Aphids Pick Their Poison: Selective Sequestration of Plant Chemicals Affects Host Plant Use in a Specialist Herbivore

Abstract

In some plant-insect interactions, specialist herbivores exploit the chemical defenses of their food plant to their own advantage. Brassica plants produce glucosinolates that are broken down into defensive toxins when tissue is damaged, but the specialist aphid, Brevicoryne brassicae, uses these chemicals against its own natural enemies by becoming a "walking mustard-oil bomb". Analysis of glucosinolate concentrations in plant tissue and associated aphid colonies reveals that not only do aphids sequester glucosinolates, but they do so selectively. Aphids specifically accumulate sinigrin to high concentrations while preferentially excreting a structurally similar glucosinolate, progoitrin. Surveys of aphid infestation in wild populations of Brassica oleracea show that this pattern of sequestration and excretion maps onto host plant use. The probability of aphid infestation decreases with increasing concentrations of progoitrin in plants. Brassica brassicae, therefore, appear to select among food plants according to plant secondary metabolite profiles, and selectively store only some compounds that are used against their own enemies. The results demonstrate chemical and behavioral mechanisms that help to explain evidence of geographic patterns and evolutionary dynamics in Brassica-aphid interactions.

What doesn’t kill you makes you stronger: The burdens and benefits of toxin sequestration in a milkweed aphid

“…Structural elucidation will be required to identify the types of modifications involved, and further quantification and characterization of cardenolides in different aphid tissue types (e.g., head vs. gut vs. haemocoel) are required to fully elucidate cardenolide sequestration by A. nerii . There are however surprising parallels between this aphid and other sequestration systems; for example, monarch caterpillars match the concentration of their host plant at intermediate levels, but concentrate the toxins from cardenolide‐poor hosts (Agrawal, Ali, Rasmann, & Fishbein, ), and cabbage aphids preferentially sequester specific glucosinolate compounds from a range of structurally similar compounds in their host plant (Goodey, Florance, Smirnoff, & Hodgson, ). Therefore, many sequestering herbivores with variable predator pressures may face the same dilemma of conflicting demands when choosing their host plant.…”

“…A. syriaca differs not only in its cardenolide profile, but also in the chemical structures of its primary cardenolides (Araya, Kindscher, & Timmermann, 2012;Zhang et al, 2014 (Agrawal, Ali, Rasmann, & Fishbein, 2015), and cabbage aphids preferentially sequester specific glucosinolate compounds from a range of structurally similar compounds in their host plant (Goodey, Florance, Smirnoff, & Hodgson, 2015). Therefore, many sequestering herbivores with variable predator pressures may face the same dilemma of conflicting demands when choosing their host plant.…”

Additive effects of plant chemotype, mutualistic ants and predators on aphid performance and survival

“…One example is the recruitment of predators or parasitoids by herbivore‐infested plants (plant–natural enemy–herbivores; e.g., Bálint et al, ; Linhart, Keefover‐Ring, Mooney, Breland, & Thompson, ; Ninkovic, Al Abassi, & Pettersson, ). Some herbivore species (Erb & Robert, ; Goodey, Florance, Smirnoff, & Hodgson, ; Opitz & Müller, ; Prudic, Khera, Sólyom, & Timmermann, ) have also evolved to take advantage of host‐plant‐derived secondary metabolites (including nonvolatile defensive compounds, e.g., salicin derivatives or glucosinolates, and volatile defensive compounds, e.g., benzaldehyde) to use them in their own defence strategies against predation (Dyer, ; Gauld, Gaston, & Janzen, ). Thus, plant within‐species variation in the abundance and composition of secondary metabolites, like VOCs, leading to so‐called different plant chemotypes (i.e., a group of plants with similar chemical profiles; Clancy et al, ; Ghirardo, Heller, Fladung, Schnitzler, & Schroeder, ; Holopainen, Hiltunen, & von Schantz, ; Keefover‐Ring, Thompson, & Linhart, ), can have multiple effects on herbivore populations and the associated arthropod community.…”

Induced plant defences in biological control of arthropod pests: a double‐edged sword

“…Finally, some specialist insect pests may selectively sequester resistance compounds from their host plant and use them for their own defence against their natural enemies . A well‐known example is the selective sequestration of glucosinolates and the concomitant enzyme myrosinase in the cabbage aphid Brevicoryne brassicae (L.), which ‘makes them walking mustard oil bombs’ that are less palatable to predators and parasitoids. Thus, breeding for resistance to generalist pests and pathogens by increasing the levels of glucosinolates may incur the risk of reducing the effectiveness of biocontrol agents.…”