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.

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Nonconsumptive effects (NCE) from natural enemy presence are known to change the behavior, morphology, and development of potential victims. However, the overwhelming majority of these studies focus on predation, documenting changes in prey behavior; far less is understood about parasitism risk and impacts on host physiology. We used the caterpillar Manduca sexta (Lepidoptera: Sphingidae) and two of its main natural enemies—a specialist parasitoid (wasp), Cotesia congregata (Hymenoptera: Braconidae), and a generalist predator (soldier bug), Podisus maculiventris (Hemiptera: Pentatomidae)—to determine how the threat of parasitism and predation during larval development alter prey growth and immunity. Caterpillars developing near female predators and parasitoids were ~ 85% larger compared to individuals without enemy exposure. Development time was not affected by natural enemies when compared to controls, but male P. maculiventris slowed M. sexta development compared to the other natural enemies. For immune functionality, phenoloxidase (PO) activity only responded to parasitoids, with wasp‐exposed caterpillars exhibiting 35% lower PO activity than all other treatments, while lysozyme activity was unaffected by any enemy treatment. This work emphasizes that parasites can induce changes to host immunity that potentially affect wasp development. More broadly, NCEs on victim immunity are likely given immunity's contribution to host defense but have been under‐appreciated compared to more easily observed phenotypes like behavior and morphology.