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.

Hybridization is an important evolutionary mechanism that can increase the fitness and adaptive potential of populations. A growing body of evidence supports its importance as a key factor contributing to rapid evolution in invasive species, but the effects of hybridization have rarely been assessed in intentionally introduced biological control agents. We investigated hybrids between a Swiss and an Italian population of the beetle, Longitarsus jacobaeae, a biological control agent of Jacobaea vulgaris, by reciprocally crossing individuals in the laboratory. Phenological traits of F1 and F2 hybrid lineages showed intermediate values relative to their parental populations, with some maternal influence. Fitness of the F2 generation, measured as lifetime fecundity, was higher than that of the Italian parent in one of the lineages and higher than that of either parent in the other hybrid lineage. The increased fecundity of hybrids may benefit tansy ragwort biological control by increasing the establishment success and facilitating a more rapid population buildup in the early generations. Even though the long-term consequences of hybridization in this and other systems are hard to predict, intentional hybridization may be a useful tool in biological control strategies as it would promote similar microevolutionary processes operating in numerous targeted invasive species.

Transmission of plant pathogens by insect vectors is a complex biological process involving interactions between the plant, insect, and pathogen. Pathogen-induced plant responses can include changes in volatile and nonvolatile secondary metabolites as well as major plant nutrients. Experiments were conducted to understand how a plant pathogenic bacterium, Candidatus Liberibacter asiaticus (Las), affects host preference behavior of its psyllid (Diaphorina citri Kuwayama) vector. D. citri were attracted to volatiles from pathogen-infected plants more than to those from non-infected counterparts. Las-infected plants were more attractive to D. citri adults than non-infected plants initially; however after feeding, psyllids subsequently dispersed to non-infected rather than infected plants as their preferred settling point. Experiments with Las-infected and non-infected plants under complete darkness yielded similar results to those recorded under light. The behavior of psyllids in response to infected versus non-infected plants was not influenced by whether or not they were carriers of the pathogen. Quantification of volatile release from non-infected and infected plants supported the hypothesis that odorants mediate psyllid preference. Significantly more methyl salicylate, yet less methyl anthranilate and D-limonene, was released by infected than non-infected plants. Methyl salicylate was attractive to psyllids, while methyl anthranilate did not affect their behavior. Feeding on citrus by D. citri adults also induced release of methyl salicylate, suggesting that it may be a cue revealing location of conspecifics on host plants. Infected plants were characterized by lower levels of nitrogen, phosphorus, sulfur, zinc, and iron, as well as, higher levels of potassium and boron than non-infected plants. Collectively, our results suggest that host selection behavior of D. citri may be modified by bacterial infection of plants, which alters release of specific headspace volatiles and plant nutritional contents. Furthermore, we show in a laboratory setting that this apparent pathogen-mediated manipulation of vector behavior may facilitate pathogen spread.

Author Summary

In this investigation, we experimentally demonstrate specific mechanisms through which a bacterial plant pathogen induces plant responses that modify behavior of its insect vector. Candidatus Liberibacter asiaticus, a fastidious, phloem-limited bacterium responsible for causing huanglongbing disease of citrus, induced release of a specific volatile chemical, methyl salicylate, which increased attractiveness of infected plants to its insect vector, Diaphorina citri, and caused vectors to initially prefer infected plants. However, the insect vectors subsequently dispersed to non-infected plants as their preferred location of prolonged settling because of likely sub-optimal nutritional content of infected plants. The duration of initial feeding on infected plants was sufficiently long for the vectors to acquire the pathogen before they dispersed to non-infected plants, suggesting that the bacterial pathogen manipulates behavior of its insect vector to promote its own proliferation. The behavior of psyllids in response to infected versus non-infected plants was not influenced by whether or not they were carriers of the pathogen and was similar under both light and dark conditions. Feeding on citrus by D. citri adults also induced the release of methyl salicylate, suggesting that it may be a cue revealing location of conspecifics on host plants.

The influence of viral disease symptoms on the behaviour of virus vectors has implications for disease epidemiology. Here we show that previously reported preferential colonization of potatoes infected by potato leafroll virus (genus Polerovirus) (luteovirus) (PLRV) by alatae of Myzus persicae, the principal aphid vector of PLRV, is influenced by volatile emissions from PLRV-infected plants. First, in our bioassays both differential immigration and emigration were involved in preferential colonization by aphids of PLRV-infected plants. Second, M. persicae apterae aggregated preferentially, on screening above leaflets of PLRV-infected potatoes as compared with leaflets from uninfected plants, or from plants infected with potato virus X (PVX) or potato virus Y (PVY). Third, the aphids aggregated preferentially on screening over leaflet models treated with volatiles collected from PLRV-infected plants as compared with those collected from uninfected plants. The specific cues eliciting the aphid responses were not determined, but differences between headspace volatiles of infected and uninfected plants suggest possible ones.

Crop traits can alter economically important interactions between plants, pests, and biological control agents. For example, a reduced waxy bloom on the surface of pea plants alters interactions between pea aphids and their natural enemies. In this study, we assess whether the effect of wax reduction extends beyond the 2 or 3 arthropod species closely associated with the plants and into the structure of the broader arthropod community of over 200 taxa at our site. We sampled arthropods on lines of peas with normal and reduced wax in Latah Co., Idaho using pitfall traps within randomly assigned pairs of 5 × 5 meter plots. During the 1998 and 1999 growing seasons, we collected 12,113 individual arthropods from 221 unambiguously identified morphospecies. The number of individuals collected from each morphospecies responded idiosyncratically to the reduced wax peas. To test whether arthropod community structure differed between the collections from plots having peas with normal or reduced wax, we performed a randomization test. The collection from peas with reduced wax had higher species evenness and thus higher community diversity despite having lower species richness. Our results demonstrate the potential of a single plant trait, epicuticular wax, to affect a community of arthropods. Two pests of peas had opposite responses to peas with reduced wax. The number of pea aphids collected was greater from peas with normal wax peas than those with reduced wax. In contrast, the number of pea leaf weevils collected was greater from peas with reduced wax.