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Journal of Applied Phycology

, Volume 20, Issue 5, pp 979–989 | Cite as

Phylogeography of the genus Ulva (Ulvophyceae, Chlorophyta), with special reference to the Japanese freshwater and brackish taxa

  • Satoshi Shimada
  • Naoko Yokoyama
  • Shogo Arai
  • Masanori Hiraoka
Article

Abstract

The nuclear-encoded ITS and associated 5.8S rDNA regions were sequenced for 72 specimens of Ulva collected from 44 rivers across Japan, including U. prolifera Müller from the Shimanto River, Kochi Prefecture, as well as 26 samples originally identified as U. linza L. from 20 coastal marine areas. Sequence data revealed that the samples fall into six distinct clades: the U. flexuosa Wulfen clade (2 samples), the Ulva linza-procera-prolifera (LPP) complex clade (75 samples), Ulva sp. 1 clade (3 samples), Ulva sp. 2 clade (7 samples), Ulva sp. 3 clade (4 samples) and Ulva sp. 4 clade (7 samples). The LPP complex contained a mixture of 26 samples collected from seashores and 49 samples obtained from rivers, including U. prolifera from the Shimanto River, and GenBank data for U. linza and U. procera Ahlner. The samples of the LPP complex differed by only 0–7 substitutions (0–1.149%). Subsequent phylogeographic analyses of the LPP complex based on the 5S rDNA spacer region revealed the presence of two further groupings: a group including 22 strictly marine littoral U. linza samples and a U. prolifera group composed of a mixture of 4 marine samples and all 49 river samples. The monophyly of all river samples indicates that adaptation to low salinity might have occurred only once in the evolutionary history of the LPP complex.

Keywords

Taxonomy River Freshwater Japan Phylogeography Ulva 

Notes

Acknowledgements

We thank Dr. A. Kurihara of Hokkaido University and Dr. M. Iima of Nagasaki University, who generously collected some of the materials. We are deeply indebted to Dr. E.J. Faye of Port and Airport Research Institute, Yokosuka, for helpful discussions. The help of Professor C.A. Maggs of Queen’s University, Belfast, with stimulating discussion, constructive criticism and valuable suggestions on an early version of the manuscript was greatly appreciated. This research was partially supported by the Ministry of Education, Science, Sports and Culture, Grant-in-Aid for Encouragement of Young Scientists (A), 17687007, 2005–2007.

References

  1. Blomster J, Maggs CA, Stanhope MJ (1998) Molecular and morphological analysis of Enteromorpha intestinalis and E. compressa (Chlorophyta) in the British Isles. J Phycol 34:319–340CrossRefGoogle Scholar
  2. Brodie J, Guiry MD, Masuda M (1991) Life history and morphology of Chondrus nipponicus (Gigartinales, Rhodophyta) from Japan. Br Phycol J 26:33–50CrossRefGoogle Scholar
  3. Canter-Lund H, Lund JWG (1995) Freshwater Algae. Their microscopic world explored. Biopress, BristolGoogle Scholar
  4. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659PubMedCrossRefGoogle Scholar
  5. Coat G, Dion P, Noailles MC, De Reviers B, Fontaine JM, Bergaer-Perrot Y, Loiseaux-De Goër S (1998) Ulva armoricana (Ulvales, Chlorophyta) from the coasts of Brittany (France). II. Nuclear rDNA ITS sequences analysis. Eur J Phycol 33:81–86CrossRefGoogle Scholar
  6. Dan A, Hirosawa A, Makino K, Ohno M, Critchley AT (2002) Observations on the effect of salinity and photon fluency rate on the induction of sporulation and rhizoid formation in the green alga, Enteromorpha prolifera (Müller) J. Agardh (Chlorophyta, Ulvales). Fish Sci 68:1182–1188CrossRefGoogle Scholar
  7. Dan A, Hirosawa A, Makino K, Ohno M, Notoya M (2003) Low temperature storage of young Enteromorpha prolifera (Ulvacea; Chlorophyta). Suisanzoushoku 51:7–14Google Scholar
  8. Edwards DM, Reed RH, Stewart WDP (1988) Osmoacclimation in Enteromorpha intestinalis: long-term effects of osmotic stress on organic solute accumulation. Mar Biol 98:467–476CrossRefGoogle Scholar
  9. Guiry MD, Guiry GM (2007) AlgaeBase version 4.2. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org; searched on 14 March 2007
  10. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  11. Hayden HS, Blomster J, Maggs CA, Silva PC, Stanhope MJ, Waaland JR (2003) Linnaeus was light all along: Ulva and Enteromorpha are not distinct genera. Eur J Phycol 38:277–294CrossRefGoogle Scholar
  12. Hiraoka M, Dan A, Shimada S, Hagihira M, Migita M, Ohno M (2003) Different life histories of Enteromorpha prolifera (Ulvales, Chlorophyta) from four rivers on Shikoku Island. Phycologia 42:275–284CrossRefGoogle Scholar
  13. Hiraoka M, Shimada S (2004) Biology of a special green laver, Ulva prolifera from the Shimanto River. Aquabiology 26:508–515Google Scholar
  14. Horikoshi M, Nagata Y, Sato T, Handa N (1996) Nature in Japan: Sea around Japanese archipelago. Iwanami-shoten, TokyoGoogle Scholar
  15. Kamer K, Fong P (2000) A fluctuating salinity regime mitigates the negative effects of reduced salinity on the estuarine macroalga, Enteromorpha intestinalis (L.) Link. J Exp Mar Biol Ecol 254:53–69PubMedCrossRefGoogle Scholar
  16. Malta EJ, Draisma SGA, Kamermans P (1999) Free-floating Ulva in the southwest Netherlands: species or morphotypes? A morphological, molecular and ecological comparison. Eur J Phycol 34:443–454CrossRefGoogle Scholar
  17. Martins I, Oliveria JM, Flindt MR, Marques JC (1999) The effect of salinity on the growth rate of the macroalgae Enteromorpha intestinalis (Chlorophyta) in the Mondego estuary (west Portugal). Acta Oecol 20:259–265CrossRefGoogle Scholar
  18. Masuda M, Abe T, Saito Y (1992) The conspecificity of Laurencia yendoi Yamada and L. nipponica Yamada (Ceramiales, Rhodophyta). Jpn J Phycol 40:125–133Google Scholar
  19. McAvoy KM, Klug JL (2005) Positive and negative effects of riverine input on the estuarine green alga Ulva intestinalis (syn. Enteromorpha intestinalis)(Linnaeus). Hydobiologia 545:1–9CrossRefGoogle Scholar
  20. Müller OF (1778) Icones plantarum. Florae danicae, vol. 5, fasc 13. . CopenhagenGoogle Scholar
  21. Nakura G (1921) Report of seaweeds, vol 6. Rep Aichi Fish Res Inst 24:1–18Google Scholar
  22. Ohno M (ed) (2004) Biology and technology of economic seaweeds. Uchida-Roukakuho, TokyoGoogle Scholar
  23. Ohno M, Mizutani Y, Taino, Takahashi I (1999) Ecology of the edible green alga Enteromorpha prolifera in Shimanto River, southern Japan. Bull Mar Sci Fish Kochi Univ 19:27–35Google Scholar
  24. Ohno M, Takahashi I (1988) The horizontal and vertical distribution of the food alga Enteromorpha prolifera in Shimanto River, southern Japan. Rep Usa Mar Biol Inst Kochi Univ 10:45–54Google Scholar
  25. Pandey RS, Ohno M (1985) An ecological study of cultivated Enteromorpha. Rep Usa Mar Biol Inst Kochi Univ 7:21–31Google Scholar
  26. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformation 14:817–818CrossRefGoogle Scholar
  27. Pringle JD (1986) Swarmer release and distribution of life-cycle phases of Enteromorpha intestinalis (Chlorophyta) in relation to environmental factors. J Exp Mar Biol Ecol 100:97–112CrossRefGoogle Scholar
  28. Reed RH, Russell G (1979) Adaptation to salinity stress in populations of Enteromorpha intestinalis (L.) Link. Estuar Coast Mar Sci 8:251–258CrossRefGoogle Scholar
  29. Ritchie RJ, Larkum AWD (1985) Potassium transport in Enteromorpha intestinalis: II. Effects of medium composition and metabolic inhibitors. J Exp Bot 36:394–412CrossRefGoogle Scholar
  30. Sherwood AR, Shea TB, Sheath RG (2002) European freshwater Hildenbrandia (Hildenbrandiales, Rhodophyta) has not been derived from multiple invasions from marine habitats. Phycologia 41:87–95CrossRefGoogle Scholar
  31. Shimada S, Masuda M (2003) Reassessment of the taxonomic status of Gelidium subfastigiatum (Gelidiales, Rhodophyta). Phycol Res 51:271–278CrossRefGoogle Scholar
  32. Shimada S, Hiraoka M, Nabata S, Iima M, Masuda M (2003) Molecular phylogenetic analyses of the Japanese Ulva and Enteromorpha (Ulvales, Ulvophyceae), with special reference to the free-floating Ulva. Phycol Res 51:99–108CrossRefGoogle Scholar
  33. Shimada S, Yokoyama N, Masuda M (2007) Genus Ulva (Ulvophyceae, Chlorophyta) in Hokkaido, Japan. Jpn J Bot 82 (in press)Google Scholar
  34. Swofford DL (2002) PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods), Version 4. Sinauer, Sunderland, Mass.Google Scholar
  35. Uchimura T, Faye EJ, Shimada S, Arai S, Inoue T, Nakamura Y (2006) Are-evaluation of the taxonomic status of Halophila euphlebia Makino (Hydrocharitaceae) based on morphological features and ITS sequence data. Bot Mar 49:111–121CrossRefGoogle Scholar
  36. van den Hoek C, Mann DG, Jahns HM (1995) Algae. An Introduction to Phycology. Cambridge University Press, CambridgeGoogle Scholar
  37. Yoshida Y, Shimada S, Yoshinaga K, Nakajima Y (2005) Checklist of marinealgae of Japan. Jpn J Phycol 53:179–228Google Scholar
  38. Yotsukura N, Kawai T, Kawashima S, Ebata H, Ichimura T (2006) Nucleotide sequence diversity of the 5S rDNA spacer in the simple blade kelp genera Laminaria, Cymathaere and Kjellmaniella (Laminariales, Phaeophyceae) from northern Japan. Phycol Res 54:269–279CrossRefGoogle Scholar
  39. Yotsukura N, Kawai T, Motomura T, Ichimura T (2002) Tandem 5S ribosomal RNA genes and spacer region sequences of three Japanese Laminaria species. J Appl Phycol 14:233–239CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Satoshi Shimada
    • 1
  • Naoko Yokoyama
    • 2
  • Shogo Arai
    • 3
  • Masanori Hiraoka
    • 4
  1. 1.Creative Research Initiative SouseiHokkaido UniversitySapporoJapan
  2. 2.Department of Natural History Sciences, Faculty of ScienceHokkaido UniversitySapporoJapan
  3. 3.Marine Algal Research Co., Ltd.FukuokaJapan
  4. 4.Usa Marine Biological InstituteKochi UniversityKochiJapan

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