Evolutionary changes in an invasive plant support the defensive role of plant volatiles

It is increasingly evident that plants interact with their outside world through the production of volatile organic compounds,1–5 but whether the volatiles have evolved to serve in plant defense is still a topic of considerable debate.3,6–8 Unharmed leaves constitutively release small amounts of volatiles, but when the leaves are damaged by herbivorous arthropods, they emit substantially more volatiles. These herbivore-induced plant volatiles (HIPVs) attract parasitoids and predators that kill insect herbivores,9–12 and this can benefit the plants.13,14 As yet, however, there is no tangible evolutionary evidence that this tritrophic interplay contributes to the selection forces that have shaped the volatile emissions of plants.2,3,5–8,15 With this in mind, we investigated the evolutionary changes in volatile emissions in invasive common ragwort and the respective defensive roles of its constitutive and inducible volatiles. This Eurasian plant has invaded other continents, where it evolved for many generations in the absence of specialized herbivores and their natural enemies. We found that, compared to native ragworts, invasive plants release higher levels of constitutive volatiles but considerably lower levels of herbivore-induced volatiles. As a consequence, invasive ragwort is more attractive to a specialist moth but avoided by an unadapted generalist moth. Importantly, conforming to the indirect defense hypothesis, a specialist parasitoid was much more attracted to caterpillar-damaged native ragwort, which was reflected in higher parasitism rates in a field trial. The evolution of foliar volatile emissions appears to be indeed driven by their direct and indirect roles in defenses against insects. [Display omitted] •The evolution of invasive plants can provide insight into the function of volatiles•Invasive ragwort releases more constitutive but fewer inducible volatiles•The invader is more attractive to a specialist herbivore but less to its parasitoid•The evolution of volatiles from invasive ragwort supports their defensive function Lin et al. compare constitutive and herbivore-induced volatiles emitted by ragwort plants from native and invasive areas. The observed differences and the corresponding behavioral responses of a specialist and a generalist herbivore as well as of a parasitic wasp support the hypothesis that volatiles evolved as plant defenses.