Abstract
Biogeographic regions have been extensively used as reference units in macroecological studies and to prioritize biodiversity conservation efforts. However, classical bioregionalizations were delineated based on taxonomical similarity across space, and thus the importance of historical factors may have been underrated. This limitation may be particularly relevant for lineages with long and complex evolutionary histories, such as ferns. Here, we drew on an exhaustive distribution dataset including all fern species and subspecies of Europe (661 grid-cells of c. 110 × 110 km each), as well as a nearly complete molecular phylogeny to define fern phyloregions based on their phylogenetic relatedness. Also, we quantified the degree of specificity of individual phylogenetic clades to the phyloregions using a new index of geographical confinement based on phylogenetic diversity. Six distinct phyloregions were identified, with a primary divide between north-eastern and south-western Europe. Both phylogenetic beta diversity and clade specificity were overall low, supporting the idea that dispersal limitation is not a major driver of fern distribution. Yet, the phylogenetic specificity analysis revealed that ancient fern lineages show preference for northern latitudes, which explained the northeast to southwest split of the territory. More than 40 years after the only bioregionalization analysis for the European fern flora, our study provides a fresh regional delineation that takes into account the evolutionary history of the group. In addition to classical bioregionalization approaches, our phylogenetic specificity index allowed us to elucidate the identity of the clades that ultimately shaped the bioregions, which might otherwise had remained obscure.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Code availability
The R code for the phylogenetic specificity analysis is provided in Appendix S2.
Data availability
All data will be available at Dryad repository after acceptation of the manuscript.
References
Alsos IG, Ehrich D, Eidesen PB et al (2015) Long-distance plant dispersal to North Atlantic islands: colonization routes and founder effect. AoB Plants 7:1–19. https://doi.org/10.1093/aobpla/plv036/200777
Barrington DS (1993) Ecological and historical factors in fern biogeography. J Biogeogr 20:275–279. https://doi.org/10.2307/2845635
Barrón EJ (1985) Explanations of the tertiary global cooling trend. Palaeogeogr Palaeoclimatol Palaeoecol 50:45–61. https://doi.org/10.1016/S0031-0182(85)80005-5
Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Glob Ecol Biogeogr 19:134–143. https://doi.org/10.1111/j.1466-8238.2009.00490.x
Baselga A, Orme D, Villeger S, Bortoli JD, Leprieur F (2018) betapart: partitioning beta diversity into turnover and nestedness components. R package version 1.5.1
Birks HJB (1976) The distribution of European pteridophytes: a numerical analysis. New Phytol 77:257–287. https://doi.org/10.1111/j.1469-8137.1976.tb01517.x
Bocard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 73:1045–1055. https://doi.org/10.2307/1940179
Bruch AA, Uhl D, Mosbrugger V (2007) Miocene climate in Europe—patterns and evolution. Palaeogeogr Palaeoclimatol Palaeoecol 253:1–7. https://doi.org/10.1016/j.palaeo.2007.03.030
Bryant JA, Lamanna C, Morlon H, Kerkhoff AJ, Enquist BJ, Green JL (2008) Microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. PNAS 105:11505–11511. https://doi.org/10.1073/pnas.0801920105
Calatayud J, Hortal J, Medina NG, Turin H, Bernard R, Casale A, Ortuño VM, Penev L, Rodríguez MÁ (2016) Glaciations, deciduous forests, water availability and current geographical patterns in the diversity of European Carabus species. J Biogeogr 43:2343–2353. https://doi.org/10.1111/jbi.12811
Calatayud J, Rodríguez MÁ, Molina-Venegas R, Leo M, Horreo JL, Hortal J (2019) Pleistocene climate change and the formation of regional species pools. Proc R Soc B 286:20190291. https://doi.org/10.1098/rspb.2019.0291
Castro-Insua A, Gómez-Rodríguez C, Baselga A (2018) Dissimilarity measures affected by richness differences yield biased delimitations of biogeographic realms. Nat Commun 9:5084. https://doi.org/10.1038/s41467-018-06291-1
Christenhusz MJM, Chase MW (2014) Trends and concepts in fern classification. Ann Bot 113:571–594. https://doi.org/10.1093/aob/mct299
Collinson ME, Hooker JJ (2003) Paleogene vegetation of Eurasia: framework for mammalian faunas. Deinsea 10:41–84
Dapporto L, Ramazzotti M, Fattorini S, Talavera G, Vila R, Dennis RLH (2013) recluster: an unbiased clustering procedure for beta-diversity turnover. Ecography 36:1070–1075. https://doi.org/10.1111/j.1600-0587.2013.00444.x
Daru BH, van der Bank M, Maurin O, Yessoufou K, Schaefer H, Slingsby JA, Davies TJ (2016) A novel phylogenetic regionalization of phytogeographical zones of southern Africa reveals their hidden evolutionary affinities. J Biogeogr 43:155–166. https://doi.org/10.1111/jbi.12619
Daru BH, Elliott TL, Park DS, Davies TJ (2017) Understanding the processes underpinning patterns of phylogenetic regionalization. Trends Ecol Evol 32:845–860. https://doi.org/10.1016/j.tree.2017.08.013
Des Marais DL, Smith AR, Britton DM, Pryer KM (2003) Phylogenetic relationships and evolution of extant horsetails, Equisetum, based on chloroplast DNA sequence data (rbcL and trnL-F). Int J Plant Sci 164:737–751
Dezsi Ş, Mîndrescu M, Petrea D et al (2018) High-resolution projections of evapotranspiration and water availability for Europe under climate change. Int J Clim 38:3832–3841. https://doi.org/10.1002/joc.5537
Dupont P (1962) La flore atlantique européenne. Introduction a l’étude du secteur ibéro-atlantique. Documents pour les cartes des productions végétales. Série Europe-Atlantique, vol I. Faculté des Scientes, Toulouse
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. https://doi.org/10.1016/0006-3207(92)91201-3
Ferrer-Castán D, Vetaas OR (2005) Pteridophyte richness, climate and topography in the Iberian Peninsula: comparing spatial and nonspatial models of richness patterns. Glob Ecol Biogeogr 14:155–165. https://doi.org/10.1111/j.1466-822X.2004.00140.x
Fraser-Jenkins CR (2007) The species and subspecies in the Dryopteris affinis group. Fern Gaz 18:1–26
Gilbert JKB, Lechowicz MJ (2005) Fern community assembly: the roles of chance and the environment at local and intermediate scales. Ecology 86:2473–2486. https://doi.org/10.1890/04-1420
Hantemirova EV, Heinze B, Knyazeva SG, Musaev AM, Lascoux M, Semerikov VL (2017) A new Eurasian phylogeographical paradigm? Limited contribution of southern populations to the recolonization of high latitude populations in Juniperus communis L. (Cupressaceae). J Biogeogr 44:271–282. https://doi.org/10.1111/jbi.12867
Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112. https://doi.org/10.1006/bijl.1999.0332
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978. https://doi.org/10.1002/joc.1276
Holt BG, Lessard J-P, Borregaard MK et al (2013) An update of Wallace’s zoogeographic regions of the world. Science 339:74–78. https://doi.org/10.1126/science.1228282
Hortal J, Diniz-Filho JA, Bini LISM, Rodríguez MÁ, Baselga A, Nogués-Bravo D, Rangel TF, Hawkins BA (2011) Ice age climate, evolutionary constraints and diversity patterns of European dung beetles. Ecol Lett 14:1–21. https://doi.org/10.1111/j.1461-0248.2011.01634.x
Jalas J, Suominen J (1972) Atlas Florae Europaeae, Volume I Pteridophyta (Psilotaceae to Azollaceae). The committee for mapping the flora of Europe and Societas Biologica Fennica Vanamo, Helsinki
Jønsson KA, Holt BG (2015) Islands contribute disproportionately high amounts of evolutionary diversity in passerine birds. Nat Commun 6:8538. https://doi.org/10.1038/ncomms9538
Juslén A, Väre H, Wikström N (2011) Relationships and evolutionary origins of polyploid Dryopteris (Dryopteridaceae) from Europe inferred using nuclear pgiC and plastid trnL-F sequence data. Taxon 60:1284–1294. https://doi.org/10.1002/tax.605005
Kelley LA, Gardner SP, Sutcliffe MJ (1996) An automated approach for clustering an ensemble of NMR-derived protein structures into conformationally related subfamilies. Protein Eng 9:1063–1065. https://doi.org/10.1093/protein/9.11.1063
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. https://doi.org/10.1093/bioinformatics/btq166
Kreft H, Jetz W (2010) A framework for delineating biogeographical regions based on species distributions. J Biogeogr 37:2029–2053. https://doi.org/10.1111/j.1365-2699.2010.02375.x
Kreft H, Jetz W, Mutke J, Barthlott W (2010) Contrasting environmental and regional effects on global pteridophyte and seed plant diversity. Ecography 33:408–419. https://doi.org/10.1111/j.1600-0587.2010.06434.x
Lehtonen S, Silvestro D, Karger DN, Scotese C, Tuomisto H, Kessler M, Peña C, Wahlberg N, Antonelli A (2017) Environmentally driven extinction and opportunistic origination explain fern diversification patterns. Sci Rep 7:1–12. https://doi.org/10.1038/s41598-017-05263-7
Leprieur F, Albouy C, De Bortoli J, Cowman PF, Bellwood DR, Mouillot D (2012) Quantifying phylogenetic beta diversity: distinguishing between ‘true’ turnover of lineages and phylogenetic diversity gradients. PLoS ONE 7:e42760. https://doi.org/10.1371/journal.pone.0042760
Mai DH (1989) Development and regional differentiation of the European vegetation during the Tertiary. Plant Syst Evol 162:79–91. https://doi.org/10.1007/978-3-7091-3972-1_4
Mai DH (1991) Palaeofloristic changes in Europe and the confirmation of the Arctotertiary-Palaeotropical geofloral concept. Rev Palaeobot Palynol 68:29–36. https://doi.org/10.1016/0034-6667(91)90055-8
Marchetti D (2004) Le pteridofite d’Italia. Ann Mus Civ Rov 19:71–231
Molina-Venegas R, Aparicio A, Slingsby JA, Lavergne S, Arroyo J (2015) Investigating the evolutionary assembly of a Mediterranean biodiversity hotspot: deep phylogenetic signal in the distribution of eudicots across elevational belts. J Biogeogr 42:507–518. https://doi.org/10.1111/jbi.12398
Molina-Venegas R, Aparicio A, Lavergne S, Arroyo J (2017) Climatic and topographical correlates of plant palaeo- and neoendemism in a Mediterranean biodiversity hotspot. Ann Bot 119:229–238. https://doi.org/10.1093/aob/mcw093
Montalvo-Mancheno CS, Ondei S, Brook BW, Buettel JC (2020) Bioregionalization approaches for conservation: methods, biases, and their implications for Australian biodiversity. Biodivers Conserv 29:1–17. https://doi.org/10.1007/s10531-019-01913-6
Montoya D, Rodríguez MA, Zavala MA, Hawkins BA (2007) Contemporary richness of holarctic trees and the historical pattern of glacial retreat. Ecography 30:173–182. https://doi.org/10.1111/j.0906-7590.2007.04873.x
Moran RC (2008) Diversity, biogeography, and floristics. In: Ranker TA, Haufler CH (eds) Biology and evolution of ferns and lycophytes. Cambridge University Press, Cambridge, pp 367–394
Moreno-Saiz JC, Lobo JM (2008) Iberian-Balearic fern regions and their explanatory variables. Plant Ecol 198:149–167. https://doi.org/10.1007/s11258-007-9392-8
Moreno-Saiz JC, Donato M, Katinas L, Crisci JV, Posadas P (2013) New insights into the biogeography of south-western Europe: spatial patterns from vascular plants using cluster analysis and parsimony. J Biogeogr 40:90–104. https://doi.org/10.1111/j.1365-2699.2012.02774.x
Moreno-Saiz JC, Pataro L, Pajarón S (2015) Atlas de los pteridófitos de la Península Ibérica e Islas Baleares. Acta Bot Malac 40:5–55. https://doi.org/10.24310/abm.v40i0.2540
Oksanen J, Blanchet FG, Kindt R et al (2015) vegan: Community ecology package. R package version 2.4-1
Palamarev E (1989) Paleobotanical evidences of the Tertiary history and origin of the Mediterranean sclerophyll dendroflora. Plant Syst Evol 162:93–107. https://doi.org/10.1007/BF00936912
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290. https://doi.org/10.1093/bioinformatics/btg412
Pausas JG, Sáez L (2000) Pteridophyte richness in the NE Iberian Peninsula: biogeographic patterns. Plant Ecol 148:1–11. https://doi.org/10.1023/A:1009899615852
Pichi-Sermolli REG, España L, Salvo AE (1988) El valor biogeográfico de la pteridoflora ibérica. Lazaroa 10:187
Postigo-Mijarra JM, Barrón E, Gómez Manzaneque F, Morla C (2009) Floristic changes in the Iberian Peninsula and Balearic Islands (south-west Europe) during the Cenozoic. J Biogeogr 36:2025–2043. https://doi.org/10.1111/j.1365-2699.2009.02142.x
PPG I (2016) A community-based classification for extant ferns and lycophytes. J Syst Evol 54:563–603. https://doi.org/10.1111/jse.12229
Pryer KM, Schneider H, Smith AR, Cranfill R, Wolf PG, Hunt JS, Sipes SD (2001) Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409:618–622. https://doi.org/10.1038/35054555
Pryer KM, Schuettpelz E, Wolf PG, Schneider H, Smith AR, Cranfill R (2004) Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. Am J Bot 91:1582–1598. https://doi.org/10.3732/ajb.91.10.1582
R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rothfels CJ, Li FW, Sigel EM et al (2015) The evolutionary history of ferns inferred from 25 low-copy nuclear genes. Am J Bot 102:1089–1107. https://doi.org/10.3732/ajb.1500089
Rumsey FJ, Vogel JC, Russell SJ, Barrett JA, Gibby M (1998) Climate, colonisation and celibacy: population structure in central European Trichomanes speciosum (Pteridophyta). Bot Acta 111:481–489. https://doi.org/10.1111/j.1438-8677.1998.tb00736.x
Salvador S, Chan P (2004) Determining the number of clusters/segments in hierarchical clustering/segmentation algorithms. Proceedings of the sixteenth IEEE international conference on tools with artificial intelligence, pp 576–584. Institute of Electrical and Electronics Engineers, Piscataway, New Jersey, USA. https://ieeexplore.ieee.org/document/1374239
Schuettpelz E, Pryer KM (2009) Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. PNAS 106:11200–11205. https://doi.org/10.1073/pnas.0811136106
Sharpe JM, Mehltreter K, Walker LR (2010) In: Mehltreter K, Walker LR, Sharpe JM (eds) Ecological importance of ferns. Fern ecology. Cambridge University Press, Cambridge, pp 1–21. https://doi.org/10.1017/CBO9780511844898.002
Singh G (1988) History of aridland vegetation and climate: a global perspective. Biol Rev 63:159–195. https://doi.org/10.1111/j.1469-185X.1988.tb00629.x
Svendsen JI, Alexanderson H, Astakhov VI et al (2004) Late quaternary ice sheet history of northern Eurasia. Quat Sci Rev 23:1229–1271. https://doi.org/10.1016/j.quascirev.2003.12.008
Svenning JC, Skov F (2007) Could the tree diversity pattern in Europe be generated by postglacial dispersal limitation? Ecol Lett 10:453–460. https://doi.org/10.1111/j.1461-0248.2007.01038.x
Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464. https://doi.org/10.1046/j.1365-294x.1998.00289.x
Testo W, Sundue M (2016) A 4000-species dataset provides new insight into the evolution of ferns. Mol Phylogen Evol 105:200–211. https://doi.org/10.1016/j.ympev.2016.09.003
Thompson JD (2005) Plant evolution in the Mediterranean. Oxford University Press, Oxford
Trabucco A, Zomer RJ (2010) Global soil water balance geospatial database. CGIAR Consortium for Spatial Information. Available from the CGIAR-CSI GeoPortal at: http://www.cgiar-csi.org
Tryon R (1986) The biogeography of species, with special reference to ferns. Bot Rev 52:117–156. https://doi.org/10.1007/BF02860999
Utescher T, Mosbrugger V (2007) Eocene vegetation patterns reconstructed from plant diversity—a global perspective. Palaeogeogr Palaeoclimatol Palaeoecol 247:243–271. https://doi.org/10.1016/j.palaeo.2006.10.022
van den Dool H, Huang J, Fan Y (2003) Performance and analysis of the constructed analogue method applied to U.S. soil moisture over 1981–2001. J Geophys Res Atmos 108:8617. https://doi.org/10.1029/2002JD003114
Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York
Vogel JC, Rumsey FJ, Schneller JJ, Barrett JA, Gibby M (1999) Where are the glacial refugia in Europe? Evidence from pteridophytes. Biol J Linn Soc 66:23–37. https://doi.org/10.1111/j.1095-8312.1999.tb01915.x
Wagner WH, Wagner FS (1983) Genus communities as a systematic tool in the study of new world Botrychium (Ophioglossaceae). Taxon 32:51–63. https://doi.org/10.2307/1219850
Weigand A, Abrahamczyk S, Aubin I et al (2020) Global fern and lycophyte richness explained: how regional and local factors shape plot richness. J Biogeogr 47:59–71. https://doi.org/10.1111/jbi.13782
White D, Gramacy RB (2012) maptree: mapping, pruning, and graphing tree models. R package version 1.4-7
Wolf PG, Schneider H, Ranker TA (2001) Geographic distributions of homosporous ferns: does dispersal obscure evidence of vicariance? J Biogeogr 28:263–270. https://doi.org/10.1046/j.1365-2699.2001.00531.x
Acknowledgements
We thank our colleagues Santiago Pajarón, Marcelo Arana and Llorenç Sáez for their comments on an earlier version of the manuscript and suggestions for taxonomic treatment. LP holds a CAPES PhD Grant (1192-13-2) and RMV was supported by a TALENTO fellow of the regional government of Madrid, Spain (2018-T2/AMB-10332). This work was supported by the Spanish Ministry of Science, Innovation and Universities through the Bioregions 2.0 project (CGL2017-86926-P grant to M.A.R. and J.C.M-S).
Author information
Authors and Affiliations
Contributions
L.P., J.C.M.S. and M.A.R. designed the research; L.P. conducted the analysis; L.P. and R.M.V. built the phylogenetic tree; R.M.V, J.C. and M.A.R. contributed analytical tools; R.M.V. led the writing with help from all the authors.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare no conflicts of interests.
Additional information
Communicated by Daniel Sanchez Mata.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10531_2020_2087_MOESM1_ESM.pdf
Supplementary material 1 (PDF 817 kb) Appendix S1: Phylogenetic reconstruction methods, checklist and supplementary results
Rights and permissions
About this article
Cite this article
Pataro, L., Molina-Venegas, R., Calatayud, J. et al. An updated phylogenetic bioregionalization for the European fern flora. Biodivers Conserv 30, 201–215 (2021). https://doi.org/10.1007/s10531-020-02087-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-020-02087-2