A two-locus hybrid incompatibility is widespread, polymorphic, and active in natural populations of Mimulus

Abstract

Reproductive isolation, which is essential for the maintenance of species in sympatry, is often incomplete between closely related species. In these taxa, reproductive barriers must continue to evolve within species, without being degraded by ongoing gene flow. To better understand this dynamic, we investigated the frequency and distribution of incompatibility alleles at a two-locus, recessive-recessive hybrid lethality system between species of yellow monkeyflower (Mimulus guttatus and M. nasutus) that hybridize in nature. We found that M. guttatus typically carries hybrid lethality alleles at one locus (hl13) and M. nasutus typically carries hybrid lethality alleles at the other locus (hl14). As a result, most naturally formed hybrids will carry incompatible alleles at both loci, with the potential to express hybrid lethality in later generations. Despite this general pattern, we also discovered considerable polymorphism at both hl13 and hl14 within both Mimulus species. For M. guttatus, polymorphism at both loci even occurs within populations, meaning that incompatible allele pairings might also often arise through regular, intraspecific gene flow. By examining genetic variation linked to hl13 and hl14, we discovered that introgression from M. nasutus is a primary driver of this polymorphism within M. guttatus. Additionally, patterns of introgression at the two hybrid lethality loci suggest that natural selection acts to eliminate incompatible allele pairings, providing evidence that even weak reproductive barriers might promote genomic divergence between species.