viruses Review The Unconventional Viruses of Ichneumonid Parasitoid Wasps Anne-Nathalie Volkoff 1,* and Michel Cusson 2 1 Diversity, Genomes, Insects-Microorganisms Interactions (DGIMI), Université de Montpellier, Institut National de Recherche pour L’Agriculture, L’Alimentation et L’Environnement (INRAE), 34095 Montpellier, France 2 Laurentian Forestry Centre, Natural Resources Canada, Quebec City, QC G1V 4C7, Canada; [email protected] * Correspondence: anne-nathalie.volkoff@inrae.fr Received: 14 September 2020; Accepted: 8 October 2020; Published: 15 October 2020 Abstract: To ensure their own immature development as parasites, ichneumonid parasitoid wasps use endogenous viruses that they acquired through ancient events of viral genome integration. Thousands of species from the campoplegine and banchine wasp subfamilies rely, for their survival, on their association with these viruses, hijacked from a yet undetermined viral taxon. Here, we give an update of recent findings on the nature of the viral genes retained from the progenitor viruses and how they are organized in the wasp genome. Keywords: parasitoid wasp; ichnovirus; virus-like particles; endogenous viruses; mutualistic viruses; genomic architecture 1. Introduction The ichneumonid wasps (Hymenoptera: Ichneumonidae) form a very large and diverse group of insects [1] that share a life cycle involving parasitism. Around 25,000 ichneumonid species have been described to date [2], but their actual numbers are estimated to be about four times this high [3]. Many ichneumonid species are endoparasitoids: the females lay their eggs inside another insect, usually an insect larva, where their progeny develops (Figure1). Amazingly, in many cases the parasitized insect continues its development, and usually only dies once the parasitoid has completed its larval development. This life history strategy presents a number of challenges for the parasitoid. In particular, the developing wasp needs to escape the immune response of its host and modulate host development and metabolism in a way that is beneficial to its own development. There are many strategies parasitoids employ to inhibit host immune defenses and to finely tune host development to suit their own. The females of some species, for instance, produce specific immunosuppressive proteins in their venom gland and inject them into the host during parasitization. Another amazing strategy, described only in some ichneumonid and braconid subfamilies, involves the production, in the female genital tract, of virus-like particles that allow the transfer of effector molecules from the wasp to the host. Strikingly, these entities were recently discovered to result from the “domestication” of conventional viruses in these wasp lineages. Viruses 2020, 12, 1170; doi:10.3390/v12101170 www.mdpi.com/journal/viruses Viruses 2020, 12, 1170 2 of 12 Viruses 2020, 12, x FOR PEER REVIEW 2 of 12 Figure 1. LifeLife cycle cycle of of an an ichneumonid ichneumonid parasitoid wasp associated with mutualistic viruses. The adult female wasp injects virus particlesparticles alongalong withwith thethe eggseggs duringduring parasitization.parasitization. The progeny develops within the body of the parasitized insect. At the en endd of larval development, the mature larva egresses from the host and spins aa cocooncocoon wherewhere pupationpupation takestakes place. A free-living adult then emerges from the cocoon. 2. A Brief History About the Discovery of Mutualistic Viruses in Parasitoids Virus-like particles associated with parasitoids and necessary for successful parasitism were discovered in the 1970s, the firstfirst exampleexample beingbeing thethe immunosuppressiveimmunosuppressive particles described in the ichneumonid wasp Venturia canescens, aa parasitoidparasitoid ofof pyralidpyralid caterpillarscaterpillars [[4].4]. SubsequentSubsequent studiesstudies showed that these particles, produced in the wasp ovaries, were composed of wasp proteins and devoid ofof nucleic nucleic acids acids [5 ].[5]. Concomitantly, Concomitantly, other other particles particles resembling resembling viruses viruses were described were described in various in waspvarious species wasp belonging species belonging to the families to the Ichneumonidae families Ichneumonidae and Braconidae and Braconidae [6,7]. In contrast [6,7]. toIn those contrast found to inthoseV. canescensfound in, V. these canescens particles, these contained particles multiple contained circular, multiple double-stranded circular, double-stranded DNAs, with DNAs, aggregate with genomeaggregate sizes genome ranging sizes from ranging 150 tofrom more 150 than to more 600 kbthan [8, 9600]. Likekb [8,9]. the particlesLike the particles of V. canescens, of V. canescens,they are producedthey are produced in wasp in ovaries wasp andovaries injected and injected into the into host the along host withalong the with parasitoid the parasitoid egg. Particlesegg. Particles then rapidlythen rapidly infect theinfect parasitized the parasitized host’s cells, host’s which cells, leads which to expression leads to expression of viral genes of [viral10] and genes alterations [10] and of hostalterations physiology of host necessary physiology for the necessary successful for developmentthe successful of development the wasp progeny of the [ 11wasp,12]. progeny Early work [11,12]. also highlightedEarly work also some highlighted atypical features some atypical of these features viruses: of although these viruses: they contain although DNA, they they contain do not DNA, replicate they indo thenot parasitizedreplicate in insectthe parasitized [13] and areinsect only [13] transmitted and are only vertically transmitted through vertically the wasp through germline the wasp [14]. Itgermline was further [14]. It shown was further that the shown DNA that segments the DN includedA segments in theseincluded particles in these are particles indeed maintainedare indeed integratedmaintained in integrated the wasp genomein the wasp [15]. genome However, [15]. and Howe despitever, their and atypicaldespite lifetheir cycle, atypical they life were cycle, formally they recognizedwere formally in 1991 recognized by the International in 1991 by Committee the International on Taxonomy Committee of Viruses on Taxonomy as members of of Viruses a family as of insectmembers viruses, of a family named ofPolydnaviridae insect viruses,[16 named], although Polydnaviridae their status [16], as although true viruses their has status been, as and true remains, viruses ahas contentious been, and issue.remains, a contentious issue. The polydnavirus (PDV) family includes two taxa, the bracoviruses (BVs) and the ichnoviruses (IVs), associatedassociated withwith wasps wasps from from the the braconid braconid and and ichneumonid ichneumonid families, families, respectively. respectively. Although Although they sharethey share a common a common life cycle, life BVs cycle, and BVs IVs wereand separatedIVs were inseparated two groups in becausetwo groups of their because morphological of their dimorphologicalfferences (BVs differences have cylindrical (BVs have nucleocapsids cylindrical of nucleocapsids variable length of surroundedvariable length by asurrounded single envelope; by a IVssingle have envelope; lenticular IVs nucleocapsidshave lenticular more nucleocapsids or less uniform more or in less size, uniform enveloped in size, with enveloped two membranes). with two Subsequentmembranes). studies Subsequent confirmed studies their confirmed distinctive their features: distin theyctive di features:ffer in the they nature differ of in the the genes nature harbored of the bygenes their harbored packaged by genomestheir packaged [17] and genomes derive from[17] an distinctd derive viral from ancestors distinct [18 viral,19]. ancestors [18,19]. Virus-like particles devoid of nucleic acids have recently been described in the ovaries of the braconid waspwasp FopiusFopius arisanus arisanus[ 20[20].]. We We may may well well be be only only at theat the beginning beginning of discoveries of discoveries of viruses of viruses and virus-likeand virus-like particles particles associated associated with, wi andth, usedand used by, parasitoid by, parasitoid wasps. wasps. Viruses 2020, 12, 1170 3 of 12 3. DiversityViruses of2020 Ichneumonid, 12, x FOR PEER REVIEW Virus Particles 3 of 12 Virus3. Diversity particles of associatedIchneumonid with Virus ichneumonid Particles wasps have so far been described only in two ichneumonid subfamilies, the Campopleginae and the Banchinae. However, surveys have been made Virus particles associated with ichneumonid wasps have so far been described only in two essentiallyichneumonid by electron subfamilies, microscopy, the Campopleginae a technique and that the does Banchinae. not permit However, screening surveys have of large been made numbers of wasps [21essentially]. With by the electron recent microscopy, development a technique of new that sequencing does not permit technologies, screening new of large viruses numbers will of likely be discoveredwasps in [21]. the With near the future. recent development of new sequencing technologies, new viruses will likely be Campopleginediscovered in the and near banchine future. wasp species both harbor polydnaviruses of the ichnovirus group. Campoplegine and banchine wasp species both harbor polydnaviruses of the ichnovirus group. Banchine IV virions typically harbor several nucleocapsids [22,23] whereas most virions of campoplegine Banchine IV virions typically harbor several nucleocapsids