A field test of the directed deterrence hypothesis in two species of wild chili

Levey, Douglas J.; Tewksbury, Joshua J.; Cipollini, Martin L.; Carlo, Tomás A.

doi:10.1007/s00442-006-0496-y

Cited by 92 publications

(43 citation statements)

References 76 publications

(91 reference statements)

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“…2A). Nonpungent and pungent fruits are visually indistinguishable in the field, and their nutritional profiles are virtually identical (20). Nonetheless, the large difference in seed infection we observed between pungent and nonpungent plants could be because of a factor other than the presence or absence of capsaicinoids.…”

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confidence: 66%

“…We have studied this polymorphism most intensively in Capsicum chacoense Hunz., which is native to the Chaco region of Bolivia, Argentina, and Paraguay (19). In polymorphic populations, C. chacoense plants producing fruits that contain capsaicinoids grow alongside plants with fruits that are nutritionally similar (20) but completely lack capsaicinoids (18) [see supporting information (SI)]. In addition, the proportion of plants producing capsaicinoids varies widely among populations.…”

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confidence: 99%

“…If this reduction were caused by the presence of capsaicinoids in the pungent fruit, we should be able to generate a similar effect size in a more controlled experimental setting where capsaicinoid content is the sole independent variable. To test this we created artificial fruit media that mimicked the nutritional composition of C. chacoense fruit (20), differing only in the presence and concentration of the two primary capsaicinoids, capsaicin and dihydrocapsaicin. Inoculating these media with Fusarium isolates cultured from C. chacoense seeds from the same population showed that both capsaicin and dihydrocapsaicin cause strong dosedependent inhibition of Fusarium growth (Fig.…”

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Evolutionary ecology of pungency in wild chilies

Tewksbury

Reagan

Machnicki

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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159

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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...

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Evolutionary ecology of pungency in wild chilies

Tewksbury

Reagan

Machnicki

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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159

147

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“…Grasses grow well under the scant canopy of Prosopis, but not at all under Celtis, and harvester ants forage preferentially on grassy habitats (Whitford 1978). Mammalian seed predators can be excluded from the picture as mammals are deterred by the capsaicins that make chiltepins very hot (Tewksbury & Nabhan 2001;Levey et al 2006). Another alternative non-exclusive explanation for the reduced emergence of chiltepins under Prosopis is reduced by seed dormancy.…”

Section: Discussionmentioning

confidence: 99%

Directness and tempo of avian seed dispersal increases emergence of wild chiltepins in desert grasslands

Carlo

Tewksbury

2013

Journal of Ecology

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Summary1. Seed dispersal is thought to be unpredictable and outside a plant's control. But directed seed dispersal by mutualistic birds can increase probabilities of germination and survival by the non-random deposition of seeds in suitable microhabitats. 2. In the Sonoran Desert grasslands of southern Arizona (USA), bird-dispersed wild chiltepin peppers (Capscium annuum var. glabriusculum) grow in non-random association under bird-dispersed nurse trees and shrubs that serve as perches. We tested the hypothesis that the pattern is maintained by directional avian seed-dispersal patterns. Alternatively, post-dispersal processes, such as differential seed predation and seedling mortality, could create the associations. 3. For 3 years, we sampled the bird-generated seed rain under desert trees in four chiltepin subpopulations, comparing seed dispersal into microhabitats of fleshy-fruited trees and non-fleshy-fruited trees. Celtis pallida (fleshy-fruited) and Prosopis vellutina (non-fleshy-fruited) trees accounted for > 90% of the cover available for chiltepin recruitment. We tracked seedling emergence and survival in the two microhabitats and conducted a controlled seed-addition experiment to measure the effects of microhabitat, seed-addition density and temporal seed deposition on chiltepin emergence, growth and survival. 4. Approximately twice as many bird-dispersed seeds arrived at fleshy-fruited microhabitats compared with non-fleshy microhabitats. The numbers of seeds arriving and the number of seedlings emerging in microhabitats the following year were positively correlated. Survival of naturally emerged seedlings was similar at both microhabitats, but the seed-addition experiment revealed that more seeds are able to emerge under the denser foliage of fleshy-fruited microhabitats. The experiment also shows a significant effect of temporal deposition: when seeds were added gradually in a microhabitat (emulating repeated avian seed deposition under perches) instead of all at once, seedling emergence increased twofold on average. 5. Synthesis: Birds dispersed disproportionally high quantities of chiltepin seeds into favourable recruitment microhabitats, showing a case of directed dispersal. Birds also increase seedling emergence through the temporal deposition of seeds under fleshy-fruited trees, most likely as a result of reducing the odds of seed predation. A coupling between directed seed dispersal with classic facilitative plant-plant interactions leads to the formation of pattern and self-organization in a plant community.

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“…In particular, capsaicin appears to protect chili fruits and seeds from Fusarium attack. It also protects chili fruits from consumption by granivorous rodents without reducing consumption by seed-dispersing birds [28,29]. Given these well-documented benefits of capsaicin, we ask: is the observed polymorphism in wild chilies maintained by a cost of pungency?…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2011

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Evolutionary biologists increasingly recognize that evolution can be constrained by trade-offs, yet our understanding of how and when such constraints are manifested and whether they restrict adaptive divergence in populations remains limited. Here, we show that spatial heterogeneity in moisture maintains a polymorphism for pungency (heat) among natural populations of wild chilies (Capsicum chacoense) because traits influencing water-use efficiency are functionally integrated with traits controlling pungency (the production of capsaicinoids). Pungent and non-pungent chilies occur along a cline in moisture that spans their native range in Bolivia, and the proportion of pungent plants in populations increases with greater moisture availability. In high moisture environments, pungency is beneficial because capsaicinoids protect the fruit from pathogenic fungi, and is not costly because pungent and non-pungent chilies grown in well-watered conditions produce equal numbers of seeds. In low moisture environments, pungency is less beneficial as the risk of fungal infection is lower, and carries a significant cost because, under drought stress, seed production in pungent chilies is reduced by 50 per cent relative to non-pungent plants grown in identical conditions. This large difference in seed production under water-stressed (WS) conditions explains the existence of populations dominated by non-pungent plants, and appears to result from a genetic correlation between pungency and stomatal density: non-pungent plants, segregating from intra-population crosses, exhibit significantly lower stomatal density (p ¼ 0.003), thereby reducing gas exchange under WS conditions. These results demonstrate the importance of trait integration in constraining adaptive divergence among populations.

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A field test of the directed deterrence hypothesis in two species of wild chili

Cited by 92 publications

References 76 publications

Evolutionary ecology of pungency in wild chilies

Evolutionary ecology of pungency in wild chilies

Directness and tempo of avian seed dispersal increases emergence of wild chiltepins in desert grasslands

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

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