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Natural selection on cork oak: allele frequency reveals divergent selection in cork oak populations along a temperature cline

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Abstract

A recent study of population divergence at neutral markers and adaptive traits in cork oak has observed an association between genetic distances at locus QpZAG46 and genetic distances for leaf size and growth. In that study it was proposed that certain loci could be linked to genes encoding for adaptive traits in cork oak and, thus, could be used in adaptation studies. In order to investigate this hypothesis, here we (1) looked for associations between molecular markers and a set of adaptive traits in cork oak, and (2) explored the effects of the climate on among-population patterns in adaptive traits and molecular markers. For this purpose, we chose 9-year-old plants originating from thirteen populations spanning a broad range of climatic conditions. Plants established in a common garden site were genotyped at six nuclear microsatellites and phenotypically characterized for six functional traits potentially related to plant performance. Our results supported the proposed linkage between locus QpZAG46 and genes encoding for leaf size and growth. Temperature caused adaptive population divergence in leaf size and growth, which was expressed as differences in the frequencies of the alleles at locus QpZAG46.

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References

  • Aranda I, Castro L, Alía R, Pardos JA, Gil L (2005) Low temperature during winter elicits differential responses among populations of the Mediterranean evergreen cork oak (Quercus suber). Tree Physiol 25:1085–1090

    CAS  PubMed  Google Scholar 

  • Aranda I, Pardos M, Puértolas J, Jiménez MD, Pardos JA (2007) Water use efficiency in cork oak (Quercus suber L.) is modified by the interaction of water and light availabilities. Tree Physiol 27:671–677

    PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc 57:289–300

    Google Scholar 

  • Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155

    Article  Google Scholar 

  • Brendel O, Le Thiec D, Scotti-Saintagne C, Kremer A, Guehl JM (2008) Quantitative trait loci controlling water use efficiency and related traits in Quercus robur L. Tree Genet Genom 4:263–278

    Article  Google Scholar 

  • Burgarella C, Lorenzo Z, Jabbour-Zahab R, Lumaret R, Guichoux E, Petit RJ, Soto A, Gil L (2009) Detection of hybrids in nature: application to oaks (Quercus suber and Q.ilex). Heredity 102:442–452

    Article  CAS  PubMed  Google Scholar 

  • Casper BB, Forseth IN, Wait DA (2005) Variation in carbon isotope discrimination in relation to plant performance in a natural population of Cryptantha flava. Oecologia 145:541–548

    Article  Google Scholar 

  • Cobb N, Mitton JB, Whitham TG (1994) Genetic variation associated with chronic water and nutrient stress in pinyon pine. Am J Bot 81:936–940

    Article  Google Scholar 

  • Davis MB, Shaw RG (2001) Range shifts and adaptive responses to quaternary climate change. Science 292:673–679

    Article  CAS  PubMed  Google Scholar 

  • Davis MB, Zabinski C (1992) Changes in geographical range resulting from greenhouse warming effects on biodiversity in forests. In: Peters RL, Lovejoy TL (eds) Global warming and biological diversity. Yale University Press, New Haven, pp 298–308

    Google Scholar 

  • Díaz-Fernández PM, Jiménez P, Catalán G, Martín S, Gil L (1995) Regiones de procedencia de Quercus suber L. ICONA, Madrid 49 p

    Google Scholar 

  • Donovan LA, Dudley SA, Rosenthal DM, Ludwig F (2007) Phenotypic selection on leaf water use efficiency and related ecophysiological traits for natural populations of desert sunflowers. Oecologia 152:13–25

    Article  PubMed  Google Scholar 

  • Doyle J, Doyle J (1990) Isolation of plant DNA from fresh tissue. Focus 13:13–15

    Google Scholar 

  • Dudley SA (1996) Differing selection on plant physiological traits in response to environmental water availability: a test of adaptive hypotheses. Evolution 50:92–102

    Article  Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Longman, Essex

    Google Scholar 

  • Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust J Plant Physiol 11:539–552

    Article  CAS  Google Scholar 

  • Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 1:121–137

    Article  Google Scholar 

  • Gandour M, Khouja ML, Toumi L, Triki S (2007) Morphological evaluation of cork oak (Quercus suber): Mediterranean provenance variability in Tunisia. Ann Forest Sci 64:549–555

    Article  Google Scholar 

  • García LV (2004) Escaping the Bonferroni iron claw in ecological studies. Oikos 105:657–663

    Article  Google Scholar 

  • Gonzalez-Martinez SC, Wheeler NC, Ersoz E, Nelson CD, Neale DB (2007) Association genetics in Pinus taeda L. I. Wood property traits. Genetics 175:399–409

    Article  PubMed  Google Scholar 

  • González-Martínez SC, Huber D, Ersoz E, Davis JM, Neale DB (2008) Association genetics in Pinus taeda L. II. Carbon isotope discrimination. Heredity 101:19–26

    Article  PubMed  Google Scholar 

  • Hamrick JL, Allard RW (1972) Microgeographical variation in allozyme frequencies in Avena barbata. Proc Natl Acad Sci USA 69:2100–2104

    Article  CAS  PubMed  Google Scholar 

  • Hamrick JL, Holden LR (1979) Influence of microhabitat heterogeneity on gene frequency distribution and gametic phase disequilibrium in Avena barbata. Evolution 33:521–533

    Article  Google Scholar 

  • Higgins PAT, Harte J (2006) Biophysical and biogeochemical responses to climate change depend on dispersal and migration. Bioscience 56:407–417

    Article  Google Scholar 

  • Hirschhorn JN, Daly MJ (2005) Genome-wide association studies for common diseases and complex traits. Nat Rev Genet 6:95–108

    Article  CAS  PubMed  Google Scholar 

  • Huestis DL, Marshall JL (2006) Is natural selection a plausible explanation for the distribution of Idh-1 alleles in the cricket Allonemobius socius? Ecol Entomol 41:91–98

    Article  Google Scholar 

  • IPCC (2007) Climate change 2007: the physical basis. contribution of working group i to the fourth assessment of the intergovernmental panel on climate change. IPCC Secretariat, Geneva, Switzerland

  • Jiménez P, Agundez D, Alia R, Gil L (1999) Genetic variation in central and marginal populations of Quercus suber L. Silvae Genet 48:278–284

    Google Scholar 

  • Jump AS, Hunt JM, Martinez-Izquierdo JA, Peñuelas J (2006) Natural selection and climate change: Temperature-linked spatial and temporal trends in gene frequency in Fagus sylvatica. Mol Ecol 15:3469–3480

    Article  CAS  PubMed  Google Scholar 

  • Kampfer S, Lexer C, Glössl J, Steinkellner H (1998) Characterization of (GA)n microsatellite loci from Quercus robur. Hereditas 129:183–186

    Article  CAS  Google Scholar 

  • Kawecki TJ, Ebert T (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

    Article  Google Scholar 

  • Kelly CK, Chase MW, de Bruijn A, Fay MF, Woodward FI (2003) Temperature-based population segregation in birch. Ecol Lett 6:87–89

    Article  Google Scholar 

  • Li YC, Fahima T, Beiles A, Korol AB, Nevo E (1999) Microclimatic stress and adaptive DNA differentiation in wild emmer wheat, Triticum dicoccoides. Theor Appl Genet 98:873–883

    Article  CAS  Google Scholar 

  • Li YC, Fahima T, Krugman T, Krugman T, Beiles A, Röder MS, Korol AB, Nevo E (2000) Parallel microgeographic patterns of genetic diversity and divergence revealed by allozyme, RAPD, and microsatellites in Triticum dicoccoides at Ammiad, Israel. Conserv Genet 1:191–207

    Article  CAS  Google Scholar 

  • Marchini J, Cardon LR, Phillips MS, Donnelly P (2004) The effects of human population structure on large genetic association studies. Nat Genet 36:512–517

    Article  CAS  PubMed  Google Scholar 

  • Mitton JB (1997) Selection in natural populations. Oxford University Press, New York

    Google Scholar 

  • Mitton JB, Duran KL (2004) Genetic variation in pinyon pine, Pinus edulis, associated with summer precipitation. Mol Ecol 13:1259–1264

    Article  CAS  PubMed  Google Scholar 

  • Mitton JB, Stutz HP, Schuster WSF, Shea KL (1989) Genotypic differentiation at PGM in Engelmann spruce from wet and dry sites. Silvae Genet 38:217–221

    Google Scholar 

  • Mitton JB, Grant MC, Yoshino AM (1998) Variation in allozymes and stomatal size in pinyon (Pinus edulis, Pinaceae), associated with soil moisture. Am J Bot 85:1262–1265

    Article  Google Scholar 

  • Mullen LM, Hoekstra HE (2008) Natural selection along an environmental gradient: a classic cline in mouse pigmentation. Evolution 62–7:1555–1570

    Article  Google Scholar 

  • Owuor ED, Fahima T, Beiles A, Korol A, Nevo E (1997) Population genetic response to microsite ecological stress in wild barley, Hordeum spontaneum. Mol Ecol 6:1177–1187

    Article  Google Scholar 

  • Owuor ED, Beharav A, Fahima T, Krzhner VM, Korol AB, Nevo E (2003) Microscale ecological stress causes RAPD molecular selection in wild barley, Neve Yaar microsite, Israel. Genetic Resour Crop Evol 50:213–223

    Article  CAS  Google Scholar 

  • Ramírez-Valiente JA, Valladares F, Gil L, Aranda I (2009a) Population differences in juvenile survival under increasing drought are mediated by seed size in cork oak (Quercus suber L.). Forest Ecol Manag 257:1676–1683

    Article  Google Scholar 

  • Ramírez-Valiente JA, Lorenzo Z, Soto A, Valladares F, Gil L, Aranda I (2009b) Elucidating the role of genetic drift and natural selection in cork oak differentiation regarding drought tolerance. Mol Ecol 18:3803–3815

    Article  PubMed  Google Scholar 

  • Rank NE, Dahlhoff EP (2002) Allele frequency shifts in response to climate change and physiological consequences of allozyme variation in a montane insect. Evolution 56:2278–2289

    CAS  PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Reich PB, Waters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Natl Acad Sci USA 94:13730–13734

    Article  CAS  PubMed  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  Google Scholar 

  • Savolainen O, Hedrick P (1995) Heterozygosity and fitness: no association in Scots Pine. Genetics 140:755–766

    CAS  PubMed  Google Scholar 

  • Savolainen O, Pyhajarvi T, Knurr T (2007) Gene flow and local adaptation in trees. Annu Rev Ecol Evol Syst 38:595–619

    Article  Google Scholar 

  • Schmidt PS, Rand DM (2001) Adaptive maintenance of genetic polymorphism in an intertidal barnacle: habitat- and life-stage-specific survivorship of MPI genotypes. Evolution 55:1336–1344

    CAS  PubMed  Google Scholar 

  • Scotti-Saintagne C, Mariette S, Porth I, Goiecoechea PG, Barreneche T, Bodénès C, Burg K, Kremer A (2004) Genome scanning for interspecific differentiation between two closely related oak species (Quercus robur L. and Q. petraea (Matt.) Liebl.). Genetics 168:1615–1626

    Article  CAS  PubMed  Google Scholar 

  • Soto A, Lorenzo Z, Gil L (2003) Nuclear microsatellite markers for the identification of Quercus ilex L. and Q. suber L. hybrids. Silvae Genet 52:63–66

    Google Scholar 

  • Soto A, Lorenzo Z, Gil L (2007) Differences in fine-scale genetic structure and dispersal in Quercus ilex L. and Q. suber L.: consequences for regeneration of mediterranean open woods. Heredity 99:601–607

    Article  CAS  PubMed  Google Scholar 

  • Steinkellner H, Fluch S, Turetschek E, Lexer C, Streiff R, Kremer A, Burg K, Glossl J (1997) Identification and characterization of (GA/CT)n-microsatellite loci from Quercus petraea. Plant Mol Biol 33:1093–1096

    Article  CAS  PubMed  Google Scholar 

  • Stutz HP, Mitton JB (1988) Genetic variation in Engelmann spruce associated with soil moisture. Arct Alp Res 20:461–465

    Article  Google Scholar 

  • Thumma BR, Nolan MR, Evans R, Moran GF (2005) Polymorphisms in cinnamoyl CoA reductase (CCR) are associated with variation in microfibril angle in Eucalyptus spp. Genetics 171:1257–1265

    Article  CAS  PubMed  Google Scholar 

  • Toumi L, Lumaret R (1998) Allozyme variation in cork oak (Quercus suber L.): the role of phylogeography and genetic introgression by other Mediterranean oak species and human activities. Theor Appl Genet 97:647–656

    Article  CAS  Google Scholar 

  • Valladares F, Wright SJ, Lasso E, Kitajima K, Pearcy RW (2000) Plastic phenotypic response to light of 16 congeneric shrubs from Panamanian rainforest. Ecology 81:1925–1936

    Article  Google Scholar 

  • Valladares F, Gianoli E, Gómez JM (2007) Ecological limits to plant phenotypic plasticity. New Phytol 146:749–763

    Article  Google Scholar 

  • Watt WB (1992) Eggs, enzymes, and evolution: natural genetic variants change insect fecundity. Proc Natl Acad Sci USA 89:10608–10612

    Article  CAS  PubMed  Google Scholar 

  • Watt WB, Carter PA, Blower SM (1985) Adaptation at specific loci. IV. Differential mating success among glycolytic allozyme genotypes of Colias butterflies. Genetics 109:157–175

    CAS  PubMed  Google Scholar 

  • White TL, Adams WT, Neale DB (2007) Forest genetics. CAB International, Wallingford, UK

    Chapter  Google Scholar 

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Acknowledgments

This study was funded by the Spanish Ministry of Environment and DGB (Convenio UPM-DGB), the Spanish Ministry of Science and Innovation (PLASTOFOR, AGL-00536/FOR and BOSALIM, CGL2007-66066-C04-02/CGL2007-66066-C04-03 projects and BES-2005-7573 fellowship). We thank Pedro Díaz-Fernández, Laura Castro, Regina Chambel, José María Climent, Pilar Jiménez and the rest of the people who collaborated in the setting up of the cork oak field common gardens under the EU concerted action on cork oak, FAIR I CT 95 0202. We thank to AEMET (Agencia estatal de Meteorología) for providing the climatic data. We thank Matthew Robson who made a thorough review of the English version and contributed with valuable suggestions. We thank Santiago de Blas, José Antonio Mancha and other field assistants for their help during the experiment. We are grateful to Salustiano Iglesias and DGB for the maintenance of the common gardens. Finally, we would like to thank to Santiago González-Martínez for his useful suggestions and comments on the final version of the manuscript.

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Correspondence to I. Aranda.

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Ramírez-Valiente, J.A., Lorenzo, Z., Soto, A. et al. Natural selection on cork oak: allele frequency reveals divergent selection in cork oak populations along a temperature cline. Evol Ecol 24, 1031–1044 (2010). https://doi.org/10.1007/s10682-010-9365-6

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