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

Abstract

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, because 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 one of its host plants (Cucurbita pepo cv. 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 increases the attractiveness of infected plants to aphids by inducing elevated emissions of a plant volatile blend otherwise similar to that emitted by healthy plants. Thus, CMV appears to attract vectors deceptively to infected plants from which they then disperse rapidly, a pattern highly conducive to the nonpersistent transmission mechanism employed by CMV and very different from the pattern previously reported for persistently transmitted viruses that require sustained aphid feeding for transmission. In addition to providing a documented example of a pathogen inducing a deceptive signal of host-plant quality to vectors, our results suggest that the transmission mechanism is a major factor shaping pathogen-induced changes in host-plant phenotypes. Furthermore, our findings yield a general hypothesis that, when vector-borne plant or animal pathogens reduce host quality for vectors, pathogen-induced changes in host phenotypes that enhance vector attraction frequently will involve the exaggeration of existing host-location cues.