Evolutionary history of the Dactylorhiza maculata polyploid complex (Orchidaceae)

Biological Journal of the Linnean Society

Volumn 101, Issue 3, 2010, Pages 503-525

  Ståhlberg, David ^a   Hedrén, Mikael ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Genetic variation; Glacial refugia; Hybrid zone; ITS; Phylogeography; Plastid DNA; Polyploid evolution; Recombination; Systematics

Indexed keywords

CONTACT ZONE; EVOLUTIONARY BIOLOGY; GENE FLOW; GENETIC MARKER; GEOGRAPHICAL DISTRIBUTION; HERB; HYBRID ZONE; LAST GLACIATION; MIGRATION; PHYLOGEOGRAPHY; PLASTID; POLYPLOIDY; POSTGLACIAL; RECOMBINATION; REFUGIUM; SURVIVAL; TAXONOMY;

EUROPE; RUSSIAN FEDERATION; URALS;

DACTYLORHIZA MACULATA; ORCHIDACEAE;

EID: 77958584756     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2010.01505.x     Document Type: Article

References (112)

1. Adams JM. 1997. Global land environments since the last interglacial. Tennessee:Oak Ridge National Laboratory. Available at
2. Adams JM, Faure H. 1997. Review and Atlas of Palaeovegetation: preliminary land ecosystem maps of the world since the Last Glacial Maximum. Tennessee: Oak Ridge National Laboratory. Available at
3. Alexandersson R, Ågren J. 2000. Genetic structure in the nonrewarding, bumblebee-pollinated orchid Calypso bulbosa. Heredity 85: 401-409.
4. Alsos IG, Engelskjøn T, Gielly L, Taberlet P, Brochmann C. 2005. Impact of ice ages on circumpolar molecular diversity: insights from an ecological key species. Molecular Ecology 14: 2739-2753.
5. Averyanov LV. 1977. Chromosome numbers of some species of the Orchidaceae family in the Leningrad and Vologda districts. Botanical Zhurnal 62: 547-553 (in Russian).
6. Averyanov LV. 1990. A review of the genus Dactylorhiza. In: Arditti J, ed. Orchid biology. Reviews and perspectives. Portland, OR: V. Timber Press, 159-206.
7. Avise JC. 2000. Phylogeography: the history and formation of species. Cambridge, MA: Harvard University Press.
8. Barr CM, Neiman M, Taylor DR. 2005. Inheritance and recombination of mitochondrial genomes in plants, fungi and animals. New Phytologist 168: 39-50.
9. Bateman RM, Denholm I. 1989. A reappraisal of the British and Irish dactylochids, 3. The spotted-orchids. Watsonia 17: 319-349.
10. Bateman RM, Denholm I. 2003. The Heath Spotted-orchid (Dactylorhiza maculata (L.) Soó) in the British Isles: a cautionary case-study in delimitating infraspecific taxa and inferring their evolutionary relationships. Journal Europäischer Orchideen 35: 3-36.
11. Bateman RM, Hollingsworth PM, Preston J, Yi-Bo L, Pridgeon AM, Chase MW. 2003. Molecular phylogenetics and evolution of Orchidinae and selected Habenariinae (Orchidaceae). Botanical Journal of the Linnean Society 142: 1-40.
12. Bengtsson BO, Weibull P, Ghatnekar L. 1995. The loss of alleles by sampling: a study of the common outbreeding grass Festuca ovina over three geographic scales. Hereditas 122: 221-238.
13. Berglund M. 2004. Holocene shore displacement and chronology in Ångermanland, eastern Sweden, the Scandinavian glacio-isostatic uplift centre. Boreas 33: 48-60.
14. Bergthorsson U, Adams KL, Thomason B, Palmer JD. 2003. Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424: 197-201.
15. Bertolini V, Del Prete C, Garbari F. 2000. Karyological and biometrical studies on some species of the genus Dactylorhiza Necker ex Nevski, sect. Dactylorhiza (Orchidaceae) of Central-Northern Italy. Portugaliae Acta Biologica 19: 249-265.
16. Cafasso D, Widmer A, Cozzolino S. 2005. Chloroplast DNA inheritance in the orchid Anacamptis palustris using single-seed polymerase chain reaction. Journal of Heredity 96: 66-70.
17. Cavalli-Sforza L, Edwards AWF. 1967. Phylogenetic analysis: models and estimation procedures. Evolution 32: 550-570.
18. Corriveau JL, Coleman AW. 1988. Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. American Journal of Botany 75: 1443-1458.
19. Delforge P. 1995. Orchids of Britain and Europe. London: Harper Collins Publishers.
20. Demesure B, Comps B, Petit RJ. 1996. Chloroplast DNA phylogeography of the common beech (Fagus sylvatica) in Europe. Evolution 50: 2525-2520.
21. Devey DS, Bateman RM, Fay MF, Hawkins JA. 2009. Genetic structure and systematic relationships within the Ophrys fuciflora aggregate (Orchidaceae: Orchidinae): high diversity in Kent and a wind-induced discontinuity bisecting the Adriatic. Annals of Botany 104: 483-495.
22. Devos N, Tyteca D, Raspé O, Wesselingh RA, Jacquemart A-L. 2003. Patterns of chloroplast diversity among western European Dactylorhiza species (Orchidaceae). Plant Systematics and Evolution 243: 85-97.
23. Devos N, Oh S-H, Raspé O, Jacquemart A-L, Manos PS. 2005. Nuclear ribosomal DNA sequence variation and evolution of spotted marsh-orchids (Dactylorhiza maculata group). Molecular Phylogenetics and Evolution 36: 568-580.
24. Devos N, Raspé O, Oh S-H, Tyteca D, Jacquemart A-L. 2006. The evolution of Dactylorhiza (Orchidaceae) allotetraploid complex: insights from nrDNA sequences and cpDNA PCR-RFLP data. Molecular Phylogenetics and Evolution 38: 767-778.
25. Dressler RL. 1993. Phylogeny and classification of the orchid family. Cambridge: Cambridge University Press.
26. Dufrêne M, Gathoye JL, Tyteca D. 1991. Biostatistical studies on western European Dactylorhiza (Orchidaceae): the D. maculata group. Plant Systematics and Evolution 175: 55-72.
27. Excoffier L, Laval G, Schneider S. 2005. Arlequin version. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47-50.
28. Ferris C, King RA, Hewitt GM. 1999. Isolation within species and the history of glacial refugia. In: Hollingsworth RM, Bateman RM, Gornall RJ, eds. Molecular systematics and plant evolution. London: Taylor & Francis, 20-34.
29. Fredga K. 1996. The chromosome races of Sorex araneus in Scandinavia. Hereditas 125: 123-135.
30. Frey JE, Frey B, Forcioli D. 2005. Quantitative assessment of heteroplasmy levels in Senecio vulgaris chloroplast DNA. Genetica 123: 255-261.
31. Gathoye J-L, Tyteca D. 1989. Contribution à l'étude cytotaxonomique des Dactylorhiza d' Europe occidentale. Mémoire de la Société Royale de Botanique de Belgique 11: 30-42.
32. Gölz P, Reinhard HR. 1997. Über die Gattung Dactylorhiza - neue Erkenntnisse und neue Fragen. Journal Europäischer Orchideen 29: 585-640.
33. Grant V. 1981. Plant speciation. New York: Columbia University Press.
34. Groll M. 1965. Fruchtansatz, Bestäubung und Merkmalsanalyse bei diploiden und polyploiden Sippen von Dactylorchis (Orchis) maculata und Gymnadenia conopsea. Österreichische botanische Zeitschrift 112: 657-700.
35. Hammer Ø, Harper DAT, Ryan PD. 2001. Palaeontological statistics software package for education and data analysis. Palaentologia Electronica 4: 9.
36. Hamrick JL, Godt MJW. 1989. Allozyme diversity in plant species. In: Brown AHD, Clegg MT, Kahler AL, Weir BS, eds. Plant population genetics, breeding and germplast resources. Sunderland, MA: Sinauer, Sunderland, 43-63.
37. Hamrick JL, Godt MJW. 1996. Effects of life history traits on genetic diversity in plant species. Philosophical Transactions of the Royal Society of London, Biological Sciences 351: 1291-1298.
38. Hansen AK, Escobar LK, Gilbert LE, Jansen RK. 2007. Paternal, maternal and biparental inheritance of the chloroplast genome in Passiflora (Passifloraceae): implications for phylogenetic studies. American Journal of Botany 94: 42-46.
39. Hedrén M. 1996. Genetic differentiation, polypoidization and hybridization in Northern European Dactylorhiza (Orchidaceae): evidence from allozyme markers. Plant Systematics and Evolution 201: 31-55.
40. Hedrén M. 2001. Systematics of the Dactylorhiza euxina/incarnata/maculata polyploid complex (Orchidaceae) in Turkey: evidence from allozyme data. Plant Systematics and Evolution 229: 23-44.
41. Hedrén M. 2002. Speciation patterns in the Dactylorhiza incarnata/maculata polyploid complex (Orchidaceae): evidence from molecular markers. Journal Europäischer Orchideen 34: 707-731.
42. Hedrén M. 2003. Plastid DNA variation in the Dactylorhiza incarnata/maculata polyploid complex and the origin of allotetraploid D. sphagnicola (Orchidaceae). Molecular Ecology 12: 2669-2680.
43. Hedrén M, Fay MF, Chase MW. 2001. Amplified fragment length polymorphisms (AFLP) reveal details of polyploid evolution in Dactylorhiza (Orchidaceae). American Journal of Botany 88: 1868-1880.
44. Hedrén M, Nordström S, Persson Hovmalm HA, Pedersen HÆ, Hansson S. 2007. Patterns of polyploid evolution in Greek Marsh Orchids (Dactylorhiza Orchidaceae) as revealed by allozymes, AFLPs and plastid DNA data. American Journal of Botany 94: 1205-1218.
45. Hedrén M, Nordström S, Ståhlberg D. 2008. Polyploid evolution and plastid DNA variation in the Dactylorhiza incarnata/maculata complex (Orchidaceae) in Scandinavia. Molecular Ecology 17: 5075-5091.
46. Heslop-Harrison J. 1951. A comparison of some Swedish and British forms of Orchis maculata L. sens. lat. Svensk Botanisk Tidskrift 45: 608-635.
47. Hewitt GM. 1988. Hybrid zones - natural laboratories for evolutionary studies. Trends in Ecology and Evolution 3: 158-167.
48. Hewitt GM. 1996. Some genetic consequences of ice ages, and their role in divergence and speciation. Botanical Journal of the Linnean Society 58: 247-276.
49. Hewitt GM. 2000. The genetic legacy of the Quaternary ice ages. Nature 405: 907-913.
50. Hewitt GM. 2001. Speciation, hybrid zones and phylogeography - or seeing genes in space and time. Molecular Ecology 10: 537-549.
51. Hewitt GM. 2004. Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London, Biological Sciences 359: 183-195.
52. Huang S, Chiang YC, Schaal BA, Chou CH, Chiang TY. 2001. Organelle DNA phylogeography of Cycas taitungensis, a relict species in Taiwan. Molecular Ecology 10: 2669-2681.
53. Hudson RR, Kaplan NL. 1985. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111: 147-164.
54. Hultén E, Fries M. 1986. Atlas of North European vascular plants: north of the Tropic of Cancer I-III. Königstein: Koeltz Scientific Books.
55. Huntley B, Birks HJB. 1983. An Atlas of past and present pollen maps for Europe: 0-13 000 years ago. Cambridge: Cambridge University Press.
56. Jaarola M, Tegelström H. 1995. Colonization history of north European field voles (Migrotus agrestis) revealed by mitochondrial DNA. Molecular Ecology 4: 299-310.
57. Jagiełło M. 19861987. Analysis of population variability and distribution of species from the Dactylorhiza maculata group (Orchidaceae) in Poland. Fragmenta Floristica et Geobotanica 31-32: 333-383.
58. Jagiełło M, Lankosz-Mróz M. 19861987. Cytotaxonomic studies in the Dactylorhiza maculata (L.) Soó group in Poland (Orchidaceae). Fragmenta Floristica et Geobotanica 31-32: 385-394.
59. Jakobsson M, Säll T, Lind-Halldén C, Halldén C. 2007. The evolutionary history of the common chloroplast genome of Arabidopsis thaliana and A. suecica. Journal of Evolutionary Biology 20: 104-121.
60. Kimura M. 1953. 'Stepping-stone' model of population. Annual Report of the National Institute of Genetics, Japan 3: 62-63.
61. Kimura M, Crow JF. 1964. The number of alleles that can be maintained in a finite population. Genetics 49: 725-738.
62. Koulintchenko M, Konstantinov Y, Dietrich A. 2003. Plant mitochondria actively import DNA via the permeability transition pore complex. EMBO Journal 22: 1245-1254.
63. Lagercrantz U, Ryman N. 1990. Genetic structure of Norway spruce (Picea abies): concordance of morphological and allozymic variation. Evolution 7: 38-53.
64. Litynska-Zajac M. 1995. Anthracological analysis. In: Hromada J, Kozlowski J, eds. Complex of upper palaeolithic sites near Moravany, Western Slovakia. Krakow: Jagiellonian University Press, 74-79.
65. Lowe A, Harris S, Ashton P. 2004. Ecological genetics: design, analysis and application. Oxford: Blackwell Publishing Ltd
66. Magri D, Vendramin GG, Comps B, Dupanloup I, Geburek T, Gömöry D, Latałowa M, Litt T, Paule L, Roure JM, Tantau I, Van Der Knaap WO, Petit RM, De Beaulieu J-L. 2006. A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytologist 171: 199-221.
67. Malm JU, Prentice HC. 2005. Chloroplast DNA haplotypes in Nordic Silene dioica: postglacial immigration from the east and the south. Plant Systematics and Evolution 250: 27-38.
68. Marshall HD, Newton C, Ritland K. 2001. Sequence-repeat polymorphisms exhibit the signature of recombination in lodgepole pine chloroplast DNA. Molecular Biology and Evolution 18: 2136-2138.
69. Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GAB, Kents J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853-858.
70. Nordal I, Jonsell B. 1998. A phylogeographic analysis of Viola rupestris: three post-glacial immigration routes into the Nordic area? Botanical Journal of the Linnean Society 128: 105-122.
71. Nyberg Berglund A-B, Westerbergh A. 2001. Two postglacial lineages of the polyploid Cerastium alpinum (Caryophyllaceae). Hereditas 134: 171-183.
72. Nybom H, Bartish IV. 2000. Effects of life history traits and sampling strategies on genetic diversity estimates obtained with RAPD markers in plants. Perspectives in Plant Ecology and Evolutionary Systematics 3: 93-114.
73. Ohta T, Kimura M. 1973. The model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a genetic population. Genetical Research 22: 201-204.
74. Palmé AE, Su Q, Rautenberg A, Manni F, Lascoux M. 2003. Postglacial recolonization and cpDNA variation of silver birch, Betula pendula. Molecular Ecology 12: 201-212.
75. Pedersen HÆ. 1998. Species concept and guidelines for infraspecific taxonomic ranking in Dactylorhiza (Orchidaceae). Nordic Journal of Botany 18: 289-311.
76. Petit RJ, Kremer A, Wagner DB. 1993. Geographical structure of chloroplast DNA polymorphism in European oaks. Theoretical and Applied Genetics 87: 122-128.
77. Petit RJ, Aguinagalde I, De Beaulieu J-L, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Müller-Starck G, Demesure-Musch B, Palmé A, Martín JP, Rendell S, Vendramin GG. 2003. Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300: 1563-1565.
78. Pillon Y, Fay MF, Shipunov AB, Chase MW. 2006. Species diversity versus phylogenetic diversity: a practical study in the taxonomically difficult genus Dactylorhiza (Orchidaceae). Biological Conservation 129: 4-13.
79. Pillon Y, Fay MF, Hedrén M, Bateman RM, Devey DS, Shipunov AB, Van Der Bank M, Chase MW. 2007. Evolution and temporal diversification of western European polyploid species complexes in Dactylorhiza (Orchidaceae). Taxon 56: 1185-1208.
80. Reinhard HR. 1985. Skandinavische und alpine Dactylorhiza-arten (Orchidaceae). Ergebnisse populationsstatistischer Untersuchungen. Mitteilungsblatts des Arbeitskreises Heimische Orchideen Baden-Württemberg 17: 321-416.
81. Reinhardt J. 1988. Zur Zytotaxonomie einiger Dactylorhiza fuchsii (Druce) Soó-Sippen im. Eichsfeld. Mitteilungsblatts des Arbeitskreises Heimische Orchideen Baden-Württemberg 17: 14-18.
82. Rendell S, Ennos RA. 2002. Chloroplast DNA diversity in Calluna vulgaris (heather) populations in Europe. Molecular Ecology 11: 69-78.
83. Richardson AO, Palmer JD. 2007. Horizontal gene transfer in plants. Journal of Experimental Botany 58: 1-9.
84. Rohlf FJ. 2005. NTSYS-pc. Numerical taxonomy and multivariate analysis system, version 2.2. New York: Exeter Software, Setauket.
85. Scharfenberg K. 1977. Beiträge zur Kenntnis der Sippenstruktur der Gattung Dactylorhiza Necker ex Nevski in den Bezirken Cottbus, Potsdam, Frankfurt (Oder) und Neubrandenburg. Gleditschia 5: 65-127.
86. Shipunov AB, Fay MF, Pillon Y, Bateman RM, Chase MW. 2004. Dactylorhiza (Orchidaceae) in European Russia: combined molecular and morphological analysis. American Journal of Botany 91: 1419-1426.
87. Shipunov AB, Fay MF, Chase MW. 2005. Evolution of Dactylorhiza baltica (Orchidaceae) in European Russia: evidence from molecular markers and morphology. Botanical Journal of the Linnean Society 147: 257-274.
88. Skrede I, Bronken Eidesen P, Piñeiro Portela R, Brochmann C. 2006. Refugia, differentiation and postglacial migration in arctic-alpine Eurasia, exemplified by the mountain avens (Dryas octopetala L.). Molecular Ecology 15: 1827-1840.
89. Smith SE. 1989. Biparental inheritance of organelles and its implications for crop improvement. Plant Breeding Reviews 6: 361-393.
90. Soliva M, Widmer A. 1999. Genetic and floral divergence among sympatric populations of Gymnadenia conopsea s.l. (Orchidaceae) with different flowering phenology. International Journal of Plant Sciences 160: 897-905.
91. Soltis DE, Soltis PS, Tate JA. 2003. Advances in the study of polyploidy since Plant speciation. New Phytologist 161: 173-191.
92. Sommer RS, Nadachowski A. 2006. Glacial refugia of mammals in Europe: evidence from fossil records. Mammal Review 36: 251-265.
93. Soó R. 1960. Synopsis generis Dactylorhiza (Dactylorchis). Annales Universitatis Scientiarum Budapestinensis Sectio Biologica 3: 335-357.
94. Ståhlberg D. 2007. Systematics, phylogeography and polyploid evolution in the Dactylorhiza maculata complex (Orchidaceae). PhD thesis, Lund University, Lund.
95. Ståhlberg D, Hedrén M. 2008. Systematics and phylogeography of the Dactylorhiza maculata complex (Orchidaceae) in Scandinavia: insights from cytological, morphological and molecular data. Plant Systematics and Evolution 273: 107-132.
96. Ståhlberg D, Hedrén M. 2009. Habitat differentiation, hybridization and gene flow patterns in mixed populations of diploid and autotetraploid Dactylorhiza maculata s.l. (Orchidaceae). Evolutionary Ecology 23: 295-328.
97. Stebbins GL. 1971. The morphological, physiological, and cytogenetic significance of polyploidy. In: Barrington EJ, Willis AJ, eds. Chromosomal evolution in higher plants. London: Arnold E., 124-154.
98. Stebbins GL. 1984. Polyploidy and the distribution of the arctic-alpine flora: new evidence and a new approach. Botanica Helvetica 94: 1-13.
99. Stewart JR, Lister AM. 2001. Cryptic northern refugia and the origins of the modern biota. Trends in Ecology and Evolution 16: 608-613.
100. Sundermann H. 1980. Europäische und mediterrane Orchideen. Eine Bestimmungsflora mit Berücksichtigung der Ökologie. Hildesheim: Brücke-Verlag Kurt Schmersow.
101. Taberlet P, Bouvet J. 1994. Mitochrondrial DNA polymorphism, phylogeography, and conservation genetics of the brown bear Ursus arctos in Europe. Proceedings of the Royal Society of London, Biological Sciences 255: 195-200.
102. Tsaousis AD, Martin DP, Ladoukakis ED, Posada D, Zouros E. 2005. Widespread recombination in published animal mtDNA sequences. Molecular Biology and Evolution 22: 925-933.
103. Tyteca D. 2001. Systematics and biostatistics of Dactylorhiza in western Europe: some recent contributions. Journal Europäischer Orchideen 33: 179-199.
104. Tyteca D, Gathoye J-L. 2004. Morphometric analyses of the Dactylorhiza maculata (L.) Soó group in western Europe. Berichte aus den Arbeitskreisen Heimische Orchideen 21: 4-35.
105. Ursenbacher S, Carlsson M, Helfer V, Tegelström H, Fumagalli L. 2006. Phylogeography and Pleistocene refugia of the adder (Vipera berus) as inferred from mitochondrial DNA sequence data. Molecular Ecology 15: 3425-3437.
106. Vaucher C. 1966. Contribution a l'étude cytologique du genre Dactylorchis (Klinge) Vermeulen. Bulletin de la Société des Sciences Naturelles de Neuchatel 89: 75-85.
107. Vellend M, Geber MA. 2005. Connections between species diversity and genetic diversity. Ecology Letters 8: 767-781.
108. Vöth W. 1978. Biometrische Untersuchungen an Dactylorhiza maculata s.l. - Sippen in Niederösterreich. Linzer biologische Beiträge 10: 179-215.
109. Vöth W, Greilhuber J. 1980. Zur Karyosystematik von Dactylorhiza maculata s.l. und ihrer Verbreitung, insbesondere in Niederösterreich. Linzer biologische Beiträge 12: 415-468.
110. Vuilleumier BS. 1971. Pleistocene changes in the fauna and flora of South America. Science 173: 771-780.
111. Widmer A, Lexer C. 2001. Glacial refugia: sanctuaries for allelic richness, but not for gene diversity. Trends in Ecology and Evolution 16: 267-269.
112. Willis KJ, Van Andel TH. 2004. Trees or no trees? The environments of central and eastern Europe during the last glaciation. Quaternary Science Reviews 2369-2387.