Does a shift to a novel host plant create a defence-free space for a specialist herbivore species?

While host switches can promote speciation in herbivorous insects, the benefits of switching hosts have only been ascribed to escaping competition and natural enemies. Herbivores might also escape from the defences of their ancestral host if their new host species lacks those defences, but ‘defence-free space’ has not been tested as a potential driver of host-associated speciation by increasing the likelihood of host shifts. We used field and laboratory experiments to test this hypothesis in goldenrod (Solidago spp.) and its gall fly (Eurosta solidaginis). The ancestral host (S. altissima) senses the volatile emissions (a putative sex pheromone) of male flies and increases its defences against both gall induction by the fly and chewing herbivory from co-occurring herbivore species, while the effect of exposure to this emission was unknown for the derived host (S. gigantea). In growth chamber experiments, we found that both host plant species responded similarly to fly pheromone in the levels of signalling phytohormones jasmonic acid and salicylic acid but that only S. altissima experienced reduced feeding by leaf beetles after pheromone exposure. In the field, S. altissima ramets were less preferred by ovipositing female gall flies after pheromone exposure, while there was no effect for S. gigantea. Conversely, pheromone exposure made S. gigantea ramets more susceptible to one type of herbivory: bunch galling by midge species. Our data show that the derived host, S. gigantea, does respond to the gall fly pheromone, but does so in a way that appears maladaptive for the plant, suggesting that escaping the defence of the ancestral host species provides an additional benefit to herbivores and an ecological mechanism for host switching and eventual speciation. Read the free Plain Language Summary for this article on the Journal blog.