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Abstract 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 guttatusandMimulus nasutus,from the sympatric Catherine Creek population. We discover that the threeM. guttatusfounders differ dramatically in admixture history, with nearly a quarter of one founder's genome introgressed fromM. nasutus. Comparative genetic mapping in the three RIL populations reveals three new putative inversions, each one segregating among theM. guttatusfounders, 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 threeM. guttatuslines, we discover abundant segregating variation for hybrid incompatibilities withM. nasutus,suggesting this population harbours diverse contributors to postzygotic isolation. Moreover, even with substantial admixture, hybrid incompatibilities betweenMimulusspecies persist, suggesting postzygotic isolation might be a potent force in maintaining species barriers in this system.
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This content will become publicly available on March 31, 2026
Fluctuating reproductive isolation and stable ancestry structure in a fine-scaled mosaic of hybridizing Mimulus monkeyflowers
Hybridization among taxa impacts a variety of evolutionary processes from adaptation to extinction. We seek to understand both patterns of hybridization across taxa and the evolutionary and ecological forces driving those patterns. To this end, we use whole-genome low-coverage sequencing of 458 wild-grown and 1565 offspring individuals to characterize the structure, stability, and mating dynamics of admixed populations ofMimulus guttatusandMimulus nasutusacross a decade of sampling. In three streams, admixed genomes are common and aM. nasutusorganellar haplotype is fixed inM. guttatus,but new hybridization events are rare. Admixture is strongly unidirectional, but each stream has a unique distribution of ancestry proportions. In one stream, three distinct cohorts of admixed ancestry are spatially structured at ~20-50m resolution and stable across years. Mating system provides almost complete isolation ofM. nasutusfrom bothM. guttatusand admixed cohorts,and is a partial barrier between admixed andM. guttatuscohorts. Isolation due to phenology is near-complete betweenM. guttatusandM. nasutus.Phenological isolation is a strong barrier in some years between admixed andM. guttatuscohorts, but a much weaker barrier in other years, providing a potential bridge for gene flow. These fluctuations are associated with differences in water availability across years, supporting a role for climate in mediating the strength of reproductive isolation. Together, mating system and phenology accurately predict fluctuations in assortative mating across years, which we estimate directly using paired maternal and offspring genotypes. Climate-driven fluctuations in reproductive isolation may promote the longer-term stability of a complex mosaic of hybrid ancestry, preventing either complete isolation or complete collapse of species barriers.
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- Award ID(s):
- 1856180
- PAR ID:
- 10610200
- Editor(s):
- Lasky, Jesse
- Publisher / Repository:
- PLoS Genetics
- Date Published:
- Journal Name:
- PLOS Genetics
- Volume:
- 21
- Issue:
- 3
- ISSN:
- 1553-7404
- Page Range / eLocation ID:
- e1011624
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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