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1. Assortative mating enhances postzygotic barriers to gene flow via ancestry bundling

   https://doi.org/10.1073/pnas.2122179119  

   Muralidhar, Pavitra; Coop, Graham; Veller, Carl (July 2022, Proceedings of the National Academy of Sciences)

   Hybridization and subsequent genetic introgression are now known to be common features of the histories of many species, including our own. Following hybridization, selection often purges introgressed DNA genome-wide. While assortative mating can limit hybridization in the first place, it is also known to play an important role in postzygotic selection against hybrids and, thus, the purging of introgressed DNA. However, this role is usually thought of as a direct one: a tendency for mates to be conspecific reduces the sexual fitness of hybrids, reducing the transmission of introgressed ancestry. Here, we explore a second, indirect role of assortative mating as a postzygotic barrier to gene flow. Under assortative mating, parents covary in their ancestry, causing ancestry to be “bundled” in their offspring and later generations. This bundling effect increases ancestry variance in the population, enhancing the efficiency with which postzygotic selection purges introgressed DNA. Using whole-genome simulations, we show that the bundling effect can comprise a substantial portion of mate choice’s overall effect as a postzygotic barrier to gene flow. We then derive a simple method for estimating the impact of the bundling effect from standard metrics of assortative mating. Applying this method to data from a diverse set of hybrid zones, we find that the bundling effect increases the purging of introgressed DNA by between 1.2-fold (in a baboon system with weak assortative mating) and 14-fold (in a swordtail system with strong assortative mating). Thus, assortative mating’s bundling effect contributes substantially to the genetic isolation of species. 

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2. Sexual selection promotes reproductive isolation in barn swallows

   https://doi.org/10.1126/science.adj8766  

   Schield, Drew R; Carter, Javan K; Scordato, Elizabeth_S C; Levin, Iris I; Wilkins, Matthew R; Mueller, Sarah A; Gompert, Zachariah; Nosil, Patrik; Wolf, Jochen_B W; Safran, Rebecca J (December 2024, Science)

   Despite the well-known effects of sexual selection on phenotypes, links between this evolutionary process and reproductive isolation, genomic divergence, and speciation have been difficult to establish. We unravel the genetic basis of sexually selected plumage traits to investigate their effects on reproductive isolation in barn swallows. The genetic architecture of sexual traits is characterized by 12 loci on two autosomes and the Z chromosome. Sexual trait loci exhibit signatures of divergent selection in geographic isolation and barriers to gene flow in secondary contact. Linkage disequilibrium between these genes has been maintained by selection in hybrid zones beyond what would be expected under admixture alone. Our findings reveal that selection on coupled sexual trait loci promotes reproductive isolation, providing key empirical evidence for the role of sexual selection in speciation. 

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3. Understanding species limits through the formation of phylogeographic lineages

   https://doi.org/10.1002/ece3.70263  

   Burbrink, Frank T; Myers, Edward A; Pyron, R Alexander (October 2024, Ecology and Evolution)

   Abstract The outcomes of speciation across organismal dimensions (e.g., ecological, genetic, phenotypic) are often assessed using phylogeographic methods. At one extreme, reproductively isolated lineages represent easily delimitable species differing in many or all dimensions, and at the other, geographically distinct genetic segments introgress across broad environmental gradients with limited phenotypic disparity. In the ambiguous gray zone of speciation, where lineages are genetically delimitable but still interacting ecologically, it is expected that these lineages represent species in the context of ontology and the evolutionary species concept when they are maintained over time with geographically well‐defined hybrid zones, particularly at the intersection of distinct environments. As a result, genetic structure is correlated with environmental differences and not space alone, and a subset of genes fail to introgress across these zones as underlying genomic differences accumulate. We present a set of tests that synthesize species delimitation with the speciation process. We can thereby assess historical demographics and diversification processes while understanding how lineages are maintained through space and time by exploring spatial and genome clines, genotype‐environment interactions, and genome scans for selected loci. Employing these tests in eight lineage‐pairs of snakes in North America, we show that six pairs represent 12 “good” species and that two pairs represent local adaptation and regional population structure. The distinct species pairs all have the signature of divergence before or near the mid‐Pleistocene, often with low migration, stable hybrid zones of varying size, and a subset of loci showing selection on alleles at the hybrid zone corresponding to transitions between distinct ecoregions. Locally adapted populations are younger, exhibit higher migration, and less ecological differentiation. Our results demonstrate that interacting lineages can be delimited using phylogeographic and population genetic methods that properly integrate spatial, temporal, and environmental data. 

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4. Pollinator and habitat-mediated selection as potential contributors to ecological speciation in two closely related species

   https://doi.org/10.1093/evlett/qrad060  

   Campbell, Diane R; Powers, John M; Crowell, Madison (November 2023, Evolution Letters)

   Abstract In ecological speciation, incipient species diverge due to natural selection that is ecologically based. In flowering plants, different pollinators could mediate that selection (pollinator-mediated divergent selection) or other features of the environment that differ between habitats of 2 species could do so (environment-mediated divergent selection). Although these mechanisms are well understood, they have received little rigorous testing, as few studies of divergent selection across sites of closely related species include both floral traits that influence pollination and vegetative traits that influence survival. This study employed common gardens in sites of the 2 parental species and a hybrid site, each containing advanced generation hybrids along with the parental species, to test these forms of ecological speciation in plants of the genus Ipomopsis. A total of 3 vegetative traits (specific leaf area, leaf trichomes, and photosynthetic water-use efficiency) and 5 floral traits (corolla length and width, anther insertion, petal color, and nectar production) were analyzed for impacts on fitness components (survival to flowering and seeds per flower, respectively). These traits exhibited strong clines across the elevational gradient in the hybrid zone, with narrower clines in theory reflecting stronger selection or higher genetic variance. Plants with long corollas and inserted anthers had higher seeds per flower at the Ipomopsis tenuituba site, whereas selection favored the reverse condition at the Ipomopsis aggregata site, a signature of divergent selection. In contrast, no divergent selection due to variation in survival was detected on any vegetative trait. Selection within the hybrid zone most closely resembled selection within the I. aggregata site. Across traits, the strength of divergent selection was not significantly correlated with width of the cline, which was better predicted by evolvability (standardized genetic variance). These results support the role of pollinator-­mediated divergent selection in ecological speciation and illustrate the importance of genetic variance in determining divergence across hybrid zones. 

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5. Replicate geographic transects across a hybrid zone reveal parallelism and differences in the genetic architecture of reproductive isolation

   https://doi.org/10.1093/evlett/qraf009  

   Semenov, Georgy; Kenyon, Haley; Funk, Erik; Anderson, William; McQuillan, Michael; Spinelli, Joan; Russell, Austin; Martinez, Noel; Van_Huynh, Alex; Alexander, Alana; et al (May 2025, Evolution Letters)

   Abstract Determining the genetic architecture of traits involved in adaptation and speciation is one of the key components of understanding the evolutionary mechanisms behind biological diversification. Hybrid zones provide a unique opportunity to use genetic admixture to identify traits and loci contributing to partial reproductive barriers between taxa. Many studies have focused on the temporal dynamics of hybrid zones, but geographical variation in hybrid zones that span distinct ecological contexts has received less attention. We address this knowledge gap by analyzing hybridization and introgression between black-capped and Carolina chickadees in two geographically remote transects across their extensive hybrid zone, one located in eastern and one in central North America. Previous studies demonstrated that this hybrid zone is moving northward as a result of climate change but is staying consistently narrow due to selection against hybrids. In addition, the hybrid zone is moving ~5× slower in central North America compared to more eastern regions, reflecting continent-wide variation in the rate of climate change. We use whole genome sequencing of 259 individuals to assess whether variation in the rate of hybrid zone movement is reflected in patterns of hybridization and introgression, and which genes and genomic regions show consistently restricted introgression in distinct ecological contexts. Our results highlight substantial similarities between geographically remote transects and reveal large Z-linked chromosomal rearrangements that generate measurable differences in the degree of gene flow between transects. We further use simulations and analyses of climatic data to examine potential factors contributing to continental-scale nuances in selection pressures. We discuss our findings in the context of speciation mechanisms and the importance of sex chromosome inversions in chickadees and other species. 

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