On the causes of correlated genomic ancestry across contrasting hybridization histories in a monkeyflower species pair.

Abstract

Hybridization is a powerful force shaping the evolutionary trajectories of species, yet its outcomes are highly variable both across taxa and within a pair of species. In this study, we examine the processes shaping variation in the extent of hybrid ancestry, both among populations and across the genome. We use low-coverage sequencing data to infer local ancestry across the genome for 782 individuals from multiple populations across two geographic regions within the broadly overlapping range of Mimulus guttatus and Mimulus nasutus. We find that the extent of hybrid ancestry is variable across populations, supporting disparate historical patterns of hybridization. However, genomic patterns of hybrid ancestry are correlated across groups, indicating they are shaped by parallel processes. Correlations are highest in geographically proximal populations, including between sympatric and allopatric locations, providing evidence that introgression is not locally constrained but spreads via migration across the landscape. We find that features of the genome are predictive of hybrid ancestry and its correlations among populations. However, contrary to findings in some other species, these patterns are likely not driven by simple linked selection against hybrid ancestry. Genomic outliers for high hybrid ancestry are often shared among populations, suggesting a role for parallel positive selection on ancestry. However, known loci associated with reproductive isolation are poor predictors of ancestry variation across populations, indicating that selection acting in natural hybrid populations is highly polygenic and that the underlying genetic architecture varies across space. Overall, this study demonstrates how ecological, demographic, and genomic features all interact to shape the outcomes of hybridization.