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

Abstract

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 http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13144/suppinfo is available for this article.

Cardenolide Intake, Sequestration, and Excretion by the Monarch Butterfly along Gradients of Plant Toxicity and Larval Ontogeny

“…pulchra. These milkweeds are closely related, have similar stem and leaf morphologies and all typically occur in mesic habitats, but vary broadly in cardenolide concentrations (Züst et al 2018). The subspecies Asclepias I. pulchra and A. i. incarnata are distinct phylogenetically (Fishbein et al 2011), and differ in a range of traits including leaf shape and trichomes (Agrawal et al 2009).…”

“…Experiment 4: In Vitro Inhibition of the Na + /K + -ATPase In Experiment 4 we used an enzyme assay to examine the inhibitory effects of the extracts of leaves, frass, and adult butterflies from Experiment 1. The same samples were partitioned for analysis in the Na + /K + ATPase assay and HPLC, allowing direct comparison of estimates of cardenolide concentrations from their enzyme inhibition versus from peak area (Petschenka and Agrawal 2015;Züst et al 2018;Züst et al 2019). The enzyme assay offers the opportunity to examine biological activity, which can be more ecologically meaningful than HPLC-quantification.…”

“…A benefit of investigating sequestration among these close plant relatives is that many of the cardenolides are shared between species. Nonetheless, our host plants exhibit tremendous quantitative variation in cardenolides of more than ten-fold in total concentration (Züst et al 2018). We estimate cardenolide concentrations and diversity using high performance liquid chromatography (HPLC), and additionally we assess inhibition of Na + /K + -ATPase in vitro in order to quantify the inhibitory effects of leaf, frass, and adult butterfly extracts to address the relative toxicity of consumed versus sequestered cardenolides.…”

Consequences of pharmacophagous uptake from plants and conspecifics in a sawfly elucidated using chemical and molecular techniques

“…Although the extent to which sequestration is actually costly varies considerably between species (Zvereva and Kozlov, 2016), there are some clear cases where dealing with high toxin load during pharmacophagy incurs a physiological burden (Camara, 1997;Züst et al, 2018). The variability between species does however suggest that sequestration costs likely depend heavily on the nature of the compound/s being obtained and on an organism's physiological mechanisms for dealing with them (Heckel, 2014).…”

Interacting phenotypes and the coevolutionary process: Interspecific indirect genetic effects alter coevolutionary dynamics

“…Examples of interspecific phenotypic manipulation are common in nature (Table 1), and many of these cases can be argued to be putative cases of IIGEs. One possible example occurs in arbuscular mycorrhizae, where the genotypes of fungal mutualists can alter root traits in the plants they plantmicrobe joint trait microbially mediated trait diffuse (Friesen et al 2011, O'Brien et al 2021 hostmicrobiome host control host-microbiome interaction diffuse (Stappenbeck andVirgin 2016, Foster et al 2017) consumerresource toxin sequestration both (Züst et al 2018) inhabit (Gianinazzi-Pearson et al 2007). In host-parasite systems, parasite manipulation of host traits (such as behavior) and reciprocal host manipulation of parasite traits (such as growth rate, via immune response) are key features of species interactions (Thomas et al 2012).…”