Endoparasitoid lifestyle promotes endogenization and domestication of dsDNA viruses

Author:

Guinet Benjamin1ORCID,Lepetit David1ORCID,Charlat Sylvain1ORCID,Buhl Peter N2,Notton David G3ORCID,Cruaud Astrid4,Rasplus Jean-Yves4ORCID,Stigenberg Julia5,de Vienne Damien M1ORCID,Boussau Bastien1ORCID,Varaldi Julien1ORCID

Affiliation:

1. Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR 5558, F-69622

2. Zoological Museum, Department of Entomology, University of Copenhagen, Universitetsparken

3. Natural Sciences Department, National Museums Collection Centre

4. INRAE, UMR 1062 CBGP, 755 avenue 11 du campus Agropolis CS 30016, 34988

5. Department of Zoology, Swedish Museum of Natural History

Abstract

The accidental endogenization of viral elements within eukaryotic genomes can occasionally provide significant evolutionary benefits, giving rise to their long-term retention, that is, to viral domestication. For instance, in some endoparasitoid wasps (whose immature stages develop inside their hosts), the membrane-fusion property of double-stranded DNA viruses have been repeatedly domesticated following ancestral endogenizations. The endogenized genes provide female wasps with a delivery tool to inject virulence factors that are essential to the developmental success of their offspring. Because all known cases of viral domestication involve endoparasitic wasps, we hypothesized that this lifestyle, relying on a close interaction between individuals, may have promoted the endogenization and domestication of viruses. By analyzing the composition of 124 Hymenoptera genomes, spread over the diversity of this clade and including free-living, ecto, and endoparasitoid species, we tested this hypothesis. Our analysis first revealed that double-stranded DNA viruses, in comparison with other viral genomic structures (ssDNA, dsRNA, ssRNA), are more often endogenized and domesticated (that is, retained by selection) than expected from their estimated abundance in insect viral communities. Second, our analysis indicates that the rate at which dsDNA viruses are endogenized is higher in endoparasitoids than in ectoparasitoids or free-living hymenopterans, which also translates into more frequent events of domestication. Hence, these results are consistent with the hypothesis that the endoparasitoid lifestyle has facilitated the endogenization of dsDNA viruses, in turn, increasing the opportunities of domestications that now play a central role in the biology of many endoparasitoid lineages.

Funder

Agence Nationale de la Recherche

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

Reference108 articles.

1. Alonso C. 2023. ICTV Report Chapter. Virus Taxonomy The ICTV Report on Virus Classification and Taxon Nomenclature Asfarviridae Chapter.

2. Evolutionary history of endogenous human Herpesvirus 6 reflects human migration out of Africa;Aswad;Molecular Biology and Evolution,2021

3. Genomic and Proteomic analyses indicate that Banchine and Campoplegine Polydnaviruses have Sim- Ilar, if not identical, viral ancestors;Béliveau;Journal of Virology,2015

4. Polydnaviruses of Braconid Wasps derive from an ancestral Nudivirus;Bézier;Science,2009

5. Understanding Computational Bayesian Statistics

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