Molly Schumer

All Publications

• Phylogenomic analyses of all species of swordtail fishes (genus Xiphophorus) show that hybridization preceded speciation. Nature communications Du, K., Ricci, J. M., Lu, Y., Garcia-Olazabal, M., Walter, R. B., Warren, W. C., Dodge, T. O., Schumer, M., Park, H., Meyer, A., Schartl, M. 2024; 15 (1): 6609

  Abstract

  Hybridization has been recognized to play important roles in evolution, however studies of the genetic consequence are still lagging behind in vertebrates due to the lack of appropriate experimental systems. Fish of the genus Xiphophorus are proposed to have evolved with multiple ancient and ongoing hybridization events. They have served as an informative research model in evolutionary biology and in biomedical research on human disease for more than a century. Here, we provide the complete genomic resource including annotations for all described 26 Xiphophorus species and three undescribed taxa and resolve all uncertain phylogenetic relationships. We investigate the molecular evolution of genes related to cancers such as melanoma and for the genetic control of puberty timing, focusing on genes that are predicted to be involved in pre-and postzygotic isolation and thus affect hybridization. We discovered dramatic size-variation of some gene families. These persisted despite reticulate evolution, rapid speciation and short divergence time. Finally, we clarify the hybridization history in the entire genus settling disputed hybridization history of two Southern swordtails. Our comparative genomic analyses revealed hybridization ancestries that are manifested in the mosaic fused genomes and show that hybridization often preceded speciation.

  View details for DOI 10.1038/s41467-024-50852-6

  View details for PubMedID 39098897

  View details for PubMedCentralID 2769149

• Hybridization in the Anthropocene - how pollution and climate change disrupt mate selection in freshwater fish. Biological reviews of the Cambridge Philosophical Society Ramirez-Duarte, W. F., Moran, B. M., Powell, D. L., Bank, C., Sousa, V. C., Rosenthal, G. G., Schumer, M., Rochman, C. M. 2024

  Abstract

  Chemical pollutants and/or climate change have the potential to break down reproductive barriers between species and facilitate hybridization. Hybrid zones may arise in response to environmental gradients and secondary contact between formerly allopatric populations, or due to the introduction of non-native species. In freshwater ecosystems, field observations indicate that changes in water quality and chemistry, due to pollution and climate change, are correlated with an increased frequency of hybridization. Physical and chemical disturbances of water quality can alter the sensory environment, thereby affecting chemical and visual communication among fish. Moreover, multiple chemical compounds (e.g. pharmaceuticals, metals, pesticides, and industrial contaminants) may impair fish physiology, potentially affecting phenotypic traits relevant for mate selection (e.g. pheromone production, courtship, and coloration). Although warming waters have led to documented range shifts, and chemical pollution is ubiquitous in freshwater ecosystems, few studies have tested hypotheses about how these stressors may facilitate hybridization and what this means for biodiversity and species conservation. Through a systematic literature review across disciplines (i.e. ecotoxicology and evolutionary biology), we evaluate the biological interactions, toxic mechanisms, and roles of physical and chemical environmental stressors (i.e. chemical pollution and climate change) in disrupting mate preferences and inducing interspecific hybridization in freshwater fish. Our study indicates that climate change-driven changes in water quality and chemical pollution may impact visual and chemical communication crucial for mate choice and thus could facilitate hybridization among fishes in freshwater ecosystems. To inform future studies and conservation management, we emphasize the importance of further research to identify the chemical and physical stressors affecting mate choice, understand the mechanisms behind these interactions, determine the concentrations at which they occur, and assess their impact on individuals, populations, species, and biological diversity in the Anthropocene.

  View details for DOI 10.1111/brv.13126

  View details for PubMedID 39092475

• Pervasive gene flow despite strong and varied reproductive barriers in swordtails. bioRxiv : the preprint server for biology Aguillon, S. M., Haase Cox, S. K., Langdon, Q. K., Gunn, T. R., Baczenas, J. J., Banerjee, S. M., Donny, A. E., Moran, B. M., Gutierrez-Rodriguez, C., Rios-Cardenas, O., Morris, M. R., Powell, D. L., Schumer, M. 2024

  Abstract

  One of the mechanisms that can lead to the formation of new species occurs through the evolution of reproductive barriers. However, recent research has demonstrated that hybridization has been pervasive across the tree of life even in the presence of strong barriers. Swordtail fishes (genus Xiphophorus ) are an emerging model system for studying the interface between these barriers and hybridization. We document overlapping mechanisms that act as barriers between closely related species, X. birchmanni and X. cortezi , by combining genomic sequencing from natural hybrid populations, artificial crosses, behavioral assays, sperm performance, and developmental studies. We show that strong assortative mating plays a key role in maintaining subpopulations with distinct ancestry in natural hybrid populations. Lab experiments demonstrate that artificial F 1 crosses experience dysfunction: crosses with X. birchmanni females were largely inviable and crosses with X. cortezi females had a heavily skewed sex ratio. Using F 2 hybrids we identify several genomic regions that strongly impact hybrid viability. Strikingly, two of these regions underlie genetic incompatibilities in hybrids between X. birchmanni and its sister species X. malinche . Our results demonstrate that ancient hybridization has played a role in the origin of this shared genetic incompatibility. Moreover, ancestry mismatch at these incompatible regions has remarkably similar consequences for phenotypes and hybrid survival in X. cortezi O X. birchmanni hybrids as in X. malinche O X. birchmanni hybrids. Our findings identify varied reproductive barriers that shape genetic exchange between naturally hybridizing species and highlight the complex evolutionary outcomes of hybridization.Significance Statement: Biologists are fascinated by how the diverse species we see on Earth have arisen and been maintained. One driver of this process is the evolution of reproductive barriers between species. Despite the commonality of these barriers, many species still exchange genes through a process called hybridization. Here, we show that related species can have a striking array of reproductive barriers-from genetic interactions that harm hybrids to mate preferences that reduce hybridization in the first place. However, we also find that genetic exchange between these species is very common, and may itself play an important role in the evolution of reproductive barriers. Together, our work highlights the complex web of interactions that impact the origin and persistence of distinct species.

  View details for DOI 10.1101/2024.04.16.589374

  View details for PubMedID 38659793

• CRP-Tree: a phylogenetic association test for binary traits JOURNAL OF THE ROYAL STATISTICAL SOCIETY SERIES C-APPLIED STATISTICS Zhang, J., Preising, G. A., Schumer, M., Palacios, J. A. 2024; 73 (2): 340-377

  View details for DOI 10.1093/jrsssc/qlad098

  View details for Web of Science ID 001186796700001

• Patterns of recombination in snakes reveal a tug-of-war between PRDM9 and promoter-like features. Science (New York, N.Y.) Hoge, C., de Manuel, M., Mahgoub, M., Okami, N., Fuller, Z., Banerjee, S., Baker, Z., McNulty, M., Andolfatto, P., Macfarlan, T. S., Schumer, M., Tzika, A. C., Przeworski, M. 2024; 383 (6685): eadj7026

  Abstract

  In some mammals, notably humans, recombination occurs almost exclusively where the protein PRDM9 binds, whereas in vertebrates lacking an intact PRDM9, such as birds and canids, recombination rates are elevated near promoter-like features. To determine whether PRDM9 directs recombination in nonmammalian vertebrates, we focused on an exemplar species with a single, intact PRDM9 ortholog, the corn snake (Pantherophis guttatus). Analyzing historical recombination rates along the genome and crossovers in pedigrees, we found evidence that PRDM9 specifies the location of recombination events, but we also detected a separable effect of promoter-like features. These findings reveal that the uses of PRDM9 and promoter-like features need not be mutually exclusive and instead reflect a tug-of-war that is more even in some species than others.

  View details for DOI 10.1126/science.adj7026

  View details for PubMedID 38386752

• A lethal mitonuclear incompatibility in complex I of natural hybrids. Nature Moran, B. M., Payne, C. Y., Powell, D. L., Iverson, E. N., Donny, A. E., Banerjee, S. M., Langdon, Q. K., Gunn, T. R., Rodriguez-Soto, R. A., Madero, A., Baczenas, J. J., Kleczko, K. M., Liu, F., Matney, R., Singhal, K., Leib, R. D., Hernandez-Perez, O., Corbett-Detig, R., Frydman, J., Gifford, C., Schartl, M., Havird, J. C., Schumer, M. 2024

  Abstract

  The evolution of reproductive barriers is the first step in the formation of new species and can help us understand the diversification of life on Earth. These reproductive barriers often take the form of hybrid incompatibilities, in which alleles derived from two different species no longer interact properly in hybrids1-3. Theory predicts that hybrid incompatibilities may be more likely to arise at rapidly evolving genes4-6 and that incompatibilities involving multiple genes should be common7,8, but there has been sparse empirical data to evaluate these predictions. Here we describe a mitonuclear incompatibility involving three genes whose protein products are in physical contact within respiratory complex I of naturally hybridizing swordtail fish species. Individuals homozygous for mismatched protein combinations do not complete embryonic development or die as juveniles, whereas those heterozygous for the incompatibility have reduced complex I function and unbalanced representation of parental alleles in the mitochondrial proteome. We find that the effects of different genetic interactions on survival are non-additive, highlighting subtle complexity in the genetic architecture of hybrid incompatibilities. Finally, we document the evolutionary history of the genes involved, showing signals of accelerated evolution and evidence that an incompatibility has been transferred between species via hybridization.

  View details for DOI 10.1038/s41586-023-06895-8

  View details for PubMedID 38200310

  View details for PubMedCentralID 6502311

• The Ecology of Hybrid Incompatibilities. Cold Spring Harbor perspectives in biology Thompson, K. A., Brandvain, Y., Coughlan, J. M., Delmore, K. E., Justen, H., Linnen, C. R., Ortiz-Barrientos, D., Rushworth, C. A., Schneemann, H., Schumer, M., Stelkens, R. 2023

  Abstract

  Ecologically mediated selection against hybrids, caused by hybrid phenotypes fitting poorly into available niches, is typically viewed as distinct from selection caused by epistatic Dobzhansky-Muller hybrid incompatibilities. Here, we show how selection against transgressive phenotypes in hybrids manifests as incompatibility. After outlining our logic, we summarize current approaches for studying ecology-based selection on hybrids. We then quantitatively review QTL-mapping studies and find traits differing between parent taxa are typically polygenic. Next, we describe how verbal models of selection on hybrids translate to phenotypic and genetic fitness landscapes, highlighting emerging approaches for detecting polygenic incompatibilities. Finally, in a synthesis of published data, we report that trait transgression-and thus possibly extrinsic hybrid incompatibility in hybrids-escalates with the phenotypic divergence between parents. We discuss conceptual implications and conclude that studying the ecological basis of hybrid incompatibility will facilitate new discoveries about mechanisms of speciation.

  View details for DOI 10.1101/cshperspect.a041440

  View details for PubMedID 38151331

• Genome evolution is surprisingly predictable after initial hybridization. bioRxiv : the preprint server for biology Langdon, Q. K., Groh, J. S., Aguillon, S. M., Powell, D. L., Gunn, T., Payne, C., Baczenas, J. J., Donny, A., Dodge, T. O., Du, K., Schartl, M., Ríos-Cárdenas, O., Gutierrez-Rodríguez, C., Morris, M., Schumer, M. 2023

  Abstract

  Over the past two decades, evolutionary biologists have come to appreciate that hybridization, or genetic exchange between distinct lineages, is remarkably common - not just in particular lineages but in taxonomic groups across the tree of life. As a result, the genomes of many modern species harbor regions inherited from related species. This observation has raised fundamental questions about the degree to which the genomic outcomes of hybridization are repeatable and the degree to which natural selection drives such repeatability. However, a lack of appropriate systems to answer these questions has limited empirical progress in this area. Here, we leverage independently formed hybrid populations between the swordtail fish Xiphophorus birchmanni and X. cortezi to address this fundamental question. We find that local ancestry in one hybrid population is remarkably predictive of local ancestry in another, demographically independent hybrid population. Applying newly developed methods, we can attribute much of this repeatability to strong selection in the earliest generations after initial hybridization. We complement these analyses with time-series data that demonstrates that ancestry at regions under selection has remained stable over the past ~40 generations of evolution. Finally, we compare our results to the well-studied X. birchmanni×X. malinche hybrid populations and conclude that deeper evolutionary divergence has resulted in stronger selection and higher repeatability in patterns of local ancestry in hybrids between X. birchmanni and X. cortezi.

  View details for DOI 10.1101/2023.12.21.572897

  View details for PubMedID 38187753

  View details for PubMedCentralID PMC10769416

• Patterns of recombination in snakes reveal a tug of war between PRDM9 and promoter-like features. bioRxiv : the preprint server for biology Hoge, C., de Manuel, M., Mahgoub, M., Okami, N., Fuller, Z., Banerjee, S., Baker, Z., McNulty, M., Andolfatto, P., Macfarlan, T. S., Schumer, M., Tzika, A. C., Przeworski, M. 2023

  Abstract

  In vertebrates, there are two known mechanisms by which meiotic recombination is directed to the genome: in humans, mice, and other mammals, recombination occurs almost exclusively where the protein PRDM9 binds, while in species lacking an intact PRDM9, such as birds and canids, recombination rates are elevated near promoter-like features. To test if PRDM9 also directs recombination in non-mammalian vertebrates, we focused on an exemplar species, the corn snake (Pantherophis guttatus). Unlike birds, this species possesses a single, intact PRDM9 ortholog. By inferring historical recombination rates along the genome from patterns of linkage disequilibrium and identifying crossovers in pedigrees, we found that PRDM9 specifies the location of recombination events outside of mammals. However, we also detected an independent effect of promoter-like features on recombination, which is more pronounced on macro- than microchromosomes. Thus, our findings reveal that the uses of PRDM9 and promoter-like features are not mutually-exclusive, and instead reflect a tug of war, which varies in strength along the genome and is more lopsided in some species than others.

  View details for DOI 10.1101/2023.07.11.548536

  View details for PubMedID 37502971

  View details for PubMedCentralID PMC10369914

• Individual variation in preference behavior in sailfin fish refines the neurotranscriptomic pathway for mate preference. Ecology and evolution Young, R. L., Price, S. M., Schumer, M., Wang, S., Cummings, M. E. 2023; 13 (7): e10323

  Abstract

  Social interactions can drive distinct gene expression profiles which may vary by social context. Here we use female sailfin molly fish (Poecilia latipinna) to identify genomic profiles associated with preference behavior in distinct social contexts: male interactions (mate choice) versus female interactions (shoaling partner preference). We measured the behavior of 15 females interacting in a non-contact environment with either two males or two females for 30min followed by whole-brain transcriptomic profiling by RNA sequencing. We profiled females that exhibited high levels of social affiliation and great variation in preference behavior to identify an order of magnitude more differentially expressed genes associated with behavioral variation than by differences in social context. Using a linear model (limma), we took advantage of the individual variation in preference behavior to identify unique gene sets that exhibited distinct correlational patterns of expression with preference behavior in each social context. By combining limma and weighted gene co-expression network analyses (WGCNA) approaches we identified a refined set of 401 genes robustly associated with mate preference that is independent of shoaling partner preference or general social affiliation. While our refined gene set confirmed neural plasticity pathways involvement in moderating female preference behavior, we also identified a significant proportion of discovered that our preference-associated genes were enriched for 'immune system' gene ontology categories. We hypothesize that the association between mate preference and transcriptomic immune function is driven by the less well-known role of these genes in neural plasticity which is likely involved in higher-order learning and processing during mate choice decisions.

  View details for DOI 10.1002/ece3.10323

  View details for PubMedID 37492456

• Genomes of two Extinct-in-the-Wild reptiles from Christmas Island reveal distinct evolutionary histories and conservation insights. Molecular ecology resources Dodge, T. O., Farquharson, K. A., Ford, C., Cavanagh, L., Schubert, K., Schumer, M., Belov, K., Hogg, C. J. 2023

  Abstract

  Genomics can play important roles in biodiversity conservation, especially for Extinct-in-the-Wild species where genetic factors greatly influence risk of total extinction and probability of successful reintroductions. The Christmas Island blue-tailed skink (Cryptoblepharus egeriae) and Lister's gecko (Lepidodactylus listeri) are two endemic reptile species that went extinct in the wild shortly following the introduction of a predatory snake. After a decade of management, captive populations have expanded from 66 skinks and 43 geckos to several thousand individuals; however, little is known about patterns of genetic variation in these species. Here, we use PacBio HiFi long-read and Hi-C sequencing to generate highly contiguous reference genomes for both reptiles, including the XY chromosome pair in the skink. We then analyze patterns of genetic diversity to infer ancient demography and more recent histories of inbreeding. We observe high genome-wide heterozygosity in the skink (0.007 heterozygous sites per base-pair) and gecko (0.005), consistent with large historical population sizes. However, nearly 10% of the blue-tailed skink reference genome falls within long (>1Mb) runs of homozygosity (ROH), resulting in homozygosity at all major histocompatibility complex (MHC) loci. In contrast, we detect a single ROH in Lister's gecko. We infer from the ROH lengths that related skinks may have established the captive populations. Despite a shared recent extinction in the wild, our results suggest important differences in these species' histories and implications for management. We show how reference genomes can contribute evolutionary and conservation insights, and we provide resources for future population-level and comparative genomic studies in reptiles.

  View details for DOI 10.1111/1755-0998.13780

  View details for PubMedID 36872490

• Complex hybridization between deeply diverged fish species in a disturbed ecosystem. Evolution; international journal of organic evolution Banerjee, S. M., Powell, D. L., Moran, B. M., Ramírez-Duarte, W. F., Langdon, Q. K., Gunn, T. R., Vazquez, G., Rochman, C., Schumer, M. 2023

  Abstract

  Over the past two decades researchers have documented the extent of natural hybridization between closely related species using genomic tools. Many species across the tree of life show evidence of past hybridization with their evolutionary relatives. In some cases, this hybridization is complex - involving gene flow between more than two species. While hybridization is common over evolutionary timescales, some researchers have proposed that it may be even more common in contemporary populations where anthropogenic disturbance has modified a myriad of aspects of the environments in which organisms live and reproduce. Here, we develop a flexible tool for local ancestry inference in hybrids derived from three source populations and describe a complex, recent hybridization event between distantly related swordtail fish lineages (Xiphophorus) and its potential links to anthropogenic disturbance.

  View details for DOI 10.1093/evolut/qpad019

  View details for PubMedID 36753531

• Introgression. Current biology : CB Aguillon, S. M., Dodge, T. O., Preising, G. A., Schumer, M. 2022; 32 (16): R865-R868

  Abstract

  Biologists have forever sought to understand how species arise and persist. Historically, species that rarely interbreed, or are reproductively isolated, were considered the norm, while those with incomplete reproductive isolation were considered less common. Over the last few decades, advances in genomics have transformed our understanding of the frequency of gene flow between species and with it our ideas about reproductive isolation in nature. These advances have uncovered a rich and often complicated history of genetic exchange between species - demonstrating that such genetic introgression is an important evolutionary process widespread across the tree of life (Figure 1).

  View details for DOI 10.1016/j.cub.2022.07.004

  View details for PubMedID 35998591

• Introgression CURRENT BIOLOGY Aguillon, S. M., Dodge, T. O., Preising, G. A., Schumer, M. 2022; 32 (16): R865-R868

  View details for Web of Science ID 000859009300005

• Genomic insights into variation in thermotolerance between hybridizing swordtail fishes. Molecular ecology Payne, C., Bovio, S., Powell, D., Gunn, T., Banerjee, S., Grant, V., Rosenthal, G. G., Schumer, M. 2022

  Abstract

  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.

  View details for DOI 10.1111/mec.16489

  View details for PubMedID 35510780

• Imbalanced segregation of recombinant haplotypes in hybrid populations reveals inter- and intrachromosomal Dobzhansky-Muller incompatibilities. PLoS genetics Li, J., Schumer, M., Bank, C. 2022; 18 (3): e1010120

  Abstract

  Dobzhansky-Muller incompatibilities (DMIs) are a major component of reproductive isolation between species. DMIs imply negative epistasis and are exposed when two diverged populations hybridize. Mapping the locations of DMIs has largely relied on classical genetic mapping. Approaches to date are hampered by low power and the challenge of identifying DMI loci on the same chromosome, because strong initial linkage of parental haplotypes weakens statistical tests. Here, we propose new statistics to infer negative epistasis from haplotype frequencies in hybrid populations. When two divergent populations hybridize, the variance in heterozygosity at two loci decreases faster with time at DMI loci than at random pairs of loci. When two populations hybridize at near-even admixture proportions, the deviation of the observed variance from its expectation becomes negative for the DMI pair. This negative deviation enables us to detect intermediate to strong negative epistasis both within and between chromosomes. In practice, the detection window in hybrid populations depends on the demographic scenario, the recombination rate, and the strength of epistasis. When the initial proportion of the two parental populations is uneven, only strong DMIs can be detected with our method unless migration prevents parental haplotypes from being lost. We use the new statistics to infer candidate DMIs from three hybrid populations of swordtail fish. We identify numerous new DMI candidates, some of which are inferred to interact with several loci within and between chromosomes. Moreover, we discuss our results in the context of an expected enrichment in intrachromosomal over interchromosomal DMIs.

  View details for DOI 10.1371/journal.pgen.1010120

  View details for PubMedID 35344560

• PRDM9 losses in vertebrates are coupled to those of paralogs ZCWPW1 and ZCWPW2. Proceedings of the National Academy of Sciences of the United States of America Cavassim, M. I., Baker, Z., Hoge, C., Schierup, M. H., Schumer, M., Przeworski, M. 2022; 119 (9)

  Abstract

  In most mammals and likely throughout vertebrates, the gene PRDM9 specifies the locations of meiotic double strand breaks; in mice and humans at least, it also aids in their repair. For both roles, many of the molecular partners remain unknown. Here, we take a phylogenetic approach to identify genes that may be interacting with PRDM9 by leveraging the fact that PRDM9 arose before the origin of vertebrates but was lost many times, either partially or entirely-and with it, its role in recombination. As a first step, we characterize PRDM9 domain composition across 446 vertebrate species, inferring at least 13 independent losses. We then use the interdigitation of PRDM9 orthologs across vertebrates to test whether it coevolved with any of 241 candidate genes coexpressed with PRDM9 in mice or associated with recombination phenotypes in mammals. Accounting for the phylogenetic relationship among a subsample of 189 species, we find two genes whose presence and absence is unexpectedly coincident with that of PRDM9: ZCWPW1, which was recently shown to facilitate double strand break repair, and its paralog ZCWPW2, as well as, more tentatively, TEX15 and FBXO47 ZCWPW2 is expected to be recruited to sites of PRDM9 binding; its tight coevolution with PRDM9 across vertebrates suggests that it is a key interactor within mammals and beyond, with a role either in recruiting the recombination machinery or in double strand break repair.

  View details for DOI 10.1073/pnas.2114401119

  View details for PubMedID 35217607

• Analysis of ancestry heterozygosity suggests that hybrid incompatibilities in threespine stickleback are environment dependent. PLoS biology Thompson, K. A., Peichel, C. L., Rennison, D. J., McGee, M. D., Albert, A. Y., Vines, T. H., Greenwood, A. K., Wark, A. R., Brandvain, Y., Schumer, M., Schluter, D. 1800; 20 (1): e3001469

  Abstract

  Hybrid incompatibilities occur when interactions between opposite ancestry alleles at different loci reduce the fitness of hybrids. Most work on incompatibilities has focused on those that are "intrinsic," meaning they affect viability and sterility in the laboratory. Theory predicts that ecological selection can also underlie hybrid incompatibilities, but tests of this hypothesis using sequence data are scarce. In this article, we compiled genetic data for F2 hybrid crosses between divergent populations of threespine stickleback fish (Gasterosteus aculeatus L.) that were born and raised in either the field (seminatural experimental ponds) or the laboratory (aquaria). Because selection against incompatibilities results in elevated ancestry heterozygosity, we tested the prediction that ancestry heterozygosity will be higher in pond-raised fish compared to those raised in aquaria. We found that ancestry heterozygosity was elevated by approximately 3% in crosses raised in ponds compared to those raised in aquaria. Additional analyses support a phenotypic basis for incompatibility and suggest that environment-specific single-locus heterozygote advantage is not the cause of selection on ancestry heterozygosity. Our study provides evidence that, in stickleback, a coarse-albeit indirect-signal of environment-dependent hybrid incompatibility is reliably detectable and suggests that extrinsic incompatibilities can evolve before intrinsic incompatibilities.

  View details for DOI 10.1371/journal.pbio.3001469

  View details for PubMedID 35007278

• Predictability and parallelism in the contemporary evolution of hybrid genomes. PLoS genetics Langdon, Q. K., Powell, D. L., Kim, B., Banerjee, S. M., Payne, C., Dodge, T. O., Moran, B., Fascinetto-Zago, P., Schumer, M. 1800; 18 (1): e1009914

  Abstract

  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 Powell, D. L., Moran, B., Kim, B., Banerjee, S. M., Aguillon, S. M., Fascinetto-Zago, P., Langdon, Q., Schumer, M. 2021

  Abstract

  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. eLife Moran, B. M., Payne, C., Langdon, Q., Powell, D. L., Brandvain, Y., Schumer, M. 2021; 10

  Abstract

  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 Powell, D. L., Payne, C., Banerjee, S. M., Keegan, M., Bashkirova, E., Cui, R., Andolfatto, P., Rosenthal, G. G., Schumer, M. 2021

  Abstract

  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.) Powell, D. L., García-Olazábal, M. n., Keegan, M. n., Reilly, P. n., Du, K. n., Díaz-Loyo, A. P., Banerjee, S. n., Blakkan, D. n., Reich, D. n., Andolfatto, P. n., Rosenthal, G. G., Schartl, M. n., Schumer, M. n. 2020; 368 (6492): 731–36

  Abstract

  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 Schumer, M. n., Powell, D. L., Corbett-Detig, R. n. 2020

  Abstract

  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

• Draft Genome Assembly and Annotation of the Gila Topminnow Poeciliopsis occidentalis FRONTIERS IN ECOLOGY AND EVOLUTION Mateos, M., Kang, D., Klopp, C., Parrinello, H., Garcia-Olazabal, M., Schumer, M., Jue, N. K., Guiguen, Y., Schartl, M. 2019; 7

  View details for DOI 10.3389/fevo.2019.00404

  View details for Web of Science ID 000496952000001

• Natural selection interacts with recombination to shape the evolution of hybrid genomes SCIENCE Schumer, M., Xu, C., Powell, D. L., Durvasula, A., Skov, L., Holland, C., Blazier, J. C., Sankararaman, S., Andolfatto, P., Rosenthal, G. G., Przeworski, M. 2018; 360 (6389): 656–59

  Abstract

  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

• How the manakin got its crown: A novel trait that is unlikely to cause speciation PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA Rosenthal, G. G., Schumer, M., Andolfatto, P. 2018; 115 (18): E4144–E4145

  View details for DOI 10.1073/pnas.1804061115

  View details for Web of Science ID 000431119600001

  View details for PubMedID 29669913

  View details for PubMedCentralID PMC5939116

• What do we mean when we talk about hybrid speciation? HEREDITY Schumer, M., Rosenthal, G. G., Andolfatto, P. 2018; 120 (4): 379–82

  View details for DOI 10.1038/s41437-017-0036-z

  View details for Web of Science ID 000426887000008

  View details for PubMedID 29302049

  View details for PubMedCentralID PMC5842215

• Assortative mating and persistent reproductive isolation in hybrids PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA Schumer, M., Powell, D. L., Delclos, P. J., Squire, M., Cui, R., Andolfatto, P., Rosenthal, G. G. 2017; 114 (41): 10936–41

  Abstract

  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

• Repeated losses of PRDM9-directed recombination despite the conservation of PRDM9 across vertebrates ELIFE Baker, Z., Schumer, M., Haba, Y., Bashkirova, L., Holland, C., Rosenthal, G. G., Przeworski, M. 2017; 6

  Abstract

  Studies of highly diverged species have revealed two mechanisms by which meiotic recombination is directed to the genome-through PRDM9 binding or by targeting promoter-like features-that lead to dramatically different evolutionary dynamics of hotspots. Here, we identify PRDM9 orthologs from genome and transcriptome data in 225 species. We find the complete PRDM9 ortholog across distantly related vertebrates but, despite this broad conservation, infer a minimum of six partial and three complete losses. Strikingly, taxa carrying the complete ortholog of PRDM9 are precisely those with rapid evolution of its predicted binding affinity, suggesting that all domains are necessary for directing recombination. Indeed, as we show, swordtail fish carrying only a partial but conserved ortholog share recombination properties with PRDM9 knock-outs.

  View details for DOI 10.7554/eLife.24133

  View details for Web of Science ID 000405904400001

  View details for PubMedID 28590247

  View details for PubMedCentralID PMC5519329

• Early social learning triggers neurogenomic expression changes in a swordtail fish PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES Cui, R., Delclos, P. J., Schumer, M., Rosenthal, G. G. 2017; 284 (1854)

  Abstract

  Mate choice can play a pivotal role in the nature and extent of reproductive isolation between species. Mating preferences are often dependent on an individual's social experience with adult phenotypes throughout development. We show that olfactory preference in a swordtail fish (Xiphophorus malinche) is affected by previous experience with adult olfactory signals. We compare transcriptome-wide gene expression levels of pooled sensory and brain tissues between three treatment groups that differ by social experience: females with no adult exposure, females exposed to conspecifics and females exposed to heterospecifics. We identify potential functionally relevant genes and biological pathways differentially expressed not only between control and exposure groups, but also between groups exposed to conspecifics and heterospecifics. Based on our results, we speculate that vomeronasal receptor type 2 paralogs may detect species-specific pheromone components and thus play an important role in reproductive isolation between species.

  View details for DOI 10.1098/rspb.2017.0701

  View details for Web of Science ID 000404425100001

  View details for PubMedID 28515207

  View details for PubMedCentralID PMC5443958

• Determining epistatic selection in admixed populations MOLECULAR ECOLOGY Schumer, M., Brandvain, Y. 2016; 25 (11): 2577–91

  Abstract

  When two diverging species begin hybridizing, selection against hybridization is likely driven not by single substitutions, but by interactions between incompatible mutations. To identify these incompatibilities in natural populations, researchers examine the extent of nonrandom associations between ancestry at physically unlinked loci in admixed populations. In this approach, which we call 'AD scans', locus pairs with significantly positive 'ancestry disequilibrium' (AD, i.e. locus pairs that positively covary by ancestry) represent incompatible alleles. Past research has uniformly revealed an excess of locus pairs with significantly positive AD, suggesting that dozens to hundreds of incompatibilities separate species. With forward simulations, we show that many realistic demographic scenarios, including recent and/or ongoing hybridization, generate a bias towards positive ancestry disequilibrium. We suggest steps that researchers can take to avoid pitfalls in interpreting AD scans, and present a novel measure of AD, which minimizes but does not fully eliminate bias in the AD distribution. We also show, by simulation, that the tail of the AD distribution is enriched for true incompatibilities. To illustrate the potential power and appropriate caution in interpretation of AD scans, we reanalyse previously published data from two admixed populations of Xiphophorus fishes. Our results imply that the prevalence of positive LD in admixed populations does not in itself support the idea that two-locus incompatibilities are widespread, but the co-enrichment of top AD hits across the two Xiphophorus populations supports the idea that AD scans can identify candidate interspecific incompatibilities.

  View details for DOI 10.1111/mec.13641

  View details for Web of Science ID 000378941100019

  View details for PubMedID 27061282

• Ancient hybridization and genomic stabilization in a swordtail fish MOLECULAR ECOLOGY Schumer, M., Cui, R., Powell, D. L., Rosenthal, G. G., Andolfatto, P. 2016; 25 (11): 2661–79

  Abstract

  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

• Admix'em: a flexible framework for forward-time simulations of hybrid populations with selection and mate choice BIOINFORMATICS Cui, R., Schumer, M., Rosenthal, G. G. 2016; 32 (7): 1103–5

  Abstract

  We introduce a new forward-time simulator, Admix'em, that allows for rapid and realistic simulations of admixed populations with selection. Complex selection can be achieved through user-defined fitness and mating-preference probability functions. Users can specify realistic genomic landscapes and model neutral SNPs in addition to sites under selection. Admix'em is designed to simulate selection in admixed populations but can also be used as a general population simulator. Usage and examples are in the supplement.C ++ and OpenMP, supports 64-bit Linux/Unix-like platforms. https://github.com/melop/admixemrcui@age.mpg.deSupplementary data are available at Bioinformatics online.

  View details for DOI 10.1093/bioinformatics/btv700

  View details for Web of Science ID 000374236400024

  View details for PubMedID 26615212

• simMSG: an experimental design tool for high-throughput genotyping of hybrids MOLECULAR ECOLOGY RESOURCES Schumer, M., Cui, R., Rosenthal, G. G., Andolfatto, P. 2016; 16 (1): 183–92

  Abstract

  Hybridization between closely related species, whether naturally occurring or laboratory generated, is a useful tool for mapping the genetic basis of the phenotypic traits that distinguish species. The development of next-generation sequencing techniques has greatly improved our ability to assign ancestry to hybrid genomes. One such next-generation sequencing technique, multiplexed shotgun genotyping (or MSG), can be a powerful tool for genotyping hybrids. However, it is difficult a priori to predict the accuracy of MSG in natural hybrids because accuracy depends on ancestry tract length and number of ancestry informative markers. Here, we present a simulator, 'simMSG', that will allow researchers to design MSG experiments and show that in many cases MSG can accurately assign ancestry to hundreds of thousands of sites in the genomes of natural hybrids. The simMSG tool can be used to design experiments for diverse applications including QTL mapping, genotyping introgressed lines or admixture mapping.

  View details for DOI 10.1111/1755-0998.12434

  View details for Web of Science ID 000369141000019

  View details for PubMedID 26032857

• Genetics of Intraspecies Variation in Avoidance Behavior Induced by a Thermal Stimulus in Caenorhabditis elegans GENETICS Ghosh, R., Bloom, J. S., Mohammadi, A., Schumer, M. E., Andolfatto, P., Ryu, W., Kruglyak, L. 2015; 200 (4): 1327-+

  Abstract

  Individuals within a species vary in their responses to a wide range of stimuli, partly as a result of differences in their genetic makeup. Relatively little is known about the genetic and neuronal mechanisms contributing to diversity of behavior in natural populations. By studying intraspecies variation in innate avoidance behavior to thermal stimuli in the nematode Caenorhabditis elegans, we uncovered genetic principles of how different components of a behavioral response can be altered in nature to generate behavioral diversity. Using a thermal pulse assay, we uncovered heritable variation in responses to a transient temperature increase. Quantitative trait locus mapping revealed that separate components of this response were controlled by distinct genomic loci. The loci we identified contributed to variation in components of thermal pulse avoidance behavior in an additive fashion. Our results show that the escape behavior induced by thermal stimuli is composed of simpler behavioral components that are influenced by at least six distinct genetic loci. The loci that decouple components of the escape behavior reveal a genetic system that allows independent modification of behavioral parameters. Our work sets the foundation for future studies of evolution of innate behaviors at the molecular and neuronal level.

  View details for DOI 10.1534/genetics.115.178491

  View details for Web of Science ID 000359917000027

  View details for PubMedID 26092720

  View details for PubMedCentralID PMC4574258

• Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities PLOS GENETICS Schumer, M., Cui, R., Rosenthal, G. G., Andolfatto, P. 2015; 11 (3): e1005041

  Abstract

  Despite its role in homogenizing populations, hybridization has also been proposed as a means to generate new species. The conceptual basis for this idea is that hybridization can result in novel phenotypes through recombination between the parental genomes, allowing a hybrid population to occupy ecological niches unavailable to parental species. Here we present an alternative model of the evolution of reproductive isolation in hybrid populations that occurs as a simple consequence of selection against genetic incompatibilities. Unlike previous models of hybrid speciation, our model does not incorporate inbreeding, or assume that hybrids have an ecological or reproductive fitness advantage relative to parental populations. We show that reproductive isolation between hybrids and parental species can evolve frequently and rapidly under this model, even in the presence of substantial ongoing immigration from parental species and strong selection against hybrids. An interesting prediction of our model is that replicate hybrid populations formed from the same pair of parental species can evolve reproductive isolation from each other. This non-adaptive process can therefore generate patterns of species diversity and relatedness that resemble an adaptive radiation. Intriguingly, several known hybrid species exhibit patterns of reproductive isolation consistent with the predictions of our model.

  View details for DOI 10.1371/journal.pgen.1005041

  View details for Web of Science ID 000352197100031

  View details for PubMedID 25768654

  View details for PubMedCentralID PMC4359097

• Environmental heterogeneity generates opposite gene-by-environment interactions for two fitness-related traits within a population EVOLUTION Culumber, Z. W., Schumer, M., Monks, S., Tobler, M. 2015; 69 (2): 541–50

  Abstract

  Theory predicts that environmental heterogeneity offers a potential solution to the maintenance of genetic variation within populations, but empirical evidence remains sparse. The live-bearing fish Xiphophorus variatus exhibits polymorphism at a single locus, with different alleles resulting in up to five distinct melanistic "tailspot" patterns within populations. We investigated the effects of heterogeneity in two ubiquitous environmental variables (temperature and food availability) on two fitness-related traits (upper thermal limits and body condition) in two different tailspot types (wild-type and upper cut crescent). We found gene-by-environment (G × E) interactions between tailspot type and food level affecting upper thermal limits (UTL), as well as between tailspot type and thermal environment affecting body condition. Exploring mechanistic bases underlying these G × E patterns, we found no differences between tailspot types in hsp70 gene expression despite significant overall increases in expression under both thermal and food stress. Similarly, there was no difference in routine metabolic rates between the tailspot types. The reversal of relative performance of the two tailspot types under different environmental conditions revealed a mechanism by which environmental heterogeneity can balance polymorphism within populations through selection on different fitness-related traits.

  View details for DOI 10.1111/evo.12574

  View details for Web of Science ID 000348916200020

  View details for PubMedID 25496554

• High-resolution Mapping Reveals Hundreds of Genetic Incompatibilities in Hybridizing Fish Species ELIFE Schumer, M., Cui, R., Powell, D., Dresner, R., Rosenthal, G. G., Andolfatto, P. 2014; 3

  Abstract

  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

• HOW COMMON IS HOMOPLOID HYBRID SPECIATION? EVOLUTION Schumer, M., Rosenthal, G. G., Andolfatto, P. 2014; 68 (6): 1553–60

  Abstract

  Hybridization has long been considered a process that prevents divergence between species. In contrast to this historical view, an increasing number of empirical studies claim to show evidence for hybrid speciation without a ploidy change. However, the importance of hybridization as a route to speciation is poorly understood, and many claims have been made with insufficient evidence that hybridization played a role in the speciation process. We propose criteria to determine the strength of evidence for homoploid hybrid speciation. Based on an evaluation of the literature using this framework, we conclude that although hybridization appears to be common, evidence for an important role of hybridization in homoploid speciation is more circumscribed.

  View details for DOI 10.1111/evo.12399

  View details for Web of Science ID 000337558900001

  View details for PubMedID 24620775

• PHYLOGENOMICS REVEALS EXTENSIVE RETICULATE EVOLUTION IN XIPHOPHORUS FISHES EVOLUTION Cui, R., Schumer, M., Kruesi, K., Walter, R., Andolfatto, P., Rosenthal, G. G. 2013; 67 (8): 2166–79

  Abstract

  Hybridization is increasingly being recognized as a widespread process, even between ecologically and behaviorally divergent animal species. Determining phylogenetic relationships in the presence of hybridization remains a major challenge for evolutionary biologists, but advances in sequencing technology and phylogenetic techniques are beginning to address these challenges. Here we reconstruct evolutionary relationships among swordtails and platyfishes (Xiphophorus: Poeciliidae), a group of species characterized by remarkable morphological diversity and behavioral barriers to interspecific mating. Past attempts to reconstruct phylogenetic relationships within Xiphophorus have produced conflicting results. Because many of the 26 species in the genus are interfertile, these conflicts are likely due to hybridization. Using genomic data, we resolve a high-confidence species tree of Xiphophorus that accounts for both incomplete lineage sorting and hybridization. Our results allow us to reexamine a long-standing controversy about the evolution of the sexually selected sword in Xiphophorus, and demonstrate that hybridization has been strikingly widespread in the evolutionary history of this genus.

  View details for DOI 10.1111/evo.12099

  View details for Web of Science ID 000322329500002

  View details for PubMedID 23888843

• Infestation by a Common Parasite is Correlated with Ant Symbiont Identity in a Plant-Ant Mutualism BIOTROPICA Schumer, M., Birger, R., Tantipathananandh, C., Aurisano, J., Maggioni, M., Mwangi, P. 2013; 45 (3): 276–79

  View details for DOI 10.1111/btp.12038

  View details for Web of Science ID 000318314900002

• Genetic accommodation and behavioural evolution: insights from genomic studies ANIMAL BEHAVIOUR Renn, S. P., Schumer, M. E. 2013; 85 (5): 1012–22

  View details for DOI 10.1016/j.anbehav.2013.02.012

  View details for Web of Science ID 000319332000019

• AN EVALUATION OF THE HYBRID SPECIATION HYPOTHESIS FOR XIPHOPHORUS CLEMENCIAE BASED ON WHOLE GENOME SEQUENCES EVOLUTION Schumer, M., Cui, R., Boussau, B., Walter, R., Rosenthal, G., Andolfatto, P. 2013; 67 (4): 1155–68

  Abstract

  Once thought rare in animal taxa, hybridization has been increasingly recognized as an important and common force in animal evolution. In the past decade, a number of studies have suggested that hybridization has driven speciation in some animal groups. We investigate the signature of hybridization in the genome of a putative hybrid species, Xiphophorus clemenciae, through whole genome sequencing of this species and its hypothesized progenitors. Based on analysis of this data, we find that X. clemenciae is unlikely to have been derived from admixture between its proposed parental species. However, we find significant evidence for recent gene flow between Xiphophorus species. Although we detect genetic exchange in two pairs of species analyzed, the proportion of genomic regions that can be attributed to hybrid origin is small, suggesting that strong behavioral premating isolation prevents frequent hybridization in Xiphophorus. The direction of gene flow between species is potentially consistent with a role for sexual selection in mediating hybridization.

  View details for DOI 10.1111/evo.12009

  View details for Web of Science ID 000317133800019

  View details for PubMedID 23550763

  View details for PubMedCentralID PMC3621027

• Parallel Molecular Evolution in an Herbivore Community SCIENCE Zhen, Y., Aardema, M. L., Medina, E. M., Schumer, M., Andolfatto, P. 2012; 337 (6102): 1634–37

  Abstract

  Numerous insects have independently evolved the ability to feed on plants that produce toxic secondary compounds called cardenolides and can sequester these compounds for use in their defense. We surveyed the protein target for cardenolides, the alpha subunit of the sodium pump, Na(+),K(+)-ATPase (ATPα), in 14 species that feed on cardenolide-producing plants and 15 outgroups spanning three insect orders. Despite the large number of potential targets for modulating cardenolide sensitivity, amino acid substitutions associated with host-plant specialization are highly clustered, with many parallel substitutions. Additionally, we document four independent duplications of ATPα with convergent tissue-specific expression patterns. We find that unique substitutions are disproportionately associated with recent duplications relative to parallel substitutions. Together, these findings support the hypothesis that adaptation tends to take evolutionary paths that minimize negative pleiotropy.

  View details for DOI 10.1126/science.1226630

  View details for Web of Science ID 000309215400039

  View details for PubMedID 23019645

  View details for PubMedCentralID PMC3770729

• Comparative gene expression profiles for highly similar aggressive phenotypes in male and female cichlid fishes (Julidochromis) JOURNAL OF EXPERIMENTAL BIOLOGY Schumer, M., Krishnakant, K., Renn, S. P. 2011; 214 (19): 3269–78

  Abstract

  Julidochromis marlieri and Julidochromis transcriptus are two closely related Tanganyikan cichlids that have evolved different behavior and mating strategies since they diverged from their common ancestor. While J. transcriptus follows the ancestral pattern of male dominance, male-biased sexual size dimorphism and territoriality, the pattern is reversed in J. marlieri. In J. marlieri, females show all of these behavioral and morphological characteristics. This raises the question of whether female J. marlieri achieve the dominant phenotype by expressing the same genes as J. transcriptus males or whether novel brain gene expression patterns have evolved to produce a similar behavioral phenotype in the females of J. marlieri. This study used cDNA microarrays to investigate whether female J. marlieri and male J. transcriptus show conserved or divergent patterns of brain gene expression. Analysis of microarray data in both species showed certain gene expression patterns associated with sex role independent of gonadal sex and, to a lesser extent, gene expression patterns associated with sex independent of sex role. In general, these data suggest that while there has been substantial divergence in gene expression patterns between J. transcriptus and J. marlieri, we can detect a highly significant overlap for a core set of genes related to aggression in both species. These results suggest that the proximate mechanisms regulating aggressive behavior in J. transcriptus and J. marlieri may be shared.

  View details for DOI 10.1242/jeb.055467

  View details for Web of Science ID 000294663300020

  View details for PubMedID 21900474

  View details for PubMedCentralID PMC3168378

• A serine cluster mediates BMAL1-dependent CLOCK phosphorylation and degradation CELL CYCLE Spengler, M. L., Kuropatwinski, K. K., Schumer, M., Antoch, M. P. 2009; 8 (24): 4138–46

  Abstract

  The circadian clock regulates biological processes from gene expression to organism behavior in a precise, sustained rhythm that is generated at the unicellular level by coordinated function of interlocked transcriptional feedback loops and post-translational modifications of core clock proteins. CLOCK phosphorylation regulates transcriptional activity, cellular localization and stability; however little is known about the specific residues and enzymes involved. We have identified a conserved cluster of serines that include, Ser431, which is a prerequisite phosphorylation site for the generation of BMAL dependent phospho-primed CLOCK and for the potential GSK-3 phosphorylation at Ser427. Mutational analysis and protein stability assays indicate that this serine cluster functions as a phospho-degron. Through the use of GSK-3 activators/inhibitors and kinase assays, we demonstrate that GSK-3beta regulates the degron site by increasing CLOCK phosphorylation/degradation, which correlates with an increase in the expression of CLOCK responsive promoters. Stabilization of phospho-deficient CLOCK delays the phase of oscillation in synchronized fibroblasts. This investigation begins the characterization of a complex phospho-regulatory site that controls the activity and degradation of CLOCK, a core transcription factor that is essential for circadian behavior.

  View details for DOI 10.4161/cc.8.24.10273

  View details for Web of Science ID 000273232300032

  View details for PubMedID 19946213

  View details for PubMedCentralID PMC4073639