Unique structure and positive selection promote the rapid divergence of Drosophila Y chromosomes
- University of Rochester, United States
- Cornell University, United States
- 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).
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Genome sequencing of males in Drosophila simulans cladeNCBI Bioproject, PRJNA748438.
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Unique structure and positive selection promote the rapid divergence of Drosophila Y chromosomesDryad Digital Repository, doi:10.5061/dryad.280gb5mr6.
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Drosophila mauritiana Genome sequencingNCBI Bioproject, PRJNA158675.
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DSPR Founder GenomesNCBI Bioproject, PRJNA418342.
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Drosophila simulans Raw sequence readsNCBI Bioproject, PRJNA477366.
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Novel quality metrics identify high-quality assemblies of piRNA clustersNCBI Bioproject, PRJNA618654.
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Nanopore-based assembly of many drosophilid genomesNCBI Bioproject, PRJNA675888.
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Transcriptome sequencing of Drosophila simulans cladeNCBI Bioproject, PRJNA541548.
Article and author information
Author details
Colin D Meiklejohn
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
- Daniel R Matute, University of North Carolina, Chapel Hill, United States
Publication history
- Received: November 24, 2021
- Accepted: December 18, 2021
- Accepted Manuscript published: January 6, 2022 (version 1)
- 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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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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