A behavior-manipulating virus relative as a source of adaptive genes for parasitoid wasps

Abstract

11To circumvent host immune response, some hymenopteran endo-parasitoids produce 12 virus-like structures in their reproductive apparatus that are injected into the host 13 together with the eggs. These viral-like structures are absolutely necessary for 14 the reproduction of these wasps. The viral evolutionary origin of these viral-like 15 particles has been demonstrated in only a few cases of wasp species all belonging to 16 the Ichneumonoidea superfamily. In addition, the nature of the initial virus-wasp 17 association remains unknown for all. This is either because no closely related 18 descendant infects the wasps, because it has not been sampled yet, or because 19 the virus lineage went extinct. In this paper, we show that the virus-like particles 20 (VLPs) produced by endoparasitoids of Drosophila belonging to the Leptopilina 21 genus (superfamily Cynipoidea) do have a viral origin, solving the debate on their 22 origin. Furthermore, the ancestral donor virus still has close relatives infecting 23 one of the wasp species, thus giving us insights on the ecological interaction that 24 possibly allowed the domestication process. Intriguingly, this contemporary virus is 25 both vertically and horizontally transmitted and has the particularity to manipulate 26 the superparasitism behavior of the wasp. This raises the possibility that behavior 27 manipulation has been instrumental in the birth of such association between wasps 28 and viruses. 29 1 1 Introduction 30 Genetic information is typically passed on from generation to generation 31 through reproduction, ie vertical transmission. However, at some point during 32 the course of evolution, organisms may gain DNA from unrelated organisms, 33 through horizontal gene transfer (HGT). Most horizontally acquired DNA 34 is probably purged from the genomes of the population either because it 35 did not reach the germinal cells in case of metazoan species and/or because 36 no advantage is carried by the foreign sequence. However, natural selection 37 may retain the foreign DNA leading ultimately to genetic innovation in the 38 population/species [38]. 39 The high frequency and relevance of such phenomenon has been recognized 40 for decades for bacteria but was considered to have had a marginal impact 41 on the evolution of metazoans[40]. However, this view has been recently 42 challenged due to the discovery of numerous examples of HGT in metazoans 43 with some of them leading to genetic innovation[8]. The most notorious 44 example involves retroviral envelope genes that have been endogenized, 45 domesticated and multiply replaced in mammalian genomes[45]. In this 46 case, the fusogenic and immunosuppressive properties of these viral proteins 47 (syncitins) have been repeatedly recruited to permit the evolution of placental 48 structures during mammalian diversification. Interestingly, a similar case 49 of syncitin domestication was recently described in a clade of viviparous 50 Scincidae lizards that also rely on a placenta-like structure to feed their 51 o↵spring [...

Immune Suppressive Extracellular Vesicle Proteins ofLeptopilina heterotomaAre Encoded in the Wasp Genome

“…Unlike the well-characterized Drosophila hosts, the biology and molecular-genetics of their parasitic wasps have remained relatively obscure with only recent characterizations of Leptopilina and Ganaspis spp. (Melk and Govind 1999;Colinet et al 2013;Goecks et al 2013;Heavner et al 2013;Mortimer et al 2013;Heavner et al 2017;Di Giovanni et al 2019). Our proteomic, transcriptomic and genomic results here expand the available information on L. heterotoma.…”

“…We also searched the Lh MSEV superset for presence of L. boulardi Filamentous Virus (LbFV) homologs (LbFV is a behavior manipulating virus of Lb (Varaldi et al 2006;Patot et al 2012)). Of LbFV's 108 genes, 13 are present in genomes of Lb, Lh and related species, and the 13 transcripts are expressed in the Lb venom gland (Di Giovanni et al 2019). Within our thresholds, we obtained only three (of 13) sequences with similarity to LbFV ORFs.…”

“…Interpretation of their identity also varies. For example, Di Giovanni et al (2019) contend that MSEVs/VLPs are derived from a virus ancestral to the LbFV. Our analysis of the expanded proteomic superset does not lend strong support to this line of thinking.…”