A chromosomal inversion accumulates adaptive and barrier loci in a cold-adapted insect species

Chromosomal inversions can play a crucial role in population adaptation and divergence by reducing gene flow and preserving adaptive allelic combinations between populations with different arrangements. However, demonstrating this empirically is challenging due to numerous interacting processes with similar genomic signatures affecting inversion evolution. In this study, we characterized a large (9.5Mb) polymorphic inversion in the cold-adapted and widely distributed species, Drosophila montana, using long- and short-read sequencing across several populations. The origin of this inversion predates the divergence of North American (NA) and Fennoscandian (North European) populations, suggesting it emerged in the ancestral D. montana population in the Rocky Mountains of NA. Despite the species expansion across the northern hemisphere, this inversion has remained exclusive to the Rocky Mountains populations, where it is fixed in the southernmost high-elevation population and appears at lower frequencies in the more northern and lower-elevation populations. By independently mapping SNPs linked to climate adaptation and barriers to gene flow (barrier loci; identified through reduced migration rates), we found enrichment of both within the inversion, with barrier and adaptive regions partially overlapping. However, the inversion was not enriched for SNPs related to cold tolerance. These findings suggest that inversions may maintain associations between multiple adaptive and barrier loci, effectively coupling them, and that locally adaptive regions may act as barriers to gene flow. Our study provides empirical evidence that inversions can contribute to population adaptation and divergence by reducing gene flow, maintaining adaptive allelic combinations, and facilitating the coupling of different barriers to gene flow. SignificanceChromosomal inversions, genomic rearrangements with reversed gene order, are important drivers of population adaptation and divergence, but demonstrating this empirically is challenging due to complex interacting processes that produce similar genomic signatures. We characterized and analysed a large polymorphic inversion in Drosophila montana, a cold-adapted and widely distributed insect, using whole-genome sequencing data, phenotypic experiments, and recent methodological developments. This inversion is found only in mountain populations and is enriched with SNPs potentially associated with climate adaptation, as well as regions that act as barriers to gene flow, with these regions partially overlapping. These results suggest that adaptive loci can act as barriers to gene flow and that inversions help maintain adaptive allelic combinations and associations between multiple barrier loci, thereby contributing to population adaptation and divergence.