Abstract
In order to investigate how episodes of geological and climatic change have influenced the distribution and evolutionary diversification of Arctic to cold temperate-North Atlantic seaweed species, intraspecific genetic variation was analyzed among isolates of the sublittoral, benthic red alga Phycodrys rubens (collected between June 1992 and January 1994). Rooted phylogenetic analyses of nuclear ribosomal DNA internal transcribed spacer (ITS) sequences and the plastid encoded Rubisco spacer sequences suggest that P. rubens invaded the North Atlantic from the Pacific shortly after the opening of the Bering Strait (3 to 3.5 million years ago), colonizing both the western and eastern Atlantic coasts. Based on these data we further hypothesize that P. rubens survived along the European coasts during the more recent Pleistocene glaciations, while becoming locally extinct along the North American Atlantic coasts. Following retraction of the last ice sheet, the western Atlantic coast was colonized a second time from the Pacific. The presence of two distinct genetic types (based on ITS and Rubisco sequences) along the European coasts is postulated to be a result of isolation and subsequent differentiation. This is likely because ice-free areas are known to have existed in northern Scotland and Norway during the last glaciation. The presence of an East Atlantic genetic type along the West Atlantic coast is believed to be a recent introduction (caused by human activity) of P. rubens to Newfoundland.
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Bakker FT, Olsen JL, Stam WT, van den Hoek C (1992) Nuclear ribosomal DNA internal transcribed spacer regions (ITS1 and ITS2) define discrete biogeographic groups in Cladophora albida (Chlorophyta). J Phycol 28:839–845
Bakker FT, Olsen JL, Stam WT (1995) Evolution of rDNA ITS sequences in the Cladophora albida/sericea clade (Chlorophyta) J Molec Evolut 41: in press
Bakker FT, Olsen JL, Stam WT, van den Hoek C (1994) The Cladophora complex (Chlorophyta): new views based on 18S rRNA gene sequences. Molec Phylogenet Evolut 3(4):365–382
Breeman AM (1990) Expected effects of changing seawater temperatures on the geographic distribution of seaweed species. In: Beukema JJ, Wolff WJ, Brouns JJWM (eds) Expected effects of climatic changes on marine coastal ecosystems. Kluwer Academic Publishers, Dordrecht. The Netherlands, pp 55–67
Breeman AM, Pakker H (1994) Temperature ecotypes in seaweeds: adaptive significance and biogeographic implications. Bot mar 37:171–180
Briggs JC (1970) A faunal history of the North Atlantic. Syst Zool 19:19–34
Dawson AG (1992) Ice age earth: late quaternary geology and climate. Routledge, New York
Destombe C, Douglas SE (1991) Rubisco spacer sequence divergence in the rhodophyte alga Gracilaria verrucosa and closely related species. Curr Genet 19:395–398
Devereux J, Haeverli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395
Douglas SE, Dunford DG (1989) The small subunit of the ribulose-1,5-biphosphate carboxylase is plastid encoded in the chlorophyll c-containing alga Cryptomonas ϕ. Pl molec Biol 13:13–20
Dunton K (1992) Arctic biogeography: the paradox of the marine benthic fauna and flora. Trends Ecol Evol 7(6):183–189
Gardes M, White TJ, Fortin JA, Bruns TD, Taylor JW (1991) Identification of indigenous and introduced symbiotic fungi in ectomycorrhizae by amplification of nuclear and mitochondrial ribosomal DNA Can J Bot 69:180–190
Goff LJ, Moon DA, Coleman AW (1994) Molecular delineation of species and species' relationships in the red algal agarophytes Gracilariopsis and Gracilaria (Gracilariales). J Phycol 30:521–537
Gunderson JM, Elwood H, Ingold A, Kindle K, Sogin ML (1987) Phylogenetic relationships between chlorophytes, chrysophytes and oomycetes. Proc natn Acad Sci USA 84:5823–5827
Hillis DM, Huelsenbeck JP (1992) Signal, noise, and reliability in melecular phylogenetic analyses. J Heredity 83:189–195
Holmquist R (1983) Transitions and transversions in evolutionary descent: an approach to understanding. J Molec Evolut 19:134–144
Hong Y-K, Coury DA, Polne-Fuller M, Gibor A (1992) Lithium chloride extraction of DNA from the seaweed Porphyra perforata (Rhodophyta). J Phycol 28:717–720
Kennett JP (1982) Marine Geology. Prentice-Hall, Englewood Cliffs, New Jersey
Kooistra WHCF, Stam WT, Olsen JL, van den Hock C (1992) Biogeography of the green alga Cladophorpsis membranacea (Chlorophyta) based on nuclear rDNA ITS sequences. J Phycol 28:660–668
Kumar S, Tamura K, Nei M (1993) MEGA: molecular evolutionary genetios analysis, version 1.01. The Pennsylvania State University, University Park, Pennsylvania
Lee SB, Taylor JW (1992) Phylogeny of five fungus-like protoctistan Phytophthora species, inferred from the internal transcribed spacers of ribosomal DNA. Molec Biol Evolut 9(4):636–653
Lindstrom SC, South GR (1989) Evidence of species' relationships in the Palmariaceae (Palmariales, Rhodophyta) based on starch gel electrophoresis. Crybiol 1:32–41
Lüning K (1990) Seaweeds. Their environment, biogeography and ecophysiology. John Wiley & Sons, New York
Maggs CA, Douglas SE, Fenety J, Bird CJ (1992) A molecular and morphological analysis of the Gymnogrongus devoniensis (Rhodophyta) complex in the North Atlantic. J Phycol 28:214–232
McDonald JH, Koehn RK (1988) The mussels Mytilus galloprovincialis and M. trossulus on the Pacific coast of North America. Mar Biol 99:111–118
McIntyre A et al. (CLIMAP project members) (1976) The surface of ice-age earth. Science, NY 191:1131–1137
McIntyre A et al. (CLIMAP project members) (1981) Seasonal reconstructions of the earth's surface at the last glacial maxima. Geol Soc Am Map Chart Ser MC-36, Boulder, Colorado
Novaczek I, Lubbers GW, Breeman AM (1990) Thermal ecotypes of amphi-Atlantic algae. I. Algae of Arctic to cold-temperate distribution (Chaetomorpha melagonium, Devaleraea ramentacea and Phycodrys rubens). Helgoländer Meeresunters 44:459–474
Ochman H, Wilson AC (1987) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Molec Evolut 26:74–86
O'Donnell K (1992) Ribosomal DNA internal transcribed spacers are highly divergent in the phytopathogenic ascomycete Fusarium sambucinum (Giberella pulicaris). Curr Genet 22:213–220
Olsen JL, Stam WT, Berger S, Menzel D (1994) 18S rDNA evolution in the Dasycladales (Chlorophyta): modern living fossils. J Phycol 30:729–744
Palumbi SR, Kessing BD (1991) Population biology of the trans-Arctic exchange: MtDNA sequence similarity between Pacific and Atlantic sea urchins. Evolution 45(8):1790–1805
Pleyte KA, Duncan SD, Phillips RB (1992) Evolutionary relationships of the salmonis fish genus Salvelinus inferred from DNA sequences of the first internal transcribed spacer (ITS1) of ribosomal DNA. Molec Phylogenet Evolut 1(3):223–230
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molec Biol Evolut 4:406–425
Sambrook J, Fritch EF, Maniatis T (1989) Molecular Cloning: A laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York
Saunders GW, Druehi LD (1993) Nucleotide sequences of the internal transcribed spacers and 5.8S rRNA genes from Alaria marginata and Postelsia palmaeformis (Phaeophyta: Laminariales). Mar Biol 115:347–352
Savard L, Michaud M, Bousquet J (1993) Genetic diversity and phylogenetic relationships between birches and alders using ITS, 18 S rRNA, and rbcL gene sequences. Molec Phylogenet Evolut 2(2):112–118
Scagel RF, Gabrielson PW, Garbary DJ, Golden L, Hawkes MW. Lindstrom SC, Oliviera JC, Widdowson TB (1993) A synopsis of the benthic marine algae of British Columbia, Southeast Alaska, Washington and Oregon. Univ of British Columbia Press, Vancouver
Schlötterer C, Hauser M-T, von Haeseler A, Tautz D (1994) Comparative evolutionary analysis of rDNA ITS regions in Drosophila. Molec Biol Evolut 11(3):513–522
Stam WT, Bot PVM, Boele-Bos SA, van Rooij JM, van den Hoek C (1988) Single-copy DNA-DNA hybridizations among five species of Laminaria (Phaeophyceae): phylogenetic and biogeographic implications. Helgoländer Meeresunters 42:251–267
Sutherland DG (1984) The quaternary deposits and landforms of Scotland and the neighbouring shelves: a review. Q Sci Rev 3:157–254
Swofford DL (1993) PAUP: phylogenetic analysis using parsimony, Version 3.1. Laboratory of Molecular Systematics, Smithsonian Institute. Washington DC
Tajima F, Nei M (1984) Estimation of evolutionary distance between nucleotide sequences. Molec Biol Evolut 1(3):269–285
Tautz D, Hancock JM, Webb DA, Tautz C, Dover GA (1988) Drosophila melanogaster. Molec Biol Evolut 5:366–376
Torres RA, Ganal M, Hemleben V (1990) GC balance in the internal transcribed spacers ITS1 and ITS2 of nuclear ribosomal RNA genes. J Molec Evolut 30:170–181
Valentin K, Zetsche K (1990) Rubisco genes indicate a close phylogenetic relation between the plastids of Chromophyta and Rhodophyta. Pl Molec Biol 15:575–584
van den Hoek C, Breeman AM (1990) Seaweed biogeography of the North Atlantic: Where are we now? In: Garbary DJ, South GR (eds) Evolutionary biogeography of marine algae in the North Atlantic. NATO ASI Ser G22. Springer Verlag, New York, pp 55–87
van Oppen MJH, Diekmann OE, Wiencke C, Stam WT, Olsen JL (1994) Tracking dispersal routes: phylogeography of the Arctic-Antarctic disjunct seaweed Acrosiphonia arcta (Chlorophyta). J Phycol 30:67–80
van Oppen MJH, Olsen JL, Stam WT, van den Hoek C, Wiencke C (1993) Arctic-Antarctic disjunctions in the benthic seaweeds Acrosiphonia arcta (Chlorophyta) and Desmarestia viridis/willii (Phaeophyta) are of recent origin. Mar Biol 115:381–386
Vermeij GJ (1991a) Anatomy of an invasion: the trans-Arctic interchange. Paleobiology 17(3):281–307
vermeij GJ (1991b) When biotas meet: understanding biotic interchange. Science, NY 253:1099–1104
Vorren TO, Vorren K-D, Alm T, Gulliksen S, Lovlie R (1988) The last deglaciation (20000 to 11000 BP) on Andoya, northern Norway. Boreas 17:41–77
Wesson DM, Porter CH, Collins FH, (1992) Sequence and secondary structure comparisons of ITS rDNA in mosquitoes (Diptera: Cilicidae). Mol Phyl Evol 1(4):253–269
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols. A guide to methods and applications. Academic Press, Inc., San Diego, California, pp 315–322
Wynne MJ (1970) Marine algae of Amchitka Island (Aleutian islands). I. Delesseriaceae. Syesis 3:95–144
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Communicated by O. Kinne, Oldendorf/Luhe
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van Oppen, M.J.H., Draisma, S.G.A., Olsen, J.L. et al. Multiple trans-Arctic passages in the red alga Phycodrys rubens: evidence from nuclear rDNA ITS sequences. Marine Biology 123, 179–188 (1995). https://doi.org/10.1007/BF00350338
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DOI: https://doi.org/10.1007/BF00350338