Fatal attraction of non‐vector impairs fitness of manipulating plant virus

Abstract

Abstract Host manipulation refers to the expression of a host phenotype that is partly under the genetic control of a parasite. This phenomenon can enhance parasite transmission rates and is responsible for biological marvels such as “Zombie‐ants” and the “fatal attraction” of Toxoplasma‐infected rodents to their feline predators. Such host manipulation has evolved in all major phylogenetic lineages of parasites and is assumed to enhance the fitness of the parasite. However, the capacity to manipulate is not ubiquitous; that is, many clades of parasites comprise manipulating and non‐manipulating species. This pattern leads to the prediction of costs that select against the evolution of manipulation, but this has been difficult to show empirically. In the present study, we used a tripartitate system consisting of chili (Capsicum annuum) plants infected with Pepper golden mosaic virus and colonized by non‐vector whiteflies (Trialeurodes vaporariorum), to study the effects on viral load when a non‐vector herbivore feeds on the infected plants. We observed that virus‐infected plants emitted odours that attracted adult whiteflies, contained three times more amino acids in the phloem than mock‐inoculated controls and supported higher whitefly reproduction as compared to controls. However, viral load decreased almost 100‐fold in whitefly‐carrying plants, which was associated with a depletion of phloem amino acids. Synthesis. We show that a plant virus can suffer from a reduced within‐host reproduction rate when virus‐induced alterations of the plant cause a “fatal attraction” of a non‐vector insect that exploits the altered plant phenotype at its own benefits. The resulting fitness costs might represent a force that can select against the evolution of host manipulation by parasites.