Tree Genetics & Genomes

, Volume 9, Issue 5, pp 1193–1205 | Cite as

Can gene flow among populations counteract the habitat loss of extremely fragile biotopes? An example from the population genetic structure in Salix daphnoides

  • Michal Sochor
  • Radim J. VašutEmail author
  • Eva Bártová
  • Ľuboš Majeský
  • Jaroslav Mráček
Original Paper


Wild river gravel banks (RGB) represent an extremely fragile biotope that is significantly endangered by human activities due to its fragmentation over the past century. The consequences of such processes were studied using the endangered violet willow (Salix daphnoides) at the westernmost foothills of the Carpathian Mountains. We quantified population genetic characteristics for 14 ecologically and demographically characterised populations using simple sequence repeats (SSR) and amplified fragment length polymorphism (AFLP) markers. We found a significant correlation between the biotope, sex, age and genetic structure of the populations. The natural RGB populations revealed high genotypic variability when using SSR markers, in contrast to low genotypic variability of the populations of other biotopes of Cirsium wet meadows (CWM) and Ash-alder forests (AAF) that consisted of one to two clones at each site. High heterozygosity (H obs = 0.428–0.532) was similar across all natural (RGB) populations; however, these populations were deficient in heterozygotes (F IS/ρ IS > 0). All RGB populations exhibited moderate to very significant genetic differentiation for microsatellites, despite the fact that the AFLP data showed strong differentiation only between CWM and AAF populations. Division into clusters by Structure confirmed consistent geographic groups for the RGB populations. According to our results, the strong decrease in previously continuous and large natural habitats for the violet willow is slightly counterbalanced by among-population gene flow. However, the survival of natural populations is tightly linked to the presence of river gravel banks and bars. Strict protection of this habitat is therefore essential for the conservation of the species.


Conservation Genetic diversity Population genetics River gravel banks Salix daphnoides Willow 



We wish to thank M. Popelářová (PLA Beskydy) for providing information on the distribution of the species in the Beskydy Mountains, M. Kitner (Palacký University in Olomouc) for lab assistance and V. Bruna (JE Purkyně University in Ustí nad Labem) for giving us permission to use historical maps. This project was funded by the Norway grants (no. CZ0138), the Internal Grant Agency of the Palacký University in Olomouc (IGA 2010/1, 2011/3 and 2012/1) and by the Internal Grant Agency of the Faculty of Forestry and Wood Technology at Mendel University in Brno (no. 12/2010). RJV was further supported by the Czech Science Foundation (GACR:, Grant no. 206/09/P356.

Supplementary material

11295_2013_628_MOESM1_ESM.doc (32 kb)
Supplementary table 1 (DOC 31 kb)


  1. Albaladejo RG, Carrillo LF, Aparicio A, Fernandez-Manjarres JF, Gonzalez-Varo JP (2009) Population genetic structure in Myrtus communis L. in a chronically fragmented landscape in the Mediterranean: can gene flow counteract habitat perturbation? Plant Biol 11:442–453PubMedCrossRefGoogle Scholar
  2. Aparicio A, Hampe A, Fernandez-Carrillo L, Albaladejo RG (2012) Fragmentation and comparative genetic structure of four mediterranean woody species: complex interactions between life history traits and the landscape context. Divers Distrib 18:226–235CrossRefGoogle Scholar
  3. Bacles CFE, Lowe AJ, Ennos RA (2004) Genetic effects of chronic habitat fragmentation on tree species: the case of Sorbus aucuparia in a deforested Scottish landscape. Mol Ecol 13:573–584PubMedCrossRefGoogle Scholar
  4. Bacles CFE, Burczyk J, Lowe AJ, Ennos RA (2005) Historical and contemporary mating patterns in remnant populations of the forest tree Fraxinus excelsior L. Evolution 59:979–990PubMedGoogle Scholar
  5. Barker JHA, Pahlich A, Trybush S, Edwards KJ, Karp A (2003) Microsatellite markers for diverse Salix species. Mol Ecol Notes 3:4–6CrossRefGoogle Scholar
  6. Bártová E, Vašut RJ (2011) Distribution of the violet willow (Salix daphnoides Vill.) in eastern Moravia and Silesia. Acta Carp Occ 2:3–10 [in Czech language]Google Scholar
  7. Brennan AC, Barker D, Hiscock SJ, Abbott RJ (2012) Molecular genetic and quantitative trait divergence associated with recent homoploid hybrid speciation: a study of Senecio squalidus (Asteraceae). Heredity 108:87–95Google Scholar
  8. Castiglione S, Cicatelli A, Lupi R, Patrignani G, Fossati T, Brundu G, Sabatti M, van Loo M, Lexer C (2010) Genetic structure and introgression in riparian populations of Populus alba L. Plant Biosyst 144:656–668CrossRefGoogle Scholar
  9. Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631PubMedCrossRefGoogle Scholar
  10. Chmelař J, Meusel W (1986) Die Weiden Europas: Die Gattung Salix. Die Neue Brehm-Bücherei 494. A. Ziemsen Verlag, Wittenberg LutherstadtGoogle Scholar
  11. Chytrý M, Kučera T, Kočí M, Grulich V, Lustyk P (eds) (2010) Katalog biotopů České republiky [Habitat Catalogue of the Czech Republic], 2nd edition. AOPaK ČR, 445 ppGoogle Scholar
  12. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  13. Dayanandan S, Dole J, Bawa K, Kesseli R (1999) Population structure delineated with microsatellite markers in fragmented populations of a tropical tree, Carapa guianensis (Meliaceae). Mol Ecol 8:1585–1592PubMedCrossRefGoogle Scholar
  14. Douhovnikoff V, Dodd RS (2003) Intra-clonal variation and a similarity threshold for identification of clones: application to Salix exigua using AFLP molecular markers. Theor Appl Genet 106:1307–1315PubMedGoogle Scholar
  15. Douhovnikoff V, McBride JR, Dodd RS (2005) Salix exigua clonal growth and population dynamics in relation to disturbance regime variation. Ecology 86:446–452CrossRefGoogle Scholar
  16. Douhovnikoff V, Goldsmith GR, Tape KD, Huang C, Sur N, Bret-Harte MS (2010) Clonal diversity in an expanding community of arctic Salix spp. and a model for recruitment modes of arctic plants. Arct Antarct Alp Res 42:406–411CrossRefGoogle Scholar
  17. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  18. Ehrich D (2006) AFLPDAT: a collection of R functions for convenient handling of AFLP data. Mol Ecol Notes 6:603–604CrossRefGoogle Scholar
  19. Ellis JR, McCauley DE (2009) Phenotypic differentiation in fitness related traits between populations of an extremely rare sunflower: conservation management of isolated populations. Biol Conserv 142:1836–1843CrossRefGoogle Scholar
  20. Ellstrand NC, Roose ML (1987) Patterns of genotypic diversity in clonal plant-species. Am J Bot 74:123–131CrossRefGoogle Scholar
  21. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software Structure: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  22. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578PubMedCrossRefGoogle Scholar
  23. Förster N, Ulrichs C, Zander M, Kätzel R, Mewis I (2009) Salicylate-rich willow bark for the pharmaceutical industry. Gesunde Pflanzen 61:129–134CrossRefGoogle Scholar
  24. Förster N, Ulrichs C, Zander M, Katzel R, Mewis I (2010) Factors influencing the variability of antioxidative phenolic glycosides in Salix species. J Agric Food Chem 58:8205–8210PubMedCrossRefGoogle Scholar
  25. Gage EA, Cooper DJ (2005) Patterns of willow seed dispersal, seed entrapment, and seedling establishment in a heavily browsed montane riparian ecosystem. Can J Bot 83:678–687CrossRefGoogle Scholar
  26. Hegland SJ, van Leeuwen M, Oostermeijer JGB (2001) Population structure of Salvia pratensis in relation to vegetation and management of Dutch dry floodplain grasslands. J Appl Ecol 38:1277–1289CrossRefGoogle Scholar
  27. Holub J, Procházka F (2000) Red list of vascular plants of the Czech Republic (2000). Preslia 72:187–230Google Scholar
  28. Hörandl E, Florineth F, Hadacek F (2002) Weiden in Österreich und angrenzenden Gebieten. Universität für Bodenkultur, WienGoogle Scholar
  29. Houle G, Babeux P (1993) Temporal variations in the rooting ability of cuttings of Populus balsamifera and Salix planifolia from natural clones populations of sub-arctic Quebec. Can J For Res 23:2603–2608CrossRefGoogle Scholar
  30. Imbert E, Lefevre F (2003) Dispersal and gene flow of Populus nigra (Salicaceae) along a dynamic river system. J Ecol 91:447–456CrossRefGoogle Scholar
  31. 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 23:1801–1806PubMedCrossRefGoogle Scholar
  32. Jalas J, Suominen J (eds) (1988) Atlas Florae Europaeae. Distribution of vascular plants in Europe. 2. Angiospermae (part): 3. Salicaceae to Balanophoraceae, Polygonaceae, Chenopodiaceae to Basellaceae. Cambridge University Press, CambridgeGoogle Scholar
  33. Jaquiery J, Guelat J, Broquet T, Berset-Brandli L, Pellegrini E, Moresi R, Hirzel AH, Perrin N (2008) Habitat-quality effects on metapopulation dynamics in greater white-toothed shrews, Crocidura russula. Ecology 89:2777–2785PubMedCrossRefGoogle Scholar
  34. Karrenberg S, Suter M (2003) Phenotypic trade-offs in the sexual reproduction of Salicaceae from flood plains. Am J Bot 90:749–754PubMedCrossRefGoogle Scholar
  35. Karrenberg S, Edwards PJ, Kollmann J (2002) The life history of Salicaceae living in the active zone of floodplains. Freshw Biol 47:733–748CrossRefGoogle Scholar
  36. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241CrossRefGoogle Scholar
  37. Kikuchi S, Suzuki W, Sashimura N (2011) Gene flow in an endangered willow Salix hukaoana (Salicaceae) in natural and fragmented riparian landscapes. Conserv Genet 12:79–89CrossRefGoogle Scholar
  38. Krasny ME, Vogt KA, Zasada JC (1988) Establishment of 4 Salicaceae species on river bars in interior Alaska. Holarct Ecol 11:210–219Google Scholar
  39. Lee KM, Kim YY, Hyun JO (2011) Genetic variation in populations of Populus davidiana Dode based on microsatellite marker analysis. Genes Genomics 33:163–171CrossRefGoogle Scholar
  40. Lin J, Gibbs JP, Smart LB (2009) Population genetic structure of native versus naturalized sympatric shrub willows (Salix, Salicaceae). Am J Bot 96:771–785PubMedCrossRefGoogle Scholar
  41. Lynch M, Milligan BG (1994) Analysis of population genetic structure with RAPD markers. Mol Ecol 3:91–99PubMedCrossRefGoogle Scholar
  42. Mahoney JM, Rood SB (1998) Streamflow requirements for cottonwood seedling recruitment—an integrative model. Wetlands 18:634–645CrossRefGoogle Scholar
  43. Majeský Ľ, Vašut RJ, Kitner M, Trávníček B (2012) The pattern of genetic variability in apomictic clones of Taraxacum officinale indicates the alternation of asexual and sexual histories of apomicts. PLoS One 7(8):e41868. doi: 10.1371/journal.pone.0041868 PubMedCrossRefGoogle Scholar
  44. Malanson GP (1993) Riparian landscapes. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  45. Mariette S, Cottrell J, Csaikl UM, Goikoechea P, Konig A, Lowe AJ, van Dam BC, Barreneche T, Bodenes C, Streiff R, Burg K, Groppe K, Munro RC, Tabbener H, Kremer A (2002a) Comparison of levels of genetic diversity detected with AFLP and microsatellite markers within and among mixed Q. petraea (Matt.) Liebl. and Q. robur L. stands. Silvae Genet 51:72–79Google Scholar
  46. Mariette S, Le Corre V, Austerlitz F, Kremer A (2002b) Sampling within the genome for measuring within-population diversity: trade-offs between markers. Mol Ecol 11:1145–1156PubMedCrossRefGoogle Scholar
  47. Meerow AW, Gideon M, Kuhn DN, Mopper S, Nakamura K (2011) The genetic mosaic of Iris series Hexagonae in Florida: inferences on the Holocene history of the Louisiana Irises and anthropogenic effects on their distribution. Int J Plant Sci 172:1026–1052CrossRefGoogle Scholar
  48. Meirmans PG, Hedrick PW (2011) Assessing population structure: F ST and related measures. Mol Ecol Resour 11:5–18PubMedCrossRefGoogle Scholar
  49. Meirmans PG, van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794CrossRefGoogle Scholar
  50. Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Nat Acad Sci U S A 70:3321–3323CrossRefGoogle Scholar
  51. Newsholme C (2003) Willows: the genus Salix. Timber Press, PortlandGoogle Scholar
  52. Pimm SL, Raven P (2000) Biodiversity—extinction by numbers. Nature 403:843–845PubMedCrossRefGoogle Scholar
  53. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  54. Raymond M, Rousset F (1995) GENEPOP (version 1.2)—population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  55. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  56. Rousset F (2008) GENEPOP ' 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106PubMedCrossRefGoogle Scholar
  57. Schwarcz KD, Pataca CL, Abreu AG, Bariani JM, Macrini CMT, Solferini VN (2010) Genetic diversity in Atlantic Forest trees: fragmentation effects on Astronium graveolens (Anacardiaceae) and Metrodorea nigra (Rutaceae), species with distinct seed dispersal strategies. Bot J Linn Soc 164:326–336CrossRefGoogle Scholar
  58. Sebbenn AM, Carvalho ACM, Freitas MLM, Moraes SMB, Gaino A, da Silva JM, Jolivet C, Moraes MLT (2011) Low levels of realized seed and pollen gene flow and strong spatial genetic structure in a small, isolated and fragmented population of the tropical tree Copaifera langsdorffii Desf. Heredity 106:134–145PubMedCrossRefGoogle Scholar
  59. Skálová D, Navrátilová B, Richterová L, Knitl M, Sochor M, Vašut RJ (2012) Biotechnological methods for in vitro propagation in willows (Salix spp.). Cent Eur. J Biol 7:931–940Google Scholar
  60. Skvortsov AK (1999) Willows of Russia and adjacent countries, taxonomical and geographical revision. University of Joensuu, JoensuuGoogle Scholar
  61. Smulders MJM, Cottrell JE, Lefevre F, van der Schoot J, Arens P, Vosman B, Tabbener HE, Grassi F, Fossati T, Castiglione S, Krystufek V, Fluch S, Burg K, Vornam B, Pohl A, Gebhardt K, Alba N, Agundez D, Maestro C, Notivol E, Volosyanchuk R, Pospiskova M, Bordacs S, Bovenschen J, van Dam BC, Koelewijn HP, Halfmaerten D, Ivens B, van Slycken J, Broeck AV, Storme V, Boerjan W (2008) Structure of the genetic diversity in black poplar (Populus nigra L.) populations across European river systems: consequences for conservation and restoration. For Ecol Manag 255:1388–1399CrossRefGoogle Scholar
  62. Stamati K, Blackie S, Brown JWS, Russell J (2003) A set of polymorphic SSR loci for subarctic willow (Salix lanata, S. lapponum and S. herbacea). Mol Ecol Notes 3:280–282CrossRefGoogle Scholar
  63. Stamati K, Hollingsworth PM, Russell J (2007) Patterns of clonal diversity in three species of sub-arctic willow (Salix lanata, Salix lapponum and Salix herbacea). Plant Syst Evol 269:75–88CrossRefGoogle Scholar
  64. Steltzer H, Hufbauer RA, Welker JM, Casalis M, Sullivan PF, Chimner R (2008) Frequent sexual reproduction and high intraspecific variation in Salix arctica: implications for a terrestrial feedback to climate change in the High Arctic. J Geophys Res-Biogeo 113:11. doi: 10.1029/2007jg000503 Google Scholar
  65. Stewart JF, Liu YY, Tauer CG, Nelson CD (2010) Microsatellite versus AFLP analyses of pre-management introgression levels in loblolly pine (Pinus taeda L.) and shortleaf pine (P. echinata Mill.). Tree Genet Genomes 6:853–862CrossRefGoogle Scholar
  66. Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498–2504. doi: 10.1093/bioinformatics/btn478 PubMedCrossRefGoogle Scholar
  67. Valière N (2002) GIMLET: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2:377–379Google Scholar
  68. van Loo M, Joseph JA, Heinze B, Fay MF, Lexer C (2008) Clonality and spatial genetic structure in Populus × canescens and its sympatric backcross parent P. alba in a Central European hybrid zone. New Phytol 177:506–516PubMedGoogle Scholar
  69. van Puyvelde K, Triest L (2007) ISSRs indicate isolation by distance and spatial structuring in Salix alba populations along Alpine upstream rivers (Alto Adige and Upper Rhine). Belg J Bot 140:100–108Google Scholar
  70. Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935PubMedCrossRefGoogle Scholar
  71. Vekemans X, Beauwens T, Lemaire M, Roldan-Ruiz I (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol Ecol 11:139–151PubMedCrossRefGoogle Scholar
  72. Vos P, Hogers R, Bleeker M, Reijans M, Vandelee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP—a new technique for DNA-fingerprinting. Nucleic Acids Res 23:4407–4414PubMedCrossRefGoogle Scholar
  73. White GM, Boshier DH, Powell W (2002) Increased pollen flow counteracts fragmentation in a tropical dry forest: an example from Swietenia humilis Zuccarini. Proc Nat Acad Sci U S A 99:2038–2042CrossRefGoogle Scholar
  74. Winkler M, Koch M, Hietz P (2011) High gene flow in epiphytic ferns despite habitat loss and fragmentation. Conserv Genet 12:1411–1420PubMedCrossRefGoogle Scholar
  75. Yeh FC, Yang RC, Boyle TJB, Ye ZH, Mao JX (1999) POPGENE, the user-friendly shareware for population genetic analysis. Molecular Biology and Biotechnology Centre. University of Alberta, EdmontonGoogle Scholar
  76. Young AG, Brown AHD (1996) Comparative population genetic structure of the rare woodland shrub Daviesia suaveolens and its common congener D-mimosoides. Conserv Biol 10:1220–1228CrossRefGoogle Scholar
  77. Young AG, Merriam HG, Warwick SI (1993) The effect of forest fragmentation on genetic variation in Acer saccharum Marsh. (sugar maple) populations. Heredity 71:277–289CrossRefGoogle Scholar
  78. Young AG, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Michal Sochor
    • 1
  • Radim J. Vašut
    • 1
    Email author
  • Eva Bártová
    • 1
  • Ľuboš Majeský
    • 1
  • Jaroslav Mráček
    • 2
  1. 1.Department of Botany, Faculty of SciencePalacký University in OlomoucOlomoucCzech Republic
  2. 2.Department of Forest Botany, Dendrology and GeobiocoenologyMendel University in BrnoBrnoCzech Republic

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