Virus-mediated changes in insect vector tolerance to a neonicotinoid insecticide

Beet curly top virus (BCTV), the causal agent of curly top disease, is an important viral pathogen of sugar beets in the western United States. BCTV is exclusively transmitted by the beet leafhopper (BLH, Neoalitarus tenellus (Baker), also referred to as Circulifer tenullus) in a circulative, non-propagative manner and is primarily managed through insecticides targeting vector. Vector-borne plant viruses have been shown to modify vector biology, behavior, or both, thereby favoring their transmission. In this study, viruliferous BLHs demonstrated increased survival compared to non-viruliferous insects when exposed to a neonicotinoid insecticide at a sub-lethal rate of 0.1x rate but not at the 1x rate. In contrast, no significant difference in survival was observed between viruliferous and non-viruliferous insects treated with a pyrethroid insecticide at either 0.1x or 1x rates. Transcriptomic analysis of BLHs exposed to a 0.1x neonicotinoid treatment revealed that differentially expressed transcripts (DETs) associated with detoxification, ubiquitination, and proteolysis, innate immunity, and stress were upregulated in viruliferous BLHs, potentially contributing to their enhanced survival. In contrast, DETs associated with locomotion and cuticular structure were concomitantly downregulated, suggesting that virus-mediated behavioral adaptations are unlikely to contribute to neonicotinoid tolerance in BLHs. This study represents the first comprehensive transcriptomic investigation of virus-mediated tolerance to a neonicotinoid insecticide.