Plants collectively produce hundreds of thousands of specialized metabolites that are not required for growth or development. Each species has a qualitatively unique profile, with variation among individuals, growth stages, and tissues. By the 1950s, entomologists began to recognize the supreme importance of these metabolites in shaping insect herbivore communities. Plant defense theories arose to address observed patterns of variation, but provided few testable hypotheses because they did not distinguish clearly among proximate and ultimate causes. Molecular plant-insect interaction research has since revealed the sophistication of plant metabolic, developmental, and signaling networks. This understanding at the molecular level, rather than theoretical predictions, has driven the development of new hypotheses and tools and pushed the field forward. We reflect on the utility of the functional perspective provided by the optimal defense theory, and propose a conceptual model of plant defense as a series of layers each at a different level of analysis, illustrated by advances in the molecular ecology of plant-insect interactions.

More than 87% of flowering plant species are animal-pollinated [1] and produce floral scents and other signals to attract pollinators. These floral cues may however also attract antagonistic visitors, including herbivores [2]. The dilemma is exacerbated when adult insects pollinate the same plant that their larvae consume. It remains largely unclear how plants maximize their fitness under these circumstances. Here we show that in the night-flowering wild tobacco Nicotiana attenuata, the emission of a sesquiterpene, (E)-α-bergamotene, in flowers increases adult Manduca sexta moth-mediated pollination success, while the same compound in leaves is known to mediate indirect defense against M. sexta larvae [3, 4]. Forward and reverse genetic analyses demonstrated that both herbivory-induced and floral (E)-α-bergamotene are regulated by the expression of a monoterpene-synthase-derived sesquiterpene synthase (NaTPS38). The expression pattern of NaTPS38 also accounts for variation in (E)-α-bergamotene emission among natural accessions. These results highlight that differential expression of a single gene that results in tissue-specific emission of one compound contributes to resolving the dilemma for plants when their pollinators are also herbivores. Furthermore, this study provides genetic evidence that pollinators and herbivores interactively shape the evolution of floral signals and plant defense.

Plants emit an extraordinary diversity of chemicals that provide information about their identity and mediate their interactions with insects. However, most studies of this have focused on a few model species in controlled environments, limiting our capacity to understand plant-insect chemical communication in ecological communities. Here, by integrating information theory with ecological and evolutionary theories, we show that a stable information structure of plant volatile organic compounds (VOCs) can emerge from a conflicting information process between plants and herbivores. We corroborate this information “arms race” theory with field data recording plant-VOC associations and plant-herbivore interactions in a tropical dry forest. We reveal that plant VOC redundancy and herbivore specialization can be explained by a conflicting information transfer. Information-based communication approaches can increase our understanding of species interactions across trophic levels.