Although species radiations on island archipelagos are broadly studied, the geographic and ecological modes of speciation that underlie diversification are often not fully understood. Both allopatry and sympatry play a role during radiations, particularly on islands with profound habitat diversity. Here, we use the most diverse Canary Island plant radiation, Aeonium (Crassulaceae), to phylogenetically test two hypotheses: (1) allopatric speciation, which predicts that closely related taxa are ecologically similar but do not co-occur, and (2) sympatric speciation, whereby closely related taxa co-occur geographically but are ecologically distinct. We fitted niche and spatial distribution models based on extensive field surveys to quantify geographic and ecological divergence among taxa integrated in a phylogenetic context. While allopatry seems to be the main driver in speciation among islands, within-island speciation occurs in sympatry. Contrary to our expectation, phylogenetically closely related species tend to occupy similar ecological niches, suggesting that ecological niche divergence among species accumulates slowly, even in sympatry. This suggests that evolutionary young taxa, may be partially reproductively isolated due to subtle phenotypic differences, such as reproductive morphology and phenology rather than by ecology and may putatively exacerbate divergence among populations. Thus, allopatry and sympatry are complementary speciation mechanisms on oceanic islands, jointly spurring this enigmatic radiation.

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.

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.