Tree Genetics & Genomes

, Volume 10, Issue 4, pp 1015–1025

High genetic similarity between Polish and North European Scots pine (Pinus sylvestris L.) populations at nuclear gene loci

  • Witold Wachowiak
  • Błażej Wόjkiewicz
  • Stephen Cavers
  • Andrzej Lewandowski
Original Paper

Abstract

Nucleotide polymorphisms in a set of 32 nuclear genes were studied in 19 mountain, peatbog and lowland populations of Scots pine representing known phenotypic races and populations of presumably relict character for the species in Poland. At 29 genes, the pattern of genetic variation was compared to 11 reference populations from Northern, Western and Southern Europe. Similar levels of nucleotide polymorphism and excess of low-frequency mutations were observed in Polish populations (πtot = 0.0055, D = −0.308) and as compared to the reference samples (πtot = 0.0054, D = −0.170). Bayesian assignment and conventional frequency-based statistics indicate that Polish populations share the same genetic background at the analysed nuclear gene markers. However, the populations showed a much closer genetic relationship with North European samples than other regional groups of populations. Across the very uniform genetic background of the populations, we identified several genes with outlier patterns of haplotype, polymorphism frequency variation and departures from compound neutrality tests. Our data indicate that the Central and North European parts of the Scots pine distribution seem particularly suitable for association genetic studies to link phenotypic and genetic variation at a large geographical scale.

Keywords

Nucleotide polymorphisms Population structure Natural selection Recolonization 

Supplementary material

11295_2014_739_MOESM1_ESM.pdf (470 kb)
ESM 1(PDF 469 kb)

References

  1. Achaz G (2009) Frequency spectrum neutrality tests: one for all and all for one. Genetics 183(1):249–258. doi:10.1534/genetics.109.104042 PubMedCentralPubMedCrossRefGoogle Scholar
  2. 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(3):1309–1321PubMedCentralPubMedGoogle Scholar
  3. Blarquez O, Carcaillet C, Bremond L, Mourier B, Radakovitch O (2010) Trees in the subalpine belt since 11 700 cal. BP: origin, expansion and alteration of the modern forest. The Holocene 20(1):139–146CrossRefGoogle Scholar
  4. Boratyński A (1993) Systematics and geographical distribution. In: Biology of Scots pine. Edit Białobok S, Boratyński A, Bugała W (in Polish) Sorus, Poznań, KórnikGoogle Scholar
  5. Burczyk J, Dzialuk A, Lewandowski A (2000) Genetic variability of Scots pine (Pinus sylvestris L.) on the seed orchard in Gniewkowo (in Polish). Sylwan CXLIV (7): 65–74Google Scholar
  6. Cheddadi R, Vendramin G, Litt T, François L, Kageyama M, Lorentz S, Laurent J, Beaulieu J, Sadori L, Jost A, Lunt D (2006) Imprints of glacial refugia in the modern genetic diversity of Pinus sylvestris. Glob Ecol Biogeogr 15:271–282CrossRefGoogle Scholar
  7. Corander J, Tang J (2007) Bayesian analysis of population structure based on linked molecular information. Math Biosci 205(1):19–31PubMedCrossRefGoogle Scholar
  8. Derory J, Scotti-Saintagne C, Bertocchi E, Le Dantec L, Graignic N, Jauffres A, Casasoli M, Chancerel E, Bodenes 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(5):438–448PubMedCrossRefGoogle Scholar
  9. Dvornyk V, Sirvio A, Mikkonen M, Savolainen O (2002) Low nucleotide diversity at the pal1 locus in the widely distributed Pinus sylvestris. Mol Biol Evol 19(2):179–188PubMedCrossRefGoogle Scholar
  10. Eckert AJ, Bower AD, Wegrzyn JL, Pande B, Jermstad KD, Krutovsky KV, St. Clair JB, Neale DB (2009) Association genetics of coastal Douglas fir (Pseudotsuga menziesii var. menziesii, Pinaceae). I. Cold-hardiness related traits. Genetics 182(4):1289–1302PubMedCentralPubMedCrossRefGoogle Scholar
  11. Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13(4):853–864PubMedCrossRefGoogle Scholar
  12. 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(3):564–567PubMedCrossRefGoogle Scholar
  13. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinformatics Online 1:47–50Google Scholar
  14. Garcia-Gil MR, Mikkonen M, Savolainen O (2003) Nucleotide diversity at two phytochrome loci along a latitudinal cline in Pinus sylvestris. Mol Ecol 12(5):1195–1206PubMedCrossRefGoogle Scholar
  15. Giertych M, Oleksyn J (1992) Studies on genetic variation in Scots pine (Pinus sylvestris L.) coordinated by IUFRO. Silvae Genet 41(3):133–143Google Scholar
  16. González-Martinez SC, Wheeler NC, Ersoz E, Nelson CD, Neale DB (2007) Association genetics in Pinus taeda L. I. Wood property traits. Genetics 175(1):399–409PubMedCentralPubMedCrossRefGoogle Scholar
  17. Hill WG, Robertson A (1968) Linkage disequilibrium in finite populations. Theor Appl Genet 38:226–231PubMedCrossRefGoogle Scholar
  18. 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(12):1247–1266CrossRefGoogle Scholar
  19. Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155(4):2011–2014PubMedCentralPubMedGoogle Scholar
  20. Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116(1):153–159PubMedCentralPubMedGoogle Scholar
  21. Hudson RR, Boos DD, Kaplan NL (1992) A statistical test for detecting geographic subdivision. Mol Biol Evol 9(1):138–151PubMedGoogle Scholar
  22. Hurme P, Repo T, Savolainen O, Paakkonen T (1997) Climatic adaptation of bud set and frost hardiness in Scots pine (Pinus sylvestris). Can J For Res 27(5):716–723Google Scholar
  23. Ingvarsson PK, Garcia 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(3):1845–1853PubMedCentralPubMedCrossRefGoogle Scholar
  24. 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(1–2):215–221PubMedCrossRefGoogle Scholar
  25. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7(12):1225–1241CrossRefGoogle Scholar
  26. Kinloch BB, Parks GK, Fowler CW (1970) White pine blister rust: simply inherited resistance in sugar pine. Science 167(3915):193–195. doi:10.1126/science.167.3915.193 PubMedCrossRefGoogle Scholar
  27. Krakau U-K, Liesebach M, Aronen T, Lelu-Walter M-A, Schneck V (2013) Scots pine (Pinus sylvestris L.). In: Pâques LE (ed) Forest tree breeding in Europe, vol 25. Managing forest ecosystems. Springer, Netherlands, pp 267–323CrossRefGoogle Scholar
  28. Kujala S, Savolainen O (2012) Sequence variation patterns along a latitudinal cline in Scots pine (Pinus sylvestris): signs of clinal adaptation? Tree Genet Genome 8(6):1451–1467CrossRefGoogle Scholar
  29. Latta RG (2004) Relating processes to patterns of genetic variation across landscapes. For Ecol Manag 197(1–3):91–102CrossRefGoogle Scholar
  30. Le Corre V, Kremer A (2003) Genetic variability at neutral markers, quantitative trait loci and trait in a subdivided population under selection. Genetics 164(3):1205–1219PubMedCentralPubMedGoogle Scholar
  31. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452PubMedCrossRefGoogle Scholar
  32. Lynch M, Crease TJ (1990) The analysis of population survey data on DNA sequence variation. Mol Biol Evol 7(4):377–394PubMedGoogle Scholar
  33. 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(1):233PubMedCentralPubMedCrossRefGoogle Scholar
  34. Neale DB, Ingvarsson PK (2008) Population, quantitative and comparative genomics of adaptation in forest trees. Curr Opin Plant Biol 11(2):149–155. doi:10.1016/j.pbi.2007.12.004 PubMedCrossRefGoogle Scholar
  35. Neale DB, Kremer A (2011) Forest tree genomics: growing resources and applications. Nat Rev Genet 12(2):111–122PubMedCrossRefGoogle Scholar
  36. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  37. Oleksyn J, Tjoelker MG, Reich PB (1992) Growth and biomass partitioning of populations of European Pinus sylvestris L. under simulated 50° and 60° N daylengths: evidence for photoperiodic ecotypes. New Phytol 120(4):561–574CrossRefGoogle Scholar
  38. Parducci L, Jørgensen T, Tollefsrud MM, Elverland E, Alm T, Fontana SL, Bennett KD, Haile J, Matetovici I, Suyama Y, Edwards ME, Andersen K, Rasmussen M, Boessenkool S, Coissac E, Brochmann C, Taberlet P, Houmark-Nielsen M, Larsen NK, Orlando L, Gilbert MTP, Kjær KH, Alsos IG, Willerslev E (2012) Glacial survival of boreal trees in northern Scandinavia. Science 335(6072):1083–1086PubMedCrossRefGoogle Scholar
  39. Petit RJ, Aguinagalde I, de Beaulieu J-L, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Muller-Starck G, Demesure-Musch B, Palme A, Martin JP, Rendell S, Vendramin GG (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300(5625):1563–1565PubMedCrossRefGoogle Scholar
  40. Prus-Glowacki W, Urbaniak L, Bujas E, Curtu AL (2012) Genetic variation of isolated and peripheral populations of Pinus sylvestris (L.) from glacial refugia. Flora 207(2):150–158CrossRefGoogle Scholar
  41. Pyhäjärvi T, Garcia-Gil MR, Knürr T, Mikkonen M, Wachowiak W, Savolainen O (2007) Demographic history has influenced nucleotide diversity in European Pinus sylvestris populations. Genetics 177(3):1713–1724PubMedCentralPubMedCrossRefGoogle Scholar
  42. Pyhäjärvi T, Salmela MJ, Savolainen O (2008) Colonization routes of Pinus sylvestris inferred from distribution of mitochondrial DNA variation. Tree Genet Genome 4(2):247–254CrossRefGoogle Scholar
  43. Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20(1):76–86. doi:10.1093/molbev/msg009 PubMedCrossRefGoogle Scholar
  44. Sabor J (2006) Intraspecific variability of forest trees. Scots pine and Norway spruce. In: The elements of genetics and selective breeding of forest trees. Edi Sabor J (in polish) Wyd CILP, WarszawaGoogle Scholar
  45. Salmela MJ, Cavers S, Cottrell JE, Iason GR, Ennos RA (2013) Spring phenology shows genetic variation among and within populations in seedlings of Scots pine (Pinus sylvestris L.) in the Scottish Highlands. Plant Ecol Divers 6(3–4):523–536CrossRefGoogle Scholar
  46. Savolainen O, Pyhäjärvi T (2007) Genomic diversity in forest trees. Curr Opin Plant Biol 10(2):162–167PubMedCrossRefGoogle Scholar
  47. Savolainen O, Pyhäjärvi T, Knürr T (2007) Gene flow and local adaptation in trees. Annu Rev Ecol Evol Syst 38(1):595–619CrossRefGoogle Scholar
  48. 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(9):1205–1211PubMedCrossRefGoogle Scholar
  49. Tajima F (1989) Statistical-method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595PubMedCentralPubMedGoogle Scholar
  50. Wachowiak W, Prus-Głowacki W (2008) Hybridisation processes in sympatric populations of pines Pinus sylvestris L., P. mugo Turra and P. uliginosa Neumann. Plant Syst Evol 271(1):29–40CrossRefGoogle Scholar
  51. Wachowiak W, Balk P, 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 Genome 5(1):117–132CrossRefGoogle Scholar
  52. Wachowiak W, Salmela MJ, Ennos RA, Iason G, Cavers S (2010) High genetic diversity at the extreme range edge: nucleotide variation at nuclear loci in Scots pine (Pinus sylvestris L.) in Scotland. Heredity 106:775–787PubMedCentralPubMedCrossRefGoogle Scholar
  53. Wachowiak W, Palme AE, Savolainen O (2011) Speciation history of three closely related pines Pinus mugo (T.), P. uliginosa (N.) and P. sylvestris (L.). Mol Ecol 20(8):1729–1743PubMedCrossRefGoogle Scholar
  54. Wachowiak W, Boratyńska K, Cavers S (2013a) Geographical patterns of nucleotide diversity and population differentiation in three closely related European pine species in the Pinus mugo complex. Bot J Linn Soc 172(2):225–238CrossRefGoogle Scholar
  55. Wachowiak W, Iason GR, Cavers S (2013b) Among population differentiation at nuclear genes in native Scots pine (Pinus sylvestris L.) in Scotland. Flora 208(2):79–86Google Scholar
  56. Wang XR, Szmidt AE, Lindgren D (1991) Allozyme differentiation among populations of Pinus sylvestris L. from Sweden and China. Hereditas 114(3):219–226CrossRefGoogle Scholar
  57. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38(6):1358–1370CrossRefGoogle Scholar
  58. 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(23–24):2369–2387CrossRefGoogle Scholar
  59. Wright SI, Andolfatto P (2008) The impact of natural selection on the genome: emerging patterns in Drosophila and Arabidopsis. Annu Rev Ecol Evol Syst 39(1):193–213CrossRefGoogle Scholar
  60. Wright SI, Gaut BS (2005) Molecular population genetics and the search for adaptive evolution in plants. Mol Biol Evol 22(3):506–519PubMedCrossRefGoogle Scholar
  61. Zeng K, Shi S, Wu C-I (2007) Compound tests for the detection of hitchhiking under positive selection. Mol Biol Evol 24(8):1898–1908PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Witold Wachowiak
    • 1
    • 2
    • 3
  • Błażej Wόjkiewicz
    • 2
  • Stephen Cavers
    • 3
  • Andrzej Lewandowski
    • 2
  1. 1.Institute of Environmental Biology, Faculty of BiologyAdam Mickiewicz UniversityPoznańPoland
  2. 2.Institute of DendrologyPolish Academy of SciencesKórnikPoland
  3. 3.Centre for Ecology and Hydrology EdinburghMidlothianUK

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