Genetic loci with parent of origin effects cause hybrid seed lethality between Mimulus species
Austin G Garner, Amanda M Kenney, Lila Fishman, Andrea L Sweigart
The classic finding in both flowering plants and mammals that hybrid lethality often depends on parent of origin effects suggests that divergence in the underlying loci might be an important source of hybrid incompatibilities between species. In flowering plants, there is now good evidence from diverse taxa that seed lethality arising from interploidy crosses is often caused by endosperm defects associated with deregulated imprinted genes. A similar seed lethality phenotype occurs in many crosses between closely related diploid species, but the genetic basis of this form of early-acting F1 postzygotic reproductive isolation is largely unknown. Here, we show that F1 hybrid seed lethality is an exceptionally strong isolating barrier between two closely related Mimulus species, M. guttatus and M. tilingii, with reciprocal crosses producing less than 1% viable seeds. Using a powerful crossing design and high-resolution genetic mapping, we identify both maternally- and paternally-derived loci that contribute to hybrid seed incompatibility. Strikingly, these two sets of loci are largely non-overlapping, providing strong evidence that genes with parent of origin effects are the primary driver of F1 hybrid seed lethality between M. guttatus and M. tilingii. We find a highly polygenic basis for both parental components of hybrid seed lethality suggesting that multiple incompatibility loci have accumulated to cause strong postzygotic isolation between these closely related species. Our genetic mapping experiment also reveals hybrid transmission ratio distortion and chromosomal differentiation, two additional correlates of functional and genomic divergence between species.