Abstract

Recombination suppression in sex chromosomes and mating type loci can lead to degeneration as a result of reduced selection efficacy and Muller's ratchet effects. However, genetic exchange in the form of noncrossover gene conversions may still take place within crossover-suppressed regions. Recent work has found evidence that gene conversion may explain the low degrees of allelic differentiation in the dimorphic mating-type locus (MT) of the isogamous alga Chlamydomonas reinhardtii. However, no one has tested whether gene conversion is sufficient to avoid the degeneration of functional sequence within MT. Here, we calculate degree of linkage disequilibrium (LD) across MT as a proxy for recombination rate and investigate its relationship to patterns of population genetic variation and the efficacy of selection in the region. We find that degree of LD predicts selection efficacy across MT, and that purifying selection is stronger in shared genes than in MT-limited genes to the point of being equivalent to that of autosomal genes. We argue that while crossover suppression is needed in the mating-type loci of many isogamous systems, these loci are less likely to experience selection to differentiate further. Thus, recombination can act in these regions and prevent degeneration caused by Hill-Robertson effects.

Highlights

  • Sexual reproduction is widespread across both unicellular and multicellular eukaryotes primarily to shuffle genetic material between compatible mates

  • We find that levels of linkage disequilibrium (LD) predict selection efficacy across mating type locus (MT), and that purifying selection is stronger in shared genes than MT -limited genes to the point of being equivalent to that of autosomal genes

  • We argue that isogamous systems without secondary sexual characteristics exhibit reduced selective pressure to differentiate sex chromosomes, and that recombination via gene conversion plays an important role in both reducing differentiation and preventing degeneration of crossover suppressed mating type loci

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Summary

Introduction

Sexual reproduction is widespread across both unicellular and multicellular eukaryotes primarily to shuffle genetic material between compatible mates. Despite the role of sex in promoting recombination and improving the efficacy of selection in the genome, evidence and theory suggest that sex or mating-type determining regions themselves are often recombination-suppressed (Bachtrog et al, 2011, Abbott et al, 2017) Recombination suppression in these regions is thought to be a result of selection to preserve linkage between sex-determining loci that and sexually antagonistic alleles (Charlesworth, 1996; but see Branco et al 2017 and Ponnikas et al 2018). Recombination suppression can result in reduced efficacy of selection against structural mutations, including transposable element insertions, gene loss, and chromosomal inversions Such structural mutations, chromosomal inversions, drive further reductions in recombination by disrupting pairing of homologous chromosomes in meiosis and can expand the boundaries of sex- or mating type-determining regions (Lahn and Page, 1999, Kirkpatrick, 2010, Wright et al, 2016)

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