Parallel loss of anthocyanins triggers the incipient sympatric speciation in an alpine ginger.

Abstract

Change of flower color can readily lead to a shift in pollinators, potentially causing pollinator mediated reproductive isolation or even speciation. Here, we examined the ecological and evolutionary consequences of flower color polymorphism in Roscoea cautleoides, an alpine ginger with sympatric distribution of purple- and yellow-flowered plants. Variations in pollinator visitation and specialization to the flower color contributed greatly to pre-zygotic reproductive isolation, with post-zygotic isolation also observed in reciprocal pollination. Yellow-flowered plants evolved independently from purple-flowered plants in two populations due to the absence of anthocyanins, as supported by metabolic, expression, and genetic analysis. Despite early genetic divergence between the two-flower-colored plants, highly differentiated genes were associated with reproduction and stress, while highly selective genes were enriched in stress. Our results suggest that parallel loss of anthocyanins leads to flower color polymorphism in different populations of R. cautleoides, with pollinator preference contributing to reproductive isolation and subsequent genetic differentiation, indicating the process of incipient speciation triggered by flower color changes with sympatric distribution.