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

1. 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 defenses, specific metabolites, or
macro-nutritional
quality.      2. We
used the tobacco hornworm (Manduca sexta), a specialist herbivore on
plants in the nightshade family (Solanaceae), to investigate tradeoffs 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. 3. 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. 4. 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 tri-trophic interactions.