The evolution of selfing from outcrossing ancestors in Brassicaceae: What have we learned from variation at the S-locus?

Abstract

Evolutionary transitions between mating systems have occurred repetitively and independently in flowering plants. One of the most spectacular advances of the recent empirical literature in the field was the discovery of the underlying genetic machinery, which provides the opportunity to retrospectively document the scenario of the outcrossing to selfing transitions in a phylogenetic perspective. In this review, we explore the literature describing patterns of polymorphism and molecular evolution of the locus controlling self-incompatibility (S-locus) in selfing species of the Brassicaceae family in order to document the transition from outcrossing to selfing, a retrospective approach that we describe as the 'mating system genes approach'. The data point to strikingly contrasted scenarios of transition from outcrossing to selfing. We also perform original analyses of the fully sequenced genomes of four species showing self-compatibility, to compare the orthologous S-locus region with that of functional S-locus haplotypes. Phylogenetic analyses suggest that all species we investigated evolved independently towards loss of self-incompatibility, and in most cases almost intact sequences of either of the two S-locus genes suggest that these transitions occurred relatively recently. The S-locus region in Aethionema arabicum, representing the most basal lineage of Brassicaceae, showed unusual patterns so that our analysis could not determine whether self-incompatibility was lost secondarily, or evolved in the core Brassicaceae after the split with this basal lineage. Although the approach we detail can only be used when mating system genes have been identified in a clade, we suggest that its integration with phylogenetic and population genetic approaches should help determine the main routes of this predominant mating system shift in plants. © 2014 European Society For Evolutionary Biology.