Plant-mediated interactions between a vector and a non-vector herbivore promote the spread of a plant virus

Herbivores that transmit plant pathogens often share hosts with non-vector herbivores. These co-occurring herbivores can affect vector fitness and behaviour through competition and by altering host plant quality. However, few studies have examined how such interactions may both directly and indirectly influence the spread of a plant pathogen. Here, we conducted field and greenhouse trials to assess whether a defoliating herbivore (Sitona lineatus) mediated the spread of a plant pathogen, Pea enation mosaic virus (PEMV), by affecting the fitness and behaviour of Acrythosiphon pisum, the PEMV vector. We observed higher rates of PEMV spread when infectious A. pisum individuals shared hosts with S. lineatus individuals. Using structural equation models, we showed that herbivory from S. lineatus increased A. pisum fitness, which stimulated vector movement and PEMV spread. Moreover, plant susceptibility to PEMV was indirectly enhanced by S. lineatus, which displaced A. pisum individuals to the most susceptible parts of the plant. Subsequent analyses of plant defence genes revealed considerable differences in plant phytohormones associated with anti-herbivore and anti-pathogen defence when S. lineatus was present. Given that vectors interact with non-vector herbivores in natural and managed ecosystems, characterizing how such interactions affect pathogens would greatly enhance our understanding of disease ecology.