Fluctuating selection in a Monkeyflower hybrid zone.

While 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 guttatus and Mimulus 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 to M. laciniatus's seasonally dry rocky outcrop habitat than M. guttatus's moist 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, than M. guttatus in both species' habitats, as well as phenotypic selection for M. 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 from M. laciniatus into M. 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 of M. laciniatus introgression. 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 these Mimulus species.

Short-term fluctuating and long-term divergent selection on sympatric Monkeyflowers: insights from decade-spanning reciprocal transplants.

Sympatric species often adapt to distinct microhabitats, leading to reproductive isolation and phenotypic diversity. However, temporal variation in selection may cause local maladaptation and species boundary breakdown, especially in years with large climatic events leading to episodic selection. Repeated reciprocal transplants can reveal short and long-term patterns of natural selection. To examine evolutionary trajectories of sympatric Monkeyflowers adapted to different niches, Mimulus guttatus and M. laciniatus, we performed three replicated transplants and combined them with previous experiments to leverage a dataset of five transplants spanning 10 years. We performed phenotypic selection analyses on parents and hybrids in parental habitats in Yosemite NP, CA during years of differing snowpack. If there is ecological isolation, then we predicted local adaptation and divergent phenotypic selection between habitats in line with species' differences. We found interannual fluctuations in selection, often not in predicted directions. Episodic selection due to extreme high snowpack caused a reversal of local adaptation and contributed to overall maladaptation of M. guttatus . However, a combined-year analysis detected longer-term divergent selection on flowering time, a key temporally isolating and adaptative trait, in agreement with species' differences. In conclusion, even with annual fluctuations, longer-term divergent selection may still promote species boundaries.