Different molecular changes underlie the same phenotypic transition: Origins and consequences of independent shifts to homostyly within species

The repeated transition from outcrossing to selfing is a key topic in
evolutionary biology. However, the molecular basis of such shifts has been
rarely examined due to lack of knowledge of the genes controlling these
transitions. A classic example of mating system transition is the repeated
shift from heterostyly to homostyly. Occurring in 28 angiosperm families,
heterostyly is characterized by the reciprocal position of male and female
sexual organs in two (or three) distinct, usually self-incompatible floral
morphs. Conversely, homostyly is characterized by a single,
self-compatible floral morph with reduced separation of male and female
organs, facilitating selfing. Here, we investigate the origins of
homostyly in Primula vulgaris and its microevolutionary consequences by
integrating surveys of the frequency of homostyles in natural populations,
DNA sequence analyses of the gene controlling the position of female
sexual organs (CYPᵀ), and microsatellite genotyping of both progeny arrays
and natural populations characterized by varying frequencies of
homostyles. As expected, we found that homostyles displace short-styled
individuals, but long-style morphs are maintained at low frequencies
within populations. We also demonstrated that homostyles repeatedly
evolved from short-styled individuals in association with different types
of loss-of-function mutations in CYPᵀ. Additionally, homostyly triggers a
shift to selfing, promoting increased inbreeding within and genetic
differentiation among populations. Our results elucidate the causes and
consequences of repeated transitions to homostyly within species, and the
putative mechanisms precluding its fixation in P. vulgaris. This study
represents a benchmark for future analyses of losses of heterostyly in
other angiosperms.