Plant Systematics and Evolution

, Volume 302, Issue 1, pp 23–40 | Cite as

The structure of allozyme variation in Silene nutans (Caryophyllaceae) in Denmark and in north-western Europe

  • Fabienne Van Rossum
  • Inger R. Weidema
  • Hélène Martin
  • Solenn Le Cadre
  • Pascal Touzet
  • Honor C. Prentice
  • Marianne Philipp
Original Article


We used allozymes to investigate the structure of genetic variation in populations of the perennial herb Silene nutans at local (Denmark), regional (Nordic area) and wide (over a 19° latitudinal gradient) geographic scales in north-western Europe. New data from Denmark were combined with data from previously studied Fennoscandian and western populations. We related patterns of nuclear variation for 26 Fennoscandian and western populations to the phylogeographic patterns revealed by four plastid (chloroplast) DNA markers. Levels of genetic diversity were similar within Denmark and Sweden/N Finland. Compared to Sweden/N Finland, the Danish populations show lower and nonsignificant F IS values. The genetic structure reveals no grouping of the Danish populations according to their geographic origin (Jutland-Zealand). Within Nordic populations (from Denmark, Sweden and N Finland), there is a weak geographic pattern of allozyme differentiation. The high latitude populations are genetically depauperate compared with populations from Western Europe. At the whole north-western European scale, the structure of allozyme variation within S. nutans shows geographic differentiation (Nordic versus western populations), and some congruence with plastid phylogeographic patterns. A high level of allozyme genetic differentiation is found between Nordic and western populations (8.0 %), but also between populations within haplotype categories (19.4 %). The overall geographic structure of allozyme variation of S. nutans appears to be primarily a reflection of past (postglacial) migration history, whereas more recent adaptive and stochastic processes have occurred at more local scales.


Allozymes Chloroplast DNA Genetic structure Latitude Phylogeography Silene nutans 



We thank Ruth Bruus Jacobsen and Karna Heinsen for field and laboratory assistance, Hans Henrik Bruun and Thure Hauser for providing coordinates of the Danish populations, and Christian Parisod and three anonymous referees for comments on the manuscript. STRUCTURE analyses were carried out using the European Grid Infrastructure with the Biomed virtual organization via DIRAC portal supported by France Grilles. This study was funded by the Danish Research Council, the Fondation belge de la Vocation and the Swedish Institute, the National Fund for Scientific Research (FNRS, Belgium) and the National Fund for Research Luxembourg (AFR grant for S. Le Cadre).

Supplementary material

606_2015_1240_MOESM1_ESM.docx (27 kb)
Supplementary material 1 (DOCX 27 kb)
606_2015_1240_MOESM2_ESM.doc (7.2 mb)
Supplementary material 2 (DOC 7332 kb)
606_2015_1240_MOESM3_ESM.doc (348 kb)
Supplementary material 3 (DOC 347 kb)
606_2015_1240_MOESM4_ESM.doc (9.4 mb)
Supplementary material 4 (DOC 9663 kb)


  1. Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9:968–980. doi: 10.1111/j.1461-0248.2006.00927.x PubMedCrossRefGoogle Scholar
  2. Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Molec Ecol 17:5177–5188. doi: 10.1111/j.1365-294X.2008.03971.x CrossRefGoogle Scholar
  3. Angeloni F, Ouborg NJ, Leimu R (2011) Meta-analysis on the association of population size and life history with inbreeding depression in plants. Biol Conservation 144:35–43. doi: 10.1016/j.biocon.2010.08.016 CrossRefGoogle Scholar
  4. Ansell SW, Stenøien HK, Grundmann M, Schneider H, Hemp A, Bauer N, Russell SJ, Vogel JC (2010) Population structure and historical biogeography of European Arabidopsis lyrata. Heredity 105:543–544. doi: 10.1038/hdy.2010.10 PubMedCrossRefGoogle Scholar
  5. Beatty GE, Provan J (2011) Phylogeographic analysis of North American populations of the parasitic herbaceous plant Monotropa hypopitys L. reveals a complex history of range expansion from multiple glacial refugia. J Biogeogr 38:1585–1599. doi: 10.1111/j.1365-2699.2011.02513.x CrossRefGoogle Scholar
  6. Beatty GE, Provan J (2014) Phylogeographical analysis of two cold-tolerant plants with disjunct Lusitanian distributions does not support in situ survival during the last glaciation. J Biogeogr 41:2185–2193. doi: 10.1111/jbi.12371 CrossRefGoogle Scholar
  7. Beatty GE, Lennon JJ, O’Sullivan CJ, Provan J (2015) The not-so-Irish spurge: Euphorbia hyberna (Euphorbiaceae) and the Littletonian plant ‘steeplechase’. Biol J Linn Soc 114:249–259. doi: 10.1111/bij.12435 CrossRefGoogle Scholar
  8. Beck JB, Schmuths H, Schaal BA (2008) Native range genetic variation in Arabidopsis thaliana is strongly geographically structured and reflects Pleistocene glacial dynamics. Molec Ecol 17:902–915. doi: 10.1111/j.1365-294X.2007.03615.x CrossRefGoogle Scholar
  9. Bettinger A, Buttler KP, Caspari S, Klotz J, May R, Metzing D (2013) Verbreitungsatlas der Farn- und Blütenpflanzen Deutschlands. NetPhyD and BfN, BonnGoogle Scholar
  10. Bruun HH, Van Rossum F, Ström L (2001) Exudation of low molecular weight organic acids by germinating seeds of two edaphic ecotypes of Silene nutans. Acta Oecol 22:285–291. doi: 10.1016/S1146-609X(01)01126-2 CrossRefGoogle Scholar
  11. BSBI (2015) Online atlas of the British and Irish Flora. Available at: Accessed 1 Aug 2015
  12. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Molec Ecol 9:1657–1659. doi: 10.1046/j.1365-294x.2000.01020.x CrossRefGoogle Scholar
  13. Comps B, Thiébaut B, Paule L, Merzeau D, Letouzey J (1990) Allozymic variability in beechwoods (Fagus sylvatica L.) over central Europe: spatial differentiation among and within populations. Heredity 65:407–417. doi: 10.1038/hdy.1990.111 CrossRefGoogle Scholar
  14. Cornille A, Giraud T, Bellard C, Tellier A, Le Cam B, Smulders MJM, Kleinschmit J, Roldan-Ruiz I, Gladieux P (2013) Postglacial recolonization history of the European crabapple (Malus sylvestris Mill.), a wild contributor to the domesticated apple. Molec Ecol 22:2249–2263. doi: 10.1111/mec.12231 CrossRefGoogle Scholar
  15. De Bilde J (1973) Etude génécologique du Silene nutans L. en Belgique: populations du Silene nutans L. sur substrats siliceux et calcaires. Rev Gén Bot 80:161–176Google Scholar
  16. De Bilde J (1977) Effet de l’aluminium et du calcium sur l’activité phosphatasique acide des racines d’écotypes calcicole et silicicole de Silene nutans L. (Caryophyllaceae). Bull Soc Roy Bot Belgique 110:151–160Google Scholar
  17. De Bilde J (1978) Nutrient adaptation in native and experimental calcicolous and silicicolous populations of Silene nutans. Oikos 31:383–391. doi: 10.2307/3543666 CrossRefGoogle Scholar
  18. De Bilde J, Gorenflot R, Briane J-P (1977) Traitement numérique de populations du Silene nutans L. d’Europe nord-occidentale et centrale. Rev Gén Bot 84:341–354Google Scholar
  19. Dorken ME, Eckert CG (2001) Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). J Ecol 89:339–350. doi: 10.1046/j.1365-2745.2001.00558.x CrossRefGoogle Scholar
  20. Dufaÿ M, Lahiani E, Brachi B (2010) Gender variation and inbreeding depression in gynodioecious-gynomonoecious Silene nutans (Caryophyllaceae). Int J Pl Sci 171:53–62. doi: 10.1086/647916 CrossRefGoogle Scholar
  21. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resources 4:359–361. doi: 10.1007/s12686-011-9548-7 CrossRefGoogle Scholar
  22. Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Molec Ecol 17:1170–1188. doi: 10.1111/j.1365-294X.2007.03659.x CrossRefGoogle Scholar
  23. El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree (Argania spinosa (L.) Skeels) endemic to Morocco. Theor Appl Genet 92:832–839. doi: 10.1007/BF00221895 PubMedCrossRefGoogle Scholar
  24. Elberling H, Olesen JM (1999) The structure of a high latitude plant-flower visitor system: the dominance of flies. Ecography 22:314–323. doi: 10.1111/j.1600-0587.1999.tb00507.x CrossRefGoogle Scholar
  25. Ellstrand NC (1984) Multiple paternity within the fruits of wild radish, Raphanus sativus. Amer Naturalist 123:819–828CrossRefGoogle Scholar
  26. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molec Ecol 14:2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x CrossRefGoogle Scholar
  27. Excoffier L (2001) Analysis of population subdivision. In: Balding DJ, Bishop M, Cannings C (eds) Handbook of statistical genetics. Wiley and Sons, Chichester, pp 217–308Google Scholar
  28. Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  29. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinf 1:47–50Google Scholar
  30. Fitter A (1978) An atlas of the wild flowers of Britain and Northern Europe. Collins Sons and Co, GlasgowGoogle Scholar
  31. Floron F (2011) Nieuwe atlas van de Nederlandse flora—verspreiding van wilde planten in Nederland. KNNV, ZeistGoogle Scholar
  32. Ghazoul J (2005) Pollen and seed dispersal among dispersed plants. Biol Rev 80:413–443. doi: 10.1017/S1464793105006731 PubMedCrossRefGoogle Scholar
  33. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version Available at: Accessed 20 Aug 2015 [Updated from Goudet (1995)]
  34. Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans Roy Soc Lond Ser B 351:1291–1298. doi: 10.1098/rstb.1996.0112 CrossRefGoogle Scholar
  35. Hathaway L, Malm JU, Prentice HC (2009) Geographically congruent large-scale patterns of plastid haplotype variation in the European herbs Silene dioica and S. latifolia (Caryophyllaceae). Bot J Linn Soc 161:153–170. doi: 10.1111/j.1095-8339.2009.01003.x CrossRefGoogle Scholar
  36. Hauser TP, Siegismund HR (2000) Inbreeding and outbreeding effects on pollen fitness and zygote survival in Silene nutans (Caryophyllaceae). J Evol Biol 13:446–454. doi: 10.1046/j.1420-9101.2000.00183.x CrossRefGoogle Scholar
  37. Hegi G (1979) Illustrierte flora von Mittel-Europa, Band III, Teil 2. Parey, BerlinGoogle Scholar
  38. Hepper FN (1956) Silene nutans L. Biological flora of the British Isles. J Ecol 44:693–700. doi: 10.2307/2256856 CrossRefGoogle Scholar
  39. Heuertz M, Fineschi S, Anzidei M, Pastorelli R, Salvini D, Paule L, Frascaria-Lacoste N, Hardy OJ, Vekemans X, Vendramin GG (2004) Chloroplast DNA variation and postglacial recolonization of common ash (Fraxinus excelsior L.) in Europe. Molec Ecol 13:3437–3452. doi: 10.1111/j.1365-294X.2004.02333.x CrossRefGoogle Scholar
  40. Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112. doi: 10.1111/j.1095-8312.1999.tb01160.x CrossRefGoogle Scholar
  41. Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913. doi: 10.1038/35016000 PubMedCrossRefGoogle Scholar
  42. Hewitt GM (2011) Quaternary phylogeography: the roots of hybrid zones. Genetica 139:617–638. doi: 10.1007/s10709-011-9547-3 PubMedCrossRefGoogle Scholar
  43. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Molec Ecol Resources 9:1322–1332. doi: 10.1111/j.1755-0998.2009.02591.x CrossRefGoogle Scholar
  44. Hultén E (1971) Atlas över växternas utbredning i Norden. Generalstabens Litografiska Anstalts Förlag, StockholmGoogle Scholar
  45. Ibáñez I, Katz DSW, Peltier D, Wolf SM, Connor Barrie BT (2014) Assessing the integrated effects of landscape fragmentation on plants and plant communities: the challenge of multiprocess-multiresponse dynamics. J Ecol 102:882–895. doi: 10.1111/1365-2745.12223 CrossRefGoogle Scholar
  46. 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 23:1801–1806. doi: 10.1093/bioinformatics/btm233 PubMedCrossRefGoogle Scholar
  47. Jürgens A, Witt T, Gottsberger G (1996) Reproduction and pollination in central European populations of Silene and Saponaria species. Bot Acta 109:316–324. doi: 10.1111/j.1438-8677.1996.tb00579.x CrossRefGoogle Scholar
  48. Kalinowski ST (2002) How many alleles per locus should be used to estimate genetic distances? Heredity 88:62–65. doi: 10.1038/sj.hdy.6800009 PubMedCrossRefGoogle Scholar
  49. Kirby GC (1975) Heterozygote frequencies in small subpopulations. Theor Populat Biol 8:31–48. doi: 10.1016/0040-5809(75)90037-4 CrossRefGoogle Scholar
  50. Koch M, Bernhardt K-G (2004) Comparative biogeography of the cytotypes of annual Microthlaspi perfoliatum (Brassicaceae) in Europe using isozymes and cpDNA data: refugia, diversity centers, and postglacial colonization. Amer J Bot 91:115–124. doi: 10.3732/ajb.91.1.115 CrossRefGoogle Scholar
  51. Kwak MM, Velterop O, van Andel J (1998) Pollen and gene flow in fragmented habitats. Appl Veg Sci 1:37–54. doi: 10.2307/1479084 CrossRefGoogle Scholar
  52. Lahiani E, Dufaÿ M, Castric V, Le Cadre S, Charlesworth D, Van Rossum F, Touzet P (2013) Disentangling the effects of mating systems and mutation rates on cytoplasmic diversity in gynodioecious Silene nutans and dioecious Silene otites. Heredity 111:157–164. doi: 10.1038/hdy.2013.32 PubMedPubMedCentralCrossRefGoogle Scholar
  53. Magalhaes IS, Gleiser G, Labouche A-M, Bernasconi G (2011) Comparative population genetic structure in a plant-pollinator/seed predator system. Molec Ecol 20:4618–4630. doi: 10.1111/j.1365-294X.2011.05296.x CrossRefGoogle Scholar
  54. 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 RJ, De Beaulieu J-L (2006) A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol 171:199–221. doi: 10.1111/j.1469-8137.2006.01740.x PubMedCrossRefGoogle Scholar
  55. Malm JU, Prentice HC (2002) Immigration history and gene dispersal: allozyme variation in Nordic populations of the red campion, Silene dioica (Caryophyllaceae). Biol J Linn Soc 77:23–34. doi: 10.1046/j.1095-8312.1999.00079.x CrossRefGoogle Scholar
  56. Mattioni C, Angela Martin M, Pollegioni P, Cherubini M, Villani F (2013) Microsatellite markers reveal a strong geographical structure in European populations of Castanea sativa (Fagaceae): evidence for multiple glacial refugia. Amer J Bot 100:951–961. doi: 10.3732/ajb.1200194 CrossRefGoogle Scholar
  57. Mayer C, Van Rossum F, Jacquemart A-L (2012) Evaluating pollen flow indicators for an insect-pollinated plant species. Basic Appl Ecol 13:690–697. doi: 10.1016/j.baae.2012.09.012 CrossRefGoogle Scholar
  58. Michaud H, Toumi I, Lumaret R, Li TX, Romane F, Digiusto F (1995) Effect of geographical discontinuity on genetic variation in Quercus ilex L. (holm oak): evidence from enzyme polymorphism. Heredity 74:590–606. doi: 10.1038/hdy.1995.83 CrossRefGoogle Scholar
  59. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedPubMedCentralGoogle Scholar
  60. Nei M, Chesser RK (1983) Estimation of fixation indices and diversities. Ann Hum Genet 47:253–259. doi: 10.1111/j.1469-1809.1983.tb00993.x PubMedCrossRefGoogle Scholar
  61. Oostermeijer JGB, Luijten SH, den Nijs JCM (2003) Integrating demographic and genetic approaches in plant conservation. Biol Conservation 113:389–398. doi: 10.1016/S0006-3207(03)00127-7 CrossRefGoogle Scholar
  62. Ouborg NJ, Piquot Y, van Groenendael JMM (1999) Population genetics, molecular markers, and the study of dispersal in plants. J Ecol 87:551–568. doi: 10.1046/j.1365-2745.1999.00389.x CrossRefGoogle Scholar
  63. Pamilo P, Savolainen O (1999) Postglacial colonization, drift, local selection and conservation of populations: a northern perspective. Hereditas 130:229–238. doi: 10.1111/j.1601-5223.1999.00229.x CrossRefGoogle Scholar
  64. Pauwels M, Vekemans X, Godé C, Frérot H, Castric V, Saumitou-Laprade P (2012) Nuclear and chloroplast DNA phylogeography reveals vicariance among European populations of the model species for the study of metal tolerance, Arabidopsis halleri (Brassicaceae). New Phytol 193:916–928. doi: 10.1111/j.1469-8137.2011.04003.x PubMedCrossRefGoogle Scholar
  65. Petit RJ, Csaikl U, Bordács S, Burg K, Coart E, Cottrell J, van Dam B, Deans JD, Glaz I, Dumolin-Lapègue S, Fineschi S, Finkeldey R, Gillies A, Goicoechea PG, Jensen JS, König A, Lowe AJ, Madsen SF, Mátyás G, Munro RC, Olalde M, Pemonge M-H, Popescu F, Slade D, Tabbener H, Taurchini D, Ziegenhagen B, Kremer A (2002) Chloroplast DNA variation in European white oaks: phylogeography and patterns of diversity based on data from over 2,600 populations. Forest Ecol Managem 156:5–26. doi: 10.1016/S0378-1127(01)00645-4 CrossRefGoogle Scholar
  66. Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organisation of chloroplast, mitochondrial and nuclear diversity in plant populations. Molec Ecol 14:689–701. doi: 10.1111/j.1365-294X.2004.02410.x CrossRefGoogle Scholar
  67. Petit RJ, Hu FS, Dick CW (2008) Forests of the past: a window to future changes. Science 320:1450–1452. doi: 10.1126/science.1155457 PubMedCrossRefGoogle Scholar
  68. Prentice HC, Andersson S, Månsby E (2011) Mosaic variation in allozyme and plastid DNA markers in the European ranges of Silene vulgaris and its partially sympatric relative S. uniflora (Caryophyllaceae). Bot J Linn Soc 166:127–148. doi: 10.1111/j.1095-8339.2011.01128.x CrossRefGoogle Scholar
  69. Pritchard JK, Wen W (2002) Documentation for Structure software: version 2. Available at: Accessed 29 Aug 2014
  70. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:949–959Google Scholar
  71. Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225. doi: 10.2307/2409177 CrossRefGoogle Scholar
  72. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Molec Ecol Notes 4:137–138. doi: 10.1046/j.1471-8286.2003.00566.x CrossRefGoogle Scholar
  73. Schaal BA, Hayworth DA, Olsen KM, Rauscher JT, Smith WA (1998) Phylogeographic studies in plants: problems and prospects. Molec Ecol 7:465–474. doi: 10.1046/j.1365-294x.1998.00318.x CrossRefGoogle Scholar
  74. Sjörs H (1999) 1. The background: geology, climate and zonation. Acta Phytogeogr Suec 84:5–14Google Scholar
  75. Soltis DE, Haufler CH, Darrow DC, Gastony GJ (1983) Starch gel electrophoresis of ferns: a compilation of grinding buffers, gel and electrode buffers, and staining schedules. Amer Fern J 73:9–27. doi: 10.2307/1546611 CrossRefGoogle Scholar
  76. Soubani E, Hedrén M, Widén B (2014) Phylogeography of the European rock rose Helianthemum nummularium (Cistaceae): incongruent patterns of differentiation in plastid DNA and morphology. Bot J Linn Soc 176:311–331. doi: 10.1111/boj.12209 CrossRefGoogle Scholar
  77. StatSoft, Inc. (2010) STATISTICA (data analysis software system), version 10. Available at: Accessed 9 Aug 2011
  78. Taberlet P, Fugamalli L, Wust-Saucy A-G, Cosson J-F (1998) Comparative phylogeography and postglacial colonization routes in Europe. Molec Ecol 7:453–464. doi: 10.1046/j.1365-294x.1998.00289.x CrossRefGoogle Scholar
  79. Talavera S, Bastida F, Ortiz PL, Arista M (2001) Pollinator attendance and reproductive success in Cistus libanotis L. (Cistaceae). Int J Pl Sci 162:343–352. doi: 10.1086/319573 CrossRefGoogle Scholar
  80. Tamme R, Götzenberger L, Zobel M, Bullock JM, Hooftman DAP, Kaasik H, Pärtel M (2014) Predicting species’ maximum dispersal distances from simple plant traits. Ecology 95:505–513. doi: 10.1890/13-1000.1 PubMedCrossRefGoogle Scholar
  81. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633PubMedGoogle Scholar
  82. Thuiller W, Lavorel S, Araújo M (2005) Niche properties and geographical extent as predictor of species sensitivity to climate change. Global Ecol Biogeogr 14:347–357. doi: 10.1111/j.1466-822X.2005.00162.x CrossRefGoogle Scholar
  83. Torres AM, Bergh BO (1978) Isozymes as indicator of outcrossing among ‘Pinkerton’ seedlings. Yearb Calif Avocado Ass 62:103–110Google Scholar
  84. Trøjelsgaard K, Olesen JM (2013) Macroecology of pollination networks. Global Ecol Biogeogr 22:149–162. doi: 10.1111/j.1466-8238.2012.00777.x CrossRefGoogle Scholar
  85. Tyler T, Prentice HC, Widén B (2002) Geographic variation and dispersal history in Fennoscandian populations of two forest herbs. Pl Syst Evol 233:47–64. doi: 10.1007/s006060200054 CrossRefGoogle Scholar
  86. Tzedakis PC, Emerson BC, Hewitt GM (2013) Cryptic or mystic? Glacial tree refugia in northern Europe. Trends Ecol Evol 28:696–704. doi: 10.1016/j.tree.2013.09.001 PubMedCrossRefGoogle Scholar
  87. Van Rossum F (1996) Ecologie, génétique et biologie des populations de Silene nutans L., une espèce rare en Belgique. PhD Thesis, Université Libre de Bruxelles, BrusselsGoogle Scholar
  88. Van Rossum F (2000) Amplitude synécologique de Silene nutans L. (Caryophyllaceae) en Belgique. Dumortiera 75:11–24Google Scholar
  89. Van Rossum F (2008) Conservation of long-lived perennial forest herbs in an urban context: Primula elatior as study case. Conservation Genet 9:119–128. doi: 10.1007/s10592-007-9314-2 CrossRefGoogle Scholar
  90. Van Rossum F (2009) Pollen dispersal and genetic variation in an early-successional forest herb in a peri-urban forest. Pl Biol 11:725–737. doi: 10.1111/j.1438-8677.2008.00176.x CrossRefGoogle Scholar
  91. Van Rossum F, Prentice HC (2004) Structure of allozyme variation in Nordic Silene nutans (Caryophyllaceae): population size, geographic position and immigration history. Biol J Lin Soc 81:357–371. doi: 10.1111/j.1095-8312.2003.00301.x CrossRefGoogle Scholar
  92. Van Rossum F, De Bilde J, Lefèbvre C (1996) Barriers to hybridization in calcicolous and silicicolous populations of Silene nutans from Belgium. Belg J Bot 129:13–18Google Scholar
  93. Van Rossum F, Vekemans X, Meerts P, Gratia E, Lefèbvre C (1997) Allozyme variation in relation to ecotypic differentiation and population size in marginal populations of Silene nutans. Heredity 78:552–560. doi: 10.1038/hdy.1997.86 CrossRefGoogle Scholar
  94. Van Rossum F, Meerts P, Gratia E, Tanghe M (1999) Ecological amplitude in relation to allozyme variation in Silene nutans at the western margin of its distribution. J Veg Sci 10:253–260. doi: 10.2307/3237146 CrossRefGoogle Scholar
  95. Van Rossum F, Vekemans X, Gratia E, Meerts P (2003) A comparative study of allozyme variation of peripheral and central populations of Silene nutans L. (Caryophyllaceae) from Western Europe: implications for conservation. Pl Syst Evol 242:49–61. doi: 10.1007/s00606-003-0049-3 CrossRefGoogle Scholar
  96. Van Rossum F, Campos De Sousa S, Triest L (2004) Genetic consequences of habitat fragmentation in an agricultural landscape on the common Primula veris, and comparison with its rare congener. P. vulgaris. Conservation Genet 5:231–245. doi: 10.1023/B:COGE.0000030007.85492.70 CrossRefGoogle Scholar
  97. Vekemans X, Lefèbvre C (1997) On the evolution of heavy-metal tolerant populations in Armeria maritima: evidence from allozyme variation and reproductive barriers. J Evol Biol 10:175–191. doi: 10.1046/j.1420-9101.1997.10020175.x CrossRefGoogle Scholar
  98. Vrancken J, Brochmann C, Wesselingh RA (2012) A European phylogeography of Rhinanthus minor compared to Rhinanthus angustifolius: unexpected splits and signs of hybridization. Ecol Evol 2:1531–1548. doi: 10.1002/ece3.276 PubMedPubMedCentralCrossRefGoogle Scholar
  99. Ward JH (1963) Hierarchical grouping to optimize an objective function. J Amer Statist Assoc 58:236–244. doi: 10.1080/01621459.1963.10500845 CrossRefGoogle Scholar
  100. Weidema IR, Siegismund HR, Philipp M (1996) Distribution of genetic variation within and among Danish populations of Armeria maritima, with special reference to the effects of population size. Hereditas 124:121–129. doi: 10.1111/j.1601-5223.1996.00121.x CrossRefGoogle Scholar
  101. Weidema IR, Magnussen LS, Philipp M (2000) Gene flow and mode of pollination in a dry-grassland species, Filipendula vulgaris (Rosaceae). Heredity 84:311–320. doi: 10.1046/j.1365-2540.2000.00669.x PubMedCrossRefGoogle Scholar
  102. Weir BS (1990) Genetic data analysis. Sinauer, SunderlandGoogle Scholar
  103. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370. doi: 10.2307/2408641 CrossRefGoogle Scholar
  104. Wendel JF, Weeden NF (1989) Visualization and interpretation of plant isozymes. In: Soltis DE, Soltis PS (eds) Isozymes in Plant Biology. Chapman and Hall, London, pp 5–45CrossRefGoogle Scholar
  105. Wilcock C, Neiland R (2002) Pollination failure in plants: why it happens and when it matters. Trends Pl Sci 7:270–277. doi: 10.1016/S1360-1385(02)02258-6 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2015

Authors and Affiliations

  • Fabienne Van Rossum
    • 1
    • 2
    • 3
    • 4
  • Inger R. Weidema
    • 5
  • Hélène Martin
    • 6
  • Solenn Le Cadre
    • 6
  • Pascal Touzet
    • 6
  • Honor C. Prentice
    • 4
  • Marianne Philipp
    • 5
  1. 1.Department of Vascular PlantsMeise Botanic Garden (Formerly National Botanic Garden of Belgium)MeiseBelgium
  2. 2.Ecologie végétale et BiogéochimieUniversité Libre de BruxellesBrusselsBelgium
  3. 3.Fédération Wallonie-BruxellesBrusselsBelgium
  4. 4.Biodiversity, Department of BiologyLund UniversityLundSweden
  5. 5.Department of Plant EcologyBotanical Institute, University of CopenhagenCopenhagenDenmark
  6. 6.Unité Evolution, Ecologie et PaléontologieUMR 8198 CNRS, Université de Lille 1– Sciences et Technologies, Bâtiment SN2Villeneuve d’AscqFrance

Personalised recommendations