Leaf herbivory increases plant fitness via induced resistance to seed predators

Early-season herbivory can cause plants to induce resistance to subsequent herbivores, and this ubiquitous plant defense strategy has been shown to be adaptive when subsequent vegetative-feeding herbivores impact plant fitness. However, a growing number of studies show that leaf herbivory can also induce defenses in plant reproductive tissues, which may deter mutualists such as pollinators and seed dispersers, or antagonists such as florivores and seed predators. Due to their direct interaction with plant reproductive tissues, deterrence of these mutualists or antagonists may have large negative or positive effects on plant fitness. Despite numerous predictions, we know little regarding the fitness consequences of leaf-to-reproductive tissue induction in nature. Here, using observations of natural populations and manipulative field experiments, we show that leaf herbivory by the invasive Japanese beetle (Popillia japonica) induces an accumulation of jasmonic acid and complex phenolics in reproductive tissues of the common evening primrose (Oenothera biennis). Consequently, seed predation by three native Lepidoptera is reduced by 77% on beetle-induced plants, while leaf herbivory itself has little impact on lifetime reproductive output. These results show that O. biennis benefits from being consumed by an invasive folivore, and that leaf-to-reproductive tissue induction can be an adaptive trait. Induced plant defenses can therefore be beneficial in a broader community context than previously realized.