Fluctuating selection in a Monkeyflower hybrid zone

Abstract

AbstractWhile hybridization was viewed as a hindrance to adaptation and speciation by early evolutionary biologists, recent studies have demonstrated the importance of hybridization in facilitating evolutionary processes. However, it is still not well-known what role spatial and temporal variation in natural selection play in the maintenance of naturally occurring hybrid zones. To identify whether hybridization is adaptive between two closely related monkeyflower species,Mimulus guttatusandMimulus laciniatus, we performed repeated reciprocal transplants between natural hybrid and pure species’ populations. We planted parental genotypes along with multiple experimental hybrid generations in a dry (2021) and extremely wet (2023) year in the Sierra Nevada, CA. By taking fine scale environmental measurements, we found that the environment of the hybrid zone is more similar toM. laciniatus’sseasonally dry rocky outcrop habitat thanM. guttatus’smoist meadows. In our transplants hybridization does not appear to be maintained by a consistent fitness advantage of hybrids over parental species in hybrid zones, but rather a lack of strong selection against hybrids. We also found higher fitness of the drought adapted species,M. laciniatus,thanM. guttatusin both species’ habitats, as well as phenotypic selection forM. laciniatus-like traits in the hybrid habitat in the dry year of our experiment. These findings suggest that in this system hybridization might function to introduce drought-adapted traits and genes fromM. laciniatusintoM. guttatus, specifically in years with limited soil moisture. However, we also find evidence of genetic incompatibilities in second generation hybrids in the wetter year, which may balance a selective advantage ofM. laciniatusintrogression. Therefore, we find that hybridization in this system is both potentially adaptive and costly, and that the interaction of positive and negative selection likely determines patterns of gene flow between theseMimulusspecies.Lay SummaryEarly evolutionary biologists understood hybridization, or interbreeding between species, as limiting to adaptation. While recent studies have shown that hybridization is important for adaptation, much remains to be learned about the role of natural selection in maintaining hybridization. We use a repeated transplant experiment in dry and wet years with two closely related monkeyflower species,Mimulus guttatusandMimulus laciniatus, and experimental hybrids, to identify how hybridization is maintained. By measuring environmental variables, we found that the hybrid zone is more similar toM. laciniatus’shabitat thanM. guttatus’sin some years. We found that hybrids do equally well as parental species in hybrid zones. Additionally, the drought adapted species,M. laciniatus,performed better thanM. guttatusin both parental habitats, and there was selection for moreM. laciniatus-like traits in the hybrid habitat. These results suggest that hybridization might introduce drought-adapted traits and genes fromM. laciniatusin a dry year. In a wet year, first generation hybrids performed better than advanced generation hybrids, possibly due to negative genetic interactions. In summary, we find that hybridization is beneficial and costly, and variation in environmental factors likely determines patterns of hybridization.