Epistatic selection on a selfish Segregation Distorter supergene: drive, recombination, and genetic load

  1. Beatriz Navarro-Dominguez
  2. Ching-Ho Chang
  3. Cara L Brand
  4. Christina A Muirhead
  5. Daven C Presgraves  Is a corresponding author
  6. Amanda M Larracuente  Is a corresponding author
  1. University of Granada, Spain
  2. University of Rochester, United States

Abstract

Meiotic drive supergenes are complexes of alleles at linked loci that together subvert Mendelian segregation resulting in preferential transmission. In males, the most common mechanism of drive involves the disruption of sperm bearing one of a pair of alternative alleles. While at least two loci are important for male drive- the driver and the target- linked modifiers can enhance drive, creating selection pressure to suppress recombination. In this work, we investigate the evolution and genomic consequences of an autosomal, multilocus, male meiotic drive system, Segregation Distorter (SD) in the fruit fly, Drosophila melanogaster. In African populations, the predominant SD chromosome variant, SD-Mal, is characterized by two overlapping, paracentric inversions on chromosome arm 2R and nearly perfect (~100%) transmission. We study the SD-Mal system in detail, exploring its components, chromosomal structure, and evolutionary history. Our findings reveal a recent chromosome-scale selective sweep mediated by strong epistatic selection for haplotypes carrying Sd, the main driving allele, and one or more factors within the double inversion. While most SD-Mal chromosomes are homozygous lethal, SD-Mal haplotypes can recombine with other, complementing haplotypes via crossing over, and with wildtype chromosomes via gene conversion. SD-Mal chromosomes have nevertheless accumulated lethal mutations, excess non-synonymous mutations, and excess transposable element insertions. Therefore, SD-Mal haplotypes evolve as a small, semi-isolated subpopulation with a history of strong selection. These results may explain the evolutionary turnover of SD haplotypes in different populations around the world, and have implications for supergene evolution broadly.

Data availability

Raw sequence data are deposited in NCBI's short read archive under project accession PRJNA649752. All code for data analysis and figure generation is available in Github (https://github.com/bnavarrodominguez/sd_popgen). Data and code will be deposited in Dryad digital repository.

The following data sets were generated

Article and author information

Author details

  1. Beatriz Navarro-Dominguez

    Department of Genetics, University of Granada, Granada, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4077-8696
  2. Ching-Ho Chang

    Department of Biology, University of Rochester, Rochester, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9361-1190
  3. Cara L Brand

    Department of Biology, University of Rochester, Rochester, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Christina A Muirhead

    Department of Biology, University of Rochester, Rochester, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Daven C Presgraves

    Department of Biology, University of Rochester, Rochester, United States
    For correspondence
    daven.presgraves@rochester.edu
    Competing interests
    The authors declare that no competing interests exist.
  6. Amanda M Larracuente

    Department of Biology, University of Rochester, Rochester, United States
    For correspondence
    alarracu@UR.Rochester.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5944-5686

Funding

National Institute of General Medical Sciences (R35 GM119515)

  • Amanda M Larracuente

Stephen Biggar and Elisabeth Asaro Fellowship in Data Science (NA)

  • Amanda M Larracuente

David and Lucile Packard Foundation

  • Daven C Presgraves

University of Rochester funds

  • Daven C Presgraves

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Detlef Weigel, Max Planck Institute for Biology Tübingen, Germany

Version history

  1. Preprint posted: December 24, 2021 (view preprint)
  2. Received: April 3, 2022
  3. Accepted: April 20, 2022
  4. Accepted Manuscript published: April 29, 2022 (version 1)
  5. Accepted Manuscript updated: May 3, 2022 (version 2)
  6. Version of Record published: May 20, 2022 (version 3)

Copyright

© 2022, Navarro-Dominguez 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.

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  1. Beatriz Navarro-Dominguez
  2. Ching-Ho Chang
  3. Cara L Brand
  4. Christina A Muirhead
  5. Daven C Presgraves
  6. Amanda M Larracuente
(2022)
Epistatic selection on a selfish Segregation Distorter supergene: drive, recombination, and genetic load
eLife 11:e78981.
https://doi.org/10.7554/eLife.78981

Share this article

https://doi.org/10.7554/eLife.78981

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