View Program - 2022 Population, Evolutionary, and Quantitative Genetics Conference

Chromosomal inversions are an important type of structural variation, with increasing evidence for their role in local adaptation across diverse species. However, since inversions can be challenging to detect, the prevalence and hence significance of inversions segregating within species remains largely unknown, especially in natural populations of mammals. Here, by combining population-genomic and long-read sequencing analyses in a single, widespread species of deer mouse (Peromyscus maniculatus), we identified 25 novel polymorphic inversions and explored their role in adaptation. Overall, these inversions are large, ranging in size from 1.5-43 Mb, and in total, affect 17% of the P. maniculatus genome. By localizing the inversion breakpoints, we found that genomic regions harboring breakpoints are enriched for long inverted repeats (0.5-50 kb), suggesting that these inversions likely arose via ectopic recombination. We then genotyped the inversions in 13 populations across the species range and found that the inversions are highly polymorphic, not only within the species, but also within populations, such that the inversions are frequently heterozygous. Because we found that the inversions cause near complete suppression of recombination in heterozygotes (genome average: 0.81 cM/Mb; heterozygous inversion: 0.01 cM/Mb), the inversions have a strong effect on recombination rates and patterns of linkage disequilibrium in natural populations. In addition, the inversions have accumulated significant levels of nucleotide divergence (0.2-0.9%) from the ancestral haplotypes, as a consequence of suppressed recombination. Finally, we found that the inversions substantially contribute to differentiation between locally adapted populations: for example, a closely-related pair of populations adapted to forest versus prairie habitats differed by >50% in their frequencies of 13 inversions despite ongoing gene flow. One inversion in particular plays a critical role in maintaining multiple adaptive trait differences between forest-prairie ecotypes, both by carrying adaptive mutations (for pigmentation and tail length) as well as enabling their co-inheritance through suppressed recombination. Together, we find that inversion polymorphisms have a significant impact on recombination, genome structure and genetic diversity in deer mice, and are possibly a key source of genetic variation facilitating local adaptation across this species’ widespread range.

Chromosomal inversions shape the genomic landscape of the deer mouse