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1. Genetics and the Evolution of Prezygotic Isolation

   https://doi.org/10.1101/cshperspect.a041439  

   Merrill, Richard M.; Arenas-Castro, Henry; Feller, Anna F.; Harenčár, Julia; Rossi, Matteo; Streisfeld, Matthew A.; Kay, Kathleen M. (February 2024, Cold Spring Harbor Perspectives in Biology)

   The significance of prezygotic isolation for speciation has been recognized at least since the Modern Synthesis. However, fundamental questions remain. For example, how are genetic associations between traits that contribute to prezygotic isolation maintained? What is the source of genetic variation underlying the evolution of these traits? And how do prezygotic barriers affect patterns of gene flow? We address these questions by reviewing genetic features shared across plants and animals that influence prezygotic isolation. Emerging technologies increasingly enable the identification and functional characterization of the genes involved, allowing us to test established theoretical expectations. Embedding these genes in their developmental context will allow further predictions about what constrains the evolution of prezygotic isolation. Ongoing improvements in statistical and computational tools will reveal how pre- and postzygotic isolation may differ in how they influence gene flow across the genome. Finally, we highlight opportunities for progress by combining theory with appropriate data. 

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2. Genetic Basis of Reproductive Isolation in Torrey Pine ( Pinus torreyana Parry): Insights From Hybridization and Adaptation

   https://doi.org/10.1111/eva.70094  

   Di_Santo, Lionel_N; Mead, Alayna; Wright, Jessica_W; Hamilton, Jill_A (March 2025, Evolutionary Applications)

   ABSTRACT Tree species are often locally adapted to their environments, but the extent to which environmental adaptation contributes to incipient speciation is unclear. One of the rarest pines in the world, Torrey pine (Pinus torreyanaParry), persists naturally across one island and one mainland population in southern California. The two populations are morphologically and genetically differentiated but experience some connectivity, making it an ideal system for assessing the evolution of reproductive isolation. Previous work has found evidence of heterosis in F1 mainland‐island hybrids, suggesting genetic rescue could be beneficial in the absence of reproductive barriers. Using ddRADseq and GWAS for a common garden experiment of island, mainland, and F1 individuals, we identified candidate loci for environmentally driven reproductive isolation, their function, and their relationship to fitness proxies. By simulating neutral evolution and admixture between the two populations, we identified loci that exhibited reduced heterozygosity in the F1s, evidence of selection against admixture. SNPs with reduced F1 heterozygosity were enriched for growth and pollination functions, suggesting genetic variants that could be involved in the evolution of reproductive barriers between populations. One locus with reduced F1 heterozygosity exhibited strong associations with growth and reproductive fitness proxies in the common garden, with the mainland allele conferring increased fitness. If this locus experiences divergent selection in the two natural populations, it could promote their reproductive isolation. Finally, although hybridization largely reduced allele fixation in the F1s initially, indicating heterosis is likely due to the masking of deleterious alleles, the emergence of reproductive isolation between populations may diminish the longer‐term benefits of genetic rescue in F2 or advanced‐generation hybrids. As Torrey pine is a candidate for interpopulation genetic rescue, caution is warranted where longer‐term gene flow between diverged populations may result in reduced fitness if barriers have evolved. 

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3. Strong postmating reproductive isolation in Mimulus section Eunanus

   https://doi.org/10.1111/jeb.14219  

   Farnitano, Matthew C.; Sweigart, Andrea L. (October 2023, Journal of Evolutionary Biology)

   Abstract Postmating reproductive isolation can help maintain species boundaries when premating barriers to reproduction are incomplete. The strength and identity of postmating reproductive barriers are highly variable among diverging species, leading to questions about their genetic basis and evolutionary drivers. These questions have been tackled in model systems but are less often addressed with broader phylogenetic resolution. In this study we analyse patterns of genetic divergence alongside direct measures of postmating reproductive barriers in an overlooked group of sympatric species within the model monkeyflower genus, Mimulus. Within this Mimulus brevipes species group, we find substantial divergence among species, including a cryptic genetic lineage. However, rampant gene discordance and ancient signals of introgression suggest a complex history of divergence. In addition, we find multiple strong postmating barriers, including postmating prezygotic isolation, hybrid seed inviability and hybrid male sterility. M. brevipes and M. fremontii have substantial but incomplete postmating isolation. For all other tested species pairs, we find essentially complete postmating isolation. Hybrid seed inviability appears linked to differences in seed size, providing a window into possible developmental mechanisms underlying this reproductive barrier. While geographic proximity and incomplete mating isolation may have allowed gene flow within this group in the distant past, strong postmating reproductive barriers today have likely played a key role in preventing ongoing introgression. By producing foundational information about reproductive isolation and genomic divergence in this understudied group, we add new diversity and phylogenetic resolution to our understanding of the mechanisms of plant speciation. Abstract Hybrid seed inviability and other postmating reproductive barriers isolate species in Mimulus section Eunanus. Variation in seed size may help explain hybrid seed failure. Whole-genome sequencing indicates a complex history of divergence, including signals of ancient introgression and cryptic diversity. 

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4. Do genetic loci that cause reproductive isolation in the lab inhibit gene flow in nature?

   https://doi.org/10.1093/evolut/qpae044  

   Frayer, Megan_E; Payseur, Bret_A; Linnen, ed., Catherine; Wolf, ed., Jason (March 2024, Evolution)

   Abstract The genetic dissection of reproductive barriers between diverging lineages provides enticing clues into the origin of species. One strategy uses linkage analysis in experimental crosses to identify genomic locations involved in phenotypes that mediate reproductive isolation. A second framework searches for genomic regions that show reduced rates of exchange across natural hybrid zones. It is often assumed that these approaches will point to the same loci, but this assumption is rarely tested. In this perspective, we discuss the factors that determine whether loci connected to postzygotic reproductive barriers in the laboratory are inferred to reduce gene flow in nature. We synthesize data on the genetics of postzygotic isolation in house mice, one of the most intensively studied systems in speciation genetics. In a rare empirical comparison, we measure the correspondence of loci tied to postzygotic barriers via genetic mapping in the laboratory and loci at which gene flow is inhibited across a natural hybrid zone. We find no evidence that the two sets of loci overlap beyond what is expected by chance. In light of these results, we recommend avenues for empirical and theoretical research to resolve the potential incongruence between the two predominant strategies for understanding the genetics of speciation. 

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5. Postzygotic barriers persist despite ongoing introgression in hybridizing Mimulus species

   https://doi.org/10.1111/mec.17261  

   Mantel, Samuel J.; Sweigart, Andrea L. (January 2024, Molecular Ecology)

   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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