Phenotypic and genetic differentiation among yellow monkeyflower populations from thermal and non-thermal soils in Yellowstone National Park

In flowering plants, soil heterogeneity can generate divergent natural selection over fine spatial scales, and thus promote local adaptation in the absence of geographic barriers to gene flow. Here, we investigate phenotypic and genetic differentiation in one of the few flowering plants that thrives in both geothermal and non-thermal soils in Yellowstone National Park (YNP). Yellow monkeyflowers (Mimulus guttatus) growing at two geothermal (thermal) sites in YNP were distinct in growth form and phenology from paired populations growing nearby (< 500 m distant) in non-thermal soils. In simulated thermal and non-thermal environments, thermal plants remained significantly divergent from non-thermal plants in vegetative, floral, mating system, and phenological traits. Plants from both thermal populations flowered closer to the ground, allocated relatively more to sexual reproduction, were more likely to initiate flowering under short daylengths, and made smaller flowers that could efficiently self-fertilize without pollinators. These shared differences are consistent with local adaptation to life in the ephemeral window for growth and reproduction created by winter and spring snowmelt on hot soils. In contrast, habitat type (thermal vs. non-thermal) explained little of the genetic variation at neutral markers. Instead, we found that one thermal population (Agrostis Headquarters; AHQ-T) was strongly differentiated from all other populations (all F (ST) > 0.34), which were only weakly differentiated from each other (all F (ST) < 0.07). Phenotypic differentiation of thermal M. guttatus, but little population genetic evidence of long-term ecotypic divergence, encourages further investigations of the potential for fine-scale adaptation and reproductive isolation across the geothermal gradient in Yellowstone.