Inventing monogamy: innovation and adaptation in the epigenome

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How do new behaviors evolve? Recent technical advances allow us to ask exactly which deoxyribonucleic acid (DNA) sequences underlie evolutionary innovations in gene expression, neural function, and complex behaviors. The ability of an organism to form a bond with another individual is a complex behavior, one that shapes the social behaviors exhibited by many species, including humans. In the current project, the investigators identify evolutionary adaptations that underlie social bonding in a well-studied species, the monogamous prairie vole. The investigators compare the subtle changes in DNA sequences that distinguish monogamous prairie voles from promiscuous relatives. They also ask whether these changes in DNA influence gene function in brain regions important for pair-bonding as well as brain regions important for spatial memory because space use is a major factor in animal mating systems. Lastly, the investigators ask whether natural selection has operated on these DNA sequences by examining patterns of DNA variation. The findings will help understand how changes in complex behavior can emerge from variation in DNA. To complete the studies, the investigators will recruit and train undergraduates from under-represented groups. Further, the investigators will develop and disseminate research tools needed to perform similar studies on a great variety of species, making it easier to do cutting-edge studies of genome function and behavior in any species. The answers obtained from this work will elucidate the relation between behavior and subtle genetic variations that contribute to diversity and disease.How is an existing genotype sculpted, locus by locus, to result in a new phenotype? The investigators use the genus Microtus as a model for understanding the epigenetic innovations that gave rise to social monogamy, building on an extensive body of work in social neuroscience, molecular genetics, and behavioral ecology. They examine the epigenome and its evolution in three vole species: the monogamous prairie vole, M. ochrogaster; the promiscuous meadow vole, M. pennsylvanicus; and a promiscuous outgroup, the California vole, M. californicus. Although many brain regions merit study, the investigators focus on four brain regions: reward structures (nucleus accumbens, ventral pallidum) and spatial memory structures (hippocampus, retrosplenial cortex). In the first aim, they use RNA-seq and ChIP-seq to identify species differences in gene regulation. In second aim, they use phylogenetic and population genetic methods to identify adaptations within the epigenome. The intersection of these two data sets will identify regulatory regions likely to be causally involved in pair-bond formation, and in mating system differences in spatial cognition. Finally, the investigators test whether the evolution of monogamy in this group relied predominantly on changes related to bonding, to cognition, or both. The identified DNA sequences can then be subject to manipulation in future studies.