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

Specialized insect herbivores commonly co‐opt plant defences for protection against predators, but the costs, benefits and mechanisms of sequestration are poorly understood. We quantified sequestration of toxic cardenolides by the specialist aphid Aphis nerii when reared on four closely related milkweed (Asclepias) species with >20‐fold variation in cardenolide content, and in the presence or absence of generalist ladybug predators. Increasing concentrations of apolar plant cardenolides increased sequestered amounts in aphids. High concentrations in plants impaired aphid population growth, but also reduced the top‐down effects of predators. An in vitro enzymatic assay of total cardenolides in aphid bodies using the cardenolides’ target (animal Na⁺/K⁺‐ATPase) revealed that the subset of sequestered cardenolides is disproportionally more toxic than cardenolides in leaves. All aphids accumulated two cardenolides not present in their host plant, even on plants with very low foliar cardenolide concentrations. Sequestration of potent cardenolides by A. nerii thus involves passive, concentration‐dependent uptake from the host plant, as well as a presumably more active mechanism of modification and up‐concentration of plant cardenolides. The concentration of toxins in the host plant thus not only determines the negative impacts on growth and performance of an aphid, but also the ease and efficiency by which toxins are sequestered for the aphid’s defence, making the costs and benefits of plant toxins highly context‐dependent for both the plant and the herbivore. Therefore, variation in plant toxins is of central importance for co‐evolutionary plant–insect interactions, particularly in environments with variable predator pressure. A plain language summary is available for this article.