species, suggesting that the pronounced sexual dimorphism observed in olfactorymediated behaviors - including parental behavior - is not driven by alteration at the periphery but rather has its origin in divergence at higher processing centers. Taken together, this study provides insights into the evolution of the mammalian olfactory system, and differences in the olfactory repertoires likely mediate the divergent social behaviors of these two species of deer mice.