Parasitoid-host interactions are influenced by virus-induced changes in plant chemistry

Plant viruses alter the chemistry, nutritional value, and morphology of hosts. These changes have implications for both pathogen transmission and the fitness of other organisms utilizing infected plants. While plant viruses have been well studied in terms of host performance and yield, few studies have examined how infection influences insect herbivores and their natural enemies. In this study, we examined the chemical mediation of interactions among a widespread plant pathogen (Cucumber mosaic virus [CMV]), a common host (cultivated squash), an aphid vector (Myzus persicae), and the aphid parasitoid Aphidius colemani. Previous research in this system has demonstrated that CMV-infected plants are poor hosts for aphids relative to healthy plants. In addition to disrupting aphid reproduction, we found that CMV-infection in aphid host plants is associated with an increase in susceptibility to A. colemani. A higher percentage of wasp larvae successfully completed their development in aphids growing on CMV-infected plants relative to healthy plants. Furthermore, we found that the timing of exposure to CMV-infected plants is critical and that the differences in development do not stem from female wasps failing to parasitize hosts on healthy plants. Chemical analysis of infected and healthy plants documented several key differences in plant hormones and amino acids that may be mediating reduced aphid reproduction and increased susceptibility to parasitoids. In addition to demonstrating that a plant pathogen can influence populations of predatory insects, these results have important implications for aphid host behavior and virus transmission.