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Abstract
Understanding the nature of species boundaries, including the mechanisms underlying their formation, maintenance, and breakdown, has long been a goal of evolutionary biology. Reproductive isolation between lineages is astoundingly variable across space, across time, across lineages, and across genomic loci, but we still have much to learn about the evolutionary, environmental, and genetic factors that shape this variation. Here, we use multiple species groups of Mimulus monkeyflowers as models to investigate the causes and consequences of variation in reproductive isolation at different scales. First, we characterize genomic patterns of divergence and components of postmating reproductive isolation within an understudied group of species in Mimulus section Eunanus. We find near-complete postmating isolation across all species pairs, driven by a combination of pollen-pistil incompatibility, hybrid seed inviability, and hybrid sterility. Consistent with these patterns, we find substantial genetic divergence and cryptic diversity, but signatures of ancient hybridization are still detectable. Next, we shift our focus to Mimulus guttatus and Mimulus nasutus, a recently diverged species pair with ongoing hybridization. We investigate spatial and temporal heterogeneity in patterns of hybrid ancestry across a decade of sampling, using genome-wide ancestry inference combined with measures of premating isolation. We find that hybrid ancestry is pervasive, structured at incredibly small spatial scales, and stable across time. Phenological isolation fluctuates widely across years, likely driven by changes in water availability, with impacts on gene flow between admixture groups. Finally, we generate genomic data from a second area ~1000km away to examine parallelism across the genome in hybrid ancestry, and to ask how well reproductive barrier loci from controlled crosses can predict introgression outcomes in wild populations. We see differences in the extent of hybridization, but substantial parallelism in hybrid ancestry patterns across distant geographic areas. Known reproductive barrier loci are poor predictors of hybrid ancestry patterns, highlighting the importance of multiple complementary approaches to understanding drivers of reproductive isolation. Overall, these three studies demonstrate how careful characterization of reproductive barriers across multiple axes of variation can inform our understanding of the speciation process as it plays out in complex environments.