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Sweigart, A. L.

Publications and source records attributed to Sweigart, A. L..

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

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.

evolutionary biology

Gene duplicates cause hybrid lethality between sympatric species of Mimulus

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.

evolutionary biology

Mechanisms of transmission ratio distortion at hybrid sterility loci within and between Mimulus species

Hybrid incompatibilities are a common correlate of genomic divergence and a potentially important contributor to reproductive isolation. However, we do not yet have a detailed understanding of how hybrid incompatibility loci function and evolve within their native species, or why they are dysfunctional in hybrids. Here, we explore these issues for a well-studied, two-locus hybrid incompatibility between hybrid male sterility 1 (hms1) and hybrid male sterility 2 (hms2) in the closely related yellow monkeyflower species Mimulus guttatus and M. nasutus. By performing reciprocal backcrosses with introgression lines, we find evidence for gametic expression of the hms1-hms2 incompatibility. Surprisingly, however, hybrid transmission ratios at hms1 do not reflect this incompatibility, suggesting additional mechanisms counteract the effects of gametic sterility. Indeed, our backcross experiment shows hybrid transmission bias toward M. guttatus through both pollen and ovules, an effect that is particularly strong when hms2 is homozygous for M. nasutus alleles. In contrast, we find little evidence for hms1 transmission bias in crosses within M. guttatus, providing no indication of selfish evolution at this locus. Although we do not yet have sufficient genetic resolution to determine if hybrid sterility and transmission ratio distortion map to the same loci, our preliminary fine-mapping uncovers a genetically independent hybrid lethality system involving at least two loci linked to hms1. This fine-scale dissection of transmission ratio distortion at hms1 and hms2 provides insight into genomic differentiation between closely related Mimulus species and reveals multiple mechanisms of hybrid dysfunction.

evolutionary biology