Skip to main content
Log in

Allopatric hybrids as evidence for past range dynamics in Sempervivum (Crassulaceae), a western Eurasian high mountain oreophyte

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

Abstract

Fossil evidence, phylogeographic analyses, species distribution modelling and ancient DNA analyses have all shown that plant distributions have been highly dynamic through time. We use the geographical distribution of intra- and interspecific hybrids in Sempervivum, a western Eurasian high mountain oreophyte, as evidence for the past range dynamics of their parents. Sequences of the nuclear ribosomal internal transcribed spacer (ITS), parts of the nuclear ribosomal intergenic spacer region (IGS), and the three chloroplast markers atpI–atpH, rps16-intron and trnQ–rps16 were generated for 101 individuals of Sempervivum from across its entire distribution range. Hybrid individuals were identified by the presence of double base calls in direct sequencing of polymerase chain reaction products of ITS and IGS. Parentage was inferred from comparison with sequences without double base calls and with cpDNA sequences. We identified 27 hybrid individuals, which were found outside the current distribution range of one parent in 10 cases and with both (or all three) parents in eight cases. Geographical distance of hybrids and allopatric parents ranged from 25 to 2100 km. The distribution of hybrid individuals in relation to their parents provides evidence for past range dynamics and migration over sometimes large geographical distances. As all taxa involved had been postulated to be of Quaternary origin in an earlier study, we hypothesise that hybridisation took place in glacial refugia where the parental species came into contact.

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.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abbott RJ, Brennan AC (2014) Altitudinal gradients, plant hybrid zones and evolutionary novelty. Philos Trans R Soc B 369:20130346. doi:10.1098/rstb.2013.0346

    Article  Google Scholar 

  • Alsos IG, Alm T, Normand S, Brochmann C (2009) Past and future range shifts and loss of diversity in dwarf willow (Salix herbacea L.) inferred from genetics, fossils and modelling. Global Ecol Biogeogr 18:223–239. doi:10.1111/j.1466-8238.2008.00439.x

    Article  Google Scholar 

  • Álvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol 29:417–434. doi:10.1016/S1055-7903(03)00208-2

    Article  PubMed  Google Scholar 

  • Alvarez N, Thiel-Egenter C, Tribsch A, Holderegger R, Manel S, Schönswetter P, Taberlet P et al (2009) History or ecology? Substrate type as a major driver of spatial genetic structure in alpine plants. Ecol Lett 12:632–640. doi:10.1111/j.1461-0248.2009.01312.x

    Article  PubMed  Google Scholar 

  • Ansell SW, Grundmann M, Russell SJ, Schneider H, Vogel JC (2008) Genetic discontinuity, breeding-system change and population history of Arabis alpina in the Italian Peninsula and adjacent Alps. Mol Ecol 17:2245–2257. doi:10.1111/j.1365-294X.2008.03739.x

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Baldwin BG, Markos S (1998) Phylogenetic utility of the external transcribed spacer (ETS) of 18S–26S rDNA: congruence of ETS and ITS trees of Calycadenia (Compositae). Mol Phylogenet Evol 10:449–463. doi:10.1006/mpev.1998.0545

    Article  CAS  PubMed  Google Scholar 

  • Bennett KD (1997) Evolution and ecology: the pace of life. Cambridge University Press, Cambridge

    Google Scholar 

  • Bhagwat SA, Willis KJ (2008) Species persistence in northerly glacial refugia of Europe: a matter of chance or biogeographical traits? J Biogeogr 35:464–482. doi:10.1111/j.1365-2699.2007.01861.x

    Article  Google Scholar 

  • Birks HJB, Willis KJ (2008) Alpines, trees, and refugia in Europe. Plant Ecol Divers 1:147–160. doi:10.1080/17550870802349146

    Article  Google Scholar 

  • Brinkmann R (1976) Geology of Turkey, 1st edn. Enke, Stuttgart

    Google Scholar 

  • Campbell CS, Wojciechowski MF, Baldwin BG, Alice LA, Donoghue MJ (1997) Persistent nuclear ribosomal DNA sequence polymorphism in the Amelanchier agamic complex (Rosaceae). Mol Biol Evol 14:81–90

    Article  CAS  PubMed  Google Scholar 

  • Comes HP, Kadereit JW (1998) The effect of Quaternary climatic changes on plant distribution and evolution. Trends Plant Sci 3:432–438. doi:10.1016/S1360-1385(98)01327-2

    Article  Google Scholar 

  • Cordova CE, Harrison SP, Mudie PJ, Riehl S, Leroy SA, Ortiz N (2009) Pollen, plant macrofossil and charcoal records for palaeovegetation reconstruction in the Mediterranean-Black Sea Corridor since the Last Glacial Maximum. Quat Int 197:12–26. doi:10.1016/j.quaint.2007.06.015

    Article  Google Scholar 

  • Corriveau JL, Coleman AW (1988) Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 Angiosperm species. Am J Bot 75:1443–1458. doi:10.2307/2444695

    Article  Google Scholar 

  • Dixon CJ, Schönswetter P, Schneeweiss GM (2007) Traces of ancient range shifts in a mountain plant group (Androsace halleri complex, Primulaceae). Mol Ecol 16:3890–3901. doi:10.1111/j.1365-294X.2007.03342.x

    Article  PubMed  Google Scholar 

  • Edwards CE, Soltis DE, Soltis PS (2006) Molecular phylogeny of Conradina and other scrub mints (Lamiaceae) from the Southeastern USA: evidence for hybridization in Pleistocene refugia? Syst Bot 31:193–207. doi:10.1600/036364406775971688

    Article  Google Scholar 

  • Favarger C, Maeder AM, Zesiger F (1968) Hybrides interspécifiques et intergénériques chez les Joubarbes. Archiv der Julius Klaus-Stiftung für Vererbungsforschung, Sozialanthropologie und Rassenhygiene 43:18–30

    PubMed  Google Scholar 

  • Feldhusen J (2012) Hybridisierung in der Gattung Sempervivum L. (Crassulaceae): Sempervivum leucanthum Pančić als Hybrid zwischen S. ciliosum Craib und S. marmoreum Griseb. im Rila-Gebirge in Bulgarien. Diploma-Thesis, Johannes Gutenberg-Universität Mainz

  • Feurdean A, Bhagwat SA, Willis KJ, Birks HJB, Lischke H, Hickler T, Nogues-Bravo D (2013) Tree migration-rates: narrowing the gap between inferred post-glacial rates and projected rates. PLoS One 8:e71797. doi:10.1371/journal.pone.0071797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gould BA, Leon B, Buffen AM, Thompson LG (2010) Evidence of a high-Andean, mid-Holocene plant community: an ancient DNA analysis of glacially preserved remains. Am J Bot 97:1579–1584. doi:10.3732/ajb.1000058

    Article  PubMed  Google Scholar 

  • Grassi F, Minuto L, Casazza G, Labra M, Sala F (2009) Haplotype richness in refugial areas: phylogeographical structure of Saxifraga callosa. J Plant Res 122:377–387. doi:10.1007/s10265-009-0230-z

    Article  CAS  PubMed  Google Scholar 

  • Grossheim AA (1945) Flora Kavkaza. Vol. 3, Saururaceae—Caryophyllaceae, Azerbajdzhanskogo Filiala Akademii Nauk SSSR, Baku

  • Guisan A, Zimmermann NE (2000) Predictive habitat distribution models in ecology. Ecol Model 135:147–186. doi:10.1016/S0304-3800(00)00354-9

    Article  Google Scholar 

  • Gurgenidze MZ (1969) Generis Sempervivum L. novae e Caucaso. Zametki po Sistematike i Geografii Rasteniĭ 27:30–43

    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. doi:10.1111/j.1095-8312.1996.tb01434.x

    Article  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913. doi:10.1038/35016000

    Article  CAS  PubMed  Google Scholar 

  • Hugall A, Moritz C, Moussalli A, Stanisic J (2002) Reconciling paleodistribution models and comparative phylogeography in the Wet Tropics rainforest land snail Gnarosophia bellendenkerensis (Brazier 1875). Proc Natl Acad Sci USA 99:6112–6117. doi:10.1073/pnas.092538699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hungerer KB, Kadereit JW (1998) The phylogeny and biogeography of Gentiana L. sect. Ciminalis (Adans.) Dumort.: a historical interpretation of distribution ranges in the European high mountains. Perspect Plant Ecol 1:121–135. doi:10.1078/1433-8319-00055

    Article  Google Scholar 

  • Jakob SS, Rodder D, Engler JO, Shaaf S, Ozkan H, Blattner FR, Kilian B (2014) Evolutionary history of wild barley (Hordeum vulgare subsp. spontaneum) analyzed using multilocus sequence data and paleodistribution modeling. Genome Biol Evol 6:685–702. doi:10.1093/gbe/evu047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jalas J, Suominen J, Lampinen R, Kurtto A (1999) Atlas florae Europaeae. Vol. 12, Resedaceae to Platanaceae, Helsinki University Printing House, Helsinki, pp 52–69

  • Jørgensen T, Haile J, Möller PE, Andreev A, Boessenkool S, Rasmussen M, Kienast F et al (2012) A comparative study of ancient sedimentary DNA, pollen and macrofossils from permafrost sediments of northern Siberia reveals long-term vegetational stability. Mol Ecol 21:1989–2003. doi:10.1111/j.1365-294X.2011.05287.x

    Article  PubMed  Google Scholar 

  • Kadereit JW (2015) The geography of hybrid speciation in plants. Taxon 64:673–687. doi:10.12705/644.1

    Article  Google Scholar 

  • Kadereit JW, Licht W, Uhink CH (2008) Asian relationships of the flora of the European Alps. Plant Ecol Divers 1:171–179. doi:10.1080/17550870802328751

    Article  Google Scholar 

  • Kaplan Z, Fehrer J (2007) Molecular evidence for a natural primary triple hybrid in plants revealed from direct sequencing. Ann Bot-Lond 99:1213–1222. doi:10.1093/aob/mcm072

    Article  CAS  Google Scholar 

  • Karaer F, Celep F, Kutbay HG (2010) Morphological, ecological and palynological studies on Sempervivum sosnowskyi Ter-Chatsch (Crassulaceae) with a new distribution record from Turkey. Aust J Crop Sci 4:247–251

    Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. doi:10.1093/molbev/mst010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klein JT (2015) Phylogenie, Evolution und Biogeographie der Gattungen Sempervivum und Jovibarba. Dissertation, Johannes Gutenberg-Universität Mainz

  • Klein JT, Kadereit JW (2015) Phylogeny, biogeography, and evolution of edaphic association in the European oreophytes Sempervivum and Jovibarba (Crassulaceae). Int J Plant Sci 176:44–71. doi:10.1086/677948

    Article  Google Scholar 

  • Lang G (1994) Quartäre Vegetationsgeschichte Europas. Fischer, Jena

    Google Scholar 

  • Lippert W (1995) Crassulaceae. In: Hegi G, Conert HJ, Jäger E, Kadereit JW, Schultze-Motel W, Weber HE (eds) Illustrierte Flora von Mitteleuropa, vol 4, 3rd edn. Blackwell Wissenschafts-Verlag, Berlin, pp 77–97

    Google Scholar 

  • Manton I (1950) Problems of cytology and evolution in the Pteridophyta. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • McKinnon GE, Jordan GJ, Vaillancourt RE, Steane DA, Potts BM (2004) Glacial refugia and reticulate evolution: the case of the Tasmanian eucalypts. Philos Trans R Soc B 359:275–284. doi:10.1098/rstb.2003.1391

    Article  Google Scholar 

  • Meusel H, Jäger E, Weinert E (1965) Vergleichende Chorologie der zentraleuropäischen Flora, vol 1. Gustav Fischer, Stuttgart

    Google Scholar 

  • Moore AJ, Merges D, Kadereit JW (2013) The origin of the serpentine endemic Minuartia laricifolia subsp. ophiolitica by vicariance and competitive exclusion. Mol Ecol 22:2218–2231. doi:10.1111/mec.12266

    Article  CAS  PubMed  Google Scholar 

  • Mugrabi de Kuppler A, Fagúndez J, Bellstedt D, Oliver E, Léon J, Pirie M (2015) Testing reticulate versus coalescent origins of Erica lusitanica using a species phylogeny of the northern heathers (Ericeae, Ericaceae). Mol Phylogenet Evol 88:121–131. doi:10.1016/j.ympev.2015.04.005

    Article  CAS  PubMed  Google Scholar 

  • Muirhead CW (1969) Turkish species of Sempervivum. Notes from the Royal Botanic Garden Edinburgh 29:15–27

  • Muirhead CW (1972) Sempervivum L. In: Davis PH (ed) Flora of Turkey and the East Aegean Islands. Edinburgh University Press, Edinburgh, pp 244–248

    Google Scholar 

  • Neeff P (2008) Contributions to the taxonomy of the genus Sempervivum L. (Crassulaceae) with particular regard to the groups occurring in Asia Minor. Schumannia 5:5–98

    Google Scholar 

  • Nieto Feliner G (2011) Southern European glacial refugia: a tale of tales. Taxon 60:365–372

    Google Scholar 

  • Parnell JAN (1989) A new Sempervivum species (Crassulaceae) from Iran. Willdenowia 18:419–421

    Google Scholar 

  • Pelser PB, Abbott RJ, Comes HP, Milton JJ, Möller M, Looseley ME, Cron GV et al (2012) The genetic ghost of an invasion past: colonization and extinction revealed by historical hybridization in Senecio. Mol Ecol 21:369–387. doi:10.1111/j.1365-294X.2011.05399.x

    Article  CAS  PubMed  Google Scholar 

  • Peşmen H, Güner A (1978) Four new taxa from Anatolia. Notes from the Royal Botanic Garden Edinburgh 36:35–38

  • Praeger RL (1932) An account of the Sempervivum group. Royal Horticultural Society, London

    Google Scholar 

  • Provan J, Bennett K (2008) Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23:564–571. doi:10.1016/j.tree.2008.06.010

    Article  PubMed  Google Scholar 

  • Rieseberg LH (1995) The role of hybridization in evolution: old wine in new skins. Am J Bot 82:944–953

    Article  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. doi:10.1111/j.1365-294X.2005.02683.x

    Article  PubMed  Google Scholar 

  • Schorr G, Holstein N, Pearman PB, Guisan A, Kadereit JW (2012) Integrating species distribution models (SDMs) and phylogeography for two species of Alpine Primula. Ecol Evol 2:1260–1277. doi:10.1002/ece3.100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schorr G, Pearman PB, Guisan A, Kadereit JW (2013) Combining palaeodistribution modelling and phylogeographical approaches for identifying glacial refugia in Alpine Primula. J Biogeogr 40:1947–1960. doi:10.1111/jbi.12132

    Google Scholar 

  • Şenkul Ç, Doğan U (2013) Vegetation and climate of Anatolia and adjacent regions during the Last Glacial period. Quat Int 302:110–122. doi:10.1016/j.quaint.2012.04.006

    Article  Google Scholar 

  • Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC et al (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 92:142–166. doi:10.3732/ajb.92.1.142

    Article  CAS  PubMed  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. Am J Bot 94:275–288. doi:10.3732/ajb.94.3.275

    Article  CAS  PubMed  Google Scholar 

  • Smith MC (1981) Sempervivum (Crasulaceae) in Spain and the Pyrenees. Lagascalia 10:1–23

    Google Scholar 

  • Sonibare MA, Armagan M, Özgökce F, Yaprak AE, Mayland-Quellhorst E, Albach DC (2014) Analysis of taxonomic and geographic patterns of Turkish Veronica orientalis using nuclear and plastid DNA and morphological data. Plant Syst Evol 300:645–664. doi:10.1007/s00606-013-0909-4

    Article  Google Scholar 

  • Stebbins GL (1942) Polyploid complexes in relation to ecology and the history of floras. Am Nat 76:36–45

    Article  Google Scholar 

  • Stebbins GL (1950) Variation and evolution in plants. Columbia University Press, New York

    Google Scholar 

  • Stebbins GL (1985) Polyploidy, hybridization, and the invasion of new habitats. Ann Mo Bot Gard 72:824–832

    Article  Google Scholar 

  • Stewart JR, Lister AM (2001) Cryptic northern refugia and the origins of the modern biota. Trends Ecol Evol 16:608–613. doi:10.1016/S0169-5347(01)02338-2

    Article  Google Scholar 

  • Surina B, Schönswetter P, Schneeweiss GM (2011) Quaternary range dynamics of ecologically divergent species (Edraianthus serpyllifolius and E. tenuifolius, Campanulaceae) within the Balkan refugium. J Biogeogr 38:1381–1393. doi:10.1111/j.1365-2699.2011.02493.x

    Article  Google Scholar 

  • ’t Hart H (2002) Crassulaceae. In: Strid A, Tan K (eds) Flora Hellenica. A. R. G. Gantner, Ruggell pp 304–335

    Google Scholar 

  • ’t Hart H, Sandbrink JM, Csikos I, van Ooyen A, van Brederode J (1993) The allopolyploid origin of Sedum rupestre subsp. rupestre (Crassulaceae). Plant Syst Evol 184:195–206. doi:10.1007/BF00937435

    Article  Google Scholar 

  • ’t Hart H, Bleij B, Zonneveld B (2005) Sempervivum. In: Eggli U (ed) Illustrated handbook of succulent plants: Crassulaceae, 2nd edn. Springer, Berlin, pp 332–349

    Google Scholar 

  • Sang T, Crawford DJ, Stuessy TF (1995) Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution. Proc Natl Acad Sci USA 92:6813–6817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taberlet P, Fumagalli L, Wust-Saucy A-G, Cosson J-F (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464. doi:10.1046/j.1365-294x.1998.00289.x

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takahata N, Nei M (1985) Gene genealogy and variance of interpopulational nucleotide differences. Genetics 110:325–344

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tarıkahya-Hacıoğlu B, Karacaoğlu Ç, Özüdoğru B (2014) The speciation history and systematics of Carthamus (Asteraceae) with special emphasis on Turkish species by integrating phylogenetic and Ecological Niche Modelling data. Plant Syst Evol 300:1349–1359. doi:10.1007/s00606-013-0966-8

    Article  Google Scholar 

  • Tarkhnishvili D, Gavashelishvili A, Mumladze L (2012) Palaeoclimatic models help to understand current distribution of Caucasian forest species. Biol J Linn Soc 105:231–248. doi:10.1111/j.1095-8312.2011.01788.x

    Article  Google Scholar 

  • Thiede J, Eggli U (2007) Crassulaceae. In: Kubitzki K (ed) The families and genera of vascular plants, vol 9. Springer, Berlin, pp 83–118

    Google Scholar 

  • Tribsch A, Schönswetter P (2003) Patterns of endemism and comparative phylogeography confirm palaeoenvironmental evidence for Pleistocene refugia in the Eastern Alps. Taxon 52:477–497. doi:10.2307/3647447

    Article  Google Scholar 

  • Tzedakis P, Emerson B, Hewitt G (2013) Cryptic or mystic? Glacial tree refugia in northern Europe. Trends Ecol Evol 28:696–704. doi:10.1016/j.tree.2013.09.001

    Article  CAS  PubMed  Google Scholar 

  • Valtueña FJ, Preston CD, Kadereit JW (2012) Phylogeography of a Tertiary relict plant, Meconopsis cambrica (Papaveraceae), implies the existence of northern refugia for a temperate herb. Mol Ecol 21:1423–1437. doi:10.1111/j.1365-294X.2012.05473.x

    Article  PubMed  Google Scholar 

  • Veith M, Schmidtler JF, Kosuch J, Baran I, Seitz A (2003) Palaeoclimatic changes explain Anatolian mountain frog evolution: a test for alternating vicariance and dispersal events. Mol Ecol 12:185–199. doi:10.1046/j.1365-294X.2003.01714.x

    Article  CAS  PubMed  Google Scholar 

  • Wales N, Allaby R, Willerslev E, Gilbert M (2013) Ancient plant DNA. In: Elias SA, Mock CJ (eds) Encyclopedia of Quaternary science. 2nd edn. Elsevier, Edinburgh, pp 705–715. doi: 10.1016/B978-0-444-53643-3.00202-8

  • White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Willerslev E, Cappellini E, Boomsma W, Nielsen R, Hebsgaard MB, Brand TB, Hofreiter M et al (2007) Ancient biomolecules from deep ice cores reveal a forested southern Greenland. Science 317:111–114. doi:10.1126/science.1141758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors thank S. Gencheva and V. Klein for assistance in the field, U. Möllecken and C. Uribe for assistance in the lab and the officials of the following countries for granting permission to sample according to the Convention on Biological Diversity: Spain, France, Italy, Switzerland, Austria, Slovenia, Croatia, Macedonia, Greece, and Bulgaria. We very gratefully acknowledge the receipt of living material from field collections by P. Neeff (Essen), U. Eggli (Sukkulenten-Sammlung, Zürich), M. Höhn (Corvinus University, Budapest), R. Letz (Slovak Academy of Sciences, Bratislava) and S. Shetekauri (State University, Tbilisi). Furthermore, we thank A.J. Moore (Brown University, Providence, RI) and M. Pirie (Mainz University) for discussion of parts of our results, two anonymous reviewers for very helpful comments, and A.J. Moore for help with the English. This study was supported by the Deutsche Forschungsgemeinschaft (Grant KA 635/17-1 to J.W. Kadereit).

Author contributions

J.T.K. and J.W.K. conceived the ideas; J.T.K. collected and analysed the data; J.T.K. and J.W.K. wrote the paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Johannes T. Klein.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 94 kb)

Supplementary material 2 (PDF 1599 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Klein, J.T., Kadereit, J.W. Allopatric hybrids as evidence for past range dynamics in Sempervivum (Crassulaceae), a western Eurasian high mountain oreophyte. Alp Botany 126, 119–133 (2016). https://doi.org/10.1007/s00035-016-0164-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00035-016-0164-8

Keywords

Navigation