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Phenotypically Different Microalgal Morphospecies with Identical Ribosomal DNA: A Case of Rapid Adaptive Evolution?

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Abstract

The agents driving the divergence and speciation of free-living microbial populations are still largely unknown. We investigated the dinoflagellate morphospecies Scrippsiella hangoei and Peridinium aciculiferum, which abound in the Baltic Sea and in northern temperate lakes, respectively. Electron microscopy analyses showed significant interspecific differences in the external cellular morphology, but a similar plate pattern in the characteristic dinoflagellate armor. Experimentally, S. hangoei grew in a wide range of salinities (0–30), whereas P. aciculiferum only grew in low salinities (0–3). Despite these phenotypic differences and the habitat segregation, molecular analyses showed identical ribosomal DNA sequences (ITS1, ITS2, 5.8S, SSU, and partial LSU) for both morphospecies. Yet, a strong interspecific genetic isolation was indicated by amplified fragment length polymorphism (F ST = 0.76) and cytochrome b (cob) sequence divergence (∼1.90%). Phylogenetic reconstructions based on ribosomal (SSU, LSU) and mitochondrial (cob) DNA indicated a recent marine ancestor for P. aciculiferum. In conclusion, we suggest that the lacustrine P. aciculiferum and the marine-brackish S. hangoei diverged very recently, after a marine–freshwater transition that exposed the ancestral populations to different selective pressures. This hypothetical scenario agrees with mounting data indicating a significant role of natural selection in the divergence of free-living microbes, despite their virtually unrestricted dispersal capabilities. Finally, our results indicate that identical ITS rDNA sequences do not necessarily imply the same microbial species, as commonly assumed.

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References

  1. 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 (Dinophyceae). J Phycol 30: 857–863

    Article  CAS  Google Scholar 

  2. Anderson, JR, Bentley, S, Irwin, JAG, Mackie, JM, Neate, S, Pattemore, JA (2004) Characterization of Rhizoctonia solani isolates causing root canker of lucerne in Australia. Australas Plant Pathol 33: 241–247

    Article  CAS  Google Scholar 

  3. Avise, JC (2004) Molecular Markers, Natural History, and Evolution, 2nd ed. Sinauer Associates, MA

    Google Scholar 

  4. Baas-Becking, LGM (1934) Geobiologie of Inleiding Tot De Milieukunde, Serie 18/19. Van Stockum's Gravenhange, The Hague, The Netherlands

    Google Scholar 

  5. Balech, E (1963) Dos dinoflagelados de una laguna salobre de la Argentina. Not Mus La Plata 20: 111–123

    Google Scholar 

  6. Bensch, S, Perez-Tris, J, Waldenstrom, J, Hellgren, O (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution 58: 1617–1621

    PubMed  CAS  Google Scholar 

  7. Berry, JP, Reece, KS, Rein, KS, Baden, DG, Haas, LW, Ribeiro, WL, Shields, JD, Snyder, RV, Vogelbein, WK, Gawley, RE (2002) Are Pfiesteria species toxicogenic? Evidence against production of ichthyotoxins by Pfiesteria shumwayae. Proc Natl Acad Sci USA 99: 10970–10975

    Article  PubMed  CAS  Google Scholar 

  8. Bjorck, S (1995) A review of the history of the Baltic Sea, 13.0–8.0 Ka Bp. Quatern Int 27: 19–40

    Google Scholar 

  9. Bourelly, P (1968) Notes sur les Péridiniens d'eau douce. Protistologica 4: 5–14

    Google Scholar 

  10. Casamatta, DA, Vis, ML, Sheath, RG (2003) Cryptic species in cyanobacterial systematics: a case study of Phormidium retzii (Oscillatoriales) using RAPD molecular markers and 16S rDNA sequence data. Aquat Bot 77: 295–309

    Article  CAS  Google Scholar 

  11. Cavalier-Smith, T (2004) Only six kingdoms of life. Proc R Soc Lond B Biol 271 :1251–1262

    Article  CAS  Google Scholar 

  12. Connell, LB (2000) Nuclear ITS region of the alga Heterosigma akashiwo (Chromophyta: Raphidophyceae) is identical in isolates from Atlantic and Pacific basins. Mar Biol 136: 953–960

    Article  CAS  Google Scholar 

  13. Coyne, JA, Orr, HA (2004) Speciation. Sinauer Associates, MA

    Google Scholar 

  14. Darling, KF, Wade, CM, Stewart, IA, Kroon, D, Dingle, R, Brown, AJL (2000) Molecular evidence for genetic mixing of Arctic and Antarctic subpolar populations of planktonic foraminifers. Nature 405: 43–47

    Article  PubMed  CAS  Google Scholar 

  15. Dawson, MN, Hamner, WM (2005) Rapid evolutionary radiation of marine zooplankton in peripheral environments. Proc Natl Acad Sci USA 102: 9235–9240

    Article  PubMed  CAS  Google Scholar 

  16. Doebeli, M, Dieckmann, U, Metz, JAJ, Tautz, D (2005) What we have also learned: adaptive speciation is theoretically plausible. Evolution 59: 691–695

    PubMed  Google Scholar 

  17. Edvardsen, B, Shalchian-Tabrizi, K, Jakobsen, KS, Medlin, LK, Dahl, E, Brubak, S, Paasche, E (2003) Genetic variability and molecular phylogeny of Dinophysis species (Dinophyceae) from Norwegian waters inferred from single cell analyses of rDNA. J Phycol 39: 395–408

    CAS  Google Scholar 

  18. Ekman, P, Fries, M (1970) Studies of sediments from Lake Erken, Eastern Central Sweden. GFF 92: 214–224

    CAS  Google Scholar 

  19. Fenchel, T (1993) There are more small than large species. Oikos 68: 375–378

    Article  Google Scholar 

  20. Finlay, BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296: 1061–1063

    Article  PubMed  CAS  Google Scholar 

  21. Finlay, BJ (2004) Protist taxonomy: an ecological perspective. Philos Trans R Soc, B 359: 599–610

    Article  Google Scholar 

  22. Finlay, BJ, Clarke, KJ (1999) Ubiquitous dispersal of microbial species. Nature 400: 828

    Article  CAS  Google Scholar 

  23. Fukuyo, Y, Hideaki, T, Chihara, M, Matsuoka, K (1990) Red Tide Organisms in Japan—An Illustrated Taxonomic Guide. U Rokakuho Publ, Tokyo

    Google Scholar 

  24. Gottschling, M, Keupp, H, Plotner, J, Knop, R, Willems, H, Kirsch, M (2005) Phylogeny of calcareous dinoflagellates as inferred from ITS and ribosomal sequence data. Mol Phylogenet Evol 36: 444–455.

    Article  PubMed  CAS  Google Scholar 

  25. Guillard, RR, Lorenzen, CJ (1972) Yellow-green algae with Chlorophyllide C. J Phycol 8: 10–14

    Article  CAS  Google Scholar 

  26. Guillard, RR, Ryther, JH (1962) Studies of marine planktonic diatoms .1. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can J Microbiol 8: 229–239

    Article  PubMed  CAS  Google Scholar 

  27. Hall, TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95–98

    CAS  Google Scholar 

  28. Hendry, AP, Wenburg, JK, Bentzen, P, Volk, EC, Quinn, TP (2000) Rapid evolution of reproductive isolation in the wild: evidence from introduced salmon. Science 290: 516–518

    Article  PubMed  CAS  Google Scholar 

  29. Hewitt, G (2000) The genetic legacy of the Quaternary ice ages. Nature 405: 907–913

    Article  PubMed  CAS  Google Scholar 

  30. Hewitt, GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58: 247–276

    Article  Google Scholar 

  31. Horiguchi, T, Pienaar, RN (1988) Ultrastructure of a new sand-dwelling dinoflagellate, Scrippsiella arenicola sp. nov. J Phycol 24: 426–438

    Google Scholar 

  32. Huelsenbeck, JP, Ronquist, F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755

    Article  PubMed  CAS  Google Scholar 

  33. Kauserud, H, Stensrud, O, Decock, C, Shalchian-Tabrizi, K, Schumacher, T (2006) Multiple gene genealogies and AFLPs suggest cryptic speciation and long-distance dispersal in the basidiomycete Serpula himantioides (Boletales). Mol Ecol 15: 421–431

    Article  PubMed  CAS  Google Scholar 

  34. Kim, E, Wilcox, L, Graham, L, Graham, J (2004) Genetically distinct populations of the dinoflagellate Peridinium limbatum in neighboring Northern Wisconsin lakes. Microbial Ecol 48: 521–527

    Article  CAS  Google Scholar 

  35. Kisselev, IA (1950) Pantzyrnye Zhgutikonostsy (Dinoflagellata) Morey i Presnovodnykh vod SSSR. Opredelitel po faune SSSR 33, Akad Nauka SSSR, Moskva

    Google Scholar 

  36. Kremp, A, Elbrachter, M, Schweikert, M, Wolny, JL, Gottschling, M (2005) Woloszynskia halophila (Biecheler) comb. nov.: a bloom-forming cold-water dinoflagellate co-occurring with Scrippsiella hangoei (Dinophyceae) in the Baltic Sea. J Phycol 41: 629–642

    Article  Google Scholar 

  37. Larsen, J, Kuosa, H, Ikävalko, J, Kivi, K, Hällfors, S (1995) A redescription of Scrippsiella-hangoei (Schiller) comb. nov.—a red tide dinoflagellate from the Northern Baltic. Phycologia 34: 135–144

    Google Scholar 

  38. Leblond, JD, Chapman, PJ (2002) A survey of the sterol composition of the marine dinoflagellates Karenia brevis, Karenia mikimotoi, and Karlodinium micrum distribution of sterols within other members of the class Dinophyceae. J Phycol 38: 670–682

    Article  CAS  Google Scholar 

  39. Lee, CE, Bell, MA (1999) Causes and consequences of recent freshwater invasions by saltwater animals. Trends Ecol Evol 14: 284–288

    Article  CAS  PubMed  Google Scholar 

  40. Lefèvre, M (1932) Monographie des espèces d'eau douce du genre Peridinium. Ehrb Arch Bot 2: 1–208

    Google Scholar 

  41. Lindemann, E (1919) Untersuchungen über süsswasserperidineen und ihre variationsformen. Arch Protistenk 39: 209–262

    Google Scholar 

  42. Lopez-Garcia, P, Rodriguez-Valera, F, Pedros-Alio, C, Moreira, D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409: 603–607

    Article  PubMed  CAS  Google Scholar 

  43. Loret, P, Tengs, T, Villareal, TA, Singler, H, Richardson, B, McGuire, P, Morton, S, Busman, M, Campbell, L (2002) No difference found in ribosomal DNA sequences from physiologically diverse clones of Karenia brevis (Dinophyceae) from the Gulf of Mexico. J Plankton Res 24: 735–739

    Article  CAS  Google Scholar 

  44. Lynch, M, Milligan, BG (1994) Analysis of population genetic-structure with RAPD markers. Mol Ecol 3: 91–99

    PubMed  CAS  Google Scholar 

  45. Massana, R, DeLong, EF, Pedros-Alio, C (2000) A few cosmopolitan phylotypes dominate planktonic archaeal assemblages in widely different oceanic provinces. Appl Environ Microbiol 66: 1777–1787

    Article  PubMed  CAS  Google Scholar 

  46. McDonald, JH, Kreitman, M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351: 652–654

    Article  PubMed  CAS  Google Scholar 

  47. McKinnon, JS, Rundle, HD (2002) Speciation in nature: the three-spine stickleback model systems. Trends Ecol Evol 17: 480–488

    Article  Google Scholar 

  48. Mendelson, TC, Shaw, KL (2005) Rapid speciation in an arthropod. Nature 433: 375–376

    Article  PubMed  CAS  Google Scholar 

  49. Miller, MP (1997) Tools for Population Genetic Analysis (TFPGA) 1.3: a Windows program for the analysis of allozyme and molecular population genetic data. Distributed by the author

  50. Miscampbell, AE, Lankester, MW, Adamson, ML (2004) Molecular and morphological variation within swim bladder nematodes, Cystidicola spp. Can J Fish Aquat Sci 61: 1143–1152

    Article  CAS  Google Scholar 

  51. Montresor, M (1995) Scrippsiella ramonii sp nov (Peridiniales, Dinophyceae), a marine dinoflagellate producing a calcareous resting cyst. Phycologia 34: 87–91

    Google Scholar 

  52. Montresor, M, Lovejoy, C, Orsini, L, Procaccini, G, Roy, S (2003) Bipolar distribution of the cyst-forming dinoflagellate Polarella glacialis. Polar Biol 26: 186–194

    Google Scholar 

  53. Montresor, M, Sgrosso, S, Procaccini, G, Kooistra, WHCF (2003) Intraspecific diversity in Scrippsiella trochoidea (Dinophyceae): evidence for cryptic species. Phycologia 42: 56–70

    Article  Google Scholar 

  54. Montresor, M, Zingone, A (1988) Scrippsiella precaria sp nov (Dinophyceae), a marine dinoflagellate from the Gulf of Naples. Phycologia 27: 387–394

    Google Scholar 

  55. Moon-van der Staay, SY, De Wachter, R, Vaulot, D (2001) Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409: 607–610

    Article  PubMed  CAS  Google Scholar 

  56. Muir, G, Fleming, CC, Schlotterer, C (2001) Three divergent rDNA clusters predate the species divergence in Quercus petraea (Matt.) Liebl. and Quercus robur L. Mol Biol Evol 18: 112–119

    PubMed  CAS  Google Scholar 

  57. Nei, M (1972) Genetic distance between populations. Am Nat 106: 283–292

    Article  Google Scholar 

  58. Niemi, Å (1975) Ecology of phytoplankton in the Tvärminne area, SW coast of Finland: II. Primary production and environmental conditions in the archipelago and the sea zone. Acta Bot Fenn 105: 1–73

    Google Scholar 

  59. Orr, MR, Smith, TB (1998) Ecology and speciation. Trends Ecol Evol 13: 502–506

    Article  Google Scholar 

  60. Ostenfeld, CH, Wesenberg-Lund, C (1906) A regular fortnightly exploration of the phytoplankton of the two Icelandic lakes, Thingvallavatn and Myvatn. Proc R Soc Edinburgh 25: 1092–1176

    Google Scholar 

  61. Pace, NR (1997) A molecular view of microbial diversity and the biosphere. Science 276: 734–740

    Article  PubMed  CAS  Google Scholar 

  62. Page, RDM (1996) Treeview: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12: 357–358

    PubMed  CAS  Google Scholar 

  63. Papke, RT, Ramsing, NB, Bateson, MM, Ward, DM (2003) Geographical isolation in hot spring cyanobacteria. Environ Microbiol 5 :650–659

    Article  PubMed  CAS  Google Scholar 

  64. Papke, RT, Ward, DM (2004) The importance of physical isolation to microbial diversification. FEMS Microbiol Ecol 48: 293–303

    Article  CAS  PubMed  Google Scholar 

  65. Pearce, I, Hallegraeff, GM (2004) Genetic affinities, ecophysiology and toxicity of Prorocentrum playfairii and P. foveolata (Dinophyceae) from Tasmanian freshwaters. Phycologia 43: 271–281

    Article  Google Scholar 

  66. Pfiester, LA, Anderson, DM (1987) Dinoflagellate reproduction. In: Taylor, FJR (Eds.) The Biology of Dinoflagellates. Botanical Monographs, vol. 21, Blackwell, Oxford, pp 611–648

    Google Scholar 

  67. Popovsky, J, Pfiester, LA (1990) Dinophyceae. In: Ettl, H, Gerloff, J, Heynig, H, Mollenhauer, D (Eds.) Süßwasserflora von Mitteleuropa, vol. 6, Gustav Fischer Verlag, Stuttgart

    Google Scholar 

  68. Posada, D, Crandall, KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818

    Article  PubMed  CAS  Google Scholar 

  69. Rainey, PB, Buckling, A, Kassen, R, Travisano, M (2000) The emergence and maintenance of diversity: insights from experimental bacterial populations. Trends Ecol Evol 15: 243–247

    Article  PubMed  Google Scholar 

  70. Rainey, PB, Travisano, M (1998) Adaptive radiation in a heterogeneous environment. Nature 394: 69–72

    Article  PubMed  CAS  Google Scholar 

  71. Rengefors, K (1998) Seasonal succession of dinoflagellates coupled to the benthic cyst dynamics in Lake Erken, Sweden. Arch Hydrobiol 51: 123–141

    Google Scholar 

  72. Riseberg, LH, Wendel, JF (1993) Introgression and its consequences. In: Harrison, RG (Eds.) Hybrid Zones and the Evolutionary Process. Oxford University Press, New York, pp 70–109

    Google Scholar 

  73. Rozas, J, Sanchez-DelBarrio, JC, Messeguer, X, Rozas, R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496–2497

    Article  PubMed  CAS  Google Scholar 

  74. Rundle, HD, Nagel, L, Boughman, JW, Schluter, D (2000) Natural selection and parallel speciation in sympatric sticklebacks. Science 287: 306–308

    Article  PubMed  CAS  Google Scholar 

  75. Rynearson, TA, Armbrust, EV (2000) DNA fingerprinting reveals extensive genetic diversity in a field population of the centric diatom Ditylum brightwellii. Limnol Oceanogr 45: 1329–1340

    Article  Google Scholar 

  76. Rynearson, TA, Armbrust, EV (2004) Genetic differentiation among populations of the planktonic marine diatom Ditylum brightwellii (Bacillariophyceae). J Phycol 40: 34–43

    Google Scholar 

  77. Saez, AG, Probert, I, Geisen, M, Quinn, P, Young, JR, Medlin, LK (2003) Pseudo-cryptic speciation in coccolithophores. Proc Natl Acad Sci USA 100: 7163–7168

    Article  PubMed  CAS  Google Scholar 

  78. Saldarriaga, JF, Taylor, FJR, Keeling, PJ, Cavalier-Smith, T (2001) Dinoflagellate nuclear SSU rRNA phylogeny suggests multiple plastid losses and replacements. J Mol Evol 53: 204–213

    Article  PubMed  CAS  Google Scholar 

  79. Schmidt, LE, Hansen, PJ (2001) Allelopathy in the prymnesiophyte Chrysochromulina polylepis: effect of cell concentration, growth phase and pH. Mar Ecol Prog Ser 216: 67–81

    CAS  Google Scholar 

  80. Scholin, CA, Herzog, M, Sogin, M, Anderson, DM (1994) Identification of group-specific and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae): II. Sequence analysis of a fragment of the LSU rRNA gene. J Phycol 30: 999–1011

    Article  CAS  Google Scholar 

  81. Smayda, TJ (1997) Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol Oceanogr 42: 1137–1153

    Article  Google Scholar 

  82. Steidinger, KA, Balech, E (1977) Scrippsiella subsalsa (Ostenfeld) comb nov (Dinophyceae) with a discussion on Scrippsiella. Phycologia 16: 69–73

    Google Scholar 

  83. Taylor, FJR (1987) The biology of dinoflagellates. Botanical Monographs, vol. 21. Blackwell, Oxford

    Google Scholar 

  84. Tengs, T, Bowers, HA, Glasgow, HB, Burkholder, JM, Oldach, DW (2003) Identical ribosomal DNA sequence data from Pfiesteria piscicida (Dinophyceae) isolates with different toxicity phenotypes. Environ Res 93: 88–91

    Article  PubMed  CAS  Google Scholar 

  85. Thompson, JD, Gibson, TJ, Plewniak, F, Jeanmougin, F, Higgins, DG (1997) The CLUSTALX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876–4882

    Article  PubMed  CAS  Google Scholar 

  86. Tyler, PA (1996) Endemism in freshwater algae. Hydrobiologia 336: 127–135

    Google Scholar 

  87. Uwe, J, Fensome, RA, Medlin, LK (2003) The application of a molecular clock based on molecular sequences and the fossil record to explain biogeographic distributions within the Alexandrium tamarense “Species Complex” (Dinophyceae). Mol Biol Evol 20: 1015–1027

    Article  Google Scholar 

  88. Vekemans, X (2002) AFLP-SURV v.1.0. Distributed by the author. Laboratoire de Génétique et Ecologie Végétale, Université Libre de Bruxelles, Belgium

  89. von der Heyden, S, Chao, EE, Cavalier-Smith, T (2004) Genetic diversity of goniomonads: an ancient divergence between marine and freshwater species. Eur J Phycol 39: 343–350

    Article  CAS  Google Scholar 

  90. von Stosch, HA (1973) Observations on vegetative reproduction and sexual life cycles of two freshwater dinoflagellates Gymnodinium pseudopalustre Schiller and Woloszynkskia apiculata sp. nov. Br Phycol J 8: 105–134

    Google Scholar 

  91. Vos, P, Hogers, R, Bleeker, M, Reijans, M, Vandelee, T, Hornes, M, Frijters, A, Pot, J, Peleman, J, Kuiper, M, Zabeau, M (1995) AFLP—a new technique for DNA-fingerprinting. Nucleic Acids Res 23: 4407–4414

    Article  PubMed  CAS  Google Scholar 

  92. Wetzel, RG (2001) Limnology. Lake and River Ecosystems, 3rd ed. Academic Press, California

    Google Scholar 

  93. Weyhenmeyer, G (1999) Lake Erken: Meteorological, Physical, Chemical and Biological Data and List of Publications from 1933 to 1998. Norr Malma field station report, Evolutionary Biology Centre, Uppsala University http://www.ebc.uu.se/norr.malma/publikationer/Erken%20Data%20Report.pdf)

  94. Whitaker, RJ, Grogan, DW, Taylor, JW (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301: 976–978

    Article  PubMed  CAS  Google Scholar 

  95. Woloszynska, J (1928) Dinoflagellatae polskiego Baltyku i blot nad Piasnica. Arch Hydrobiol Ryb 3: 153–278

    Google Scholar 

  96. Zhang, H, Bhattacharya, D, Lin, S (2005) Phylogeny of dinoflagellates based on mitochondrial cytochrome b and nuclear small subunit rDNA sequence comparisons. J Phycol 41: 411–420

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The Swedish Research Council and the SEED project contract, GOCE-CT-2005-003875 (European Commission Directorate General Research), financed this study. We thank S. Bensch for his assistance with AFLP analyses and J. Pérez-Tris for comments on early versions of the manuscript. Dr. C. Luxoro is thanked for methodological help during the initial phase of this work and T. Rolfsen (UiO) for assistance with SEM. Preliminary parts of this work were carried out in D. Anderson's laboratory at Woods Hole. Special thanks to the three anonymous reviewers who have helped to improve this manuscript. Phylogenies were computed in the University of Oslo Bioportal, (http://www.bioportal.uio.no/).

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  1. Limnology Division, Ecology Department, Lund University, Sölvegatan 37, SE-223 62, Lund, Sweden

    Ramiro Logares & Karin Rengefors

  2. Tvärminne Zoological Station, University of Helsinki, 10900, Hanko, Finland

    Anke Kremp

  3. Department of Zoology, University of Oxford, South Park Road, OX1 3PS, Oxford, UK

    Kamran Shalchian-Tabrizi

  4. Departamento Científico Ficología, Paseo del Bosque s/n°, Museo de La Plata, 1900, La Plata, Argentina

    Andrés Boltovskoy

  5. National Veterinary Institute, Section of Food and Feed Microbiology, Ullevaalsveien 68, N-0454, Oslo, Norway

    Torstein Tengs

  6. FWC, Fish & Wildlife Research Institute, St. Petersburg, FL, 33701, USA

    Aaron Shurtleff

  7. Department of Biology, Section Limnology, University of Oslo, Pb. 1064, N-0316, Blindern, Oslo, Norway

    Dag Klaveness

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  1. Ramiro Logares
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Logares, R., Rengefors, K., Kremp, A. et al. Phenotypically Different Microalgal Morphospecies with Identical Ribosomal DNA: A Case of Rapid Adaptive Evolution?. Microb Ecol 53, 549–561 (2007). https://doi.org/10.1007/s00248-006-9088-y

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