A chromosomal inversion contributes to divergence in multiple traits between deer mouse ecotypes

Abstract

How locally adapted ecotypes are established and maintained within a species is a long-standing question in evolutionary biology. Using forest and prairie ecotypes of deer mice ( Peromyscus maniculatus ), we characterized the genetic basis of variation in two defining traits—tail length and coat color—and discovered a 41-megabase chromosomal inversion linked to both. The inversion frequency is 90% in the dark, long-tailed forest ecotype; decreases across a habitat transition; and is absent from the light, short-tailed prairie ecotype. We implicate divergent selection in maintaining the inversion at frequencies observed in the wild, despite high levels of gene flow, and explore fitness benefits that arise from suppressed recombination within the inversion. We uncover a key role for a large, previously uncharacterized inversion in the evolution and maintenance of classic mammalian ecotypes.

Chromosomal inversion polymorphisms shape the genomic landscape of deer mice

“…We took advantage of previous work on two populations, representing forest and prairie deer mouse ecotypes (populations c and e, Fig. 4a), which are well characterized and widespread 20 . Forest and prairie mice show many pronounced phenotypic differences (for example, coat colour, tail length, foot length) despite ongoing gene flow.…”

“…Forest and prairie mice show many pronounced phenotypic differences (for example, coat colour, tail length, foot length) despite ongoing gene flow. We previously identified an inversion on chromosome 15 (inv15.0) that contributes to phenotypic divergence between these ecotypes 20 . Returning to this system, we found that multiple newly identified inversions were also major contributors to differentiation between these populations.…”

“…Here, we perform an unbiased genome-wide scan for inversion polymorphisms in the deer mouse, Peromyscus maniculatus. The deer mouse is the most abundant and widespread mammal in North America: it has large effective population sizes 20,21 and a range spanning all major terrestrial habitats, including dense forests and open prairies 22 . Early cytogenetic work in deer mice identified at least 13 visible chromosomal rearrangements 23,24 .…”

Dynamic molecular evolution of a supergene with suppressed recombination in white-throated sparrows

“…Recent genome-scale studies have illuminated wide-ranging impacts of supergene evolution on complex phenotypes across diverse taxa (e.g. Schwander et al, 2014 ; Pearse et al, 2019 ; Hager et al, 2022 ; Joron et al, 2011 ; Kunte et al, 2014 ; Kess et al, 2019 ; Lundberg et al, 2017 ; Roberts et al, 2009 ; Sanchez-Donoso et al, 2022 ; Funk et al, 2021 ). Currently, the mechanisms by which functionally divergent supergene haplotypes evolve in the face of multiple evolutionary forces remain poorly understood, presenting a critical gap in knowledge.…”

The rate of inversion fixation in plant genomes is highly variable

“…For example, loci that are locally adaptive can benefit from inversions since they can be co-inherited as an adaptive multi-loci haplotype and protected from recombination with non-adaptive alleles (Kirkpatrick and Barton 2006). Numerous non-model systems have been observed to have inversions with adaptive significance: sunflower (Todesco et al 2020), monkeyflower (Lowry and Willis 2010), rainbow trout (Leitwein et al 2017), Atlantic cod (Barth et al 2017; Sodeland et al 2022), stickleback (Jones et al 2012), deer mice (Hager et al 2022; Harringmeyer and Hoekstra 2022).…”