Caterpillar counter-adaptations to hooked trichomes: does the coevolutionary arms race continue?

Abstract

Plants protect themselves against herbivory with diverse chemical and physical defences, and many herbivores have evolved counter-adaptations against these defences. So far, little is known about herbivore counter-adaptations to physical plant defences and their underlying mechanisms. Here, we investigated how specialised Heliconiini caterpillars are able to cope with the hooked trichomes of Passiflora adenopoda vines. P. adenopoda trichomes have sharp tips reinforced with silica, in contrast to simpler trichomes of other Passiflora that do not deter Heliconiini larvae. While Heliconius melpomene and H. erato caterpillars placed on P. adenopoda leaves were arrested and their soft cuticle was pierced by the sharp hooked trichomes, H. charithonia and Dryas iulia caterpillars of all sizes could move easily over the leaves without any injury. The superior performance of these two species on trichome-bearing leaves can be explained by their thicker and more puncture-resistant cuticle. Morphological and penetrometry measurements showed that the relevant cuticle regions in H. charithonia and D. iulia caterpillars are significantly thicker and more puncture-resistant than in H. melpomene and H. erato. When we tested the ability of the caterpillars to feed on P. adenopoda leaves with hooked trichomes, only H. charithonia survived, indicating the existence of further, previously unknown post-ingestive adaptations. Understanding insect counter-adaptations to physical plant defences is essential for studying the evolutionary arms-race between plants and insect herbivores.