Molly Schumer, Postdoctoral Faculty Sponsor
Predictability and parallelism in the contemporary evolution of hybrid genomes.
1800; 18 (1): e1009914
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.
View details for DOI 10.1371/journal.pgen.1009914
View details for PubMedID 35085234
Two new hybrid populations expand the swordtail hybridization model system.
Evolution; international journal of organic evolution
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 fish Xiphophorus cortezi and X. birchmanni from collection sites on two rivers. We use simulations and new genetic reference panels to develop sensitive and accurate local ancestry calling in this novel system. Strikingly, we find that hybrid populations on both rivers consist of two genetically distinct subpopulations: a cluster of pure X. birchmanni individuals and one of phenotypically intermediate hybrids that derive 85-90% of their genome from X. cortezi. Simulations suggest that initial hybridization occurred 150 generations ago at both sites, with little evidence for contemporary gene flow between subpopulations. This population structure is consistent with strong assortative mating between individuals of similar ancestry. The patterns of population structure uncovered here mirror those seen in hybridization between X. birchmanni and its sister species, X. malinche, indicating an important role for assortative mating in the evolution of hybrid populations. Future comparisons will provide a window into the shared mechanisms driving the outcomes of hybridization not only among independent hybridization events between the same species but also across distinct species pairs. This article is protected by copyright. All rights reserved.
View details for DOI 10.1111/evo.14337
View details for PubMedID 34460102
The genomic consequences of hybridization.
In the past decade, advances in genome sequencing have allowed researchers to uncover the history of hybridization in diverse groups of species, including our own. Although the field has made impressive progress in documenting the extent of natural hybridization, both historical and recent, there are still many unanswered questions about its genetic and evolutionary consequences. Recent work has suggested that the outcomes of hybridization in the genome may be in part predictable, but many open questions about the nature of selection on hybrids and the biological variables that shape such selection have hampered progress in this area. We synthesize what is known about the mechanisms that drive changes in ancestry in the genome after hybridization, highlight major unresolved questions, and discuss their implications for the predictability of genome evolution after hybridization.
View details for DOI 10.7554/eLife.69016
View details for PubMedID 34346866
The Genetic Architecture of Variation in the Sexually Selected Sword Ornament and Its Evolution in Hybrid Populations.
Current biology : CB
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 and evolutionary loss of a sexually selected ornament, the "sword" fin extension that characterizes many species of swordtail fish (Xiphophorus). Using sworded and swordless sister species of Xiphophorus, 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 quantitative trait locus (QTL) that explains ~5% of the overall variation in the trait. Using a series of approaches, we narrow this large QTL interval to several likely candidate genes, including genes involved in fin regeneration and growth. Furthermore, we find evidence of selection on ancestry at one of these candidates in four natural hybrid populations, consistent with selection against the sword in these populations.
View details for DOI 10.1016/j.cub.2020.12.049
View details for PubMedID 33513352
Natural hybridization reveals incompatible alleles that cause melanoma in swordtail fish.
Science (New York, N.Y.)
2020; 368 (6492): 731–36
The establishment of reproductive barriers between populations can fuel the evolution of new species. A genetic framework for this process posits that "incompatible" interactions between genes can evolve that result in reduced survival or reproduction in hybrids. However, progress has been slow in identifying individual genes that underlie hybrid incompatibilities. We used a combination of approaches to map the genes that drive the development of an incompatibility that causes melanoma in swordtail fish hybrids. One of the genes involved in this incompatibility also causes melanoma in hybrids between distantly related species. Moreover, this melanoma reduces survival in the wild, likely because of progressive degradation of the fin. This work identifies genes underlying a vertebrate hybrid incompatibility and provides a glimpse into the action of these genes in natural hybrid populations.
View details for DOI 10.1126/science.aba5216
View details for PubMedID 32409469
Versatile simulations of admixture and accurate local ancestry inference with mixnmatch and ancestryinfer.
Molecular ecology resources
It has become clear that hybridization between species is much more common than previously recognized. As a result, we now know that the genomes of many modern species, including our own, are a patchwork of regions derived from past hybridization events. Increasingly researchers are interested in disentangling which regions of the genome originated from each parental species using local ancestry inference methods. Due to the diverse effects of admixture, this interest is shared across disparate fields, from human genetics to research in ecology and evolutionary biology. However, local ancestry inference methods are sensitive to a range of biological and technical parameters which can impact accuracy. Here we present paired simulation and ancestry inference pipelines, mixnmatch and ancestryinfer, to help researchers plan and execute local ancestry inference studies. mixnmatch can simulate arbitrarily complex demographic histories in the parental and hybrid populations, selection on hybrids, and technical variables such as coverage and contamination. ancestryinfer takes as input sequencing reads from simulated or real individuals, and implements an efficient local ancestry inference pipeline. We perform a series of simulations with mixnmatch to pinpoint factors that influence accuracy in local ancestry inference and highlight useful features of the two pipelines. mixnmatch is a powerful tool for simulations of hybridization while ancestryinfer facilitates local ancestry inference on real or simulated data.
View details for DOI 10.1111/1755-0998.13175
View details for PubMedID 32324964
Testing Wallace's intuition: water type, reproductive isolation and divergence in an Amazonian fish
JOURNAL OF EVOLUTIONARY BIOLOGY
2018; 31 (6): 882–92
Alfred Russel Wallace proposed classifying Amazon rivers based on their colour and clarity: white, black and clear water. Wallace also proposed that black waters could mediate diversification and yield distinct fish species. Here, we bring evidence of speciation mediated by water type in the sailfin tetra (Crenuchus spilurus), a fish whose range encompasses rivers of very distinct hydrochemical conditions. Distribution of the two main lineages concords with Wallace's water types: one restricted to the acidic and nutrient-poor waters of the Negro River (herein Rio Negro lineage) and a second widespread throughout the remaining of the species' distribution (herein Amazonas lineage). These lineages occur over a very broad geographical range, suggesting that despite occurring in regions separated by thousands of kilometres, individuals of the distinct lineages fail to occupy each other's habitats, hundreds of metres apart and not separated by physical barrier. Reproductive isolation was assessed in isolated pairs exposed to black-water conditions. All pairs with at least one individual of the lineage not native to black waters showed significantly lower spawning success, suggesting that the water type affected the fitness and contributed to reproductive isolation. Our results endorse Wallace's intuition and highlight the importance of ecological factors in shaping diversity of the Amazon fish fauna.
View details for DOI 10.1111/jeb.13272
View details for Web of Science ID 000434358800009
View details for PubMedID 29577482
Natural selection interacts with recombination to shape the evolution of hybrid genomes
2018; 360 (6389): 656–59
To investigate the consequences of hybridization between species, we studied three replicate hybrid populations that formed naturally between two swordtail fish species, estimating their fine-scale genetic map and inferring ancestry along the genomes of 690 individuals. In all three populations, ancestry from the "minor" parental species is more common in regions of high recombination and where there is linkage to fewer putative targets of selection. The same patterns are apparent in a reanalysis of human and archaic admixture. These results support models in which ancestry from the minor parental species is more likely to persist when rapidly uncoupled from alleles that are deleterious in hybrids. Our analyses further indicate that selection on swordtail hybrids stems predominantly from deleterious combinations of epistatically interacting alleles.
View details for DOI 10.1126/science.aar3684
View details for Web of Science ID 000431790900046
View details for PubMedID 29674434
View details for PubMedCentralID PMC6069607
Assortative mating and persistent reproductive isolation in hybrids
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2017; 114 (41): 10936–41
The emergence of new species is driven by the establishment of mechanisms that limit gene flow between populations. A major challenge is reconciling the theoretical and empirical importance of assortative mating in speciation with the ease with which it can fail. Swordtail fish have an evolutionary history of hybridization and fragile prezygotic isolating mechanisms. Hybridization between two swordtail species likely arose via pollution-mediated breakdown of assortative mating in the 1990s. Here we track unusual genetic patterns in one hybrid population over the past decade using whole-genome sequencing. Hybrids in this population formed separate genetic clusters by 2003, and maintained near-perfect isolation over 25 generations through strong ancestry-assortative mating. However, we also find that assortative mating was plastic, varying in strength over time and disappearing under manipulated conditions. In addition, a nearby population did not show evidence of assortative mating. Thus, our findings suggest that assortative mating may constitute an intermittent and unpredictable barrier to gene flow, but that variation in its strength can have a major effect on how hybrid populations evolve. Understanding how reproductive isolation varies across populations and through time is critical to understanding speciation and hybridization, as well as their dependence on disturbance.
View details for DOI 10.1073/pnas.1711238114
View details for Web of Science ID 000412653900060
View details for PubMedID 28973863
View details for PubMedCentralID PMC5642718
What artifice can and cannot tell us about animal behavior
2017; 63 (1): 21–26
Artifice-the manipulation of social and environmental stimuli-is fundamental to research in animal behavior. State-of-the-art techniques have been developed to generate and present complex visual stimuli. These techniques have unique strengths and limitations. However, many of the issues with synthetic animation and virtual reality are common to playback experiments in general, including those using unmanipulated video or auditory stimuli. Playback experiments, in turn, fall into the broader category of experiments that artificially manipulate the array of stimuli experienced by a subject. We argue that the challenges of designing and interpreting experiments using virtual reality or synthetic animations are largely comparable to those of studies using older technologies or addressing other modalities, and that technology alone is unlikely to solve these challenges. We suggest that appropriate experimental designs are the key to validating behavioral responses to artificial stimuli and to interpreting all studies using artifice, including those that present complex visual displays.
View details for DOI 10.1093/cz/zow091
View details for Web of Science ID 000396213400003
View details for PubMedID 29491959
View details for PubMedCentralID PMC5804151
Ancient hybridization and genomic stabilization in a swordtail fish
2016; 25 (11): 2661–79
A rapidly increasing body of work is revealing that the genomes of distinct species often exhibit hybrid ancestry, presumably due to postspeciation hybridization between closely related species. Despite the growing number of documented cases, we still know relatively little about how genomes evolve and stabilize following hybridization, and to what extent hybridization is functionally relevant. Here, we examine the case of Xiphophorus nezahualcoyotl, a teleost fish whose genome exhibits significant hybrid ancestry. We show that hybridization was relatively ancient and is unlikely to be ongoing. Strikingly, the genome of X. nezahualcoyotl has largely stabilized following hybridization, distinguishing it from examples such as human-Neanderthal hybridization. Hybridization-derived regions are remarkably distinct from other regions of the genome, tending to be enriched in genomic regions with reduced constraint. These results suggest that selection has played a role in removing hybrid ancestry from certain functionally important regions. Combined with findings in other systems, our results raise many questions about the process of genomic stabilization and the role of selection in shaping patterns of hybrid ancestry in the genome.
View details for DOI 10.1111/mec.13602
View details for Web of Science ID 000378941100025
View details for PubMedID 26937625
Stable isotope evidence for trophic overlap of sympatric Mexican Lake Chapala silversides (Teleostei: Atherinopsidae: Chirostoma spp.)
2015; 13 (2): 389–400
View details for DOI 10.1590/1982-0224-20140079
View details for Web of Science ID 000358438400014
High-resolution Mapping Reveals Hundreds of Genetic Incompatibilities in Hybridizing Fish Species
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.
View details for DOI 10.7554/eLife.02535
View details for Web of Science ID 000336837300003
View details for PubMedID 24898754
View details for PubMedCentralID PMC4080447