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

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.

Reviewing Editor

  1. Gil McVean, Oxford University, United Kingdom

Publication history

  1. Received: February 14, 2014
  2. Accepted: June 2, 2014
  3. Accepted Manuscript published: June 4, 2014 (version 1)
  4. Version of Record published: July 8, 2014 (version 2)

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

  • 4,970
    Page views
  • 659
    Downloads
  • 67
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

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

Further reading

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

    1. Developmental Biology
    2. Genetics and Genomics
    Melanie MY Chan, Omid Sadeghi-Alavijeh ... Daniel P Gale
    Research Article Updated

    Posterior urethral valves (PUV) are the commonest cause of end-stage renal disease in children, but the genetic architecture of this rare disorder remains unknown. We performed a sequencing-based genome-wide association study (seqGWAS) in 132 unrelated male PUV cases and 23,727 controls of diverse ancestry, identifying statistically significant associations with common variants at 12q24.21 (p=7.8 × 10−12; OR 0.4) and rare variants at 6p21.1 (p=2.0 × 10-8; OR 7.2), that were replicated in an independent European cohort of 395 cases and 4151 controls. Fine mapping and functional genomic data mapped these loci to the transcription factor TBX5 and planar cell polarity gene PTK7, respectively, the encoded proteins of which were detected in the developing urinary tract of human embryos. We also observed enrichment of rare structural variation intersecting with candidate cis-regulatory elements, particularly inversions predicted to affect chromatin looping (p=3.1 × 10-5). These findings represent the first robust genetic associations of PUV, providing novel insights into the underlying biology of this poorly understood disorder and demonstrate how a diverse ancestry seqGWAS can be used for disease locus discovery in a rare disease.