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Trans-Pacific and trans-Arctic pathways of the intertidal macroalga Fucus distichus L. reveal multiple glacial refugia and colonizations from the North Pacific to the North Atlantic

2010; Wiley; Volume: 38; Issue: 4 Linguagem: Inglês

10.1111/j.1365-2699.2010.02437.x

1365-2699

James A. Coyer, Galice Hoarau, Jaap van Schaik, Pepijn Luijckx, Jørn Olsen,

Marine Biology and Ecology Research

Journal of BiogeographyVolume 38, Issue 4 p. 756-771 ORIGINAL ARTICLES Trans-Pacific and trans-Arctic pathways of the intertidal macroalga Fucus distichus L. reveal multiple glacial refugia and colonizations from the North Pacific to the North Atlantic James A. Coyer, Corresponding Author James A. Coyer Department of Marine Benthic Ecology and Evolution, Center for Ecological and Evolutionary Studies, University of Groningen, Centre for Life Sciences, Nijenborgh 7, 9747 AG Groningen, The Netherlands James A. Coyer, Department of Marine Benthic Ecology and Evolution, CEES, University of Groningen, Centre for Life Sciences, Nijenborgh 7, 9747 AG Groningen, The Netherlands.E-mail: [email protected]Search for more papers by this authorGalice Hoarau, Galice Hoarau Marine Ecology Group, Faculty of Biosciences and Aquaculture, Hogskølen I Bodø, 8049 Bodø, NorwaySearch for more papers by this authorJaap Van Schaik, Jaap Van Schaik Department of Marine Benthic Ecology and Evolution, Center for Ecological and Evolutionary Studies, University of Groningen, Centre for Life Sciences, Nijenborgh 7, 9747 AG Groningen, The NetherlandsSearch for more papers by this authorPepijn Luijckx, Pepijn Luijckx Department of Marine Benthic Ecology and Evolution, Center for Ecological and Evolutionary Studies, University of Groningen, Centre for Life Sciences, Nijenborgh 7, 9747 AG Groningen, The Netherlands Universität Basel, Zoologisches Institut Evolutionsbiologie, Vesalgasse 1 CH-4051 Basel, SwitzerlandSearch for more papers by this authorJeanine L. Olsen, Jeanine L. Olsen Department of Marine Benthic Ecology and Evolution, Center for Ecological and Evolutionary Studies, University of Groningen, Centre for Life Sciences, Nijenborgh 7, 9747 AG Groningen, The NetherlandsSearch for more papers by this author James A. Coyer, Corresponding Author James A. Coyer Department of Marine Benthic Ecology and Evolution, Center for Ecological and Evolutionary Studies, University of Groningen, Centre for Life Sciences, Nijenborgh 7, 9747 AG Groningen, The Netherlands James A. Coyer, Department of Marine Benthic Ecology and Evolution, CEES, University of Groningen, Centre for Life Sciences, Nijenborgh 7, 9747 AG Groningen, The Netherlands.E-mail: [email protected]Search for more papers by this authorGalice Hoarau, Galice Hoarau Marine Ecology Group, Faculty of Biosciences and Aquaculture, Hogskølen I Bodø, 8049 Bodø, NorwaySearch for more papers by this authorJaap Van Schaik, Jaap Van Schaik Department of Marine Benthic Ecology and Evolution, Center for Ecological and Evolutionary Studies, University of Groningen, Centre for Life Sciences, Nijenborgh 7, 9747 AG Groningen, The NetherlandsSearch for more papers by this authorPepijn Luijckx, Pepijn Luijckx Department of Marine Benthic Ecology and Evolution, Center for Ecological and Evolutionary Studies, University of Groningen, Centre for Life Sciences, Nijenborgh 7, 9747 AG Groningen, The Netherlands Universität Basel, Zoologisches Institut Evolutionsbiologie, Vesalgasse 1 CH-4051 Basel, SwitzerlandSearch for more papers by this authorJeanine L. Olsen, Jeanine L. Olsen Department of Marine Benthic Ecology and Evolution, Center for Ecological and Evolutionary Studies, University of Groningen, Centre for Life Sciences, Nijenborgh 7, 9747 AG Groningen, The NetherlandsSearch for more papers by this author First published: 03 December 2010 https://doi.org/10.1111/j.1365-2699.2010.02437.xCitations: 54Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstract Aim We examined the phylogeography of the cold-temperate macroalgal species Fucus distichus L., a key foundation species in rocky intertidal shores and the only Fucus species to occur naturally in both the North Pacific and the North Atlantic. Location North Pacific and North Atlantic oceans (42° to 77° N). Methods We genotyped individuals from 23 populations for a mitochondrial DNA (mtDNA) intergenic spacer (IGS) (n = 608) and the cytochrome c oxidase subunit I (COI) region (n = 276), as well as for six nuclear microsatellite loci (n = 592). Phylogeographic structure and connectivity were assessed using population genetic and phylogenetic network analyses. Results IGS mtDNA haplotype diversity was highest in the North Pacific, and divergence between Pacific haplotypes was much older than that of the single cluster of Atlantic haplotypes. Two ancestral Pacific IGS/COI clusters led to a widespread Atlantic cluster. High mtDNA and microsatellite diversities were observed in Prince William Sound, Alaska, 11 years after severe disturbance by the 1989 Exxon Valdez oil spill. Main conclusions At least two colonizations occurred from the older North Pacific populations to the North Atlantic between the opening of the Bering Strait and the onset of the Last Glacial Maximum. One colonization event was from the Japanese Archipelago/eastern Aleutians, and a second was from the Alaskan mainland around the Gulf of Alaska. Japanese populations probably arose from a single recolonization event from the eastern Aleutian Islands before the North Pacific–North Atlantic colonization. In the North Atlantic, the Last Glacial Maximum forced the species into at least two known glacial refugia: the Nova Scotia/Newfoundland (Canada) region and Andøya (northern Norway). The presence of two private haplotypes in the central Atlantic suggests the possibility of colonization from other refugia that are now too warm to support F. distichus. With the continuing decline in Arctic ice cover as a result of global climate change, renewed contact between North Pacific and North Atlantic populations of Fucus species is expected. Supporting Information Appendix S1 Locations of study sites. 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_2437_sm_AppS1.doc47 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 Addison, J.A. & Hart, M.W. (2005) Colonization, dispersal, and hybridization influence phylogeography of North Atlantic sea urchins (Strongylocentrotus droebachiensis). Evolution, 59, 532–543. Adey, W.H. & Hayek, L.-A.C. (2005) The biogeographic structure of the western North Atlantic rocky intertidal. Cryptogamie Algologie, 26, 35–66. Ægisdóttir, H.H. & Þórhallsdóttir, E. (2005) Theories on migration and history of the North-Atlantic flora: a review. Jökull, 54, 1–16. Alm, T. & Birks, H.H. (1991) Late Weichselian flora and vegetation of Andøya, northern Norway – macrofossil (seed and fruit). Evidence from the Nedre Aerasvatn. Nordic Journal of Botany, 11, 465–476. Anderson, L.J., Hu, F.S., Nelson, D.M., Petit, R.J. & Paige, K.N. (2006) Ice-age endurance: DNA evidence of a white spruce refugium in Alaska. Proceedings of the National Academy of Sciences USA, 103, 12447–12450. Arrontes, J. (1993) Nature of the distributional boundary of Fucus serratus on the north shore of Spain. Marine Ecology Progress Series, 93, 183–193. Avise, J.C. (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, MA. Barriel, V. (1994) Molecular phylogenies and nucleotide insertion-deletion. Comptes Rendus de l'Academie des Sciences, Paris, 317, 693–701. Belkhir, K., Borsa, P., Goudet, J., Chikhi, L. & Bonhomme, F. (2001) GENETIX, logiciel sous Windows™ pour la genetique des populations. Laboratoire Genome et populations, Montpellier, France. Bennett, K.D. & Provan, J. (2008) What do we mean by 'refugia'? Quaternary Science Reviews, 27, 2449–2455. Benzécri, J.P. (1973) L'analyse des données: T. 2, I'analyse des correspondances. Dunod, Paris. Berndt, M.L., Callow, J.A. & Brawley, S. (2002) Gamete concentrations and timing and success of fertilization in a rocky shore seaweed. Marine Ecology Progress Series, 226, 273–285. Bigg, G.R., Cunningham, C.W., Ottersen, G., Pogson, G.H., Wadley, M.R. & Williamson, P. (2008) Ice-age survival of Atlantic cod: agreement between palaeoecology models and genetics. Proceedings of the Royal Society B: Biological Sciences, 275, 163–172. Bradwell, T., Stoker, M.S., Golledge, N.R., Wilson, C.K., Merritt, J.W., Long, D., Everest, J.D., Hestvik, O.B., Stevenson, A.G., Hubbard, A.L., Finlayson, A.G. & Mathers, H.E. (2008) The northern sector of the last British Ice Sheet: maximum extent and demise. Earth-Science Reviews, 88, 207–226. Brawley, S., Coyer, J.A., Blakeslee, A.M.H., Hoarau, G., Johnson, L.E., Byers, J.E., Stam, W.T. & Olsen, J.L. (2009) Historical invasions of the intertidal zone of Atlantic North America associated with distinctive patterns of trade and emigration. Proceedings of the National Academy of Sciences USA, 106, 8239–8244. Briggs, J.C. (2003) Marine centres of origin as evolutionary engines. Journal of Biogeography, 30, 1–18. Brunhoff, C., Yoccoz, N.G., Ims, R.A. & Jaarola, M. (2006) Glacial survival or late glacial colonization? Phylogeography of the root vole (Microtus oeconomus) in north-west Norway. Journal of Biogeography, 33, 2136–2144. Cavalli-Sforza, L.L. & Edwards, A.W.F. (1967) Phylogenetic analysis: models and estimation procedures. American Journal of Human Genetics, 19, 233–257. Chapman, A.R.O. (1995) Functional ecology of fucoid algae: twenty-three years of progress. Phycologia, 34, 1–32. Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1659. Coleman, M.A. & Brawley, S.H. (2005) Are life history characteristics good predictors of genetic diversity and structure? A case study of the intertidal alga Fucus spiralis (Heterokontophyta; Phaeophyceae). Journal of Phycology, 41, 753–762. Coyer, J.A., Peters, A.F., Hoarau, G., Stam, W.T. & Olsen, J.L. (2002a) Inheritance patterns of ITS1, chloroplasts, and mitochondria in artificial hybrids of the marine rockweeds, Fucus serratus and F. evanescens (Heterokontophyta; Fucaceae). European Journal of Phycology, 37, 173–178. Coyer, J.A., Veldsink, J.H., Stam, W.T. & Olsen, J.L. (2002b) Characterization of microsatellite loci in the marine rockweeds, Fucus serratus and F. evanescens (Heterokontophyta; Fucaceae). Molecular Ecology Notes, 2, 35–37. Coyer, J.A., Peters, A.F., Stam, W.T. & Olsen, J.L. (2003) Post-Ice Age recolonization and differentiation of Fucus serratus L. (Fucaceae: Phaeophyta) populations in Northern Europe. Molecular Ecology, 12, 1817–1829. Coyer, J.A., Hoarau, G., Oudot-Le Secq, M.-P., Stam, W.T. & Olsen, J.L. (2006a) A mtDNA-based phylogeny of the brown algal genus Fucus (Heterokontophyta; Phaeophyta). Molecular Phylogenetics and Evolution, 39, 209–222. Coyer, J.A., Hoarau, G., Skage, M., Stam, W.T. & Olsen, J.L. (2006b) Origin of Fucus serratus (Heterokontophyta; Fucaceae) populations on Iceland and the Faroes: a microsatellite-based assessment. European Journal of Phycology, 41, 235–246. Coyer, J.A., Hoarau, G., Beszerti, B., Pearson, G. & Olsen, J.L. (2009) Expressed sequence tag derived polymorphic SSR markers for Fucus serratus and amplification in other species of Fucus. Molecular Ecology Resources, 9, 168–170. Cunningham, C.W. & Collins, T.M. (1998) Beyond area relationships: extinction and recolonization in molecular marine biogeography. Molecular approaches to ecology and evolution (ed. by R. DeSale and B. Schierwater), pp. 297–321. Birkhäuser, Basel. Dahlgren, T.G., Weinberg, J.R. & Halanych, K.M. (2000) Phylogeography of the ocean quahog (Arctica islandica): influences of paleoclimate on genetic diversity and species range. Marine Biology, 137, 487–495. Davies, N., Villablanca, F.X. & Roderick, G.K. (1999) Determining the source of newly founded populations: multilocus genotyping in nonequilibrium population genetics. Trends in Ecology and Evolution, 14, 17–21. Dodson, J.J., Tremblay, S., Colombani, F., Carscadden, J.E. & Leconte, F. (2007) Trans-Arctic dispersal and the evolution of a circumpolar marine fish species complex, the capellin (Mallotus villosus). Molecular Ecology, 16, 5030–5043. Dudgeon, S., Kübler, J.E., Wright, W.A., Vadas, R.L. & Petraitis, P.S. (2001) Natural variability in zygote dispersal of Ascophyllum nodosum at small spatial scales. Functional Ecology, 15, 595–604. Ebbesmeyer, C.C. & Ingraham, W.J., Jr (1994) Pacific toy spill fuels ocean current pathways research. EOS, Transactions, American Geophysical Union, 75, 425. Engel, C.R., Brawley, S., Edwards, K.J. & Serrão, E. (2003) Isolation and cross-species amplification of microsatellite loci from the fucoid seaweeds Fucus vesiculosus, F. serratus, and Ascophyllum nodosum (Heterokontophyta, Fucaceae). Molecular Ecology Notes, 3, 180–182. Engel, C.R., Daguin, C. & Serrão, E. (2005) Genetic entities and mating system in hermaphroditic Fucus spiralis and its close dioecious relative F. vesiculosus (Fucaceae, Phaeophyceae). Molecular Ecology, 14, 2033–2046. Excoffier, L., Laval, G. & Schneider, S. (2005) ARLEQUIN vers. 3.0: an integrated software package for population genetics data analysis. Evolutionary bioinformatics Online, 1, 47–50. Fedorov, V.B. & Stenseth, N.C. (2001) Glacial survival of the Norwegian lemming (Lemmus lemmus) in Scandinavia: inference from the mitochondrial DNA variation. Proceedings of the Royal Society B: Biological Sciences, 268, 809–814. Felsenstein, J. (1994) PHYLIP (Phylogeny inference package). Department of Genetics, University of Washington, Seattle, WA. Fraser, C.I., Nikula, R., Spencer, H.G. & Waters, J.M. (2009) Kelp genes reveal the extent of subantarctic sea ice during the Last Glacial Maximum. Proceedings of the National Academy of Sciences USA, 106, 3249–3253. 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 Science, Budapest. Gladenkov, A.Y., Oleinik, A.E., Marincovich, L.J. & Barinov, K.B. (2002) A refined age for the earliest opening of the Bering Strait. Palaeogeography, Palaeoclimatology, Palaeoecology, 183, 321–328. Govindarajan, A.F., Halanych, K.M. & Cunningham, C.W. (2005) Mitochondrial evolution and phylogeography in the hydrozoan Obelia geniculata (Cnidaria). Marine Biology, 146, 213–222. Håkansson, L., Briner, J., Alexanderson, H., Aldahan, A. & Possnert, G. (2007) 10Be ages from central east Greenland constrain the extent of the Greenland ice sheet during the Last Glacial Maximum. Quaternary Science Reviews, 26, 2316–2321. Hayashi, K. (1991) PCR-SSCP: a simple and sensitive method for detection of mutations in the genomic DNA. Genome Research, 1, 34–38. Hewitt, G.M. (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society B: Biological Sciences, 359, 183–195. Hickerson, M.J. & Cunningham, C.W. (2005) Contrasting Quaternary histories in an ecologically divergent sister pair of flow-dispersing intertidal fish (Xiphister) revealed by multilocus DNA analysis. Evolution, 59, 344–360. Hoarau, G., Coyer, J.A., Veldsink, J.H., Stam, W.T. & Olsen, J.L. (2007a) Glacial refugia and recolonization patterns in the brown seaweed Fucus serratus. Molecular Ecology, 16, 3606–3616. Hoarau, G., Coyer, J.A., Stam, W.T. & Olsen, J.L. (2007b) A fast and inexpensive DNA extraction/purification method for brown macroalgae. Molecular Ecology Notes, 7, 191–193. Hommersand, M.H., Fredericq, S., Freshwater, D.W. & Hughey, J. (1999) Recent developments in the systematics of the Gigartinaceae (Gigartinales, Rhodophyta) based on rbcL sequence analysis and morphological evidence. Phycological Research, 47, 139–151. Hultén, E. (1962) The circumpolar plants. I. Vascular cryptograms, conifers, monocotyledons Kungilga Svenska Vetenskapsakademiens Handlingar. Fjärde Serien, 8, 1–275. Ingólfsson, A. (2009) A marine refugium in Iceland during the last glacial maximum: fact or fiction? Zoological Scripta, 38, 663–665. Jacobs, D.K., Haney, T.A. & Louie, K.D. (2004) Genes, diversity, and geologic processes on the Pacific coast. Annual Review of Earth and Planetary Sciences, 32, 601–652. Jaramillo-Correa, J.P., Beaulieu, J. & Bousquet, J. (2004) Variation in mitrochondrial DNA reveals multiple distant glacial refugia in black spruce (Picea mariana), a transcontinental North American conifer. Molecular Ecology, 13, 2735–2747. Jenkyns, H.C., Forster, A., Schouten, S. & Sinninghe Damsté, J.S. (2004) High temperatures in the Late Cretaceous Arctic Ocean. Nature, 432, 888–892. Jørstad, K.E. (2004) Evidence for two highly differentiated herring groups at Goose Bank in the Barents Sea and the genetic relationship to Pacific herring, Clupea pallasi. Environmental Biology of Fishes, 69, 211–221. Kalinowski, S.T. (2004) Hp-rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes, 5, 187–189. Kelly, D.W., Macisaac, H.J., Heath, D.D. & Crandall, K. (2009) Vicariance and dispersal effects on phylogeographic structure and speciation in a widespread estuarine invertebrate. Evolution, 60, 257–267. Kucera, H. & Saunders, G.W. (2008) Assigning morphological variants of Fucus (Fucales, Phaeophyceae) in Canadian waters to recognized species using DNA barcoding. Botany, 86, 1065–1079. Lawver, L.A., Müller, R.D., Srivastava, S.P. & Roest, W. (1990) The opening of the Arctic Ocean. Geological history of the polar oceans: Arctic vs. Antarctic (ed. by U. Bliel and J. Thiede), pp. 29–62. Kluwer Academic, Dordrecht. Lindstrom, S.C. (2001) The Bering Strait connection: dispersal and speciation in boreal macroalgae. Journal of Biogeography, 28, 243–251. Lüning, K. (1990) Seaweeds: their environment, biogeography and ecophysiology. John Wiley, New York. Lüning, K. & tom Dieck, I. (1990) The distribution and evolution of the Laminariales: North Pacific–Atlantic relationships. Evolutionary biogeography of the marine algae of the North Atlantic (ed. by D.J. Garbary and G.R. South), pp. 187–204. Springer-Verlag, Berlin. Luttikhuizen, P.C., Drent, J. & Baker, A.J. (2003) Disjunct distribution of highly diverged mitochondrial lineage clade and population subdivision in a marine bivalve with pelagic larval dispersal. Molecular Ecology, 12, 2215–2229. Maggs, C.A., Castilho, R., Foltz, D.W., Henzler, C., Jolly, M.T., Kelly, J., Olsen, J.L., Perez, K.E., Stam, W.T., Vainola, R., Viard, F. & Wares, J.P. (2008) Evaluating signatures of glacial refugia for north Atlantic benthic marine taxa. Ecology, 89, S108–S122. Mallet, J. (2005) Hybridization as an invasion of the genome. Trends in Ecology and Evolution, 20, 229–237. Marincovich, L.J. & Gladenkov, A.Y. (1999) Evidence for an early opening of the Bering Strait. Nature, 397, 149–151. Marincovich, L.J., Brouwers, E.M., Hopkins, D.M. & Mckenna, M.C. (1990) Late Mesozoic and Cenozoic paleogeographic and paleoclimatic history of the Arctic Ocean basin, based on shallow-water marine faunas and terrestrial vertebrates. The Arctic Ocean region: the geology of North America (ed. by A. Grantz, L. Johson and F. Sweeny), pp. 403–426. Geological Society of America, Boulder, CO. Marko, P.B., Hoffman, J.M., Emme, S.A., Mcgovern, T.M., Keever, C.C. & Cox, L.C. (2010) The 'Expansion–Contraction' model of Pleistocene biogeography: rocky shores suffer a sea change? Molecular Ecology, 19, 146–169. Nei, M. (1987) Molecular evolutionary genetics. Columbia University Press, New York. Nikula, R., Strelkov, P. & Väinölä, R. (2007) Diversity and trans-Arctic invasion history of mitochondrial lineages in the North Atlantic Macoma balthica complex (Bivalvia: Tellinidae). Evolution, 61, 928–941. Norðdahl, H., Ingólfsson, Ó., Pétursson, H.G. & Hallsdóttir, M. (2008) Late Weichselian and Holocene environmental history of Iceland. Jökull, 58, 343–364. Norton, T.A. (1992) Dispersal by macroalgae. British Phycological Journal, 27, 293–301. Olsen, J.L., Stam, W.T., Coyer, J.A., Reusch, T.B.H., Billingham, M., Boström, C., Calvert, E., Christie, H., Granger, S., La Lumière, R., Milchakova, N., Oudot-Le Secq, M.-P., Procaccini, G.A., Sanjabi, B., Serrão, E., Veldsink, J.H., Widdicombe, S. & Wyllie-Echeverria, S. (2004) North Atlantic phylogeography and large-scale population differentiation of the seagrass Zostera marina L. Molecular Ecology, 13, 1923–1941. Olsen, J.L., Zechman, F.W., Hoarau, G., Coyer, J.A., Stam, W.T., Valero, M. & Åberg, P. (2010) The phylogeographic architecture of the fucoid seaweed Ascophyllum nodosum: an intertidal 'marine tree' and survivor of more than one glacial–interglacial cycle. Journal of Biogeography, 37, 842–856. van Oppen, M.J.H., Draisma, S.G.A., Olsen, J.L. & Stam, W.T. (1995) Multiple trans-Arctic passages in the red alga Phycodrys rubens: evidence from nuclear rDNA ITS sequences. Marine Biology, 123, 179–183. Orita, M., Iwahana, H., Kanazawa, H., Hayashi, K. & Sekiya, T. (1989) Detection of polymorphisms of human DNA by gel electrophoresis as single-strand conformation polymorphisms. Proceedings of the National Academy of Sciences USA, 86, 2766–2770. Orti, G., Bell, M.A., Reimchen, T.E. & Meyer, A. (1994) Global survey of mitochondrial-DNA sequences in the threespine stickleback – evidence for recent migrations. Evolution, 48, 608–622. Oudot-Le Secq, M.-P., Fontaine, J.-M., Rousvoal, S., Kloareg, B. & Loiseaux-De Goër, S. (2001) The complete sequence of a brown algal mitochondrial genome, the ectocarpale Pylaiella littoralis (L.) Kjellm. Journal of Molecular Evolution, 53, 80–88. Paine, R.T., Ruesink, J.L., Sun, A., Soulanille, E.L., Wonham, M.J., Harley, C.D.G., Brumbaugh, D. & Secord, D.L. (1996) Trouble on oiled waters: lessons from the Exxon Valdez oil spill. Annual Review of Ecology and Systematics, 27, 197–235. Palumbi, S.R. & Kessing, B.D. (1991) Population biology of the trans-Arctic exchange: mtDNA sequence similarity between Pacific and Atlantic sea urchins. Evolution, 45, 1790–1805. Pearson, G. & Brawley, S. (1996) Reproductive ecology of Fucus distichus (Phaeophyceae): an intertidal alga with successful external fertilization. Marine Ecology Progress Series, 143, 211–223. Pereyra, R.T., Bergström, L., Kautsky, L. & Johannesson, K. (2009) Rapid speciation in a newly opened postglacial marine environment, the Baltic Sea. BMC Evolutionary Biology, 9, 70. Perovich, D.K. & Richter-Menge, J.A. (2009) Loss of sea ice in the Arctic. Annual Review of Marine Science, 1, 417–441. Peterson, C.H., Rice, S.D., Short, J.W., Esler, D., Bodkin, J.L., Ballachey, B.E. & Irons, D.B. (2003) Long-term ecosystem response to the Exxon Valdez oil spill. Science, 302, 2082–2086. Pielou, E.C. (1991) After the Ice Age: the return of life to glaciated North America. University of Chicago Press, Chicago. Posada, D. & Crandall, K.A. (1998) ModelTest: testing the model of DNA substitution. Bioinformatics, 14, 817–818. Provan, J. & Bennett, K.D. (2008) Phylogeographic insights into cryptic glacial refugia. Trends in Ecology and Evolution, 23, 564–571. Ravson, P.D. & Harper, F.M. (2009) Colonization of the northwest Atlantic by the blue mussel, Mytilus trossulus postdates the last glacial maximum. Marine Biology, 156, 1857–1868. Rawson, P.D. & Hilbish, T.J. (1995) Evolutionary relationships among the male and female mitochondrial DNA lineages in the Mytilus edulis species complex. Molecular Biology and Evolution, 12, 893–901. Rice, W.R. (1989) Analyzing tables of statistical tests. Evolution, 43, 223–225. Roberts, S.J., Sigurvinsson, J.R., Westgate, J.A. & Sandhu, A. (2007) Late Pliocene glaciation and landscape evolution of Vestfirðir, Northwest Iceland. Quaternary Science Reviews, 26, 243–263. Saillard, J., Forster, P., Lynnerup, N., Bandelt, H.-J. & Nøberg, S. (2000) MtDNA variation among Greenland Eskimos: the edge of the Beringian expansion. American Journal of Human Genetics, 67, 718–726. Schneider, S., Roessli, D. & Excoffier, L. (2000) Arlequin ver. 2.000: a software for population genetic data analysis. Genetics and Biometry Laboratory. University of Geneva, Switzerland. Serrão, E.A., Kautsky, L., Lifvergren, T. & Brawley, S. (1997) Gamete dispersal and pre-recruitment mortality in Baltic Fucus vesiculosus. Phycologia Supplement, 36, 101–102. Serrão, E.A., Alice, L.A. & Brawley, S.H. (1999) Evolution of the Fucaceae (Phaeophyceae) inferred from nrDNA-ITS. Journal of Phycology, 35, 382–394. Shaw, J. (2006) Palaeogeography of Atlantic Canadian continental shelves from the last glacial maximum to the present, with an emphasis on Flemish Cap. Journal of Northwest Atlantic Fishery Science, 37, 119–126. Shaw, J., Piper, D.J.W., Fader, G.B.J., King, E.L., Todd, B.J., Bell, T., Batterson, M.J. & Liverman, D.G.E. (2006) A conceptual model of the deglaciation of Atlantic Canada. Quaternary Science Reviews, 25, 2059–2081. She, X., Autem, M., Kotulas, G., Pasteur, N. & Bonhomme, F. (1987) Multivariate analysis of genetic exchanges between Solea aegyptiaca and Solea senegalensis (Teleosts, Soleidae). Biological Journal of the Linnean Society, 32, 357–371. Slanina, S. (2010) Glaciers and ice sheets in the Arctic. Encyclopedia of earth (ed. by C.J. Cleveland). National Council for Science and the Environment, Washington, DC. Available at: http://www.eoearth.org/article/Glaciers_and_ice_sheets_in_the_Arctic. Solem, J.O. & Alm, T. (1994) Southwards migration of freshwater invertebrates from northern Norway. Fauna Norvegica Series A, 15, 9–18. Stewart, J.R., Lister, A.M., Barnes, I. & Dalén, L. (2010) Refugia revisited: individualistic responses of species in space and time. Proceedings of the Royal Society B: Biological Sciences, 277, 661–671. Stroeve, J., Holland, M.M., Meier, W., Scambos, T. & Terreze, M. (2007) Arctic sea ice decline: faster than forecast. Geophysical Research Letters, 34, L09501. Svitoch, A.A. & Taldenkova, E.E. (1994) Recent history of the Bering Strait. Oceanology, 34, 400–411 (in Russian). Swofford, D.L. (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods) 4.0 Beta. Sinauer, Sunderland, MA. Thiel, M. & Gutow, L. (2005) The ecology of rafting in the marine environment. I. The floating substrata. Oceanography and Marine Biology Annual Review, 42, 181–263. Tsukada, M. (1982) Cryptomeria japonica: glacial refugia and late-glacial and postglacial migration. Ecology, 63, 1091–1105. Väinölä, R. (2003) Repeated trans-Arctic invasions in littoral bivalves: molecular zoogeography of the Macoma balthica complex. Marine Biology, 143, 935–946. Varvio, S.L., Koehn, R.K. & Väinölä, R. (1988) Evolutionary genetics of the Mytilus edulis complex in the North Atlantic region. Marine Biology, 98, 51–60. Vermeij, G.J. (1991) Anatomy of an invasion: the trans-Arctic exchange. Paleobiology, 17, 281–307. Vermeij, G.J. & Roopnarine, P.D. (2008) The coming Arctic invasion. Science, 321, 780–781. Walter, R. & Epperson, B.K. (2005) Geographic pattern of genetic diversity in Pinus resinosa: contact zone between descendants of glacial refugia. American Journal of Botany, 92, 92–100. Wares, J.P. (2001) Intraspecific variation and geographic isolation in Idothea balthica (Isopoda: Valvifera). Journal of Crustacean Biology, 21, 1007–1013. Wares, J.P. & Cunningham, C.W. (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution, 55, 2455–2469. Young, A.M., Torres, C., Mack, J.E. & Cunningham, C.W. (2002) Morphological and genetic evidence for vicariance and refugium in Atlantic and Gulf of Mexico populations of the hermit crab (Pagurus longicarpus). Marine Biology, 140, 1059–1066. Citing Literature Volume38, Issue4April 2011Pages 756-771 ReferencesRelatedInformation