Fungal adaptation to spicy environments: Tradeoffs, local adaptation, and the potential for a coevolutionary arms race

Most species depend on other species for their survival and reproduction, thus coevolution arguably plays a dominant role in the origin and organization of biodiversity. The study of reciprocal adaptation requires systems with strongly interacting partners, variation in selective pressures across landscapes, and knowledge of the context in which selection occurs. Chili peppers (Capsicum) and their fruit-associated fungal pathogens provide an ideal system for the study of coevolution and local adaptation. Working in three species of wild chili polymorphic for the production of capsaicinoids, we show that Fusarium infection of fruits negatively impacts plant fitness, and that the production of capsaicinoids in the fruits of chilies mediates this interaction by inhibiting fungal growth in fruits. Further, we map the geographic structure of capsaicinoid production within and across species, and show that Capsicum populations vary in the percentage of plants that contain capsaicinoids, the total capsaicinoid concentration in pungent fruit, and in the ratio of capsaicin to dihydrocapsaicin, the two primary capsaicinoids. This geographic structure in chemical environments suggests the potential for local coadaptation between fungal pathogens and fruit phenotypes. We used a media-based approach to look for local adaptation of fungal growth rates and to determine if variance in the ratio of capsaicinoids in fruit affects fungal growth. We measured growth of 18 fungal isolates derived from high, medium, and low capsaicinoid environments on media with 11 treatments varying total capsaicinoid level and capsaicin to dihydrocapsaicin ratio. Our results demonstrate that capsaicin is more effective at deterring fungal growth than dihydrocapsaicin, indicating that relatively small chemical changes in fruit chemistry have an impact on fungal performance. Finally, in the absence of capsaicin, strains originating from less pungent fruits have greater growth than strains originating from very pungent fruits, suggesting that increased tolerance to capsaicin comes with costs for the fungus.