Skip to main content

Advertisement

Log in

Phylogeography of the moonwort fern Botrychium lunaria (Ophioglossaceae) based on chloroplast DNA in the Central-European Mountain System

  • Original Article
  • Published:
Alpine Botany Aims and scope Submit manuscript

Abstract

Botrychium s.s. is a cosmopolitan fern genus comprising about 35 currently recognized species. Despite unexpected high genetic diversity recently highlighted within Botrychium lunaria in the circumboreal region, few studies have included representative samples from Central Europe. Therefore, the aim of this work was to study the phylogeography of B. lunaria in the Central-European Mountain System and to compare it with that of flowering plants. Two noncoding chloroplast regions (psbA-trnH and trnL-F) were sequenced (918 bp) from 87 individuals from 34 populations in the major European mountain chains (Sierra Nevada, Pyrenees, Massif Central, Jura, Vosges, Black Forest, Alps, Apennines, and Carpathians). Among the 24 haplotypes found in the B. lunaria aggregate in Europe, bayesian phylogeny and median-joining network support four main clades (LUN1, LUN2, LUN3, and TUN). NST and GST comparison as well as homogeneous groups indicated by SAMOVA indicate a clear phylogeographical pattern. However, unlinked to geographical distance, genetic diversity is greatest in the Prealps and highlights three main barriers to gene flow: S–N of Central Alps (Aosta-Lepontic Alps), and two separating E–W Alps (Lago di Como-Rhaetian Alps and Dolomites-Noric-Julian Alps). Our results indicate that alpine populations of the B. lunaria aggregate survived the Quaternary glaciations in situ in two main refugia, in the southern and eastern periphery of the Alps. Not only areas with higher values of genetic diversity, but also refugia and sites of geographical boundaries to gene flow, appear similar in both ferns and flowering plants.

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

Access this article

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
Fig. 4

Similar content being viewed by others

References

  • Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Proceedings of the second international symposium on information theory, pp 267–281. Akademiai Kiado, Budapest, Hungary

  • Barrington DS (1993) Ecological and historical factors in fern biogeography. J Biogeogr 20:275

    Article  Google Scholar 

  • Bauert MR, Kälin M, Edwards PJ, Baltisberger M (2007) Genetic structure and phylogeography of alpine relict populations of Ranunculus pygmaeus and Saxifraga cernua. Bot Helv 117:181–196

    Article  Google Scholar 

  • Bettin O, Cornejo C, Edwards PJ, Holderegger R (2007) Phylogeography of the high alpine plant Senecio halleri (Asteraceae) in the European Alps: in situ glacial survival with postglacial stepwise dispersal into peripheral areas. Mol Ecol 16:2517–2524

    Article  CAS  PubMed  Google Scholar 

  • Birks HJB (1976) The distribution of European pteridophytes: a numerical analysis. New Phytol 77:257–287

    Article  Google Scholar 

  • Brockmann-Jerosch H, Brockmann-Jerosch M (1926) Die Geschichte der Schweizerischen Alpen-flora. In: Schröter C (ed) Das Pflanzenleben der Alpen. Raustein, Zürich, pp 1110–1215

    Google Scholar 

  • Bystriakova N, Ansell SW, Russell SJ, Grundmann M, Vogel JC, Schneider H (2014) Present, past and future of the European rock fern Asplenium fontanum: combining distribution modelling and population genetics to study the effect of climate change on geographic range and genetic diversity. Ann Bot 113:453–465

    Article  PubMed  Google Scholar 

  • Chodat R, Pampanini R (1902) Sur la distribution des plantes des Alpes austro-orientales et plus particulièrement d’un choix déplantés des Alpes cadoriques et vénitiennes. Globe Rev Genevoise Géographie 41:63–132

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Dauphin B, Farrar DR, Maccagni A, Grant JR (in press) A worldwide molecular phylogeny provides new insight on cryptic diversity within the moonworts (Botrychium s.s., Ophioglossaceae). Syst Bot

  • Dauphin B, Vieu J, Grant JR (2014) Molecular phylogenetics supports widespread cryptic species in moonworts (Botrychium s.s., Ophioglossaceae). Am J Bot 101:128–140

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581

    Article  CAS  PubMed  Google Scholar 

  • Ehlers J, Gibbard PL (2008) Quaternary glaciations: extent and chronology. Development in quaternary science, vol 2. CD. Elsevier, Amsterdam

    Google Scholar 

  • Farrar DR (1998) Population genetics of moonwort Botrychium. In: Berlin N, Miller P, Borovansky J, Seal US, Byers O (eds) Population and habitat viability assessment for the goblin fern (Botrychium mormo), pp 109–113. Final Report. The Conservation Breeding Specialist Group, Apple Valley, Minnesota, USA

  • Farrar DR (2011) Systematics and taxonomy of genus Botrychium. http://www.public.iastate.edu/~herbarium/botrychium/Moonwort-Systematics.pdf

  • Finsinger W, Tinner W (2007) Pollen and plant macrofossils at Lac de Fully (2135 m asl): Holocene forest dynamics on a highland plateau in the Valais, Switzerland. Holocene 17:1119–1127

    Article  Google Scholar 

  • Hauk WD, Haufler CH (1999) Isozyme variability among cryptic species of Botrychium subgenus Botrychium (Ophioglossaceae). Am J Bot 86:614–633

    Article  CAS  PubMed  Google Scholar 

  • Hauk WD, Kennedy L, Hawke HM (2012) A phylogenetic investigation of Botrychium s.s. (Ophioglossaceae): evidence from three plastid DNA sequence datasets. Syst Bot 37:320–330

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holderegger R, Thiel-Egenter C, Parisod C (2011) Marie Brockmann-Jerosch and her influence on alpine phylogeography. Alp Bot 121:5–10

    Article  Google Scholar 

  • Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132:583–589

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hunt HV, Ansell SW, Russell SJ et al (2009) Genetic diversity and phylogeography in two diploid ferns, Asplenium fontanum subsp. fontanum and A. petrarchae subsp. bivalens, in the western Mediterranean. Mol Ecol 18:4940–4954

    Article  CAS  PubMed  Google Scholar 

  • Ivy-Ochs S (2015) Glacier variations in the European Alps at the end of the last glaciation. Cuad Investig Geogr 41:295–315

    Article  Google Scholar 

  • Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76:173–190

    Article  PubMed  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • Marazzi S (2005) Atlante orografico delle Alpi: SOIUSA: suddivisione orografica internazionale unificata del sistema alpino. Priuli & Verlucca, Pavone Canavese (Torino)

    Google Scholar 

  • Merxmüller H (1952) Untersuchungen zur Sippengliederung und Arealbildung in den Alpen. Verein zum Schutze der Alpenpflanzen und -Tiere 17:96–133

    Google Scholar 

  • Monmonier MS (1973) Maximum-difference barriers: an alternative numerical regionalization method. Geogr Anal 5:245–261

    Article  Google Scholar 

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

    Google Scholar 

  • Ozenda P (2002) Perspectives pour une geobiologie des montagnes. Presse polytechniques et universitaires romandes, Lausanne, p. 196

    Google Scholar 

  • Parisod C (2008) Postglacial recolonisation of plants in the Western Alps of Switzerland. Bot Helv 118:1–12

    Article  Google Scholar 

  • Parisod C, Besnard G (2007) Glacial in situ survival in the Western Alps and polytopic autopolyploidy in Biscutella laevigata L. (Brassicaceae). Mol Ecol 16:2755–2767

    Article  PubMed  Google Scholar 

  • Petit RJ, Csaikl UM, Bordács S et al (2002) Chloroplast DNA variation in European white oaks: phylogeography and patterns of diversity based on data from over 2600 populations. For Ecol Manag 156:5–26

    Article  Google Scholar 

  • Petit RJ, Aguinagalde I, de Beaulieu J-L et al (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ronikier M, Schneeweiss GM, Schönswetter P (2012) The extreme disjunction between Beringia and Europe in Ranunculus glacialis sl (Ranunculaceae) does not coincide with the deepest genetic split—a story of the importance of temperate mountain ranges in arctic–alpine phylogeography. Mol Ecol 21:5561–5578

    Article  CAS  PubMed  Google Scholar 

  • Sang T, Crawford D, Stuessy T (1997) Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). Am J Bot 84:1120

    Article  CAS  PubMed  Google Scholar 

  • Schönswetter P, Tribsch A, Barfuss M, Niklfeld H (2002) Several Pleistocene refugia detected in the high alpine plant Phyteuma globulariifolium Sternb. & Hoppe (Campanulaceae) in the European Alps. Mol Ecol 11:2637–2647

    Article  PubMed  Google Scholar 

  • Schönswetter P, Paun O, Tribsch A, Niklfeld H (2003) Out of the Alps: colonization of northern Europe by East Alpine populations of the glacier buttercup Ranunculus glacialis L. (Ranunculaceae). Mol Ecol 12:3373–3381

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Smouse P (1998) To tree or not to tree. Mol Ecol 7:399–412

    Article  Google Scholar 

  • Stehlik I (2000) Nunataks and peripheral refugia for alpine plants during quaternary glaciation in the middle part of the Alps. Bot Helv 110:25–30

    Google Scholar 

  • Stehlik I (2002) Glacial history of the alpine herb Rumex nivalis (Polygonaceae): a comparison of common phylogeographic methods with nested clade analysis. Am J Bot 89:2007–2016

    Article  PubMed  Google Scholar 

  • Stehlik I, Schneller JJ, Bachmann K (2001) Resistance or emigration: response of the high-alpine plant Eritrichium nanum (L.) Gaudin to the ice age within the Central Alps. Mol Ecol 10:357–370

    Article  CAS  PubMed  Google Scholar 

  • Stensvold M (2008) A taxonomic and phylogeographic study of the Botrychium lunaria complex. Ph.D. Dissertation, Iowa State University, USA

  • Stensvold MC, Farrar DR (2017) Genetic diversity in the worldwide Botrychium lunaria (Ophioglossaceae) complex, with new species and new combinations. Brittonia. doi:10.1007/s12228-016-9455-z (Printed online 13 December 2016)

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Taberlet P, Zimmermann NE, Englisch T et al (2012) Genetic diversity in widespread species is not congruent with species richness in alpine plant communities. Ecol Lett 15:1439–1448

    Article  PubMed  Google Scholar 

  • Tate JA, Simpson BB (2003) Paraphyly of Tarasa (Malvaceae) and diverse origins of the polyploid species. Syst Bot 28:723–737

    Google Scholar 

  • The Pteridophyte Phylogeny Group. (PPG1) (2016) A community-derived classification for extant lycophytes and ferns. J Syst Evol 54(6):563–603

    Article  Google Scholar 

  • Thiel-Egenter C, Alvarez N, Holderegger R et al (2011) Break zones in the distributions of alleles and species in alpine plants. J Biogeogr 38:772–782

    Article  Google Scholar 

  • Trewick SA, Morgan-Richards M, Russell SJ et al (2002) Polyploidy, phylogeography and Pleistocene refugia of the rockfern Asplenium ceterach: evidence from chloroplast DNA. Mol Ecol 11:2003–2012

    Article  CAS  PubMed  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 

  • Tribsch A, Schönswetter P, Stuessy TF (2002) Saponaria pumila (Caryophyllaceae) and the ice age in the European Alps. Am J Bot 89:2024–2033

    Article  PubMed  Google Scholar 

  • Vogel JC, Rumsey FJ, Schneller JJ et al (1999) Where are the glacial refugia in Europe? Evidence from pteridophytes. Biol J Linn Soc 66:23–37

    Article  Google Scholar 

  • Williams EW, Waller DM (2012) Phylogenetic placement of species within the genus Botrychium ss (Ophioglossaceae) on the basis of plastid sequences, amplified fragment length polymorphisms, and flow cytometry. Int J Plant Sci 173:516–531

    Article  CAS  Google Scholar 

  • Winkler M, Tribsch A, Schneeweiss GM et al (2012) Tales of the unexpected: phylogeography of the arctic-alpine model plant Saxifraga oppositifolia (Saxifragaceae) revisited. Mol Ecol 21:4618–4630

    Article  PubMed  Google Scholar 

  • Winther JL, Friedman WE (2007) Arbuscular mycorrhizal symbionts in Botrychium (Ophioglossaceae). Am J Bot 94:1248–1255

    Article  CAS  PubMed  Google Scholar 

  • Wohlgemut T (2002) Alpine plant species richness in the Swiss Alps: diversity hot spots reconsidered. Mém. Soc. Bot. Genève 3:63–74

    Google Scholar 

Download references

Acknowledgements

This work was supported by the Fonds des donations of the Université de Neuchâtel. We would like to thank collectors of material: Amadej Trnkoczy (Triglavski, Slovenia), Benjamin Dauphin (Sierra Nevada, Spain), Claudia Danau (Retezat, Romania), Daniel Sandoz and Frédéric A. Sandoz (Dôle, Switzerland), Jozsef Sulyok (Nagy-mezo, Hungary), and Michela N. Meier. We also want to thank Olivier Bachmann and Julien Vieu for their support in the lab and two anonymous reviewers for their insightful comments on the manuscript.

Declaration of authorship

AM and JRG conceived and designed the research. AM conducted the field- and lab-work. AM and CP analyzed the data. All authors contributed to writing and approved the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alessio Maccagni.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 80 kb)

Supplementary material 2 (PDF 55 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maccagni, A., Parisod, C. & Grant, J.R. Phylogeography of the moonwort fern Botrychium lunaria (Ophioglossaceae) based on chloroplast DNA in the Central-European Mountain System. Alp Botany 127, 185–196 (2017). https://doi.org/10.1007/s00035-017-0188-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00035-017-0188-8

Keywords

Navigation