Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts

Previous studies have shown that vector-borne pathogens can alter the phenotypes of their hosts and vectors in ways that influence the frequency and nature of interactions between them, with significant implications for the transmission and spread of disease. For insect-borne pathogens, host odors are particularly likely targets for manipulation, as both plant- and animal-feeding insects use volatile compounds derived from their hosts as key foraging cues. Here, we document the effects of a widespread plant pathogen, Cucumber mosaic virus (CMV), on the quality and attractiveness of its host-plant (Cucurbita pepo ‘Dixie’) for two aphid vectors, Myzus persicae and Aphis gossypii. Our results indicate that CMV greatly reduces host-plant quality—aphids performed poorly on infected plants and rapidly emigrated from them—but, remarkably, increases the attractiveness of infected plants to aphids by inducing elevated emissions of a plant volatile blend otherwise similar to that of healthy plants. Thus, CMV appears to deceptively attract vectors to infected plants from which they then rapidly disperse, a pattern highly conducive to the non-persistent transmission mechanism employed by CMV, and very different from the pattern previously reported for persistently transmitted viruses—which require sustained aphid feeding for transmission. Our results thus suggest that transmission mechanism is a major factor shaping pathogen-induced changes in host plant phenotypes. Furthermore, our findings yield a general hypothesis that, where vector-borne plant or animal pathogens reduce host quality for vectors, pathogen-induced changes in host phenotypes that enhance vector attraction will frequently involve the exaggeration of existing host-location cues.