The nutritional properties of fruits that attract dispersers can also attract harmful organisms such as microbes and seed predators. Production of defensive chemicals in fruits is often invoked as a way to mediate interactions between dispersers and consumers that negatively impact plant fitness. We examine the relationship between fungal fruit pathogens, insect vectors, and fruit defensive chemistry in wild chili peppers. We take advantage of a natural polymorphism in capsaicin production (the chemical responsible for heat in chilies) in wild populations of Capsicum chacoense to study the impact of capsaicin on fungal performance and insect-mediated transmission in the field. A fungal pathogen, Fusarium, infects fruit and kills seeds. Fungal infection appears actively facilitated by insects, as previous work has demonstrated a positive relationship between the number of insect foraging scars and the degree of fungal infection on seeds. We used a low pungency polymorphic population (LP) and a completely pungent population (HP) to ask the following questions: 1) Are fungal strains locally adapted to the capsaicin levels they experience? If so, does tolerance come with costs? 2) Are insects actively transmitting fungus? What is the relative impact of different insect species on fungal infection? Do capsaicin-producing plants have lower infection rates?
To address question set 1, we used false-fruit media with manipulated levels of capsaicin to test fungal performance. We demonstrate that strains isolated from the HP population exhibit higher growth rates in the presence of capsaicin than the LP population. Furthermore, we show that capsaicin tolerance comes with costs; strains from the LP population grew faster without capsaicin than strains from the HP population. To address question set 2, we used these populations to create reciprocal transplant gardens and conduct a field experiment with treatments that included surface sterilized fruits, bagged insects, and sterile needle holes. We found that insect holes have higher infection rates than those made by sterile needles and that not all insects are equal in their ability to transmit fungus. Finally, we found that pungent plants had lower overall seed infection rates than non pungent plants.