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.

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

“…http://dx.doi.org/10.1101/339986 doi: bioRxiv preprint first posted online Jun. 7, 2018; (Figure 1, Zuellig and Sweigart 2018). In this study, if an F1 hybrid inherited an incompatible 162 experimental allele at either hl13 or hl14, one of the two experimental-tester F2 progeny sets was 163 expected to segregate white seedlings at a frequency of one sixteenth (Figure 1).…”

“…7, 2018; duplicates at hl13 and hl14. Genetic distances were calculated from a F2 mapping population of 671 white F2 seedlings (DPR104-nas x DPR102-gutt) described in Zuellig and Sweigart (2018). was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.…”

The role of copy-number variation in the reinforcement of sexual isolation between the two European subspecies of the house mouse

“…Copy-number variation can contribute to phenotypic divergence by altering gene products, creating paralogues that can diverge and neofunctionalize, or by altering gene dosage [ 32 , 33 ]. CNVs can also act as Bateson–Dobzhansky–Muller [ 34 – 36 ] incompatibilities if independent pseudogeneization or neofunctionalization of duplicated paralogues in divergent lineages leads to dysfunctional genes in hybrids, [ 37 ] as observed in sympatric Mimulus species [ 38 ].…”

Patterns of Transmission Ratio Distortion in Interspecific Lettuce Hybrids Reveal a Sex-Independent Gametophytic Barrier

“…Another explanatory model for the digenic HI could be gene duplication, followed by loss of function in one of the redundant gene copies (Bikard et al 2009;Zuellig and Sweigart 2018). In 1957, Oka proposed reciprocal loss of duplicated genes for hybrid sterility in rice (Oka 1957).…”

“…DM incompatibilities can evolve by various processes. One of these processes is gene duplication, followed by loss of function in one of the redundant gene copies (Bikard et al 2009;Zuellig and Sweigart 2018). When functional genes end up in different genomic locations in related species, some individuals of interspecific hybrid-derived progenies may inherit only nonfunctional copies.…”