A genetic basis for facultative parthenogenesis in Drosophila
Abstract
Facultative parthenogenesis enables sexually reproducing organisms to switch between sexual and asexual parthenogenetic reproduction. To gain insights into this phenomenon, we sequenced the genomes of sexually reproducing and parthenogenetic strains of Drosophila mercatorum and identified differences in the gene expression in their eggs. We then tested whether manipulating the expression of candidate gene homologs identified in Drosophila mercatorum could lead to facultative parthenogenesis in the non-parthenogenetic species Drosophila melanogaster. This identified a polygenic system whereby increased expression of the mitotic protein kinase polo and decreased expression of a desaturase, Desat2, caused facultative parthenogenesis in the non-parthenogenetic species that was enhanced by increased expression of Myc. The genetically induced parthenogenetic Drosophila melanogaster eggs exhibit de novo centrosome formation, fusion of the meiotic products, and the onset of development to generate predominantly triploid offspring. Thus, we demonstrate a genetic basis for sporadic facultative parthenogenesis in an animal.
Copyright and License
© 2023 The Authors. Published by Elsevier Under a Creative Commons license - Attribution 4.0 International (CC BY 4.0)
Acknowledgement
We would like to thank Isabel Palacios, John Welch, and Jose Casal for reading the manuscript and/or discussions about the work. We would like to thank Richard Durbin for advice, discussions, and computation assistance and Frank Jiggins for advice and discussions. We would like to thank Jonathan Day (Frank Jiggins's Lab) and Bettina Fischer (Richard Durbin's Lab) for advice on library preparation, technical assistance, protocols, reagents, and endless patience. We would like to thank Harry Choi and Mike Liu from Molecular Instruments for troubleshooting and for gifted reagents during optimization of the HCR in situ protocol for use on DNA. We thank Pallavi Panda for a transgenic Rcd4 fly stock, Paula Almeida-Coelho for technical advice on in situ hybridization and karyotyping techniques, and Frank Sprenger for flies, kindly brought to Cambridge. We are grateful to the Genetics Fly Facility for embryo injections, particularly Dr. Alla Madich for multiple attempts to develop transgenics in D. mercatorum. We thank TRiP at Harvard Medical School (NIH/NIGMS R01-GM084947) for providing transgenic RNAi fly stocks used in this study. The genomics analysis was supported by NIH/NIDA U01DA047638 and NIH/NIGMS R01GM123489 (E.G.). The biological and gene expression work was supported by the Leverhulme Trust Project Grant (RPG-2018-229) and the Wellcome Trust Institutional Strategic Support Fund (RG89305) (D.M.G. and A.L.S.).
Contributions
A.L.S. conceived this study, performed all biological experiments, and wrote the first draft of the manuscript. D.K.F. performed all gene expression related analysis and genome annotations. E.G. performed all genomics related analysis. A.L.S., D.K.F., E.G., and D.M.G. contributed to choices in methodology, experimental design, and the interpretation of results. Funding for the genomics analysis was obtained by E.G. The funding for all biological experiments, data, and gene expression analysis was obtained by A.L.S. and D.M.G.
Conflict of Interest
The authors declare no competing interests.
Data Availability
- All code is publicly available. The genome assembly, analysis, and quality control code are on https://github.com/ekg/Drosophila. The annotation, transcriptomics analysis, and quality control code are on https://github.com/FabianDK/drosophila_parthenogenesis
- All raw and analyzed D. mercatorum genomic data is available on ENA (European Nucleotide Archive): PRJEB64421.
- The gene expression data generated by this study is on ENA: PRJEB43100.
- Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request.
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Additional details
- DOI
- 10.1016/j.cub.2023.07.006
- PMCID
- PMC11044649
- National Institutes of Health
- R01-GM084947
- National Institutes of Health
- U01DA047638
- National Institutes of Health
- R01GM123489
- Leverhulme Trust
- RPG-2018-229
- Wellcome Trust
- RG89305
- Caltech groups
- Division of Biology and Biological Engineering