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Shifts in Plant Chemical Defenses of Chile Pepper (Capsicum annuum L.) Due to Domestication in Mesoamerica

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.

Introduction

What changes occur in a Neotropical plant’s chemical defenses when it is domesticated for crop production as a food, medicine, vermifuge or condiment, or for all four of these uses? There is remarkably little tested ecological theory regarding how domestication affects plant chemical defenses (Rindos, 1984; Johns, 1990; Casas et al., 2015). This may be because most phytogeographic, agroecological, and archaeobotanical studies of plant domestication have largely used morphological indicators to track the domestication process rather than identifying phytochemical indicators of changes in ecological interactions. As recently argued by Zeder (2017), ecologists need to identify tractable model systems that allows for an assessment of the core assumptions of the Extended Evolutionary Synthesis (EES).

The domestication of crop plants by human cultures provides one such case study opportunity. That is why we propose that the genus Capsicum can serve as important model system for discerning how changes in secondary metabolites (SMs) reveal shifts in plant chemical defenses that have occurred with domestication. In the case of domesticated chile peppers, these shifts influenced both (1) antagonistic interactions with predators and abiotic pressures, and (2) facilitated (including mutualistic) interactions among chiles, their avian dispersers, nurse plants and human cultures. The integration of ethnobotanical, paleoecological, archeological, linguistic, genetic and evolutionary perspectives on chile domestication that has been in process for the last two decades (Tewksbury and Nabhan, 2001; Pickersgill, 2007; Tewksbury et al., 2008b; Aguilar-Meléndez et al., 2009; Haak et al., 2012; Kraft et al., 2014; Carrizo-García et al., 2016) has already contributed substantively to the possibilities of such an EES.

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