Mating system and environment predict the direction and extent of introgression between incipient Clarkia species

Abstract Introgression is pervasive across the tree of life, varying across taxa, geography, and genomes. However, we are only beginning to understand the factors that modulate this variation and how they may be affected by global change. Here, we used 200 genomes and a 15-year site-specific environmental dataset to investigate the effect of mating system divergence and environmental variation on the magnitude of introgression between two recently diverged annual plants. Two subspecies of Clarkia xantiana diverged ca. 65k years ago and subsequently came into secondary sympatry where they form replicated contact zones. We found that introgression is asymmetric between taxa, with substantially more introgression from the self-fertilizing taxon to the outcrossing taxon. This asymmetry is caused by a bias in the direction of initial F1 hybrid formation and subsequent backcrossing. We also found extensive variation in the outcrosser’s admixture proportion among contact zones, which is predicted nearly entirely by interannual variance in spring precipitation. Greater fluctuations in spring precipitation result in higher admixture proportions, likely mediated by the effects of spring precipitation on the expression of traits that determine premating reproductive isolation. Climate-driven hybridization dynamics may be particularly affected by global change, potentially reshaping species boundaries and adaptation to novel environments.