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 are often locally adapted to distinct microhabitats. However, temporal variation may cause local maladaptation and species boundary breakdown, especially during extreme climatic events leading to episodic selection. Repeated reciprocal transplants can reveal the interplay between 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 drastically differing snowpack. If there is ecological isolation, then we predicted divergent phenotypic selection between habitats in line with species' differences and local adaptation. We found interannual fluctuations in phenotypic selection, often in unpredicted directions. However, a combined-year analysis detected longer-term divergent selection on flowering time, a key temporally isolating and adaptative trait, suggesting that selection may reinforce species boundaries despite short-term fluctuations. Finally, we found temporal variation in local adaptation with M. laciniatus locally adapted in low snowpack years, while an extremely high snowpack year contributed to average local maladaptation of M. guttatus .

Spatially and temporally varying selection influence species boundaries in two sympatric Mimulus.

Spatially and temporally varying selection can maintain genetic variation within and between populations, but it is less well known how these forces influence divergence between closely related species. We identify the interaction of temporal and spatial variation in selection and their role in either reinforcing or eroding divergence between two closely related Mimulus species. Using repeated reciprocal transplant experiments with advanced generation hybrids, we compare the strength of selection on quantitative traits involved in adaptation and reproductive isolation in Mimulus guttatus and Mimulus laciniatus between two years with dramatically different water availability. We found strong divergent habitat-mediated selection on traits in the direction of species differences during a drought in 2013, suggesting that spatially varying selection maintains species divergence. However, a relaxation in divergent selection on most traits in an unusually wet year (2019), including flowering time, which is involved in pre-zygotic isolation, suggests that temporal variation in selection may weaken species differences. Therefore, we find evidence that temporally and spatially varying selection may have opposing roles in mediating species boundaries. Given our changing climate, future growing seasons are expected to be more similar to the dry year, suggesting that in this system climate change may actually increase species divergence.

Darwin's vexing contrivance: a new hypothesis for why some flowers have two kinds of anther.

Heteranthery, the presence of two or more anther types in the same flower, is taxonomically widespread among bee-pollinated angiosperms, yet has puzzled botanists since Darwin. We test two competing hypotheses for its evolution: the long-standing 'division of labour' hypothesis, which posits that some anthers are specialized as food rewards for bees whereas others are specialized for surreptitious pollination, and our new hypothesis that heteranthery is a way to gradually release pollen that maximizes pollen delivery. We examine the evolution of heteranthery and associated traits across the genus Clarkia (Onagraceae) and study plant-pollinator interactions in two heterantherous Clarkia species. Across species, heteranthery is associated with bee pollination, delayed dehiscence and colour crypsis of one anther whorl, and movement of that anther whorl upon dehiscence. Our mechanistic studies in heterantherous species show that bees notice, forage on and export pollen from each anther whorl when it is dehiscing, and that heteranthery promotes pollen export. We find no support for division of labour, but multifarious evidence that heteranthery is a mechanism for gradual pollen presentation that probably evolved through indirect male-male competition for siring success.