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Understanding how organisms adapt to changing environments is a core focus of research in evolutionary biology. One common mechanism is adaptive introgression, which has received increasing attention as a potential route to rapid adaptation in populations struggling in the face of ecological change, particularly global climate change. However, hybridization can also result in deleterious genetic interactions that may limit the benefits of adaptive introgression. Here, we used a combination of genome-wide quantitative trait locus mapping and differential gene expression analyses between the swordtail fish species Xiphophorus malinche and X. birchmanni to study the consequences of hybridization on thermotolerance. While these two species are adapted to different thermal environments, we document a complicated architecture of thermotolerance in hybrids. We identify a region of the genome that contributes to reduced thermotolerance in individuals heterozygous for X. malinche and X. birchmanni ancestry, as well as widespread misexpression in hybrids of genes that respond to thermal stress in the parental species, particularly in the circadian clock pathway. We also show that a previously mapped hybrid incompatibility between X. malinche and X. birchmanni contributes to reduced thermotolerance in hybrids. Together, our results highlight the challenges of understanding the impact of hybridization on complex ecological traits and its potential impact on adaptive introgression.

Natural hybridization events provide unique windows into the barriers that keep species apart as well as the consequences of their breakdown. Here we characterize hybrid populations formed between the northern swordtail fishXiphophorus corteziandX. birchmannifrom collection sites on two rivers. We develop sensitive and accurate local ancestry calling for this system based on low coverage whole genome sequencing. Strikingly, we find that hybrid populations on both rivers consist of two genetically distinct subpopulations: a cluster of nearly pureX. birchmanniindividuals and one of phenotypically intermediate hybrids that derive ~85-90% of their genome fromX. cortezi. Simulations and empirical data suggest that at both sites initial hybridization occurred ~150 generations ago, with little evidence for contemporary gene flow between subpopulations, likely due to strong assortative mating. The patterns of population structure uncovered here mirror those seen in hybridization betweenX. birchmanniand its sister species,X. malinche. Future comparisons will provide a window into the repeatability of the outcomes of hybridization not only across independent hybridization events between the same species but also across distinct species pairs.

Biologists since Darwin have been fascinated by the evolution of sexually selected ornaments, particularly those that reduce viability. Uncovering the genetic architecture of these traits is key to understanding how they evolve and are maintained. Here, we investigate the genetic architecture of a sexually selected ornament, the “sword” fin extension that characterizes many species of swordtail fish (Xiphophorus). Using sworded and swordless sister species ofXiphophorus, we generated a mapping population and show that the sword ornament is polygenic – with ancestry across the genome explaining substantial variation in the trait. After accounting for the impacts of genome-wide ancestry, we identify one major effect QTL that explains ∼5% of the overall variation in the trait. Using a series of approaches, we narrow this large QTL interval to a handful of likely candidate genes, including the genesp8. Notably,sp8plays a regulatory role in fin regeneration and harbors several derived substitutions that are predicted to impact protein function in the species that has lost the sword ornament. Furthermore, we find evidence of selection on ancestry atsp8in four natural hybrid populations, consistent with selection against the sword in these populations.