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The late rise of sky-island vegetation in the European Alps

Nature Plants volume 11, pages 1142–1153 (2025)Cite this article

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Abstract

Our understanding of the emergence of mountain floras rests on our ability to infer how orogeny, landscape dynamics and climate change altered their evolutionary trajectories. Here we reconstruct the assembly of the diverse sky-island flora of the European Alps and test the impact of key geo-climatic events. We use a dated 5,231-species phylogeny, including 96% of the sky-island flora. The assembly of this flora occurred through the colonization of over a thousand distinct lineages, of which 46% speciated from their lowland or non-Alpine ancestor and 6% underwent in situ cladogenesis. The young ages of extant sky-island lineages show that their accumulation was decoupled from ancient geo-climatic events but accelerated throughout the Plio-Pleistocene. The sky-island vegetation therefore assembled through recent lineage turnover, which was triggered, rather than impeded, by Pleistocene glacial intensification. This perspective challenges previous assumptions and highlights the complex interplay of geo-climatic factors in shaping the intricate tapestry of alpine floras.

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Fig. 1: Flora of the European Alpine sky islands (EASI).
Fig. 2: Time-calibrated ML phylogeny (branch lengths in Myr) containing 5,231 angiosperm species from 394 families.
Fig. 3: The biogeographic origins of all EASI lineages based on a literature search.
Fig. 4: Rates of assembly of the EASI flora in relation to major climatic and geological events.
Fig. 5: Model evaluation for breakpoint regression analyses.

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Data availability

All data needed to replicate the findings of this study are available on figshare at https://doi.org/10.6084/m9.figshare.25459135 (ref. 80). All raw reads data generated by the PhyloAlps and PhyloNorway projects were submitted to the EMBL-EBI Short Read Archive under the following bioprojects: PhyloAlps (PRJEB30497, PRJEB48874, PRJEB50489, PRJEB82787), PhyloNorway (PRJEB43865, PRJEB48693, https://www.ebi.ac.uk/ena/data/view/PRJEB50550). An online database of genome skimming of Arctic–Alpine plants, representing all information regarding samples, extraction, sequencing and reconstructed genomic data for the PhyloAlps and PhyloNorway projects can be found at https://phyloalps.osug.fr/main/home (ref. 81). Source data are provided with this paper.

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Acknowledgements

This paper is dedicated to the memory of Prof. Serge Aubert (1966–2015) who devoted his career to the study of alpine plants and was an invaluable source of motivation for the PhyloAlps project. This work was supported by the French National Research Agency in the framework of the ‘Investissements d’avenir’ program (ANR-15-IDEX-02). The research was funded by the joint ANR-SNF project Origin-Alps (ANR-16-CE93-0004, SNF-310030L_170059, S.L. and N.E.Z.) and the OSUG@2020 labex (ANR10 LABX56, S.L.). The sequencing was performed within the framework of the PhyloAlps project, funded by France Génomique (ANR-10-INBS-09-08, P.W.), and the PhyloNorway project funded by the Research Council of Norway (226134/F50, I.G.A.) and the Norwegian Biodiversity Information Centre (14-14, 70184209, I.G.A.). Bioinformatics and statistical analyses were carried out with the GRICAD infrastructure (https://gricad.univ-grenoble-alpes.fr). The sampling campaign and preliminary genomic analyses were partly funded by the European Research Council under the European Community’s Seventh Framework Programme FP7/2007-2013 grant agreement 281422 (TEEMBIO, W.T.) and by SNF grant 31003A_149508 (N.E.Z.). M.R. was supported by the Polish National Science Centre project no. NCN 2020/37/B/NZ8/03307. Some samples were also provided by G. Coldea, J. Sibik, R. Geremia, D. Pozarova, T. Figura, B. Offerhaus, M. Pires, Y. Morvant, G. Pellet, A. Jacotot, C. Chambrey, A. Gérard, A. Masswadeh, C. Bornand, F. Hoffer-Mallard, J. Détraz-Méroz, M. Leibundgut, M. Jutzi, P. Juillerat, S. Birrer, L. Filipaş, A. Coste, D. Suteu, A. Plecenikova, A. Guttova, J. Kucera, E. Stubnova, J. Kochjarova, I. Hodalova, S. Spaniel, R. Letz, S. Wróbel, J. Pilatova, M. Kolarova, M. Smyckova, H. Marx, R. Quesada, A. R. Frattaroli, L. Bartha, G. Sramko, V. A. Molnar, N. Passalacqua, J. L. Desrayaud, R. Giordano, B. Pont, M. Frei, F. Ojeda, J. Engel, O. Tostain, P. Anastasiu, G. Casazza, A. Hilpold, P. Koutecký, G. Schneeweiss and P. Schönswetter. Sample materials were kindly contributed from museum collections of the Jaca Herbarium, National Herbarium of Venezuela, University of Alaska Fairbanks Museum, University of Idaho Museum, Oslo Museum of Natural History, Royal Botanic Garden of Edinburgh, and the Berlin Museum of Natural History. We thank R. Ree, J. (A.) de Leeuw and H. Morlon for discussions during earlier stages of the project.

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Author notes

  1. Deceased: Serge Aubert.

Authors and Affiliations

  1. Univ. Grenoble Alpes, Univ. Savoie Mont Blanc, CNRS, LECA, Grenoble, France

    Lara M. Wootton, Florian C. Boucher, Charles Pouchon, Eric Coissac, Julien Renaud, Wilfried Thuiller, Cristina Roquet, Martí Boleda, Frédéric Boyer, Anthony Hombiat, Bruno Bzeznik, Ludovic Gielly, Pierre Taberlet, Delphine Rioux, Jan Smyčka & Sébastien Lavergne

  2. Conservatoire et Jardin botaniques de Genève, Chambésy, Switzerland

    Charles Pouchon

  3. Plant Biodiversity Centre, Plant Science Department, University of Geneva, Chambésy, Switzerland

    Charles Pouchon

  4. Systematics and Evolution of Vascular Plants - UAB, Associated Unit to CSIC by IBB, Departament de Biologia Animal, Biologia Vegetal i Ecologia, Facultat de Biociències, Universitat Autonoma de Barcelona, Bellaterra, Spain

    Cristina Roquet, Cristina Roquet & Llorenç Sáez

  5. The Arctic University Museum of Norway, UiT - The Arctic University of Norway, Tromsø, Norway

    Inger G. Alsos, Inger Greve Alsos, Marie Kristine Føreid Merkel & Youri Lammers

  6. Univ. Grenoble Alpes, Univ. Savoie Mont Blanc, CNRS, IRD, Univ. Gustave Eiffel, ISTerre, Grenoble, France

    Pierre G. Valla, Laurent Husson & Matthias Bernet

  7. Univ. Grenoble Alpes, CNRS, Lautaret, Jardin du Lautaret, Grenoble, France

    Christophe Perrier, Rolland Douzet, Maxime Rome, Jean-Gabriel Valay & Serge Aubert

  8. Génomique Metabolique, Genoscope, Institut François Jacob, CEA, CNRS, Université Evry, Université Paris-Saclay, Evry, France

    Adriana Alberti, France Denoeud, Patrick Wincker & Céline Orvain

  9. Institute for Integrative Biology of the Cell (I2BC), Université Paris-Saclay, CEA, CNRS, Gif-sur-Yvette, France

    Adriana Alberti

  10. Swiss Federal Research Institute (WSL), Birmensdorf, Switzerland

    Niklaus E. Zimmermann, Niklaus Zimmermann, Rafael O. Wüest, Sonia Latzin, John Spillmann & Linda Feichtinger

  11. Conservatoire Botanique National Alpin, Gap, France

    Jérémie Van Es, Luc Garraud, Jean-Charles Villaret, Sylvain Abdulhak, Véronique Bonnet, Stéphanie Huc, Noémie Fort, Thomas Legland, Thomas Sanz, Gilles Pache & Alexis Mikolajczak

  12. Conservatoire Botanique National Méditerranéen, Hyéres, France

    Virgile Noble & Henri Michaud

  13. Parc National des Ecrins, Gap, France

    Cédric Dentant, Pierre Salomez & Richard Bonet

  14. Parc National de la Vanoise, Chambéry, France

    Thierry Delahaye

  15. Parc National du Mercantour, Nice, France

    Marie-France Leccia & Monique Perfus

  16. Info-Flora - Centre national de données et d’informations sur la flore de Suisse, Bern, Switzerland

    Stefan Eggenberg, Adrian Möhl, Andreas Gygax, Lea Bona & Lionel Sager

  17. Institute of Biological Research, National Institute of Research and Development for Biological Sciences, Cluj-Napoca, Romania

    Bogdan-Iuliu Hurdu & Paul-Marian Szatmari

  18. Department of Taxonomy and Ecology, Faculty of Biology and Geology and Al, Borza Botanic Garden - Babeş-Bolyai University, Cluj-Napoca, Romania

    Mihai Puşcaş & Pavel Dan Turtureanu

  19. Department of Botany, Faculty of Science, Charles University, Prague, Czech Republic

    Jan Smyčka, Patrik Mráz, Kristýna Šemberova & Marek Slovák

  20. W. Szafer Institute of Botany, Polish Academy of Sciences, Kraków, Poland

    Michał Ronikier

  21. Plant Science and Biodiversity Centre, Slovak Academy of Sciences, Bratislava, Slovak Republic

    Marek Slovák & Milan Valachovic

  22. Centre de Recherche sur la Biodiversité et l’Environnement, Université de Toulouse, CNRS, IRD, Toulouse INP, Toulouse, France

    Jerome Chave & Guillaume Besnard

  23. Conservatoire d’Espaces Naturels Provence-Alpes-Cote d’Azur, Aix en Provence, France

    Heloïse Vanderpert

  24. Institut Agronomique Néo-Calédonien, Nouméa, New Caledonia

    Laure Barrabé, Herve Vandrot & Vanessa Hecquet

  25. Museum National d’Histoire Naturelle (MNHN), Paris, France

    Thomas Haervermans & Myriam Gaudeul

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  1. Lara M. Wootton
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  2. Florian C. Boucher
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  4. Cristina Roquet
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  5. Eric Coissac
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  9. Laurent Husson
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Consortia

PhyloNorway consortium

  • Inger Greve Alsos
  • , Marie Kristine Føreid Merkel
  • , Youri Lammers
  • , Eric Coissac
  • , Charles Pouchon
  • , Adriana Alberti
  • , France Denoeud
  •  & Patrick Wincker

PhyloAlps consortium

  • Sébastien Lavergne
  • , Charles Pouchon
  • , Cristina Roquet
  • , Wilfried Thuiller
  • , Niklaus Zimmermann
  • , Eric Coissac
  • , Julien Renaud
  • , Adriana Alberti
  • , Patrick Wincker
  • , Martí Boleda
  • , Frédéric Boyer
  • , Anthony Hombiat
  • , Christophe Perrier
  • , Rolland Douzet
  • , Jean-Gabriel Valay
  • , Serge Aubert
  • , France Denoeud
  • , Bruno Bzeznik
  • , Ludovic Gielly
  • , Pierre Taberlet
  • , Delphine Rioux
  • , Céline Orvain
  • , Maxime Rome
  • , Rafael O. Wüest
  • , Sonia Latzin
  • , John Spillmann
  • , Linda Feichtinger
  • , Jérémie Van Es
  • , Luc Garraud
  • , Jean-Charles Villaret
  • , Sylvain Abdulhak
  • , Véronique Bonnet
  • , Stéphanie Huc
  • , Noémie Fort
  • , Thomas Legland
  • , Thomas Sanz
  • , Gilles Pache
  • , Alexis Mikolajczak
  • , Virgile Noble
  • , Henri Michaud
  • , Cédric Dentant
  • , Pierre Salomez
  • , Richard Bonet
  • , Thierry Delahaye
  • , Marie-France Leccia
  • , Monique Perfus
  • , Stefan Eggenberg
  • , Adrian Möhl
  • , Andreas Gygax
  • , Lea Bona
  • , Lionel Sager
  • , Bogdan-Iuliu Hurdu
  • , Paul-Marian Szatmari
  • , Mihai Puşcaş
  • , Pavel Dan Turtureanu
  • , Jan Smyčka
  • , Patrik Mráz
  • , Kristýna Šemberova
  • , Michał Ronikier
  • , Marek Slovák
  • , Milan Valachovic
  • , Llorenç Sáez
  • , Jerome Chave
  • , Guillaume Besnard
  • , Heloïse Vanderpert
  • , Laure Barrabé
  • , Herve Vandrot
  • , Vanessa Hecquet
  • , Thomas Haervermans
  •  & Myriam Gaudeul

Contributions

L.M.W., F.C.B., C. Pouchon, C.R., E.C., I.G.A., P.G.V., L.H., M.B., C. Perrier, R.D., M.R., J.-G.V., N.E.Z., P.W., W.T., J.R. and S.L. conceived and designed the experimental/analytical approach. C.R., A.A., F.D., P.W., S.L., PhyloAlps Consortium and PhyloNorway Consortium performed the experiments/conducted fieldwork. L.M.W., F.C.B., C. Pouchon, E.C., A.A., F.D., P.W., J.R. and S.L. analysed the data. C. Pouchon, C.R., E.C., I.G.A., C. Perrier, R.D., M.R., J.-G.V., N.E.Z., S.L., PhyloAlps Consortium and PhyloNorway Consortium contributed materials/analysis tools. L.M.W., F.C.B., W.T. and S.L. wrote the paper with input from all co-authors.

Corresponding author

Correspondence to Lara M. Wootton.

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Competing interests

The authors declare no competing interests.

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Peer review information

Nature Plants thanks the anonymous reviewers for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Map of the PhyloAlps and PhyloNorway sampling.

A geographically-constrained map of the PhyloAlps and PhyloNorway sampling effort. While sampling was focused on the Alps and the Arctic, the data set contains many samples from other European mountain system ranges, such as the Pyrenees, Carpathians, Balkans and Apennines. To visualise the full data set, and explore the data further, please visit the PhyloAlps website (https://phyloalps.osug.fr/).

Extended Data Fig. 2 A schematic of the decision-making process for defining colonisation, single speciation and cladogenetic speciation.

Examples of the decision process for defining assembly processes. For each clade we combined two ancestral state reconstructions, shown here on two adjacent trees: one of elevational distribution (red and blue tip states) and the other of geographic distribution (yellow and green tip states). The ancestral state reconstructions were run on 35 Myr time slices of the phylogeny, with the state of stem node forced to be either low-elevation or non-EAS as relevant. a. A colonisation event is defined as the arrival of a lineage in the Alpine sky-islands. We consider that a sky-island species has originated via colonisation if its most recent common ancestor (MRCA) occurred at low elevations or in non-EAS regions, and its current distribution includes non-EAS regions, as illustrated by species D. b. We define a single speciation event as the generation of a new species due to a lineage splitting across the boundaries of the Alpine sky-islands. Species A, B, and D are all considered single-speciation species. Species A originated via single speciation as it has speciated across both elevational and geographic boundaries, its MRCA occurring at low elevations in non-EAS regions. Species B split across elevational boundaries, likely speciating during a transition from lower elevation zones to sky-islands within the EAS. Conversely, species D had a high-elevation ancestor, but likely underwent geographic divergence after arriving from a non-EAS mountain range. c. We define a cladogenetic speciation event as lineage splitting within the boundaries of the Alpine sky-island. In the left-hand example, species B, C, and D are considered a sky-island group that originated through cladogenetic speciation, as their MRCAs are all reconstructed to occur in the sky-islands and the EAS. In this scenario, species B is assumed to have originated in the sky-island and since extended its range to include non-EAS regions. Species E is not considered part of the group, as it does not occur in the sky-islands. Although species E has sky-island and EAS ancestors, its non-sky-island distribution suggests that speciation occurred across the treeline rather than within the sky-island boundaries. Species A is not included in the group as it does not have sky-island ancestry. In the right-hand example, all five species have sky-island ancestry. Non-EAS ancestry is reconstructed at the starred node however, suggesting that at this node lineage splitting did not occur in a sky-island context. Therefore, we circumscribe two groups, the first containing species A and B, and the second containing species D and E. Species C is then considered a single speciation event.

Extended Data Fig. 3 A worked example for defining assembly processes.

A worked example for defining assembly processes within Viola. The coloured squares on the tips represent the current elevational and geographic states for each species. The pie charts on the internal nodes display the likelihoods of each state based on ancestral state reconstructions. All species that occur in the sky-islands (denoted by red squares) are considered sky-island species. Endemism status (green and yellow squares) allow us to differentiate between species that have assembled in the sky-islands through colonisation or through single speciation. Blue text on tip labels represent colonist species (for example V. palustris). Colonists are not endemic to the EAS (green squares) and their ancestors occurred at low elevations or in non-EAS regions. Orange text on tip labels represent species that originated via single speciation (for example V. thomasiana). Single-speciation species are endemic to the EAS (yellow squares) and their ancestors occurred at low elevations or in non-EAS regions, but they are not (yet) part of an EASI clade. Red tip labels represent cladogenetic species (for example V. cenisia). Cladogenetic species are endemic to the EAS (yellow squares) and their ancestors occurred at high-elevations and were EAS endemics. The size of a sky-island clade is determined by the node depth to which high-elevation and EAS endemism is reconstructed. In this example, all nodes between the tips and the starred node are reconstructed as high-elevation EAS endemics, and therefore all species below the starred node (with the exceptions of V. declinata and V. dacica) are considered to be part of a single clade that diversified in situ. V. declinata and V. dacica do not occur in the sky-islands, and thus are not considered part of the sky-island clade. The speciation events leading to their formation are not used in our calculation of cladogenetic rate. All other branching events within the clade are, however, used in the calculation of cladogenetic rate.

Extended Data Fig. 4 Distribution of the ages of the fossils used to calibrate the dating analysis.

Distribution of the ages of fossils used to calibrate the dating analysis. In total, 130 fossils were used, spanning 45 different orders and 96 different families. All fossils were sourced from the database of [51].

Source data

Extended Data Fig. 5 Comparison of node ages recovered in the dating analysis of this study to those sourced from previously published phylogenies.

Comparison of selected node ages (n = 29) recovered in the dating analysis of this study to those sourced from dated phylogenies across 19 different articles from the literature search described in the section 5.3 of the methods. Each article is represented by 1-5 points in the figure. The dashed grey line represents a 1:1 reference line.

Source data

Extended Data Fig. 6 EASI colonization events per genus.

Number of times each sky-island genus has independently entered the sky-islands.

Source data

Extended Data Fig. 7 Distribution of clade sizes in the EASI flora.

Distribution of clade sizes in the EASI flora, demonstrating that cladogenetic speciation in the sky-islands has occurred predominately in small clades of 2-3 species.

Source data

Extended Data Fig. 8 Examples of EASI plant species.

Examples of Alpine plant species occurring in the sky-islands which originated through colonisation (left column, top to bottom: Allium oleraceum, Primula farinosa, Eleocharis quinqueflora, Lilium martagon, Laserpitium latifolium), single speciation (centre column, top to bottom: Artemisia glacialis, Potentilla delphinensis, Trifolium alpinum, Myosotis alpestris, Soldanella alpina), and cladogenesis (right column, top to bottom: Scabiosa lucida, Homogyne alpina, Phyteuma scheuchzeri, Festuca alpina, Rhinanthus glacialis). All photographs copyright Jardin du Lautaret.

Extended Data Table 1 Assembly rate estimates for the EASI flora using an island biogeography model
Full size table

Supplementary information

Supplementary Information

Supplementary Tables 1–6, Fig. 1, Extended Methods, Fossil information and Biogeographic literature search references.

Reporting Summary

Source data

Source Data Fig. 2

Dated phylogeny.

Source Data Fig. 3

Statistical source data.

Source Data Fig. 4

Statistical source data.

Source Data Fig. 5

Statistical source data.

Source Data Extended Data Fig. 4

Statistical source data.

Source Data Extended Data Fig. 5

Statistical source data.

Source Data Extended Data Fig. 6

Statistical source data.

Source Data Extended Data Fig. 7

Statistical source data.

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Wootton, L.M., Boucher, F.C., Pouchon, C. et al. The late rise of sky-island vegetation in the European Alps. Nat. Plants 11, 1142–1153 (2025). https://doi.org/10.1038/s41477-025-02001-0

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