Skip to main content

The Iberian endemic species Ranunculus cabrerensis Rothm.: an intricate history in the Ranunculus parnassiifolius L. polyploid complex

Plant Systematics and Evolution volume 298, pages 121–138 (2012)Cite this article

Abstract

The orophilous plant, Ranunculus parnassiifolius L., is a polyploid complex that is widespread throughout the southern European mountains, where at least five taxa have traditionally been recognized. The aim of this study was to test whether R. parnassiifolius subsp. cabrerensis should be treated as an independent species of the R. parnassiifolius polyploid complex and constitutes, therefore, an evolutionary line in itself. To disentangle its evolutionary history and taxonomy, we used genome size estimation based on flow cytometric measurements (FCM), multivariate morphometric analyses, polymerase chain reaction-restriction fragment length polymorphisms (PCR–RFLPs) and subsequent sequencing of cpDNA regions (trnS, trnR-atpA, atpH-atpI). This study provides molecular and morphological evidence for the recognition of R. cabrerensis at the species level, rather than as an intraspecific taxon of R. parnassiifolius. Furthermore, it is concluded that those plants previously known as R. parnassiifolius subsp. muniellensis should be systematized at the subspecies level as R. cabrerensis subsp. muniellensis. This contribution highlights the benefit of combining diverse approaches to obtain knowledge about relict populations and for the implementation of suitable conservation measures.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Agarwal M, Shrivastava N, Padh H (2008) Advances in molecular marker techniques and their applications in plant sciences. Plant Cell Rep 27:617–631

    PubMed  Article  CAS  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Avise JC (2009) Phylogeography: retrospect and prospect. J Biogeogr 36:3–15

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Besnard G, Rubio de Casas R, Vargas P (2007) Plastid and nuclear DNA polymorphism reveals historical processes of isolation and reticulation in the olive tree complex (Olea europaea). J Biogeogr 34:736–752

    Article  Google Scholar 

  • Bouxin G (2005) Ginkgo, a multivariate analysis package. J Veg Sci 16:355–359

    Article  Google Scholar 

  • Bryan GJ, McNicoll J, Ramsay G, Meyer RC, De Jong WS (1999) Polymorphic simple sequence repeat markers in chloroplast genomes of Solanaceous plants. Theor Appl Genet 99:859–867

    Article  CAS  Google Scholar 

  • Bueno Sánchez A, Fernández Casado MA, Fernández Prieto JA (1992) A new subspecies of Ranunculus parnassiifolius L. (Ranunculaceae) from the Cantabrian Mountains, Spain. Bot J Linn Soc 109:359–367

    Article  Google Scholar 

  • Bussell JD, Waycott M, Chappill JA (2005) Arbitrarily amplified DNA markers as characters for phylogenetic inference. Perspect Plant Ecol Evol Syst 7(1):3–26

    Article  Google Scholar 

  • Carrillo i Ortuño E, Ninot i Sugranyes JM (1992) Flora i vegetació de les valls d’Espot i Boí. Institut d’Estudis Catalans, Arxius Secció Ciències, Barcelona

    Google Scholar 

  • Carroll SP, Fox CW (eds) (2008) Conservation biology: evolution in action. Oxford University Press, New York

    Google Scholar 

  • Chung SM, Staub JE (2003) The development and evaluation of consensus chloroplast primer pairs that possess highly variable sequence regions in a diverse array of plant taxa. Theor Appl Genet 107:757–767

    PubMed  Article  CAS  Google Scholar 

  • Cires E, Cuesta C, Peredo EL, Revilla MA, Fernández Prieto JA (2009) Genome size variation and morphological differentiation within Ranunculus parnassifolius group (Ranunculaceae) from calcareous screes in the Northwest of Spain. Pl Syst Evol 281:193–208

    Article  Google Scholar 

  • Cires E, Cuesta C, Revilla MA, Fernández Prieto JA (2010) Intraspecific genome size variation and morphological differentiation of Ranunculus parnassifolius (Ranunculaceae), an Alpine-Pyrenean-Cantabrian polyploid group. Biol J Linn Soc 101:251–271

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molec Ecol 9:1657–1659

    Article  CAS  Google Scholar 

  • Comes HP, Kadereit JW (2003) Spatial and temporal patterns in the evolution of the flora of the European Alpine System. Taxon 52:451–462

    Article  Google Scholar 

  • Cook CDK, Grau J, López González G (1986) Ranunculus L. Sect. Ranuncella (Spach) Freyn. In: Castroviejo S, Laínz M, López González G, Montserrat P, Muñoz Garmendia F, Paiva J, Villar L (eds) Flora Iberica. Vol I. Lycopodiaceae-Papaveraceae. Real Jardín Botánico, C.S.I.C, Madrid, pp 279–371

    Google Scholar 

  • Demesure B, Sodzi N, 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 

  • Diosdado JC, Pastor JE (1991) Observaciones cariológicas en el género Ranunculus L. sect. Ranuncella (Spach) Freyn en la Península Ibérica. Nuovo Giorn Bot Ital 125(6):879–894

    Google Scholar 

  • Dixon CJ, Schönswetter P, Schneeweiss GM (2007) Traces of ancient range shifts in a mountain plant group (Androsace halleri complex, Primulaceae). Molec Ecol 16:3890–3901

    Article  Google Scholar 

  • Dixon CJ, Schönswetter P, Schneeweiss GM (2008) Morphological and geographical evidence are misleading with respect to the phylogenetic position and origin of the narrow endemic polyploid Androsace cantabrica (Primulaceae). Syst Bot 33:384–389

    Article  Google Scholar 

  • Doležel J, Greilhuber J, Suda J (eds) (2007) Flow cytometry with plant cells. Analysis of genes, chromosomes and genomes. Wiley-VCH Verlag GmbH and Co. KGaA, Weinheim

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

    Google Scholar 

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

    CAS  Google Scholar 

  • GBIF (2010) Global biodiversity information facility. URL http://www.gbif.org/. Accessed 27 Oct 2009

  • Gemeinholzer B (2008) Phylogenetic networks. In: Schreiber F, Junker B (eds) Analysis of biological networks. John Wiley and Sons, Inc, Hoboken, New Jersey, pp 255–281

    Chapter  Google Scholar 

  • Gower JC (1971) A general coefficient of similarity and some of its properties. Biometrics 27(4):857–871

    Article  Google Scholar 

  • Greilhuber J, Doležel J, Lysák MA, Bennett MD (2005) The origin, evolution and proposed stabilization of the terms ‘genome size’ and ‘C-value’ to describe nuclear DNA contents. Ann Bot 95:255–260

    PubMed  Article  CAS  Google Scholar 

  • Grivet D, Heinze B, Vendramin GG, Petit RJ (2001) Genome walking with consensus primers: application to the large single copy region of chloroplast DNA. Molec Ecol Notes 1:345–349

    Article  CAS  Google Scholar 

  • Habel JC, Assmann T, Schmitt T, Avise JC (2010a) Relict species: from past to future. In: Habel JC, Assmann T (eds) Relict species phylogeography and conservation biology. Springer, Heidelberg, pp 1–5

    Google Scholar 

  • Habel JC, Schmitt T, Assmann T (2010b) Relict species research: some concluding remarks. In: Habel JC, Assmann T (eds) Relict species phylogeography and conservation biology. Springer, Heidelberg, pp 441–442

    Google Scholar 

  • Hickerson MJ, Carstens BC, Cavender-Bares J, Crandall KA, Graham CH, Johnson JB, Rissler L, Victoriano PF, Yoder AD (2009) Phylogeography’s past, present, and future: 10 years after Avise 2000. Mol Phylogenet Evol 54:291–301

    PubMed  Article  Google Scholar 

  • Hörandl E (2009) Geographical parthenogenesis: opportunities for asexuality. In: Schoen I, Martens K, Van Dijk P (eds) Lost sex. Springer, Heidelberg, pp 161–186

    Chapter  Google Scholar 

  • Hörandl E (2011) Evolution and biogeography of alpine apomictic plants. Taxon 60:390–402

    Google Scholar 

  • Hörandl E, Paun O, Johansson JT, Lehnebach C, Armstrong T, Chen L, Lockhart P (2005) Phylogenetic relationships and evolutionary traits in Ranunculus s.l. (Ranunculaceae) inferred from ITS sequence analysis. Mol Phylogenet Evol 36:305–327

    PubMed  Article  Google Scholar 

  • Hörandl E, Cosendai A-C, Temsch E (2008) Understanding the geographic distributions of apomictic plants: a case for a pluralistic approach. Plant Ecol Divers 1:309–320

    PubMed  Article  Google Scholar 

  • Hufbauer RA, Sforza R (2008) Multiple introductions of two invasive Centaurea taxa inferred from cpDNA haplotypes. Diversity Distrib 14:252–261

    Article  Google Scholar 

  • Iriondo JM, Maxted N, Dulloo ME (eds) (2008) Conserving plant genetic diversity in protected areas: population management of crop wild relatives. CABI Publishing, Wallingford

    Google Scholar 

  • Jalas J, Suominen J (eds) (1989) Atlas Florae Europaeae. Distribution of vascular plants in Europe. 8. Nymphaeaceae to Ranunculaceae. The Committee for Mapping the Flora of Europe and Societas Biologica Fennica Vanamo, Helsinki

  • Kelchner SA (2000) The evolution of non-coding chloroplast DNA and its application in plant systematics. Ann Missouri Bot Gard 87:482–498

    Article  Google Scholar 

  • Kelchner SA (2009) Phylogenetic models and model selection for noncoding DNA. Pl Syst Evol 282:109–126

    Article  CAS  Google Scholar 

  • Kolář F, Štech M, Trávníček P, Rauchová J, Urfus T, Vít P, Kubešová M, Suda J (2009) Towards resolving the Knautia arvensis agg. (Dipsacaceae) puzzle: primary and secondary contact zones and ploidy segregation at landscape and microgeographic scales. Ann Bot 103:963–974

    PubMed  Article  Google Scholar 

  • Kropf M, Kadereit JW, Comes HP (2003) Differential cycles of range contraction and expansion in European high mountain plants during the Late Quaternary: insights from Pritzelago alpina (L.) O. Kuntze (Brassicaceae). Molec Ecol 12:931–949

    Article  CAS  Google Scholar 

  • Kropf M, Comes HP, Kadereit JW (2006) Long-distance dispersal vs. vicariance: the origin and genetic diversity of alpine plants in the Spanish Sierra Nevada. New Phytol 172:169–184

    PubMed  Article  Google Scholar 

  • Kropf M, Comes HP, Kadereit JW (2008) Causes of the genetic architecture of southwest European high mountain disjuncts. Plant Ecol Div 1(2):217–228

    Article  Google Scholar 

  • Küpfer P (1974) Reserches sur les liens de parenté entre la flore orophile des Alpes et celle des Pyrénées. Boissiera 23:1–322

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452

    PubMed  Article  CAS  Google Scholar 

  • Mort ME, Archibald JK, Randle CP, Levsen ND, O’Leary TR, Topalov K, Wiegand CM, Crawford DJ (2007) Inferring phylogeny at low taxonomic levels: utility of rapidly evolving cpDNA and nuclear ITS loci. Amer J Bot 94:173–183

    Article  Google Scholar 

  • Naciri Y, Gaudeul M (2007) Phylogeography of the endangered Eryngium alpinum L. (Apiaceae) in the European Alps. Molec Ecol 16:2721–2733

    Article  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nève G, Verlaque R (2010) Genetic differentiation between and among refugia. In: Habel JC, Assmann T (eds) Relict species phylogeography and conservation biology. Springer, Heidelberg, pp 277–294

    Google Scholar 

  • Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Molec Ecol 13:1143–1155

    Article  CAS  Google Scholar 

  • Paun O, Lehnebach C, Johansson JT, 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 

  • Peredo EL, Revilla MA, Jiménez-Alfaro B, Bueno A, Fernández Prieto JA, Abbott RJ (2009) Historical biogeography of a disjunctly distributed Spanish alpine plant, Senecio boissieri (Asteraceae). Taxon 58:883–892

    Google Scholar 

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

    PubMed  Article  Google Scholar 

  • Provan J, Soranzo N, Wilson NJ, Goldstein DB, Powell W (1999) A low mutation rate for chloroplast microsatellites. Genetics 153:943–947

    PubMed  CAS  Google Scholar 

  • Rothmaler W (1934) Species novae vel nomina nova florae hispanicae. Bol Soc Esp Hist Nat 34(2–3):147–155

    Google Scholar 

  • Schmitt T, Muster C, Schönswetter P (2010) Are disjunct alpine and arctic-alpine animal and plant species in the western Palearctic really “relics of a cold past”? In: Habel JC, Assmann T (eds) Relict species phylogeography and conservation biology. Springer, Heidelberg, pp 239–252

    Google Scholar 

  • Schönswetter P, Stehlik I, Holderegger R, Tribsch A (2005) Molecular evidence for glacial refugia of mountain plants in the European Alps. Molec Ecol 14:3547–3555

    Article  Google Scholar 

  • Schönswetter P, Solstad H, García PE, Elven R (2009) A combined molecular and morphological approach to the taxonomically intricate European mountain plant Papaver alpinum s.l. (Papaveraceae)––taxa or informal phylogeographical groups? Taxon 58:1326–1343

    Google Scholar 

  • Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC, Winder CT, Schilling EE, Small RL (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Amer J Bot 92:142–166

    Article  CAS  Google Scholar 

  • Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Amer J Bot 94:275–288

    Article  CAS  Google Scholar 

  • Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381

    PubMed  Article  CAS  Google Scholar 

  • Small RL, Ryburn JA, Cronn RC, Seelanan T, Wendel JF (1998) The tortoise and the hare: choosing between noncoding plastome and nuclear ADH sequences for phylogeny reconstruction in a recently diverged plant group. Amer J Bot 85(9):1301–1315

    Article  CAS  Google Scholar 

  • Suda J, Krahulcová A, Trávníček P, Rosenbaumová R, Peckert T, Krahulec F (2007) Genome size variation and species relationships in Hieracium subgen. Pilosella (Asteraceae) as inferred by flow cytometry. Ann Bot 100:1323–1335

    PubMed  Article  Google Scholar 

  • Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460

    PubMed  CAS  Google Scholar 

  • 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 132:619–633

    PubMed  CAS  Google Scholar 

  • Terrab A, Schönswetter P, Talavera S, Vela E, Stuessy TF (2008) Range-wide phylogeography of Juniperus thurifera L., a presumptive keystone species of western Mediterranean vegetation during cold stages of the Pleistocene. Mol Phylogenet Evol 48:94–102

    PubMed  Article  CAS  Google Scholar 

  • Tribsch A, Schönswetter P (2003) Patterns of endemism and comparative phylogeography confirm palaeo-environmental evidence for Pleistocene refugia in the Eastern Alps. Taxon 52:477–497

    Article  Google Scholar 

  • Vargas P (2003) Molecular evidence for multiple diversification patterns of alpine plants in Mediterranean Europe. Taxon 52:463–476

    Article  Google Scholar 

  • Vigo i Bonada J (1983) El poblament vegetal de la Vall de Ribes. I. Generalitats catàleg floristic. Acta Bot Barcinon 35:1–793

    Google Scholar 

  • Weising K, Gardner RC (1999) A set of conserved PCR primers for the analysis of simple sequence repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms. Genome 42:9–19

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Candela Cuesta, Dr. Pablo Vargas, Dr. Matthias Krop and Dr. Ginés A. López for comments and suggestions. We acknowledge the technical assistance of José Luis Martínez Fernández and Rebeca Alvarez García (Sequencing Services, University of Oviedo). We are grateful to Ana Fernández, J. Ignacio A. Felpete, Álvaro Bueno, Manuel A. Rosado, Sara G. Robinson, B. Jiménez-Alfaro, Leticia Fernández García and Linda González de Paz for helping in the sampling. We wish to recognize the significant contribution made by the photographer José María Fernández Formentí (Fig. 1a). We would like to thank Dr. J. Doležel (Laboratory of Molecular Cytogenetics and Cytometry, Institute of Experimental Botany, Olomouc, Czech Republic) for providing the internal reference standard for FCM analyses. This research was funded by the Spanish Ministerio de Educación y Ciencia (CGL2006-11743). E. Cires is supported by a predoctoral grant by the University of Oviedo (UNOV-06-BECDOC-2).

Author information

Authors and Affiliations

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

    Eduardo Cires & José Antonio Fernández Prieto

Authors
  1. Eduardo Cires
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José Antonio Fernández Prieto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eduardo Cires.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 882 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Cires, E., Prieto, J.A.F. The Iberian endemic species Ranunculus cabrerensis Rothm.: an intricate history in the Ranunculus parnassiifolius L. polyploid complex. Plant Syst Evol 298, 121–138 (2012). https://doi.org/10.1007/s00606-011-0529-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-011-0529-9

Keywords

  • cpDNA network
  • Genome size
  • Iberian Peninsula
  • Polyploidy
  • Ranunculaceae
  • Taxonomy