Population genomic consequences of novel life history and mating system adaptation to a geothermal soil mosaic in yellow monkeyflowers (Mimulus guttatus)

Local selection can promote phenotypic divergence despite gene flow across habitat mosaics, but adaptation itself may generate substantial barriers to genetic exchange. In plants, life-history, phenology, and mating system divergence have been particularly proposed to promote genetic differentiation in sympatry. In this study, we investigate phenotypic and genetic variation in Mimulus guttatus (yellow monkeyflowers) across a geothermal soil mosaic in Yellowstone National Park (YNP). Plants from thermal annual and nonthermal perennial habitats were heritably differentiated for life history and mating system traits, consistent with local adaptation to the ephemeral thermal-soil growing season. However, genome-wide genetic variation primarily clustered plants by geographic region, with little variation sorting by habitat. The one exception was an extreme thermal population also isolated by a 200m geographical gap. Individual inbreeding coefficients (FIS) were higher (and predicted by trait variation) in annual plants and annual pairs showed greater isolation by distance at local (<1km) scales. Finally, YNP adaptation does not re-use a widespread inversion polymorphism diagnostic of annual vs. perennial M. guttatus range-wide, suggesting a novel genetic mechanism. Overall, this work suggests that life history and mating system adaptation strong enough to shape individual mating patterns does not necessarily generate incipient speciation without geographical barriers.