Advertisement

Tree Genetics & Genomes

, Volume 8, Issue 6, pp 1451–1467 | Cite as

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

  • Sonja T. KujalaEmail author
  • Outi Savolainen
Original Paper

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.

Keywords

Cline Demography Pinus sylvestris Selection Sequence variation 

Notes

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.

Supplementary material

11295_2012_532_MOESM1_ESM.docx (5.4 mb)
ESM 1 (DOCX 5.40 mb)

References

  1. Aho ML (1994) Autumn frost hardening of one-year-old Pinus sylvestris (L.) seedlings: effect of origin and parent trees. Scand J For Res 9:17–24CrossRefGoogle Scholar
  2. Barton NH (1999) Clines in polygenic traits. Genet Res 74:223–236PubMedCrossRefGoogle Scholar
  3. Beaumont MA, Zhang W, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035PubMedGoogle Scholar
  4. Bennett KD, Tzedakis PC, Willis KJ (1991) Quaternary refugia of North European trees. J Biogeogr 18:103–115CrossRefGoogle Scholar
  5. 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 19:2609–2625PubMedCrossRefGoogle Scholar
  6. Biswas S, Akey JM (2006) Genomic insights into positive selection. Trends Genet 22:437–446PubMedCrossRefGoogle Scholar
  7. Bridle JR, Polechová J, Kawata M, Butlin RK (2010) Why is adaptation prevented at ecological margins? New insights from individual-based simulations. Ecol Lett 13:485–494PubMedCrossRefGoogle Scholar
  8. 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 101:15255–15260PubMedCrossRefGoogle Scholar
  9. 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 102:13939–13943PubMedCrossRefGoogle Scholar
  10. 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 15:271–282Google Scholar
  11. 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 60:107–124CrossRefGoogle Scholar
  12. Chevin LM, Hospital F (2008) Selective sweep at a quantitative trait locus in the presence of background genetic variation. Genetics 180:1645–1660PubMedCrossRefGoogle Scholar
  13. Close TJ (1997) Dehydrins: a commonalty in the response of plants to dehydration and low temperature. Physiol Plant 100:291–296CrossRefGoogle Scholar
  14. Costa R, Peixoto AA, Barbujani G, Kyriacou CP (1992) A latitudinal cline in a Drosophila clock gene. Proc R Soc of Lond B 250:43–49CrossRefGoogle Scholar
  15. Csilléry K, Blum MGB, Gaggiotti OE, François O (2010) Approximate Bayesian computation (ABC) in practice. Trends Ecol Evol 25:410–418PubMedCrossRefGoogle Scholar
  16. 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 19:1638–1650CrossRefGoogle Scholar
  17. 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 177:2123–2133PubMedCrossRefGoogle Scholar
  18. Depaulis F, Mousset S, Veuille M (2003) Power of neutrality test to detect bottlenecks and hitchhiking. J Mol Evol 57:S190–S200PubMedCrossRefGoogle Scholar
  19. 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 104:438–448PubMedCrossRefGoogle Scholar
  20. 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 398–407Google Scholar
  21. 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 53:775–782CrossRefGoogle Scholar
  22. 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 19:179–188PubMedCrossRefGoogle Scholar
  23. 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 183:289–298PubMedCrossRefGoogle Scholar
  24. 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 19:3789–3805PubMedCrossRefGoogle Scholar
  25. 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 185:969–982PubMedCrossRefGoogle Scholar
  26. Endler JA (1977) Geographic variation, speciation, and clines. Princeton University Press, PrincetonGoogle Scholar
  27. Espartero J, Pintor-Toro J, Pardo J (1994) Differential accumulation of s-adenosylmethionine synthetase transcripts in response to salt stress. Plant Mol Biol 25:217–227PubMedCrossRefGoogle Scholar
  28. 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 25:417–437PubMedCrossRefGoogle Scholar
  29. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  30. Excoffier L, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40:481–501CrossRefGoogle Scholar
  31. Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993PubMedCrossRefGoogle Scholar
  32. François O, Blum MGB, Jakobsson M, Rosenberg NA (2008) Demographic history of European populations of Arabidopsis thaliana. PLoS Genet 4:e1000075PubMedCrossRefGoogle Scholar
  33. Franklin KA, Quail PH (2010) Phytochrome functions in Arabidopsis development. J Exp Bot 61:11–24PubMedCrossRefGoogle Scholar
  34. García-Gil MR, Mikkonen M, Savolainen O (2003) Nucleotide diversity at two phytochrome loci along a latitudinal cline in Pinus sylvestris. Mol Ecol 12:1195–1206PubMedCrossRefGoogle Scholar
  35. 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 165:1269–1278PubMedGoogle Scholar
  36. González-Martínez SC, Huber D, Ersoz E, Davis JM, Neale DB (2008) Association genetics in Pinus taeda L. II. Carbon isotope discrimination. Heredity 101:19–26PubMedCrossRefGoogle Scholar
  37. 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 27:1822–1832CrossRefGoogle Scholar
  38. 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 28:101–116PubMedCrossRefGoogle Scholar
  39. 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 144:248–257PubMedCrossRefGoogle Scholar
  40. Hahn MW (2008) Toward a selection theory of molecular evolution. Evolution 62:255–265PubMedCrossRefGoogle Scholar
  41. 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 61:2849–2860PubMedCrossRefGoogle Scholar
  42. Hall D, Ma XF, Ingvarsson PK (2011) Adaptive evolution of the Populus tremula photoperiod pathway. Mol Ecol 20:1463–1474PubMedCrossRefGoogle Scholar
  43. Hayama R, Coupland G (2003) Shedding light on the circadian clock and the photoperiodic control of flowering. Curr Opinion in Plant Biol 6:13–19CrossRefGoogle Scholar
  44. Hedrick PW (2006) Genetic polymorphism in heterogeneous environments: the age of genomics. Annu Rev Ecol Evol Syst 37:67–93CrossRefGoogle Scholar
  45. Hedrick PW, Ginevan ME, Ewing EP (1976) Genetic polymorphism in heterogeneous environments. Annu Rev Ecol Syst 7:1–32CrossRefGoogle Scholar
  46. 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 331:920–924PubMedCrossRefGoogle Scholar
  47. 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 174:2095–2105PubMedCrossRefGoogle Scholar
  48. Hill WG, Robertson AV (1968) Linkage disequilibrium in finite populations. Theor Appl Genet 38:226–231CrossRefGoogle Scholar
  49. Hill WG, Weir BS (1988) Variances and covariances of squared linkage disequilibria in finite populations. Theor Popul Biol 33:54–78PubMedCrossRefGoogle Scholar
  50. 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 171:1059–1071PubMedCrossRefGoogle Scholar
  51. 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 47:105–115PubMedCrossRefGoogle Scholar
  52. 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 188:501–514PubMedCrossRefGoogle Scholar
  53. Holliday JA, Yuen M, Ritland K, Aitken S (2010b) Postglacial history of a widespread conifer produces inverse clines in selective neutrality tests. Mol Ecol 19:3857–3864PubMedCrossRefGoogle Scholar
  54. Hudson RR (2001) Two-locus sampling distributions and their application. Genetics 159:1805–1817PubMedGoogle Scholar
  55. Hudson RR, Kreitman M, Aguadé M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159PubMedGoogle Scholar
  56. Huntley B, Birks HJB (1983) An atlas of past and present pollen maps for Europe 0–13 000 years ago. Cambridge University Press, CambridgeGoogle Scholar
  57. 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 27:716–723CrossRefGoogle Scholar
  58. 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 156:1309–1322PubMedGoogle Scholar
  59. Ingvarsson PK (2008) Multilocus patterns of nucleotide polymorphism and the demographic history of Populus tremula. Genetics 180:329–340PubMedCrossRefGoogle Scholar
  60. 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 172:1845–1853PubMedCrossRefGoogle Scholar
  61. 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 178:2217–2226PubMedCrossRefGoogle Scholar
  62. 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 10:22PubMedCrossRefGoogle Scholar
  63. Jesus FF, Wilkins JF, Solferini VN, Wakeley J (2006) Expected coalescence times and segregating sites in a model of glacial cycles. Genet Mol Res 5:466–474PubMedGoogle Scholar
  64. 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 93:215–221CrossRefGoogle Scholar
  65. 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 156:1967–1977PubMedCrossRefGoogle Scholar
  66. 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 183:678–690PubMedCrossRefGoogle Scholar
  67. 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 188:941–952PubMedCrossRefGoogle Scholar
  68. Kelly JK (2006) Geographical variation in selection, from phenotypes to molecules. Am Nat 167:481–495PubMedCrossRefGoogle Scholar
  69. 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 449:356–362PubMedCrossRefGoogle Scholar
  70. Kremer A, Le Corre V (2012) Decoupling of differentiation between traits and their underlying genes in response to divergent selection. Heredity 108:375–385Google Scholar
  71. 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 156:75–87CrossRefGoogle Scholar
  72. Latta RG (1998) Differentiation of allelic frequencies at quantitative trait loci affecting locally adaptive traits. Am Nat 151:283–292PubMedCrossRefGoogle Scholar
  73. Le Corre V, Kremer A (2003) Genetic variability at neutral markers, quantitative trait loci and trait in a subdivided population under selection. Genetics 164:1205–1219PubMedGoogle Scholar
  74. Lepoittevin C (2009) Association genetics in maritime pine (Pinus pinaster Ait.) for growth and wood quality traits. Dissertation, University of BordeauxGoogle Scholar
  75. Lewontin RC, Krakauer J (1973) Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics 74:175–195PubMedGoogle Scholar
  76. Li Q-H, Yang H-Q (2007) Cryptochrome signaling in plants. Photochem Photobiol 83:94–101PubMedCrossRefGoogle Scholar
  77. 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 27:1001–1014PubMedCrossRefGoogle Scholar
  78. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452PubMedCrossRefGoogle Scholar
  79. 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 4:279–292CrossRefGoogle Scholar
  80. 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 186:1033–1044PubMedCrossRefGoogle Scholar
  81. Más P, Yanovsky MJ (2009) Time for circadian rhythms: plants get synchronized. Curr Opinion in Plant BiolGoogle Scholar
  82. Maynard Smith J, Haigh J (1974) The hitch-hiking effect of a favorable gene. Genet Res 23:23–35CrossRefGoogle Scholar
  83. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654PubMedCrossRefGoogle Scholar
  84. McVean G, Awadalla P, Fearnhead P (2002) A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160:1231–1241PubMedGoogle Scholar
  85. Mikola J (1982) Bud-set phenology as an indicator of climatic adaptation of Scots pine in Finland. Silvae Fenn 16:178–184Google Scholar
  86. Mirov N (1967) The genus Pinus. Ronald Press, New YorkGoogle Scholar
  87. Moeller DA, Tiffin P (2008) Geographic variation in adaptation at the molecular level: a case study of plant immunity genes. Evolution 62:3069–3081PubMedCrossRefGoogle Scholar
  88. 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 190:1145–1148Google Scholar
  89. 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 59:235–245CrossRefGoogle Scholar
  90. 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 70:371–386PubMedCrossRefGoogle Scholar
  91. 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 7:233PubMedCrossRefGoogle Scholar
  92. Nicholas KB, Nicholas HB Jr, Deerfield DW II (1997) GeneDoc: analysis and visualization of genetic variation. EMBNEW NEWS 4:14Google Scholar
  93. Nordborg M, Innan H (2003) The genealogy of sequences containing multiple sites subject to strong selection in a subdivided population. Genetics 163:1201–1213PubMedGoogle Scholar
  94. 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 30:190–193PubMedCrossRefGoogle Scholar
  95. Nordborg M, Hu TT, Ishino Y et al (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3:1289–1299CrossRefGoogle Scholar
  96. 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 37:540–551CrossRefGoogle Scholar
  97. 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 36:86–96CrossRefGoogle Scholar
  98. 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 25:2567–2577PubMedCrossRefGoogle Scholar
  99. Palmé AE, Pyhäjärvi T, Wachowiak W, Savolainen O (2009) Selection on nuclear genes in a Pinus phylogeny. Mol Biol Evol 26:893–905PubMedCrossRefGoogle Scholar
  100. 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 66:205–214Google Scholar
  101. 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 108:273–284Google Scholar
  102. Przeworski M (2002) The signature of positive selection at randomly chosen loci. Genetics 160:1179–1189PubMedGoogle Scholar
  103. 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 177:1713–1724PubMedCrossRefGoogle Scholar
  104. Pyhäjärvi T, Salmela MJ, Savolainen O (2008) Colonization routes of Pinus sylvestris inferred from distribution of mitochondrial DNA variation. Tree Genet Genom 4:247–254CrossRefGoogle Scholar
  105. 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 7:385–397CrossRefGoogle Scholar
  106. Sabeti PC, Reich DE, Higgins JM et al (2002) Detecting recent positive selection in the human genome from haplotype structure. Nature 419:832–837PubMedCrossRefGoogle Scholar
  107. 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 128:377–386CrossRefGoogle Scholar
  108. 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 168:923–931PubMedCrossRefGoogle Scholar
  109. 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 9:1205–1211PubMedCrossRefGoogle Scholar
  110. Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100:9440–9445PubMedCrossRefGoogle Scholar
  111. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  112. 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 25:4876–4882PubMedCrossRefGoogle Scholar
  113. Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034PubMedCrossRefGoogle Scholar
  114. 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 25:101–108PubMedCrossRefGoogle Scholar
  115. 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 5:117–132CrossRefGoogle Scholar
  116. 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 106:775–787PubMedCrossRefGoogle Scholar
  117. Willis KJ, van Andel TH (2004) Trees or no trees? The environments of central and eastern Europe during the Last Glaciation. Quat Sci Rev 23:2369–2387CrossRefGoogle Scholar
  118. Zeng K, Fu YX, Shi S, Wu CI (2006) Statistical tests for detecting positive selection by utilizing high-frequency variants. Genetics 174:1431–1439PubMedCrossRefGoogle Scholar
  119. Zeng K, Shi S, Wu CI (2007) Compound tests for the detection of hitchhiking under positive selection. Mol Biol Evol 24:1898–1908PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.Department of BiologyUniversity of OuluOuluFinland
  2. 2.Biocenter OuluUniversity of OuluOuluFinland

Personalised recommendations