Endogenization from diverse viral ancestors is common and widespread in parasitoid wasps

Abstract

The Ichneumonoidea (Ichneumonidae and Braconidae) is an incredibly diverse superfamily of parasitoid wasps that includes species that produce virus-like entities in their reproductive tracts to promote successful parasitism of host insects. Research on these entities has traditionally focused upon two viral genera Bracovirus (in Braconidae) and Ichnovirus (in Ichneumonidae). These viruses are produced using genes known collectively as endogenous viral elements (EVEs) that represent historical, now heritable viral integration events in wasp genomes. Here, new genome sequence assemblies for eleven species and six publicly available genomes from the Ichneumonoidea were screened with the goal of identifying novel EVEs and characterizing the breadth of species in lineages with known EVEs. Exhaustive similarity searches combined with the identification of ancient core genes revealed sequences from both known and novel EVEs. Two species harbored novel, independently derived EVEs related to a divergent large double-stranded DNA (dsDNA) virus that manipulates behavior in other hymenopteran species. While bracovirus or ichnovirus EVEs were identified as expected in three species, the absence of ichnoviruses in several species suggests that they are independently derived and present in two younger, less widespread lineages than previously thought. Overall, this study presents a novel bioinformatic approach for EVE discovery in genomes and shows that three divergent virus families (nudiviruses, the ancestors of ichnoviruses, and LbFV-like viruses) are recurrently acquired as EVEs in parasitoid wasps. Virus acquisition in the parasitoid wasps is a common process that has occurred in many more than two lineages from a diverse range of arthropod-infecting dsDNA viruses. SignificanceParasitoid wasps are an extremely diverse group of animals that are known to harbor Endogenous Virus Elements (EVEs) that produce virions or virus-like particles of key importance in wasps parasitism success. However, the prevalence and diversity of independently acquired EVEs in parasitoid wasp lineages has remained largely uncharacterized on a widespread scale. This study represents an important first step and hints at the massive, untapped diversity of EVEs in parasitoid wasps via the identification of several novel virus co-option events from diverse groups of double-stranded DNA virus pathogens.