Patterns of Post-Glacial Genetic Differentiation in Marginal Populations of a Marine Microalga

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Tahvanainen, Pia ^a,b   Alpermann, Tilman J ^c,d   Figueroa, Rosa Isabel ^e,f   John, Uwe ^g   Hakanen, Päivi ^a   Nagai, Satoshi ^h   Blomster, Jaanika ^b   Kremp, Anke ^a  

^a FINNISH ENVIRONMENT INSTITUTE   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c BIODIVERSITY AND CLIMATE RESEARCH CENTRE BIK F   (Germany)

^d SENCKENBERG RESEARCH INSTITUTE   (Germany)

^e LUND UNIVERSITY   (Sweden)

^f INSTITUTO ESPAÑOL DE OCEANOGRAFÍA   (Spain)

^g ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^h FISHERIES RESEARCH AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INTERNAL TRANSCRIBED SPACER;

ALEXANDRIUM OSTENFELDII; ALGAL COMMUNITY; ALGAL GENETICS; ALGAL GROWTH; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ARTICLE; BALTIC SEA; CONTROLLED STUDY; DINOFLAGELLATE; ESTUARY; GENE FREQUENCY; GENE STRUCTURE; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; GEOGRAPHIC ORIGIN; MARINE SPECIES; MICROALGA; MOLECULAR CLONING; NONHUMAN; PHYLOGENY; POPULATION STRUCTURE; SPECIES DIFFERENCE;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; BIOLOGICAL EVOLUTION; GENETIC DRIFT; GENETIC VARIATION; GENETICS, POPULATION; MICROALGAE; MICROSATELLITE REPEATS; OCEANS AND SEAS;

ALEXANDRIUM OSTENFELDII; DINOPHYCEAE; EUKARYOTA;

EID: 84871815279     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053602     Document Type: Article

References (75)

1. Finlay BJ, Fenchel T, (2004) Cosmopolitan metapopulations of free-living microbial eukaryotes. Protist 155 (2): 237-244.
2. Foissner W, (2006) Biogeography and dispersal of microorganisms: A review emphasizing protists. Acta Protozoolociga (45): 111-136.
3. Waples RS, Gaggiotti O, (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol. Ecol 15: 1419-1439.
4. Bolch C, Orr PT, Jones GJ, Blackburn SI, (1999) Genetic, morphological, and toxicological variation among globally distributed strains of Nodularia (cyanobacteria) Journal of Phycology. (35): 339-355.
5. John U, Groben R, Beszteri B, Medlin L, (2004) Utility of amplified fragment length polymorphisms (AFLP) to analyse genetic structures within the Alexandrium tamarense species complex. Protist 155(2): 169-179.
6. Godhe A, Harnstrom K, (2010) Linking the planktonic and benthic habitat: Genetic structure of the marine diatom Skeletonema marinoi. Mol Ecol 19 (20): 4478-4490.
7. Logares R, Rengefors K, Kremp A, Shalchian-Tabrizi K, Boltovskoy A, et al. (2007) Phenotypically different microalgal morphospecies with identical ribosomal DNA: A case of rapid adaptive evolution? Microb. Ecol 53(4): 549-561.
8. Nagai S, Lian C, Yamaguchi S, Hamaguchi M, Matsuyama Y, et al. (2007) Microsatellite markers reveal population genetic structure of the toxic dinoflagellate Alexandrium tamarense (Dinophyceae) in Japanese coastal waters. Journal of Phycology (43): 43-54.
9. Rynearson TA, Armbrust EV (2004) Genetic differentiation among populations of the planktonic marine diatom Ditylum brightwellii. Journal of Phycology: 34-43.
10. Alpermann TJ, Tillmann U, Beszteri B, Cembella A, John U, (2010) Phenotypic variation and genotypic diversity in a planktonic population of toxigenic marine dinoflagellate Alexandrium tamarense (Dinophyceae). Journal of Phycology (46): 18-32.
11. Alpermann TJ, Beszteri B, John U, Tillmann U, Cembella AD, (2009) Implications of life-history transitions on the population genetic structure of the toxigenic marine dinoflagellate Alexandrium tamarense. Mol Ecol 18 (10): 2122-2133.
12. Brosnahan ML, Kulis DM, Solow AR, Erdner DL, Percy L, et al. (2010) Outbreeding lethality between toxic Group I and non toxic Group III Alexandrium tamarense spp. isolates: Predominance of heterotypic encystment and implications formatting interactions and biogeography. Deep-Sea Res. II 57: 175-189.
13. Björk (1995) A review of the history of the Baltic Sea, 13,0-8,0 Ka BP. Quat. Int 27: 19-40.
14. Johannesson K, André C, (2006) Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea. Mol. Ecol 15: 2013-2029.
15. Booy G, Hendriks RJJ, Smulders MJM, (2000) Genetic diversity and the survival of populations. Plant Biology 2: 379-395.
16. Eckert CG, (2002) The loss of sex in clonal plants. Evol. Ecol 15: 501-520.
17. Nikula R, Strelkov P, Väinölä R, (2008) A broad transition zone between an inner Baltic hybrid swarm and a pure North Sea subspecies of Macoma balthica (Mollusca, Bivalvia). MolEcol 17: 1505-1522.
18. Tatarenkov A, Bergström L, Jönsson RB, Serrão EA, Kautsky L, et al. (2005) Intriguing asexual life in marginal populations of the brown seaweed Fucu svesiculosus. Mol. Ecol 14: 647-651.
19. Johannesson K, Johansson D, Larsson KH, Huenchunir CJ, Perus J, et al. (2011) Frequent clonality in fucoids (Fucusradicansand F. vesiculosus; Fucales Phaeophyceae) in the Baltic Sea. J Phycol 47: 990-998.
20. Hughes AR, Stachowizc JJ, (2004) Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. P NatlAcadSci USA 101: 8998-9002.
21. Ehlers A, Worm B, Reusch TBH, (2008) Importance of genetic diversity in eelgrass Zostera marina for its resilience to global warming. Mar Ecol Prog Ser 355: 1-7.
22. Nikula R, Väinölä R, (2003) Phylogeography of Cerastoderma glaucum (Bivalvia: Cardiidae) across Europe: a major break in the Eastern Mediterranean. Mar Biol 143: 339-350.
23. Olsen JL, Stam WT, Coyer JA, Reusch TB, Billingham M, et al. (2004) North Atlantic phylogeography and large-scale population differentiation of the seagrass Zostera marina L. Mol Ecol. 13: 1923-41.
24. Laamanen M, Forsström L, Sivonen K, (2002) Diversity of Aphanizomenon flos-aquae (Cyanobacterium) populations along a Baltic Sea Salinity Gradient. Appl. Env. Microbiol 68: 5296-5303.
25. Halinen K, Fewer DP, Sihvonen LM, Lyra C, Eronen E, et al. (2008) Genetic diversity in strains of the genus Anabaena isolated from planktonic and benthic habitats of the Gulf of Finland (Baltic Sea). FEMS Microbiol. Ecol 64: 199-208.
26. Moestrup Ø, Hansen PJ, (1988) On the occurrence of the potentially toxic dinoflagellates Alexandrium tamarense (Gonyaulax excavata) and A. ostenfeldii in Danish and Faroese waters. Ophelia 28: 195-213.
27. Cembella AD, Bauder AG, Lewis NI, Quilliam MA, (2001) Association of the gonyaulacoid dinoflagellate Alexandrium ostenfeldii with spirolide toxins in size-fractionated plankton. J Plankton Res 23: 1413-1419.
28. John U, Fensome R, Medlin LK, (2003) The application of a molecular clock based on molecular sequences and the fossil records to explain biogeographic distributions within the Alexandrium tamarense "species complex" (Dinophyceae). Mol. Biol. Evol 20: 1015-27.
29. Hakanen P, Suikkanen S, Franzén J, Franzén H, Kankaanpää H, et al. (2012) Bloom and toxin dynamics of Alexandrium ostenfeldii in a shallow embayment at the SW coast of Finland, northern Baltic Sea. Harmful Algae 15: 91-99.
30. Kremp A, Lindholm T, Dreßler N, Erler K, Gerdts G, et al. (2009) Bloom forming Alexandrium ostenfeldii (Dinophyceae) in shallow waters of the Åland Archipelago, Northern Baltic Sea. Harmful Algae 8: 318-328.
31. Figueroa RI, Garces E, Massana R, Camp J, (2008) Description, host-specificity, and strain selectivity of the dinoflagellate parasite Parvilucifera sinerae sp. nov. (Perkinsozoa). Protist 159: 563-578.
32. Elken J, Matthäus W (2008) Assessment of Climate Change for the Baltic Sea Basin In: BACC author team (Ed.), Baltic Sea Oceanography. Springer-Verlag, Berlin, pages 379-385.
33. Adachi M, Sako Y, Ishida Y, (1994) Restriction fragment length polymorphism of ribosomal DNA internal transcribed spacer and 5.8S regions in Japanese Alexandrium species (Dinophyce- ae). J. Phycol. 30: 857-63.
34. Katoh K, Asimenos G, Toh H, (2009) Multiple alignment of DNA sequences with MAFFT. Method MolBiol 537: 39-64.
35. Gouy M, Guindon S, Gascuel O, (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27(2): 221-224.
36. Ronquist F, Huelsenbeck JP, (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
37. Rodríguez F, Oliver JL, Marín A, Medina JR, (1990) The general stochastic model on nucleotide substitution. J Theor. Biol 22: 485-501.
38. Posada D, (2008) jModelTest: Phylogenetic Model Averaging. Mol. Biol. Evol 25: 1253-1256.
39. Rambaut A, Drummond AJ (2007) Tracer v1.4, BEAST Software website. Available: http://beast.bio.ed.ac.uk/Tracer. Accessed 2011 Aug 5.
40. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol.52 (5): 696-704. PubMed PMID: 14530136.
41. Bandelt HJ, Forster P, Röhl A, (1999) Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol 16: 37-48.
42. Clement M, Posada D, Crandall KA, (2000) TCS: a computer program to estimate gene genealogies. Mol. Ecol 9: 1657-1659.
43. Swofford DL (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) Version 4. Sinauer Associates, Sunderland, Massachusetts.
44. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, et al. (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23: 4407-4414.
45. Figueroa RI, Rengefors K, Bravo I, Bench S, (2010) From homothally to heterothally: Mating preferences and genetic variation within clones of the dinoflagellate Gymnodinium catenatum. Deep Sea Res II 57: 190-198.
46. Lohuis MR, Miller DJ, (1998) Hypermethylation at CpG-motifs in the dinoflagellates Amphidinium carterae (Dinophyceae) and Symbiodinium microadriaticum (Dinophyceae): Evidence from restriction analyses, 5-azacytidine and ethionine treatment. J Phycol 34: 152-159.
47. Whitlock R, Hipperson H, Mannarelli M, Butlin RK, Burke T, (2008) An objective, rapid and reproducible method for scoring AFLP peak-height data that minimizes genotyping error. Mol. Ecol Resources 8: 725-735.
48. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
49. Falush D, Stephens M, Pritchard JK, (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics164: 1567-1587.
50. Evanno G, Regnaut S, Goudet J, (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol 14: 2611-2620.
51. Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources vol. 4 (2) 359-361.
52. Pritchard JK, Wen X, Falush D (2010) Documentation for structure software: Version 2.3. 38 pp.
53. Excoffier L, Lischer L, (2010) ARLEQUIN suite ver. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resources 10: 564-567.
54. Abdi H (2007) Bonferroni and Šidák corrections for multiple comparisons. In N.J. Salkind (ed.). Thousand Oaks, CA: Sage. Encyclopedia of measurement and statistics.
55. Ryman N, Palm S, (2006) POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol. Ecol Notes 6: 600-602.
56. Nei M (1987) Molecular Evolutionary Genetics, 1st ed. Columbia University Press, New York, 512 pp.
57. Ehrich D, (2006) AFLPdat: a collection of R functions for convenient handling of AFLP data. Mol. Ecol. Notes, 6, 603-604.A simulated annealing approach to define the genetic structure of populations. Mol. Ecol 11: 2571-2581.
58. Haubold B, Travisano M, Rainey PB, Hudson RR, (1998) Detecting linkage disequilibrium in bacterial populations. Genetics 150: 1341-1348.
59. Haubold B, Hudson RR, (2000) LIAN 3.0: detecting linkage dis- equilibrium in multilocus data. Bioinformatics 16: 847-848.
60. Anderson DM, Alpermann TJ, Cembella AD, Collos Y, Masseret E, et al. (2012) The globally distributed genus Alexandrium: Multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae 14, 10-35.
61. Gu H, (2011) Morphology, phylogenetic position, and ecophysiology of Alexandrium ostenfeldii (Dinophyceae) from the Bohai Sea, China. J. Syst. Evol. 49: 606-616.
62. LaJeunesse TC, (2005) "Species" radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol. Biol. Evol 22: 570-581.
63. Logares R, Boltovskoy A, Bensch S, Layborn-Parry J, Rengefors K, (2009) Genetic diversity pattern in five protist species occurring in lakes. Protist 160: 301-317.
64. Piganeau G, Eyre-Walker A, Grimsley N, Moreau H, (2011) How and Why DNA Barcodes Underestimate the Diversity of Microbial Eukaryotes. PLoS ONE 6: e16342 doi:10.1371/journal.pone.0016342.
65. Pereyra RT, Bergström L, Kautsky L, Johannesson K, (2009) Rapid speciation in a newly opened postglacial marine environment, the Baltic Sea. BMC Evolutionary Biology 9: 70.
66. Nikula R, Strelkov P, Väinölä R, (2007) Diversity and trans-Arctic invasion history of mitochondrial lineages in the north Atlantic Macoma baltica complex (Bivalvia: Tellinidae). Evolution 61: 928-941.
67. Casabianca S, Penna A, Pecchioli E, Jordi A, Basterretxea G, et al. (2011) Population genetic structure and connectivity of the harmful dinoflagellate Alexandrium minutum in the Mediterranean Sea. In: P Roy SocLond B Bio 1-10.
68. Tatarenkov A, Jönsson RB, Kautsky L, Johannesson K, (2007) Genetic structure in populations of Fucus vesiculosus (Phaeophyceae) over spatial scales from 10 to 800 km. J. Phycol 43: 675-685.
69. Olsson J, Mo K, Florin A-B, Aho T, Ryman T, (2011) Genetic population structure of perch Perca fluviatilis along the Swedish coast of the Baltic Sea. J Fish Biol 79: 122-137.
70. Reusch BH, Boström C, Stam WT, Olsen JL, (1999) An ancient eelgrass clone in the Baltic. Mar. Ecol. Prog. Ser 183: 301-304.
71. Nielsen EE, Hansen MM, Ruzzante DE, Meldrup D, Grønkjær P (2003) Evidence of a hybrid-zone in Atlantic cod (Gadus morhua) in the Baltic and the Danish Belt Sea, revealed by individual admixture analysis. Molecular Ecology, 12, 1497-1508.
72. Xu J (2005) Fundamentals of fungal molecular population genetic analyses. In Evolutionary Genetics of Fungi (Ed. Xu J) Horizon Scientific Press, England, 87-116.
73. Kremp A, Parrow MW, (2006) Evidence for asexual resting cysts in the life cycle of the marine peridinoid dinoflagellate, Scrippsiella hangoei. J. Phycol 42: 400-409.
74. Xu J (2010) Metagenomics and population Genetics. In book Microbial Population Genetics. Ed. Xu J. Caister Academic Press.
75. Kremp A, Godhe A, Egardt J, Dupont S, Suikkanen S, et al. (2012) Intraspecific variability in the response of bloom forming marine microalgae to changing climatic conditions. Ecol. Evol. 2: 1195-1207.