Breakdown of dimorphic enantiostyly is linked to reduced herkogamy and increased self-pollination

The evolutionary breakdown of outcrossing mechanisms has occurred repeatedly across angiosperm lineages. Stylar polymorphisms are of particular interest because their floral morphs exhibit discrete variation with pronounced spatial separation between reproductive organs (herkogamy), a trait strongly influencing outcrossing. These polymorphisms are typically maintained by negative frequency-dependent selection resulting from disassortative (between-morph) mating. In contrast, biased morph ratios and homostylous variants with anthers and stigmas adjacent to one another often signal transitions towards self-fertilization and erosion of the polymorphism. Here, we investigate this transition in three Wachendorfia species that exhibit dimorphic enantiostyly. Based on observations of biased morph ratios, we predicted the breakdown of enantiostyly to be associated with reduced herkogamy and an increased likelihood of self-pollination.

To test this hypothesis, we quantified morph ratios and reproductive-organ separation across 42 populations spanning the three species. In a subset of populations, we also measured flower width, pollinator visitation, seed set and pollen transfer to examine their association with floral polymorphism breakdown.

Populations with equal morph ratios typically exhibited well-developed herkogamy, consistent with disassortative mating. In contrast, reduced herkogamy, increasing the potential for autonomous self-pollination, was characteristic of populations with biased ratios or those that were monomorphic. Homostylous variants occurred in all three species and were characteristic of populations with low herkogamy and biased morph ratios as expected during early stages in the evolutionary modification of stylar polymorphism.

Our investigation revealed that the breakdown of outcrossing polymorphisms is not restricted to heterostylous species but also occurs in species with mirror-image flowers. In both cases of breakdown, the proximate mechanism causing increased self-pollination involves changes in herkogamy, emphasizing the importance of this key reproductive trait in influencing mating-system evolution.