Different molecular changes underlie the same phenotypic transition:
origins and consequences of independent shifts to homostyly within
species
Abstract
The molecular basis of phenotypic convergence, a key topic in
evolutionary biology and ecology, has been investigated especially
between species. However, it remains unclear whether mutations in the
same or different positions of the same gene, or in different genes
underlie phenotypic convergence within species. A classic example of
convergence is the transition from outcrossing to selfing in plants,
illustrated by the repeated shift from heterostyly to homostyly.
Heterostyly is characterized by the reciprocal position of male and
female sexual organs in two (or three) distinct, incompatible floral
morphs, while homostyly is characterized by a single, self-compatible
floral morph. Primula has long served as the prime model for
studies of heterostyly and homostyly. Here, we elucidate the phenotypic
and molecular origins of homostyly in P. vulgaris and its
microevolutionary consequences by integrating microsatellite analyses of
both progeny arrays and natural populations characterized by varying
frequencies of homostyles with DNA sequence analyses of the gene
controlling the position of female sexual organs (CYPᵀ). We found
that: homostyles evolved repeatedly from short-styled individuals in
association with different types of loss-of-function mutations in
CYPᵀ and, consequently, short-styled individuals occur at lower
frequencies than long-styled individuals across populations with all
three morphs; the shift to homostyly promotes a shift to selfing; and
intra-population frequency of homostyles is positively correlated with
selfing rate and inbreeding level, increasing genetic differentiation
among populations. These results elucidate the connections between the
genotypic and phenotypic levels of convergence and the effects of
contrasting floral morphologies on reproductive strategies.