Reciprocal plant-mediated interactions between a virus and a non-vector herbivore

Vector-borne viruses alter many physical and chemical traits of their plant hosts, indirectly affecting the fitness and behavior of vectors in ways that promote virus transmission. However, it is unclear whether viruses induce plant-mediated shifts in the behavior and fitness of non-vector herbivores, or if non-vectors affect the dynamics of vector-borne viruses. Here we evaluated reciprocal interactions between Pea enation mosaic virus (PEMV), a pathogen transmitted by the aphid Acrythosiphon pisum, and a non-vector weevil, Sitona lineatus. In the field, PEMV-infected plants experienced more defoliation from S.lineatus than uninfected plants; behavioral assays similarly showed S.lineatus adults preferred to feed on infected plants. In turn, infectious A.pisum preferred plants damaged by S.lineatus, and S.lineatus herbivory led to increased PEMV titer. These interactions may be mediated by plant phytohormone levels, as S.lineatus induced jasmonic acid, while PEMV induced salicylic acid. Levels of abscisic acid were not affected by attack from either PEMV or S.lineatus alone, but plants challenged by both had elevated levels of this phytohormone. As plant viruses and their vectors often exist in diverse communities, our study highlights the importance of non-vector species in influencing plant pathogens and their vectors through host-mediated effects.