Toxin or medication? Immunotherapeutic effects of nicotine on a specialist caterpillar

Abstract

Abstract A core tenant in the field of ecological immunology is that immune responses trade off with other physiological functions due to resource allocation costs. Caterpillars, for example, tend to exhibit reduced immune responses when reared on more toxic food plants due to a cost from detoxifying or sequestering secondary metabolites, also known as the ‘vulnerable host hypothesis’. However, support for this hypothesis is mixed, and studies have not yet mechanistically isolated the relative contributions of total plant defences, specific metabolites or macro‐nutritional quality. We used the tobacco hornworm Manduca sexta, a specialist herbivore on plants in the nightshade family (Solanaceae), to investigate trade‐offs in immune response. This system is ideal given the availability of solanaceous plant lines varying in general (i.e. jasmonate‐induced) and specific (i.e. nicotine) resistance traits. We also applied a geometric diet stoichiometry approach to examine how phytochemical toxicity and nutritional quality interactively impact insect immunity and performance. We predicted that as plant toxicity increased, immune activity and herbivore performance would decrease. Increasing food plant toxicity reduced insect growth and development, as predicted, but contrary to our hypothesis, plant toxicity did not trade off with immune parameters. Surprisingly, specific plant chemicals, in this case nicotine, appeared immunotherapeutic, stimulating the phenoloxidase (PO) immune response of M. sexta. Available nutrients in artificial diets, mainly protein, also strongly impacted insect growth, but did not affect PO activity, while diets supplemented with nicotine enhanced the PO and melanization response. This work highlights how specific secondary metabolites, and not overall plant toxicity, impact the immune response. Importantly, our data also suggest an alternative mechanism (i.e. immune enhancement) for reduced parasitoid performance when reared from hosts on toxic plants via tritrophic interactions. A free Plain Language Summary can be found within the Supporting Information of this article.