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 evolve within species, without being degraded by ongoing gene flow. To better understand this dynamic, we investigated the frequency and geographic distribution of alleles underlying a two-locus, hybrid lethality system between naturally hybridizing species of monkeyflower (Mimulus guttatus and M. nasutus). 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, natural hybrids carry incompatible alleles at both loci, and express hybrid lethality in later generations. We also discovered considerable polymorphism at both hl13 and hl14 within both species. For M. guttatus, polymorphism at both loci occurs within populations, meaning that incompatible allele pairings likely arise through intraspecific gene flow. Genetic variation at markers linked to hl13 and hl14 suggest that introgression from M. nasutus is the primary driver of this polymorphism within M. guttatus. Additionally, patterns of introgression at the two hybrid lethality loci suggest that natural selection eliminates incompatible allele pairings, suggesting that even weak reproductive barriers might promote genomic divergence between species.

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.

Population Genetics of the Rubber-Producing Russian Dandelion (Taraxacum kok-saghyz).

The Russian dandelion, Taraxacum kok-saghyz (TKS), is a perennial species native to Central Asia that produces high quality, natural rubber. Despite its potential to help maintain a stable worldwide rubber supply, little is known about genetic variation in this species. To facilitate future germplasm improvement efforts, we developed simple-sequence repeat (SSR) markers from available expressed-sequence tag (EST) data and used them to investigate patterns of population genetic diversity in this nascent crop species. We identified numerous SSRs (1,510 total) in 1,248 unigenes from a larger set of 6,960 unigenes (derived from 16,441 ESTs) and designed PCR primers targeting 767 of these loci. Screening of a subset of 192 of these primer pairs resulted in the identification of 48 pairs that appeared to produce single-locus polymorphisms. We then used the most reliable 17 of these primer pairs to genotype 176 individuals from 17 natural TKS populations. We observed an average of 4.8 alleles per locus with population-level expected heterozygosities ranging from 0.28 to 0.50. An average pairwise FST of 0.11 indicated moderate but statistically significant levels of genetic differentiation, though there was no clear geographic patterning to this differentiation. We also tested these 17 primer pairs in the widespread common dandelion, T. officinale, and a majority successfully produced apparently single-locus amplicons. This result demonstrates the potential utility of these markers for genetic analyses in other species in the genus.

Evolutionary genetics of plant adaptation: insights from new model systems.

Flowering time and mating system divergence are two of the most common adaptive transitions in plants. We review recent progress toward understanding the genetic basis of these adaptations in new model plant species. For flowering time, we find that individual crosses often reveal a simple genetic basis, but that the loci involved almost always vary within species and across environments, indicating a more complex genetic basis species-wide. Similarly, the transition to self-fertilization is often genetically complex, but this seems to depend on the amount of standing variation and time since species divergence. Recent population genomic studies also raise doubts about the long-term adaptive potential of self-fertilization, providing evidence that purifying selection is less effective in highly selfing species.

Hybrid watermilfoil lineages are more invasive and less sensitive to a commonly used herbicide than their exotic parent (Eurasian watermilfoil).

Hybridization may stimulate the evolution of invasiveness in human-impacted habitats if unique hybrid genotypes have higher fitness than parental genotypes. Human efforts to control invasive taxa frequently involve the intentional alteration of habitats, but few studies have considered whether hybridization can result in decreased sensitivity to control measures. Here, we investigate whether interspecific hybrids between introduced Eurasian watermilfoil (Myriophyllum spicatum) and native northern watermilfoil (M. sibiricum) are more invasive than parental Eurasian watermilfoil, especially in regard to their relative responses to an herbicide commonly applied for their control (2,4-dichlorophenoxyacetic acid; 2,4-D). In two separate laboratory experiments, hybrids on average grew faster and were less sensitive to 2,4-D compared with parental Eurasian watermilfoil. These two invasive traits appear to be common in hybrid watermilfoils, as opposed to being restricted to a few unique lineages, because they were found in a diversity of hybrid genotypes from several independent hybridization events. In addition, we found that hybrids occurred more frequently than parental species in natural lakes previously treated with 2,4-D. Our results provide compelling empirical evidence that hybridization is associated with the evolution of increased invasiveness in watermilfoils, and have important implications for their management.