Skip to main content
SpringerLink
Log in

Allopolyploid origin of the Balkan endemic Ranunculus wettsteinii (Ranunculaceae) inferred from nuclear and plastid DNA sequences

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

The Balkan Peninsula, characterized by high rates of endemism, is recognised as one of the most diverse and species-rich areas of Europe. However, little is known about the origin of Balkan endemics. The present study addresses the phylogenetic position of the Balkan endemic Ranunculus wettsteinii, as well as its taxonomic status and relationship with the widespread R. parnassiifolius, based on nuclear DNA (internal transcribed spacer, ITS) and plastid regions (rpl32-trnL, rps16-trnQ, trnK-matK and ycf6-psbM). Maximum parsimony and Bayesian inference analyses revealed a well-supported clade formed by accessions of R. wettsteinii. Furthermore, our phylogenetic and network analyses supported previous hypotheses of a likely allopolyploid origin for R. wettsteinii between R. montenegrinus and R. parnassiifolius, with the latter as the maternal parent.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Albach, D. C., von Sternburg, M., Scalone, R., & Bardy, K. E. (2009). Phylogenetic analysis and differentiation of Veronica subgenus Stenocarpon in the Balkan Peninsula. Botanical Journal of the Linnean Society, 159, 616–636.

    Article  Google Scholar 

  • Baltisberger, M. (1992). Botanische Notizen und zytologische Untersuchungen an einigen Pflanzen (insbesondere aus den Gattungen Ranunculus und Achillea) aus dem albanisch-jugoslawischen Grenzgebiet (Korab, Sar Planina). Berichte des Geobotanischen Institutes der Eidgenössische Technische Hochschule, Stiftung Rübel, Zürich 58, 192–211.

  • Bardy, K. E., Albach, D. C., Schneeweiss, G. M., Fischer, M. A., & Schönswetter, P. (2010). Disentangling phylogeography, polyploid evolution and taxonomy of a woodland herb (Veronica chamaedrys group, Plantaginaceae s.l.) in southeastern Europe. Molecular Phylogenetics and Evolution, 57, 771–786.

    Article  PubMed Central  PubMed  Google Scholar 

  • Bennett, K. D., Tzedakis, P. C., & Willis, K. J. (1991). Quaternary refugia of north European trees. Journal of Biogeography, 18, 103–115.

    Article  Google Scholar 

  • Bittkau, C., & Comes, H. P. (2005). Evolutionary processes in a continental island system: molecular phylogeography of the Aegean Nigella arvensis alliance (Ranunculaceae) inferred from chloroplast DNA. Molecular Ecology, 14, 4065–4083.

    Article  CAS  PubMed  Google Scholar 

  • Brochmann, C., Gabrielsen, T. M., Nordal, I., Landvik, J. Y., & Elven, R. (2003). Glacial survival or tabula rasa? The history of North Atlantic biota revisited. Taxon, 52, 417–450.

    Article  Google Scholar 

  • Casazza, G., Granato, L., Minuto, L., & Conti, E. (2012). Polyploid evolution and Pleistocene glacial cycles: a case study from the alpine primrose Primula marginata (Primulaceae). BMC Evolutionary Biology, 12, 56.

    Article  PubMed Central  PubMed  Google Scholar 

  • Chase, M. W., Paun, O., & Fay, M. F. (2010). Hybridization and speciation in angiosperms: a role for pollinator shifts? BMC Biology, 8, 45.

    Article  PubMed Central  PubMed  Google Scholar 

  • Cires, E., & Fernández Prieto, J. A. (2012). The Iberian endemic species Ranunculus cabrerensis Rothm.: an intricate history in the Ranunculus parnassiifolius L. polyploid complex. Plant Systematics and Evolution, 298, 121–138.

    Article  Google Scholar 

  • Cires, E., Cuesta, C., Peredo, E. L., Revilla, M. A., & Fernández Prieto, J. A. (2009). Genome size variation and morphological differentiation within Ranunculus parnassifolius group (Ranunculaceae) from calcareous screes in the Northwest of Spain. Plant Systematics and Evolution, 281, 193–208.

    Article  Google Scholar 

  • Cires, E., Cuesta, C., Revilla, M. A., & Fernández Prieto, J. A. (2010). Intraspecific genome size variation and morphological differentiation of Ranunculus parnassifolius (Ranunculaceae), an Alpine-Pyrenean-Cantabrian polyploid group. Botanical Journal of the Linnean Society, 101, 251–271.

    Article  Google Scholar 

  • Cires, E., Cuesta, C., Fernández Casado, M. A., Fernández-Carvajal, M. C., & Fernández Prieto, J. A. (2011). Malformación polínica y niveles de ploidía en Ranunculus grex parnassiifolius. Acta Botanica Malacitana, 36, 145–158.

    Google Scholar 

  • Cires, E., Cuesta, C., Vargas, P., & Fernández Prieto, J. A. (2012). Unravelling the evolutionary history of the polyploid complex Ranunculus parnassiifolius (Ranunculaceae). Botanical Journal of the Linnean Society, 107, 477–493.

    Article  Google Scholar 

  • Dolphin, K., Belshaw, R., Orme, C. D. L., & Quicke, D. L. J. (2000). Noise and incongruence: interpreting results of the incongruence length difference test. Molecular Phylogenetics and Evolution, 17, 401–406.

    Article  CAS  PubMed  Google Scholar 

  • Dörfler, I. (1918). Ranunculus wettsteinii Dörfler spec. nova. Anzeiger der Kaiserliche Akademie der wissenschaften in Wien–Mathematisch-naturwissenschaftliche Klasse 55. 282.

  • Dumolin-Lapègue, S., Pemonge, M.-H., & Petit, R. J. (1997). An enlarged set of consensus primers for the study of organelle DNA in plant. Molecular Ecology, 6, 393–397.

    Article  PubMed  Google Scholar 

  • Ehlers, J., & Gibbard, P. L. (2003). Extent and chronology of glaciations. Quaternary Science Reviews, 22, 1561–1568.

    Article  Google Scholar 

  • Emadzade, K., & Hörandl, E. (2011). Northern Hemisphere origin, transoceanic dispersal, and diversification of Ranunculeae DC. (Ranunculaceae) in the Cenozoic. Journal of Biogeography, 38, 517–530.

    Article  Google Scholar 

  • Emadzade, K., Lehnebach, C., Lockhart, P., & Hörandl, E. (2010). A molecular phylogeny, morphology and classification of genera of Ranunculeae (Ranunculaceae). Taxon, 59, 809–828.

    Google Scholar 

  • Farris, J. S., Källersjö, M., Kluge, A. G., & Bult, C. (1995). Testing significance of incongruence. Cladistics, 10, 315–319.

    Article  Google Scholar 

  • Frajman, B., & Oxelman, B. (2007). Reticulate phylogenetics and phytogeographical structure of Heliosperma (Sileneae, Caryophyllaceae) inferred from chloroplast and nuclear DNA sequences. Molecular Phylogenetics and Evolution, 43, 140–155.

    Article  CAS  PubMed  Google Scholar 

  • Frajman, B., & Schneeweiss, G. M. (2009). A Campanulaceous fate: the Albanian stenoendemic Asyneuma comosiforme in fact belongs to isophyllous Campanula. Systematic Botany, 34, 595–601.

    Article  Google Scholar 

  • Frodin, D. G. (2004). History and concepts of big plant genera. Taxon, 53, 753–776.

    Article  Google Scholar 

  • Gaston, K. J., & David, R. (1994). Hotspots across Europe. Biodiversity Letters, 2, 108–116.

    Article  Google Scholar 

  • Hayek, A. (1924). Zweiter Beitrag zur Kenntnis der Flora von Albanien. Anzeiger der Kaiserliche Akademie der wissenschaften in Wien–Mathematisch-naturwissenschaftliche Klasse 99, 101–223.

  • Hewitt, G. M. (2000). The genetic legacy of the Quaternary iceages. Nature, 405, 907–913.

    Article  CAS  PubMed  Google Scholar 

  • Hipp, A. L., Hall, J. C., & Sytsma, K. J. (2004). Phylogenetic accuracy, congruence between data partitions, and performance of the ILD. Systematic Biology, 53, 81–89.

    Article  PubMed  Google Scholar 

  • Hörandl, E., & Emadzade, K. (2012). Evolutionary classification: a case study on the diverse plant genus Ranunculus L. (Ranunculaceae). Perspectives in Plant Ecology Evolution and Systematics, 14, 310–324.

    Article  Google Scholar 

  • Hörandl, E., Paun, O., Johansson, J. T., Lehnebach, C., Armstrong, T., Chen, L., et al. (2005). Phylogenetic relationships and evolutionary traits in Ranunculus s.l. (Ranunculaceae) inferred from ITS sequence analysis. Molecular Phylogenetics and Evolution, 36, 305–327.

    Article  PubMed  Google Scholar 

  • Huber, W. (1988). Natürliche Bastardierungen zwischen weissblühenden Ranunculus-Arten in den Alpen. Veröffentlichungen des Geobotanischen Institutes der ETH Zürich, Stiftung Rübel 100, 1–160.

  • Husband, B. C. (2000). Constraints on polyploid evolution: a test of the minority cytotype exclusion principle. Proceedings of the Royal Society B, 267, 217–223.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huson, D. H., & Bryant, D. (2006). Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23, 254–267.

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim, K. M., Nichols, R. A., & Hewitt, G. M. (1996). Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity, 77, 282–291.

    Article  Google Scholar 

  • Johnson, L. A., & Soltis, D. E. (1994). matK DNA sequences and phylogenetic reconstruction in Saxifragaceae s.s. Systematic Botany, 19, 143–156.

    Article  Google Scholar 

  • Krigas, N., Mouflis, G., Grigoriadou, K., & Maloupa, E. (2010). Conservation of important plants from the Ionian Islands at the Balkan Botanic Garden of Kroussia, N Greece: linking with GIS the in situ collection data with plant propagation and the ex situ cultivation. Biodiversity and Conservation, 19, 3583–3603.

    Article  Google Scholar 

  • Kryštufek, B., & Reed, J. M. (2004). Pattern and process in Balkan biodiversity—an overview. In H. I. Griffiths, B. Kryštufek, & J. M. Reed (Eds.), Balkan biodiversity—pattern and process in the European hotspot (pp. 1–8). Dordrecht: Kluwer.

    Chapter  Google Scholar 

  • Kučera, J., Tremetsberger, K., Vojta, J., & Marhold, K. (2008). Molecular study of the Cardamine maritima group (Brassicaceae) from the Balkan and Apennine Peninsulas based on amplified fragment length polymorphism. Plant Systematics and Evolution, 275, 193–207.

    Article  Google Scholar 

  • Lo Presti, R. M., Oppolzer, S., & Oberprieler, C. (2010). A molecular phylogeny and a revised classification of the Mediterranean genus Anthemis s.l. (Compositae, Anthemideae) based on three molecular markers and micromorphological characters. Taxon, 59, 1441–1456.

    Google Scholar 

  • Magyari, E. K., Chapman, J. C., Gaydarska, B., Marinova, E., Deli, T., Huntley, J. P., et al. (2008). The ‘oriental’ component of the Balkan flora: evidence of its presence on the Thracian Plain during the Weichselian late-glacial. Journal of Biogeography, 35, 865–883.

    Article  Google Scholar 

  • Mallet, J. (2007). Hybrid speciation. Nature, 446, 279–283.

    Article  CAS  PubMed  Google Scholar 

  • Mereďa, P., Jr., Hodálová, I., Kučera, J., Zozomová-Lihová, J., Letz, D. R., & Slovák, M. (2011). Genetic and morphological variation in Viola suavis s.l. (Violaceae) in the western Balkan Peninsula: two endemic subspecies revealed. Systematics and Biodiversity, 9, 211–231.

    Article  Google Scholar 

  • Ministry of Environment and Physical Planning (2003). Country study for biodiversity of the Republic of Macedonia (First National Report), Skopje.

  • Nei, M., & Kumar, S. (2000). Molecular evolution and phylogenetics. New York: Oxford University Press.

    Google Scholar 

  • Nylander, J. A. A. (2004). MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University. Available at: http://www.abc.se/~nylander/.

  • Park, J.-M., Kovačić, S., Liber, Z., Eddie, W. M. M., & Schneeweiss, G. M. (2006). Phylogeny and biogeography of isophyllous species of Campanula (Campanulaceae) in the Mediterranean area. Systematic Botany, 31, 862–880.

    Article  Google Scholar 

  • Paun, O., Lehnebach, C., Johansson, J. T., Lockhart, P., & Hörandl, E. (2005). Phylogenetic relationships and biogeography of Ranunculus and allied genera (Ranunculaceae) in the Mediterranean region and in the European alpine system. Taxon, 54, 911–930.

    Article  Google Scholar 

  • Paun, O., Forest, F., Fay, M. F., & Chase, M. W. (2009). Hybrid speciation in angiosperms: parental divergence drives ploidy. New Phytologist, 182, 507–518.

    Article  PubMed Central  PubMed  Google Scholar 

  • Rambaut, A., & Drummond, A. J. (2007). Tracer v1.5. See http://beast.bio.ed.ac.uk/Tracer.

  • Ramsey, J., & Schemske, D. W. (1998). Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annual Review of Ecology and Systematics, 29, 467–501.

    Article  Google Scholar 

  • Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.

    Article  PubMed Central  PubMed  Google Scholar 

  • Schönswetter, P., & Schneeweiss, G. M. (2009). Androsace komovensis sp. nov., a long mistaken local endemic from the southern Balkan Peninsula with biogeographic links to the Eastern Alps. Taxon, 58, 544–549.

    Google Scholar 

  • Shaw, J., Lickey, E. B., Beck, J. T., Farmer, S. B., Liu, W., Miller, J., et al. (2005). The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. American Journal of Botany, 92, 142–166.

    Article  CAS  PubMed  Google Scholar 

  • Shaw, J., Lickey, E. B., Schilling, E. E., & Small, R. L. (2007). Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. American Journal of Botany, 94, 275–288.

    Article  CAS  PubMed  Google Scholar 

  • Slovák, M., Urfus, T., Vít, P., & Marhold, K. (2009). The Balkan endemic Picris hispidissima (Compositae): morphology, nuclear DNA content and relationship to the polymorphic P. hieracioides. Plant Systematics and Evolution, 278, 187–201.

    Article  Google Scholar 

  • Stebbins, G. L. (1984). Polyploidy and the distribution of the arctic-alpine flora: new evidence and a new approach. Botanica Helvetica, 94, 1–14.

    Google Scholar 

  • Sun, Y., Skinner, D. Z., Liang, G. H., & Hulbert, S. H. (1994). Phylogenetic analysis of Sorghum and related taxa using internal transcribed spacers of nuclear ribosomal DNA. Theoretical and Applied Genetics, 89, 26–32.

    Article  CAS  PubMed  Google Scholar 

  • Surina, B., Schönswetter, P., & Schneeweiss, G. M. (2011). Quaternary range dynamics of ecologically divergent species (Edraianthus serpyllifolius and E. tenuifolius, Campanulaceae) within the Balkan refugium. Journal of Biogeography, 38, 1381–1393.

    Article  Google Scholar 

  • Swofford, D. L. (2002). PAUP* Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland. Massachusetts: Sinauer Associates.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tamura, M. (1995). Angiospermae. Ordnung Ranunculales. Fam. Ranunculaceae. II. Systematic Part. In P. Hiepko (Ed.), Die natürliche Pflanzenfamilien, ed. 2, 17aIV (pp. 223–519). Berlin: Duncker & Humblot.

    Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thompson, J. D., & Lumaret, R. (1992). The evolutionary dynamics of polyploid plants: origins, establishment and persistence. Trends in Ecology & Evolution, 7, 302–307.

    Article  CAS  Google Scholar 

  • Tutin, T. G., & Akeroyd, J. R. (1993). Ranunculus L. In T. G. Tutin, N. A. Burges, A. O. Chater, J. R. Edmondson, V. H. Heywood, D. M. Moore, D. H. Valentine, S. M. Walters, & D. A. Webb (Eds.), Flora Europaea. Vol. 1. Psilotaceae to Platanaceae (2nd ed., pp. 269–286). Cambridge: Cambridge University Press.

    Google Scholar 

  • Tzedakis, P. C., Lawson, I. T., Frogley, M. R., Hewitt, G. M., & Preece, R. C. (2002). Buffered tree population changes in a Quaternary refugium: evolutionary implications. Science, 297, 2044–2047.

    Article  CAS  PubMed  Google Scholar 

  • Walter, K. S., & Gillett, H. J. (1998). 1997 IUCN Red List of Threatened Plants. Compiled by the World Conservation Monitoring Centre (p. 484). Gland, Switzerland and Cambridge, UK: IUCN—The World Conservation Union.

    Google Scholar 

Download references

Acknowledgments

The authors thank Emilio Cano for laboratory assistance and Bernardo García for helping with the sampling. We would like to thank three anonymous reviewers for useful comments that improved the manuscript. Part of this work was conducted during a short stay of E. Cires at Real Jardín Botánico de Madrid (CSIC) funded partially by the University of Oviedo (V20090232). This research was funded by the Spanish Ministry of Science (CGL2006-11743).

Author information

Author notes

  1. Eduardo Cires & Candela Cuesta

    Present address: Institute of Science and Technology Austria (IST Austria), Am Campus 1, 3400, Klosterneuburg, Austria

Authors and Affiliations

  1. Departamento de Biología de Organismos y Sistemas, Universidad de Oviedo, Catedrático Rodrigo Uría s/n, 33071, Oviedo, Spain

    Eduardo Cires & José Antonio Fernández Prieto

  2. Plant Ecological Genetics, Institute of Integrative Biology, ETH Zurich, Universitaetstr. 16, 8092, Zurich, Switzerland

    Matthias Baltisberger

  3. Real Jardín Botánico de Madrid, CSIC, Plaza Murillo 2, 28014, Madrid, Spain

    Pablo Vargas

Authors
  1. Eduardo Cires
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthias Baltisberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Candela Cuesta
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pablo Vargas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. José Antonio Fernández Prieto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eduardo Cires.

Appendix

Appendix

Plant materials, voucher information and GenBank accessions for DNA sequences used in this paper. Sequences directly retrieved from GenBank are in italics. Systematics of Ranunculus parnassiifolius is based on Cires et al. (2012).

Ranunculus taxa (population code); Locality; Ploidy Level; Collector; Collection number and herbarium; ITS GenBank no.; rpl32-trnL GenBank no.; trnQ-rps16 GenBank no.; trnK-matK GenBank no.; ycf6-psbM GenBank no.

Ficaria verna Huds. (=R. ficaria L.); (1); Villaviciosa (Asturias, Spain); 2n = 2x; J.A. Fernández Prieto & J. Homet 31967 (FCO); JX025227; JX025320; JX025282; KF528859; KF528890. Ranunculus aconitifolius L.; (1); Somiedo (Asturias, Spain); 2n = 2x; E. Cires & J.A. Fernández Prieto 31859 (FCO); JX025228; JX025321; JX025283; KF528860; KF528891. R. amplexicaulis L.; (1); Portillo de las Yeguas (Cantabria, Spain); 2n = 2x; A. Bueno & E. Cires 31962 (FCO); JX025229; JX025322; JX025284; KF528861; KF528892. (2); Somiedo (Asturias, Spain); 2n = 2x; E. Cires & J.A. Fernández Prieto 31963 (FCO); JX025230; JX025323; JX025285; KF528862; KF528893. R. cabrerensis Rothm.; (1); Abelgas de Luna (León, Spain); 2n = 2x; C. Cuesta & E. Cires 31368 (FCO); JX025237; JX025328; JX025290; KF528863; KF528894. (2); Lago de la Baña (León, Spain); 2n = 2x; E. Cires, B. Jiménez-Alfaro & L. González 31369 (FCO); JX025234; JX025327; JX025289; KF528864; KF528895. (3); Portillo de las Yeguas (Cantabria, Spain); 2n = 2x; A. Bueno & E. Cires 31371 (FCO); JX025239; JX025330; JX025292; KF528865; KF528896. R. cabrerensis subsp. muniellensis (Bueno, Fern. Casado & Fern. Prieto) Fern. Prieto & Cires; (1); Muniellos Biosphere Reserve (Asturias, Spain); 2n = 2x; E. Cires 31370 (FCO); JX025271; JX025350; JX025312; KF528866; KF528897. R. gramineus L.; (1); Somiedo (Asturias, Spain); 2n = 2x; E. Cires & J.A. Fernández Prieto 31968 (FCO); JX025232; JX025325; JX025287; KF528867; KF528898. R. montenegrinus Lindtner; (1); Dinibeg (Sar Planina, Macedonia); 2n = 4x; M. Baltisberger no. 12258 (Z/ZT); KF528832; KF528841; KF528850; KF528868; KF528899. (2); Kom Kucki (Komovi, Montenegro), 2n = 5x; M. Baltisberger no. 11444 (Z/ZT); KF528833; KF528842; KF528851; KF528869; KF528900. (3); Mali Titov Vrv (Sar Planina, Macedonia); 2n = 4x; M. Baltisberger no. 12269 (Z/ZT); KF528834; KF528843; KF528852; KF528870; KF528901. R. parnassiifolius subsp. favargeri P. Küpfer; (1); Somiedo (Asturias, Spain); 2n = 4x; E. Cires & J.A. Fernández Prieto 31103 (FCO); JX025247; JX025335; JX025297; KF528871; KF528902. (2); Jou de los Boches (Asturias, Spain); 2n = 2x; A. Fernández & E. Cires 31105 (FCO); JX025266; JX025346; JX025308; KF528872; KF528903. (3); La Canalona (Cantabria, Spain); 2n = 2x; A. Fernández & E. Cires 31107 (FCO); JX025263; JX025344; JX025306; KF528873; KF528904. (4); Pandébano (Asturias, Spain); 2n = 2x; A. Fernández & E. Cires 31115 (FCO); JX025268; JX025347; JX025309; KF528874; KF528905. (5); Urriellu (Asturias, Spain); 2n = 2x; A. Fernández & E. Cires 31117 (FCO); JX025270; JX025349; JX025311; KF528875; KF528906. R. parnassiifolius subsp. heterocarpus P. Küpfer; (1); Albulapass (Graubünden, Switzerland); 2n = 4x; C. Cuesta, E. Cires, M. Ceballos & J.A. Fernández Prieto 31353 (FCO); JX025243; JX025332; JX025294; KF528876; KF528907. (2); Cortina d'Ampezzo (Belluno, Italy); 2n = 4x; C. Cuesta, E. Cires, M. Ceballos & J.A. Fernández Prieto 31354 (FCO); JX025245; JX025334; JX025296; KF528877; KF528908. (3); Grand Chavalard (Valais, Switzerland); 2n = 4x; C. Cuesta, E. Cires, M. Ceballos & J.A. Fernández Prieto 31366 (FCO); JX025241; JX025331; JX025293; KF528878; KF528909. R. parnassiifolius subsp. parnassiifolius L.; (1); Col d’Arlas (Aquitaine, France); 2n = 2x; E. Cires & J.A. Fernández Prieto 31355 (FCO); JX025265; JX025345; JX025307; KF528879; KF528910. (2); Chisagües (Huesca, Spain); 2n = 4x; E. Cires & J.A. Fernández Prieto 31360 (FCO); JX025253; JX025339; JX025301; KF528880; KF528911. R. pyrenaeus L.; (1); Chisagües (Huesca, Spain); 2n = 2x; E. Cires & J.A. Fernández Prieto 31971 (FCO); JX025276; JX025353; JX025315; KF528881; KF528912. (2); Pas de la Casa (Encamp, Andorra); 2n = 2x; E. Cires & J.A. Fernández Prieto 31372 (FCO); JX025277; JX025354; JX025316; KF528882; KF528913. (3); Fontalba (Gerona, Spain); 2n = 2x; E. Cires & J.A. Fernández Prieto 31972 (FCO); JX025278; JX025355; JX025317; KF528883; KF528914. R. seguieri Vill.; (1); M. Vettore, (NE of Rome, C Italy); 2n = 2x; M. Baltisberger no. 12857 (Z/ZT); KF528835; KF528844; KF528853; KF528884; KF528915. (2); Feltre, (E of Trento, N Italy); 2n = 2x; M. Baltisberger no. 12056 (Z/ZT); KF528836; KF528845; KF528854; KF528885; KF528916. R. wettsteinii Dörfl.; (1, identified as R. parnassiifolius from the Balkan Peninsula by M. Baltisberger); Kula Ziberit (Korab, Albania-Macedonia); 2n = 4x; M. Baltisberger no. 12421 (Z/ZT); KF528837; KF528846; KF528855; KF528886; KF528917. (2, identified as R. parnassiifolius from the Balkan Peninsula by M. Baltisberger); Kula Ziberit (Korab, Albania-Macedonia); 2n = 4x; M. Baltisberger s.n.; KF528838; KF528847; KF528856; KF528887; KF528918. (3, identified as R. wettsteinii from the Balkan Peninsula by M. Baltisberger); Kula Ziberit (Korab, Albania-Macedonia); 2n = 4x; M. Baltisberger no. 12426 (Z/ZT); KF528839; KF528848; KF528857; KF528888; KF528919. (4, identified as R. wettsteinii from the Balkan Peninsula by M. Baltisberger); Kula Ziberit (Korab, Albania-Macedonia); 2n = 4x; M. Baltisberger s.n.; KF528840; KF528849; KF528858; KF528889; KF528920.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cires, E., Baltisberger, M., Cuesta, C. et al. Allopolyploid origin of the Balkan endemic Ranunculus wettsteinii (Ranunculaceae) inferred from nuclear and plastid DNA sequences. Org Divers Evol 14, 1–10 (2014). https://doi.org/10.1007/s13127-013-0150-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-013-0150-6

Keywords

Search

Navigation