Can Molecular Techniques Change Our Ideas About the Species Concept?

  • Linda K. Medlin
  • Martin Lange
  • Gary L. A. Barker
  • Paul K. Hayes
Part of the NATO ASI Series book series (volume 38)

Abstract

Molecular techniques can now be used to address many important questions concerning taxonomic affinity, genetic diversity, gene flow and dispersal. These data (protein or nucleic acid sequence information) can augment our understanding of a species in the marine environment. There is growing evidence that speciation and dispersal mechanisms in the marine environment are very different from terrestrial systems and occur at different rates. We have examined species/genetic diversity in three ecologically important members of the marine phytoplankton: the prymnesiophytes Phaeocystis and Emiliania huxleyi and the diatom Skeletonema costatum. All are high dispersal taxa. Differences among Phaeocystis species as measured by 18S rDNA sequence comparison indicate that extant Phaeocystis species probably arose from a cosmopolitan warm-water ancestor. Speciation events in this genus appear to have responded to major global cooling events. Two species complexes are apparent: one corresponds to taxa from polar regions and the other to taxa from temperate to tropical regions. Emiliania huxleyi, a much younger species, has dispersed across many océanographie barriers during much colder climatic conditions. Sequence data from coding and non-coding regions confirm that it is a single taxon, but RAPD techniques reveal extensive genetic diversity with both spatial and short-term temporal resolution. Sequence comparison of isolates of Skeletonema costatum, a cosmopolitan neritic form, reveals at least one cryptic species, which can also be differentiated by certain morphological features, and a cluster of isolates that may be sibling species. It may be that in many planktonic forms molecular speciation has proceeded, whereas morphological divergence has not. The abundance of sibling species in the marine environment is only now being revealed (Knowlton 1993). The fitness of form resulting in similar if not identical morphotypes has analogies at all taxonomic levels in the sea (Knowlton 1993, Sournia 1988).

Keywords

Chlorophyll Phytoplankton Polysaccharide Cretaceous Microbe 

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References

  1. Amann RI, Lin C, Key R, Montgomery L, Stahl DA (1992) Diversity among Fibrobacter isolates: Towards a phylogenetic classification. System Appl Microbiol 15: 23–31Google Scholar
  2. Aiken J, Moore GF, Holligan PM (1992) Remote sensing of oceanic biology in relation to global climate change. J Phycol 28: 579–590CrossRefGoogle Scholar
  3. Baumann MEM and Jahnke J (1986) Marine Planktonalgen der Arktis. I. Die Haptophycee Phaeocysiisjpouchetii. Mikro 75: 262–5Google Scholar
  4. Baumann MEM, Brandini FP, Staubes R (1994a) The influence of light and temperature on carbon specific DMS-release by cultures of Phaeocystis antarctica and three antarctic diatoms. Mar Chem 45: 129–136CrossRefGoogle Scholar
  5. Baumann MEM, Lancelot C, Brandini FP, Sakshaug E, John DM (1994b) The taxonomic identity of the cosmopolitan prymnesiophyte Phaeocystis: a morphological and ecophysiological approach. J Mar Sys 5: 23–39CrossRefGoogle Scholar
  6. Beam CA, Preparata R-M, Himes M, Nanney DL (1993) Ribosomal RNA sequencing of members of the Crypthecodinium cohnii (Dinophyceae) species complex: comparison with soluble enzyme studies. J Euk Microbio 40: 660–667CrossRefGoogle Scholar
  7. Bhattacharya D, Medlin L, Wainwright PO, Arizitia EV, Bibeau C, Stickel SK, Sogin ML (1992) Algae containing chlorophylls a + c are paraphyletic: molecular evolutionary analysis of the Chromophyta. Evol 46: 1801–1817CrossRefGoogle Scholar
  8. Bird CJ, Ragan MA, Critchley AT, Rice EL, Gutell RR (1994) Molecular relationships in the Gracilariaceae (Rhodophyta): further observations on some undetermined species. Eur J Phycol 29: 195–202CrossRefGoogle Scholar
  9. Brand LE (1982) Genetic variability and spatial patterns of genetic differentiation in the reproductive rates of the marine coccolithophores Emiliania huxleyi and Gephyrocapsa oceanica. Limnol Oceanogr 27: 236–245CrossRefGoogle Scholar
  10. Campbell L, Shapiro LP, Haugen EM, Morris L (1989) Immunochemical approaches to the identification of the ultraplankton: assets and limitations. In Novel Phytoplankton Blooms EM Cosper, VM Bricelj, EJ Carpenter (eds) Springer-Verlag, Berlin 39–56Google Scholar
  11. Conte MH, Volkman JK, Eglinton G (1994) Lipid biomarkers of the Prymnesiophyceae. In The Haptophyte Algae JC Green and BSC Leadbeater (eds) Clarendon Press, Oxford 351–378Google Scholar
  12. Cracraft J (1989) Speciation and its ontology: the empirical consequences of alternative species concepts for understanding patterns and process of differentiation. In Speciation and Its Consequences D Orte and JA Endler (eds) Sinauer Assoc, Sunderland 28–59Google Scholar
  13. Crame JA (1993) Latitudinal range fluctuations in the marine realm through geological time. Tree 3: 162–166Google Scholar
  14. Davidson AT and Marchant H (1992) The biology and ecology of Phaeocystis (Prymnesiophyceae). In Progress in Phycological Research Vol 8 (FE Round and DJ Chapman eds) Biopress, Bristol 1–45Google Scholar
  15. Freshwater DW and Rueness J (1994) Phylogenetic relationships of some European Gelidium (Gelidiales, Rhodophyta) species, based on rbcL nucleotide sequence analysis. Phycologia 33: 187–194CrossRefGoogle Scholar
  16. Friedl T and Zeltner C (1994) Assessing the relationships of some coccoid green lichen algae and the Microthamniales (Chlorophyta) with 18S ribosomal RNA gene sequence comparisons. J Phycol 30: 500–506CrossRefGoogle Scholar
  17. Gallagher JC (1980) Population genetics of Skeletonema costatum (Bacillariophyceae) in Narragansett Bay. J Phycol 16: 464–474CrossRefGoogle Scholar
  18. Gallagher JC (1990a) The relative roles of space and time in controlling genetic differentiation in populations of the marine diatom Skeletonema costatum: preliminary data and a comparison of methods of analysis. J Phycol 26 (suppl): 17Google Scholar
  19. Gallagher JC (1990b) Comparisons of sampling methods and data analysis of molecular evolutionary studies of diatoms. Abstract 11th International Symposium on Living and Fossil Diatoms, San FranciscoGoogle Scholar
  20. 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: 521–537CrossRefGoogle Scholar
  21. Gosling EM (1994) Speciation and species concepts in the marine environment. In Genetics and Evolution of Aquatic Organisms (AR Beaumont ed) Chapman and Hall, London 1–15Google Scholar
  22. Hasle GR (1973) Morphology and taxonomy of Skeletonema costatum (Bacillariphyceae). Norw J Botl 20: 109–137Google Scholar
  23. Hedgecock D (1994) Population genetics of marine organisms. US GLOBEC News 6: 1–3, 11Google Scholar
  24. Huss VAR, Huss G, Kessler E (1989) Deoxyribonucleic acid reassociation and interspecies relationships of the genus Chlorella (Chlorophyceae). PI Syst Evol 168: 1–82CrossRefGoogle Scholar
  25. Huss VAR, Dörr R, Grossman U, Kessler E (1986) Deoxyribonucleic acid reassociation in the taxonomy of the genus Chlorella, Arch Microbiol 145:329–333CrossRefGoogle Scholar
  26. Huss VAR and Sogin ML (1991) Phylogenetic position of some Chlorella species within the Chlorococcales based upon complete small-subunit ribosomal RNA sequences. J Mol Evol 31:432–442CrossRefGoogle Scholar
  27. Jahnke J (1989) The light and temperature dependence of growth rate and elemental composition of Phaeocystis jglobosa Scherffel and P. pouchetii (Har.) Lagerh. in batch cultures. Neth J Sea Res 23: 15–21CrossRefGoogle Scholar
  28. Jahnke J and Baumann MEM (1986) Die marine planktonalge Phaeocystis globosa: eine Massenform unserer Küstengewässer. Mikro 75: 357–359Google Scholar
  29. Jahnke J, Baumann M (1987) Differentiation between Phaeocystis pouchetii (Har.) Lagerheim and Phaeocystis globosa Scherffel. I. Colony shapes and temperature tolerances. Hydro Bull 21: 141–147CrossRefGoogle Scholar
  30. Knowlton N (1993) Sibling species in the sea. Ann Rev Ecol Sys 24: 189–216CrossRefGoogle Scholar
  31. Karsten G (1905) Das Phytoplankton des Antarktischen Meeres nach dem Material der Deutschen Tiefsee-Expedition 1898–1899. Wiss Erg Deut Tiefsee-Exp ‘Valdivia’ 1898–1899. Band II Teil 2 1–136Google Scholar
  32. Kooistra WHCF (1993) Historical biogeography in tropical Atlantic populations of Cladophoropsis membranAcea and related species. Ph D Dissertation. University of Groningen, pp 111Google Scholar
  33. Kornmann P (1955) Beobachtungen an Phaeocystis-Kultartn. Hei Wiss Meeres 5: 218–233CrossRefGoogle Scholar
  34. Lagerheim G 1893) Phaeocystis nov. gen. grundadt På Tetraspora pouched Har. Bot Not 1: 32–33Google Scholar
  35. Lancelot C, Billen G, Sournia A, Weisse T, Colijn F, Veldhuis MJW, Davies A, Wassmann P (1987) Phaeocystis blooms and nutrient enrichment in the continental coastal zones of the North Sea. Ambio 16: 38–46Google Scholar
  36. Lancelot C, Billen G, Barth H (1991) The dynamics of Phaeocystis blooms in nutrients enriched coastal zones. Wat Poll Res Rep 23: 1–106Google Scholar
  37. Larsen J and Moestrup Ø (1989) Guide to Toxic and Potentially Toxic Marine Algae. Fish Inspection Service, Minister of Fisheries, Copenhagen, 49–51Google Scholar
  38. Manhart JR and McCourt RM (1992) Molecular data and species concepts in the algae. J Phycol 28: 730–737CrossRefGoogle Scholar
  39. Medlin LK, Elwood HJ, Stickel S, Sogin ML (1991) Morphological and genetic variation within the diatom Skeletonema castatum (Bacillariophyta): evidence for a new species Skeletonemapseudocostatum. J Phycol 27: 514–524CrossRefGoogle Scholar
  40. Medlin LK, Lange M, Baumann MEM (1994a) Genetic differentiation among three colony-forming species of Phaeocystis: further evidence for the phylogeny of the Prymnesiophyta. Phycologia 33: 199–212CrossRefGoogle Scholar
  41. Medlin LK, Barker GLA, Baumann, MEM, Hayes PK, Lange M (1994b) Molecular biology and systematics. In The Haptophyte Algae (JC Green and BSC Leadbeater eds), Clarendon Press, Oxford 393–412Google Scholar
  42. Moestrup Ø (1979) Identification by electron microscopy of marine nanoplankton from New Zealand including the description of four new species. N Zea J Bot 17: 61–95Google Scholar
  43. Moestrup Ø and Larsen J (1992) Potenially toxic Phytoplankton. 1 Haptophyceae (Prymnesiophyceae). In ICES Identification Leaflets for Plankton, Leaflet No 179 (JS Lindley ed),. Natural Environmental Research Council, Plymouth 1–11Google Scholar
  44. Nanney DL, Meyer EB, Simon EM, Preparata R-M (1989) Comparison of ribosomal and isozymic phylogenies of Tetrahymenine ciliates. J Prot 36: 1–8Google Scholar
  45. Ochman H and Wilson AC (1987) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26: 74–86PubMedCrossRefGoogle Scholar
  46. Olsen JL, Stam WT, Berger S, Menzel D (1994) 18S rDNA and evolution in the Dasycladales (Chlorophyta): modern living fossils. J Phycol in pressGoogle Scholar
  47. Palumbi SR (1992) Marine speciation on a small planet. Tree 7: 114–118PubMedGoogle Scholar
  48. Pouchet G (1892) Sur une algue pélagique nouvelle. Compte Rendues séance à 16 Janvier Google Scholar
  49. Preparata R-M, Beam CA, Hirnes M, Nanney DL, Meyer EB, Simon EM (1992) Crypthecodinium and Tetrahymena: an exercise in comparative evolution. J Mol Evol 32:209–218CrossRefGoogle Scholar
  50. Scherffel A (1900) Phaeocystis globosa nov. spec, nebst einiger Betrachtungen über die Phylogenie niederer ins besonderer brauner Organismen. Wiss Meeres Ab Hel 4: 1–29Google Scholar
  51. Sogin ML, Ingold A, Karlok M, Nielsen H, Engberg J (1986) Phylogenetic evidence for the acquisition of ribosomal RNA introns subsequent to the divergence of some of the major Tetrahymena groups. EMBO 5: 3625–3630Google Scholar
  52. Sournia A (1988) Phaeocystis (Prymnesiophyceae): how many species? Nova Hedw 47:211–217Google Scholar
  53. Stiller JW and Waaland JR (1993) Molecular analysis reveals cryptic diversity in Porphyra (Rhodophyta). J Phycol 29: 506–517CrossRefGoogle Scholar
  54. van Bleijswijk J, van der Wal P, Kempers R, Veldhuis M, Young JR, Muyzer G, de Vrindde Jong E, Westbroek P (1991) Distribution of two types of Emiliania huxleyi Prymnesiophyceae in the northeast Atlantic region as determined by immunofluorescence and coccolith morphology. J Phycol 27: 566–570CrossRefGoogle Scholar
  55. Vaulot D, Birrien J-L, Marie D, Casorti R, Veldhuis M, Kraay G, Chrétiennot-Dinet M-J (1994) Morphology, ploidy, pigment composition and genome size of cultured strains of Phaeocystis (Prymnesiophyceae). J Phycol in pressGoogle Scholar
  56. Wood AM and Leatham T (1992) The species concept in phytoplankton ecology. J Phycol 28: 723–729CrossRefGoogle Scholar
  57. Young JR and Westbroek P (1991) Phenotypic variation in the coccolithophorid species Emiliania huxleyi. Mar Micropaleont 18:5–23CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1995

Authors and Affiliations

  • Linda K. Medlin
    • 1
  • Martin Lange
    • 1
  • Gary L. A. Barker
    • 2
  • Paul K. Hayes
    • 2
  1. 1.Alfred-Wegener-InstituteBremerhavenGermany
  2. 2.School of Biological SciencesUniversity of BristolBristolUK

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