Pathogens and parasites can induce changes in host or vector behavior that enhance their transmission. In plant systems, such effects are largely restricted to vectors, because they are mobile and may exhibit preferences dependent upon plant host infection status. Here we report the first evidence that acquisition of a plant virus directly alters host selection behavior by its insect vector. We show that the aphid Rhopalosiphum padi, after acquiring Barley yellow dwarf virus (BYDV) during in vitro feeding, prefers noninfected wheat plants, while noninfective aphids also fed in vitro prefer BYDV-infected plants. This behavioral change should promote pathogen spread since noninfective vector preference for infected plants will promote acquisition, while infective vector preference for noninfected hosts will promote transmission. We propose the “Vector Manipulation Hypothesis” to explain the evolution of strategies in plant pathogens to enhance their spread to new hosts. Our findings have implications for disease and vector management.

The transmission of insect-borne plant pathogens, including viruses, bacteria, phytoplasmas, and fungi depends upon the abundance and behavior of their vectors. These pathogens should therefore be selected to influence their vectors to enhance their transmission, either indirectly, through the infected host plant, or directly, after acquisition of the pathogen by the vector. Accumulating evidence provides partial support for the occurrence of vector manipulation by plant pathogens, especially for plant viruses, for which a theoretical framework can explain patterns in the specific effects on vector behavior and performance depending on their modes of transmission. The variability in effects of pathogens on their vectors, however, suggests inconsistency in the occurrence of vector manipulation but also may reflect incomplete information about these systems. For example, manipulation can occur through combinations of specific effects, including direct and indirect effects on performance and behavior, and dynamics in those effects with disease progression or pathogen acquisition that together constitute syndromes that promote pathogen spread. Deciphering the prevalence and forms of vector manipulation by plant pathogens remains a compelling field of inquiry, but gaps and opportunities to advance it remain. A proposed research agenda includes examining vector manipulation syndromes comprehensively within pathosystems, expanding the taxonomic and genetic breadth of the systems studied, evaluating dynamic effects that occur during disease progression, incorporating the influence of biotic and abiotic environmental factors, evaluating the effectiveness of putative manipulation syndromes under field conditions, deciphering chemical and molecular mechanisms whereby pathogens can influence vectors, expanding the use of evolutionary and epidemiological models, and seeking opportunities to exploit these effects to improve management of insect-borne, economically important plant pathogens. We expect this field to remain vibrant and productive in its own right and as part of a wider inquiry concerning host and vector manipulation by plant and animal pathogens and parasites.

The attractiveness of Barley yellow dwarf luteovirus (BYDV)–infected wheat plants to Rhopalosiphum padi L. was evaluated under laboratory conditions.

In choice bioassays, Rhopalosiphum padi L. nonviruliferous apterae preferentially locate near volatile organic compounds (VOCs) emitted from Barley y