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Chloroplast DNA variation in the European herb Silene dioica (red campion): postglacial migration and interspecific introgression

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Summary

Many recent studies of intraspecific geographic variation in maternally inherited chloroplast DNA (cpDNA) in European trees have revealed haplotype distributions that can be interpreted in terms of scenarios of postglacial migration and range expansion. However, there is still a lack of comparable information from widespread herb species. In the present study, we investigated the geographic distribution of cpDNA variation in 124 populations, covering a large part of the range of the widespread, dioecious, European herb, Silene dioica. PCR-RFLP analysis revealed 24 different cpDNA haplotypes. As in the majority of European tree species, the large-scale geographic distributions of the most common S. dioica haplotypes suggest that the species colonized Europe from more than one geographic source. Material from 16 populations of S. latifolia and five hybrid populations was also included in the study for comparative purposes. Five out of seven haplotypes detected in S. latifolia were shared with S. dioica. The similarity of the geographic distributions of the shared haplotypes in both species is consistent with a history of past and/or recent interspecific hybridization and introgression between these closely related plants. The two haplotypes detected only in S. latifolia were present in populations in the Mediterranean region – on the southern margin of the species’ area of sympatry, or outside the range of S. dioica.

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References

  • Abbott RJ and Comes HP (2003). Evolution in the Arctic: a phylogeographic analysis of the circumarctic plant, Saxifraga oppositifolia (Purple saxifrage). New Phytol 161: 211–224

    Article  CAS  Google Scholar 

  • Bacilieri R, Ducousso A, Petit RJ and Kremer A (1996). Mating system and asymmetric hybridization in a mixed stand of European oaks. Evolution 50: 900–908

    Article  Google Scholar 

  • Baker HG (1947). Biological flora of the British Isles. Melandrium (Roehling em.) Fries. (Lychnis L. (1753) partim.). J Ecol 35: 271–292

    Article  Google Scholar 

  • Baker HG (1948). Stages in invasion and replacement demonstrated by species of Melandrium. J Ecol 36: 96–119

    Article  Google Scholar 

  • Brewer S, Cheddadi R, de Beaulieu JL, and Reille M (2002). The spread of deciduous Quercus throughout Europe since the last glacial period. For Ecol Manage 156: 27–48

    Article  Google Scholar 

  • Comes HP and Abbott RJ (2001). Molecular phylogeny, reticulation and lineage sorting in Mediterranean Senecio sect. Senecio (Asteraceae). Evolution 55: 1943–1962

    PubMed  CAS  Google Scholar 

  • Comes HP and Kadereit JW (1998). The effect of Quaternary climatic changes on plant distribution and evolution. Trends Pl Sci 3: 432–438

    Article  Google Scholar 

  • Demesure B, Sodzi N and Petit RJ (1995). A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Molec Ecol 4: 129–131

    Article  CAS  Google Scholar 

  • Desfeux C and Lejeune B (1996). Systematics of Euromediterranean Silene (Caryophyllaceae): evidence from a phylogenetic analysis using ITS sequences. Comptes Rendus de L’Academie des Sciences Paris, Serie III – Sciences de la Vie/Life Sciences 319: 351–358

    CAS  Google Scholar 

  • Desplanque B, Viard F, Bernard J, Forcioli D, Saumitou-Laprade P, Cuguen J and van Dijk H (2000). The linkage disequilibrium between chloroplast DNA and mitochondrial DNA haplotypes in Beta vulgaris ssp. maritima (L.): the usefulness of both genomes for population genetic studies. Molec Ecol 9: 141–154

    Article  CAS  Google Scholar 

  • Dumolin-Lapègue S, Demesure B, Fineschi S Le Corre V and Petit RJ (1997). Phylogeographic structure of white oaks throughout the European continent. Genetics 146: 1475–1487

    PubMed  Google Scholar 

  • Dumolin-Lapègue S, Kremer A and Petit RJ (1999). Are chloroplast and mitochondrial DNA variation species independent in oaks?. Evolution 53: 1406–1413

    Article  Google Scholar 

  • Ennos RA (1994). Estimating the relative rates of pollen and seed migration among plant populations. Heredity 72: 250–259

    Article  Google Scholar 

  • Excoffier L, Laval G and Schneider S (2005). Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1: 47–50

    CAS  PubMed  Google Scholar 

  • Ferris C, Oliver RP, Davy AJ and Hewitt GM (1993). Native oak chloroplasts reveal an ancient divide across Europe. Molec Ecol 2: 337–344

    Article  CAS  Google Scholar 

  • Ferris C, King RA, Väinölä R and Hewitt GM (1998). Chloroplast DNA recognizes three refugial sources of European oaks and suggests independent eastern and western immigrations to Finland. Heredity 80: 584–593

    Article  PubMed  Google Scholar 

  • Filatov DA, Laporte V, Vitte C and Charlesworth D (2001). DNA Diversity in sex-linked and autosomal genes of the plant species Silene latifolia and Silene dioica. Molec Biol Evol 18: 1442–1454

    PubMed  CAS  Google Scholar 

  • Fjellheim S, Rognli OA, Fosnes K and Brochmann C (2006). Phylogeographical history of the widespread meadow fescue (Festuca pratensis Huds.) inferred from chloroplast DNA sequences. J Biogeogr 33: 1470–1478

    Article  Google Scholar 

  • Giles BE and Goudet J (1997). Genetic differentiation in Silene dioica metapopulations: estimation of spatio-temporal effects in a successional plant species. Amer Naturalist 149: 507–526

    Article  Google Scholar 

  • Goulson D and Jerrim K (1997). Maintenance of the species boundary between Silene dioica and S. latifolia (red and white campion). Oikos 79: 115–126

    Article  CAS  Google Scholar 

  • Griffin SR and Barrett SCH (2004). Post-glacial history of Trillium grandiflorum (Melanthiaceae) in eastern North America: inferences from phylogeography. Amer J Bot 91: 465–473

    Article  CAS  Google Scholar 

  • Heuertz M, Fineschi S, Anzidei M, Pastorelli R, Salvini D, Paule L, Frascaria-Lacoste N, Hardy OJ, Vekemans X and Vendramin GG (2004). Chloroplast DNA variation and postglacial recolonization of common ash (Fraxinus excelsior L.) in Europe. Molec Ecol 13: 3437–3452

    Article  CAS  Google Scholar 

  • Heuertz M, Carnevale S, Fineschi S, Sebastiani F, Hausman JF, Paule L and Vendramin GG (2006). Molec Ecol 15: 2131–2140

    Article  CAS  Google Scholar 

  • Hewitt GM (1996). Some genetic consequences of ice ages and their role in divergence and speciation. Biol J Linn Soc 58: 247–276

    Google Scholar 

  • Hewitt GM (1999). Post-glacial re-colonization of European biota. Biol J Linn Soc 68: 87–112

    Google Scholar 

  • Hewitt GM (2000). The genetic legacy of the Quaternary ice ages. Nature 405: 907–913

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ibrahim KM, Nichols RA and Hewitt GM (1996). Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77: 282–291

    Article  Google Scholar 

  • Ironside JE and Filatov D (2005). Extreme population structure and high interspecific divergence of the Silene Y chromosome. Genet 171: 705–713

    Article  CAS  Google Scholar 

  • Jalas J, Suominen J (1986) Atlas Florae Europaeae, vol 7. Caryophyllaceae (Silenoideae). The Committee for the Mapping of the Flora of Europe and Societas Biologica Fennica, Vanamo, Helsingin Liikekirjapaino Oy, Helsinki

  • King RA and Ferris C (1998). Chloroplast DNA phylogeography of Alnus glutinosa (L.) Gaertn. Molec Ecol 7: 1151–1162

    Article  CAS  Google Scholar 

  • King RA and Ferris C (2000). Chloroplast DNA and nuclear DNA variation in the sympatric alder species, Alnus cordata (Lois.) Duby and Alnus glutinosa (L.) Gaertn. Biol J Linn Soc 70: 147–160

    Google Scholar 

  • Kremer A, Kleinschmit J, Cottrell J, Cundall EP, Deans JD, Ducousso A, König A, Lowe AD, Munro R, Petit RJ and Stephan BR (2002). Is there a correlation between chloroplastic and nuclear divergence, or what are the roles of history and selection on genetic diversity in European oaks?. For Ecol Manage 156: 75–87

    Article  Google Scholar 

  • Laporte V, Filatov DA, Kamau E and Charlesworth D (2005). Indirect evidence from DNA sequence diversity for genetic degeneration of the Y-chromosome in dioecious species of the plant Silene: the SlY4/SlX4 and DD44-X/DD44-Y gene pairs. J Evol Biol 18: 337–347

    Article  PubMed  CAS  Google Scholar 

  • Magni CR, Ducousso A, Caron H, Petit RJ and Kremer A (2005). Chloroplast variation of Quercus rubra L. in North America and comparison with other Fagaceae. Molec Ecol 14: 513–524

    Article  CAS  Google Scholar 

  • Malm JU and 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

    Article  Google Scholar 

  • Malm JU and Prentice HC (2005). Chloroplast DNA haplotypes in Nordic Silene dioica: postglacial immigration from the east and the south. Pl Syst Evol 250: 27–38

    Article  CAS  Google Scholar 

  • Mátyás G and Sperisen C (2001). Chloroplast DNA polymorphisms provide evidence for postglacial re-colonization of oaks (Quercus spp.) across the Swiss Alps. Theor Appl Genet 102: 12–20

    Article  Google Scholar 

  • McCauley DE (1994). Contrasting the distribution of chloroplast DNA and allozyme polymorphism among local populations of Silene alba: implications for studies of gene flow in plants. Proc Natl Acad Sci USA 91: 8127–8131

    Article  PubMed  CAS  Google Scholar 

  • McCauley DE (1997). The relative contributions of seed and pollen movement to the local genetic structure of Silene alba. J Heredity 88: 257–263

    Google Scholar 

  • Minder AM, Rothenbuehler C and Widmer A (2007). Genetic structure of hybrid zones between Silene latifolia and Silene dioica (Caryophyllaceae): evidence for introgressive hybridization. Molec Ecol 16: 2504–2516

    Article  CAS  Google Scholar 

  • Oddou-Muratorio S, Petit RJ, Le Guerroue, Guesnet D and Demesure B (2001). Pollen- versus seed-mediated gene flow in a scattered forest tree species. Evol 55: 1123–1135

    CAS  Google Scholar 

  • Page RDM (1996). TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12: 357–358

    PubMed  CAS  Google Scholar 

  • Palmé AE and Vendramin GG (2002). Chloroplast DNA variation, postglacial recolonization and hybridization in hazel, Corylus avellana. Molec Ecol 11: 1769–1779

    Article  Google Scholar 

  • Palmé AE, Su Q, Rautenberg A, Manni F and Lascoux M (2003). Postglacial recolonization and cpDNA variation of silver birch, Betula pendula. Molec Ecol 12: 201–212

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Petit RJ, Kremer A and Wagner DB (1993). Geographic structure of chloroplast DNA polymorphisms in European oaks. Theor Appl Genet 87: 122–128

    Article  CAS  Google Scholar 

  • Petit RJ, Pineau E, Demesure B, Bacilieri R, Ducousso A and Kremer A (1997). Chloroplast DNA footprints of postglacial recolonization by oaks. Proc Natl Acad Sci USA 94: 9996–10001

    Article  PubMed  CAS  Google Scholar 

  • Petit RJ, Brewer S, Bordács S, Burg K, Cheddadi R, Coart E, Cottrell J, Csaikl UM, van Dam B, Deans JD, Espinel S, Fineschi S, Finkeldey R, Glaz I, Goicoechea PG, Jensen JS, König AO, Lowe AJ, Madsen SF, Mátyás G, Munro RC, Popescu F, Slade D, Tabbener H, de Vries SGM, Ziegenhagen B, de Beaulieu J-L and Kremer A (2002a). Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. For Ecol Manage 156: 49–74

    Article  Google Scholar 

  • Petit RJ, Csaikl UM, Bordács S, Burg K, Coart E, Cottrell J, van Dam B, Deans JD, Dumolin-Lapègue S, Fineschi S, Finkeldey R, Gillies A, Glaz I, Goicoechea PG, Jensen JS, König AO, Lowe AJ, Madsen SF, Mátyás G, Munro RC, Olalde M, Pemonge M-H, Popescu F, Slade D, Tabbener H, Taurchini D, de Vries SGM, Ziegenhagen B and Kremer A (2002b). Chloroplast DNA variation in European white oaks: phylogeography and patterns of diversity based on data from over 2600 populations. For Ecol Manage 156: 5–26

    Article  Google Scholar 

  • Petit RJ, Bodénès C, Ducousso A, Roussel G and Kremer A (2003). Hybridization as a mechanism of invasion in oaks. New Phytol 161: 151–164

    Article  CAS  Google Scholar 

  • Potts BM and Reid JB (1988). Hybridization as a dispersal mechanism. Evolution 42: 1245–1255

    Article  Google Scholar 

  • Prentice HC (1978). Experimental taxonomy of Silene section Elisanthe (Caryophyllaceae): crossing experiments. Bot J Linn Soc 77: 203–216

    Article  Google Scholar 

  • Prentice HC (1979). Numerical analysis of infraspecific variation in European Silene alba and S. dioica (Caryophyllaceae). Bot J Linn Soc 78: 181–212

    Article  Google Scholar 

  • Prentice HC (1980). Variation in Silene dioica (L.) Clairv.: numerical analysis of populations from Scotland. Watsonia 13: 11–26

    Google Scholar 

  • Prentice HC (1986a). Climate and clinal variation in seed morphology of the white campion, Silene latifolia (Caryophyllaceae). Biol J Linn Soc 27: 179–189

    Article  Google Scholar 

  • Prentice HC (1986b). Continuous variation and classification. In: Styles, BT (eds) Infraspecific classification of wild and cultivated plants, pp 21–32. Oxford University Press, Oxford

    Google Scholar 

  • Prentice HC (1988). Silene section Elisanthe in the Iberian Peninsula. Monografías del Instituto Pirenaico de Ecología, Jaca 4: 321–324

    Google Scholar 

  • Prentice HC, Malm JU, Mateu-Andrés I and Segarra-Moragues JG (2003). Allozyme and chloroplast DNA variation in island and mainland populations of the rare Spanish endemic, Silene hifacensis (Caryophyllaceae). Conserv Genet 4: 543–555

    Article  CAS  Google Scholar 

  • Purrington CB and Schmitt J (1995). Sexual dimorphism of dormancy and survivorship in buried seeds of Silene latifolia. J Ecol 83: 795–800

    Article  Google Scholar 

  • Rieseberg LH and Soltis DE (1991). Phylogenetic consequences of cytoplasmic gene flow in plants. Evol Trends Pl 5: 65–84

    Google Scholar 

  • Rieseberg LH and Welch ME (2002). Gene transfer through introgressive hybridization: history, evolutionary significance and phylogenetic consequences. In: Syvanen, M and Kado, CI (eds) Horizontal gene transfer, pp 199–216. Academic Press, San Diego

    Chapter  Google Scholar 

  • Rieseberg LH, Beckstrom-Sternberg S and Doan K (1990). Helianthus annuus ssp. texanus has chloroplast DNA and nuclear ribosomal RNA genes of Helianthus debilis ssp. cucumerifolius. Proc Natl Acad Sci USA 87: 593–597

    Article  PubMed  CAS  Google Scholar 

  • Runyeon-Lager H and Prentice HC (2000). Morphometric variation in a hybrid zone between the weed, Silene vulgaris and the endemic, Silene uniflora ssp. petraea (Caryophyllaceae), on the Baltic island of Öland. Canad J Bot 78: 1384–1397

    Article  Google Scholar 

  • Schaal BA, Hayworth DA, Olsen KM, Rauscher JT and Smith WA (1998). Phylogeographic studies in plants: problems and prospects. Molec Ecol 7: 465–474

    Article  Google Scholar 

  • Schönswetter P, Popp M and Brochmann C (2006). Rare arctic-alpine plants of the European Alps have different immigration histories: the snowbed species Minuartia biflora and Ranunculus pygmaeus. Molec Ecol 15: 709–720

    Article  CAS  Google Scholar 

  • Soltis DE, Gitzendanner MA, Strenge DD and Soltis PS (1997). Chloroplast DNA intraspecific phylogeography of plants from the Pacific Northwest of North America. Pl Syst Evol 206: 353–373

    Article  Google Scholar 

  • Taberlet P, Gielly L, Patou G and Bouvet J (1991). Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Molec Biol 17: 1105–1109

    Article  CAS  Google Scholar 

  • Taberlet P, Fumagalli L, Wust-Saucy A-G and Cosson J-F (1998). Comparative phylogeography and postglacial colonization routes in Europe. Molec Ecol 7: 453–464

    Article  CAS  Google Scholar 

  • Tsitrone A, Kirkpatrick M and Levin DA (2003). A model for chloroplast capture. Evolution 57: 1776–1782

    PubMed  Google Scholar 

  • Tyler T, Prentice HC and Widén B (2002). Geographic variation and dispersal history in Fennoscandian populations of two forest herbs. Pl Syst Evol 233: 47–64

    Article  Google Scholar 

  • Vellekoop P, Buntjer JB, Maas JW and van Brederode J (1996). Can the spread of agriculture in Europe be followed by tracing the spread of the weed Silene latifolia. A RAPD study. Theor Appl Genet 92: 1085–1090

    Article  Google Scholar 

  • Walters SM (1975). Silene L. In: Stace, CA (eds) Hybridization and the flora of the British Isles, pp 168–169. Academic Press, London

    Google Scholar 

  • Whittemore AT and Schaal BA (1991). Interspecific gene flow in sympatric oaks. Proc Natl Acad Sci USA 88: 2540–2544

    Article  PubMed  CAS  Google Scholar 

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  1. Plant Ecology and Systematics, Department of Ecology, Lund University, Sölvegatan 37, 223 62, Lund, Sweden

    Honor C. Prentice, J. U. Malm & L. Hathaway

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  1. Honor C. Prentice
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  2. J. U. Malm
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Prentice, H.C., Malm, J.U. & Hathaway, L. Chloroplast DNA variation in the European herb Silene dioica (red campion): postglacial migration and interspecific introgression. Plant Syst Evol 272, 23–37 (2008). https://doi.org/10.1007/s00606-007-0629-8

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