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.

Figure 1. Diagrammatic illustration of the dual-choice bioassay arena used in experiments.

Adapted from Castle et al.. 1, BYDV-infected wheat; 2, sham-inoculated wheat; 3, vial (5.5 x2.5 cm; Lx D) initially containing 50 aphids; 4, tube (16x2.5 cm; LxD); 5, platform (15 cm; D); 6, lid enclosing the arena.

Figure 2. Mean proportion of infective and noninfective aphids responding in a dual-choice bioassay examining host plant selection preferences to BYDV-infected and sham-inoculated wheat (noninfected plants previously fed upon by noninfective aphids) as influenced by indirect effects of feeding on virus-infected plants.

Each replicate (n = 12) consisted of one arena with noninfective aphids paired with one arena of infective aphids, randomized in a complete block design over time. Statistical analyses compared the response of infective and noninfective aphids to the BYDV-infected or sham-inoculated plant treatment. (a) Aphid responses at the first observation point made 12 h after release. Noninfective aphids preferred BYDV-infected wheat compared to infective aphids (generalized linear model; χ² = 3.12, p = 0.0774, marginally significant). Infective aphids preferred sham-inoculated plants compared to noninfective aphids (generalized linear model; χ² = 3.12, p = 0.0774, marginally significant). (b) Aphid responses pooled over time (6 observations). Noninfective aphids significantly preferred BYDV-infected wheat compared to infective aphids (generalized linear model; χ² = 19.33, p < 0.0001). Infective aphids significantly preferred sham-inoculated plants compared to noninfective aphids (generalized linear model; χ² = 20.14, p < 0.0001). Data are means ± SE following logit transformation. Errors bars are s.e.m.

Figure 3. Diagrammatic illustration of a membrane feeding chamber.

1, artificial diet solution (100 µL); 2, upper layer of Parafilm®; 3, bottom layer of Parafilm®; 4, humid chamber; 5, petri dish (5.5 cm; D); 6, moist filter paper.

Figure 4. Mean proportion of infective and noninfective aphids responding in a dual-choice bioassay examining host plant selection preferences to BYDV-infected and sham-inoculated wheat plants as influenced by direct effects of virus acquisition following membrane feeding.

Each replicate (n = 12) consisted of one arena with noninfective aphids paired with one arena of infective aphids, randomized in a complete block design over time. Statistical analyses compared the response of infective and noninfective aphids to the BYDV-infected or sham-inoculated plant treatment. (a) Aphid responses at the first observation point made 12 h after release. Noninfective aphids significantly preferred BYDV-infected wheat compared to infective aphids (generalized linear model; χ² = 4.24, p = 0.0394). Infective aphids significantly preferred sham-inoculated wheat compared to noninfective aphids (generalized linear model; χ² = 5.64, p = 0.0176). (b) Aphid responses pooled over time (6 observations). Noninfective aphids significantly preferred BYDV-infected wheat compared to infective aphids (generalized linear model; χ² = 16.18, p < 0.0001). Infective aphids significantly preferred sham-inoculated wheat compared to noninfective aphids (generalized linear model; χ² = 16.32, p < 0.0001). Data are means ± SE following logit transformation. Errors bars are s.e.m.