Asymmetry of plant-mediated interactions between specialist aphids and caterpillars on two milkweeds

Plant-mediated interactions between co-occurring herbivores play an important role in insect herbivore communities. Although induced resistance pathways associated with jasmonic acid and salicylic acid are often implicated in such plant-mediated interactions, there are few examples from non-model systems involving specialized herbivores that regularly interact in nature. Here, we tested reciprocal impacts between co-occurring specialist herbivores from two feeding guilds, monarch caterpillars Danaus plexippus and oleander aphids Aphis nerii, on two co-occurring and closely related, but defensively contrasting milkweeds, Asclepias syriaca and A. tuberosa. Larvae grew 38% faster on aphid-infested A. syriaca compared to controls. Reciprocally, aphid growth was >50% lower on caterpillar-damaged A. syriaca compared to controls. While caterpillar feeding on A. syriaca induced a jasmonate burst and higher defensive end products (cardenolides and latex), this induction was substantially attenuated in the presence of aphids. We found a negative correlation between jasmonic acid and salicylic acid only on A. syriaca infested by both caterpillars an aphids. Asclepias tuberosa displayed distinct hormonal dynamics and lacked induction of defensive end products. Accordingly, we found no evidence for plant-mediated interactions between monarchs and aphids on A. tuberosa. Thus, A. syriaca has specific responses to each herbivore, but if challenged simultaneously, the outcome is asymmetric: monarchs benefit from defence attenuation by aphids, while aphids are impaired by monarch feeding. Our results suggest phytohormonal trade-offs induced by two feeding guilds can differ between closely related plant species, and our notion of trade-offs in defence based on phytohormonal pathways would improve with further comparative designs from both model and non-model systems.