How the chili got its spice: Ecological and evolutionary interactions between fungal fruit pathogens and wild chilies

Abstract

Most species depend on other species for survival and reproduction, thus coevolution - reciprocal evolutionary change between species - arguably plays a dominant role in the origin and organization of biodiversity. We used a novel model system to study coevolutionary dynamics: wild chili peppers and their fruit-associated fungal pathogens. The spiciness of chilies (caused by the antimicrobial chemical capsaicin) protects chili fruits from fungi that can destroy seeds. We examined the ecological and evolutionary interactions between chilies and fungal pathogens by using a combination of field experiments, lab work, and biodiversity analyses. We demonstrate that fungal pathogen pressure varies across the landscape, and impacts fruit infection rates and alters the role of fungal insect vectors. We also show that variation in chili spiciness selects for fungal tolerance to plant defenses and drives fungal local adaptation. However, increased fungal tolerance to capsaicin comes with costs that impact fungal competitive ability and constrain the process of coevolution. Finally, we show that the production of capsaicin by chilies impacts the biodiversity and community structure of fungal fruit inhabitants. We demonstrate that capsaicin has a positive effect on fungal diversity, and that capsaicin has differential impacts on taxa within the fungal community. Combined, these findings provide compelling evidence that coevolutionary dynamics between plants and fungal pathogens are likely to be responsible for the major property of one of the most popular spice plants in the world: the spiciness of chilies.