Consequences of Asexuality in Natural Populations: Insights from Stick Insects.

Jens Bast,Kirsten M Jalvingh,Patrick Tran Van,Tanja Schwander,Emeric Figuet,Darren J Parker,Kamil S Jaron,Nicolas Galtier,Zoé Dumas,Alexander Brandt

doi:10.1093/molbev/msy058

Abstract

Recombination is a fundamental process with significant impacts on genome evolution. Predicted consequences of the loss of recombination include a reduced effectiveness of selection, changes in the amount of neutral polymorphisms segregating in populations, and an arrest of GC-biased gene conversion. Although these consequences are empirically well documented for nonrecombining genome portions, it remains largely unknown if they extend to the whole genome scale in asexual organisms. We identify the consequences of asexuality using de novo transcriptomes of five independently derived, obligately asexual lineages of stick insects, and their sexual sister-species. We find strong evidence for higher rates of deleterious mutation accumulation, lower levels of segregating polymorphisms and arrested GC-biased gene conversion in asexuals as compared with sexuals. Taken together, our study conclusively shows that predicted consequences of genome evolution under asexuality can indeed be found in natural populations.

Highlights

The absence of recombination is a common feature in eukaryotic genomes and it can span over a few hundred bases, entire chromosomes and, as in the case of asexual organisms, over complete genomes
Open reading frames (ORFs) were identified in 7,329–10,436 of the transcripts, and these ORFs were used to determine orthologs shared between the two species of a pair as well as orthologs shared across all ten species (3,010 orthologs; see Materials and Methods for details, supplementary data 1 and supplementary tables 1 and 2, Supplementary Material online)
The absence of recombination is predicted to be associated with reduced GC content, reduced effectiveness of selection on short and long evolutionary timescales, and affect levels of neutral genetic variation segregating in populations (Muller 1964; Hill and Robertson 1966; Felsenstein 1974; Marais 2003; Keightley and Otto 2006)

Summary

Introduction

The absence of recombination is a common feature in eukaryotic genomes and it can span over a few hundred bases, entire chromosomes and, as in the case of asexual organisms, over complete genomes. Theory predicts two major consequences for selection on genome portions and complete genomes that lack recombination. Selection is less effective, because physical linkage among loci hinders selection’s ability to act upon loci independently (Muller 1964; Hill and Robertson 1966; Felsenstein 1974; Keightley and Otto 2006). This should translate into decreased rates of adaptation and increased accumulation of mildly deleterious mutations, including point mutations and repetitive elements. Mitotic gene conversion and selection at linked sites (background selection) lead to a loss of heterozygosity and diversity in the absence of recombination, which can translate to lower polymorphism in recombining than nonrecombining genome portions (Hill and Robertson 1966; Charlesworth et al 1993)

Methods

Results

Conclusion