Herbivore offense and plant defense in a community of specialized herbivores

Xosé López Goldar, Amy P. Hastings and Anurag A. Agrawal, Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, Tobias Züst, Institute of Plant Sciences, University of Bern, Bern, NY, Switzerland

Background/Question/Methods
The diversity and complexity of plant-enemy interactions stem from their degree of coevolutionary specialization and asymmetric nature, especially when multiple specialists feed on the same host plant. As a result, most plants species evolved a diverse array of defensive compounds in their tissues. Despite the fact that herbivore species frequently feed on different plant tissues, the extent to which ‘plant defense-insect offense’ interactions are evolutionarily compartmentalized among plant tissues is unknown. Here we test how roots, leaves, buds and seeds of the tropical milkweed (Asclepias curassavica) are differentially defended by cardenolide toxins, and how their respective specialized herbivores are adapted to the concentration and potency (i.e., relative toxicity of a fixed concentration) of cardenolides from those plant tissues. We quantified cardenolide diversity and concentrations in extracts of plant tissues by liquid chromatography, and also applied extracts to in vitro assays of the insects’ neural Na/K-ATPases, the specific target of cardenolides.
Results/Conclusions
Tolerance of plant toxins in three specialist herbivores was proportional to the cardenolide concentrations they typically encounter in the plant tissues they eat. Nonetheless, because of an apparent trade-off between concentration and potency of cardenolides, these specialists are not necessarily well-adapted to the specific cocktail of toxins in their home tissue. The seed bug was well-adapted to both the high concentration and low potency of cardenolides from its home tissue (seeds). In contrast, the monarch was compromised by both the concentration and potency of toxins in the tissues it eats (buds and leaves) compared to other tissues. Finally, the root beetle, which also feeds on leaves and buds as an adult, was most adapted to root tissues due to their low cardenolide concentration, despite their strong potency. The matches and mismatches between plant tissue defense and insects’ tolerance of toxins shown here suggests ‘lock and key’ coevolutionary mechanisms between the insect enzyme and specific plant cardenolides. It appears that multiple independent coevolutionary interactions may be proceeding between a plant species and its associated herbivore community with species that feed on different plant tissues.