Mantel, S. J. | Search bioRxiv

bioRxiv2023

Postzygotic barriers persist despite ongoing introgression in hybridizing Mimulus species

O_LIThe 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. C_LIO_LIHere, 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. C_LIO_LIThe 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. C_LIO_LIRemarkably, 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. C_LI

genetics↗

bioRxiv2023

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 two 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 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 inter-chromosomal linkage disequilibrium in both F2s and RILs identified a novel two-locus genic incompatibility causing sex-independent gametophytic (haploid) lethality. The latter interaction eliminated three of the expected nine 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.

genetics↗