Unique structure and positive selection promote the rapid divergence of Drosophila Y chromosomes
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
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
-
- 2,773
- views
-
- 361
- downloads
-
- 28
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
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)
Further reading
-
- Evolutionary Biology
Spatial patterns in genetic diversity are shaped by individuals dispersing from their parents and larger-scale population movements. It has long been appreciated that these patterns of movement shape the underlying genealogies along the genome leading to geographic patterns of isolation-by-distance in contemporary population genetic data. However, extracting the enormous amount of information contained in genealogies along recombining sequences has, until recently, not been computationally feasible. Here, we capitalize on important recent advances in genome-wide gene-genealogy reconstruction and develop methods to use thousands of trees to estimate per-generation dispersal rates and to locate the genetic ancestors of a sample back through time. We take a likelihood approach in continuous space using a simple approximate model (branching Brownian motion) as our prior distribution of spatial genealogies. After testing our method with simulations we apply it to Arabidopsis thaliana. We estimate a dispersal rate of roughly 60 km2/generation, slightly higher across latitude than across longitude, potentially reflecting a northward post-glacial expansion. Locating ancestors allows us to visualize major geographic movements, alternative geographic histories, and admixture. Our method highlights the huge amount of information about past dispersal events and population movements contained in genome-wide genealogies.
-
- Evolutionary Biology
Understanding the genomic basis of natural variation in plant pest resistance is an important goal in plant science, but it usually requires large and labor-intensive phenotyping experiments. Here, we explored the possibility that non-target reads from plant DNA sequencing can serve as phenotyping proxies for addressing such questions. We used data from a whole-genome and -epigenome sequencing study of 207 natural lines of field pennycress (Thlaspi arvense) that were grown in a common environment and spontaneously colonized by aphids, mildew, and other microbes. We found that the numbers of non-target reads assigned to the pest species differed between populations, had significant SNP-based heritability, and were associated with climate of origin and baseline glucosinolate contents. Specifically, pennycress lines from cold and thermally fluctuating habitats, presumably less favorable to aphids, showed higher aphid DNA load, i.e., decreased aphid resistance. Genome-wide association analyses identified genetic variants at known defense genes but also novel genomic regions associated with variation in aphid and mildew DNA load. Moreover, we found several differentially methylated regions associated with pathogen loads, in particular differential methylation at transposons and hypomethylation in the promoter of a gene involved in stomatal closure, likely induced by pathogens. Our study provides first insights into the defense mechanisms of Thlaspi arvense, a rising crop and model species, and demonstrates that non-target whole-genome sequencing reads, usually discarded, can be leveraged to estimate intensities of plant biotic interactions. With rapidly increasing numbers of large sequencing datasets worldwide, this approach should have broad application in fundamental and applied research.