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

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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

(2021) Genome sequencing of males in Drosophila simulans clade
NCBI Bioproject, PRJNA748438.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA748438
(2021) Unique structure and positive selection promote the rapid divergence of Drosophila Y chromosomes
Dryad Digital Repository, doi:10.5061/dryad.280gb5mr6.

https://datadryad.org/stash/share/aCTfiGeOA2P8xvVi_CrKTJiFZ1NKTyqBWIB-sS3h57Q

The following previously published data sets were used

1. Garrigan et al.
(2012) Drosophila mauritiana Genome sequencing
NCBI Bioproject, PRJNA158675.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA158675
1. Modencode
2. Smibert et al.
(2012) D. melanogaster Dissected Tissue RNASeq
NCBI study, SRP003905.

https://trace.ncbi.nlm.nih.gov/Traces/sra/?study=SRP003905
1. Gerstein et al.
(2014) modENCODE D. melanogaster Developmental Total RNA-Seq
NCBI study, SRP001696.

https://trace.ncbi.nlm.nih.gov/Traces/sra/?study=SRP001696
1. Chakraborty et al.
(2017) DSPR Founder Genomes
NCBI Bioproject, PRJNA418342.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA418342/
1. Wei et al.
(2018) D. melanogaster, D. simulans, D. sechellia, D. erecta, D. ananassae, D. pseudoobscura, D. persimilis, D mojavensis, and D. virilis Raw sequence reads
NCBI Bioproject, PRJNA423291.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA423291
1. Laktionov et. al.
(2018) Genome-wide profiling of gene expression and transcription factors binding reveals new insights into the mechanisms of gene regulation during Drosophila spermatogenesis [RNA-Seq]
NCBI Bioproject, PRJNA380909.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA380909
1. Lin et al.
(2018) Drosophila simulans Raw sequence reads
NCBI Bioproject, PRJNA477366.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA477366
1. Shah et al.
(2020) Novel quality metrics identify high-quality assemblies of piRNA clusters
NCBI Bioproject, PRJNA618654.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA618654/
1. Kim BY et al.
(2021) Nanopore-based assembly of many drosophilid genomes
NCBI Bioproject, PRJNA675888.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA675888/
1. Chakraborty et al.
(2021) Transcriptome sequencing of Drosophila simulans clade
NCBI Bioproject, PRJNA541548.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA541548

Article and author information

Author details

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.

"This ORCID iD identifies the author of this article:" 0000-0001-9361-1190
Lauren E Gregory

Department of Biology, University of Rochester, Rochester, United States

Competing interests
The authors declare that no competing interests exist.
Kathleen E Gordon

Department of Molecular Biology and Genetics, Cornell University, Ithaca, United States

Competing interests
The authors declare that no competing interests exist.
Colin D Meiklejohn

School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-2708-8316
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.

Copyright

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.