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
-
- 2,936
- views
-
- 372
- 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
Mammalian gut microbiomes are highly dynamic communities that shape and are shaped by host aging, including age-related changes to host immunity, metabolism, and behavior. As such, gut microbial composition may provide valuable information on host biological age. Here, we test this idea by creating a microbiome-based age predictor using 13,563 gut microbial profiles from 479 wild baboons collected over 14 years. The resulting ‘microbiome clock’ predicts host chronological age. Deviations from the clock’s predictions are linked to some demographic and socio-environmental factors that predict baboon health and survival: animals who appear old-for-age tend to be male, sampled in the dry season (for females), and have high social status (both sexes). However, an individual’s ‘microbiome age’ does not predict the attainment of developmental milestones or lifespan. Hence, in our host population, gut microbiome age largely reflects current, as opposed to past, social and environmental conditions, and does not predict the pace of host development or host mortality risk. We add to a growing understanding of how age is reflected in different host phenotypes and what forces modify biological age in primates.
-
- Evolutionary Biology
A major question in animal evolution is how genotypic and phenotypic changes are related, and another is when and whether ancient gene order is conserved in living clades. Chitons, the molluscan class Polyplacophora, retain a body plan and general morphology apparently little changed since the Palaeozoic. We present a comparative analysis of five reference quality genomes, including four de novo assemblies, covering all major chiton clades, and an updated phylogeny for the phylum. We constructed 20 ancient molluscan linkage groups (MLGs) and show that these are relatively conserved in bivalve karyotypes, but in chitons they are subject to re-ordering, rearrangement, fusion, or partial duplication and vary even between congeneric species. The largest number of novel fusions is in the most plesiomorphic clade Lepidopleurida, and the chitonid Liolophura japonica has a partial genome duplication, extending the occurrence of large-scale gene duplication within Mollusca. The extreme and dynamic genome rearrangements in this class stands in contrast to most other animals, demonstrating that chitons have overcome evolutionary constraints acting on other animal groups. The apparently conservative phenome of chitons belies rapid and extensive changes in genome.
