Insect-vectored diseases cause serious losses in many agricultural crops worldwide, and disease management strategies often focus on managing vector populations to limit pathogen transmission. Improved understanding of the complex interactions among plants, pathogens, and insect vectors will therefore inform the development of more effective and sustainable management strategies. The impact of infection on plant quality and attractiveness to insect vectors is a key issue, and the dependence of pathogens and herbivores on a common host plant creates the potential for both mutualistic and antagonistic interactions. We examined interactions among the ubiquitous, non-persistently transmitted pathogen Cucumber mosaic virus (CMV), two common aphid vectors (Myzus persicae and Aphis gossypii), and the cultivated squash plant Cucurbita pepo ‘Dixie’. The effects of CMV on host-plant quality for aphids and on plant volatile production were examined in field and greenhouse experiments. Aphid population growth, host-plant preferences, and behavioral responses to plant odors and plant surfaces were assayed.
Our results indicate that CMV induces changes in host plants that enhance the initial attraction aphid vectors but lead to rapid dispersal. We found that infection induces increased production of plant volatiles in a composition similar to that of healthy plants. However, experiments examining the growth and reproduction of aphids on healthy and infected plants suggest that infected plants are relatively poor hosts for aphids. Field experiments assessing aphid preference support this result. We found that aphids vectors preferentially arrest on healthy plants over infected plants when they are grown in common plots. These results indicate that CMV induces a volatile profile that is attractive to potential vectors and that infection reduces host quality, favoring the rapid dispersal of vectors after they have acquired the virus. This induced chemical condition has important implications for virus fitness, since non-persistently transmitted viruses such as CMV are transmitted most efficiently when vectors feed on infected plants for short periods of time before dispersing to susceptible hosts.