Deleterious mutation accumulation and the long-term fate of chromosomal inversions.

Emma L Berdan,Alexandre Blanckaert,Claudia Bank,Roger K Butlin,Alex Buerkle

doi:10.1371/journal.pgen.1009411

Abstract

Chromosomal inversions contribute widely to adaptation and speciation, yet they present a unique evolutionary puzzle as both their allelic content and frequency evolve in a feedback loop. In this simulation study, we quantified the role of the allelic content in determining the long-term fate of the inversion. Recessive deleterious mutations accumulated on both arrangements with most of them being private to a given arrangement. This led to increasing overdominance, allowing for the maintenance of the inversion polymorphism and generating strong non-adaptive divergence between arrangements. The accumulation of mutations was mitigated by gene conversion but nevertheless led to the fitness decline of at least one homokaryotype under all considered conditions. Surprisingly, this fitness degradation could be permanently halted by the branching of an arrangement into multiple highly divergent haplotypes. Our results highlight the dynamic features of inversions by showing how the non-adaptive evolution of allelic content can play a major role in the fate of the inversion.

Highlights

Chromosomal inversions are large-scale structural mutations that may encompass millions of nucleotides and cause them to segregate together as a single unit due to repressed recombination
A chromosomal inversion is a segment of the chromosome that is flipped relative to the normal orientation
Such structural mutations may facilitate evolutionary processes such as adaptation and speciation, because reduced recombination in inverted regions allows beneficial combinations of alleles to behave as a single unit

Summary

Introduction

Chromosomal inversions are large-scale structural mutations that may encompass millions of nucleotides and cause them to segregate together as a single unit due to repressed recombination. Inversions are dynamic and behave in qualitatively different ways from single-nucleotide polymorphisms (SNPs), since both their allelic content and their frequency can change over time. Incorporating this concept better into evolutionary theory will improve our ability to explain and predict the evolution of inversions in natural populations [8,9,10,11]. A key feature of inversions, and large structural variants in general, is that selection acts at multiple scales. The allelic content of the arrangements is under selection, which generates indirect selection at the level of the inversion through linkage disequilibrium. As a consequence of this indirect component, selection on inversions may be overdominant due to the presence of recessive deleterious alleles, unique to each arrangement [12]

Methods

Results

Discussion

Conclusion