Abstract

The genetic breakdown of self-incompatibility (SI) and subsequent mating system shifts to inbreeding has intrigued evolutionary geneticists for decades. Most of our knowledge is derived from interspecific comparisons between inbreeding species and their outcrossing relatives, where inferences may be confounded by secondary mutations that arose after the initial loss of SI. Here, we study an intraspecific breakdown of SI and its consequences in North American Arabidopsis lyrata to test whether: (1) particular S-locus haplotypes are associated with the loss of SI and/or the shift to inbreeding; (2) a population bottleneck may have played a role in driving the transition to inbreeding; and (3) the mutation(s) underlying the loss of SI are likely to have occurred at the S-locus. Combining multiple approaches for genotyping, we found that outcrossing populations on average harbour 5 to 9 S-locus receptor kinase (SRK) alleles, but only two, S1 and S19, are shared by most inbreeding populations. Self-compatibility (SC) behaved genetically as a recessive trait, as expected from a loss-of-function mutation. Bulked segregant analysis in SC × SI F2 individuals using deep sequencing confirmed that all SC plants were S1 homozygotes but not all S1 homozygotes were SC. This was also revealed in population surveys, where only a few S1 homozygotes were SC. Together with crossing data, this suggests that there is a recessive factor that causes SC that is physically unlinked to the S-locus. Overall, our results emphasise the value of combining classical genetics with advanced sequencing approaches to resolve long outstanding questions in evolutionary biology.

Highlights

  • Uncovering the mechanisms regulating genetically controlled selfincompatibility (SI) systems in plants and fungi has been of sustained interest to the Genetics Society research community, with articles since the inception of Heredity

  • Based on S-locus receptor kinase (SRK) and its flanking genes, we conclude that two S-locus haplotypes are associated with this transition across multiple genetic backgrounds but that these are found in SI individuals from outcrossing populations, potentially reflecting the very young age of the loss of SI

  • Complete SRK genotypes were not resolved for the crosses, SC individuals were only found in cases where the SI parent had S1 (MAN18b, MAN22f but not MAN17f; Supplementary Figure S4)

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Summary

Introduction

Uncovering the mechanisms regulating genetically controlled selfincompatibility (SI) systems in plants and fungi has been of sustained interest to the Genetics Society research community, with articles since the inception of Heredity (see, for example, Lewis, 1947; Bateman, 1952). It has proven difficult to explain how these recognition systems that require paired specificity of male and female components evolve and are maintained (Charlesworth, 1988, 1995). A shift from outcrossing to inbreeding is one of the most frequent evolutionary transitions in plants (reviewed in Igic et al, 2008). What causes breakdown of genetically controlled SI systems and how inbreeding lineages can evolve in the face of inbreeding depression remains poorly understood (reviewed by Vekemans et al, 2014). The rapid technological advances of the past two decades offer new possibilities to address the possible drivers and genetic bases of these transitions

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