A large chromosomal inversion shapes gene expression in seaweed flies (Coelopa frigida).

Emma L Berdan,Henrik Pavia,Kerstin Johannesson,Claire Mérot,Roger K Butlin,Maren Wellenreuther

doi:10.1002/evl3.260

Abstract

Inversions often underlie complex adaptive traits, but the genic targets inside them are largely unknown. Gene expression profiling provides a powerful way to link inversions with their phenotypic consequences. We examined the effects of the Cf‐Inv(1) inversion in the seaweed fly Coelopa frigida on gene expression variation across sexes and life stages. Our analyses revealed that Cf‐Inv(1) shapes global expression patterns, most likely via linked variation, but the extent of this effect is variable, with much stronger effects in adults than larvae. Furthermore, within adults, both common as well as sex‐specific patterns were found. The vast majority of these differentially expressed genes mapped to Cf‐Inv(1). However, genes that were differentially expressed in a single context (i.e., in males, females, or larvae) were more likely to be located outside of Cf‐Inv(1). By combining our findings with genomic scans for environmentally associated SNPs, we were able to pinpoint candidate variants in the inversion that may underlie mechanistic pathways that determine phenotypes. Together the results of this study, combined with previous findings, support the notion that the polymorphic Cf‐Inv(1) inversion in this species is a major factor shaping both coding and regulatory variation resulting in highly complex adaptive effects.

Highlights

Chromosomal inversions, pieces of the chromosome that have been flipped 180°, are structural variants that may encompass hundreds of genes but segregate together as a single unit due to suppressed recombination
Transcriptomic analysis offers a way to address the links between individual loci and the phenotypic effects of an inversion by uncovering functionally important variation in a way that is not hindered by linkage disequilibrium in natural populations or recombination suppression in controlled crosses. This is because (1) the phenotypic effects of inversions might be underlain in part by changes in gene expression, and (2) overlap between differentially expressed genes and outlier SNPs facilitates the identification of candidate genes (Renaut et al 2011; Kozak et al 2014; Pardo-Diaz et al 2015)
Abundant evidence indicates that chromosomal inversions are key genomic factors in eco-evolutionary processes because of their multifarious impacts on genome structure, recombination, and regulation (Hoffmann and Rieseberg 2008; Wellenreuther and Bernatchez 2018)

Summary

Introduction

Chromosomal inversions, pieces of the chromosome that have been flipped 180°, are structural variants that may encompass hundreds of genes but segregate together as a single unit due to suppressed recombination. The reduced recombination and effective population size within the inverted region facilitate the accumulation of neutral and deleterious variation (Berdan et al 2021), increasing divergence between the arrangements and increasing the likelihood of detecting phenotype or environment associations with noncausative loci Larger inversions, such as the lnv4m inversion in Zea mays, may contain hundreds of genes that affect a wide variety of phenotypes that vary in their selective pressures (Crow et al 2020). This is because (1) the phenotypic effects of inversions might be underlain in part by changes in gene expression, and (2) overlap between differentially expressed genes (from transcriptomic studies) and outlier SNPs (from genomic studies, i.e., loci associated with adaptive traits or ecological factors) facilitates the identification of candidate genes (Renaut et al 2011; Kozak et al 2014; Pardo-Diaz et al 2015)

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Results

Conclusion