Skip to main content
Springer Nature Link
Log in

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

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Adler, L. S., Schmitt, J., and Bowers, M. D. 1995. Genetic variation in defensive chemistry in Plantago lanceolata (Plantaginaceae) and its effect on the specialist herbivore Junonia coenia (Nymphalidae). Oecologia 101:75–85.

    Article  Google Scholar 

  • Andrews, J. 1996. Peppers, the Domesticated Capsicums. UT Press, Austin, Utah.

    Google Scholar 

  • Baldwin, I. T. 1998. Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc. Natl. Acad. Sci. USA 95:8113–8118.

    Article  PubMed  CAS  Google Scholar 

  • Berenbaum, M. R. 1995. The chemistry of defense—theory and practice. Proc. Natl. Acad. Sci. USA 92:2–8.

    Article  PubMed  CAS  Google Scholar 

  • Berenbaum, M. R. and Feeny, P. 1981. Toxicity of angular furanocoumarins to swallowtail butterflies: escalation in a coevolutionary arms race? Science 212:927–929.

    Article  PubMed  CAS  Google Scholar 

  • Berenbaum, M. R. and Zangerl, A. R. 1998. Chemical phenotype matching between a plant and its insect herbivore. Proc. Natl. Acad. Sci. USA 95:13743–13748.

    Article  PubMed  CAS  Google Scholar 

  • Blum, E., Liu, K., Mazourek, M., Yoo, E. Y., Jahn, M., and Paran, I. 2002. Molecular mapping of the C locus for presence of pungency in Capsicum. Genome 45:702–705.

    Article  PubMed  CAS  Google Scholar 

  • Blum, E., Mazourek, M., O'Connell, M., Curry, J., Thorup, T., Liu, K. D., Jahn, M., and Paran, I. 2003. Molecular mapping of capsaicinoid biosynthesis genes and quantitative trait loci analysis for capsaicinoid content in Capsicum. Theor. Appl. Genet. 108:79–86.

    Article  PubMed  CAS  Google Scholar 

  • Bosland, P. W. 1994. Chiles—history, cultivation, and uses, pp. 347–366, in G. Charalambous (ed.). Spices, Herbs and Edible Fungi. Elsevier, Amsterdam.

    Google Scholar 

  • Cipollini, M. L. 2000. Secondary metabolites of vertebrate-dispersed fruits: evidence for adaptive functions. Rev. Chil. Hist. Nat. 73:421–440.

    Article  Google Scholar 

  • Cipollini, M. L. and Levey, D. J. 1997. Secondary metabolites of fleshy vertebrate-dispersed fruits: adaptive hypotheses and implications for seed dispersal. Am. Nat. 150:346–372.

    Article  PubMed  CAS  Google Scholar 

  • Cipollini, M. L., Paulk, E., and Cipollini, D. F. 2002. Effect of nitrogen and water treatment on leaf chemistry in horsenettle (Solanum carolinense), and relationship to herbivory by flea beetles (Epitrix spp.) and tobacco hornworm (Manduca sexta). J. Chem. Ecol. 28:2377–2398.

    Article  PubMed  CAS  Google Scholar 

  • Collins, M. D., Wasmund, L. M., and Bosland, P. W. 1995. Improved method for quantifying capsaicinoids in capsicum using high-performance liquid-chromatography. HortScience 30:137–139.

    CAS  Google Scholar 

  • Cordell, G. A. and Araujo, O. E. 1993. Capsaicin: identification, nomenclature, and pharmacotherapy. Ann. Pharmacother. 27:330–336.

    PubMed  CAS  Google Scholar 

  • Cronin, G. and Hay, M. E. 1996. Within plant variation in seaweed palatability and chemical defenses: optimal defense theory versus the growth differentiation balance hypothesis. Oecologia 105:361–368.

    Article  Google Scholar 

  • D'Arcy, W. G. and Eshbaugh, W. H. 1974. New world peppers (Capsicum–Solanaceae) north of Columbia: a resume. Baileya 19:93–105.

    Google Scholar 

  • DeWitt, D. and Bosland, P. W. 1996. Peppers of the World: An Identification Guide. Ten Speed Press, Berkeley.

    Google Scholar 

  • Eshbaugh, W. H. 1970. A biosystematic and evolutionary study of Capsicum baccatum (Solanaceae). Brittonia 22:31–43.

    Article  Google Scholar 

  • Eshbaugh, H. W. 1976. XXI. Genetic and biochemical systematic studies of chili peppers (Capsicum–Solanaceae). Bull. Torrey Bot. Club 102:396–403.

    Article  Google Scholar 

  • Eshbaugh, W. H., Smith, P. G., and Nickrent, D. L. 1983. Capsicum tovarii (Solanaceae), a new species of pepper from Peru. Brittonia 35:55–60.

    Article  Google Scholar 

  • Fornoni, J., Valverde, P. L., and Nunez-Farfan, J. 2004. Population variation in the cost and benefit of tolerance and resistance against herbivory in Datura stramonium. Evolution 58:1696–1704.

    PubMed  Google Scholar 

  • Fujiwake, H., Suzuki, T., and Iwai, K. 1982. Formation and metabolism of the pungent principle of capsicum fruits. 11. Capsaicinoid formation in the protoplast from the placenta of capsicum fruits. Agric. Biol. Chem. 46:2591–2592.

    CAS  Google Scholar 

  • Futuyma, D. J. 1998. Evolutionary Biology, 3rd ed. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Futuyma, D. J. and Mitter, C. 1996. Insect–plant interactions: the evolution of component communities. Proc. R. Soc. Biol. 351:1361–1366.

    Google Scholar 

  • Govindarajan, V. S. 1986. Capsicum—production, technology, chemistry, and quality. 3. Chemistry of the color, aroma, and pungency stimuli. Crit. Rev. Food Sci. Nutr. 24:245–355.

    PubMed  CAS  Google Scholar 

  • Govindarajan, V. S. and Sathyanarayana, M. N. 1991. Capsicum—production, technology, chemistry, and quality. 5. Impact on physiology, pharmacology, nutrition, and metabolism—structure, pungency, pain, and desensitization sequences. Crit. Rev. Food Sci. Nutr. 29:435–474.

    PubMed  CAS  Google Scholar 

  • Govindarajan, V. S., Rajalakshmi, D., and Chand, N. 1987. Capsicum—production, technology, chemistry, and quality. 4. Evaluation of quality. Crit. Rev. Food Sci. Nutr. 25: 185–282.

    Article  PubMed  CAS  Google Scholar 

  • Harvell, K. P. and Bosland, P. W. 1997. The environment produces a significant effect on pungency of chiles. HortScience 32:1292.

    Google Scholar 

  • Heiser, C. B. and Smith, P. V. 1958. New species of Capsicum from South America. Brittonia 10:194–201.

    Article  Google Scholar 

  • Iwai, K., Suzuki, T., and Fujiwake, H. 1979. Formation and accumulation of pungent principle of hot pepper fruits, capsaicin and its analogs, in Capsicum annuum var. annuum at different growth-stages after flowering. Agri. Biol. Chem. 43:2493–2498.

    CAS  Google Scholar 

  • Izhaki, I. 2002. Emodin—a secondary metabolite with multiple ecological functions in higher plants. New Phytol. 155:205–217.

    Article  CAS  Google Scholar 

  • Izhaki, I., Tsahar, E., Paluy, I., and Friedman, J. 2002. Within population variation and interrelationships between morphology, nutritional content, and secondary compounds of Rhamnus alaternus fruits. New Phytol. 156:217–223.

    Article  CAS  Google Scholar 

  • Jahn, A. E., Davis, S. E., and Saavedra Zankys, A. M. 2002. Patterns of austral bird migration in the Bolivian chaco. J. Field Ornithol. 73:258–267.

    Google Scholar 

  • Kawada, T., Watanabe, T., Katsura, K., Takami, H., and Iwai, K. 1985. Formation and metabolism of pungent principle of capsicum fruits. 15. Microdetermination of capsaicin by high-performance liquid-chromatography with electrochemical detection. J. Chromatogr. 329:99–105.

    Article  PubMed  CAS  Google Scholar 

  • Lerdau, M., Litvak, M., and Monson, R. 1994. Plant chemical defense—monoterpenes and the growth-differentiation balance hypothesis. Trends Ecol. Evol. 9:58–61.

    Article  Google Scholar 

  • McDonald, E. P., Agrell, J., and Lindroth, R. L. 1999. CO2 and light effects on deciduous trees: growth, foliar chemistry, and insect performance. Oecologia 119:389–399.

    Google Scholar 

  • McLeod, M. J., Guttman, S. I., and Eshbaugh, W. H. 1982. Early evolution of chile peppers (Capsicum). Econ. Bot. 36:361–386.

    Google Scholar 

  • McLeod, M. J., Guttman, S. I., Eshbaugh, W. H., and Rayle, R. E. 1983. An electrophoretic study of evolution in Capsicum (Solanaceae). Evolution 37:562–574.

    Article  CAS  Google Scholar 

  • Morton, C. V. 1938. Capsicum, in P. C. Standley (ed.). Flora of Costa Rica, University Microfilms.

  • Redman, A. M., Cipollini, D. F., and Schultz, J. C. 2001. Fitness costs of jasmonic acid-induced defense in tomato, Lycopersicon esculentum. Oecologia 126:380–385.

    Article  Google Scholar 

  • Ribera, M. O., Libermann, M., Beck, S., and Moraes, M. 1994. Mapa de la vegetacion y areas protegidea de Bolivia. 1:1,500,000. Centro de investigaciones y manejo de recursos naturales (CIMAR) and Universidad Autónoma Gabriel Rene Moreno (UAGRM), La Paz, Bolivia.

  • Rice, W. R. 1989. Analyzing tables of statistical tests. Evolution 43:223–225.

    Article  Google Scholar 

  • Rowell, K. and Blinn, D. W. 2003. Herbivory on a chemically defended plant as a predation deterrent in Hyalella azteca. Freshw. Biol. 48:247–254.

    Article  Google Scholar 

  • Schemske, D. W. and Bradshaw, H. D. 1999. Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc. Natl. Acad. Sci. USA 96:11910–11915.

    Article  PubMed  CAS  Google Scholar 

  • Schmitt, T. M., Hay, M. E., and Lindquist, N. 1995. Constraints on chemically mediated coevolution—multiple functions for seaweed secondary metabolites. Ecology 76:107–123.

    Article  Google Scholar 

  • Scoville, W. L. 1912. Note on capsicum. J. Am. Pharm. Assoc. 1:453.

    CAS  Google Scholar 

  • Siepielski, A. M. and Benkman, C. W. 2004. Interactions among moths, crossbills, squirrels, and lodgepole pine in a geographic selection mosaic. Evolution 58:95–101.

    PubMed  Google Scholar 

  • Stebbens, G. L. 1972. Ecological distribution of centers of major adaptive radiations in angiosperms, pp. 7–34, in D. H. Valentine (ed.). Taxonomy, Phytogeography, and Evolution. Academic Press, New York.

    Google Scholar 

  • Stebbens, G. L. and Major, J. 1965. Endemism and speciation in the California flora. Ecol. Monogr. 35:1–35.

    Article  Google Scholar 

  • Stewart, C. Jr., Kang, B. C., Kede, L., Mazourek, M., Moore, S. L., Yoo, E. Y., Kim, B. D., Paran, I., and Jahn, M. M. 2005. The Pun1 gene for pungency in pepper encodes a putative acyltransferase. Plant J. 42:675–688.

    Article  PubMed  CAS  Google Scholar 

  • Suzuki, T. and Iwai, K. 1984. Constituents of red pepper species: chemistry, biochemistry, pharmacology, and food science of the pungent principle of capsicum species, pp. 227–299, in A. Brossi (ed.). The Alkaloids: Chemistry and Pharmacology. Academic Press, San Diego.

    Google Scholar 

  • Suzuki, T., Fujiwake, H., and Iwai, K. 1980. Formation and metabolism of pungent principle of capsicum fruits. 5. Intracellular localization of capsaicin and its analogs, capsaicinoid, in capsicum fruit. 1. Microscopic investigation of the structure of the placenta of Capsicum annuum var. annuum. Plant Cell Physiol. 21:839–853.

    CAS  Google Scholar 

  • Tewksbury, J. J. 2002. Fruits, frugivores and the evolutionary arms race. New Phytol. 156:137–139.

    Article  Google Scholar 

  • Tewksbury, J. J. and Nabhan, G. P. 2001. Directed deterrence by capsaicin in chillies. Nature 412:403–404.

    Article  PubMed  CAS  Google Scholar 

  • Tewksbury, J. J., Nabhan, G. P., Norman, D., Susan, H., Tuxill, J., and Donovan, J. 1999. In situ conservation of wild chiles and their biotic associates. Conserv. Biol. 13:98–107.

    Article  Google Scholar 

  • Thompson, J. N. and Cunningham, B. M. 2002. Geographic structure and dynamics of coevolutionary selection. Nature 417:735–738.

    Article  PubMed  CAS  Google Scholar 

  • Tong, N. and Bosland, P. W. 1999. Capsicum tovarii, a new member of the Capsicum baccatum complex. Euphytica 109:71–77.

    Article  Google Scholar 

  • Tsahar, E., Friedman, J., and Izhaki, I. 2002. Impact on fruit removal and seed predation of a secondary metabolite, emodin, in Rhamnus alaternus fruit pulp. Oikos 99:290–299.

    Article  Google Scholar 

  • Tsahar, E., Friedman, J., and Izhaki, I. 2003. Secondary metabolite emodin increases food assimilation efficiency of yellow-vented bulbuls (Pycnonotus xanthopygos). Auk 120:411–417.

    Article  Google Scholar 

  • Walsh, B. M. and Hoot, S. B. 2001. Phylogenetic relationships of Capsicum (Solanaceae) using DNA sequences from two noncoding regions: the chloroplast atpB–rbcL spacer region and nuclear waxy introns. Int. J. Plant Sci. 162:1409–1418.

    Article  CAS  Google Scholar 

  • Zangerl, A. R., Arntz, A. M., and Berenbaum, M. R. 1997. Physiological price of an induced chemical defense: photosynthesis, respiration, biosynthesis, and growth. Oecologia 109:433–441.

    Article  Google Scholar 

Download references

Acknowledgments

This research was made possible through grants from the National Science Foundation (DEB-0129168) and the National Geographic Society Committee for Research and Exploration (7190-02). We thank Paul Martin, Robert Dobbs, Ian Horn, Meribeth Huzinga, Alex Jahn, Uco Sapag, and Don Odon for assistance in the field. We thank Damian Rumiz, Andy Noss, and Natalia Araujo, as well as WCS Bolivia, Fundación Amigos de la Naturaleza, and Museo de Historia Natural “Noel Kempf Mercado” for logistic support. We thank two anonymous reviewers for helpful critiques of early versions of this manuscript.

Author information

Authors and Affiliations

  1. Department of Biology, University of Washington, Box 351800, Seattle, WA, 98195, USA

    Joshua J. Tewksbury & David C. Haak

  2. Departamento de Geografia e Informatica, Museo Noel Kempff Mercado (U.A.G.R.M.), Santa Cruz, Bolivia

    Carlos Manchego

  3. Department of Zoology, University of Florida, PO 118525, Gainesville, FL, 32611-8525, USA

    Douglas J. Levey

Authors
  1. Joshua J. Tewksbury
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Carlos Manchego
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. David C. Haak
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Douglas J. Levey
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Joshua J. Tewksbury.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tewksbury, J.J., Manchego, C., Haak, D.C. et al. Where did the Chili Get its Spice? Biogeography of Capsaicinoid Production in Ancestral Wild Chili Species. J Chem Ecol 32, 547–564 (2006). https://doi.org/10.1007/s10886-005-9017-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-005-9017-4

Key Words

pFad - Phonifier reborn

Pfad - The Proxy pFad of © 2024 Garber Painting. All rights reserved.

Note: This service is not intended for secure transactions such as banking, social media, email, or purchasing. Use at your own risk. We assume no liability whatsoever for broken pages.


Alternative Proxies:

Alternative Proxy

pFad Proxy

pFad v3 Proxy

pFad v4 Proxy