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

PLoS Genet. 2021 Mar 4;17(3):e1009411. doi: 10.1371/journal.pgen.1009411. eCollection 2021 Mar.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Chromosome Inversion*
  • Evolution, Molecular
  • Gene Conversion
  • Gene Rearrangement
  • Haplotypes
  • Models, Genetic
  • Mutation*

Grants and funding

E.L.B. was supported by a Marie Skłodowska-Curie fellowship 704920 – ADAPTIVE INVERSIONS from the European Commission (https://ec.europa.eu). R.K.B. was supported by the NERC Grants NE/P001610/1 and NE/P012272/1 (https://nerc.ukri.org/) and by ERC Advanced Grant 693030 - BARRIERS from the European Research Council (https://erc.europa.eu/). C.B. is grateful for support by EMBO Installation Grant IG4152 (https://www.embo.org/). A.B. and C.B. were supported by ERC Starting Grant 804569 - FIT2GO from the European Research Council (https://erc.europa.eu/). This work was supported by Fundação Calouste Gulbenkian (https://gulbenkian.pt/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.