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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.

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.

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.

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.

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.

The influence of gut and gonad bacterial communities on insect physiology, behaviour, and ecology is increasingly recognised. Parasitism by parasitoid wasps alters many physiological processes in their hosts, including gut bacterial communities. However, it remains unclear whether these changes are restricted to the gut or also occur in other tissues and fluids, and the mechanisms underlying such changes are unknown. We hypothesise that host microbiome changes result from the injection of calyx fluid (that contain symbiotic viruses known as polydnaviruses) and venom during parasitoid oviposition and that these effects vary by host tissue. To test this, we microinjected Pieris brassicae caterpillars with calyx fluid and venom from Cotesia glomerata, using saline solution and natural parasitism by C. glomerata as controls. We analysed changes in the bacterial community composition in the gut, regurgitate, haemolymph, and labial salivary glands of the host insects. Multivariate analysis revealed distinct bacterial communities across tissues and fluids, with high diversity in the salivary glands and haemolymph. Parasitism and injection of calyx fluid and venom significantly altered bacterial communities in the salivary glands. Differential abundance analysis showed that parasitism affected bacterial relative abundance in the haemolymph, and that Wolbachia was only found in the haemolymph of parasitized caterpillars. Altogether, our findings reveal that parasitism influences the host haemolymph microbiome, and both parasitism and injection of calyx fluid and venom drive changes in the bacterial community composition within the host salivary glands. Given that the composition of salivary glands can influence plant response to herbivory, we discuss these results in the broader context of plant-parasitoid interactions.

Symbiotic relationships may provide organisms with key innovations that aid in the establishment of new niches. For example, during oviposition, some species of parasitoid wasps, whose larvae develop inside the bodies of other insects, inject polydnaviruses into their hosts. These symbiotic viruses disrupt host immune responses, allowing the parasitoid’s progeny to survive. Here we show that symbiotic polydnaviruses also have a downside to the parasitoid’s progeny by initiating a multitrophic chain of interactions that reveals the parasitoid larvae to their enemies. These enemies are hyperparasitoids that use the parasitoid progeny as host for their own offspring. We found that the virus and venom injected by the parasitoid during oviposition, but not the parasitoid progeny itself, affected hyperparasitoid attraction toward plant volatiles induced by feeding of parasitized caterpillars. We identified activity of virus-related genes in the caterpillar salivary gland. Moreover, the virus affected the activity of elicitors of salivary origin that induce plant responses to caterpillar feeding. The changes in caterpillar saliva were critical in inducing plant volatiles that are used by hyperparasitoids to locate parasitized caterpillars. Our results show that symbiotic organismsmay be key drivers of multitrophic ecological interactions. We anticipate that this phenomenon is widespread in nature, because of the abundance of symbiotic microorganisms across trophic levels in ecological communities. Their role should be more prominently integrated in community ecology to understand organization of natural and managed ecosystems, as well as adaptations of individual organisms that are part of these communities.

[...]BV and IV virions differ morphologically, and while both assemble in the nuclei of calyx cells, BVs are released by cell lysis while IVs are released by budding through the plasma membrane [4]. [...]IV proviral genomes lack homologs of any BV core genes and also encapsidate DNAs that organizationally differ from BVs [4], [19]. [...]the similar life cycles of BVs and IVs reflect convergent evolution driven by the analogous roles they play in parasitism of hosts by wasps.

Wasp parasitoids use a variety of methods to commandeer their insect hosts in order to create an environment that will support and promote their own development, usually to the detriment of the host insect. Parasitized insects typically undergo developmental arrest and die sometime after the parasitoid has become independent of its host. Parasitoids can deactivate their host's immune system and effect changes in host hormone titers and behavior. Often, host tissues or organs become refractory to stimulation by tropic hormones. Here we present an overview of the manipulative capabilities of wasp-injected calyx fluid containing polydnaviruses and venom, as well as the parasitoid larva and the teratocytes that originate from the serosal membrane that surrounds the developing embryo of the parasitoid. Possibilities for using regulatory molecules produced by the parasitoid or its products that would be potentially useful in developing new, environmentally safe insect control agents are discussed.

The effects of toxicants, such as pesticides, may be more severe for some life stages of an organism than others. However, in most toxicity studies, data is developed for only one life stage, which may lead to misleading interpretations. Furthermore, population stage-structure may interact with differential susceptibility, especially when populations consist of higher proportions of individuals in more susceptible stages at the time of toxicant exposure. We explore the interaction of differential stage susceptibility and stage distribution using a stage-structured Lefkovitch matrix model. We incorporate lab-derived toxicity data for a common parasitoid, the braconid Diaeretiella rapae (M’Intosh), a common natural enemy of the cabbage aphid ( Brevicoryne brassicae L.), exposed to the pesticide imidacloprid. We compare population outcomes of simulations in which we vary both the population stage structure along with the susceptibility of each stage to toxicants. Our results illustrate an interaction between differential susceptibility and initial stage distribution, highlighting the fact that both of these demographic features should be considered in interpreting toxicity data and the development of ecological risk assessments.