Arms race of physical defences: hooked trichomes of Macaranga ant-plants kill lycaenid caterpillars, but one specialist has a counter-defence.

Abstract

The coevolution of insects and chemical plant defences has been described as an arms race, but it is unclear whether physical plant defences can produce similar outcomes. Here, we report a previously unknown interaction from the mutualism between ants and Macaranga trees. Although Macaranga trees are well protected against herbivory by aggressive ants, caterpillars of the genus Arhopala (Lepidoptera: Lycaenidae) can feed on the leaves by appeasing the ants with nectar-like secretions. One ant-plant species, M. trachyphylla, bears hooked trichomes on its green surfaces. When placed on M. trachyphylla stems or petioles, Arhopala caterpillars associated with other Macaranga species (A. major, A. dajagaka and A. zylda) were quickly arrested by the sharp trichomes that pierced their cuticle, resulting in death by rapid blood loss and removal by ants. In striking contrast, A. amphimuta caterpillars, which occur naturally on M. trachyphylla, could easily walk over the hooked trichomes without any injury. As hooked trichomes are a novel trait within Macaranga, this interaction provides an example of de novo evolution of a physical plant defence, which in turn has been overcome by a specialist herbivore. Our study suggests that physical plant defences can lead to evolutionary arms races similar to those for chemical defences.