Postzygotic barriers persist despite ongoing introgression in hybridizing Mimulus species.

The evolution of postzygotic isolation is thought to be a key step in maintaining species boundaries upon secondary contact, yet the dynamics and persistence of hybrid incompatibilities in naturally hybridizing species are not well understood. Here, we explore these issues using genetic mapping in three independent populations of recombinant inbred lines between naturally hybridizing monkeyflowers, Mimulus guttatus and Mimulus nasutus, from the sympatric Catherine Creek population. We discover that the three M. guttatus founders differ dramatically in admixture history, with nearly a quarter of one founder's genome introgressed from M. nasutus. Comparative genetic mapping in the three RIL populations reveals three new putative inversions, each one segregating among the M. guttatus founders, two due to admixture. We find strong, genome-wide transmission ratio distortion in all RILs, but patterns are highly variable among the three populations. At least some of this distortion appears to be explained by epistatic selection favouring parental genotypes, but tests of inter-chromosomal linkage disequilibrium also reveal multiple candidate Dobzhansky-Muller incompatibilities. We also map several genetic loci for hybrid pollen viability, including two interacting pairs that coincide with peaks of distortion. Remarkably, even with this limited sample of three M. guttatus lines, we discover abundant segregating variation for hybrid incompatibilities with M. nasutus, suggesting this population harbours diverse contributors to postzygotic isolation. Moreover, even with substantial admixture, hybrid incompatibilities between Mimulus species persist, suggesting postzygotic isolation might be a potent force in maintaining species barriers in this system.

Genomic mechanisms and consequences of diverse postzygotic barriers between monkeyflower species.

The evolution of genomic incompatibilities causing postzygotic barriers to hybridization is a key step in species divergence. Incompatibilities take 2 general forms-structural divergence between chromosomes leading to severe hybrid sterility in F1 hybrids and epistatic interactions between genes causing reduced fitness of hybrid gametes or zygotes (Dobzhansky-Muller incompatibilities). Despite substantial recent progress in understanding the molecular mechanisms and evolutionary origins of both types of incompatibility, how each behaves across multiple generations of hybridization remains relatively unexplored. Here, we use genetic mapping in F2 and recombinant inbred line (RIL) hybrid populations between the phenotypically divergent but naturally hybridizing monkeyflowers Mimulus cardinalis and M. parishii to characterize the genetic basis of hybrid incompatibility and examine its changing effects over multiple generations of experimental hybridization. In F2s, we found severe hybrid pollen inviability (<50% reduction vs parental genotypes) and pseudolinkage caused by a reciprocal translocation between Chromosomes 6 and 7 in the parental species. RILs retained excess heterozygosity around the translocation breakpoints, which caused substantial pollen inviability when interstitial crossovers had not created compatible heterokaryotypic configurations. Strong transmission ratio distortion and interchromosomal linkage disequilibrium in both F2s and RILs identified a novel 2-locus genic incompatibility causing sex-independent gametophytic (haploid) lethality. The latter interaction eliminated 3 of the expected 9 F2 genotypic classes via F1 gamete loss without detectable effects on the pollen number or viability of F2 double heterozygotes. Along with the mapping of numerous milder incompatibilities, these key findings illuminate the complex genetics of plant hybrid breakdown and are an important step toward understanding the genomic consequences of natural hybridization in this model system.

Postzygotic barriers persist despite ongoing introgression in hybridizing Mimulus species.

The evolution of postzygotic isolation is thought to be a key step in maintaining species boundaries upon secondary contact, yet the dynamics and persistence of hybrid incompatibilities in sympatric species are not well understood.Here, we explore these issues using genetic mapping in three populations of recombinant inbred lines between naturally hybridizing monkeyflowers Mimulus guttatus and M. nasutus from the sympatric Catherine Creek population.The three M. guttatus founders differ dramatically in admixture history. Comparative genetic mapping also reveals three putative inversions segregating among the M. guttatus founders, two due to admixture. We observe strong, genome-wide transmission ratio distortion, but patterns are highly variable among populations. Some distortion is explained by epistatic selection favoring parental genotypes, but tests of inter-chromosomal linkage disequilibrium also reveal multiple candidate Dobzhansky-Muller incompatibilities. We also map several genetic loci for hybrid fertility, including two interacting pairs coinciding with peaks of distortion.Remarkably, in this limited sample of M. guttatus, we discover abundant segregating variation for hybrid incompatibilities with M. nasutus, suggesting this population harbors diverse contributors to postzygotic isolation. Moreover, even with substantial admixture, hybrid incompatibilities between Mimulus species persist, suggesting postzygotic isolation might be a potent force in maintaining species barriers in this system.

Divergence in drought-response traits between sympatric species of Mimulus.

Differential adaptation to local environmental conditions is thought to be an important driver of speciation. Plants, whose sedentary lifestyle necessitates fine-tuned adaptation to edaphic conditions such as water availability, are often distributed based on these conditions. Populations occupying water-limited habitats may employ a variety of strategies, involving numerous phenotypes, to prevent and withstand desiccation. In sympatry, two closely related Mimulus species-M. guttatus and M. nasutus-occupy distinct microhabitats that differ in seasonal water availability. In a common garden experiment, we characterized natural variation within and between sympatric M. guttatus and M. nasutus in the ability to successfully set seed under well-watered and drought conditions. We also measured key phenotypes for drought adaptation, including developmental timing, plant size, flower size, and stomatal density. Consistent with their microhabitat associations in nature, M. nasutus set seed much more successfully than M. guttatus under water-limited conditions. This divergence in reproductive output under drought was due to differences in mortality after the onset of flowering, with M. nasutus surviving at a much higher rate than M. guttatus. Higher seed set in M. nasutus was mediated, at least in part, by a plastic increase in the rate of late-stage development (i.e., fruit maturation), consistent with the ability of this species to inhabit more ephemeral habitats in the field. Our results suggest adaptation to water availability may be an important factor in species maintenance of these Mimulus taxa in sympatry.