Chromosomal resolution reveals symbiotic virus colonization of parasitic wasp genomes

Abstract

17Most endogenous viruses, an important proportion of eukaryote genomes, are doomed to slowly 18 decay. Little is known, however, on how they evolve when they confer a benefit to their host. 19Bracoviruses are essential for the parasitism success of parasitoid wasps, whose genomes they 20 integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp 21 genome, for the first time at a chromosomal scale, that symbiotic bracovirus genes spread to 22 and colonized all the chromosomes. Moreover, large viral clusters are stably maintained 23 suggesting strong evolutionary constraints. Genomic comparison with another wasps revealed 24 that this organization was already established ~53 mya. Transcriptomic analyses highlight 25 temporal synchronization of viral gene expression, leading to particle production. Immune 26 genes are not induced, however, indicating the virus is not perceived as foreign by the wasp. 27This recognition suggests that no conflicts remain between symbiotic partners when benefits to 28 them converge. 29 30 31 32 33 Main 34 Cotesia wasps (Hymenoptera, Braconidae) are parasitoids of Lepidoptera. Female 35 wasps lay their eggs into caterpillars and larvae develop feeding on the host hemolymph. 36Several Cotesia species are famous for their use as biological control agents to control insect 37 pests, such as Cotesia flavipes which is massively released over several million hectares of 38 sugarcane fields in Brazil 1,2 . Parasitoid wasps evolved several strategies that increase parasitic 39 success, including a sensitive olfactory apparatus to locate their hosts 3,4 and detoxification 40 mechanisms against plant toxic compounds accumulating in their host (Fig. 1). But the most 41 original strategy is the domestication of a bracovirus (BV) shared by over 46,000 braconid wasp 42 species 5 . Bracoviruses originate from a single integration event ~103 million years ago (mya) 43 of a nudivirus in the genome of the last common ancestor of this group 6-9 . Virus domestication 44 nowadays confers a benefit to the wasps that use BVs as virulence gene delivery systems 10 . 45

Quantitative trait loci involved in the reproductive success of a parasitoid wasp

“…From these studies, 67 genes of interest were identified and are listed in Table 5. Among them we found Bracovirus genes involved in the production of viral particles and other bracovirus genes similar to genes involved in the inactivation of the host immune system in other host parasitoid models (Bézier, Annaheim, et al, 2009;Burke, Walden, Whitfield, Robertson, & Strand, 2014;Chevignon et al, 2014Chevignon et al, , 2015Falabella et al, 2007;Gauthier et al, 2020;Pruijssers & Strand, 2007;Thoetkiattikul, Beck, & Strand, 2005). Some genes producing venom components were also identified (Ali, Lim, & Kim, 2015;Arvidson et al, 2019;Colinet, Mathé-Hubert, Allemand, Gatti, & Poirié, 2013;Danneels, Rivers, & de Graaf, 2010;Moreau & Asgari, 2015;Sim & Wheeler, 2016).…”

“…Scaffolds containing markers were then mapped to the annotated genome of C. congregata using BLAST to identify genes in QTLs. For this genome, an automatic annotation was performed and refined with manual inspection for some gene families (Bracovirus, Venom, Immunity, Detoxification and Chemodetection; Gauthier et al, 2020).…”

“…Gene Ontology (GO) enrichment was tested using the R package topGO (Alexa, Rahnenfuhrer, & Lengauer, 2006). Annotations were those derived from blast2GO analyses of the Cotesia congregata genome performed by Gauthier et al (2020). Two set of genes were built for each trait based of the gene content of QTL confidence interval.…”

“…The marked difference in the reproductive success of the two strains sets the stage for studying the genetic basis of these traits. Furthermore, an annotated genome of the close relative Cotesia congregata recently became available, which can be used as a reference for the identification of genes within QTL (Gauthier et al, 2020).…”

A chromosome‐level genome assembly of the parasitoid wasp Pteromalus puparum

“…These are the honey bee Apis mellifera (using Hi-C, n = 16), buff-tailed bumblebee Bombus terrestris (using Roche 454, n = 18), ant Ooceraea biroi (using Hi-C, n = 14), parasitoid N. vitripennis (using recombination mapping and long-read sequencing, n = 5) and redheaded pine sawfly Neodiprion lecontei (using quantitative trait locus [QTL] mapping, n = 7; Benetta et al, 2020;Desjardins et al, 2013;Linnen, O'Quin, Shackleford, Sears, & Lindstedt, 2018;McKenzie & Kronauer, 2018;Sadd et al, 2015;Wallberg et al, 2019;Werren et al, 2010). Recently, a chromosome-level genome assembly of the parasitoid Cotesia congregata (using Hi-C, n = 10) has been reported in the preprint server bioRxiv (Gauthier et al, 2020). Additional chromosomal-level genome assemblies will improve comparative genome analyses of the Hymenoptera.…”