Postzygotic barriers persist despite ongoing introgression in hybridizing Mimulus species

The evolution of postzygotic isolation is thought to be a key step in maintaining species boundaries upon secondary contact, yet the dynamics and persistence of hybrid incompatibilities in sympatric species are not well understood. Here, we explore these issues using genetic mapping in three populations of recombinant inbred lines between naturally hybridizing monkeyflowers Mimulus guttatus and M. nasutus from the sympatric Catherine Creek population. The three M. guttatus founders differ dramatically in admixture history. Comparative genetic mapping also reveals three putative inversions segregating among the M. guttatus founders, two due to admixture. We observe strong, genome-wide transmission ratio distortion, but patterns are highly variable among populations. Some distortion is explained by epistatic selection favoring parental genotypes, but tests of inter-chromosomal linkage disequilibrium also reveal multiple candidate Dobzhansky-Muller incompatibilities. We also map several genetic loci for hybrid fertility, including two interacting pairs coinciding with peaks of distortion. Remarkably, in this limited sample of M. guttatus, we discover abundant segregating variation for hybrid incompatibilities with M. nasutus, suggesting this population harbors diverse contributors to postzygotic isolation. Moreover, even with substantial admixture, hybrid incompatibilities between Mimulus species persist, suggesting postzygotic isolation might be a potent force in maintaining species barriers in this system.