Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Phylogeography of Populus alba (L.) and Populus tremula (L.) in Central Europe: secondary contact and hybridisation during recolonisation from disconnected refugia

Abstract

The central aim of this paper is to clarify the picture of postglacial recolonisation and the reconstruction of refugia of Populus alba (L.) and Populus tremula (L.) in the light of hybridisation of the two species. We focussed our study on Central and Southeastern Europe including reference samples from Spain, Sweden and Northern Africa.We investigated 414 individuals of 26 populations using restriction fragment length polymorphisms (PCR-RFLPs) in six maternally inherited chloroplast markers. Altogether, 57 haplotypes were analysed of which four indicated hybridisation events in the past. Phylogeographic structure was found for P. alba with low diversity in Eastern Europe versus high diversity in Italy and Central Europe. A lack of phylogeographic structure was assessed for P. tremula as expected for a boreal forest tree, and diversity was evenly distributed in the studied populations. Two main refugia were identified for P. alba in Italy and Romania. A previously described hybrid zone between species in Central Europe turned out also to be a zone of contact between southern and eastern chloroplast lineages in P. alba. In contrast, P. tremula recolonised its present habitats in Central Europe from several refugia near the former ice cap. We assume separate disconnected refugia for P. alba and P. tremula and suggest an immigration scenario involving the mixing of colonisation routes and interspecific introgression to be responsible for the observed patterns.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Bandelt H, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

  2. Bartels H (1987) Die Gattung Populus aus dendrologischer Sicht. Die Holzzucht (Hann Münden) 41:1–7

  3. Bittkau C (2002) Charakterisierung der genetischen Variation europäischer Populationen von Acer spp. und Populus tremula auf der Basis der Chloroplasten-DNA: Rückschlüsse auf die postglaziale Ausbreitung und Differenzierung forstlicher Provenienzen. Dissertation at the Technical University of Munich (Germany)

  4. Carcaillet C, Vernet JL (2001) Comments on "The full-glacial forests of central and South Eastern Europe" by Willis et al. Quaternary Res 55:385–387

  5. Comes HP, Kadereit JW (1998) The effect of quaternary climatic changes on plant distribution and evolution. Trends Plant Sci 3:432–438

  6. Cottrell JE, Krystufek V, Tabbener HE, Milner AD, Connolly T, Sing L, Fluch S, Burg K, Lefevre F, Achard P (2005) Postglacial migration of Populus nigra L.: lessons learnt from chloroplast DNA. Forest Ecol Manag 206:71–90

  7. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland

  8. Davis BAS, Brewer S, Stevenson AC, Guiot J, Data Contributors (2003) The temperature of Europe during the Holocene reconstructed from pollen data. Quaternary Sci Rev 22:1701–1716

  9. Dickmann DI, Kuzovkina J (2008) Poplars and willows in the world. Chapter 2 Working Paper IPC/9-2. FAO, Rome

  10. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bulletin 19:11–15

  11. Dumolin-Lapegue S, Demesure B, Fineschi S, Lecorre V, Petit RJ (1997) Phylogeographic structure of white oaks throughout the European continent. Genetics 146:1475–1487

  12. Eckenwalder JE (1996) Systematics and evolution of Populus. In: Stettler RF, Bradshaw HD, Heilman PE, Hinckley TM (eds) Biology of Populus and its implications for management and conservation. Natl Research Council Canada, Ottawa, pp 7–32

  13. Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

  14. Fischer MA, Adler W, Oswald K (2005) Exkursionsflora für Österreich, Liechtenstein und Südtirol. OÖ Landesmuseen, Linz

  15. Hamzeh M, Dayanandan S (2004) Phylogeny of Populus (Salicaceae) based on nucleotide sequences of chloroplast TRNT-TRNF region and nuclear rDNA. Am J Bot 91:1398–1408

  16. Heinze B (2007) A database of PCR primers for the chloroplast genomes of higher plants. Plant Methods 3:4

  17. Heuertz M, Hausman JF, Hardy OJ, Vendramin GG, Frascaria-Lacoste N, Vekemans X (2004) Nuclear microsatellites reveal contrasting patterns of genetic structure between western and southeastern European populations of the common ash (Fraxinus excelsior L.). Evolution 58:976–988

  18. Heuertz M, Carnevale S, Fineschi S, Sebastiani F, Hausman JF, Paule L, Vendramin GG (2006) Chloroplast DNA phylogeography of European ashes, Fraxinus sp. (Oleaceae): roles of hybridization and life history traits. Mol Ecol 15:2131–2140

  19. Hewitt GM (2001) Speciation, hybrid zones and phylogeography or seeing genes in space and time. Mol Ecol 10:537–549

  20. Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans R Soc B: Biol Sci 359:183–195

  21. Huntley B, Birks HJB (1983) An atlas of past and present pollen maps of Europe: 0–13000 years ago. Cambridge University Press, Cambridge

  22. Ingvarsson PK (2008) Mulitlocus patterns of nucleotide polymorphism and the demographic history of Populus tremula. Genetics 180:329–340

  23. Kotlik P, Berrebi P (2001) Phylogeography of the barbel (Barbus barbus) assessed by mitochondrial DNA variation. Mol Ecol 10:2177–2185

  24. Lazowski W (1997) Auen in Österrreich—Vegetation, Landschaft und Naturschutz. Monographien, Band 81. Umweltbundesamt, Vienna

  25. Le Corre V, Machon N, Petit RJ, Kremer A (1997) Colonization with long-distance seed dispersal and genetic structure of maternally inherited genes in forest trees: a simulation study. Genet Res (Cambridge) 69:117–125

  26. Lexer C, Fay MF, Joseph JA, Nica M-S, Heinze B (2005) Barrier to gene flow between two ecologically divergent Populus species, P. alba (white poplar) and P. tremula (European aspen): the role of ecology and life history in gene introgression. Mol Ecol 14:1045–1057

  27. Lexer C, Buerkle CA, Joseph JA, Heinze B, Fay MF (2007) Admixture in European Populus hybrid zones makes feasible the mapping of loci that contribute to reproductive isolation and trait differences. Heredity 98:74–84

  28. Lexer C, Joseph J, van Loo M, Prenner G, Heinze B, Chase MW, Kirkup D (2009) The use of digital image-based morphometrics to study the phenotypic mosaic in taxa with porous genomes. Taxon 58:5–20

  29. Maliouchenko O, Palmé AE, Buonamici A, Vendramin GG, Lascoux M (2007) Comparative phylogeography and population structure of European Betula species, with particular focus on B. pendula and B. pubescens. J Biogeogr 34:1601–1610

  30. Nathan R (2006) Long-distance dispersal of plants. Science 313:786–788

  31. Niklfeld H (1972) Der Niederösterreichische Alpenostrand-ein Glazialrefugium montaner Pflanzensippen. Jahrb Ver Schutze Alppflanzen -Tiere 37:42–94

  32. Niklfeld H (1974) Zur Historischen Deutung von Pflanzenarealen am Ostrand der Alpen. Wissenschaftliche Arbeiten Burgenland 54:46–52

  33. Palme AE, Semerikov V, Lascoux M (2003) Absence of geographical structure of chloroplast DNA variation in sallow, Salix caprea L. Heredity 91:465–474

  34. Palme AE, Su Q, Palsson S, Lascoux M (2004) Extensive sharing of chloroplast haplotypes among European birches indicates hybridization among Betula pendula. B. pubescens and B. nana. Mol Ecol 13:167–178

  35. Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

  36. Petit RJ, Aguinagalde I, De Beaulieu JL, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Muller-Starck GM, Demesure-Musch B, Palme A, Martin JP, Rendell S, Vendramin GG (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565

  37. Pons O, Petit RJ (1995) Estimation, variance and optimal sampling of gene diversity I. Haploid locus. Theor Appl Genet 90:462–470

  38. Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245

  39. Posada D, Crandall KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37–45

  40. Rajora OP, Dancik BP (1992) Chloroplast DNA inheritance in Populus. Theor Appl Genet 84:280–285

  41. Reynolds JB, Weir BS, Cockerham CC (1983) Estimation of the coancestry coefficient: basis for a short-term genetic distance. Genetics 105:767–779

  42. Rieseberg LH, Soltis DE (1991) Phylogenetic consequences of cytoplasmic gene flow in plants. Evol Trends Plants 5:65–84

  43. Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000: a software for population genetic data analysis. Genetics and Biometry Laboratory. University of Geneva, Switzerland

  44. Slavov G, DiFazio SP, Strauss SH (2004) Gene flow in forest trees: gene migration patterns and landscape modelling of transgene dispersion in hybrid poplar. In: Den Nijs HCM, Bartsch D, Sweet J (eds) Introgression from genetically modified plants into wild relatives. CABI Publishing, Wallingford

  45. Starmühlner F, Aschenbrenner L (1972) Naturnahe Landschaften, Pflanzen- und Tierwelt. In: Aschenbrenner L, Starmühlner F, Ehrendorfer F (eds) Naturgeschichte Wiens in 4 Bänden. Jugend und Volk Verl.-Ges, Vienna

  46. Stearns SC, Hoekstra RF (2005) Evolution. Oxford University Press Inc, New York

  47. Stewart JR, Lister AM (2001) Cryptic northern refugia and the origins of the modern biota. Trends Ecol Evol 16:608–613

  48. Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464

  49. Tuskan GA, DiFazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

  50. van Dillewijn C (1940) Zytologische Studien in der Gattung Populus L. Genetica 22:131–182

  51. van Loo M, Joseph JA, Heinze B, Fay MF, Lexer C (2008) Clonality and spatial genetic structure in Populus x canescens and its sympatric backcross parent P. alba in a Central European hybrid zone. New Phytol 177:506–516

  52. Widmer A, Lexer C (2001) Glacial refugia: sanctuaries for allelic richness, but not for gene diversity. Trends Ecol Evol 16:267–269

  53. Willis KJ, van Andel TH (2004) Trees or no trees? The environments of central and eastern Europe during the Last Glaciation. Quaternary Sci Rev 23:2369–2387

  54. Willis KJ, Rudner E, Sümegi P (2000) The full-glacial forests of Central and Southeastern Europe. Quaternary Res 53:203–213

Download references

Acknowledgement

We thank Wilfried Nebenführ, Hans Herz, Christian Fraissl, Franz Kovacs, Denes Bartha, Marius Sorin Nica and Adrian Ipati, for their help with sampling. We also thank Davorin Kajba, Sasa Bogdan, Attila Benke, Stefano Castiglione, Santiago González-Martínez, Helena Cvrčková and Pavlina Máchová for providing us with samples. We thank Maria del Carmen Calderón Pérez for her great help in the laboratory. Helpful advice on statistical analysis was given by Remy Petit. We thank Karl-Manfred Schweinzer for helping in designing the haplotype maps. This study was financially supported by the city of Vienna (Jubiläumsfonds der Stadt Wien für die Österreichische Akademie der Wissenschaften, J-6/2005), a DOC-fFORTE grant to B. Fussi (Österreichische Akademie der Wissenschaften) and by grant NE/E016731/1 of the British NERC to CL.

Author information

Correspondence to Barbara Fussi.

Additional information

Communicated by O. Savolainen

Electronic supplementary materials

Additional supporting information can be found in the online version of this article:

Appendix S1

Sampling locations and number of haplotypes per population (PDF 107 kb)

Appendix S2

Haplotype definition of eight variable fragments (PDF 37 kb)

Appendix S3

Haplotype distribution in Europe and Northern Africa (PDF 487 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Fussi, B., Lexer, C. & Heinze, B. Phylogeography of Populus alba (L.) and Populus tremula (L.) in Central Europe: secondary contact and hybridisation during recolonisation from disconnected refugia. Tree Genetics & Genomes 6, 439–450 (2010). https://doi.org/10.1007/s11295-009-0262-5

Download citation

Keywords

  • Postglacial recolonisation
  • Hybridisation
  • PCR-RFLPs
  • cpDNA
  • Populus alba
  • Populus tremula