AnvRV virus in the parasitoid wasp Anagyrus vladimiri: localization, effect on gene expression, and prevalence

Insect-virus associations have been studied extensively in the context of pathogenic viruses transmitted by insects, whereas research on nonpathogenic viruses remains relatively scarce. Recently, we discovered three nonpathogenic RNA viruses in the parasitoid wasp Anagyrus vladimiri: AnvRV, AnvDV, and AnvIfV. Here, using transmission electron microscopy, we detected AnvRV in the wasp oocytes and in a distinct group of cells in the ovaries, which we termed "satellite cells," but not in the venom gland or venom reservoir, indicating that AnvRV is transmitted transovarially. Next, we analyzed gene expression in AnvRV-infected and uninfected wasps and found that AnvRV modulates the immune response and alters venom composition. Notably, the NF-κB inhibitor gene was upregulated in the wasp ovaries, where AnvRV is localized, suggesting that AnvRV locally suppresses the immune response of A. vladimiri to facilitate its transmission. Next, we studied the prevalence of the three viruses in field populations of A. vladimiri and its hosts, Planococcus citri and Planococcus ficus. AnvRV was absent from both mealybug species and detected at low prevalence in A. vladimiri, whereas AnvDV and AnvIfV were consistently present in P. citri. Lastly, by datamining of public RNAseq data sets, we investigated the prevalence of these viruses in other parasitoid species and revealed only a few related viruses. Taken together, we postulate that AnvRV is an active symbiont of A. vladimiri, influencing host gene regulation. These findings provide new insights into the diversity of insect-virus interactions and their potential roles in shaping parasitoid biology.

Viruses likely represent the majority of insect symbiotic microorganisms. Yet, viral symbionts and their interactions with insect hosts were less studied, mostly due to technical difficulties stemming from their small size and lack of universal markers. Although viral symbionts are usually perceived as pathogens, there are clear instances in which they are beneficial to their hosts, providing functions that are essential in some cases and conditionally beneficial in others, shaping insect ecology and evolution. This study provides several pieces of the puzzle on the road to understanding the complex interactions within the multi-trophic system consisting of a parasitoid wasp, its mealybug host, and a double-stranded RNA virus. This system may serve as a case study of viruses' effect on insects and broaden our understanding of the possible effects of viruses on other arthropods.