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Immuno-Suppressive Virus-Like Particles of Drosophila Parasitoids bioRxiv preprint doi: https://doi.org/10.1101/342758; this version posted July 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Immuno-suppressive Virus-like particles of 2 Drosophila parasitoids derive from the 3 domestication of a behaviour-manipulating 4 virus relative 1 1 1 2 1* 5 D. Di Giovanni , D. Lepetit , M. Boulesteix , M. Ravallec , J. Varaldi 6 1 Laboratoire de Biom´etrieet Biologie Evolutive (UMR CNRS 5558), Uni- 7 versity Lyon 1 { University of Lyon, 43 boulevard du 11 novembre 1918, 69622 8 Villeurbanne cedex, France 9 10 2 Unit´eBiVi (Biologie Int´egrative et Virologie des Insectes), Universit´eMont- 11 pellier II-INRA 1231, France 12 * corresponding author : julien.varaldi at univ-lyon1.fr 13 Abstract 14 To circumvent host immune response, numerous hymenopteran endo-parasitoid 15 species produce virus-like structures in their reproductive apparatus that are in- 16 jected into the host together with the eggs. These viral-like structures are ab- 17 solutely necessary for the reproduction of these wasps. The viral evolutionary 18 origin of these viral-like particles has been demonstrated in only two cases and 19 for both, the nature of the initial virus-wasp association remains unknown. This 20 is either because no closely related descendant infect the wasps or because the 21 virus lineage went extinct. In this paper, we first show that the virus-like par- 22 ticles (VLPs) produced by endoparasitoids of Drosophila belonging to the genus 23 Leptopilina (Hymenoptera Figitidae) have a viral origin, solving the debate on 24 their origin. Furthermore, the ancestral donor virus still has close relatives infect- 25 ing one of the wasp species, thus giving us insights on the ecological interaction 26 that possibly allowed the domestication process. Intriguingly, the contemporary 27 virus is both vertically and horizontally transmitted and has the particularity to 28 manipulate the superparasitism behavior of the wasp. This raises the possibility 29 that behavior manipulation has been instrumental in the birth of such association 30 between wasps and viruses. 1 bioRxiv preprint doi: https://doi.org/10.1101/342758; this version posted July 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 31 1 Introduction 32 Genetic information is typically passed on from generation to generation 33 through reproduction, ie vertical transmission. However, at some point dur- 34 ing the course of evolution, organisms may gain DNA from unrelated organ- 35 isms, through horizontal gene transfer (HGT). Most horizontally acquired 36 DNA is probably purged from the genomes of the population either because 37 it did not reach the germinal cells in case of metazoan species and/or be- 38 cause no advantage is carried by the foreign sequence. However, in a number 39 of cases, natural selection may have retained the foreign DNA leading ulti- 40 mately to genetic innovation in the population/species. 41 The high frequency and relevance of such phenomenon has been recog- 42 nized for decades for bacteria but was considered to have had a marginal 43 impact on the evolution of metazoans. However, this view has been recently 44 challenged due to the discovery of numerous examples of HGT in metazoans 45 with some of them leading to genetic innovation[6]. For instance, it has been 46 shown that some phytophagous mites and Lepidoptera deal with chemical 47 defenses of their host plant thanks to the acquisition of a bacterial gene 48 involved in detoxification [61]. Other very distantly related phytophagous 49 arthropods (Aphids, mites and gall midges) independently acquired genes 50 involved in carotenoid biosynthesis from fungal donors[42][22][13]. These 51 carotenoid genes were previously considered as absent from animal genomes, 52 in spite of the essential role they play on several aspects of animal biology. 53 Based on its strong conservation in these groups, it is speculated that they 54 have permitted genetic innovation possibly in relation to phytophagy. 55 Regarding the question of domestication of horizontally-transfered DNA 56 in eukaryotes, endoparasitic wasps are of particular interest because they 57 have repeatedly domesticated not only single genes but entire viral machiner- 58 ies. Endoparasitic wasps lay their eggs inside the body of other arthropods, 59 usually other insects, ultimately killing them. Their progeny is thus exposed 60 to the host immune system. Notably, it has been found that the ancestor 61 of at least three monophyletic groups of endoparasitic wasps have indepen- 62 dently domesticated a battery of viral genes allowing them to deliver either 63 DNA encoding immuno-suppressive factors or immuno-suppressive proteins 64 themselves[27][48]. Strikingly, in the case DNA is delivered into the host (so- 65 called polydnaviruses, PDV), it integrates into the host hemocytes DNA and 66 gets expressed [4][12], manipulating the host physiology and behavior, ulti- 67 mately favoring the development of wasp offspring. In cases where proteins 68 are delivered, the viral machinery permits the delivery of these virulence pro- 69 teins into host immune cells, thus inhibiting the host immune response[50] 70 [15]. In both cases, virally-derived genes are used by the wasp to produce a 2 bioRxiv preprint doi: https://doi.org/10.1101/342758; this version posted July 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 71 vector toolset composed of capsids and/or envelopes. However, the virulence 72 factors themselves (or the DNA encoding the virulence factors) are of eukary- 73 otic origin, probably pre-dating the domestication event [12]. Evolution has 74 thus repeatedly favored the domestication of kits of viral genes allowing the 75 production of virus-like structures in the reproductive apparatus of parasitic 76 wasps with clear functional convergence. 77 Although we may speculate that the intimacy of the association between 78 the donor viruses and their parasitoid hosts has favored the exchanges, the 79 biology of these ancestral viruses is mostly unknown. For one such domesti- 80 cation event (in the Campopleginae sub-family, Ichneumonidae family), the 81 ancestral virus has not been identified at all, whereas a beta nudivirus as 82 been identified as the donor virus for wasps belonging to the microgastroid 83 complex of the Braconidae family. In the recently described case of a viral 84 replacement in the lineage leading to Venturia canescens (Campopleginae 85 sub-family), it has been shown that an alpha-nudivirus was the donor. How- 86 ever, close relatives of the donor viruses do not infect present-day wasps, nor 87 infect their hosts. One possible explanation is that the "donor" viral lin- 88 eages went extinct and/or have not been sampled yet. The exact nature of 89 the association wasp/virus that permitted such massive domestication events 90 is thus still unclear. 91 In this work, we identify a new independent case of virus domestication 92 in the genus Leptopilina (Family Figitidae), parasitoids of Drosophila lar- 93 vae. We provide strong evidences that the genes of viral origin permit all 94 Leptopilina wasp species to produce so called virus-like particles (VLPs). 95 VLPs have been known for decades in this genus([50]). They are produced 96 in the venom gland of the wasp, are devoid of DNA but contain virulence 97 proteins that are injected, together with the egg, into the Drosophila larva. 98 They protect wasp eggs from Drosophila immune response ([50][14]). We 99 show that a close relative of the ancestral donor virus is still segregating 100 in the species L. boulardi and its biology has been extensively studied by 101 our group[58][45][38][34][57]. The virus, known as LbFV, belongs to a pos- 102 sibly new dsDNA virus family related to Hytrosaviridae, and more distantly 103 related to Nudiviridae and Baculoviridae[34]. The virus is vertically trans- 104 mitted and manipulates the wasp behaviour by forcing infected females to 105 lay their eggs into already parasitized larvae. This virus-induced "host- 106 sharing" benefits to the virus since it allows its horizontal transmission to 107 new parasitoid lineages. On the contrary, this "superparasitism" behaviour 108 comes with a cost to wasp fitness, making it a nice example of behaviour 109 manipulation[18]. This result suggests that symbionts such as LbFV, might 110 have been instrumental in the birth of such association between wasps and 111 viruses. 3 bioRxiv preprint doi: https://doi.org/10.1101/342758; this version posted July 18, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 112 2 Results 113 We analyzed the genomic sequences of L. boulardi[57], L. clavipes[30], L. 114 heterotoma (this study) and a related species in the Ganaspis genus (G. 115 xanthopoda, this study). All Leptopilina species as well as G. xanthopoda be- 116 long to the Figitidae family and are endoparasitoids developing from various 117 species of Drosophila. 118 The basic statistics for the assemblies used in this paper are presented in 119 table 1. With an N50 of 2080 bp the G. xanthopoda assembly appeared more 120 fragmented than those from the Leptopilina species whose N50 ranges from 121 12807 bp to 17657 bp. This reflects its two to three times larger genome size 122 likely due to its higher content in repetitive sequences (44.92% vs. 24.02- 123 28.82%).
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