Abstract

Asexual populations experience weaker responses to natural selection, which causes deleterious mutations to accumulate over time. Additionally, stochastic loss of individuals free of deleterious mutations can lead to an irreversible increase in mutational load in asexuals (the “click” in Muller’s Ratchet). Here we report on the genomic divergence and distribution of mutations across eight sympatric pairs of sexual and apomictic (asexual) Boechera (Brassicaceae) genotypes. We show that apomicts harbor a greater number of derived mutations than sympatric sexual genotypes. Furthermore, in phylogenetically constrained sites that are subject to contemporary purifying selection, the ancestral, conserved allele is more likely to be retained in sexuals than apomicts. These results indicate that apomictic lineages accumulate mutations at otherwise conserved sites more often than sexuals, and support the conclusion that deleterious mutation accumulation can be a powerful force in the evolution of asexual higher plants.

Highlights

  • Within finite populations, sexual recombination can improve the probability of fixing beneficial mutations (“Hill-Robertson” effect) [1], while asexual populations are more likely to accumulate deleterious mutations [2,3,4,5]

  • Since asexual populations do not undergo recombination, ancestral adaptive genotypes cannot be recovered once deleterious alleles reach fixation, a process known as “Muller’s Ratchet” [6,7,8]. These processes are thought to increase the rate of deleterious mutation accumulation in asexual lineages [9], which may favor sexual reproduction

  • Plants that reproduce asexually via seed are commonly hybrid and/or polyploid [11,12,13], which may buffer the effects of accelerated deleterious mutation accumulation

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Summary

Introduction

Sexual recombination can improve the probability of fixing beneficial mutations (“Hill-Robertson” effect) [1], while asexual populations are more likely to accumulate deleterious mutations [2,3,4,5]. Since asexual populations do not undergo recombination, ancestral adaptive genotypes cannot be recovered once deleterious alleles reach fixation, a process known as “Muller’s Ratchet” [6,7,8]. Combined, these processes are thought to increase the rate of deleterious mutation accumulation in asexual lineages [9], which may favor sexual reproduction. Plants that reproduce asexually via seed (hereon “apomixis”) are commonly hybrid and/or polyploid [11,12,13], which may buffer the effects of accelerated deleterious mutation accumulation. The genus Boechera (Brassicaceae) offers an exceptional case among plants, where apomictic diploids are phylogenetically dispersed across as many as 30% of the >100 species [14,15,16,17]

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