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Sequence variation patterns along a latitudinal cline in Scots pine (Pinus sylvestris): signs of clinal adaptation?

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Abstract

Adaptive clinal variation is abundant in nature, and its genetic basis is of great interest. The polygenic nature of this variation poses a challenge for identifying the causative loci underlying these adaptations. Here, we have examined the patterns of sequence variation in ten candidate genes for timing of bud set and cold tolerance, traits that form strong latitudinal clines in Scots pine (Pinus sylvestris). A set of reference genes was used for comparison and to infer a simplified demographic background model with approximate Bayesian computation methods. Against the resulting bottleneck model, the neutrality tests show little signs for local adaptation, but species-wide selection is suggested in some of the studied genes. In line with the theoretical expectations, we see little evidence for adaptive differentiation with F ST methods. Instead, allele frequency clines were found in three genes (dhn1, ftl2, and prr1). Our results add to the discussion on which molecular signals best characterize a gene subject to clinally varying selection. This will be especially relevant when these kinds of observations can be examined in parallel with association study results.

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References

  • Aho ML (1994) Autumn frost hardening of one-year-old Pinus sylvestris (L.) seedlings: effect of origin and parent trees. Scand J For Res 9:17–24

    Article  Google Scholar 

  • Barton NH (1999) Clines in polygenic traits. Genet Res 74:223–236

    Article  PubMed  CAS  Google Scholar 

  • Beaumont MA, Zhang W, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035

    PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Bertorelle G, Benazzo A, Mona S (2010) ABC as a flexible framework to estimate demography over space and time: some cons, many pros. Mol Ecol 19:2609–2625

    Article  PubMed  CAS  Google Scholar 

  • Biswas S, Akey JM (2006) Genomic insights into positive selection. Trends Genet 22:437–446

    Article  PubMed  CAS  Google Scholar 

  • Bridle JR, Polechová J, Kawata M, Butlin RK (2010) Why is adaptation prevented at ecological margins? New insights from individual-based simulations. Ecol Lett 13:485–494

    Article  PubMed  Google Scholar 

  • Brown GR, Gill GP, Kuntz RJ, Langley CH, Neale DB (2004) Nucleotide diversity and linkage disequilibrium in loblolly pine. Proc Natl Acad Sci U S A 101:15255–15260

    Article  PubMed  CAS  Google Scholar 

  • Cheddadi R, de Beaulieu JL, Jouzel J, Andrieu-Ponel V, Laurent JM, Reille M, Raynaud D, Bar-Hen A (2005) Similarity of vegetation dynamics during interglacial periods. Proc Natl Acad Sci U S A 102:13939–13943

    Article  PubMed  CAS  Google Scholar 

  • Cheddadi R, Vendramin GG, Litt T, François L, Kageyama M, Lorentz S, Laurent JM, de Beaulieu JL, Sadori L, Jost A, Lunt D (2006) Imprints of glacial refugia in the modern genetic diversity of Pinus sylvestris. Global Ecol Biogeogr 15:271–282

    Google Scholar 

  • Chen Y, Xiaoyan Y, Kun H et al (2006) The MYB transcription superfamily of Arabidopsis: expression analysis and phylogenetic comparison with rice MYB family. Plant Mol Biol 60:107–124

    Article  CAS  Google Scholar 

  • Chevin LM, Hospital F (2008) Selective sweep at a quantitative trait locus in the presence of background genetic variation. Genetics 180:1645–1660

    Article  PubMed  Google Scholar 

  • Close TJ (1997) Dehydrins: a commonalty in the response of plants to dehydration and low temperature. Physiol Plant 100:291–296

    Article  CAS  Google Scholar 

  • Costa R, Peixoto AA, Barbujani G, Kyriacou CP (1992) A latitudinal cline in a Drosophila clock gene. Proc R Soc of Lond B 250:43–49

    Article  CAS  Google Scholar 

  • Csilléry K, Blum MGB, Gaggiotti OE, François O (2010) Approximate Bayesian computation (ABC) in practice. Trends Ecol Evol 25:410–418

    Article  PubMed  Google Scholar 

  • de Carvalho D, Ingvarsson PK, Joseph J, Suter L, Sedivy C, Macaya-Sanz D, Cottrell J, Heinze B, Schanzer I, Lexer C (2010) Admixture facilitates adaptation from standing variation in the European aspen (Populus tremula L.), a widespread forest tree. Mol Ecol 19:1638–1650

    Article  CAS  Google Scholar 

  • De Mita S, Ronfort J, McKhann HI, Poncet C, El Malki R, Bataillon T (2007) Investigation of the demographic and selective forces shaping the nucleotide diversity of genes involved in Nod factor signaling in Medicago truncatula. Genetics 177:2123–2133

    Article  PubMed  Google Scholar 

  • Depaulis F, Mousset S, Veuille M (2003) Power of neutrality test to detect bottlenecks and hitchhiking. J Mol Evol 57:S190–S200

    Article  PubMed  CAS  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 (2009) 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  PubMed  CAS  Google Scholar 

  • Dormling I (1979) Influence of light intensity and temperature on photoperiodic response of Norway spruce provenances. In Proc IUFRO Jt Meet Work Parties Norway Spruce provenances Norway spruce breed, Bucharest, pp 398–407

  • Ducousso A, Guyon JP, Kremer A (1996) Latitudinal and altitudinal variation of bud burst in western populations of sessile oak (Quercus petraea (Matt) Liebl). Ann Sci For 53:775–782

    Article  Google Scholar 

  • Dvornyk V, Sirviö A, Mikkonen M, Savolainen O (2002) Low nucleotide diversity at the pal1 locus in the widely distributed Pinus sylvestris. Mol Biol Evol 19:179–188

    Article  PubMed  CAS  Google Scholar 

  • Eckert AJ, Wegrzyn JL, Pande B, Jermstad KD, Lee JM, Liechty JD, Tearse BR, Krutovsky KV, Neale DB (2009) Multilocus patterns of nucleotide diversity and divergence reveal positive selection at candidate genes related to cold-hardiness in coastal Douglas-fir (Pseudotsuga menziesii var. menziesii). Genetics 183:289–298

    Article  PubMed  Google Scholar 

  • Eckert AJ, Bower AD, González-Martínez SC, Wegrzyn JL, Coop G, Neale DB (2010a) Back to nature: ecological genomics of loblolly pine (Pinus taeda, Pinaceae). Mol Ecol 19:3789–3805

    Article  PubMed  CAS  Google Scholar 

  • Eckert AJ, van Heerwaarden J, Wegrzyn JL, Nelson CD, Ross-Ibarra J, González-Martínez SC, Neale DB (2010b) Patterns of population structure and environmental associations to aridity across the range of loblolly pine (Pinus taeda L., Pinaceae). Genetics 185:969–982

    Article  PubMed  CAS  Google Scholar 

  • Endler JA (1977) Geographic variation, speciation, and clines. Princeton University Press, Princeton

    Google Scholar 

  • Espartero J, Pintor-Toro J, Pardo J (1994) Differential accumulation of s-adenosylmethionine synthetase transcripts in response to salt stress. Plant Mol Biol 25:217–227

    Article  PubMed  CAS  Google Scholar 

  • Eveno E, Collada C, Guevara MA, Léger V, Soto A, Díaz L, Léger P, González-Martínez SC, Cervera MT, Plomion C, Garnier-Gere PH (2008) Contrasting patterns of selection at Pinus pinaster Ait. drought stress candidate genes as revealed by genetic differentiation analyses. Mol Biol Evol 25:417–437

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  • Excoffier L, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40:481–501

    Article  Google Scholar 

  • Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993

    Article  PubMed  Google Scholar 

  • François O, Blum MGB, Jakobsson M, Rosenberg NA (2008) Demographic history of European populations of Arabidopsis thaliana. PLoS Genet 4:e1000075

    Article  PubMed  CAS  Google Scholar 

  • Franklin KA, Quail PH (2010) Phytochrome functions in Arabidopsis development. J Exp Bot 61:11–24

    Article  PubMed  CAS  Google Scholar 

  • García-Gil MR, Mikkonen M, Savolainen O (2003) Nucleotide diversity at two phytochrome loci along a latitudinal cline in Pinus sylvestris. Mol Ecol 12:1195–1206

    Article  PubMed  Google Scholar 

  • Glinka S, Ometto L, Mousset S, Stephan W, De Lorenzo D (2003) Demography and natural selection have shaped genetic variation in Drosophila melanogaster: a multi-locus approach. Genetics 165:1269–1278

    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  CAS  Google Scholar 

  • Gossman TI, Song B-H, Windsor AJ, Mitchell-Olds T, Dixon CJ, Kapralov MV, Filatov DA, Eyre-Walker A (2010) Genome wide analyses reveal little evidence for adaptive evolution in many plant species. Mol Biol Evol 27:1822–1832

    Article  CAS  Google Scholar 

  • Grivet D, Sebastiani F, Alía R, Bataillon T, Torre S, Zabal-Aguirre M, Vendramin GG, González-Martínez SC (2011) Molecular footprints of local adaptation in two Mediterranean conifers. Mol Biol Evol 28:101–116

    Article  PubMed  CAS  Google Scholar 

  • Gyllenstrand N, Clapham D, Källman T, Lagercrantz U (2007) A Norway spruce FLOWERING LOCUS T homolog is implicated in control of growth rhythm in conifers. Plant Physiol 144:248–257

    Article  PubMed  CAS  Google Scholar 

  • Hahn MW (2008) Toward a selection theory of molecular evolution. Evolution 62:255–265

    Article  PubMed  CAS  Google Scholar 

  • Hall D, Luquez V, Garcia VM, St Onge KR, Jansson S, Ingvarsson PK (2007) Adaptive population differentiation in phenology across a latitudinal gradient in European aspen (Populus tremula, L.): a comparison of neutral markers, candidate genes and phenotypic traits. Evolution 61:2849–2860

    Article  PubMed  Google Scholar 

  • Hall D, Ma XF, Ingvarsson PK (2011) Adaptive evolution of the Populus tremula photoperiod pathway. Mol Ecol 20:1463–1474

    Article  PubMed  Google Scholar 

  • Hayama R, Coupland G (2003) Shedding light on the circadian clock and the photoperiodic control of flowering. Curr Opinion in Plant Biol 6:13–19

    Article  CAS  Google Scholar 

  • Hedrick PW (2006) Genetic polymorphism in heterogeneous environments: the age of genomics. Annu Rev Ecol Evol Syst 37:67–93

    Article  Google Scholar 

  • Hedrick PW, Ginevan ME, Ewing EP (1976) Genetic polymorphism in heterogeneous environments. Annu Rev Ecol Syst 7:1–32

    Article  Google Scholar 

  • Hernandez RD, Kelley JL, Elyashiv E, Cord Melton S, Auton A, McVean G, 1000 Genomes Project, Sella G, Przeworski M (2011) Classic selective sweeps were rare in recent human evolution. Science 331:920–924

    Article  PubMed  CAS  Google Scholar 

  • Heuertz M, De Paoli E, Källman T, Larsson H, Jurman I, Morgante M, Lascoux M, Gyllenstrand N (2006) Multilocus patterns of nucleotide diversity, linkage disequilibrium and demographic history of Norway spruce Picea abies (L.) Karst. Genetics 174:2095–2105

    Article  PubMed  CAS  Google Scholar 

  • Hill WG, Robertson AV (1968) Linkage disequilibrium in finite populations. Theor Appl Genet 38:226–231

    Article  Google Scholar 

  • Hill WG, Weir BS (1988) Variances and covariances of squared linkage disequilibria in finite populations. Theor Popul Biol 33:54–78

    Article  PubMed  CAS  Google Scholar 

  • Hohenlohe PA, Phillips PC, Cresko WA (2010) Using population genomics to detect selection in natural populations: key concepts and methodological considerations. Int J Plant Sci 171:1059–1071

    Article  PubMed  CAS  Google Scholar 

  • Holefors A, Opseth L, Rosnes AKR, Ripel L, Snipen L, Fossdal CG, Olsen JE (2009) Identification of PaCOL1 and PaCOL2, two CONSTANS-like genes showing decreased transcript levels preceding short day induced growth cessation in Norway spruce. Plant Physiol Biochem 47:105–115

    Article  PubMed  CAS  Google Scholar 

  • Holliday JA, Ritland K, Aitken SN (2010a) Widespread, ecologically relevant genetic markers developed from association mapping of climate-related traits in Sitka spruce (Picea sitchensis). New Phytol 188:501–514

    Article  PubMed  Google Scholar 

  • Holliday JA, Yuen M, Ritland K, Aitken S (2010b) Postglacial history of a widespread conifer produces inverse clines in selective neutrality tests. Mol Ecol 19:3857–3864

    Article  PubMed  CAS  Google Scholar 

  • Hudson RR (2001) Two-locus sampling distributions and their application. Genetics 159:1805–1817

    PubMed  CAS  Google Scholar 

  • Hudson RR, Kreitman M, Aguadé M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159

    PubMed  CAS  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 

  • Hurme P, Repo T, Savolainen O, Pääkkonen T (1997) Climatic adaptation of bud set and frost hardiness in Scots pine (Pinus sylvestris). Can J For Res 27:716–723

    Article  Google Scholar 

  • Hurme P, Sillanpää MJ, Arjas E, Repo T, Savolainen O (2000) Genetic basis of climatic adaptation in Scots pine by Bayesian quantitative trait locus analysis. Genetics 156:1309–1322

    PubMed  CAS  Google Scholar 

  • Ingvarsson PK (2008) Multilocus patterns of nucleotide polymorphism and the demographic history of Populus tremula. Genetics 180:329–340

    Article  PubMed  Google Scholar 

  • Ingvarsson PK, García MV, Hall D, Luquez V, Jansson S (2006) Clinal variation in phyB2, a candidate gene for day-length-induced growth cessation and bud set, across a latitudinal gradient in European aspen (Populus tremula). Genetics 172:1845–1853

    Article  PubMed  CAS  Google Scholar 

  • Ingvarsson PK, Garcia MV, Luquez V, Hall D, Jansson S (2008) Nucleotide polymorphism and phenotypic associations within and around the phytochrome B2 locus in European aspen (Populus tremula, Salicaceae). Genetics 178:2217–2226

    Article  PubMed  CAS  Google Scholar 

  • Jaramillo-Correa JP, Verdu M, Gonzalez-Martinez SC (2010) The contribution of recombination to heterozygosity differs among plant evolutionary lineages and life-forms. BMC Evol Biol 10:22

    Article  PubMed  CAS  Google Scholar 

  • Jesus FF, Wilkins JF, Solferini VN, Wakeley J (2006) Expected coalescence times and segregating sites in a model of glacial cycles. Genet Mol Res 5:466–474

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Karlgren A, Gyllenstrand N, Källman T, Sundström JF, Moore D, Lascoux M, Lagercrantz U (2011) Evolution of the PEBP gene family in plants: functional diversification in seed plant evolution. Plant Physiol 156:1967–1977

    Article  PubMed  CAS  Google Scholar 

  • Keller SR, Sowell DR, Neiman M, Wolfe LM, Taylor DR (2009) Adaptation and colonization history affect the evolution of clines in two introduced species. New Phytol 183:678–690

    Article  PubMed  Google Scholar 

  • Keller SR, Levsen N, Ingvarsson PK, Olson MS, Tiffin P (2011) Local selection across a latitudinal gradient shapes nucleotide diversity in balsam poplar, Populus balsamifera L. Genetics 188:941–952

    Article  PubMed  CAS  Google Scholar 

  • Kelly JK (2006) Geographical variation in selection, from phenotypes to molecules. Am Nat 167:481–495

    Article  PubMed  Google Scholar 

  • Kim W-Y, Fujiwara S, Suh S-S, Kim J, Kim Y, Han L, David K, Putterill J, Nam HG, Somers DE (2007) ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449:356–362

    Article  PubMed  CAS  Google Scholar 

  • Kremer A, Le Corre V (2012) Decoupling of differentiation between traits and their underlying genes in response to divergent selection. Heredity 108:375–385

    Google Scholar 

  • Kremer A, Kleinschmit J, Cottrell J, Cundall EP, Deans JD, Ducousso A, König AO, Lowe AJ, Munro RC, Petit RJ, Stephan R (2002) Is there a correlation between chloroplastic and nuclear divergence, or what are the roles of history and selection on genetic diversity in European oaks? For Ecol Manag 156:75–87

    Article  Google Scholar 

  • Latta RG (1998) Differentiation of allelic frequencies at quantitative trait loci affecting locally adaptive traits. Am Nat 151:283–292

    Article  PubMed  CAS  Google Scholar 

  • Le Corre V, Kremer A (2003) Genetic variability at neutral markers, quantitative trait loci and trait in a subdivided population under selection. Genetics 164:1205–1219

    PubMed  Google Scholar 

  • Lepoittevin C (2009) Association genetics in maritime pine (Pinus pinaster Ait.) for growth and wood quality traits. Dissertation, University of Bordeaux

  • Lewontin RC, Krakauer J (1973) Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics 74:175–195

    PubMed  CAS  Google Scholar 

  • Li Q-H, Yang H-Q (2007) Cryptochrome signaling in plants. Photochem Photobiol 83:94–101

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Stocks M, Hemmilä S, Källman T, Zhu H, Zhou Y, Chen J, Liu J, Lascoux M (2010) Demographic histories of four spruce (Picea) species of the Qinghai-Tibetan Plateau and neighboring areas inferred from multiple nuclear loci. Mol Biol Evol 27:1001–1014

    Article  PubMed  CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  PubMed  CAS  Google Scholar 

  • Luquez V, Hall D, Albrectsen BR, Karlsson J, Ingvarsson P, Jansson S (2008) Natural phenological variation in aspen (Populus tremula): the SwAsp collection. Tree Genet Genom 4:279–292

    Article  Google Scholar 

  • Ma XF, Hall D, St. Onge KR, Jansson S, Ingvarsson PK (2010) Genetic differentiation, clinal variation and phenotypic associations with growth cessation across the Populus tremula photoperiodic pathway. Genetics 186:1033–1044

    Article  PubMed  CAS  Google Scholar 

  • Más P, Yanovsky MJ (2009) Time for circadian rhythms: plants get synchronized. Curr Opinion in Plant Biol

  • Maynard Smith J, Haigh J (1974) The hitch-hiking effect of a favorable gene. Genet Res 23:23–35

    Article  Google Scholar 

  • McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654

    Article  PubMed  CAS  Google Scholar 

  • McVean G, Awadalla P, Fearnhead P (2002) A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160:1231–1241

    PubMed  CAS  Google Scholar 

  • Mikola J (1982) Bud-set phenology as an indicator of climatic adaptation of Scots pine in Finland. Silvae Fenn 16:178–184

    Google Scholar 

  • Mirov N (1967) The genus Pinus. Ronald Press, New York

    Google Scholar 

  • Moeller DA, Tiffin P (2008) Geographic variation in adaptation at the molecular level: a case study of plant immunity genes. Evolution 62:3069–3081

    Article  PubMed  CAS  Google Scholar 

  • Moritsuka E, Hisataka Y, Tamura M, Uchiyama K, Watanabe A, Tsumura Y, Tachida H (2012) Extended linkage disequilibrium in non-coding regions in a conifer, Cryptomeria japonica. Genetics 190:1145–1148

  • Müller UC, Pross J, Bibus E (2003) Vegetation response to rapid climate change in Central Europe during the past 140,000 yr based on evidence from the Furamoos pollen record. Quat Res 59:235–245

    Article  Google Scholar 

  • Namroud MC, Guillet-Glaude C, Mackay J, Isabel N, Bousquet J (2010) Molecular evolution of regulatory genes in spruces from different species and continents: heterogeneous patterns of linkage disequilibrium and selection but correlated recent demographic changes. J Mol Evol 70:371–386

    Article  PubMed  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  CAS  Google Scholar 

  • Nicholas KB, Nicholas HB Jr, Deerfield DW II (1997) GeneDoc: analysis and visualization of genetic variation. EMBNEW NEWS 4:14

    Google Scholar 

  • Nordborg M, Innan H (2003) The genealogy of sequences containing multiple sites subject to strong selection in a subdivided population. Genetics 163:1201–1213

    PubMed  Google Scholar 

  • Nordborg M, Borevitz JO, Bergelson J, Berry CC, Chory J, Hagenblad J, Kreitman M, Maloof JN, Noyes T, Oefner PJ, Stahl EA, Weigel D (2002) The extent of linkage disequilibrium in Arabidopsis thaliana. Nature Genet 30:190–193

    Article  PubMed  CAS  Google Scholar 

  • Nordborg M, Hu TT, Ishino Y et al (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3:1289–1299

    Article  CAS  Google Scholar 

  • Notivol E, García-Gil MR, Alía R, Savolainen O (2007) Genetic variation of growth rhythm traits in the limits of a latitudinal cline in Scots pine. Can J For Res 37:540–551

    Article  Google Scholar 

  • Oakeshott JG, Gibson JB, Anderson PR, Knibb WR, Anderson DG, Chambers GK (1982) Alcohol dehydrogenase and glycerol-3-phosphate dehydrogenase clines in Drosophila melanogaster on different continents. Evolution 36:86–96

    Article  Google Scholar 

  • Palmé AE, Wright M, Savolainen O (2008) Patterns of divergence among conifer ESTs and polymorphism in Pinus sylvestris identify putative selective sweeps. Mol Biol Evol 25:2567–2577

    Article  PubMed  CAS  Google Scholar 

  • Palmé AE, Pyhäjärvi T, Wachowiak W, Savolainen O (2009) Selection on nuclear genes in a Pinus phylogeny. Mol Biol Evol 26:893–905

    Article  PubMed  CAS  Google Scholar 

  • Parkash R, Karan D, Munjal AK (1999) Geographical variation in Adh F and alcoholic resource utilization in Indian populations of Drosophila melanogaster. Biol J Linn Soc 66:205–214

    Google Scholar 

  • Pavy N, Namroud MC, Gagnon F, Isabel N, Bousquet J (2012) The heterogeneous levels of linkage disequilibrium in white spruce genes and comparative analysis with other conifers. Heredity 108:273–284

    Google Scholar 

  • Przeworski M (2002) The signature of positive selection at randomly chosen loci. Genetics 160:1179–1189

    PubMed  Google Scholar 

  • Pyhäjärvi T, García-Gil MR, Knürr T, Mikkonen M, Wachowiak W, Savolainen O (2007) Demographic history has influenced nucleotide diversity in European Pinus sylvestris populations. Genetics 177:1713–1724

    Article  PubMed  CAS  Google Scholar 

  • Pyhäjärvi T, Salmela MJ, Savolainen O (2008) Colonization routes of Pinus sylvestris inferred from distribution of mitochondrial DNA variation. Tree Genet Genom 4:247–254

    Article  Google Scholar 

  • Pyhäjärvi T, Kujala ST, Savolainen O (2011) Revisiting protein heterozygosity in plants—nucleotide diversity in allozyme coding genes of conifer Pinus sylvestris. Tree Genet Genom 7:385–397

    Article  Google Scholar 

  • Sabeti PC, Reich DE, Higgins JM et al (2002) Detecting recent positive selection in the human genome from haplotype structure. Nature 419:832–837

    Article  PubMed  CAS  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 For Res 128:377–386

    Article  CAS  Google Scholar 

  • Sezgin E, Duvernell DD, Matzkin LM et al (2004) Single-locus latitudinal clines and their relationship to temperate adaptation in metabolic genes and derived alleles in Drosophila melanogaster. Genetics 168:923–931

    Article  PubMed  CAS  Google Scholar 

  • Soranzo N, Alía 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

    Article  PubMed  CAS  Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100:9440–9445

    Article  PubMed  CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034

    Article  PubMed  CAS  Google Scholar 

  • Viherä-Aarnio A, Häkkinen R, Partanen J, Luomajoki A, Koski V (2005) Effects of seed origin and sowing time on timing of height growth cessation of Betula pendula seedlings. Tree Physiol 25:101–108

    Article  PubMed  Google Scholar 

  • Wachowiak W, Balk PA, Savolainen O (2009) Search for nucleotide diversity patterns of local adaptation in dehydrins and other cold-related candidate genes in Scots pine (Pinus sylvestris L.). Tree Genet Genom 5:117–132

    Article  Google Scholar 

  • Wachowiak W, Salmela MJ, Ennos RA, Iason G, Cavers S (2011) High genetic diversity at the extreme range edge: nucleotide variation at nuclear loci in Scots pine (Pinus sylvestris L.) in Scotland. Heredity 106:775–787

    Article  PubMed  CAS  Google Scholar 

  • Willis KJ, van Andel TH (2004) Trees or no trees? The environments of central and eastern Europe during the Last Glaciation. Quat Sci Rev 23:2369–2387

    Article  Google Scholar 

  • Zeng K, Fu YX, Shi S, Wu CI (2006) Statistical tests for detecting positive selection by utilizing high-frequency variants. Genetics 174:1431–1439

    Article  PubMed  Google Scholar 

  • Zeng K, Shi S, Wu CI (2007) Compound tests for the detection of hitchhiking under positive selection. Mol Biol Evol 24:1898–1908

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors want to thank Katri Kärkkäinen from the Finnish Forest Research Institute for providing seed material for most of the populations. The samples from Kaddekielas, Sweden, and Usinsk, Russia were kindly provided by Torgny Pärsson (Skogforsk, Sweden), the Italian sample by Giovanni Vendramin (National Research Council, Plant Genetic Institute, Italy) and Latvian sample by Aris Jansons (Latvian State Forestry Research Institute, Latvia). We would also like to thank Soile Alatalo, Hannele Parkkinen, Janita Ranta, and Katja Salminen for the laboratory work, Jaakko Tyrmi for helping with sequence submissions, and Stéphane De Mita for helping with ABC. We are also grateful to Martin Lascoux for the discussion on demographic inference. This research was supported by the EU Network of Excellence EVOLTREE (FP6 016322), the EU project NOVELTREE (FP7 211868), and Biocenter Oulu, Finland.

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Authors and Affiliations

  1. Department of Biology, University of Oulu, P.O. Box 3000, FIN-90014, Oulu, Finland

    Sonja T. Kujala & Outi Savolainen

  2. Biocenter Oulu, University of Oulu, Oulu, Finland

    Sonja T. Kujala & Outi Savolainen

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  1. Sonja T. Kujala
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  2. Outi Savolainen
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Correspondence to Sonja T. Kujala.

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Communicated by P. Ingvarsson

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Kujala, S.T., Savolainen, O. Sequence variation patterns along a latitudinal cline in Scots pine (Pinus sylvestris): signs of clinal adaptation?. Tree Genetics & Genomes 8, 1451–1467 (2012). https://doi.org/10.1007/s11295-012-0532-5

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  • DOI: https://doi.org/10.1007/s11295-012-0532-5

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