Endogenous viruses form an important proportion of eukaryote genomes and a source of novel functions. How large DNA viruses integrated into a genome evolve when they confer a benefit to their host, however, remains unknown. Bracoviruses are essential for the parasitism success of parasitoid wasps, into whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome at a chromosomal scale, that bracovirus genes colonized all ten chromosomes of Cotesia congregata. Most form clusters of genes involved in particle production or parasitism success. Genomic comparison with another wasp, Microplitis demolitor, revealed that these clusters were already established ~53 mya and thus belong to remarkably stable genomic structures, the architectures of which are evolutionary constrained. Transcriptomic analyses highlight temporal synchronization of viral gene expression without resulting in immune gene induction, suggesting that no conflicts remain between ancient symbiotic partners when benefits to them converge.

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

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Koinobiont endoparasitoid wasps regulate the host’s physiology to their own benefit during their growth and development, using maternal, immature and/or derived-tissue weaponry. The tools used to subdue the wasps’ hosts interfere directly with host transcription activity. The broad range of host tissues and pathways affected impedes our overall understanding of the host-regulation process during parasitoid development. Next-generation sequencing and de novo transcriptomes are helpful approaches to broad questions, including in non-model organisms. In the present study, we used Illumina sequencing to assemble a de novo reference transcriptome of the sugarcane borer Diatraea saccharalis, to investigate the regulation of host gene expression by the larval endoparasitoid Cotesia flavipes. We obtained 174,809,358 reads and assembled 144,116 transcripts, of which 44,325 were putatively identified as lepidopteran genes and represented a substantial number of pathways that are well described in other lepidopteran species. Comparative transcriptome analyses of unparasitized versus parasitized larvae identified 1,432 transcripts of D. saccharalis that were up-regulated under parasitization by C. flavipes, while 1,027 transcripts were down-regulated. Comparison of the transcriptomes of unparasitized and pseudoparasitized D. saccharalis larvae led to the identification of 1,253 up-regulated transcripts and 972 down-regulated transcripts in the pseudoparasitized larvae. Analysis of the differentially expressed transcripts showed that C. flavipes regulated several pathways, including the Ca+2 transduction signaling pathway, glycolysis/gluconeogenesis, chitin metabolism, and hormone biosynthesis and degradation, as well as the immune system, allowing us to identify key target genes involved in the metabolism and development of D. saccharalis.