Where did the Chili Get its Spice? Biogeography of Capsaicinoid Production in Ancestral Wild Chili Species

Abstract

The biogeography of pungency in three species of wild chili in the chaco and surrounding highland habitats of southeastern Bolivia is described. We report that Capsicum chacoense, C. baccatum, and C. eximium are polymorphic for production of capsaicin and its analogs, such that completely pungent and completely nonpungent individuals co-occur in some populations. In C. chacoense, the density of plants and the proportion of pungent plants increased with elevation. Above 900 m, all individuals in all populations except two were pungent; nonpungent individuals in at least one of the two polymorphic populations were likely a result of spreading by humans. The occurrence of pungent and nonpungent individuals in three species of ancestral Capsicum and the geographic variation of pungency within species suggest that production of capsaicin and its analogs entails both costs and benefits, which shift from one locality to another. Determining the selection pressures behind such shifts is necessary to understand the evolution of pungency in chilies.

Why are not all chilies hot? A trade-off limits pungency

“…In addition, these populations vary in the degree of pungency among pungent plants [25]. We have examined variation in pungency and the polymorphism for pungency in 21 populations along a 300 km transect in southeastern Bolivia that co-occurs with a gradient in moisture (figure 1a).…”

“…We have examined variation in pungency and the polymorphism for pungency in 21 populations along a 300 km transect in southeastern Bolivia that co-occurs with a gradient in moisture (figure 1a). In the dry northeast, populations are 15-20% pungent and the percentage of pungent plants increases towards the wetter southwest, where populations are 100 per cent pungent (in 7 census years, we have not located a non-pungent chili in these populations; figure 1a and [25] Generalized Linear Mixed Models with binomial error distribution using R [30]. All models included location as a random effect.…”

“…Model fits were estimated using maximum likelihood (ML) with a logit-link function. Pungency was determined by tasting in the field and verified by high-performance liquid chromatography as in Tewksbury et al [25].…”

“…(b) Field sampling and growing conditions We selected three polymorphic populations that span the range in rainfall, pungency (per cent of population pungent) and plant density found in polymorphic C. chacoense populations ( [25] and figure 1b; electronic supplementary material, table S1). We collected fruits from pungent and non-pungent plants in each population, and seeds from these fruits were grown in the University of Washington glasshouse.…”

“…Pungency in wild chilies has a simple genetic basis [23] and is expressed only in the fruit, where it acts to protect seeds [24], thereby providing the direct link to changes in fitness that is often missing from studies of chemical defence and herbivory [22]. Pungency is also polymorphic in some wild chili species, and multiple polymorphic populations have been identified along natural environmental gradients [24,25]. These attributes make the wild chili pepper an excellent system in which to investigate adaptive constraints.…”