The genomic outcomes of hybridization vary over time within a monkeyflower radiation

Abstract The accumulation of genetic differences through time can lead to reproductive isolation between populations and the origin of new species. However, hybridization between emerging species can occur at any point before isolation is complete. The evolutionary consequences of this hybridization may vary depending on when it occurred. If hybridization occurred later during the process, when ecological and genetic differences have accumulated between diverging lineages, low hybrid fitness can result in selection against gene flow. If hybridization occurred earlier, when barriers present were too weak to limit introgression, then hybridization can lead to genetic swamping. Alternatively, adaptive introgression can occur at any point during speciation. Thus, by understanding the history and genomic consequences of hybridization at different points along the speciation continuum, we can begin to understand how variation present within populations translates to divergence between species. Here, we identified the genomic signals of introgressive hybridization at different points during the divergence of two monkeyflower taxa endemic to the Channel Islands of California. We found that both ancient and recent introgression have shaped their genomes, but the impacts of selection on this foreign material varied. There was no signal of selection against ancient introgression, but we did find strong evidence for selection against recent introgression, potentially because there are more reproductive barriers in place now, reducing fitness in recent hybrids. Thus, this study reveals that hybridization can occur at multiple points throughout the divergence history of a radiation, but the processes shaping genome wide levels of introgression can change over time.