Plant viruses alter insect behavior to enhance their spread

Abstract

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.

Fungal DNA virus infects a mycophagous insect and utilizes it as a transmission vector

“…This is very common in plant/virus/vector systems, such as geminiviruses, which could modulate their hosts to attract whiteflies (36); tomato spotted wilt tospovirus, which could affect its transmission vector Frankliniella fusca by regulating its host plant (37); barley yellow dwarf virus, which could change its host to attract aphids (38); and cucumber mosaic virus, which could change the host's volatiles to attract pollinators (39). These natural phenomena may be universal, as SsHADV-1-infected fungal strains could release less repellent volatile compounds to attract the adults of L. ingenua than virusfree strains do.…”

New Synthesis: A Holobiontic View on Plant-Insect Interactions

“…hypothesis" has been contrasted with the "vector manipulation hypothesis" that addresses either microbe-mediated changes in the plant's phenotype or changes in insect behavior, respectively (Ingwell et al 2012). These effects could be generalized as a "sender or receiver manipulation hypothesis" in chemical plant-insect communication.…”

“…Recent findings show that microorganisms are not passive partners but manipulate either the sender or the receiver of signals and/or cues (or initiate signaling by themselves). Accordingly, for plant pathogens, the "host manipulation hypothesis" has been contrasted with the "vector manipulation hypothesis" that addresses either microbe-mediated changes in the plant's phenotype or changes in insect behavior, respectively (Ingwell et al 2012). These effects could be generalized as a "sender or receiver manipulation hypothesis" in chemical plant-insect communication.…”

“…This switch was presumably triggered by lower nutrient quality provided by the infected plants. While in this example the sender was manipulated, a study by Ingwell et al (2012) reported on the manipulation of the receiver's behavioral response towards plant cues. Aphids (Rhopalosiphum padi) carrying the Barley yellow dwarf virus preferred healthy winter wheat plants, whereas aphids not serving as vectors chose plants that were already infected with the virus, which also differ in their volatile profiles compared with healthy plants (see references in Ingwell et al 2012).…”

“…While in this example the sender was manipulated, a study by Ingwell et al (2012) reported on the manipulation of the receiver's behavioral response towards plant cues. Aphids (Rhopalosiphum padi) carrying the Barley yellow dwarf virus preferred healthy winter wheat plants, whereas aphids not serving as vectors chose plants that were already infected with the virus, which also differ in their volatile profiles compared with healthy plants (see references in Ingwell et al 2012).The hologenome theory (Rosenberg and Zilber-Rosenberg 2011) proposes that the genetic information of the microbiome associated with a host changes with environmental conditions, affects the host's and the microbes' fitness and can be transmitted to subsequent generations. The studies mentioned above do not address all aspects required to align plantinsect-microbe tritrophic interactions with the hologenome theory.…”