Pervasive gene flow despite strong and varied reproductive barriers in swordtails

The evolution of reproductive barriers leads to the formation of new species. However, recent research has demonstrated that hybridization has been pervasive across the tree of life even in the presence of strong barriers. Using swordtail fishes (genus Xiphophorus), an emerging model system, we document overlapping mechanisms that act as barriers to gene flow between Xiphophorus birchmanni and Xiphophorus cortezi by combining genomic sequencing from natural hybrid populations, experimental laboratory crosses, behavioural assays, sperm measures and developmental studies. We show that assortative mating plays a role in maintaining subpopulations with distinct ancestry within natural hybrid populations. Using F<sub>2</sub> 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 Xiphophorus 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 × X. birchmanni hybrids as in X. malinche × 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.

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Publication Details

Journal
Nature Ecology & Evolution
Published
2025-03-26
DOI
https://doi.org/10.1038/s41559-025-02669-9
Citations
10
Primary Topic
Genetic diversity and population structure
Type
article
Field-Weighted Citation Impact
18.17

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article

Pervasive gene flow despite strong and varied reproductive barriers in swordtails

Carla Gutiérrez‐Rodríguez, Paola Fascinetto‐Zago, Quinn K. Langdon, Oscar Ríos-Cárdenas et al.
10 citations
Nature Ecology & Evolution
Genetic diversity and population structure
18.17
article

Pervasive gene flow despite strong and varied reproductive barriers in swordtails

Carla Gutiérrez‐Rodríguez, Paola Fascinetto‐Zago, Quinn K. Langdon, Oscar Ríos-Cárdenas, John J. Baczenas, Benjamin M. Moran, Stepfanie M. Aguillon, Alexandra Donny, Molly R. Morris, Theresa Gunn, Molly Schumer, Daniel L. Powell, Shreya M. Banerjee, Sophia K Haase Cox
article en
10 citations

Abstract

The evolution of reproductive barriers leads to the formation of new species. However, recent research has demonstrated that hybridization has been pervasive across the tree of life even in the presence of strong barriers. Using swordtail fishes (genus Xiphophorus), an emerging model system, we document overlapping mechanisms that act as barriers to gene flow between Xiphophorus birchmanni and Xiphophorus cortezi by combining genomic sequencing from natural hybrid populations, experimental laboratory crosses, behavioural assays, sperm measures and developmental studies. We show that assortative mating plays a role in maintaining subpopulations with distinct ancestry within natural hybrid populations. Using F<sub>2</sub> 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 Xiphophorus 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 × X. birchmanni hybrids as in X. malinche × 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.

Nature Ecology & EvolutionVol. 9(5)
Louisiana State University (US), Gladstone Institutes (US), Howard Hughes Medical Institute (US), University of California, Los Angeles (US), University of Washington (US), Ohio University (US), Instituto de Ecología (MX), Centro de Investigaciones Cientifícas de las Huastecas 'Aguazarca' (MX), University of California, Davis (US), Stanford University (US)
National Science Foundation, Foundation for the National Institutes of Health, Howard Hughes Medical Institute, Alfred P. Sloan Foundation, Stanford University, Ohio University, Center for Computational, Evolutionary and Human Genomics, Stanford University
Life in Land
Openalex Percentile: Top 1%
Genetic diversity and population structure
18.17
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