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

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1735, 2012, Pages 2012-2017

  Haak, David C ^a   McGinnis, Leslie A ^a   Levey, Douglas J ^b   Tewksbury, Joshua J ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Capsaicin; Capsaicinoids; Defence; Genetic correlation; Natural selection; Secondary compounds

Indexed keywords

DIVERGENCE; DROUGHT STRESS; EVOLUTIONARY BIOLOGY; FRUIT; GAS EXCHANGE; GENETIC ANALYSIS; HETEROGENEITY; LIFE HISTORY TRAIT; MOISTURE CONTENT; NATIVE SPECIES; NATURAL SELECTION; POLYMORPHISM; TRADE-OFF; WATER USE EFFICIENCY;

BOLIVIA;

CAPSICUM CHACOENSE; FUNGI;

EID: 84859414422     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.2091     Document Type: Article

References (41)

1. Ghalambor, C. K., Reznick, D. N. & Walker, J. A. 2004 Constraints on adaptive evolution: the functional trade-off between reproduction and fast-start swimming performance in the Trinidadian guppy (Poecilia reticulata). Am. Nat. 164, 38-50. (doi:10.1086/421412)
2. Conner, J. K. 2002 Genetic mechanisms of floral trait correlations in a natural population. Nature 420, 407-410. (doi:10.1038/nature01105)
3. Via, S. & Hawthorne, D. J. 2005 Back to the future: genetic correlations, adaptation and speciation. Genetica 123, 147-156. (doi:10.1007/s10709-004-2731-y)
4. Schluter, D. 2009 Evidence for ecological speciation and its alternative. Science 323, 737-741. (doi:10.1126/science.1160006)
5. Miller, S. P., Lunzer, M. & Dean, A. M. 2006 Direct demonstration of an adaptive constraint. Science 314, 458-461. (doi:10.1126/science.1133479)
6. Hereford, J. 2009 A quantitative survey of local adaptation and fitness trade-offs. Am. Nat. 173, 579-588. (doi:10.1086/597611)
7. Futuyma, D. J. & Moreno, G. 1988 The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19, 207-233. (doi:10.1146/annurev.es.19.110188.001231)
8. Darwin, C. 1859 On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. New York, NY: D. Appleton.
9. Angert, A. L. & Schemske, D. W. 2005 The evolution of species' distributions: reciprocal transplants across the elevation ranges of Mimulus cardinalis and M. lewisii. Evolution 59, 1671-1684. (doi:10.1111/j.0014-3820. 2005.tb01817.x)
10. Levins, R. 1968 Evolution in changing environments. Princeton, NJ: Princeton University Press.
11. Hedrick, P. W. 1976 Genetic variation in a heterogeneous environment. II. Temporal heterogeneity and directional selection. Genetics 84, 145-157.
12. Hughes, B. S., Cullum, A. J., Bennett, A.F. &Travisano, M. 2007 Evolutionary adaptation to environmental pH in experimental lineages of Escherichia coli. Evolution 61, 1725-1734. (doi:10.1111/j.1558-5646.2007.00139.x)
13. Bennett, A. F. & Lenski, R. E. 2007 An experimental test of evolutionary trade-offs during temperature adaptation. Proc. Natl Acad. Sci. USA 104, 8649-8654. (doi:10. 1073/pnas.0702117104)
14. Johnson, T. & Barton, N. 2005 Theoretical models of selection and mutation on quantitative traits. Phil. Trans. R. Soc. B 360, 1411-1425. (doi:10.1098/rstb. 2005.1667)
15. Yeaman, S. & Jarvis, A. 2006 Regional heterogeneity and gene flow maintain variance in a quantitative trait within populations of lodgepole pine. Proc. R. Soc. B 273, 1587-1593. (doi:10.1098/rspb.2006.3498)
16. Felsenstein, J. 1976 The theoretical population genetics of variable selection and migration. Annu. Rev. Genet. 10, 253-280. (doi:10.1146/annurev.ge.10.120176.001345)
17. Stamp, N. 2003 Out of the quagmire of plant defense hypotheses. Q. Rev. Biol. 78, 23-55. (doi:10.1086/367580)
18. Koricheva, J., Nykanen, H. & Gianoli, E. 2004 Metaanalysis of trade-offs among plant antiherbivore defenses: are plants jacks-of-all-trades, masters of all? Am. Nat. 163, 64-75. (doi:10.1086/382601)
19. Mole, S. 1994 Trade-offs and constraints in plant-herbivore defense theory: a life-history perspective. Oikos 71, 3-12. (doi:10.2307/3546166)
20. Mitchell-Olds, T. & Schmitt, J. 2006 Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441, 947-952. (doi:10.1038/nature04878)
21. Berenbaum, M. R. & Zangerl, A. R. 1998 Chemical phenotype matching between a plant and its insect herbivore. Proc. Natl Acad. Sci. USA 95, 13 743-13 748. (doi:10.1073/pnas.95.23.13743)
22. Strauss, S. Y., Rudgers, J. A., Lau, J. A. & Irwin, R. E. 2002 Direct and ecological costs of resistance to herbivory. Trends Ecol. Evol. 17, 278-285. (doi:10.1016/S0169-5347(02)02483-7)
23. Stellari, G. M., Mazourek, M. & Jahn, M. M. 2009 Contrasting modes for loss of pungency between cultivated and wild species of Capsicum. Heredity 104, 460-471. (doi:10.1038/hdy.2009.131)
24. Tewksbury, J. J., Reagan, K. M., Machnicki, N. J., Carlo, T. A., Haak, D. C., Peñaloza, A. L. C. & Levey, D. J. 2008 Evolutionary ecology of pungency in wild chilies. Proc. Natl Acad. Sci. USA 105, 11 808-11 811. (doi:10. 1073/pnas.0802691105)
25. Tewksbury, J. J., Manchego, C., Haak, D. C. & Levey, D. J. 2006 Where did the chili get its spice? Biogeography of capsaicinoid production in ancestral wild chili species. J. Chem. Ecol. 32, 547-564. (doi:10.1007/s10886-005-9017-4)
26. Wall, M. M. & Bosland, P. W. 1998 Analytical methods for color and pungency of chiles (Capsicums). Dev. Food Sci. 39, 347-374. (doi:10.1016/S0167-4501 (98)80014-9)
27. Walsh, B. M. & 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. (doi:10.1086/323273)
28. Levey, D. J., Tewksbury, J. J., Cipollini, M. L. & Carlo, T. A. 2006 A field test of the directed deterrence hypothesis in two species of wild chili. Oecologia 150, 61-68. (doi:10.1007/s00442-006-0496-y)
29. Tewksbury, J. J. & Nabhan, G. P. 2001 Seed dispersal: directed deterrence by capsaicin in chilies. Nature 412, 403-404. (doi:10.1038/35086653)
30. R Development Core Team. 2011 R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0; http://www.R-project.org.
31. Jaimez, R. E., Rada, F. & Garcia-Nunez, C. 1999 The effect of irrigation frequency on water and carbon relations in three cultivars of sweet pepper (Capsicum chinense Jacq), in a tropical semiarid region. Scient. Horticult. 81, 301-308. (doi:10.1016/S0304-4238(99) 00017-5)
32. Venables, W. N. & Ripley, B. D. 2002 Modern applied statistics with S, 4th edn. New York, NY: Springer.
33. Galmés, J. et al. 2011 Physiological and morphological adaptations in relation to water use efficiency in Mediterranean accessions of Solanum lycopersicum. Plant Cell Environ. 34, 245-260. (doi:10.1111/j.1365-3040.2010. 02239.x)
34. Baba, M. Y., Maroto, J. V., San Bautista, A., Pascual, B., Lopez, S. & Baixauli, C. 2006 Agronomic response of sweet pepper (Capsicum annuum L.) to CO2 enrichment in greenhouses with static ventilation. Acta Hort. (ISHS), 719, 521-528. (See http://www.actahort.org/books/719/719_60.htm.)
35. Hetherington, A. M. & Woodward, F. I. 2003 The role of stomata in sensing and driving environmental change. Nature 424, 901-908. (doi:10.1038/nature01843)
36. Donaldson, J. R. & Lindroth, R. L. 2007 Genetics, environment, and their interaction determine efficacy of chemical defense in trembling aspen. Ecology 88, 729-739. (doi:10.1890/06-0064)
37. Mckay, J. K., Richards, J. H. & Mitchell-Olds, T. 2003 Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits. Mol. Ecol. 12, 1137-1151. (doi:10.1046/j.1365-294X.2003.01833.x)
38. Dilkes, B. P., Spielman, M., Weizbauer, R., Watson, B., Burkart-Waco, D., Scott, R. J. & Comai, L. 2008 The maternally expressed WRKY transcription factor TTG2 controls lethality in interploidy crosses of Arabidopsis. PLoS Biol. 6, e308. (doi:10.1371/journal. pbio.0060308)
39. Gardner, K. M. & Latta, R. G. 2007 Shared quantitative trait loci underlying the genetic correlation between continuous traits. Mol. Ecol. 16, 4195-4209. (doi:10.1111/j. 1365-294X.2007.03499.x)
40. Arnold, S. J. 1992 Constraints on phenotypic evolution. Am. Nat. 140, S85-S107. (doi:10.1086/285398)
41. Schluter, D., Price, T. D. & Rowe, L. 1991 Conflicting selection pressures and life history trade-offs. Proc. R. Soc. Lond. B 246, 11-17. (doi:10.1098/rspb. 1991.0118)