Epistatic selection on a selfish Segregation Distorter supergene: drive, recombination, and genetic load
- University of Granada, Spain
- University of Rochester, United States
Abstract
Meiotic drive supergenes are complexes of alleles at linked loci that together subvert Mendelian segregation resulting in preferential transmission. In males, the most common mechanism of drive involves the disruption of sperm bearing one of a pair of alternative alleles. While at least two loci are important for male drive- the driver and the target- linked modifiers can enhance drive, creating selection pressure to suppress recombination. In this work, we investigate the evolution and genomic consequences of an autosomal, multilocus, male meiotic drive system, Segregation Distorter (SD) in the fruit fly, Drosophila melanogaster. In African populations, the predominant SD chromosome variant, SD-Mal, is characterized by two overlapping, paracentric inversions on chromosome arm 2R and nearly perfect (~100%) transmission. We study the SD-Mal system in detail, exploring its components, chromosomal structure, and evolutionary history. Our findings reveal a recent chromosome-scale selective sweep mediated by strong epistatic selection for haplotypes carrying Sd, the main driving allele, and one or more factors within the double inversion. While most SD-Mal chromosomes are homozygous lethal, SD-Mal haplotypes can recombine with other, complementing haplotypes via crossing over, and with wildtype chromosomes via gene conversion. SD-Mal chromosomes have nevertheless accumulated lethal mutations, excess non-synonymous mutations, and excess transposable element insertions. Therefore, SD-Mal haplotypes evolve as a small, semi-isolated subpopulation with a history of strong selection. These results may explain the evolutionary turnover of SD haplotypes in different populations around the world, and have implications for supergene evolution broadly.
Data availability
Raw sequence data are deposited in NCBI's short read archive under project accession PRJNA649752. All code for data analysis and figure generation is available in Github (https://github.com/bnavarrodominguez/sd_popgen). Data and code will be deposited in Dryad digital repository.
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Epistatic selection on a selfish Segregation Distorter supergene: drive, recombination, and genetic loadDryad Digital Repository, doi:10.5061/dryad.4qrfj6qch.
Article and author information
Author details
Beatriz Navarro-Dominguez
Amanda M Larracuente
Funding
National Institute of General Medical Sciences (R35 GM119515)
- Amanda M Larracuente
Stephen Biggar and Elisabeth Asaro Fellowship in Data Science (NA)
- Amanda M Larracuente
David and Lucile Packard Foundation
- Daven C Presgraves
University of Rochester funds
- Daven C Presgraves
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Detlef Weigel, Max Planck Institute for Biology Tübingen, Germany
Version history
- Preprint posted: December 24, 2021 (view preprint)
- Received: April 3, 2022
- Accepted: April 20, 2022
- Accepted Manuscript published: April 29, 2022 (version 1)
- Accepted Manuscript updated: May 3, 2022 (version 2)
- Version of Record published: May 20, 2022 (version 3)
Copyright
© 2022, Navarro-Dominguez 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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Epistatic selection on a selfish Segregation Distorter supergene: drive, recombination, and genetic load
eLife 11:e78981.
https://doi.org/10.7554/eLife.78981
Further reading
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Copy number variation in large gene families is well characterized for plant resistance genes, but similar studies are rare in animals. The zebrafish (Danio rerio) has hundreds of NLR immune genes, making this species ideal for studying this phenomenon. By sequencing 93 zebrafish from multiple wild and laboratory populations, we identified a total of 1513 NLRs, many more than the previously known 400. Approximately half of those are present in all wild populations, but only 4% were found in 80% or more of the individual fish. Wild fish have up to two times as many NLRs per individual and up to four times as many NLRs per population than laboratory strains. In contrast to the massive variability of gene copies, nucleotide diversity in zebrafish NLR genes is very low: around half of the copies are monomorphic and the remaining ones have very few polymorphisms, likely a signature of purifying selection.
