Abstract
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 = 0.003), thereby reducing gas exchange under WS conditions. These results demonstrate the importance of trait integration in constraining adaptive divergence among populations.
References
- 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 (doi:10.1086/421412). Crossref, PubMed, ISI, Google Scholar - 2
Conner J. K. . 2002 Genetic mechanisms of floral trait correlations in a natural population. Nature 420, 407–410.doi:10.1038/nature01105 (doi:10.1038/nature01105). Crossref, PubMed, ISI, Google Scholar - 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 (doi:10.1007/s10709-004-2731-y). Crossref, PubMed, ISI, Google Scholar - 4
Schluter D. . 2009 Evidence for ecological speciation and its alternative. Science 323, 737–741.doi:10.1126/science.1160006 (doi:10.1126/science.1160006). Crossref, PubMed, ISI, Google Scholar - 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 (doi:10.1126/science.1133479). Crossref, PubMed, ISI, Google Scholar - 6
Hereford J. . 2009 A quantitative survey of local adaptation and fitness trade-offs. Am. Nat. 173, 579–588.doi:10.1086/597611 (doi:10.1086/597611). Crossref, PubMed, ISI, Google Scholar - 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 (doi:10.1146/annurev.es.19.110188.001231). Crossref, Google Scholar - 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. Crossref, Google Scholar - 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 (doi:10.1111/j.0014-3820.2005.tb01817.x). Crossref, PubMed, ISI, Google Scholar - 10
Levins R. . 1968 Evolution in changing environments. Princeton, NJ: Princeton University Press. Crossref, Google Scholar - 11
Hedrick P. W. . 1976 Genetic variation in a heterogeneous environment. II. Temporal heterogeneity and directional selection. Genetics 84, 145–157. Crossref, PubMed, ISI, Google Scholar - 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 (doi:10.1111/j.1558-5646.2007.00139.x). Crossref, PubMed, ISI, Google Scholar - 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 (doi:10.1073/pnas.0702117104). Crossref, PubMed, ISI, Google Scholar - 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 (doi:10.1098/rstb.2005.1667). Link, ISI, Google Scholar - 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 (doi:10.1098/rspb.2006.3498). Link, ISI, Google Scholar - 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 (doi:10.1146/annurev.ge.10.120176.001345). Crossref, PubMed, ISI, Google Scholar - 17
Stamp N. . 2003 Out of the quagmire of plant defense hypotheses. Q. Rev. Biol. 78, 23–55.doi:10.1086/367580 (doi:10.1086/367580). Crossref, PubMed, ISI, Google Scholar - 18
Koricheva J., Nykanen H.& Gianoli E. . 2004 Meta-analysis 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 (doi:10.1086/382601). Crossref, ISI, Google Scholar - 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 (doi:10.2307/3546166). Crossref, ISI, Google Scholar - 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 (doi:10.1038/nature04878). Crossref, PubMed, ISI, Google Scholar - 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 (doi:10.1073/pnas.95.23.13743). Crossref, ISI, Google Scholar - 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 (doi:10.1016/S0169-5347(02)02483-7). Crossref, ISI, Google Scholar - 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 (doi:10.1038/hdy.2009.131). Crossref, PubMed, ISI, Google Scholar - 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 (doi:10.1073/pnas.0802691105). Crossref, ISI, Google Scholar - 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 (doi:10.1007/s10886-005-9017-4). Crossref, PubMed, ISI, Google Scholar - 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 (doi:10.1016/S0167-4501(98)80014-9). Crossref, Google Scholar - 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 (doi:10.1086/323273). Crossref, ISI, Google Scholar - 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 (doi:10.1007/s00442-006-0496-y). Crossref, PubMed, ISI, Google Scholar - 29
Tewksbury J. J.& Nabhan G. P. . 2001 Seed dispersal: directed deterrence by capsaicin in chilies. Nature 412, 403–404.doi:10.1038/35086653 (doi:10.1038/35086653). Crossref, PubMed, ISI, Google Scholar - 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. Google Scholar
- 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 (doi:10.1016/S0304-4238(99)00017-5). Crossref, ISI, Google Scholar - 32
Venables W. N.& Ripley B. D. . 2002 Modern applied statistics with S, 4th edn. New York, NY: Springer. Crossref, Google Scholar - 33
Galmés J., 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 (doi:10.1111/j.1365-3040.2010.02239.x). Crossref, PubMed, ISI, Google Scholar - 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.). Crossref, Google Scholar - 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 (doi:10.1038/nature01843). Crossref, PubMed, ISI, Google Scholar - 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 (doi:10.1890/06-0064). Crossref, PubMed, ISI, Google Scholar - 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 (doi:10.1046/j.1365-294X.2003.01833.x). Crossref, PubMed, ISI, Google Scholar - 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 (doi:10.1371/journal.pbio.0060308). Crossref, ISI, Google Scholar - 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 (doi:10.1111/j.1365-294X.2007.03499.x). Crossref, PubMed, ISI, Google Scholar - 40
Arnold S. J. . 1992 Constraints on phenotypic evolution. Am. Nat. 140, S85–S107.doi:10.1086/285398 (doi:10.1086/285398). Crossref, PubMed, ISI, Google Scholar - 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 (doi:10.1098/rspb.1991.0118). Link, ISI, Google Scholar