Gene duplicates cause hybrid lethality between sympatric species of Mimulus

Abstract

Hybrid incompatibilities play a critical role in the evolution and maintenance of species. We have discovered a simple genetic incompatibility that causes lethality in hybrids between two closely related species of yellow monkeyflower (Mimulus guttatus and M. nasutus). This hybrid incompatibility, which causes one sixteenth of F2 hybrid seedlings to lack chlorophyll and die shortly after germination, occurs between sympatric populations that are connected by ongoing interspecific gene flow. Using complimentary genetic mapping and gene expression analyses, we show that lethality occurs in hybrids that lack a functional copy of the critical photosynthetic gene pTAC14. In M. guttatus, this gene was duplicated, but the ancestral copy is no longer expressed. In M. nasutus, the duplication is missing altogether. As a result, hybrids die when they are homozygous for the nonfunctional M. guttatus copy and missing the duplicate from M. nasutus, apparently due to misregulated transcription of key photosynthetic genes. Our study indicates that neutral evolutionary processes may play an important role in the evolution of hybrid incompatibilities and opens the door to direct investigations of their contribution to reproductive isolation among naturally hybridizing species.\n\nAuthor SummaryHybrid incompatibilities play an important role in speciation, because they act to limit gene flow between species. Identifying the genes that underlie these barriers sheds light on the evolutionary forces and genetic mechanisms that give rise to new species. We identified a reproductive barrier that causes lethality in the F2 offspring of sympatric species of yellow monkeyflower (Mimulus guttatus and M. nasutus). We show that lethality occurs in hybrids that lack a functional copy of the critical photosynthetic gene pTAC14. This gene was duplicated in M. guttatus, but the ancestral copy subsequently lost function. In M. nasutus, no duplication occurred. As a consequence, F2 hybrids that are homozygous for non-functional M. guttatus copies at one locus and missing M. nasutus duplicates at the other locus completely lack functional pTAC14 and die. Our data indicate that non-functionalization of ancestral pTAC14 in M. guttatus occurred via neutral evolutionary change. These results suggest that neutral evolutionary forces may play an important role in speciation.