Do biochemical exaptations link evolution of plant defense and pollination systems? Historical hypotheses and experimental tests with Dalechampia vines

Mapping resin secretion and pollination ecology onto the estimated phylogeny of species of the euphorb vine Dalechampia generated two historical hypotheses: resin rewards offered to pollinators by Dalechampia flowers evolved by minor modification of a preexisting, resin-based, floral defense system, and resin defense of leaves in advanced species evolved by modification of the preexisting resin-reward system. From these hypotheses, we derived two predictions: floral reward resins are chemically similar to putative floral defense resins and exhibit antiherbivore activities, and foliar resins are chemically similar to reward resins and also exhibit antiherbivore activities. We tested these predictions by chemical analyses and by using a broad sample of Neotropical herbivorous insects in a series of bioassays. All floral and foliar resins were chemically similar. Tests with two generalist (Orophus tesselatus, Orthoptera: Tettigoniidae; Atta colombica, Hymenoptera: Formicidae) and four Dalechampia-specialist herbivores (Syphraea sp., Coleoptera: Chrysomelidae; Ectima rectifasciata, Hamadryas ipthime, and Hamadryas amphinome, Lepidoptera: Nymphalidae) showed floral and foliar resin to deter significantly feeding or leaf cutting. These results support our two hypotheses and indicate that, in this system, biochemical exaptations have played a major role in the evolution of plant-insect relationships, adaptations reducing herbivory have affected the evolution of plant-pollinator relationships, and adaptations for pollination have affected the evolution of plant-herbivore relationships.