Divergent habitat selection across many loci maintains species boundaries during introgression

Abstract

Evidence of introgression between well-defined species is abundant, begging the question, how are species boundaries maintained during introgression? Work on this question has largely focused on systems where divergence is controlled by a few large effect genetic loci. However, adaptive divergence is often highly polygenic, especially between young species that remain capable of gene exchange. Here, we use phylogeny based introgression statistics and local ancestry inference to characterize the genomic, spatial, and historical extent of introgression between two recently diverged Neotropical plant species. We then use QTL analysis to investigate the genetic basis of traits under divergent abiotic and biotic selection that are involved in habitat isolation. Finally, we combine these top-down and bottom-up approaches to clarify how species with polygenic reproductive isolation maintain cohesion in the face of gene flow. We find clear evidence of both recent and ancient introgression between Costus villosissimus and C. allenii, but overall genomic divergence remains relatively high (Fst:[~] 0.27) in part due to strong divergent habitat selection. Traits involved in divergent habitat adaptation are polygenic, such that strong habitat selection is spread across many loci rather than concentrated on a few loci of large effect. In contrast to the islands of divergence seen around large effect loci in other hybridizing species pairs, we see genomically widespread and moderate peaks of both differentiation and introgression. Our results indicate that strong selection spread across many loci contributing to reproductive isolation can maintain species differentiation despite introgression. Significance StatementGene flow between species (introgression) reduces genetic differentiation. And yet, introgression between well-defined species is common. How do species remain distinct in the face of introgression? Previous work focuses on differentiation maintained by elevated divergence in a few genomic regions (loci) with large effects. However, many loci with small effects commonly control differences between species. To clarify how species with abundant differentiating loci can remain distinct during introgression, we described patterns of introgression between two Neotropical plants and characterized the genetic basis of their divergent habitat adaptation. We found that isolation by divergent habitat adaptation is likely controlled by numerous small-effect and genomically widespread loci, and that habitat selection across multiple traits is sufficient to maintain differentiation despite ongoing introgression.