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Hybridization between species is widespread across the tree of life. As a result, many species, including our own, harbor regions of their genome derived from hybridization. Despite the recognition that this process is widespread, we understand little about how the genome stabilizes following hybridization, and whether the mechanisms driving this stabilization tend to be shared across species. Here, we dissect the drivers of variation in local ancestry across the genome in replicated hybridization events between two species pairs of swordtail fish: Xiphophorus birchmanni × X . cortezi and X . birchmanni × X . malinche . We find unexpectedly high levels of repeatability in local ancestry across the two types of hybrid populations. This repeatability is attributable in part to the fact that the recombination landscape and locations of functionally important elements play a major role in driving variation in local ancestry in both types of hybrid populations. Beyond these broad scale patterns, we identify dozens of regions of the genome where minor parent ancestry is unusually low or high across species pairs. Analysis of these regions points to shared sites under selection across species pairs, and in some cases, shared mechanisms of selection. We show that one such region is a previously unknown hybrid incompatibility that is shared across X . birchmanni × X . cortezi and X . birchmanni × X . malinche hybrid populations.

Hybridization is increasingly being recognized as a common process in both animal and plant species. Negative epistatic interactions between genes from different parental genomes decrease the fitness of hybrids and can limit gene flow between species. However, little is known about the number and genome-wide distribution of genetic incompatibilities separating species. To detect interacting genes, we perform a high-resolution genome scan for linkage disequilibrium between unlinked genomic regions in naturally occurring hybrid populations of swordtail fish. We estimate that hundreds of pairs of genomic regions contribute to reproductive isolation between these species, despite them being recently diverged. Many of these incompatibilities are likely the result of natural or sexual selection on hybrids, since intrinsic isolation is known to be weak. Patterns of genomic divergence at these regions imply that genetic incompatibilities play a significant role in limiting gene flow even in young species. In nature, closely related species often interbreed to produce hybrids. However, hybrids are often less fertile or unable to compete with parent species, making them less likely to thrive in the wild. When the genomes of two different species are mixed, versions of genes that are meant to work together can become separated, which means that these genes do not work as well as they should. This reduces the hybrids' chances of survival, and a poor survival rate of hybrids is one barrier that keeps different species distinct, even though the species can interbreed. Two species of swordtail fish live in the rivers in Mexico, and although they mostly live in different stretches of these rivers, the two species interbreed to produce hybrids in the regions where they overlap. These hybrids can outnumber the parental species in these ‘hybrid zones’, but the two species have remained separate in other parts of the rivers. Though some genetic incompatibilities that might keep the species distinct have previously been suggested, it is not known how many incompatibilities there are in these fish's genomes. Schumer et al. have searched the genomes of wild hybrids between these species and found hundreds of genetic incompatibilities. These were identified by looking for species-specific pairs of genes that are found together more often than would be expected if there were no selection against hybrids. It is likely that many of these incompatibilities reduce the evolutionary fitness of the hybrid fish and Schumer et al. suggest that many could be the result of environmental pressures and the fish's mating preferences. Furthermore, Schumer et al. demonstrate that genes close to identified incompatibilities are more different between species, on average, than genes that are further away. When there is on-going interbreeding between two the species (as is the case with the swordtails), this finding is expected only if these incompatibilities reduce the hybrids' chances of finding mates or surviving. The findings of Schumer et al. demonstrate how conflicts in the genomes of two species allow these species to remain distinct even when they live in overlapping environments and frequently interbreed. Future work will investigate how these genetic incompatibilities shape the hybrid populations that are found in the wild; and which incompatibilities are caused by poor survival of the hybrids or by the fish's mating preferences selecting against the hybrids.

Mate choice is context dependent, but the importance of current context to interspecific mating and hybridization is largely unexplored. An important influence on mate choice is predation risk. We investigated how variation in an indirect cue of predation risk, distance to shelter, influences mate choice in the swordtail Xiphophorus birchmanni, a species which sometimes hybridizes with X. malinche in the wild. We conducted mate choice experiments to determine whether females attend to the distance to shelter and whether this cue of predation risk can counteract female preference for conspecifics. Females were sensitive to shelter distance independent of male presence. When conspecific and heterospecific X. malinche males were in equally risky habitats (i.e., equally distant from shelter), females associated primarily with conspecifics, suggesting an innate preference for conspecifics. However, when heterospecific males were in less risky habitat (i.e., closer to shelter) than conspecific males, females no longer exhibited a preference, suggesting that females calibrate their mate choices in response to predation risk. Our findings illustrate the potential for hybridization to arise, not necessarily through reproductive \"mistakes\", but as one of many potential outcomes of a context-dependent mate choice strategy.

Determining the costs of sexual ornaments is complicated by the fact that ornaments are often integrated with other, non-sexual traits, making it difficult to dissect the effect of ornaments independent of other aspects of the phenotype. Hybridization can produce reduced phenotypic integration, allowing one to evaluate performance across a broad range of multivariate trait values. Here we assess the relationship between morphology and performance in the swordtails Xiphophorus malinche and X. birchmanni, two naturally-hybridizing fish species that differ extensively in non-sexual as well as sexual traits. We took advantage of novel trait variation in hybrids to determine if sexual ornaments incur a cost in terms of locomotor ability. For both fast-start and endurance swimming, hybrids performed at least as well as the two parental species. The sexually-dimorphic sword did not impair swimming performance per se. Rather, the sword negatively affected performance only when paired with a sub-optimal body shape. Studies seeking to quantify the costs of ornaments should consider that covariance with non-sexual traits may create the spurious appearance of costs.

Determining the costs of sexual ornaments is complicated by the fact that ornaments are often integrated with other, non-sexual traits, making it difficult to dissect the effect of ornaments independent of other aspects of the phenotype. Hybridization can produce reduced phenotypic integration, allowing one to evaluate performance across a broad range of multivariate trait values. Here we assess the relationship between morphology and performance in the swordtails Xiphophorus malinche and X. birchmanni, two naturally-hybridizing fish species that differ extensively in non-sexual as well as sexual traits. We took advantage of novel trait variation in hybrids to determine if sexual ornaments incur a cost in terms of locomotor ability. For both fast-start and endurance swimming, hybrids performed at least as well as the two parental species. The sexually-dimorphic sword did not impair swimming performance per se. Rather, the sword negatively affected performance only when paired with a sub-optimal body shape. Studies seeking to quantify the costs of ornaments should consider that covariance with non-sexual traits may create the spurious appearance of costs.

Although private communication is considered an important diversifying force in evolution, there is little direct behavioural evidence to support this notion. Here, we show that ultraviolet (UV) signalling in northern swordtails (Xiphophorus) affords a channel for communication that is not accessible to their major predator, Astyanax mexicanus, the Mexican tetra. Laboratory and field behavioural experiments with swordtails (X. nigrensis) and predators (A. mexicanus) demonstrate that male UV ornamentation significantly increases their attractiveness to females but not to this predator, which is less sensitive to UV. UV reflectance among swordtail species correlates positively with tetra densities across habitats, and visual contrast estimates suggest that UV signals are highly conspicuous to swordtails in their natural environment. Cross-species comparisons also support the hypothesis that natural selection drives the use of UV communication. We compared two species, one with high (X. nigrensis) and one with low (X. malinche) Mexican tetra densities. Xiphophorus nigrensis males reflect significantly more UV than X. malinche, exhibit significant UV sexual dimorphism, and UV is a salient component of the sexual communication system. In X. malinche, however, males reflect minimally in the UV, there is no UV sexual dimorphism, and UV does not play a part in its communication system.

Paracreptotremarosenthali sp. n. was discovered in the intestine of Xiphophorusmalinche and Pseudoxiphophorusjonesii, collected from the headwaters of Río Malila, tributary of Río Conzintla, in the Río Pánuco basin, Hidalgo, México, during 2008-2009. The new species differs from the five known species of Paracreptotrema Choudhury, Pérez-Ponce de León, Brooks & Daverdin, 2006 by having vitelline follicles that extend from a level anterior to the pharynx to mid-testes, the seminal vesicle which is more extensively folded, and a wider cirrus sac. The new species resembles Paracreptotremaheterandriae in the length of its ceca, which surpasses the posterior margin of the ovary but do not reach the testes. A key to the species of Paracreptotrema is provided.

AbstractMale and female mate preferences have the potential to influence one another, and such interactions could help explain variation in female mate preferences. In Xiphophorus malinche, larger females prefer asymmetrical males while smaller females prefer symmetrical males. We used a two-part preference test to determine if there were differences in mate preferences between symmetrical and asymmetrical males for female size that could influence female mate preference. We found no significant difference between symmetrical and asymmetrical male's preferences. A preference for large female size was detected during the time males directly interacted with females and in standard dichotomous choice tests that followed, as long as the males had been isolated less than 30 days. We did detect variation in male preference for female size depending on male size and the amount of time a male was isolated. These results suggest that variation in male mate preference is not likely to have produced the difference in female preference for symmetry between large and small females, but should be considered where females vary in their preference for male size. In addition, our results suggest that males may shift their preferences from large to small females depending on time since last mating opportunity.

How organisms adapt to diverse environments is a foundational question in evolutionary biology. In addition to directly adapting to ecological conditions, organisms have evolved diverse reproductive strategies that impact the probability that their offspring survive to adulthood. Here, we describe divergence in reproductive strategy between two closely-related species of swordtail fish (Xiphophorus). Swordtail fish and their relatives have evolved viviparity: they have internal fertilization and give birth to fully developed fry. We find that one species, X. malinche, which lives in high-elevation environments, has evolved larger offspring than its closest relative X. birchmanni and dwarfs the offspring size of other species in the genus. The larger fry of X. malinche are more resilient to starvation than their X. birchmanni relatives, hinting that the evolution of large offspring size may be an adaptation to the particularly challenging environments in which X. malinche are born. We find that X. malinche achieves larger offspring size in part by continuing to provision their offspring over the course of embryonic development after fertilization, the first time this process has been documented in the Xiphophorus genus. Moreover, we observe differential regulation in the ovary of genes associated with post-fertilization nutrient provisioning in other species that use this reproductive strategy. These reproductive differences may drive an asymmetric hybrid incompatibility, since X. birchmanni mothers pregnant with F1 embryos give birth to premature and stillborn fry at an exceptionally high rate.Competing Interest StatementThe authors have declared no competing interest.Footnotes* https://github.com/cypayne/swordtail-offspring-size

The Xiphophorus genus has long been studied for its development of melanoma. xmrk has been identified as a potent oncogene. The recent discovery of adgre5 as a candidate tumor regulator gene in naturally hybridizing Xiphophorus birchmanni and X. malinche has shed new light on the genetic basis of melanoma. This study aimed to functionally test the role of the adgre5 alleles from each hybridizing species by analyzing their effect independently on cell growth and migration in vitro and melanoma development in vivo. In vitro experiments showed that cells with the X. birchmanni allele grew and migrated slower than those with the X. malinche allele. In vivo experiments using transgenic medaka confirmed that melanoma development was only inhibited in the presence of the X. birchmanni allele of adgre5. These findings provide new insights into the genetic basis of melanoma development in Xiphophorus and highlight the importance of adgre5 as a potential therapeutic target for the treatment of melanoma.Competing Interest StatementThe authors have declared no competing interest.