Over the course of evolution, hymenopteran parasitoids have developed a close relationship with heritable viruses, sometimes integrating viral genes into their chromosomes. For example, in Drosophila parasitoids belonging to the Leptopilina genus, 13 viral genes from the Filamentoviridae family have been domesticated to deliver immunosuppressive factors to host immune cells, thereby protecting parasitoid offspring from the host immune response. The present study aims to comprehensively characterize this domestication event in terms of the viral genes involved, the wasp diversity affected by this event and its chronology. Our genomic analysis of 41 Cynipoidea wasps from six subfamilies revealed 18 viral genes that were endogenized during the early radiation of the Eucoilini/Trichoplastini clade around 75 million years ago. Wasps from this highly diverse clade develop not only from Drosophila but also from a variety of Schizophora. This event coincides with the radiation of Schizophora, a highly speciose Diptera clade, suggesting that viral domestication facilitated wasp diversification in response to host diversification. Additionally, in one of the species, at least one viral gene was replaced by another gene derived from a related filamentovirus. This study highlights the impact of viral domestication on the diversification of parasitoid wasps.

Biology Centre of the Czech Academy of Sciences Institute of Entomology Branišovská 1160 31 České Budějovice 370 05 Czech Republic

Centre for Palaeogenetics Stockholm Sweden

Department of Bioinformatics and Genetics Swedish Museum of Natural History Stockholm Sweden

Laboratoire d'Ecobiologie des Insectes Parasitoïdes Université Rennes 1 Campus de Beaulieu Rennes Cedex 35042 France

Leibniz Institute for the Analysis of Biodiversity Change Museum Koenig Bonn Adenauerallee 160 Bonn 53113 Germany

Université Lyon 1 CNRS Laboratoire de Biométrie et Biologie Evolutive UMR 5558 Villeurbanne F 69622 France

USDA ARS Systematic Entomology Laboratory Washington D C USA

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Dating the origin of a viral domestication event in parasitoid wasps attacking Diptera