Genomic analyses elucidate S -locus evolution in response to intra-specific losses of distyly in Primula vulgaris .

Distyly, a floral dimorphism that promotes outcrossing, is controlled by a hemizygous genomic region known as the S -locus. Disruptions of genes within the S -locus are responsible for the loss of distyly and the emergence of homostyly, a floral monomorphism that favors selfing. Using whole-genome resequencing data of distylous and homostylous individuals from populations of Primula vulgaris and leveraging high-quality reference genomes of Primula we tested, for the first time, predictions about the evolutionary consequences of transitions to selfing on S -genes. Our results reveal a previously undetected structural rearrangement in CYPᵀ associated with the shift to homostyly and confirm previously reported, homostyle-specific, loss-of-function mutations in the exons of the S -gene CYPᵀ . We also discovered that the promoter and intronic regions of CYPᵀ in distylous and homostylous individuals are conserved, suggesting that down-regulation of CYPᵀ via mutations in its promoter and intronic regions is not a cause of the shift to homostyly. Furthermore, we found that hemizygosity is associated with reduced genetic diversity in S -genes compared with their paralogs outside the S -locus. Additionally, the shift to homostyly lowers genetic diversity in both the S -genes and their paralogs, as expected in primarily selfing plants. Finally, we tested, for the first time, long-standing theoretical models of changes in S -locus genotypes during early stages of the transition to homostyly, supporting the assumption that two copies of the S -locus might reduce homostyle fitness.