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Parasitoids alter host energy homeostasis to create a favorable environment for their own development. However, the mechanisms underlying this process remain largely unexplored, especially for gregarious parasitoids. Cotesia ruficrus , a gregarious endoparasitoid native to China, targets the invasive pest Spodoptera frugiperda (fall armyworm, FAW) and has been shown to effectively control FAW populations. This study investigates the role of the polydnavirus (PDV) produced by C. ruficrus in regulating lipid metabolism of FAW larvae. The results demonstrated that, following PDV injection for 5 days, both triglyceride concentrations and lipid droplet diameters in the fat bodies of FAW larvae significantly increased. RNA interference (RNAi) targeting the PDV gene CrBV3–31 led to a reduction in triglyceride concentrations and lipid droplet size, along with an upregulation of the LSD1 gene. Furthermore, silencing CrBV3–31 decreased triglyceride levels in C. ruficrus pupae and lowered its eclosion rate. These findings suggest that the PDV gene CrBV3–31 plays a crucial role in enhancing lipid accumulation in FAW larvae, thereby supporting the survival of C. ruficrus offspring. This study uncovers a novel mechanism by which gregarious endoparasitoids exploit symbiotic bracovirus genes to regulate host energy metabolism, increasing lipid levels to meet the developmental needs of their multiple offspring.

The Polydnaviridae (PDV), including the Bracovirus (BV) and Ichnovirus genera, originated from the integration of unrelated viruses in the genomes of two parasitoid wasp lineages, in a remarkable example of convergent evolution. Functionally active PDVs represent the most compelling evolutionary success among endogenous viral elements (EVEs). BV evolved from the domestication by braconid wasps of a nudivirus 100 Ma. The nudivirus genome has become an EVE involved in BV particle production but is not encapsidated. Instead, BV genomes have co-opted virulence genes, used by the wasps to control the immunity and development of their hosts. Gene transfers and duplications have shaped BV genomes, now encoding hundreds of genes. Phylogenomic studies suggest that BVs contribute largely to wasp diversification and adaptation to their hosts. A genome evolution model explains how multidirectional wasp adaptation to different host species could have fostered PDV genome extension. Integrative studies linking ecological data on the wasp to genomic analyses should provide new insights into the adaptive role of particular BV genes. Forthcoming genomic advances should also indicate if the associations between endoparasitoid wasps and symbiotic viruses evolved because of their particularly intimate interactions with their hosts, or if similar domesticated EVEs could be uncovered in other parasites.

Some DNA viruses infect host animals usually by integrating their DNAs into the host genome. However, the mechanisms for integration remain largely unknown. Here, we find that Cotesia vestalis bracovirus (CvBV), a polydnavirus of the parasitic wasp C . vestalis (Haliday), integrates its DNA circles into host Plutella xylostella (L.) genome by two distinct strategies, conservatively and randomly, through high-throughput sequencing analysis. We confirmed that the conservatively integrating circles contain an essential “8+5” nucleotides motif which is required for integration. Then we find CvBV circles are integrated into the caterpillar’s genome in three temporal patterns, the early, mid and late stage-integration. We further identify that three CvBV-encoded integrases are responsible for some, but not all of the virus circle integrations, indeed they mainly participate in the processes of early stage-integration. Strikingly, we find two P . xylostella retroviral integrases (PxIN1 and PxIN2) are highly induced upon wasp parasitism, and PxIN1 is crucial for integration of some other early-integrated CvBV circles, such as CvBV_04, CvBV_12 and CvBV_24, while PxIN2 is important for integration of a late-integrated CvBV circle, CvBV_21. Our data uncover a novel mechanism in which CvBV integrates into the infected host genome, not only by utilizing its own integrases, but also by recruiting host enzymes. These findings will strongly deepen our understanding of how bracoviruses regulate and integrate into their hosts.

To understand how extant viruses interact with their hosts, we need a historical framework of their evolutionary association. Akin to retrovirus or hepadnavirus viral fossils present in eukaryotic genomes, bracoviruses are integrated in braconid wasp genomes and are transmitted by Mendelian inheritance. However, unlike viral genomic fossils, they have retained functional machineries homologous to those of large dsDNA viruses pathogenic to arthropods. Using a phylogenomic approach, we resolved the relationships between bracoviruses and their closest free relatives: baculoviruses and nudiviruses. The phylogeny showed that bracoviruses are nested within the nudivirus clade. Bracoviruses establish a bridge between the virus and animal worlds. Their inclusion in a virus phylogeny allowed us to relate free viruses to fossils. The ages of the wasps were used to calibrate the virus phylogeny. Bayesian analyses revealed that insect dsDNA viruses first evolved at ?310 Mya in the Paleozoic Era during the Carboniferous Period with the first insects. Furthermore the virus diversification time frame during the Mesozoic Era appears linked to the diversification of insect orders; baculoviruses that infect larvae evolved at the same period as holometabolous insects. These results imply ancient coevolution by resource tracking between several insect dsDNA virus families and their hosts, dating back to 310 Mya.

Parasitic wasps produce several factors including venom, polydnaviruses (PDVs) and specialized wasp cells named teratocytes that benefit the survival of offspring by altering the physiology of hosts. However, the underlying molecular mechanisms for the alterations remain unclear. Here we find that the teratocytes of Cotesia vestalis , an endoparasitoid of the diamondback moth Plutella xylostella , and its associated bracovirus (CvBV) can produce miRNAs and deliver the products into the host via different ways. Certain miRNAs in the parasitized host are mainly produced by teratocytes, while the expression level of miRNAs encoded by CvBV can be 100-fold greater in parasitized hosts than non-parasitized ones. We further show that one teratocyte-produced miRNA (Cve-miR-281-3p) and one CvBV-produced miRNA (Cve-miR-novel22-5p-1) arrest host growth by modulating expression of the host ecdysone receptor ( EcR ). Altogether, our results show the first evidence of cross-species regulation by miRNAs in animal parasitism and their possible function in the alteration of host physiology during parasitism. The moth Plutella xylostella during its larval stage is the host of the endoparasitic wasp Cotesia vestalis . Here the authors show that the parasitoids deliver microRNAs to their hosts through their symbiotic virus and specialized cells leading to induced developmental delay.

Bracoviruses are symbiotic viruses associated with tens of thousands of species of parasitic wasps that develop within the body of lepidopteran hosts and that collectively parasitize caterpillars of virtually every lepidopteran species. Viral particles are produced in the wasp ovaries and injected into host larvae with the wasp eggs. Once in the host body, the viral DNA circles enclosed in the particles integrate into lepidopteran host cell DNA. Here we show that bracovirus DNA sequences have been inserted repeatedly into lepidopteran genomes, indicating this viral DNA can also enter germline cells. The original mode of Horizontal Gene Transfer (HGT) unveiled here is based on the integrative properties of an endogenous virus that has evolved as a gene transfer agent within parasitic wasp genomes for approximate to 100 million years. Among the bracovirus genes thus transferred, a phylogenetic analysis indicated that those encoding C-type-lectins most likely originated from the wasp gene set, showing that a bracovirus-mediated gene flux exists between the 2 insect orders Hymenoptera and Lepidoptera. Furthermore, the acquisition of bracovirus sequences that can be expressed by Lepidoptera has resulted in the domestication of several genes that could result in adaptive advantages for the host. Indeed, functional analyses suggest that two of the acquired genes could have a protective role against a common pathogen in the field, baculovirus. From these results, we hypothesize that bracovirus-mediated HGT has played an important role in the evolutionary arms race between Lepidoptera and their pathogens.

Many species of parasitoid wasps inject polydnavirus particles in order to manipulate host defenses and development. Because the DNA packaged in these particles encodes almost no viral structural proteins, their relation to viruses has been debated. Characterization of complementary DNAs derived from braconid wasp ovaries identified genes encoding subunits of a viral RNA polymerase and structural components of polydnavirus particles related most closely to those of nudiviruses--a sister group of baculoviruses. The conservation of this viral machinery in different braconid wasp lineages sharing polydnaviruses suggests that parasitoid wasps incorporated a nudivirus-related genome into their own genetic material. We found that the nudiviral genes themselves are no longer packaged but are actively transcribed and produce particles used to deliver genes essential for successful parasitism in lepidopteran hosts.

Parasitoids modulate host development for the survival of their offspring, but the mechanisms underlying this phenomenon remain largely unknown. Here, we found that the endoparasitoid Cotesia vestalis disrupted the larval-larval ecdysis in its host Plutella xylostella by the 20-hydroxyecdysone (20E) synthesis pathway. After parasitization by C. vestalis , the 20E peak of host larvae disappeared before the onset of ecdysis and the expression of ecdysone synthesis genes was significantly downregulated. We further found that a Cotesia vestalis bracovirus (CvBV) gene CvBV_28 − 5 was transiently high-level expressed prior to the host’s 20E peak, enabling the precise suppression of this critical developmental signal. Consistently, the knockdown of CvBV_28 − 5 affected the expression of 20E response transcription factors in the cuticle and several ecdysis-related genes. Furthermore, we found that CvBV_28 − 5 bound directly to the Raf, a MAP3K member of the MAPK pathwaythat functions as a critical regulator of ecdysone synthesis genes in hosts. Collectively, our results provide the first evidence that parasitoids modulate host ecdysis by affecting MAPK-20E signaling during a defined developmental window and provide novel insights into the mechanism of parasitoid regulation of host development.

The parasitic wasp, Cotesia congregata , manipulates the behaviour of its host, the caterpillar Manduca sexta . The female wasp injects her eggs and a symbiotic virus (i.e. bracovirus, CcBV) into the body of its host. The host’s behaviour remains unchanged until the wasps exit the caterpillar, and then the caterpillar becomes a non-feeding “bodyguard” for the wasp cocoons. Using proteomic, transcriptomic and qPCR studies, we discovered an increase in antimicrobial peptide gene expression and protein abundance in the host central nervous system at the time of wasp emergence, correlating with the change in host behaviour. These results support the hypothesis that the wasps hyperactivate an immune-neural connection to help create the change in behaviour. At the time of wasp emergence, there was also an increase in bracoviral gene expression and proteins in the host brain, suggesting that the bracovirus may also be involved in altering host behaviour. Other changes in gene expression and protein abundance suggest that synaptic transmission may be altered after wasp emergence, and a reduction in descending neural activity from the host’s brain provides indirect support for this hypothesis.

Increasing numbers of horizontal transfer (HT) of genes and transposable elements are reported in insects. Yet the mechanisms underlying these transfers remain unknown. Here we first quantify and characterize the patterns of chromosomal integration of the polydnavirus (PDV) encoded by the Campopleginae Hyposoter didymator parasitoid wasp (HdIV) in somatic cells of parasitized fall armyworm (Spodoptera frugiperda). PDVs are domesticated viruses injected by wasps together with their eggs into their hosts in order to facilitate the development of wasp larvae. We found that six HdIV DNA circles integrate into the genome of host somatic cells. Each host haploid genome suffers between 23 and 40 integration events (IEs) on average 72 h post-parasitism. Almost all IEs are mediated by DNA double-strand breaks occurring in the host integration motif (HIM) of HdIV circles. We show that despite their independent evolutionary origins, PDV from both Campopleginae and Braconidae wasps use remarkably similar mechanisms for chromosomal integration. Next, our similarity search performed on 775 genomes reveals that PDVs of both Campopleginae and Braconidae wasps have recurrently colonized the germline of dozens of lepidopteran species through the same mechanisms they use to integrate into somatic host chromosomes during parasitism. We found evidence of HIM-mediated HT of PDV DNA circles in no less than 124 species belonging to 15 lepidopteran families. Thus, this mechanism underlies a major route of HT of genetic material from wasps to lepidopterans with likely important consequences on lepidopterans.