The Evolutionary Significance of Chromosomal Inversions in Deer Mice

Abstract

Understanding the genomic basis of organismal adaptation remains a central goal of evolutionary biology. Chromosomal inversions – large segments of DNA in reverse orientation – can be major players in natural diversity because a single inversion can influence thousands to millions of base-pairs and dramatically change patterns of recombination. Because inversions are a challenging form of mutation to detect, there is limited knowledge on the prevalence of inversions and their role in evolution. Here, I harness recent advancements in evolutionary genomics to investigate inversions in the deer mouse (Peromyscus maniculatus), a wild mouse species adapted to diverse habitats across North America. In chapter 1, I performed a genome-wide scan for inversions, and identified 21 large inversion polymorphisms within the species that together span over 15% of the deer mouse genome. I found that the inversions have profound effects on recombination and genetic diversity, and multiple inversions contribute to local adaptation. In chapter 2, I investigated the genetic basis of deer mouse adaptation to forested habitats. I discovered a 40-megabase inversion that is strongly associated with two forest-adaptive traits, coat color and tail length. I demonstrated how this inversion leads to the co-inheritance of dark coats and long tails through suppressing recombination in heterozygotes, and helps facilitate local adaptation to forests. In chapter 3, I studied how this inversion evolved into a supergene linking multiple adaptive traits. I uncovered the specific mechanisms by which the inversion affects coat color and tail length, and I identified candidate genes within the inversion driving these phenotypic effects. I further discovered that the inversion became a supergene over time, through the accumulation of adaptive loci. Together, these studies highlight the abundance of inversion polymorphisms in a mammalian species and demonstrate the important role of inversions in driving evolutionary change.