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Large within-population genetic diversity of the widespread conifer Pinus sylvestris at its soil fertility limit characterized by nuclear and chloroplast microsatellite markers

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Abstract

Genetic variation is an important attribute of forest tree populations enabling them to adapt to spatial and temporal variations in environmental conditions. In particular, Scots pine (Pinus sylvestris L.) has an exceptionally broad area of dispersal covering different climates and soil conditions, but the genetic variability in extreme conditions has not been studied. We hypothesized that the genetic variability of P. sylvestris is enhanced at its soil fertility limit in bogs where stunted trees form a sparse canopy with reduced light competition, but in highly turbulent conditions generating ideal conditions for distant pollen dispersal. A total of 180 individuals were studied from three bog populations using five nuclear (nSSR) and five chloroplastic (cpSSR) polymorphic microsatellite loci (simple sequence repeats, SSR). According to both marker systems, high and similar level of genetic diversity (ca. 99 % within the populations and 1 % among the populations) was observed for nuclear (F ST = 0.007 and R ST = 0.022) and chloroplast (F ST = 0.015 and R ST = 0.023) genomes. Despite the low genetic differentiation among the populations, there was evidence of geographic genetic differentiation in the chloroplast genomes, suggesting that isolation by distance might be a possible mechanism shaping the present distribution of genetic variability. In addition, significant but low spatial genetic structure along habitat wetness gradient was found in nuclear genomes in one site. Significant cyto-nuclear linkage disequilibrium was shown between one of the cpSSR loci to all nSSR loci. The results demonstrate a huge within-population genetic variability in these sites and underscore the importance of pollen gene flow in homogenizing populations on these geographic scales.

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References

  • Auckland LD, Bui T, Zhou Y, Shepherd M, Williams CG (2002) Conifer microsatellite handbook. Corporate Press, Raleigh

    Google Scholar 

  • Austerlitz F, Mariette S, Machon N, Gouyon PH, Godelle B (2000) Effects of colonization processes on genetic diversity: differences between annual plants and tree species. Genetics 154:1309–1321

    PubMed  PubMed Central  CAS  Google Scholar 

  • Basten CJ, Asmussen MA (1997) The exact test for cytonuclear disequilibria. Genetics 146:1165–1171

    PubMed  PubMed Central  CAS  Google Scholar 

  • Belletti P, Ferrazzini D, Piotti A, Monteleone I, Ducci F (2012) Genetic variation and divergence in Scots pine (Pinus sylvestris L.) within its natural range in Italy. Eur J For Res 131:1127–1138. doi:10.1007/s10342-011-0584-3

    Article  Google Scholar 

  • Bennett KD, Tzedakis PC, Willis KJ (1991) Quaternary refugia of north European trees. J Biogeogr 18:103–115

    Article  Google Scholar 

  • Bock DG, Andrew RL, Rieseberg LH (2014) On the adaptive value of cytoplasmic genomes in plants. Mol Ecol 23:4899–4911. doi:10.1111/mec.12920

    Article  PubMed  Google Scholar 

  • Bouzat JL (2001) The population genetic structure of the Greater Rhea (Rhea americana) in an agricultural landscape. Biol Conserv 99:277–284. doi:10.1016/S0006-3207(00)00193-2

    Article  Google Scholar 

  • Brown AHD (1978) Isozymes, plant population genetic structure and genetic conservation. Theor Appl Genet 52:145–157

    Article  PubMed  CAS  Google Scholar 

  • Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631. doi:10.1093/molbev/msl191

    Article  PubMed  CAS  Google Scholar 

  • Cheddadi R et al (2006) Imprints of glacial refugia in the modern genetic diversity of Pinus sylvestris. Glob Ecol Biogeogr 15:271–282

    Article  Google Scholar 

  • Critchfield WB, Little EL (1966) Geographic distributions of the pines of the world. U.S.D.A. Serv Misc Public 991, Washington, DC

  • Desplanque B, Viard F, Bernard J, Forcioli D, Saumitou-Laprade P, Cuguen J, van Dijk H (2000) The linkage disequilibrium between chloroplast DNA and mitochondrial DNA haplotypes in Beta vulgaris ssp maritima (L.): the usefulness of both genomes for population genetic studies. Mol Ecol 9:141–154. doi:10.1046/j.1365-294x.2000.00843.x

    Article  PubMed  CAS  Google Scholar 

  • Dzialuk A, Muchewicz E, Boratynski A, Montserrat JM, Boratynska K, Burczyk J (2009) Genetic variation of Pinus uncinata (Pinaceae) in the Pyrenees determined with cpSSR markers. Plant Syst Evol 277:197–205. doi:10.1007/s00606-008-0123-y

    Article  CAS  Google Scholar 

  • Eliades NG, Eliades DG (2009) HAPLOTYPE ANALYSIS: software for analysis of haplotypes data. Distributed by the authors. Forest genetics and forest tree breeding, Georg-Augst University Goettingen, Germany

  • El-Kassaby YA, Rudin D, Yazdani R (1989) Levels of outcrossing and contamination in two Pinus sylvestris L. seed orchards in northern Sweden. Scand J For Res 4:41–49

    Article  Google Scholar 

  • Elsik CG, Minihan VT, Hall SE, Scarpa AM, Williams CG (2000) Low-copy microsatellite markers for Pinus taeda L. Genome 43:550–555. doi:10.1139/gen-43-3-550

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  • Fields PD, McCauley DE, McAssey EV, Taylor DR (2014) Patterns of cyto-nuclear linkage disequilibrium in Silene latifolia: genomic heterogeneity and temporal stability. Heredity 112:99–104. doi:10.1038/hdy.2013.79

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Finér L (1992) Nutrient concentrations in Pinus sylvestris growing on an ombrotrophic pine bog, and the effects of PK and NPK fertilization. Scand J For Res 7:205–218

    Article  Google Scholar 

  • Grassi F et al (2003) Genetic isolation and diffusion of wild grapevine Italian and Spanish populations as estimated by nuclear and chloroplast SSR analysis. Plant Biol 5:608–614. doi:10.1055/s-2003-44689

    Article  CAS  Google Scholar 

  • Gregorius HR (1994) Strategies for conserving genetic diversity in the face of global change. In: Boyle TJB, Boyle CEB (eds) Temperate ecosystems and global change. Springer, Berlin, pp 157–182

    Chapter  Google Scholar 

  • Gunnarsson U, Rydin H (1998) Demography and recruitment of Scots pine on raised bogs in eastern Sweden and relationships to microhabitat differentiation. Wetlands 18:133–141

    Article  Google Scholar 

  • Hamrick JL, Godt MJW, Shermanbroyles SL (1992) Factors influencing levels of genetic diversity in woody plant-species. In: Adams WT, Strauss SH, Copes DL, Griffin AR (eds) Population genetics of forest trees, vol 42, pp 95–124

  • Hansen AJ, Knight RL, Marzluff JM, Powell S, Brown K, Gude PH, Jones A (2005) Effects of exurban development on biodiversity: patterns, mechanisms, and research needs. Ecol Appl 15:1893–1905. doi:10.1890/05-5221

    Article  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  CAS  Google Scholar 

  • Harju A, Muona O (1989) Background pollination in Pinus sylvestris seed orchards. Scand J For Res 4:513–520

    Article  Google Scholar 

  • Hattemer HH (1987) Are the EEC directives on forest reproductive material genetically adequate? Silvae Genet 36:94–102

    Google Scholar 

  • Hattemer HH, Starke R, Ziehe M (1993) Changes of genetic structures in beech populations. In: Muhs H-J, VON Wühlisch G (eds) The scientific basis for the evaluation of the genetic resources of beech. Comm. Europ. Communities, Working Doc. F.II.3-SJ/0009, pp. 233–248

  • Haubold B, Hudson RR (2000) LIAN 3.0: detecting linkage disequilibrium in multilocus data. Bioinformatics 16:847–848. doi:10.1093/bioinformatics/16.9.847

    Article  PubMed  CAS  Google Scholar 

  • Hertel H, Schneck V (1999) Genetic and phenotypical variation of scots pine (Pinus sylvestris L.) populations due to seed origin and environmental conditions at experimental sites. For Genet 6:65–72

    Google Scholar 

  • Holliday JA, Suren H, Aitken SN (2011) Divergent selection and heterogeneous migration rates across the range of Sitka spruce (Picea sitchensis). Proc R Soc Lond B. doi:10.1098/rspb.2011.1805

    Google Scholar 

  • Huntley B, Birks HJB (1983) An Atlas of past and present pollen maps for Europe: 0–13,000 years ago. Cambridge University Press, Cambridge

    Google Scholar 

  • Jump AS, Hunt JM, Martínez-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  PubMed  CAS  Google Scholar 

  • Kadereit JW, Griebeler EM, Comes HP (2004) Quaternary diversification in European alpine plants: pattern and process. Philos Trans R Soc Lond B-Biol Sci 359:265–274. doi:10.1098/rstb.2003.1389

    Article  PubMed  PubMed Central  Google Scholar 

  • Kännaste A, Copolovici L, Pazouki L, Suhhorutsenko M, Niinemets Ü (2013) Highly variable chemical signatures over short spatial distances among Scots pine (Pinus sylvestris) populations. Tree Physiol 33:374–387. doi:10.1093/treephys/tpt013

    Article  PubMed  Google Scholar 

  • Karhu A, Hurme P, Karjalainen M, Karvonen P, Karkkainen K, Neale D, Savolainen O (1996) Do molecular markers reflect patterns of differentiation in adaptive traits of conifers? Theor Appl Genet 93:215–221. doi:10.1007/bf00225748

    Article  PubMed  CAS  Google Scholar 

  • Karp A, Isaac PG, Ingram DS (1998) Molecular tools for screening biodiversity: plants and animals. Chapman & Hall, London

    Book  Google Scholar 

  • Kuznetsova T, Mandre M (2006) Chemical and morphological indication of the state of lodgepole pine and Scots pine in restored oil shale opencast mining areas in Estonia. Oil Shale 23:366–384

    CAS  Google Scholar 

  • Läänelaid A (1981) Pines on bogs as indicators of fires in the past. In: Laasimer L, Trass H, Kask M (eds) Anthropogenous changes in the plant cover of Estonia. Academy of Sciences of the Estonian S.S.R. Institute of Zoology and Botany—“Man and Biosphere”. Republican Committee of the Estonian S.S.R., Tartu, pp 91–94

  • Latta RG, Linhart YB, Mitton JB (2001) Cytonuclear disequilibrium and genetic drift in a natural population of ponderosa pine. Genetics 158:843–850

    PubMed  PubMed Central  CAS  Google Scholar 

  • Li MH, Merila J (2010) Extensive linkage disequilibrium in a wild bird population. Heredity 104:600–610. doi:10.1038/hdy.2009.150

    Article  PubMed  CAS  Google Scholar 

  • Lindgren D, Paule L, Xihuan S, Yadzani R, Segerström U, Tallin JE, Lejdebro ML (1995) Can viable pollen carry Scots pine genes over long distances? Grana 34:64–69

    Article  Google Scholar 

  • Loiselle BA, Sork VL, Nason J, Graham CAJB (1995) Spatial genetic structure of a tropical understorey shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425

    Article  Google Scholar 

  • Luo H, Van Coppenolle B, Seguin M, Boutry M (1995) Mitochondrial DNA polymorphism and phylogenetic relationships in Hevea brasiliensis. Mol Breeding 1:51–63. doi:10.1007/bf01682089

    Article  CAS  Google Scholar 

  • Maaten T, Kurm M (2007) Analysis of genetic variation of Scots pine populations in Estonia based on DNA microsatellite markers. For Stud 46:45–56

    Google Scholar 

  • Michalakis Y, Excoffier L (1996) A genetic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142:1061–1064

    PubMed  PubMed Central  CAS  Google Scholar 

  • Müller-Starck G, Ziehe M (1991) Genetic variation in populations of Fagus sylvatica L., Quercus robur L. and Q. petraea Liebl. in Germany. In: Müller-Starck G, Ziehe M (eds) Genetic variation in european populations of forest trees. Sauerländer’s Verlag, Frankfurt-am Main, pp 125–140

    Google Scholar 

  • Müller-Starck G, Baradat PH, Bergmann F (1992) Genetic variation in European tree species. New Forest 6:23–47

    Article  Google Scholar 

  • Naydenov KD, Tremblay FM, Alexandrov A, Fenton NJ (2005) Structure of Pinus sylvestris L. populations in Bulgaria revealed by chloroplast microsatellites and terpenes analysis: provenance tests. Biochem Syst Ecol 33:1226–1245

    Article  CAS  Google Scholar 

  • Naydenov K, Senneville S, Beaulieu J, Tremblay F, Bousquet J (2007) Glacial vicariance in Eurasia: mitochondrial DNA evidence from Scots pine for a complex heritage involving genetically distinct refugia at mid-northern latitudes and in Asia Minor. BMC Evol Biol 7:233

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  PubMed Central  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Newton AC, Allnutt TR, Gillies ACM, Lowe AJ, Ennos RA (1999) Molecular phylogeography, intraspecific variation and the conservation of tree species. Trends Ecol Evol 14:140–145. doi:10.1016/s0169-5347(98)01555-9

    Article  PubMed  Google Scholar 

  • Nielsen R, Tarpy DR, Reeve HK (2003) Estimating effective paternity number in social insects and the effective number of alleles in a population. Mol Ecol 12:3157–3164. doi:10.1046/j.1365-294X.2003.01994.x

    Article  PubMed  Google Scholar 

  • Niinemets Ü, Ellsworth DS, Lukjanova A, Tobias M (2001) Site fertility and the morphological and photosynthetic acclimation of Pinus sylvestris needles to light. Tree Physiol 21:1231–1244

    Article  PubMed  CAS  Google Scholar 

  • Niinemets Ü, Cescatti A, Lukjanova A, Tobias M, Truus L (2002) Modification of light-acclimation of Pinus sylvestris shoot architecture by site fertility. Agric For Meteorol 111:121–140

    Article  Google Scholar 

  • Nishimura M, Setoguchi H (2011) Homogeneous genetic structure and variation in tree architecture of Larix kaempferi along altitudinal gradients on Mt. Fuji. J Plant Res 124:253–263

    Article  PubMed  Google Scholar 

  • Nowakowska JA, Zachara T, Konecka A (2014) Genetic variability of Scots pine (Pinus sylvestris L.) and Norway spruce (Picea abies L. Karst.) natural regeneration compared with their maternal stands. For Res Pap 75(1):47–54

    Google Scholar 

  • Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155. doi:10.1111/j.1365-294X.2004.02141.x

    Article  PubMed  CAS  Google Scholar 

  • Oleksyn J, Tjoelker MG, Reich PB (1998) Adaptation to changing environment in Scots pine populations across a latitudinal gradient. Silva Fennica 32:129–140

    Article  Google Scholar 

  • Pakkanen A, Pulkkinen P, Vakkari P (1991) Pollen contamination in the years 1988–1989 in some old Scots pine seed orchards of northern Finnish origin Reports from the Foundation for Forest Tree Breeding 3 Helsinki, Finland, pp 3–8

  • Pärt T, Villard MA (2006) Ecological traps: avian and human perspectives. J Ornithol 147:23

    Google Scholar 

  • Pautasso M (2009) Geographical genetics and the conservation of forest trees. Perspect Plant Ecol Evol Syst 11:157–189. doi:10.1016/j.ppees.2009.01.003

    Article  Google Scholar 

  • Pazouki L et al (2010) Genetic diversity and relationships among Pistacia species and cultivars. Conserv Genet 11:311–318. doi:10.1007/s10592-009-9812-5

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX V. 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peñuelas J, Ogaya R, Boada M, Jump AS (2007) Migration, invasion and decline: changes in recruitment and forest structure in a warming-linked shift of European beech forest in Catalonia (NE Spain). Ecography 30:829–837

    Article  Google Scholar 

  • Perks MP, McKay HM (1997) Morphological and physiological differences in Scots pine seedlings of six seed origins. Forestry 70:223–232. doi:10.1093/forestry/70.3.223

    Article  Google Scholar 

  • Pessi AM, Pulkkinen P (1994) Temporal and spatial variation of airborne Scots pine pollen. Grana 3:151–157

    Article  Google Scholar 

  • Petit JR et al (1997) Four climate cycles in Vostok ice core. Nature 387:359–360

    Article  CAS  Google Scholar 

  • Petit RJ et al (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565. doi:10.1126/science.1083264

    Article  PubMed  CAS  Google Scholar 

  • Provan J, Soranzo N, Wilson NJ, McNicol JW, Forrest GI, Cottrell J, Powell W (1998) Gene-pool variation in caledonian and European Scots pine (Pinus sylvestris L.) revealed by chloroplast simple-sequence repeats. Proc R Soc Lond B Biol Sci 265:1697–1705

    Article  CAS  Google Scholar 

  • Prus-Glowacki W, Urbaniak L, Zubrowska-Gil M (1993) Allozyme differentiation in Mid-Eropean and Scandinavian population of Scots pine (Pinus sylvestris). Genetica Polonica 34:159–176

    Google Scholar 

  • Prus-Glowacki W, Stephan BR, Bujas E, Alia R, Marciniak A (2003) Genetic differentiation of autochthonous populations of Pinus sylvestris (Pinaceae) from the Iberian peninsula. Plant Syst Evol 239:55–66. doi:10.1007/s00606-002-0256-3

    Article  Google Scholar 

  • Pulkkinen P, Rantiolehtimaki A (1995) Viability and seasonal distribution patterns of Scots pine pollen in Finland. Tree Physiol 15:515–518

    Article  PubMed  Google Scholar 

  • Pyhäjärvi T, Garcia-Gil MR, Knurr T, Mikkonen M, Wachowiak W, Savolainen O (2007) Demographic history has influenced nucleotide diversity in European Pinus sylvestris populations. Genetics 177:1713–1724. doi:10.1514/genetics.107.077099

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pyhäjärvi T, Salmela MJ, Savolainen O (2008) Colonization routes of Pinus sylvestris inferred from distribution of mitochondrial DNA variation. Tree Genet Genomes 4:247–254. doi:10.1007/s11295-007-0105-1

    Article  Google Scholar 

  • Ribeiro MM, Mariette S, Vendramin GG, Szmidt AE, Plomion C, Kremer A (2002) Comparison of genetic diversity estimates within and among populations of maritime pine using chloroplast simple-sequence repeat and amplified fragment length polymorphism data. Mol Ecol 11:869–877. doi:10.1046/j.1365-294X.2002.01490.x

    Article  PubMed  CAS  Google Scholar 

  • Robledo-Arnuncio JJ, Gil L (2005) Patterns of pollen dispersal in a small population of Pinus sylvestris L. revealed by total-exclusion paternity analysis. Heredity 94:13–22. doi:10.1038/sj.hdy.6800542

    Article  PubMed  CAS  Google Scholar 

  • Robledo-Arnuncio JJ, Alia R, Gil L (2004) Increased selfing and correlated paternity in a small population of a predominantly outcrossing conifer, Pinus sylvestris. Mol Ecol 13:2567–2577. doi:10.1111/j.1365-294X.2004.02251.x

    Article  PubMed  CAS  Google Scholar 

  • Robledo-Arnuncio JJ, Collada C, Alia R, Gil L (2005) Genetic structure of montane isolates of Pinus sylvestris L. in a Mediterranean refugial area. J Biogeogr 32:595–605. doi:10.1111/j.1365-2699.2004.01196.x

    Article  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    PubMed  PubMed Central  CAS  Google Scholar 

  • Sarvas R (1962) Investigations on the flowering and seed crop of Pinus sylvestris. Commun Inst For Fenn 53:1–198

    Google Scholar 

  • Saylor LC (1972) Karyotype analysis of the genus Pinus—subgenus Pinus. Silvae Genetica 21:155–163

    Google Scholar 

  • Scalfi M, Piotti A, Rossi M, Piovani P (2009) Genetic variability of Italian southern Scots pine (Pinus sylvestris L.) populations: the rear edge of the range. Eur J Forest Res 128:377–386. doi:10.1007/s10342-009-0273-7

    Article  CAS  Google Scholar 

  • Sgorbati S et al (2004) A survey of genetic diversity and reproductive biology of Puya raimondii (Bromeliaceae), the endangered queen of the Andes. Plant Biol 6:222–230. doi:10.1055/s-2004-817802

    Article  PubMed  CAS  Google Scholar 

  • Shanjani PS, Vettori C, Giannini R, Khavari-Nejad RA (2004) Intraspecific variation and geographic patterns of Fagus orientalis Lipsky chloroplast DNA. Silvae Genetica 53:193–197

    Google Scholar 

  • Shanjani PS, Vendramin GG, Calagari M (2010) Genetic diversity and differentiation of Fagus orientalis Lipsky in Hyrcanian forests revealed by nuclear and chloroplast microsatellite markers. Conserv Genet 11:2321–2331. doi:10.1007/s10592-010-0118-4

    Article  Google Scholar 

  • Shanjani PS, Vendramin GG, Calagari M (2011) Altitudinal genetic variations among the Fagus orientalis Lipsky populations in Iran. Iran J Biotechnol 9:11–20

    Google Scholar 

  • Sinclair WT, Morman JD, Ennos RA (1998) Multiple origins for Scots pine (Pinus sylvestris L) in Scotland: evidence from mitochondrial DNA variation. Heredity 80:233–240. doi:10.1038/sj.hdy.6882870

    Article  CAS  Google Scholar 

  • Sinclair WT, Morman JD, Ennos RA (1999) The postglacial history of Scots pine (Pinus sylvestris L.) in western Europe: evidence from mitochondrial DNA variation. Mol Ecol 8:83–88. doi:10.1046/j.1365-294X.1999.00527.x

    Article  Google Scholar 

  • Slate J, Pemberton JM (2007) Admixture and patterns of linkage disequilibrium in a free-living vertebrate population. J Evol Biol 20:1415–1427. doi:10.1111/j.1420-9101.2007.01339.x

    Article  PubMed  CAS  Google Scholar 

  • Slatkin M (1994) Linkage disequilibrium in growing and stable populations. Genetics 137:331–336

    PubMed  PubMed Central  CAS  Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    PubMed  PubMed Central  CAS  Google Scholar 

  • Sloan DB, Barr CM, Olson MS, Keller SR, Taylor DR (2008) Evolutionary rate variation at multiple levels of biological organization in plant mitochondrial DNA. Mol Biol Evol 25:243–246. doi:10.1093/molbev/msm266

    Article  PubMed  CAS  Google Scholar 

  • Soranzo N, Provan J, Powell W (1998) Characterization of microsatellite loci in Pinus sylvestris L. Mol Ecol 7:1260–1261

    PubMed  CAS  Google Scholar 

  • Soranzo N, Alia R, Provan J, Powell W (2000) Patterns of variation at a mitochondrial sequence-tagged-site locus provides new insights into the postglacial history of European Pinus sylvestris populations. Mol Ecol 9:1205–1211. doi:10.1046/j.1365-294x.2000.00994.x

    Article  PubMed  CAS  Google Scholar 

  • Strauss SH, Hong YP, Hipkins VD (1993) High levels of population differentiation for mitochondrial DNA haplotypes in Pinus radiata, muricata, andattenuata TAG. Theor Appl Genet 86:605–611. doi:10.1007/bf00838716

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Varis S, Pakkanen A, Galofre A, Pulkkinen P (2009) The extent of south-north pollen transfer in Finnish scots pine. Silva Fennica 43:717–726

    Article  Google Scholar 

  • Vendramin GG, Lelli L, Rossi P, Morgante M (1996) A set of primers for the amplification of 20 chloroplast microsatellites in Pinaceae. Mol Ecol 5:595–598

    Article  PubMed  CAS  Google Scholar 

  • Vendramin GG, Anzidei M, Madaghiele A, Bucci G (1998) Distribution of genetic diversity in Pinus pinaster Ait. as revealed by chloroplast microsatellites. Theor Appl Genet 97:456–463. doi:10.1007/s001220050917

    Article  CAS  Google Scholar 

  • Wang X-R, Szmidt AE, Lindgren DAG (1991) Allozyme differentiation among populations of Pinus sylvestris (L.) from Sweden and China. Hereditas 114:219–226. doi:10.1111/j.1601-5223.1991.tb00328.x

    Article  Google Scholar 

  • Wegmann D, Currat M, Excoffier L (2006) Molecular diversity after a range expansion in heterogeneous environments. Genetics 174:2009–2020. doi:10.1534/genetics.106.062851

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354

    Article  PubMed  CAS  Google Scholar 

  • Zhou Y, Bui T, Auckland LD, Williams CG (2002) Undermethylated DNA as a source of microsatellites from a conifer genome. Genome 45:91–99. doi:10.1139/g01-119

    Article  PubMed  CAS  Google Scholar 

  • Ziehe M, Gregorius HR, Glock H, Hattemer HH, Herzog S (1989) Gene resources and gene conservation in forest trees: general concepts. In: Scholz F, Gregorius HR, Rudin D (eds) Genetic effects of air populations in forest tree populations. Springer, Heidelberg, pp 173–186

    Chapter  Google Scholar 

  • Ziehe M, Hattemer HH, Müller-Starck R, Müller-Starck G (1999) Genetic structures as indicators for adaptation and adaptational potentials. In: Mátyás C (ed) Forest genetics and sustainability. Kluwer Academic Publishers, Dordrecht, pp 75–89

    Google Scholar 

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Acknowledgments

We thank Dr. Astrid Kännaste and Dr. Lucian Copolovici for the help in sampling Scots pine populations and Seyedeh Azimeh Motallebi Hasankola for the help to prepare some graphs. Financial support for the study has been provided by the Estonian Ministry of Science and Education (institutional Grant IUT-8-3), and the European Commission through the European Regional Fund (the Center of Excellence in Environmental Adaptation).

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Authors and Affiliations

  1. Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Kreutzwaldi 1, 51014, Tartu, Estonia

    Leila Pazouki, Marina Suhhorutšenko & Ülo Niinemets

  2. Research Institute of Forests and Rangelands, National Botanical Garden of Iran, P.O. Box 13185-116, Tehran, Iran

    Parvin Salehi Shanjani

  3. Zoological Institute, University of Basel, Vesalgasse 1, Basel, 4051, Switzerland

    Peter D. Fields

  4. Universidade Federal de São Carlos, Campus Sorocaba, Sorocaba, SP, Brazil

    Karina Martins

  5. Institute of Veterinary Medicine and Animal Sciences, Estonian University of Life Sciences, Kreutzwaldi 62, 51014, Tartu, Estonia

    Haldja Viinalass

  6. Estonian Academy of Sciences, Kohtu 6, 10130, Tallinn, Estonia

    Ülo Niinemets

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  2. Parvin Salehi Shanjani
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  3. Peter D. Fields
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  4. Karina Martins
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  5. Marina Suhhorutšenko
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Corresponding author

Correspondence to Leila Pazouki.

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Communicated by Jarmo Holopainen.

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Pazouki, L., Shanjani, P.S., Fields, P.D. et al. Large within-population genetic diversity of the widespread conifer Pinus sylvestris at its soil fertility limit characterized by nuclear and chloroplast microsatellite markers. Eur J Forest Res 135, 161–177 (2016). https://doi.org/10.1007/s10342-015-0928-5

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  • DOI: https://doi.org/10.1007/s10342-015-0928-5

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