Dichogamy correlates with outcrossing rate and defines the selfing syndrome in the mixed-mating genus Collinsia

Abstract

How and why plants evolve to become selfing is a long-standing evolutionary puzzle. The transition from outcrossing to highly selfing is less well understood in self-compatible (SC) mixed-mating (MM) species where potentially subtle interactions between floral phenotypes and the environment are at play. We examined floral morphological and developmental traits across an entire SC MM genus, Collinsia, to determine which, if any, predict potential autonomous selfing ability when pollinators are absent (AS) and actual selfing rates in the wild, s_m, and to best define the selfing syndrome for this clade. Using polymorphic microsatellite markers, we obtained 30 population-level estimates of s_m across 19 Collinsia taxa. Species grand means for the timing of herkogamy (stigma–anther contact) and dichogamy (stigmatic receptivity, SR), AS, floral size, longevity and their genetic correlations were quantified for 22 taxa. Species fell into discrete selfing and outcrossing groups based on floral traits. Loss of dichogamy defines Collinsia's selfing syndrome. Floral size, longevity and herkogamy also differ significantly between these groups. Most taxa have high AS rates (>80 %), but AS is uncorrelated with any measured trait. In contrast, s_m is significantly correlated only with SR. High variance in s_m was observed in the two groups. Collinsia species exhibit clear morphological and developmental traits diagnostic of ‘selfing’ or ‘outcrossing’ groups. However, many species in both the ‘selfing’ and the ‘outcrossing’ groups were MM, pointing to the critical influence of the pollination environment, the timing of AS and outcross pollen prepotency on s_m. Flower size is a poor predictor of Collinsia species' field selfing rates and this result may apply to many SC species. Assessment of the variation in the pollination environment, which can increase selfing rates in more ‘outcrossing’ species but can also decrease selfing rates in more ‘selfing’ species, is critical to understanding mating system evolution of SC MM taxa.