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.

Fig. 1.

Fitness impacts and mechanics of fungal infection. (A) Seed survival (proportion of seeds germinating or still viable at end of germination trials ± 1 SE) as a function of Fusarium infection score (survival = 0.53^{−0.31 × fungal score}, r² = 0.97, P < 0.0005; n = 3414 seeds). Fusarium seed infection was scored from 0 (no infection) to 10 (uniformly black on both sides of the seed) using the seed standard pictured above the abscissa. (B) Acroleucus coxalis (Stäl) (Lygaeidae) nymph, the most common hemipteran foraging on chilies, piercing a chili fruit. (C) Ripe fruit with fungal infection spreading under surface of fruit at holes (hemipteran foraging scars). (D) Mean infection score on seeds in mature fruit as a function of hemipteran foraging scars on each fruit. Open symbols = nonpungent fruits; dark red symbols = pungent fruits. Regression forced through the origin (nonpungent F_1,26 = 29, B = 0.075, P < 0.001; pungent F_1,35 = 80, B = 0.041, P < 0.001).

Fig. 2.

Effects of capsaicinoids on Fusarium infection. (A) Seed infection scores (mean ± 1 SE) in fruit from nonpungent (white) and pungent (red) plants (n = 10 pungent and 10 nonpungent per year). On each plant we evaluated five random fruits each year. Seed infection scores were assigned using the standard series shown in Fig. 1A. (B) Relative growth rate of Fusarium as a function of capsaicin (circles, solid line) and dihydrocapsaicin (squares, dashed line) concentrations. All experiments were conducted in media that mimicked the nutritional composition of wild chili fruits. Growth was measured relative to growth in a control media that lacked capsaicinoids (± 1 SE, four isolates, six replicates per isolate per treatment). Lines are quadratic functions of capsaicinoid concentration (r² > 0.99, P < 0.0005). Mean capsaicin and dihydrocapsaicin concentrations in fruit at our primary study, where we assessed fungal loads, were 2.85 mg/g dry mass (solid up arrow), and 1.43 mg/g dry mass (dashed down arrow), respectively.

Fig. 3.

Heteropteran foraging, fungal pressure, and capsaicinoid production. (A) Locations of the seven populations in which we examined the relationship between hemipteran foraging frequency and fruit chemistry. (B) Hemipteran foraging frequency on chili fruits, an index of fusarium infection pressure, is a strong nonlinear predictor of the proportion of plants producing capsaicinoids (y = alnx + b, r² = 0.91, F_1,5 = 39, P = 0.0008).