1. Endoparasitoid lifestyle promotes endogenization and domestication of dsDNA viruses
- Author
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Benjamin Guinet, David Lepetit, Sylvain Charlat, Peter N Buhl, David G Notton, Astrid Cruaud, Jean-Yves Rasplus, Julia Stigenberg, Damien M. de Vienne, Boussau Bastien, Julien Varaldi, Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Zoological Museum [Copenhagen], Natural History Museum of Denmark, Faculty of Science [Copenhagen], University of Copenhagen = Københavns Universitet (UCPH)-University of Copenhagen = Københavns Universitet (UCPH)-Faculty of Science [Copenhagen], University of Copenhagen = Københavns Universitet (UCPH)-University of Copenhagen = Københavns Universitet (UCPH), Centre de Biologie pour la Gestion des Populations (UMR CBGP), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut de Recherche pour le Développement (IRD [France-Sud])-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut Agro Montpellier, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Université de Montpellier (UM), Swedish Museum of Natural History (NRM), This work was supported by a grant from the Agence Nationale de la Recherche (ANR) to J.V. (ANR-11-JSV7-0011 Viromics). We also thank the ANR project HORIZON (ANR-17-CE02-0021, S. Charlat) for financial support., ANR-11-JSV7-0011,viromics,Distribution et impact des virus héritables dans une communauté hôtes-parasitoïdes(2011), ANR-17-CE02-0021,Horizon,Patterns and processes of horizontal DNA transfer: an in-depth exploration of the host-parasitoid route(2017), University of Copenhagen = Københavns Universitet (UCPH), Natural Sciences Department, National Museums Collection Centre, 242 West Granton Road, Granton, Edinburgh, EH5 1JA, Department of Zoology, Swedish Museum of Natural History, Box 50007, 104 05 Stockholm, and This work was supported by a grant from the Agence Nationale de la Recherche (ANR) to J.V. (ANR-11-JSV7-0011 Viromics). We also thank the ANR project HORIZON (S. Charlat) for financial support.
- Subjects
[SDV]Life Sciences [q-bio] ,[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE] ,evolutionary biology ,Hymenoptera ,EVE ,dsDNA virus ,domestication ,[SDV.GEN.GA]Life Sciences [q-bio]/Genetics/Animal genetics ,[SDV.MP.VIR]Life Sciences [q-bio]/Microbiology and Parasitology/Virology ,genomics ,horizontal gene transfer ,genetics ,parasitoid ,[SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis - Abstract
All sequencing data are available at NCBI via the BioProject accession number NCBI: PRJNA826991. All scripts and additional tables as well as all cluster phylogeny figures are available under the github repository : (BenjaminGuinet/Viral-domestication-among-Hymenoptera).; International audience; 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 viruses has been repeatedly domesticated following the ancestral endogenizations of double-stranded DNA viruses. 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 comparisons with other viral genomic structures (ssDNA, dsRNA, ssRNA), are more often integrated (that is, endogenized) and domesticated (that is, retained by selection) than expected from their estimated abundance in insect viral communities. Secondly, 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 parasitoid lineages.
- Published
- 2023