[en] Climatic fluctuations during the Last Glacial Maximum (LGM) exerted a profound influence on biodiversity patterns, but their impact on bryophytes, the second most diverse group of land plants, has been poorly documented. Approximate Bayesian computations based on coalescent simulations showed that the post-glacial assembly of European bryophytes involves a complex his- tory from multiple sources. The contribution of allochthonous migrants was 95–100% of expand- ing populations in about half of the 15 investigated species, which is consistent with the globally balanced genetic diversities and extremely low divergence observed among biogeographical regions. Such a substantial contribution of allochthonous migrants in the post-glacial assembly of Europe is unparalleled in other plants and animals. The limited role of northern micro-refugia, 2 which was unexpected based on bryophyte life-history traits, and of southern refugia, is consistent with recent palaeontological evidence that LGM climates in Eurasia were much colder and drier than what palaeoclimatic models predict.
Ledent, Alice ✱; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie de l'évolution et de la conservation - aCREA-Ulg
Désamoré, Aurélie ✱; Stockholm University > Ecology, Environment, and Plant Sciences > Science for Life laboratory
Laenen, Benjamin; Stockholm University > Ecology, Environment, and Plant Sciences > Science for Life Laboratory
Mardulyn, Patrick; Free University of Brussels > Evolutionary Biology & Ecology
McDaniel, Stuart; University of Florida > Biology Department
Zanatta, Florian ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie de l'évolution et de la conservation - aCREA-Ulg
Patino, Jairo ✱
Vanderpoorten, Alain ✱; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie de l'évolution et de la conservation - aCREA-Ulg
✱ These authors have contributed equally to this work.
Language :
English
Title :
No borders during the post-glacial assembly of European bryophytes
Alternative titles :
[fr] Pas de frontières durant la recolonisation post-glaciaire des bryophytes européennes
Publication date :
22 March 2019
Journal title :
Ecology Letters
ISSN :
1461-023X
eISSN :
1461-0248
Publisher :
Wiley, Oxford, United Kingdom
Volume :
22
Issue :
6
Pages :
973-986
Peer reviewed :
Peer Reviewed verified by ORBi
Tags :
CÉCI : Consortium des Équipements de Calcul Intensif
Abbott, R.J. & Brochmann, C. (2003). History and evolution of the arctic flora: in the footsteps of Eric Hultén. Mol. Ecol., 12, 299–313.
Alsos, I.G., Eidesen, P.B., Ehrich, D., Skrede, I., Westergaard, K., Jacobsen, G.H. et al. (2007). Frequent long-distance plant colonization in the changing Arctic. Science, 316, 1606–1609.
Bhagwat, S.A. & Willis, K.J. (2008). Species persistence in northerly glacial refugia of Europe: a matter of chance or biogeographical traits? J. Biogeogr., 35, 464–482.
Biersma, E.M., Jackson, J.A., Hyvönen, J., Koskinen, S., Linse, K., Griffiths, H. et al. (2017). Global biogeographic patterns in bipolar moss species. Roy. Soc. Open Sci., 4, 170147.
Biersma, E.M., Jackson, J.A., Stech, M., Griffiths, H., Linse, K. & Convey, P. (2018). Molecular data suggest long-term in situ Antarctic persistence within Antarctica's most speciose plant genus, Schistidium. Front. Ecol. Evol., 6, 77.
Binney, H., Edwards, M., Macias-Fauria, M., Lozhkin, A., Anderson, P., Kaplan, J.O. et al. (2017). Vegetation of Eurasia from the last glacial maximum to present: key biogeographic patterns. Quat. Sci. Rev., 157, 80–97.
Bosanquet, S. (2012). Vagrant epiphytic mosses in England and Wales. Field Bryol., 107, 3–17.
Cannone, N., Corinti, T., Malfasi, F., Gerola, P., Vianelli, A., Vanetti, I. et al. (2017). Moss survival through in situ cryptobiosis after six centuries of glacier burial. Sci. Rep., 7, 4438.
Cronberg, N. (2000). Genotypic diversity of the epiphytic bryophyte Leucodon sciudoides in formerly glaciated versus nonglaciated parts of Europe. Heredity, 84, 710–720.
Darwin, C. (1859). The Origin of Species. John Murray, London.
Désamoré, A., Patiño, J., Mardulyn, P., Laenen, B., McDaniel, S., Zanatta, F. et al. (2016). High migration rates shape the postglacial history of amphi-Atlantic bryophytes. Mol. Ecol., 25, 5568–5584.
During, H.J. (1992). Ecological classification of bryophytes and lichens. In Bryophytes and Lichens in Changing Environment. (eds Bates, J.W., Farmer, A.M.). Clarendon Press, Oxford, pp. 1–31.
Edgar, R.C. (2004). MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5, 113.
Eidesen, P.B., Ehrich, D., Bakkestuen, V., Alsos, I.G., Gilg, O., Taberlet, P. et al. (2013). Genetic roadmap of the Arctic: plant dispersal highways, traffic barriers and capitals of diversity. New Phytol., 200, 898–910.
Excoffier, L. & Lischer, H.E.L. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Res., 10, 564–567.
Excoffier, L., Dupanloup, I., Huerta-Sánchez, E., Sousa, V.C. & Foll, M. (2013). Robust demographic inference from genomic and SNP data. PLoS Genet., 9, e1003905.
Gouy, M., Guindon, S. & Gascuel, O. (2010). SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol., 27, 221–224.
Grundmann, M., Ansell, S.W., Russell, S.J., Koch, M.A. & Vogel, J.C. (2008). Hotspots of diversity in a clonal world — the Mediterranean moss Pleurochaete squarrosa in Central Europe. Mol. Ecol., 17, 825–838.
Hewitt, G.M. (1999). Post-glacial recolonisation of European biota. Biol. J. Linn. Soc., 68, 87–112.
Hewitt, G.M. (2000). The genetic legacy of the Quaternary ice ages. Nature, 405, 907–913.
Hewitt, G.M. (2004). Genetic consequences of climatic oscillations in the quaternary. Phil. Trans. Roy. Soc. B, 359, 183–195.
Hooker, J.D. (1862). Outlines on the distribution of arctic plants. Trans. Linn. Soc. London, 23, 251–348.
Hultén, E. (1937). Outline of the History of Arctic and Boreal Biota During the Quarternary Period. Lehre J. Cramer, New York.
Hutsemékers, V., Shaw, A.J., Szvovenyi, P., Gonzalez-Mancebo, J.M., Muñoz, J. & Vanderpoorten, A. (2011). Islands are not sinks of biodiversity in spore-producing plants. Proc. Natl Acad. Sci. USA, 108, 18989–18994.
Jakab, G. & Sümegi, P. (2011). The role of bryophyte paleoecology in quaternary climate reconstructions. In Bryophyte Ecology and Climate Change. (eds Tuba, Z., Slack, N.G., Stark, L.R.). Cambridge University Press, Cambridge, pp. 335–358.
Kyrkjeeide, M.O., Stenøien, H.K., Flatberg, K.I. & Hassel, K. (2014). Glacial refugia and post-glacial colonization patterns in European bryophytes. Lindbergia, 37, 47–59.
Kyrkjeeide, M.O., Hassel, K., Flatberg, K.I., Shaw, A.J., Brochmann, C. & Stenøien, H.K. (2016). Long-distance dispersal and barriers shape genetic structure of peatmosses (Sphagnum) across the Northern Hemisphere. J. Biogeogr., 43, 1215–1226.
La Farge, C., Krista, H., Williams, K.H. & England, J.H. (2013). Regeneration of Little Ice Age bryophytes emerging from a polar glacier with implications of totipotency in extreme environments. Proc. Natl Acad. Sci. USA, 110, 9839–9844.
Laenen, B., Désamoré, A., Devos, N., Shaw, A.J., Carine, M.A., Gonzalez-Mancebo, J.M. et al. (2011). Macaronesia: a source of hidden genetic diversity for post-glacial recolonization of western Europe in the leafy liverwort Radula lindenbergiana. J. Biogeogr., 38, 631–639.
Leuenberger, C. & Wegmann, D. (2010). Bayesian computation and model selection without likelihoods. Genetics, 184, 243–252.
Lintusaari, J., Gutmann, M.U., Dutta, R., Kaski, S. & Corander, J. (2017). Fundamentals and recent developments in Approximate Bayesian Computation. Syst. Biol., 66, e66–e82.
Lumibao, C.Y., Hoban, S.M. & McLachlan, J. (2017). Ice ages leave genetic diversity ‘hotspots’ in Europe but not in Eastern North America. Ecol. Lett., 20, 1459–1468.
McDaniel, S.F. & Shaw, A.J. (2005). Selective sweeps and intercontinental migration in the cosmopolitan moss Ceratodon purpureus (Hedw.). Brid. Mol. Ecol., 14, 1121–1132.
McDaniel, S.F., Baren, M.Jv, Jones, K.S., Payton, A.C. & Quatrano, R.S. (2013). Estimating the nucleotide diversity in Ceratodon purpureus (Ditrichaceae) from 218 conserved exon-primed, intron-spanning nuclear loci. Appl. Plant Sci., 1, 1200387.
Médail, F. & Diadema, K. (2009). Glacial refugia influence plant diversity patterns in the Mediterranean Basin. J. Biogeogr., 36, 1333–1345.
Normand, S., Ricklefs, R.E., Skov, F., Bladt, J., Tackenberg, O. & Svenning, J.C. (2011). Postglacial migration supplements climate in determining plant species ranges in Europe. Proc. R. Soc. Lond. B, 278, 3644–3653.
Paradis, E. (2010). Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics, 26, 419–420.
Patiño, J., Carine, M., Mardulyn, P., Devos, N., Mateo, R.G., González-Mancebo, J.M. et al. (2015). Approximate Bayesian Computation reveals the crucial role of oceanic islands for the assembly of continental biodiversity. Syst. Biol., 64, 579–589.
Pearson, R.G. (2006). Climate change and the migration capacity of species. Trends Ecol. Evol., 21, 111–113.
Petit, R.J., Aguinalde, I., de Beaulieu, J.L., Bittkau, C., Brewer, S., Cheddadi, R. et al. (2003). Glacial refugia: hotspots but not melting pots of genetic diversity. Science, 300, 1563–1565.
Pisa, S., Biersma, E.M., Convey, P., Patiño, J., Vanderpoorten, A., Werner, O. et al. (2013). The cosmopolitan moss Bryum argenteum in Antarctica: back-colonization from extra-regional Pleistocene refugia or in-situ survival? Polar Biol., 37, 1469–1477.
Roads, E., Longton, R.E. & Convey, P. (2014). Millenial timescale regeneration in a moss from Antarctica. Curr. Biol., 24, R222–R223.
Robert, C.P., Cornuet, J.M., Marin, J.M. & Pillai, N.S. (2011). Lack of confidence in approximate Bayesian computation model choice. Proc. Natl Acad. Sci. USA, 108, 15112–15117.
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.
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.
Schönswetter, P., Popp, M. & Brochmann, C. (2006). Rare arctic-alpine plants of the European Alps have different immigration histories: the snow bed species Minuartia biflora and Ranunculus pygmaeus. Mol. Ecol., 15, 709–720.
Semerikov, V.L., Semerikova, S.A., Polezhaeva, M.A., Kosintsev, P.A. & Lascoux, M. (2013). Southern montane populations did not contribute to the recolonization of West Siberian Plain by Siberian larch (Larix sibirica): a range-wide analysis of cytoplasmic markers. Mol. Ecol., 22, 4958–4971.
Skrede, I., Eidesen, P.B., Portela, R.P. & Brochmann, C. (2006). Refugia, differentiation and postglacial migration in arctic-alpine Eurasia, exemplified by the mountain avens (Dryas octopetala L.). Mol. Ecol., 15, 1827–1840.
Stenøien, H.K., Shaw, A.J., Shaw, B., Hassel, K. & Gunnarsson, U. (2011). North American origin and recent European establishment of the amphi-Atlantic peat moss Sphagnum angermanicum. Evolution, 65, 1181–1194.
Sundberg, S. (2005). Larger capsules enhance short-range spore dispersal in Sphagnum, but what happens further away? Oikos, 108, 115–124.
Svenning, J.C., Normand, S. & Kageyama, M. (2008). Glacial refugia of temperate trees in Europe: insights from species distribution modelling. J. Ecol., 96, 1117–1127.
Szövényi, P., Terracciano, S., Ricca, M., Giordano, S. & Shaw, A.J. (2008). Recent divergence, intercontinental dispersal and shared polymorphism are shaping the genetic structure of amphi-Atlantic peatmoss populations. Mol. Ecol., 17, 5364–5377.
Szövényi, P., Sundberg, S. & Shaw, A.J. (2012). Long-distance dispersal and genetic structure of natural populations: an assessment of the inverse isolation hypothesis in peat mosses. Mol. Ecol., 21, 5461–5472.
Thomé, M.T. & Carstens, B.C. (2016). Phylogeographic model selection leads to insight into the evolutionary history of four-eyed frogs. Proc. Natl Acad. Sci. USA, 113, 8010–8017.
Tzedakis, P.C., Emerson, B.C. & Hewitt, G.M. (2013). Cryptic or mystic? Glacial tree refugia in northern Europe. Trends Ecol. Evol., 28, 696–704.
Van der Velde, M. & Bijlsma, R. (2003). Phylogeography of five Polytrichum species within Europe. Biol. J. Linn. Soc., 78, 203–213.
Vanderpoorten, A., Gradstein, S.R., Carine, M.A. & Devos, N. (2010). The ghosts of Gondwana and Laurasia in modern liverwort distributions. Biol. Rev. Camb. Philos. Soc., 85, 471–487.
Wegmann, D., Leuenberger, C., Neuenschwander, S. & Excoffier, L. (2010). ABCtoolbox: a versatile toolkit for approximate Bayesian computations. BMC Bioinformatics, 11, 116.
Westergaard, K.B., Alsos, I.G., Popp, M., Engelskjøn, T., Flatberg, K.I. & Brochmann, C. (2011). Glacial survival may matter after all: nunatak signatures in the rare European populations of two west-arctic species. Mol. Ecol., 20, 376–393.