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Differentiation in phenological and physiological traits in European beech (Fagus sylvatica L.)

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Abstract

The knowledge of the extent of local adaptation is essential for forest reproductive material transfer, designing gene conservation programs and measures for mitigation of the ongoing climate change. A common methodology for assessing selection underlying local adaptation is the comparison of differentiation at neutral markers (measured by F ST) against quantitative traits (measured by Q ST). We investigated differentiation in phenology, height and diameter growth, and parameters of photosynthesis and water regime in a widespread European broadleaved tree, European beech (Fagus sylvatica L.). As the assessment of Q ST requires known pedigree structure of the tested populations, it was approximated by the coefficient of phenotypic differentiation P ST. For all phenology traits, especially budburst timing, there is a strong and reliable evidence of local adaptation as indicated by P ST > F ST. On the other hand, P ST was generally smaller than F ST for most growth and physiological traits, but the evidence for uniform selection or canalization acting at genes underlying these traits is generally absent or weak. Possible heritable basis of phenological differentiation is discussed, and implications for the current EU legislation on forest reproductive material are drawn.

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References

  • Aitken SN, Yeaman S, Holliday JA, Wang T, Curtis-McLane S (2008) Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol Appl 1:95–111

    Article  PubMed Central  PubMed  Google Scholar 

  • Akczell L, Turok J (2005) International legislation with implications on the exchange of forest genetic resources. In: Geburek T, Turok J (eds) Conservation and management of forest genetic resources in Europe. Arbora Publishers, Zvolen and IPGRI, pp 75–88

    Google Scholar 

  • Alberto FJ, Derory J, Boury C, Frigerio J-M, Zimmermann NC, Kremer A (2013) Imprints of natural selection along environmental gradients in phenology-related genes of Quercus petraea. Genetics 195:495–512

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Aranda I, Cano FJ, Gasco A, Cochard H, Nardini A, Mancha JA, Lopez R, Sanchez-Gomez D (2015) Variation in photosynthetic performance and hydraulic architecture across European beech (Fagus sylvatica L.) populations supports the case for local adaptation to water stress. Tree Phys 35:34–46

    Article  Google Scholar 

  • Barzdajn W (2008) Porównanie odziedziczalności proweniencyjnej, rodowej i indywidualnej cech wzrostowych dębu szypułkowego (Quercus robur L.) w doświadczeniu rodowo-proweniencyjnym w Nadleśnictwie Milicz. Sylwan 152:52–59

    Google Scholar 

  • Brommer JE (2011) Whither P ST ? The approximation of Q ST by P ST in evolutionary and conservation biology. J Evol Biol 24:1160–1168

    Article  CAS  PubMed  Google Scholar 

  • Bussotti F, Pollastrini M, Holland V, Bruggemann W (2015) Functional traits and adaptive capacity of European forests to climate change. Environ Exp Bot 111:91–113

    Article  Google Scholar 

  • Chambel MR, Climent J, Alía R, Valladares F (2005) Phenotypic plasticity: a useful framework for understanding adaptation in forest species. Invest Agrar Sist Recur For 14:334–344

    Article  Google Scholar 

  • Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  CAS  PubMed  Google Scholar 

  • Chmura DJ, Rożkowski R (2002) Variability of beech provenances in spring and autumn phenology. Silvae Genet 51:123–127

    Google Scholar 

  • Csilléry K, Lalagüe H, Vendramin GG, González-Martínez SC, Fady B, Oddou-Muratorio S (2014) Detecting short spatial scale local adaptation and epistatic selection in climate-related candidate genes in European beech (Fagus sylvatica) populations. Mol Ecol 23:4696–4708

    Article  PubMed  Google Scholar 

  • Derory J, Scotti-Saintagne C, Bertocchi E, Le Dantec L, Graignic N, Jauffres A, Casasoli M, Chancerel E, Bodénès C, Alberto F, Kremer A (2010) Contrasting relationships between the diversity of candidate genes and variation of bud burst in natural and segregating populations of European oaks. Heredity 104:438–448

    Article  CAS  PubMed  Google Scholar 

  • Dillon SK, Nolan MF, Matter P, Gapare WJ, Bragg JG, Southerton SG (2013) Signatures of adaptation and genetic structure among the mainland populations of Pinus radiata (D. Don) inferred from SNP loci. Tree Genet Genomes 9:1447–1463

    Article  Google Scholar 

  • Dormling I, Johnsen Ø (1992) Effects of the parental environment on full-sib families of Pinus sylvestris. Can J For Res 22:88–100

    Article  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Edelaar P, Burraco P, Gomez-Mestre I (2011) Comparisons between Q ST and F ST : how wrong have we been? Mol Ecol 20:4830–4839

    Article  PubMed  Google Scholar 

  • Eriksson G, Ekberg I, Dormling I, Matérn B, von Wettstein D (1978) Inheritance of bud-set and bud-flushing in Picea abies (L.) Karst. Theor Appl Genet 52:3–19

    Article  CAS  PubMed  Google Scholar 

  • European Communities (1999) Council Directive 1999/105/EC of 22 December 1999 on the marketing of forest reproductive material. Official Journal of the European Communities 15. 1. 2000 L 11/17–40

  • Gimeno TE, Pias B, Lemos JP, Valladares F (2009) Plasticity and stress tolerance override local adaptation in the responses of Mediterranean holm oak seedlings to drought and cold. Tree Physiol 29:87–98

    Article  PubMed  Google Scholar 

  • Gömöry D, Paule L (2011) Trade-off between height growth and spring flushing in common beech (Fagus sylvatica L.). Ann For Sci 68:975–984

    Article  Google Scholar 

  • Gömöry D, Paule L, Gömöryová E (2011) Effects of microsite variation on growth and adaptive traits in a beech provenance trial. J For Sci 57:192–199

    Google Scholar 

  • Gömöry D, Foffová E, Longauer R, Krajmerová D (2015) Memory effects associated with early-growth environment in Norway spruce and European larch. Eur J For Res 26:89–97

    Article  Google Scholar 

  • Hendry AP (2002) Q ST >=≠<F ST . Trends Ecol Evol 17:502

    Article  Google Scholar 

  • Hill WG, Goddard ME, Visscher PM (2008) Data and theory point to mainly additive genetic variance for complex traits. PLoS Genet 4:1–10

    Article  Google Scholar 

  • Howe GT, Aitken SN, Neale DB, Jermstad KD, Wheeler NC, Chen THH (2003) From genotype to phenotype: unraveling the complexities of cold adaptation in forest trees. Can J Bot 81:1247–1266

    Article  CAS  Google Scholar 

  • Johnsen Ø, Daehlen OG, Østreng G, Skrøppa T (2005) Daylength and temperature during seed production interactively affect adaptive performance of Picea abies progenies. New Phytol 168:589–596

    Article  PubMed  Google Scholar 

  • Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555

    Article  PubMed  Google Scholar 

  • König A (2005) Provenance research: evaluation of the spatial pattern of genetic variation. In: Geburek T, Turok J (eds) Conservation and management of forest genetic resources in Europe. Arbora Publishers, Zvolen and IPGRI, pp 275–334

    Google Scholar 

  • Kramer K, Buiteveld J, Forstreuter M, Geburek T, Leonardi S, Menozzi P, Povillon F, Schelhaas M, Teissier du Cros E, Vendramin GG, van der Werf DC (2008) Bridging the gap between ecophysiological and genetic knowledge to assess the adaptive potential of European beech. Ecol Model 216:333–353

  • Kreyling J, Buhk C, Backhaus S, Hallinger M, Huber G, Huber L, Jentsch A, Konnert M, Thiel D, Wilmking M, Beierkuhnlein C (2014) Local adaptations to frost in marginal and central populations of the dominant forest tree Fagus sylvatica L. as affected by temperature and extreme drought in common garden experiments. Ecol Evol 4:594–605

    Article  PubMed Central  PubMed  Google Scholar 

  • Lalagüe H, Csilléry K, Oddou-Muratorio S, Safrana J, de Quattro C, Fady B, González-Martínez SC, Vendramin GG (2014) Nucleotide diversity and linkage disequilibrium at 58 stress response and phenology candidate genes in a European beech (Fagus sylvatica L.) population from southeastern France. Tree Genet Genomes 10:15–26

    Article  Google Scholar 

  • Lamy J-B, Bouffier L, Burlett R, Plomion C, Cochard H, Delzon S (2011) Uniform selection as a primary force reducing population genetic differentiation of cavitation resistance across a species range. PLoS One 6:e23476

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lamy J-B, Plomion C, Kremer A, Delzon S (2012) Q ST  < F ST as a signature of canalization. Mol Ecol 21:5646–5655

    Article  PubMed  Google Scholar 

  • Le Corre V, Kremer A (2012) The genetic differentiation at quantitative trait loci under local adaptation. Mol Ecol 21:1548–1566

    Article  PubMed  Google Scholar 

  • Lefèvre S, Wagner S, Petit RJ, de Lafontaine G (2012) Multiplexed microsatellite markers for genetic studies of beech. Mol Ecol Res 12:484–491

    Article  Google Scholar 

  • Leinonen T, Cano JM, Mäkinen H, Merilä J (2006) Contrasting patterns of body shape and neutral genetic divergence in marine and lake populations of threespine sticklebacks. J Evol Biol 19:1803–1812

    Article  CAS  PubMed  Google Scholar 

  • Leinonen T, O’Hara RB, Cano JM, Merilä J (2008) Comparative studies of quantitative trait and neutral marker divergence: a metaanalysis. J Evol Biol 21:1–17

    CAS  PubMed  Google Scholar 

  • Lesur I, Bechade A, Lalanne C, Klopp C, Noirot C, Leplé J-C, Kremer A, Plomion C, Le Provost G (2015) A unigene set for European beech (Fagus sylvatica L.) and its use to decipher the molecular mechanisms involved in dormancy regulation. Mol Ecol. doi:10.1111/1755-0998.12373

  • Lopez R, de Heredia UL, Collada C, Cano FJ, Emerson BC, Cochard H, Gil L (2013) Vulnerability to cavitation, hydraulic efficiency, growth and survival in an insular pine (Pinus canariensis). Ann Bot 111:1167–1179

    Article  PubMed Central  PubMed  Google Scholar 

  • Magri D, Vendramin GG, Comps B, Dupanloup I, Geburek T, Gömöry D, Latalowa M, Litt T, Paule L, Roure JM, Tantau I, van der Knaap WO, Petit RJ, de Beaulieu J-L (2006) A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol 171:199–222

    Article  CAS  PubMed  Google Scholar 

  • Mátyás C (2007) What do field trials tell about the future use of forest reproductive material. In: Koskela J, Buck A, Teissier du Cros E (eds) Climate change and forest genetic diversity: implications for sustainable forest management in Europe. Bioversity International, Rome, pp 53–68

    Google Scholar 

  • McKay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol 17:285–291

    Article  Google Scholar 

  • Merilä J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14:892–903

    Article  Google Scholar 

  • Merilä J, Sheldon BC (1999) Genetic architecture of fitness and non-fitness traits: empirical patterns and development of ideas. Heredity 83:103–109

    Article  PubMed  Google Scholar 

  • Monzon-Argüello C, Consuegra S, Gajardo G, Marco-Rius F, Fowler DM, DeFaveri J, de Leaniz CG (2014) Contrasting patterns of genetic and phenotypic differentiation in two invasive salmonids in the southern hemisphere. Evol Appl 7:921–936

    Article  PubMed Central  PubMed  Google Scholar 

  • Pannatier Y (1996) VARIOWIN: software for spatial data analysis in 2D. Springer, New York

    Book  Google Scholar 

  • Pastorelli R, Smulders MJM, Van’t Westende WPC, Vosman B, Giannini R, Vettori C, Vendramin GG (2003) Characterization of microsatellite markers in Fagus sylvatica L. and Fagus orientalis Lipsky. Mol Ecol Notes 3:76–78

  • Pujol B, Wilson AJ, Ross RIC, Pannell JR (2008) Are Q ST F ST comparisons for natural populations meaningful? Mol Ecol 17:4782–4785

    Article  CAS  PubMed  Google Scholar 

  • Ramirez-Valiente JA, Valladares F, Aranda I (2014) Exploring the impact of neutral evolution on intrapopulation genetic differentiation in functional traits in a long-lived plant. Tree Genet Genomes 10:1181–1190

    Article  Google Scholar 

  • Ritland K (1996) A marker-based method for inferences about quantitative inheritance in natural populations. Evolution 50:1062–1073

    Article  Google Scholar 

  • Ritland K (2000) Marker-inferred relatedness as a tool for detecting heritability in nature. Mol Ecol 9:1195–1204

    Article  CAS  PubMed  Google Scholar 

  • Robson TM, Sanchez-Gomez D, Cano FJ, Aranda I (2012) Variation in functional leaf traits among beech provenances during a Spanish summer reflects the differences in their origin. Tree Genet Genomes 8:1111–1121

    Article  Google Scholar 

  • Santamaria ME, Hasbun R, Valera MJ (2009) Acetylated H4 histone and genomic DNA methylation patterns during bud set and bud burst in Castanea sativa. J Plant Physiol 166:1360–1369

    Article  CAS  PubMed  Google Scholar 

  • SAS (2009) SAS/STAT® user’s guide. http://support.sas.com/documentation/onlinedoc/stat/index.html

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

    Article  Google Scholar 

  • Saxe H, Cannell MGR, Johnsen B, Ryan MG, Vourlitis G (2001) Tree and forest functioning in response to global warming. New Phytol 149:369–399

    Article  CAS  Google Scholar 

  • Schneider SD, Roesli D, Excoffier L (2000) ARLEQUIN, vesion 2.0: a software for population genetic data analysis. University of Geneva, Geneva, 111 pp

  • Seifert S, Vornam B, Finkeldey R (2012a) A set of 17 single nucleotide polymorphism (SNP) markers for European beech (Fagus sylvatica L.). Conserv Genet Res 4:1045–1047

    Article  Google Scholar 

  • Seifert S, Vornam B, Finkeldey R (2012b) DNA sequence variation and development of SNP markers in beech (Fagus sylvatica L.). Eur J Forest Res 131:1761–1770

    Article  CAS  Google Scholar 

  • Skrøppa T, Tollefsrud MM, Sperisen C, Johnsen Ø (2009) Rapid change in adaptive performance from one generation to the next in Picea abies: Central European trees in a Nordic environment. Tree Genet Genomes 6:93–99

    Article  Google Scholar 

  • Spitze K (1993) Population structure in Daphnia obtusa: quantitative genetic and allozymic variation. Genetics 135:367–374

    PubMed Central  CAS  PubMed  Google Scholar 

  • Stojnić S, Orlović S, Pilipović A, Vilotić D, Šijačić-Nikolić M, Miljković D (2012) Variation in leaf physiology among three provenances of European beech (Fagus sylvatica L.) in provenance trial in Serbia. Genetika 44:341–353

    Article  Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisms, regulation and adaptation. Taylor & Francis, London, pp 445–483

    Google Scholar 

  • Tanaka K, Tsumura Y, Nakamura T (1999) Development and polymorphism of microsatellite markers for Fagus crenata and the closely related species, F. japonica. Theor Appl Genet 99:11–15

    Article  CAS  Google Scholar 

  • Vitasse Y, Basler D (2013) What role for photoperiod in the bud burst phenology of European beech. Eur J For Res 132:1–8

    Article  Google Scholar 

  • von Wühlisch G (2008) European beech. EUFORGEN technical guidelines for genetic conservation and use. Bioversity International, Rome, 6 pp

  • von Wuehlisch G, Krusche D, Muhs H-J (1995) Variation in temperature sum requirement for flushing of beech provenances. Silvae Genet 44:343–346

    Google Scholar 

  • Wang J (2012) Computationally efficient sibship and parentage assignment from multilocus marker data. Genetics 191:183–194

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wojcik AM, Polly PD, Sikorski MD, Wojcik JM (2006) Selection in a cycling population: differential response among skeletal traits. Evolution 60:1925–1935

    Article  PubMed  Google Scholar 

  • Zas R (2006) Iterative kriging for removing spatial autocorrelation in analysis of forest genetic trials. Tree Genet Genomes 2:177–185

    Article  Google Scholar 

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Acknowledgments

The provenance experiment has been established through the realization of the project European Network for the Evaluation of the Genetic Resources of Beech for Appropriate Use in Sustainable Forestry Management (AIR3-CT94-2091) under the coordination of H.-J. Muhs. The experimental plot Tále was established by L. Paule. Collection of field data was partly accomplished within the COST Action E52 Evaluation of Beech Genetic Resources for Sustainable Forestry, coordinated by G. von Wühlisch. We express our gratitude to G. Baloghová and K. Gömöryová for technical assistance with nSSR genotyping, T. Priwitzer, M. Macková, E. Pšidová and J. Majerová for the help with the measurements of physiological parameters, and K. Willingham for checking the language. The experiment was supported by the grant of the Slovak Agency for Research and Development APVV-0135-12 and the grant of the Slovak Grant Agency for Science VEGA 1/0218/12.

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Correspondence to Dušan Gömöry.

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Gömöry, D., Ditmarová, Ľ., Hrivnák, M. et al. Differentiation in phenological and physiological traits in European beech (Fagus sylvatica L.). Eur J Forest Res 134, 1075–1085 (2015). https://doi.org/10.1007/s10342-015-0910-2

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