1. Genetics and Genomics

High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species

  1. Molly Schumer  Is a corresponding author
  2. Rongfeng Cui
  3. Daniel Powell
  4. Rebecca Dresner
  5. Gil G Rosenthal
  6. Peter Andolfatto
  1. Princeton University, United States
  2. Texas A&M University, United States
https://doi.org/10.7554/eLife.02535
Share this article
Cite this article
  1. Molly Schumer
  2. Rongfeng Cui
  3. Daniel Powell
  4. Rebecca Dresner
  5. Gil G Rosenthal
  6. Peter Andolfatto
(2014)
High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species
eLife 3:e02535.
https://doi.org/10.7554/eLife.02535
  2. Download BibTeX
  3. Download .RIS

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.

Article and author information

Author details

  1. Molly Schumer

    Princeton University, Princeton, United States
    For correspondence
    schumer@princeton.edu
    Competing interests
    The authors declare that no competing interests exist.

  2. Rongfeng Cui

    Texas A&M University, College Station, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Daniel Powell

    Texas A&M University, College Station, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Rebecca Dresner

    Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Gil G Rosenthal

    Texas A&M University, College Station, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Peter Andolfatto

    Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: The procedures used in this study were approved by the Institutional Animal Care and Use Committee at Texas A&M University (Protocols # 2010-111 and 2012-164). Procedures were designed to minimize animal stress and suffering by using anesthesia during fin clipping and minimal handling of the fish. Samples were collected from the wild under Mexican federal collector's license FAUT-217 to W. Scott Monks.

Copyright

© 2014, Schumer et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 5,194
    views
  • 733
    downloads
  • 107
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Molly Schumer
  2. Rongfeng Cui
  3. Daniel Powell
  4. Rebecca Dresner
  5. Gil G Rosenthal
  6. Peter Andolfatto
(2014)
High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species
eLife 3:e02535.
https://doi.org/10.7554/eLife.02535

Share this article

https://doi.org/10.7554/eLife.02535

Categories and tags

Further reading

    1. Genetics and Genomics

    Genome-wide mapping in a house mouse hybrid zone reveals hybrid sterility loci and Dobzhansky-Muller interactions

    Leslie M Turner, Bettina Harr
    Research Article

    Mapping hybrid defects in contact zones between incipient species can identify genomic regions contributing to reproductive isolation and reveal genetic mechanisms of speciation. The house mouse features a rare combination of sophisticated genetic tools and natural hybrid zones between subspecies. Male hybrids often show reduced fertility, a common reproductive barrier between incipient species. Laboratory crosses have identified sterility loci, but each encompasses hundreds of genes. We map genetic determinants of testis weight and testis gene expression using offspring of mice captured in a hybrid zone between M. musculus musculus and M. m. domesticus. Many generations of admixture enables high-resolution mapping of loci contributing to these sterility-related phenotypes. We identify complex interactions among sterility loci, suggesting multiple, non-independent genetic incompatibilities contribute to barriers to gene flow in the hybrid zone.

  2. Hybrid approach: Listen to Molly Schumer discuss how different species remain distinct

    Podcast

    How do different species remain distinct if they can mate with each other to produce hybrid offspring?

    1. Genetics and Genomics
    2. Immunology and Inflammation

    ACK1 and BRK non-receptor tyrosine kinase deficiencies are associated with familial systemic lupus and involved in efferocytosis

    Stephanie Guillet, Tomi Lazarov ... Frédéric Geissmann
    Research Article

    Systemic lupus erythematosus (SLE) is an autoimmune disease, the pathophysiology and genetic basis of which are incompletely understood. Using a forward genetic screen in multiplex families with SLE, we identified an association between SLE and compound heterozygous deleterious variants in the non-receptor tyrosine kinases (NRTKs) ACK1 and BRK. Experimental blockade of ACK1 or BRK increased circulating autoantibodies in vivo in mice and exacerbated glomerular IgG deposits in an SLE mouse model. Mechanistically, NRTKs regulate activation, migration, and proliferation of immune cells. We found that the patients’ ACK1 and BRK variants impair efferocytosis, the MERTK-mediated anti-inflammatory response to apoptotic cells, in human induced pluripotent stem cell (hiPSC)-derived macrophages, which may contribute to SLE pathogenesis. Overall, our data suggest that ACK1 and BRK deficiencies are associated with human SLE and impair efferocytosis in macrophages.