Interactions between plants and herbivorous insects have been models for theories of specialization and coevolution for over a century, and it is well-established that phytochemicals govern many aspects of these interactions. Despite this, the mechanisms insect specialists employ to sequester or otherwise tolerate plant secondary metabolites, and the costs of these responses, remain poorly characterized. Here, we use a milkweed-specialist aphid model, the Aphis nerii system, to characterize responses of A. nerii to phytochemical variation. We use milkweed plant species that represent a broad range of toxicity test to the effects of increased plant secondary metabolites on aphid life history traits in both the laboratory and field and on whole transcriptome gene expression.
We show that increased secondary metabolites have a negative effect on aphid development and lifetime fecundity in the laboratory. In the field, A. nerii readily colonize all host plant species, but aphids feeding on increased secondary metabolite plants experience greater proportions of parasitism. Despite deleterious effects on fitness, A. nerii differenitally express only about 1% of their total transcriptome when feeding on different host plants. When feeding on host plants with higher levels of secondary metabolites, aphids differentially express a narrow, targeted set of genes including those involved in canonical detoxification processes including cytochrome P450s, hydrolases, UDP-glucuronosyltransferases, and ABC transporters. These results indicate that A. nerii marshal a variety of metabolic detoxification mechanisms in host plant specialization and circumvention of milkweed secondary compounds, but not without deleterious effects on fitness. We present the first whole transcriptome analysis for secondary metabolite degradation and metabolism in a milkweed specialist and these results provide important insights into secondary metabolite detoxification and insect adaptations to toxic host plants.