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).
-
Genome sequencing of males in Drosophila simulans cladeNCBI Bioproject, PRJNA748438.
-
Unique structure and positive selection promote the rapid divergence of Drosophila Y chromosomesDryad Digital Repository, doi:10.5061/dryad.280gb5mr6.
-
Drosophila mauritiana Genome sequencingNCBI Bioproject, PRJNA158675.
-
DSPR Founder GenomesNCBI Bioproject, PRJNA418342.
-
Drosophila simulans Raw sequence readsNCBI Bioproject, PRJNA477366.
-
Novel quality metrics identify high-quality assemblies of piRNA clustersNCBI Bioproject, PRJNA618654.
-
Nanopore-based assembly of many drosophilid genomesNCBI Bioproject, PRJNA675888.
-
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.
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.
Metrics
-
- 2,891
- views
-
- 370
- downloads
-
- 32
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
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)
Unique structure and positive selection promote the rapid divergence of Drosophila Y chromosomes
eLife 11:e75795.
https://doi.org/10.7554/eLife.75795
Further reading
-
- Evolutionary Biology
- Genetics and Genomics
Cattle (Bos taurus) play an important role in the life of humans in the Iberian Peninsula not just as a food source but also in cultural events. When domestic cattle were first introduced to Iberia, wild aurochs (Bos primigenius) were still present, leaving ample opportunity for mating (whether intended by farmers or not). Using a temporal bioarchaeological dataset covering eight millennia, we trace gene flow between the two groups. Our results show frequent hybridisation during the Neolithic and Chalcolithic, likely reflecting a mix of hunting and herding or relatively unmanaged herds, with mostly male aurochs and female domestic cattle involved. This is supported by isotopic evidence consistent with ecological niche sharing, with only a few domestic cattle possibly being managed. The proportion of aurochs ancestry in domestic cattle remains relatively constant from about 4000 years ago, probably due to herd management and selection against first generation hybrids, coinciding with other cultural transitions. The constant level of wild ancestry (~20%) continues into modern Western European breeds including Iberian cattle selected for aggressiveness and fighting ability. This study illuminates the genomic impact of human actions and wild introgression in the establishment of cattle as one of the most important domestic species today.
-
- Evolutionary Biology
- Genetics and Genomics
Expression quantitative trait loci (eQTLs) provide a key bridge between noncoding DNA sequence variants and organismal traits. The effects of eQTLs can differ among tissues, cell types, and cellular states, but these differences are obscured by gene expression measurements in bulk populations. We developed a one-pot approach to map eQTLs in Saccharomyces cerevisiae by single-cell RNA sequencing (scRNA-seq) and applied it to over 100,000 single cells from three crosses. We used scRNA-seq data to genotype each cell, measure gene expression, and classify the cells by cell-cycle stage. We mapped thousands of local and distant eQTLs and identified interactions between eQTL effects and cell-cycle stages. We took advantage of single-cell expression information to identify hundreds of genes with allele-specific effects on expression noise. We used cell-cycle stage classification to map 20 loci that influence cell-cycle progression. One of these loci influenced the expression of genes involved in the mating response. We showed that the effects of this locus arise from a common variant (W82R) in the gene GPA1, which encodes a signaling protein that negatively regulates the mating pathway. The 82R allele increases mating efficiency at the cost of slower cell-cycle progression and is associated with a higher rate of outcrossing in nature. Our results provide a more granular picture of the effects of genetic variants on gene expression and downstream traits.
