Unique structure and positive selection promote the rapid divergence of Drosophila Y chromosomes

  1. Ching-Ho Chang  Is a corresponding author
  2. Lauren E Gregory
  3. Kathleen E Gordon
  4. Colin D Meiklejohn
  5. Amanda M Larracuente  Is a corresponding author
  1. University of Rochester, United States
  2. Cornell University, United States
  3. University of Nebraska-Lincoln, United States

Abstract

Y chromosomes across diverse species convergently evolve a gene-poor, heterochromatic organization enriched for duplicated genes, LTR retrotransposons, and satellite DNA. Sexual antagonism and a loss of recombination play major roles in the degeneration of young Y chromosomes. However, the processes shaping the evolution of mature, already degenerated Y chromosomes are less well-understood. Because Y chromosomes evolve rapidly, comparisons between closely related species are particularly useful. We generated de novo long read assemblies complemented with cytological validation to reveal Y chromosome organization in three closely related species of the Drosophila simulans complex, which diverged only 250,000 years ago and share >98% sequence identity. We find these Y chromosomes are divergent in their organization and repetitive DNA composition and discover new Y-linked gene families whose evolution is driven by both positive selection and gene conversion. These Y chromosomes are also enriched for large deletions, suggesting that the repair of double-strand breaks on Y chromosomes may be biased toward microhomology-mediated end joining over canonical non-homologous end-joining. We propose that this repair mechanism contributes to the convergent evolution of Y chromosome organization across organisms.

Data availability

Genomic DNA sequence reads are in NCBI's SRA under BioProject PRJNA748438.All scripts and pipelines are available in GitHub(https://github.com/LarracuenteLab/simclade_Y) and the Dryad digital repository (doi:10.5061/dryad.280gb5mr6).

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Ching-Ho Chang

    Department of Biology, University of Rochester, Rochester, United States
    For correspondence
    cchang2@fredhutch.org
    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
  2. Lauren E Gregory

    Department of Biology, University of Rochester, Rochester, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Kathleen E Gordon

    Department of Molecular Biology and Genetics, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Colin D Meiklejohn

    School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2708-8316
  5. 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.

Funding

National Institute of General Medical Sciences (R35GM119515)

  • Amanda M Larracuente

National Institute of General Medical Sciences (R01GM123194)

  • Colin D Meiklejohn

National Science Foundation (MCB 1844693)

  • Amanda M Larracuente

Damon Runyon Cancer Research Foundation (DRG: 2438-21)

  • Ching-Ho Chang

College of Arts and Sciences, University of Nebraska-Lincoln

  • Colin D Meiklejohn

University of Rochester

  • Amanda M Larracuente

University of Rochester

  • Ching-Ho Chang

Ministry of Education, Taiwan

  • Ching-Ho Chang

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

Reviewing Editor

  1. Daniel R Matute, University of North Carolina, Chapel Hill, United States

Publication history

  1. Received: November 24, 2021
  2. Accepted: December 18, 2021
  3. Accepted Manuscript published: January 6, 2022 (version 1)
  4. Version of Record published: January 27, 2022 (version 2)

Copyright

© 2022, Chang 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. Ching-Ho Chang
  2. Lauren E Gregory
  3. Kathleen E Gordon
  4. Colin D Meiklejohn
  5. Amanda M Larracuente
(2022)
Unique structure and positive selection promote the rapid divergence of Drosophila Y chromosomes
eLife 11:e75795.
https://doi.org/10.7554/eLife.75795

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