The extreme Beringian/Atlantic disjunction in Saxifraga rivularis (Saxifragaceae) has formed at least twice
Corresponding Author
Kristine Bakke Westergaard
Tromsø University Museum, University of Tromsø, NO-9037 Tromsø, Norway
National Centre for Biosystematics, Natural History Museum, University of Oslo, PO Box 1172 Blindern, NO-0318 Oslo, Norway
Kristine Bakke Westergaard, Tromsø University Museum, University of Tromsø, NO-9037 Tromsø, Norway.E-mail: [email protected]Search for more papers by this authorMarte Holten Jørgensen
Department of Biology, Centre for Ecological and Evolutionary Synthesis (CEES), University of Oslo, PO Box 1066 Blindern, NO-0316 Oslo, Norway
Search for more papers by this authorTove M. Gabrielsen
National Centre for Biosystematics, Natural History Museum, University of Oslo, PO Box 1172 Blindern, NO-0318 Oslo, Norway
University Centre in Svalbard, PO Box 156, NO-9171 Longyearbyen, Norway
Search for more papers by this authorInger Greve Alsos
University Centre in Svalbard, PO Box 156, NO-9171 Longyearbyen, Norway
Search for more papers by this authorChristian Brochmann
National Centre for Biosystematics, Natural History Museum, University of Oslo, PO Box 1172 Blindern, NO-0318 Oslo, Norway
Search for more papers by this authorCorresponding Author
Kristine Bakke Westergaard
Tromsø University Museum, University of Tromsø, NO-9037 Tromsø, Norway
National Centre for Biosystematics, Natural History Museum, University of Oslo, PO Box 1172 Blindern, NO-0318 Oslo, Norway
Kristine Bakke Westergaard, Tromsø University Museum, University of Tromsø, NO-9037 Tromsø, Norway.E-mail: [email protected]Search for more papers by this authorMarte Holten Jørgensen
Department of Biology, Centre for Ecological and Evolutionary Synthesis (CEES), University of Oslo, PO Box 1066 Blindern, NO-0316 Oslo, Norway
Search for more papers by this authorTove M. Gabrielsen
National Centre for Biosystematics, Natural History Museum, University of Oslo, PO Box 1172 Blindern, NO-0318 Oslo, Norway
University Centre in Svalbard, PO Box 156, NO-9171 Longyearbyen, Norway
Search for more papers by this authorInger Greve Alsos
University Centre in Svalbard, PO Box 156, NO-9171 Longyearbyen, Norway
Search for more papers by this authorChristian Brochmann
National Centre for Biosystematics, Natural History Museum, University of Oslo, PO Box 1172 Blindern, NO-0318 Oslo, Norway
Search for more papers by this authorAbstract
Aim The oceanic Saxifraga rivularis L. presents one of the most extreme disjunctions known in the arctic flora: it has a small amphi-Beringian range and a larger amphi-Atlantic one. It was recently suggested to have had a single allopolyploid origin in Beringia at least one glacial cycle ago, followed by gradual expansion in a more humid period and differentiation into two allopatric subspecies (the Atlantic ssp. rivularis and the Beringian ssp. arctolitoralis). Here we explore the history of its extreme disjunction.
Location The amphi-Beringian and northern amphi-Atlantic regions.
Methods We obtained amplified fragment length polymorphisms (AFLPs) and chloroplast DNA sequences from 36 populations (287 individuals) and 13 populations (15 individuals), respectively. The data were analysed using principal coordinates analyses, Bayesian clustering methods, and analyses of molecular variance.
Results Two distinctly divergent AFLP groups were observed, corresponding to the two described subspecies, but, surprisingly, four of the West Atlantic populations belonged to the supposedly Beringian endemic ssp. arctolitoralis. This was confirmed by re-examination of their morphological characteristics. The overall AFLP diversity in the species was low (26.4% polymorphic markers), and there was no variation in the five investigated chloroplast DNA (cpDNA) regions. There was little geographic structuring of the AFLP diversity within each subspecies, even across the extreme disjunction in ssp. arctolitoralis, across the Bering Sea, and across the Atlantic Ocean, except that most plants from the arctic Svalbard archipelago formed a separate genetic group with relatively high diversity.
Main conclusions The extreme disjunction in S. rivularis has evidently formed at least twice. The first expansion from Beringia was followed by allopatric differentiation into one Beringian and one Atlantic subspecies, which are distinctly divergent at AFLP loci but still harbour identical cpDNA haplotypes, suggesting that the expansion was quite recent but before the last glaciation. The next expansion from Beringia probably occurred by means of several long-distance dispersals in the current interglacial, resulting in the colonization of the western Atlantic region by ssp. arctolitoralis. The poor geographic structuring within each subspecies suggests frequent long-distance dispersals from two main Weichselian refugia, one Beringian and one western-central European, but it is possible that the genetic group in Svalbard originates from an additional refugium.
Supporting Information
Figure S1 Summary of structure analyses of Saxifraga rivularis.
As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer-reviewed and may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors.
Filename | Description |
---|---|
JBI_2278_sm_FigureS1.pdf217.2 KB | Supporting info item |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Abbott, R.J. & Brochmann, C. (2003) History and evolution of the arctic flora: in the footsteps of Eric Hultén. Molecular Ecology, 12, 299–313.
- Abbott, R.J. & Comes, H.P. (2003) Evolution in the Arctic: a phylogeographic analysis of the circumarctic plant, Saxifraga oppositifolia (Purple saxifrage). New Phytologist, 161, 211–224.
- Abbott, R.J., Smith, L.C., Milne, R.I., Crawford, R.M.M., Wolff, K. & Balfour, J. (2000) Molecular analysis of plant migration and refugia in the Arctic. Science, 289, 1343–1346.
- Alsos, I.G., Engelskjøn, T., Gielly, L., Taberlet, P. & Brochmann, C. (2005) Impact of ice ages on circumpolar molecular diversity: insights from an ecological key species. Molecular Ecology, 14, 2739–2753.
- Alsos, I.G., Eidesen, P.B., Ehrich, D., Skrede, I., Westergaard, K., Jacobsen, G.H., Landvik, J.Y., Taberlet, P. & Brochmann, C. (2007) Frequent long-distance plant colonization in the changing Arctic. Science, 316, 1606–1609.
- Alsos, I.G., Alm, T., Normand, S. & Brochmann, C. (2008) Past and future range shifts and loss of diversity in dwarf willow (Salix herbacea L.) inferred from genetics, fossils, and modelling. Global Ecology and Biogeography, 35, 801–814.
- Andersen, B.G. & Borns, H.W., Jr (1997) The ice age world. An introduction to Quaternary history and research with emphasis on North America and Northern Europe during the last 2.5 million years. Scandinavian University Press, Oslo.
- Bennike, O. & Böcher, J. (1990) Forest-tundra neighboring the North pole: plant and insect remains from the Plio-Pleistocene Kap København formation, North Greenland. Arctic, 43, 331–338.
- Birks, H.H. (1994) Plant macrofossils and the nunatak theory of per-glacial survival. Dissertationes Botanicae, 234, 129–143.
- Birks, H.H. (2008) The Late-Quaternary history of arctic and alpine plants. Plant Ecology & Diversity, 2, 135–146.
- Birks, H.J.B. & Willis, K.J. (2008) Alpines, trees, and refugia in Europe. Plant Ecology & Diversity, 1, 147–160.
- Bonin, A., Bellemain, E., Eidesen, P.B., Pompanon, F., Brochmann, C. & Taberlet, P. (2004) How to track and assess genotyping errors in population genetics studies. Molecular Ecology, 13, 3261–3273.
- Bonin, A., Ehrich, D. & Manel, S. (2007) Statistical analysis of amplified fragment length polymorphism data: a toolbox for molecular ecologists and evolutionists. Molecular Ecology, 16, 3737–3758.
- Brochmann, C. & Brysting, A.K. (2008) The Arctic – an evolutionary freezer? Plant Ecology and Diversity, 1, 181–195.
- Brochmann, C. & Håpnes, A. (2001) Reproductive strategies in some arctic Saxifraga (Saxifragaceae), with emphasis on the narrow endemic S. svalbardensis and its parental species. Botanical Journal of the Linnean Society, 137, 31–49.
- Brochmann, C., Xiang, Q-Y., Brunsfeld, S.J., Soltis, D.E. & Soltis, P.S. (1998) Molecular evidence for polyploidy origins in Saxifraga (Saxifragaceae): the narrow endemic S. svalbardensis and its widespread allies. American Journal of Botany, 85, 135–143.
- Brochmann, C., Gabrielsen, T.M., Nordal, I., Landvik, J.Y. & Elven, R. (2003) Glacial survival or tabula rasa? The history of North Atlantic biota revisited. Taxon, 52, 417–450.
- Corander, J. & Marttinen, P. (2006) Bayesian identification of admixture events using multilocus molecular markers. Molecular Ecology, 15, 2833–2843.
- DeChaine, E. (2008) A bridge or a barrier? Beringia’s influence on the distribution and diversity of tundra plants. Plant Ecology & Diversity, 1, 197–207.
- Demesure, B., Sodzi, N. & Petit, J. (1995) A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Molecular Ecology, 4, 129–134.
- Doyle, J.J. & Doyle, J.L. (1987) A rapid DNA isolation procedure for small amounts of fresh leaf tissue. Phytochemical Bulletin, 19, 11–15.
- Ehrich, D. (2006) AFLPDAT: a collection of R functions for convenient handling of AFLP data. Molecular Ecology Notes, 6, 603–604.
- Ehrich, D., Alsos, I.G. & Brochmann, C. (2008) Where did the northern peatland species survive the dry glacials: cloudberry (Rubus chamaemorus) as an example. Journal of Biogeography, 35, 801–814.
- Eidesen, P.B., Carlsen, T., Molau, U. & Brochmann, C. (2007a) Repeatedly out of Beringia: Cassiope tetragona embraces the Arctic. Journal of Biogeography, 34, 1559–1574.
- Eidesen, P.B., Alsos, I.G., Popp, M., Stensrud, O., Suda, J. & Brochmann, C. (2007b) Nuclear vs. plastid data: complex Pleistocene history of a circumpolar key species. Molecular Ecology, 16, 3902–3925.
- R. Elven (ed.) (2007 onwards) Checklist of the Panarctic Flora (PAF) Vascular Plants, Version: May 2007. Available at: http://www.binran.ru/infsys/paflist/index.htm.
- Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611–2620.
- Excoffier, L., Smouse, P.E. & Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131, 479–491.
- Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47–50.
- Falush, D., Stephens, M. & Pritchard, J.K. (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes, 7, 574–578.
- Farris, J.S. (1989) The retention index and the rescaled consistency index. Cladistics, 5, 417–419.
- Farris, J.S., Albert, V.A., Källersjö, M., Lipscomb, D. & Kluge, A.G. (1996) Parsimony jackknifing outperforms neighbor-joining. Cladistics, 12, 99–124.
- Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 4, 783–791.
- Frenzel, B., Pécsi, M. & Velichko, A.A. (1992) Atlas of paleoclimates and paleoenvironments of the Northern Hemisphere. Late Pleistocene–Holocene. Geographical Research Institute, Hungarian Academy of Sciences. Gustav Fischer Verlag, Budapest.
- Funder, S., Hjort, C., Landvik, J.Y., Nam, S.I., Reeh, N. & Stein, R. (1998) History of a stable ice margin – Greenland during the Middle and Upper Pleistocene. Quaternary Science Reviews, 17, 77–123.
- Gaudeul, M., Taberlet, P. & Till-Bottraud, I. (2000) Genetic diversity in an endangered alpine plant, Eryngium alpinum L. (Apiaceae), inferred from amplified fragment length polymorphism markers. Molecular Ecology, 9, 1625–1637.
- Goloboff, P., Farris, J. & Nixon, K. (2008) TNT, a free program for phylogenetic analysis. Cladistics, 24, 774–786.
- Guldahl, A.S., Gabrielsen, T.M., Scheen, A.-C., Borgen, L., Steen, S.W., Spjelkavik, S. & Brochmann, C. (2005) The Saxifraga rivularis species complex in Svalbard: molecules, ploidy and morphology. Flora, 200, 207–221.
- Hamilton, M.M. (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Molecular Ecology, 8, 521–523.
- Hopkins, D.M. (1959) Cenozoic history of the Bering Land Bridge. Science, 129, 1519–1528.
- Hultén, E. (1937) Outline of the history of arctic and boreal biota during the Quaternary period. Lehre J. Cramer, New York.
- Hultén, E. (1958) The amphi-Atlantic plants and their phytogeographical connections. Kungliga Svenska Vetenskapsakademiens Handlingar, Fjärde Serien, 8, 1–275.
- Hultén, E. (1968) Flora of Alaska and neighboring territories. A manual of the vascular plants. Stanford University Press, Stanford, CA.
- Jørgensen, M.H., Elven, R., Tribsch, A., Gabrielsen, T.M., Stedje, B. & Brochmann, C. (2006) Taxonomy and evolutionary relationships in the Saxifraga rivularis complex. Systematic Botany, 31, 702–729.
- Kluge, A.G. & Farris, J.S. (1969) Quantitative phyletics and evolution of anurans. Systematic Zoology, 18, 1–32.
- Koerner, R.M. & Fisher, D.A. (2002) Ice-core evidence for widespread Arctic glacier retreat in the Last Interglacial and the early Holocene. Annals of Glaciology, 35, 19–24.
- Kosman, E. (2003) Nei’s gene diversity and the index of average differences are identical measures of diversity within populations. Plant Pathology, 52, 533–535.
- Landvik, J.Y. (1994) The last glaciation of Germania Land and adjacent areas, northeast Greenland. Journal of Quaternary Science, 9, 81–92.
- Landvik, J.Y., Brook, E.J., Gualtieri, L., Raisbeck, G., Salvigsen, O. & Yiou, F. (2003) Northwest Svalbard during the last glaciation: ice-free areas existed. Geology, 31, 905–908.
- Lid, J. & Lid, D.T. (2005). Norsk Flora, 7th edn (ed. by R. Elven) Det Norske Samlaget, Oslo.
- Lipkin, R. & Murray, D.F. (1997) Alaska rare plant field guide. US Department of the Interior, Office of Equal Opportunity, Washington, DC.
- Miller, G.H., Mode, W.N., Wolfe, A.P., Sauer, P.E., Bennike, O., Forman, S.L., Short, S.K. & Stafford, T.W. (1999) Stratified interglacial lacustrine sediments from Baffin Island, Arctic Canada: chronology and palaeoenvironmental implications. Quaternary Science Reviews, 18, 789–810.
- Ottesen, D., Dowdeswell, J.A., Landvik, J.Y. & Mienert, J. (2007) Dynamics of the Late Weichselian ice sheet on Svalbard inferred from high-resolution sea-floor morphology. Boreas, 36, 286–306.
- R Development Core Team (2007) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
- Rohlf, F. (1999) NTSYS-pc. Numerical taxonomy and multivariate analysis system. Exeter Software, New York.
- Rosenberg, N.A., Pritchard, J.K., Weber, J.L., Cann, H.M., Kidd, K.K., Zhivotovsky, L.A. & Feldman, M.W. (2002) Genetic structure of human populations. Science, 298, 2381–2385.
- Rozen, S. & Skaletsky, J. (2000) Primer 3 on the WWW for general users and for biologist programmers. Bioinformatics methods and protocols: methods in molecular biology (ed. by S. Krawetz and S. Misener), pp. 365–386. Humana Press, Totowa, NJ.
- Ryvarden, L. (1975) Studies in seed dispersal II. Winter-dispersed species at Finse, Norway. Norwegian Journal of Botany, 22, 21–24.
- Sang, T., Crawford, D.J. & Stuessy, T.F. (1997) Chloroplast DNA phylogeny, reticulate evolution and biogeography of Paeonia (Paeoniaceae). American Journal of Botany, 84, 1120–1136.
- Savile, D.B.O. (1972) Arctic adaptations in plants. Monograph No. 6. Canada Department of Agriculture, Ottawa.
- Schönswetter, P. & Tribsch, A. (2005) Vicariance and dispersal in the alpine perennial Bupleurum stellatum L. (Apiaceae). Taxon, 54, 725–732.
- Skrede, I., Borgen, L. & Brochmann, C. (2009) Genetic structuring in three closely related circumpolar plant species: AFLP versus microsatellite markers and high-arctic versus arctic–alpine distributions. Heredity, 102, 293–302.
- Soltis, P.S. & Soltis, D.E. (2009) The role of hybridization in plant species. Annual Review of Plant Biology, 60, 561–588.
- Svendsen, J.I., Alexanderson, H., Astakhov, V.I. et al. (2004) Late Quaternary ice sheet history of northern Eurasia. Quaternary Science Reviews, 23, 1229–1271.
- Taberlet, P., Gielly, L., Patou, G. & Bouvet, J. (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology, 17, 1105–1109.
- Tarasov, P.E., Volkova, V.S., Webb, T., Guiot, J., Andreev, A.A., Bezusko, L.G., Bezusko, T.V., Bykova, G.V., Dorofeyuk, N.I., Kvavadze, E.V., Osipova, I.M., Panova, N.K. & Sevastyanov, D.V. (2000) Last glacial maximum biomes reconstructed from pollen and plant macrofossil data from northern Eurasia. Journal of Biogeography, 27, 609–620.
- Van de Peer, Y. & De Wachter, R. (1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Computer Applications in the Biosciences, 10, 569–570.
- Widmer, A. & Lexer, C. (2001) Glacial refugia: sanctuaries for allelic richness, but not for gene diversity. Trends in Ecology and Evolution, 16, 267–269.