Shifts in plant chemical defenses of Chile Pepper (Capsicum annuum L.) due to domestication in Mesoamerica

Abstract

We propose that comparisons of wild and domesticated Capsicum species can serve as a model system for elucidating how crop domestication influences biotic and abiotic interactions mediated by plant chemical defenses. Perhaps no set of secondary metabolites (SMs) used for plant defenses and human health have been better studied in the wild and in milpa agro-habitats than those found in Capsicum species. However, very few scientific studies on SM variation have been conducted in both the domesticated landraces of chile peppers and in their wild relatives in the Neotropics. In particular, capsaicinoids in Capsicum fruits and on their seeds differ in the specificity of their ecological effects from broad-spectrum toxins in other members of the Solanaceae. They do so in a manner that mediates specific ecological interactions with a variety of sympatric Neotropical vertebrates, invertebrates, nurse plants and microbes. Specifically, capsaicin is a secondary metabolite (SM) in the placental tissues of the chile fruit that mediates interactions with seed dispersers such as birds, and with seed predators, ranging from fungi to insects and rodents. As with other Solanaceae, a wide range of SMs in Capsicum spp. function to ecologically mediate the effects of a variety of biotic and abiotic stresses on wild chile peppers in certain tropical and subtropical habitats. However, species in the genus Capsicum are the only ones found within any solanaceous genus that utilize capsaicinoids as their primary means of chemical defense. We demonstrate how exploring in tandem the evolutionary ecology and the ethnobotany of human-chile interactions can generate and test novel hypotheses with regard to how the domestication process shifts plant chemical defense strategies in a variety of tropical crops. To do so, we draw upon recent advances regarding the chemical ecology of a number of wild Capsicum species found in the Neotropics. We articulate three hypotheses regarding the ways in which incipient domestication through "balancing selection" in wild Capsicum annuum populations may have led to the release of selective biotic and abiotic pressures. We then analyze which shifts under cultivation generated the emergence of Capsicum chemotypes, morphotypes and ecotypes not found in high frequencies in the wild. We hypothesize that this "competitive release" can lead to a diversification of the domesticate's investment in a greater diversity of SM potency across different cultural uses, cropping systems and ecogeographic regions. While most studies of plant domestication processes focus on morphological changes that confer greater utility or productivity in human-managed environments, we conclude that changes in the chemical ecology of a useful plant can be of paramount importance to their cultivators. The genus Capsicum can therefore provide an unprecedented opportunity to compare the roles of SMs in wild plants grown in natural Neotropical ecosystems with their domesticated relatives in the milpa agro-ecosystems of Mesoamerica. Even with the current depth of knowledge available for crop species in the genus Capsicum and Solanum, our understanding of how particular SMs affect the reproduction and survival of wild vs. domesticated solanaceous plants remains in its infancy.