Repeated evolution of self-compatibility for reproductive assurance

Bart P S Nieuwenhuis,Pernilla Bjerling,Josefine Stångberg,Jochen B W Wolf,Sergio Tusso,Simone Immler

doi:10.1038/s41467-018-04054-6

Abstract

Sexual reproduction in eukaryotes requires the fusion of two compatible gametes of opposite sexes or mating types. To meet the challenge of finding a mating partner with compatible gametes, evolutionary mechanisms such as hermaphroditism and self-fertilization have repeatedly evolved. Here, by combining the insights from comparative genomics, computer simulations and experimental evolution in fission yeast, we shed light on the conditions promoting separate mating types or self-compatibility by mating-type switching. Analogous to multiple independent transitions between switchers and non-switchers in natural populations mediated by structural genomic changes, novel switching genotypes readily evolved under selection in the experimental populations. Detailed fitness measurements accompanied by computer simulations show the benefits and costs of switching during sexual and asexual reproduction, governing the occurrence of both strategies in nature. Our findings illuminate the trade-off between the benefits of reproductive assurance and its fitness costs under benign conditions facilitating the evolution of self-compatibility.

Highlights

Sexual reproduction in eukaryotes requires the fusion of two compatible gametes of opposite sexes or mating types
The mechanisms of mate compatibility are strikingly diverse across taxa and often involve sophisticated genomic structures ranging from sex chromosomes to highly complex mating types[1,2,3,4]
Analogous to the loss of self-incompatibility in angiosperms, or the evolution of hermaphroditism in animals and plants[9,14], many fungal species evolved the ability to reproduce without the need of another individual, a state known as homothallism[15,16]

Summary

Introduction

Sexual reproduction in eukaryotes requires the fusion of two compatible gametes of opposite sexes or mating types. A specific form of homothallism is mating-type switching, which evolved multiple times independently in both single-celled (i.e. yeasts) and multicellular fungi[18,22,23]. Mating-type switching is a mechanism at the genomic level occurring during mitotic asexual reproduction, which renders the resulting daughter cells sexually compatible with each other. The first hypothesis assumes that dispersal occurs by a single spore, which most often will be alone in the local patch and requires intra-clonal mating to complete the sexual phase of the life cycle[22,27] The latter suggests that when asexual reproduction continues for many generations with repeated bottlenecks or in small populations, the drift will skew the mating-type ratio, which can select for switching to restore this ratio[30]. Repeated bottlenecks of asexually reproducing populations are probably not common, favouring the lonely spore hypothesis[22]

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Results

Conclusion