A chromosomal inversion drives evolution of multiple adaptive traits in deer mice

Abstract

A long-standing question in evolutionary biology is how differences in multiple traits can evolve quickly and be maintained together during local adaptation. Using forest and prairie ecotypes in deer mice, which differ in both tail length and coat color, we discovered a 41 Mb chromosomal inversion that is strongly linked to variation in both traits. The inversion maintains highly divergent loci in strong linkage disequilibrium and likely originated ~170 kya, long before the forest-prairie divergence ~10 kya. Consistent with a role in local adaptation, inversion frequency is associated with phenotype and habitat across both a local transect and the species range. Still, although eastern and western forest subspecies share similar phenotypes, the inversion is absent in eastern North America. This work highlights the significance of inversion polymorphisms for the establishment and maintenance of multiple locally adaptive traits in mammals, and demonstrates that, even within a species, parallel phenotypes may evolve through nonparallel genetic mechanisms.

Broad geographic sampling reveals the shared basis and environmental correlates of seasonal adaptation in Drosophila

“…In these regions the seasonal signal is weaker, with a 2.5% enrichment of seasonal SNPs (p perm = 0.31). These data confirm that inversions may play a role in the adaptive response to seasonally variable environments, similar to that of structural variants or large haplotype blocks in other systems (Hager et al, 2021;Jones et al, 2012;Samuk et al, 2017;Tuttle et al, 2016).…”

Comparative linkage mapping uncovers recombination suppression across massive chromosomal inversions associated with local adaptation in Atlantic silversides

“…Clinal patterns of polymorphic inversions also underlie locally adapted ecotypes of a coastal marine snail ( Littorina saxatilis ; Faria, Chaube, et al, 2019) and have played an important role in repeated evolution of marine and freshwater sticklebacks ( Gasterosteus aculeatus ; Jones et al, 2012; Roesti et al, 2015). While many examples of inversions associated with local adaptations come from aquatic systems where there is typically high gene flow counteracting adaptive divergence among populations, there is also evidence of chromosomal rearrangements facilitating adaptation in terrestrial environments (e.g., Christmas et al, 2019; Hager et al, 2021; Todesco et al, 2020). Despite a growing appreciation for the effects of recombination on the dynamics of selection, the genomic features affecting the recombination landscape are still poorly understood in many systems because most studies have historically been limited to inbred lines of cultivated or model species (Stapley et al, 2017).…”

Integrating top-down and bottom-up approaches to understand the genetic architecture of speciation across a monkeyflower hybrid zone

“…For example, in another pair of Mimulus species, M. cardinalis and M. lewisii , large-effect QTL for multiple traits associated with pollinator isolation and hybrid sterility occur in a few genomic regions thought to harbor chromosomal inversions [4, 60]. In sunflowers ( Helianthus ), multiple traits are associated with local adaptation to dune and non-dune habitats and map to a small number of large, non-recombining haplotypes containing structural variants [61] (see [62–64] for other examples).…”