Introgressive hybridization facilitates adaptive divergence in a recent radiation of monkeyflowers

Abstract

A primary goal in evolutionary biology is to identify the historical events that have facilitated the origin and spread of adaptations. When these adaptations also lead to reproductive isolation, we can learn about the evolutionary mechanisms contributing to speciation. We reveal the complex history of the gene MaMyb2 in shaping flowercolour divergencewithin a recent radiation of monkeyflowers.In the Mimulus aurantiacus species complex, red-flowered M.a. ssp. puniceus and yellow-flowered M. a. ssp. australis are partially isolated because of differences in pollinator preferences. Phylogenetic analyses based on genome-wide variation across the complex suggest two origins of red flowers from ayellow-flowered ancestor: one in M. a. ssp. puniceus and one in M. a. ssp. flemingii. However, in both cases, red flowers are caused by cisregulatory mutations in the gene MaMyb2. Although this could be due to distinct mutations in each lineage, we show that the red allele in M. a. ssp. Puniceus did not evolve de novo or exist as standing variation in its yellow-flowered ancestor. Rather, our results suggest that a single red MaMyb2 allele evolved during the radiation of M. aurantiacus that was subsequently transferred to the yellow-flowered ancestor of M. a. ssp. puniceus via introgressive hybridization. Because gene flow is still possible among taxa, we conclude that introgressive hybridization can be a potent driver of adaptation at the early stages of divergence that can contribute to the origins of biodiversity.