, Volume 145, Issue 2, pp 209–221 | Cite as

Genetic structure of a regionally endangered orchid, the dark red helleborine (Epipactis atrorubens) at the edge of its distribution

  • Hilde HensEmail author
  • Anne Jäkäläniemi
  • Kadri Tali
  • Petr Efimov
  • Alexey V. Kravchenko
  • Laura Kvist
Original Paper


The genetic structure and diversity of species is determined by both current population dynamics and historical processes. Population genetic structure at the edge of the distribution is often expected to differ substantially from populations at the centre, as these edge populations are often small and fragmented. In addition, populations located in regions that have experienced repeated glaciations throughout the Pleistocene, may still carry imprints from the genetic consequences of frequent distribution shifts. Using chloroplast DNA sequences and nuclear microsatellite markers we studied the genetic structure of Epipactis atrorubens at the northern edge of its distribution. Contrary to populations in the centre of the distribution, populations at the northern range are regionally endangered as they are small and disjunct. Sequence data of 2 chloroplast loci and allelic data from 6 nuclear microsatellite markers were obtained from 297 samples from Finland, Estonia and Russia. We sought for genetic indicators of past population processes, such as post-glacial colonisation history of E. atrorubens. As expected, we observed low genetic variation, in terms of numbers of substitutions, haplotypes and alleles, and significant levels of differentiation, especially pronounced in the chloroplast DNA. These features suggest that the edge populations could be prone to extinction.


Genetic diversity Microsatellites Population differentiation rbcL-accD intergenic spacer trnK 



This work was supported by the Thule Institute and the Department of Biology of the University of Oulu. We would like to thank M. Mutanen and J. Hautaluoma for helping with the collection of the samples. The permits for sample collection in Finland: LAPELY/348/07.01/2011, POPELY/568/07.01/2011, POPELY/50/07.02/2013.

Supplementary material

10709_2017_9959_MOESM1_ESM.docx (32 kb)
Supplementary material 1 (DOCX 32 KB)


  1. Anderberg AA (2001) Epipactis atrorubens. Naturhistoriska riksmuseet. Accessed 23 Sep 2015
  2. Anthos (2010) Information system of the plants of Spain. Real Jardín Botánico, CSIC. Fundación Biodiversidad. Accessed 8 Aug 2016
  3. Arditti J, Ghani AKA (2000) Tansley Review No. 110. Numerical and physical properties of orchid seeds and their biological implications. New Phytol 145:367–421CrossRefGoogle Scholar
  4. ArtDatabanken (2016) The Swedish Species Information Centre. Accessed 8 Aug 2016
  5. Batty AL, Dixon KW, Brundrett M, Sivasithamparam K (2001) Constraints to symbiotic germination of terrestrial orchid seed in a mediterranean bushland. New Phytol 152:511–520CrossRefGoogle Scholar
  6. BfN (2016) FloraWeb Daten und Informationen zu Wildpflanzen und zur Vegetation Deutschlands. Cited 08 June 2016 (in German)
  7. Bidartondo MI, Read DJ (2008) Fungal specificity bottlenecks during orchid germination and development. Mol Ecol 17:3707–3716PubMedGoogle Scholar
  8. Bilz M, Kell SP, Maxted N, Lansdown RV (2011) European red list of vascular plants. Publications Office of the European Union, LuxembourgGoogle Scholar
  9. Birky CW, Fuerst P, Maruyama T (1989) Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics 121:613–627PubMedGoogle Scholar
  10. Brown JH (1984) On the relationship between abundance and distribution of species. Am Nat 124:255–279CrossRefGoogle Scholar
  11. Brussard PF (1984) Geographic patterns and environmental gradients: the central-marginal model in Drosophila revisited. Annu Rev Ecol Syst 15:25–64CrossRefGoogle Scholar
  12. Brzosko E, Tałałaj I, Wróblewska A (2006) Genetic structure of rare Epipactis atrorubens populations from two national parks in Northeast Poland. Polish Bot Studies 22:71–80Google Scholar
  13. BSBI, BRC (2008) Online atlas of the British and Irish flora. Accessed 8 Aug 2016
  14. Chung MY (2009) Lack of allozyme diversity in populations of the rare, endangered terrestrial orchids Tipularia japonica and Epipactis papillosa in Korea. Plant Syst Evol 278:203. doi: 10.1007/s00606-008-0140-x CrossRefGoogle Scholar
  15. Chung MY, Chung MG (2007) Extremely low levels of genetic diversity in the terrestrial orchid Epipactis thunbergii (Orchidaceae) in South Korea: implications for conservation. Bot J Linn Soc 155:161–169CrossRefGoogle Scholar
  16. Chung MY, Nason JD, Chung MG (2004) Spatial genetic structure in populations of the terrestrial orchid Cephalanthera longibracteata (Orchidaceae). Am J Bot 91:52–57CrossRefPubMedGoogle Scholar
  17. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefPubMedGoogle Scholar
  18. ČNFD (2016) České národní fytocenologické database. Ústavem botaniky a zoologie Přírodovědecké fakulty Masarykovy university. Accessed 8 Aug 2016
  19. Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10:556–557CrossRefPubMedGoogle Scholar
  20. CRSF, ZDSF (2012) Info Flora: Das nationale Daten-und Informationszentrum der Schweizer Flora. Chambésy. Accessed 8 Aug 2016 (in German)
  21. Davies P, Davies J, Huxley A (1983) Wild orchids of Britain and Europe. Chatto and Windus. The Hogarth Press, LondonGoogle Scholar
  22. DGRNE (2016) L’Observatoire de la Faune, de la Flore et des Habitats en Wallonie. Accessed 8 Aug 2016 (in French)
  23. Didukh YP (ed) (2009) Червона книга Украïни. Рослинний свiт. The red Book of Ukraine. Flora. National Academy of Sciences of Ukraine (in ​Ukraine) Google Scholar
  24. Diez JM (2007) Hierarchical patterns of symbiotic orchid germination linked to adult proximity and environmental gradients. J Ecol 95:159–170CrossRefGoogle Scholar
  25. Doyle JJ (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  26. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581CrossRefPubMedGoogle Scholar
  27. Durka W (1999) Genetic diversity in peripheral and subcentral populations of Corrigiola litoralis L. (Illecebraceae). Heredity 83:476–484CrossRefPubMedGoogle Scholar
  28. Dusak F, Prat D (2010) Atlas des orchidees de France. Editions Biotope, collection Parthénope, Publications scientifiques du MuséumGoogle Scholar
  29. Earl D, vonHoldt B (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  30. Eckert CG, Samis KE, Lougheed SG (2008) Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Mol Ecol 17:1170–1188CrossRefPubMedGoogle Scholar
  31. Eckstein RL, O’Neill R, Danihelka J, Otte A, Köhler W (2006) Genetic structure among and within peripheral and central populations of three endangered floodplain violets. Mol Ecol 15:2367–2379CrossRefPubMedGoogle Scholar
  32. Efimov P (2004) Genus Epipactis ZINN (Orchidaceae) in the Russia. Turczaninowia 7:8–42 (in Russian) Google Scholar
  33. Ehlers BK, Pedersen H (2000) Genetic variation in three species of Epipactis (Orchidaceae): geographic scale and evolutionary inferences. Biol J Linn Soc 69:411–430CrossRefGoogle Scholar
  34. Euro + Med (2011) Euro + Med Plantbase The information resource for Euro-Mediterranean plant diversity. Botanic Garden and Botanical Museum, Berlin. Accessed 8 Aug 2016
  35. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  36. 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 10:564–567CrossRefPubMedGoogle Scholar
  37. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  38. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedPubMedCentralGoogle Scholar
  39. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedPubMedCentralGoogle Scholar
  40. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318CrossRefPubMedGoogle Scholar
  41. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Updated from Goudet (1995)
  42. Govindaraju DR (1988) Relationship between dispersal ability and levels of gene flow in plants. Oikos 52:31–35CrossRefGoogle Scholar
  43. Gustafsson S (2000) Patterns of genetic variation in Gymnadenia conopsea, the fragrant orchid. Mol Ecol 9:1863–1872CrossRefPubMedGoogle Scholar
  44. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symp 41:95–98Google Scholar
  45. Hardy OJ, Vekemans X (2002) spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620CrossRefGoogle Scholar
  46. Hardy OJ, Charbonnel N, Fréville H, Heuertz M (2003) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482PubMedPubMedCentralGoogle Scholar
  47. Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600PubMedGoogle Scholar
  48. Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276CrossRefGoogle Scholar
  49. Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112CrossRefGoogle Scholar
  50. Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913CrossRefPubMedGoogle Scholar
  51. Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans R Soc B 359:183–195CrossRefGoogle Scholar
  52. Hollingsworth PM, Dickson JH (1997) Genetic variation in rural and urban populations of Epipactis helleborine (L) Crantz. (Orchidaceae) in Britain. Bot J Linn Soc 123:321–331Google Scholar
  53. Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evol Int J Org Evol 53:1898–1914CrossRefGoogle Scholar
  54. Ivanter EV, Kuznetsov OL (eds) (2007) Red Data Book of the Republic of Karelia. Petrozavodsk, Karelija, p 368 (in Russian)Google Scholar
  55. Jaarola M, Tegelström H (1995) Colonization history of north European field voles (Microtus agrestis) revealed by mitochondrial DNA. Mol Ecol 4:299–310CrossRefPubMedGoogle Scholar
  56. Jäkäläniemi A, Crone EE, Närhi P, Tuomi J (2011) Orchids do not pay costs at emergence for prolonged dormancy. Ecology 92:1538–1543CrossRefPubMedGoogle Scholar
  57. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806CrossRefPubMedGoogle Scholar
  58. Jakubska-Busse A, Kadej M (2011) The pollination of Epipactis Zinn, 1757 (Orchidaceae) species in Central Europe—the significance of chemical attractants, floral morphology and concomitant insects. Acta Soc Bot Polon 80:49–57CrossRefGoogle Scholar
  59. Jersáková J, Malinová T (2007) Spatial aspects of seed dispersal and seedling recruitment in orchids. New Phytol 176:237–241CrossRefPubMedGoogle Scholar
  60. Johnson LA, Soltis DE (1994) matK DNA sequences and phylogenetic reconstruction in Saxifragaceae s. str. Syst Bot 19:143–156CrossRefGoogle Scholar
  61. Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026CrossRefPubMedGoogle Scholar
  62. Julve Ph (ed) (2016) Listes départementales des plantes de France. Version 2015.08 du 30 août 2015. Programme chorologie départementale de tela-botanica. Accessed 8 Aug 2016
  63. Kålås JA, Viken Å, Henriksen S, Skjelseth S (eds) (2010) The 2010 Norwegian Red List for Species. Norwegian Biodiversity Information Centre, NorwayGoogle Scholar
  64. Kallio H (2006) The evolution of the Baltic Sea—changing shorelines and unique coasts. Geol Survey Finl 41:17–21Google Scholar
  65. Knutsen H, Jorde PE, Gonzalez EB, Robalo J, Albretsen J, Almada V (2013) Climate change and genetic structure of leading edge and rear end populations in a northwards shifting marine fish species, the Corkwing Wrasse (Symphodus melops). PLoS One 8(6):e67492. doi: 10.1371/journal.pone.0067492 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Konechnaya GY, Suslova TA (eds) (2004) Red Data Book of the Vologda region, vol 2. Plants and fungi. VGPU Izd. Rus’, Vologgda, p 360 (in Russian) Google Scholar
  67. Konstantinova NA et al (eds) (2014) Red Data Book of the Murmansk region, 2nd edn. Azia-print Publishing, Kemerovo, p 578 (in Russian) Google Scholar
  68. Kuusk V, Tabaka L, Jankeviciene R (2003) Flora of the Baltic countries. Accessed 8 Aug 2016
  69. Lampinen R, Lahti T (2016) Kasviatlas 2015. Helsingin Yliopisto, Luonnontieteellinen keskusmuseo, Helsinki. Accessed 8 Aug 2016
  70. Lammi A P Siikamäki, Mustajärvi K (1999) Genetic diversity, population size, and fitness in central and peripheral populations of a rare plant, Lychnis viscaria. Conserv Biol 13:1069–1078CrossRefGoogle Scholar
  71. Lawton JH (1993) Range, population abundances and conservation. Trends Ecol Evol 8:409–413CrossRefPubMedGoogle Scholar
  72. Lesica P, Allendorf FW (1995) When are peripheral populations valuable for conservation? Conserv Biol 9:753–760CrossRefGoogle Scholar
  73. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  74. Lilleleht V (2008) Red data book of Estonia. Threatened fungi, plants and animals. Commission for Nature Conservation of the Estonian Academy of Sciences. Accessed 08 June 2016
  75. Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425CrossRefGoogle Scholar
  76. Machon N, Bardin P, Mazer SJ, Moret J, Godelle B, Austerlitz F (2003) Relationship between genetic structure and seed and pollen dispersal in the endangered orchid Spiranthes spiralis. New Phytol 157:677–687CrossRefGoogle Scholar
  77. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  78. Meusel H, Jäger E, Weinert E (1992) Comparative chorology of the Central European flora, vol 1. Gustav Fischer Verlag, Jena, p 450Google Scholar
  79. Minasiewicz J, Znaniecka J (2014) Characterization of 15 novel microsatellite loci for Cypripedium calceolus (Orchidaceae) using MiSeq sequencing. Conserv Genet Resour 6:527–529CrossRefGoogle Scholar
  80. Murren C, Ellison A (1998) Seed dispersal characteristics of Brassavola nodosa (Orchidaceae). Am J Bot 85:675–680CrossRefPubMedGoogle Scholar
  81. Natuurpunt (2016) Waarnemingen een initiatief van Natuurpunt Studie vzw en de Stichting Natuurinformatie. Accessed 8 Aug 2016 (in Dutch)
  82. NBIC, GBIF-Norway (2016) Species Map Service. Accessed 8 Aug 2016
  83. NDFF, FLORON (2015) Verspreidingsatlas. Accessed 8 Aug 2016 (in Dutch)
  84. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  85. NetPhyt (2013) Verbreitungsatlas der Farn- und Blütenpflanzen Deutschlands. Landwirtschaftsverlag, Münster. Accessed 8 Aug 2016 (in German)
  86. Nimis PL, Bagella S, Caria MC, Filigheddu R, Moro A, Pittao E, Martello S (2013) An interactive guide to the flora of the temporary ponds of Sardinia (Italy) Accessed 8 Aug 2016
  87. Pandey M, Richards M, Sharma J (2015) Microsatellite-based genetic diversity patterns in disjunct populations of a rare orchid. Genetica 143:693–704CrossRefPubMedGoogle Scholar
  88. Paquette SR (2012) PopGenKit: useful functions for (batch) file conversion and data resampling in microsatellite datasets. R package version, 1Google Scholar
  89. Petit RJ, Kremer A, Wagner DB (1993) Finite island model for organelle and nuclear genes in plants. Heredity 71:630–641CrossRefGoogle Scholar
  90. Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini, D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14:689–701CrossRefPubMedGoogle Scholar
  91. Pfeifer M, Schatz B, Picó FX, Passalacqua NG, Fay MF, Carey PD, Jeltsch F (2009) Phylogeography and genetic structure of the orchid Himantoglossum hircinum (L.) Spreng. across its European centralmarginal gradient. J Biogeogr 36:2353–2365CrossRefGoogle Scholar
  92. Phitos D, Constantinidis T, Kamari G (eds) (2009) The Red Data Book of rare and threatened plants of Greece, vol II (E-Z), Hellenic Βotanical Society, Patra (in Greek) Google Scholar
  93. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  94. Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Genet 6:847–846CrossRefPubMedGoogle Scholar
  95. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  96. Provan J, Bennett KD (2008) Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23:564–571CrossRefPubMedGoogle Scholar
  97. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100CrossRefPubMedGoogle Scholar
  98. Rankou H (2011) Epipactis atrorubens. The IUCN Red List of Threatened Species 2011: e.T176003A7168400. Accessed 8 Aug 2016
  99. Rasmussen HN (1995) Terrestrial orchids: from seed to mycotrophic plant. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  100. Rasomavièius V, Augustauskas J, Ivinskis P, Motiejûnaitë J, Paltanavièius S, Raudonikis L (eds) (2007) Red data book of Lithuania. (Lietuvos Raudonoji Knyga). Leidykla Lututë. Ministry of Environment of the Republic of Lithuania, Vilnius (in Lithuanian) Google Scholar
  101. Rassi P, Hyvärinen E, Juslén A, Mannerkoski I (2010) The 2010 Red List of Finnish Species. Ympäristöministeriö & Suomen Ympäristökeskus, Helsinki (in Finnish) Google Scholar
  102. Raymond M, Rousset F (1995) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  103. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  104. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  105. Rousset F (2008) GENEPOP?007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106CrossRefPubMedGoogle Scholar
  106. Sagarin RD, Gaines SD (2002) The ‘‘abundant centre’’ distribution: to what extent is it a biogeographical rule? Ecol Lett 5:137–147CrossRefGoogle Scholar
  107. SFO (2016) Carte de présence : Carte espèce Epipactis atrorubens. Accessed 17 Nov 2016 (in French)
  108. Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot 94:275–288CrossRefPubMedGoogle Scholar
  109. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462PubMedPubMedCentralGoogle Scholar
  110. Snowarski M (2016) Vascular plants of Poland photoflora. Accessed 8 Aug 2016 (in Polish)
  111. Soliva M, Widmer A (2003) Gene flow across species boundaries in sympatric, sexually deceptive Ophrys (Orchidaceae) species. Evol Int J Org Evol 57:2252–2261CrossRefGoogle Scholar
  112. Stenström A, Jonsson BO, Jónsdóttir IS, Fagerström T, Augner M (2001) Genetic variation and clonal diversity in four clonal sedges (Carex) along the arctic coast of Eurasia. Mol Ecol 10:497–513CrossRefPubMedGoogle Scholar
  113. Steward JR, Lister AM, Barnes I, Dalén L (2010) Refugia revisited: individualistic responses of species in space and time. Proc R Soc B Biol Sci 277:661–671CrossRefGoogle Scholar
  114. Svendsen JI, Astakhov VI, Bolshiyanov DY, Demidov I, Dowdeswell JA, Gataullin V, Hjort C, Hubberten HW, Larsen E, Mangerud J, Melles M, Möller P, Saarnisto M, Siegert MJ (1999) Maximum extent of the Eurasian ice sheets in the Barents and Kara Sea region during the Weichselian. Boreas 28:234–242CrossRefGoogle Scholar
  115. Swarts ND, Dixon KW (2009) Perspectives on orchid conservation in botanic gardens. Trends Plant Sci 14:590–598CrossRefPubMedGoogle Scholar
  116. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109CrossRefPubMedGoogle Scholar
  117. Taberlet P, Swenson JE, Sandegren F, Bjärvall A (1995) Localization of a contact zone between two highly divergent mitochondrial DNA lineages of the brown bear (Ursus arctos) in Scandinavia. Conserv Biol 9:1255–1261CrossRefGoogle Scholar
  118. Taberlet P, Fumagalli L, Wust-Sausy A-G, Cosson J-F (1998) Comparative phylogeography and postglacial colonisation routes in Europe. Mol Ecol 7:453–464CrossRefPubMedGoogle Scholar
  119. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  120. Tałałaj I, Brzosko E (2008) Selfing potential in Epipactis palustris, E. helleborine and E. atrorubens (Orchidaceae). Plant Syst Evol 276:21–29CrossRefGoogle Scholar
  121. Templeton AR, Levin DA (1979) Evolutionary consequences of seed pools. Am Nat 114:232–249CrossRefGoogle Scholar
  122. Tikkanen M, Oksanen J (2002) Late Weichselian and Holocene shore displacement history of the Baltic Sea in Finland. Fennia 180:9–20Google Scholar
  123. Tranchida-Lombardo V, Hopkins SE, Selosse M, Cozzolina S, Taylor DL (2008) Isolation and characterization of new polymorphic microsatellite loci in the mixotrophic orchid Limodorum abortivum L. Swartz (Orchidaceae). Mol Ecol Resour 8:1117–1120CrossRefGoogle Scholar
  124. Tranchida-Lombardo V, Cafasso D, Cristaudo A, Cozzolino S (2011) Phylogeographic patterns, genetic affinities and morphological differentiation between Epipactis helleborine and related lineages in a Mediterranean glacial refugium. Ann Bot Lond 107:427–436CrossRefGoogle Scholar
  125. Tuulik T (1998) Orchids of Hiiumaa. Pirrujaak 5, KärdlaGoogle Scholar
  126. Tzvelev NN (ed) (2000) Red Data Book of nature of the Leningrad region, vol 2. Plants and Fungi. Mir i Sem’ia, Saint-Petersburg, p 672Google Scholar
  127. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  128. Vanden Broeck A, Van Landuyt W, Cox K, De Bruyn L, Gyselings R, Oostermeijer G, Valentin B, Bozic G, Dolinar B, Illyés Z, Mergeay J (2014) High levels of effective long-distance dispersal may blur ecotypic divergence in a rare terrestrial orchid. BMC Ecol 14:20. doi: 10.1186/1472-6785-14-20 CrossRefPubMedPubMedCentralGoogle Scholar
  129. Westling A (ed) (2015) Rödlistade arter i Sverige. ArtDatabanken i samarbete med Naturvårdsverket (in Swedish) Google Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Hilde Hens
    • 1
    • 2
    Email author
  • Anne Jäkäläniemi
    • 3
  • Kadri Tali
    • 4
  • Petr Efimov
    • 5
  • Alexey V. Kravchenko
    • 6
  • Laura Kvist
    • 1
  1. 1.Department of Ecology and GeneticsUniversity of OuluOuluFinland
  2. 2.Thule InstituteUniversity of OuluOuluFinland
  3. 3.Thule InstituteOulanka Research StationKuusamoFinland
  4. 4.Institute of Agricultural and Environmental SciencesEstonian University of Life SciencesTartuEstonia
  5. 5.Komarov Botanical Institute of the Russian Academy of SciencesSt. PetersburgRussia
  6. 6.Karelian Research Centre of the Russian Academy of SciencePetrozavodskRussia

Personalised recommendations