Evolutionary ecology of pungency in wild chilies

Abstract

The primary function of fruit is to attract animals that disperse viable seeds, but the nutritional rewards that attract beneficial consumers also attract consumers that kill seeds instead of dispersing them. Many of these unwanted consumers are microbes, and microbial defense is commonly invoked to explain the bitter, distasteful, occasionally toxic chemicals found in many ripe fruits. This explanation has been criticized, however, due to a lack of evidence that microbial consumers influence fruit chemistry in wild populations. In the present study, we use wild chilies to show that chemical defense of ripe fruit reflects variation in the risk of microbial attack. Capsaicinoids are the chemicals responsible for the well known pungency of chili fruits. Capsicum chacoense is naturally polymorphic for the production of capsaicinoids and displays geographic variation in the proportion of individual plants in a population that produce capsaicinoids. We show that this variation is directly linked to variation in the damage caused by a fungal pathogen of chili seeds. We find that Fusarium fungus is the primary cause of predispersal chili seed mortality, and we experimentally demonstrate that capsaicinoids protect chili seeds from Fusarium. Further, foraging by hemipteran insects facilitates the entry of Fusarium into fruits, and we show that variation in hemipteran foraging pressure among chili populations predicts the proportion of plants in a population producing capsaicinoids. These results suggest that the pungency in chilies may be an adaptive response to selection by a microbial pathogen, supporting the influence of microbial consumers on fruit chemistry. directed deterrence ͉ frugivory ͉ fruit chemistry ͉ secondary metabolite ͉ Capsicum chacoense T he evolution of fruit, a reward for animal dispersal of seeds, is a commonly cited example of a key innovation in the radiation of angiosperms (1-3). However, the nutritional qualities of fruit pulp that are responsible for attracting beneficial dispersers also attract consumers that are detrimental to plant fitness. These consumers range from vertebrate and invertebrate seed predators to microbial consumers of fruits and seeds that reduce the likelihood of dispersal and the viability of seeds (4). Fruit chemistry is commonly thought to mediate these interactions, either by deterring seed predators (4-6) or reducing microbial attack of fruits and seeds (4,7,8). These mechanisms are not mutually exclusive, but chemicals that deter fruit consumption often affect a wide range of species (7, 9), and defensive chemistry in ripe fruit must be sufficiently targeted toward detrimental organisms to allow consumption by vertebrate seed dispersers. Fruit secondary compounds that deter microbial consumers without reducing seed dispersal by vertebrates are thought to be far more plausible than secondary compounds that selectively deter vertebrate predators (7), because microbial fruit consumers are uniformly negative in their impacts on plant fitness (4) and are farther removed in...

Alkamid database: Chemistry, occurrence and functionality of plant N-alkylamides

“…The defensive properties of capsaicinoids and HCAAs were documented Tewksbury et al, 2008). Because four nitrogen possessing macrocyclic amides consume quite some energy for their biosynthesis, their importance in the plant physiology and role against endophytic or pathogenic fungi was postulated (Werner et al, 1997).…”

Phenology of tropical understory trees: patterns and correlates

“…Plants producing crops of different sizes are likely to attract different suites of seed dispersers (Gautier-Hion et al 1985, Wheelwright & Janson 1985, Foster 1990, Carlo et al 2003. Susceptibility to pathogen attack could reflect the degree to which fruits and seeds are chemically defended (Tewksbury et al 2008) which likely affects disperser identity and the relative benefits of different phenological patterns (Cipollini & Levey 1997). Phenological patterns at the species level may be constrained by their evolutionary history such that closely related species have similar phenologies despite divergence in current selective pressures.…”

GC-MS Profiling of Capsaicinoids Present in Capsicum chinense Jacq. cv. (Naga King Chilli) and Evaluation of its Antifungal Activity

“…The reason may be attributed to higher concentration of capsaicin (major component of capsaicinoids) which was found higher in dried chilli extract than in fresh chilli extract by UV spectrophotometric study. This is supported by fact that Fusarium fungus are the primary cause of pre-dispersal of chilli seed mortality and experimentally demonstrated that capsaicinoids protect chilli from the Fusarium [24]. Tewksbury et al [24] also demonstrated that more pungent chilli with higher concentration of capsaicinoids have more resistance to fungus than the chilli with lower concentration of capsaicinoids.…”

“…This is supported by fact that Fusarium fungus are the primary cause of pre-dispersal of chilli seed mortality and experimentally demonstrated that capsaicinoids protect chilli from the Fusarium [24]. Tewksbury et al [24] also demonstrated that more pungent chilli with higher concentration of capsaicinoids have more resistance to fungus than the chilli with lower concentration of capsaicinoids. Another factor responsible for less antifungal activity of fresh chilli extract may also be due to an antagonistic effect.…”