Effective purifying selection in ancient asexual oribatid mites

Alexander Brandt,Tanja Schwander,Julien Glanz,Stefan Scheu,Ina Schaefer,Mark Maraun,Jens Bast

doi:10.1038/s41467-017-01002-8

Alexander Brandt, Tanja Schwander + Show 5 more

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https://doi.org/10.1038/s41467-017-01002-8

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Abstract

Sex is beneficial in the long term because it can prevent mutational meltdown through increased effectiveness of selection. This idea is supported by empirical evidence of deleterious mutation accumulation in species with a recent transition to asexuality. Here, we study the effectiveness of purifying selection in oribatid mites which have lost sex millions of years ago and diversified into different families and species while reproducing asexually. We compare the accumulation of deleterious nonsynonymous and synonymous mutations between three asexual and three sexual lineages using transcriptome data. Contrasting studies of young asexual lineages, we find evidence for strong purifying selection that is more effective in asexual as compared to sexual oribatid mite lineages. Our results suggest that large populations likely sustain effective purifying selection and facilitate the escape of mutational meltdown in the absence of sex. Thus, sex per se is not a prerequisite for the long-term persistence of animal lineages.

Highlights

Sex is beneficial in the long term because it can prevent mutational meltdown through increased effectiveness of selection
Given the long divergence time between the six species used for sequencing of transcriptomes (>200 million years35), detectable orthologs shared among the six species are expected to be under strong purifying selection
In contrast to this established consensus, our study showed no evidence for accumulation of deleterious nonsynonymous and synonymous point mutations in oribatid mite lineages that survived without sex for several million years

Summary

Introduction

Sex is beneficial in the long term because it can prevent mutational meltdown through increased effectiveness of selection. Theoretical predictions and empirical evidence for reduced purifying selection in asexual eukaryotes have led to the established consensus that sex and recombination are beneficial for the long-term persistence of lineages This benefit derives from the ability of sexual reproduction to decouple linked loci with different fitness effects generated by genetic drift, which increases the effectiveness of purifying selection to purge mildly deleterious mutations and reduces Hill–Robertson effects[7,8,9,10]. Oribatid mites lost sex multiple times independently, several million years ago, followed by extensive radiation of parthenogenetic clades as indicated by their phylogenetic distribution and high inter- and intraspecific molecular divergence[28,29,30,31,32] This speciose, largely soil-living animal group (~10,000 species20) is well suited for comparative investigations of genomic consequences under longterm asexuality.

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