Abstract

Transposable elements (TEs) and other repetitive DNA can accumulate in the absence of recombination, a process contributing to the degeneration of Y-chromosomes and other nonrecombining genome portions. A similar accumulation of repetitive DNA is expected for asexually reproducing species, given their entire genome is effectively nonrecombining. We tested this expectation by comparing the whole-genome TE loads of five asexual arthropod lineages and their sexual relatives, including asexual and sexual lineages of crustaceans (Daphnia water fleas), insects (Leptopilina wasps), and mites (Oribatida). Surprisingly, there was no evidence for increased TE load in genomes of asexual as compared to sexual lineages, neither for all classes of repetitive elements combined nor for specific TE families. Our study therefore suggests that nonrecombining genomes do not accumulate TEs like nonrecombining genomic regions of sexual lineages. Even if a slight but undetected increase of TEs were caused by asexual reproduction, it appears to be negligible compared to variance between species caused by processes unrelated to reproductive mode. It remains to be determined if molecular mechanisms underlying genome regulation in asexuals hamper TE activity. Alternatively, the differences in TE dynamics between nonrecombining genomes in asexual lineages versus nonrecombining genome portions in sexual species might stem from selection for benign TEs in asexual lineages because of the lack of genetic conflict between TEs and their hosts and/or because asexual lineages may only arise from sexual ancestors with particularly low TE loads.

Highlights

  • Genetic linkage in the absence of recombination couples the fates of different mutations and thereby decreases the efficacy of natural selection (Muller 1964; Hill and Robertson 1966; Nuzhdin and Petrov 2003)

  • An important consequence of the reduced efficacy of selection is the accumulation of deleterious mutations and repetitive DNA in the form of transposable elements (TEs), a process well documented for the nonrecombining Y sex chromosomes (Bachtrog 2013) and other nonrecombining genome portions (Lynch and Blanchard 1998; Schwander et al 2014; Leung et al 2015)

  • Different TE types are characterized by different mechanisms through which they spread within a genome, which is known to affect their population dynamics (Burt and Trivers 2006; Pritham 2009)

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Summary

Introduction

Genetic linkage in the absence of recombination couples the fates of different mutations and thereby decreases the efficacy of natural selection (Muller 1964; Hill and Robertson 1966; Nuzhdin and Petrov 2003). An important consequence of the reduced efficacy of selection is the accumulation of deleterious mutations and repetitive DNA in the form of transposable elements (TEs), a process well documented for the nonrecombining Y (and W) sex chromosomes (Bachtrog 2013) and other nonrecombining genome portions (Lynch and Blanchard 1998; Schwander et al 2014; Leung et al 2015). Similar dynamics are known from other nonrecombining chromosomes: Muller F elements in Drosophila are repeat enriched 5–10-fold relative to recombining genome portions, whereby repeats constitute up to 50% of these elements (Leung et al 2015). The rapid proliferation of TEs in the absence of recombination stems from their ability to self-replicate, via different mechanisms, to new positions in the genome, independently of the host’s cell cycle (Hickey 1982; Burt and Trivers 2006)

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