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-locus genes. Our results confirm the presence of previously
reported homostyle-specific, loss-of-function mutations in the exons of
the S-locus gene CYPᵀ, while also revealing a previously
undetected structural rearrangement in CYPᵀ associated with the
shift to homostyly. Additionally, we discovered that the promoter region
of CYPᵀ in distylous and homostylous individuals is identical,
suggesting that down-regulation of CYPᵀ via mutations in its
promoter region is not a cause of shift to homostyly. Furthermore, we
found that hemizygosity leads to reduced genetic diversity and less
efficient purifying selection in S-locus genes compared to genes outside
the S-locus, and that the shift to homostyly further lowers genetic
diversity, as expected for mating-system shifts. 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 (diploid) copies of the S-locus might reduce
homostyle viability.