A novel cripavirus of an ectoparasitoid wasp increases pupal duration and fecundity of the wasp\u2019s Drosophila melanogaster host

Bo Yuan,Jiao Zhang,Yi Yang,Jens H Kuhn,Fei Wang,Gongyin Ye,Qi Fang,Qisheng Song,Lei Yang

doi:10.1038/s41396-021-01005-w

Abstract

We identified a 9332-nucleotide-long novel picornaviral genome sequence in the transcriptome of an agriculturally important parasitoid wasp (Pachycrepoideus vindemmiae (Rondani, 1875)). The genome of the novel virus, Rondani’s wasp virus 1 (RoWV-1), contains two long open reading frames encoding a nonstructural and a structural protein, respectively, and is 3’-polyadenylated. Phylogenetic analyses firmly place RoWV-1 into the dicistrovirid genus Cripavirus. We detected RoWV-1 in various tissues and life stages of the parasitoid wasp, with the highest virus load measured in the larval digestive tract. We demonstrate that RoWV-1 is transmitted horizontally from infected to uninfected wasps but not vertically to wasp offspring. Comparison of several important biological parameters between the infected and uninfected wasps indicates that RoWV-1 does not have obvious detrimental effects on wasps. We further demonstrate that RoWV-1 also infects Drosophila melanogaster (Meigen, 1830), the hosts of the pupal ectoparasitoid wasps, and thereby increases its pupal developmental duration and fecundity, but decreases the eclosion rate. Together, these results suggest that RoWV-1 may have a potential benefit to the wasp by increasing not only the number of potential wasp hosts but also the developmental time of the hosts to ensure proper development of wasp offspring.

Highlights

Arthropods are among the most abundant invertebrates on the planet
Analysis of the four domains yielded the following information: dsRBD consists of 68 amino acid residues and aligns with dsRBDs of, for instance, Drosophila C virus (DCV; Dicistroviridae: Cripavirus) and cellular proteins from different model organisms (Supplementary Table S4)
Alignment by ClustalW clearly indicated that the Rondani’s wasp virus 1 (RoWV-1) RNA-directed RNA polymerase (RdRp) is most closely related to that of DCV. These results indicate that RoWV-1 is a novel member of the order Picornavirales

Summary

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Arthropods are among the most abundant invertebrates on the planet. An improved understanding of arthropod viruses could lead to novel measures for protection of agriculturally beneficial insects, such as western honey bees Parasitoid wasps (order Hymenoptera) are the most common type of parasitoid insects. These wasps lay their eggs inside or on the bodies of other arthropods, which serve as food for the developing wasp larvae after hatching [10]. Parasitoid wasps are enemies of other arthropods and play an important role in biological control of pests [11,12,13]. In Europe and the United States, P. vindemmiae is one of only two parasitoid wasps that naturally and successfully attack and kill the spotted wing drosophila, Drosophila suzukii (Matsumura, 1931) [24, 25], which is a major agricultural concern, as it infests ripening fruit rather than rotting fruit. Because of the ability to attack these two pests, P. vindemmiae wasps have great potential as a biological control agent. Investigation of viral tissue distribution, developmental expression profile, transmission strategy, and direct impact on P. vindemmiae wasps revealed that the novel virus had no obvious effects on wasp but infects D. melanogaster and increases their pupal duration and fecundity, possibly providing the wasps with an increased number of pupae and extended pupal periods for parasitization

Methods

Results

Discussion

Compliance with ethical standards