Fisheries Science

, Volume 72, Issue 6, pp 1183–1190 | Cite as

Common pearl oysters in China, Japan, and Australia are conspecific: evidence from ITS sequences and AFLP

Article

Abstract

To elucidate the species status of Pinctada fucata in China, P. fucata martensii in Japan and P. imbricata in Australia, one population of each taxon was studied using internal transcribed spacer 1 and 2 (ITS1, and ITS2) and amplified fragment length polymorphism (AFLP) markers. ITS1 and ITS2 were 401–405 and 229–237 bp long, respectively. Twenty-nine ITS1 and 15 ITS2 unique genotypes were obtained from 44 and 34 individuals, respectively, with some genotypes shared by two or three populations. In AFLP analysis, each individual exhibited a distinct phenotype. No population had diagnostic markers. Mean genetic divergences within and among the three populations were very low and overlapped (between-population: 0.7–0.9% for ITS1, 0.9–1.3% for ITS2, and 53.3–55.6% for AFLP; within-population: 0.5–0.9% for ITS1, 0.8–1.2% for ITS2, and 50.4–53.6% for AFLP). Low levels of genetic differentiation were observed among the three populations while the Australian population is partially genetically isolated. Unter an infinite allele model, genetic differentiation among populations was not significant based on a permutation test. Under an infinite site model, most FST values were not significant for ITS data although they were significant for AFLP data. Network analysis using ITS data indicated that individuals from the same population did not cluster together. Analysis of molecular variance (AMOVA) demonstrated that >94% variation was contributed by within-population variation. These findings suggest that the three taxa are conspecific and Pinctada fucata is the correct name.

Key words

amplified fragment length polymorphism (AFLP) internal transcribed spacer (ITS) Pinctada fucata population genetics species status 

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References

  1. 1.
    Li G, Jin Q, Jiang W. Biochemical genetic variation in the pearl oysters, Pinctada fucata and P. chemnitzi. Acta Genetica Sinica 1985; 12: 202–214 (in Chinese).Google Scholar
  2. 2.
    Wang Z. A study of family Pteriidae (Mollusca) in China. Studia Marina Sinica 1978; 14: 101–115 (in Chinese)Google Scholar
  3. 3.
    Wada KT, Komaru A. Color and weight of pearls produced by grafting the mantle tissue from a selected population for white shell color of the Japanese pearl oyster Pinctada fucata martensii (Dunker). Aquaculture 1996; 142: 25–32.CrossRefGoogle Scholar
  4. 4.
    Shirai S. Pearls and Pearl Oysters of the World. Marine Planning Company. Okinawa, Japan, 1994; 1–108.Google Scholar
  5. 5.
    Urban HJ. Culture potential of the pearl oyster (Pinctada imbricata) from the Caribbean. I. Gametogenic activity, growth, mortality and production of a natural population. Aquaculture 2000; 189: 361–373.CrossRefGoogle Scholar
  6. 6.
    Hynd JS. A revision of the Australian pearl-shells, genus Pinctada (Lamellibranchia). Aust. J. Mar. Freshw. Res. 1955; 6: 98–137.CrossRefGoogle Scholar
  7. 7.
    Colgan DJ, Ponder WF. Genetic discrimination of morphologically similar, sympatric species of pearl oysters (Mollusca: Bivalvia: Pinctada) in eastern Australia. Mar. Freshw. Res. 2002; 53: 697–709.CrossRefGoogle Scholar
  8. 8.
    Ranson G. Les espèces d’huîtres perlières du genre Pinctada (biologie de quelques-unes d’entre elles). Institute Royal des Sciences Naturelles de Belgique, Mémoires, deuxième série, fasc. 1961; 67: 1–95, plates i–xlii, (in French).Google Scholar
  9. 9.
    Wada KT. Electrophoretic variants of leucin aminopeptidase of the Japanese pearl oyster Pinctada fucata (Gould). Bull. Natl. Pearl Res. Lab. 1975; 19: 2152–2156.Google Scholar
  10. 10.
    Atsumi T, Komaru A, Okamoto C. Genetic relationship among the Japanese pearl oyster Pinctada fucata martensii and other pearl oysters. Fish Genet. Breed. Sci. 2004; 33: 135–142 (in Japanese with English abstract).Google Scholar
  11. 11.
    Wada KT, Komaru A, Ichimura Y, Kurosaki H. Spawning peak occurs during winter in the Japanese subtropical population of the pearl oyster, Pinctada fucata fucata (Gould. 1850). Aquaculture 1995; 133: 207–214.CrossRefGoogle Scholar
  12. 12.
    Masaoka T, Kobayashi T. Species identification of Pinctada imbricata using intergenic spacer of nuclear ribosomal RNA genes and mitochondrial 1 6S ribosomal RNA gene regions. Fish. Sci. 2005; 71: 837–846.CrossRefGoogle Scholar
  13. 13.
    Wang Z. Suborder Pteriina. In: Editorial Committee of Fauna Sinica, Chinese Academy of Science (ed.), Fauna Sinica, Vol. 31 Science Press, Beijing, China. 2002; 68–98 (in Chinese).Google Scholar
  14. 14.
    Beaumont AR, Khamdan SAA. Electrophoretic and morphometric characters in population differentiation of the pearl oyster, Pinctada radiata (Leach), from around Bahrain. J. Moll. Stud. 1991; 57: 433–441.CrossRefGoogle Scholar
  15. 15.
    Masaoka T, Kobayashi T. Species identification of Pinctada radiata using intergenic spacer of nuclear ribosomal RNA genes and mitochondrial 16S ribosomal gene regions. Fish. Genet. Breed. Sci. 2006; 35: 49–59.Google Scholar
  16. 16.
    Masaoka T, Kobayashi T. Estimation of phylogenetic relationships in pearl oysters (Genus, Pinctada) based on 28S rRNA and ITS sequences. DNA Polymorphism 2003; 11: 76–81.Google Scholar
  17. 17.
    Masaoka T, Kobayashi T. Polymerase chain reaction-based species identification of pearl oyster using nuclear ribosomal DNA internal transcribed spacer regions. Fish. Genet. Breed. Sci. 2004; 33: 101–105.Google Scholar
  18. 18.
    Masaoka T, Kobayashi T. Estimation of phylogenetic relationships in pearl oysters (Mollusks: Bivalvia: Pinctada) used for pearl production based on rRNA gene sequence. DNA Polymorphism 2005; 13: 151–162.Google Scholar
  19. 19.
    Yu DH, Chu KH. Species identity and phylogenetic relationship of pearl oysters in Pinctada (Röding, 1798) based on ITS sequence analysis. Biochem. Syst. Ecol. 2006; 34: 240–250.CrossRefGoogle Scholar
  20. 20.
    Hillis DM, Dixon MT. Ribosomal DNA: Molecular evolution and phylogenetic inference. Quart. Rev. Biol. 1991; 66: 411–453.PubMedCrossRefGoogle Scholar
  21. 21.
    Anderson TJ, Adlard RD. Nucleotide sequence of a rDNA internal transcribed spacer supports synonymy of Saccostrea commercialis and S. glomerata. J. Moll. Stud. 1994; 60: 196–197.CrossRefGoogle Scholar
  22. 22.
    Van Oppen MJH, Willis BL, Van Vugt HWJA, Miller DJ. Examination of species boundaries in the Acropora cervicornis group (Scleractinia, Cnidaria) using nuclear DNA sequence analyses. Mol. Ecol. 2000; 9: 1363–1373.PubMedCrossRefGoogle Scholar
  23. 23.
    Chen CA, Chen CP, Fan TY, Yu JK, Hsieh HL. Nucleotide sequences of ribosomal internal transcribed spacers and their utility in distinguishing closely related Perinereis polychaetes (Annelida; Polychaeta; Nereididae). Mar. Biotechnol. 2002; 4: 17–29.PubMedCrossRefGoogle Scholar
  24. 24.
    López-Piňón MJ, Insua A, Méndez J. Identification of four scallop species using PCR and restriction analysis of the ribosomal DNA internal transcribed spacer region. Mar. Biotechnol. 2002; 4: 495–502.PubMedCrossRefGoogle Scholar
  25. 25.
    Harris DJ, Crandall KA. Intragenomic variation within ITS1 and ITS2 of freshwater crayfishes (Decapoda: Cambaridae): implications for phylogenetic and microsatellite studies. Mol. Biol. Evol. 2000; 17: 284–291.PubMedGoogle Scholar
  26. 26.
    Giannasi N, Thorpe RS, Malhotra A. The use of amplified fragment length polymorphism in determining species trees at fine taxonomic levels: analysis of a medically important snake, Trimeresurus albolabris. Mol. Ecol. 2001; 10: 419–426.PubMedCrossRefGoogle Scholar
  27. 27.
    Ogden R, Thorpe RS. The usefulness of amplified fragment length polymorphism markers for taxon discrimination across graduated fine evolutionary levels in Caribbean Anolis lizards. Mol. Ecol. 2002; 11: 437–445.PubMedCrossRefGoogle Scholar
  28. 28.
    Hwang J-J, Okutani T. Taxonomy and distribution of the genera Pteria and Pinctada (Bivalvia: Pteriidae) in Taiwan. J. Fish. Soc. Taiwan 2003; 30: 199–216.Google Scholar
  29. 29.
    Lamprell K, Healy J. Bivalves of Australia, Vol. 2. Backhuys, Leiden. 1998; 1–102.Google Scholar
  30. 30.
    Matsukuma A. Family Pteriidae, order Pterioida. In: Okutani T (ed.) Encyclopedia of Shellfish. Sekaibunkasha, Tokyo, 2004; 1–288 (in Japanese).Google Scholar
  31. 31.
    Chu KH, Li CP, Ho HY. The first internal transcribed spacer (ITS-1) of ribosomal DNA as a molecular marker for phylogenetic and population analyses in Crustacea. Mar. Biotechnol. 2001; 3: 355–361.PubMedCrossRefGoogle Scholar
  32. 32.
    Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 1995; 23: 4407–4414.PubMedCrossRefGoogle Scholar
  33. 33.
    Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997; 25: 4876–4882.PubMedCrossRefGoogle Scholar
  34. 34.
    Wheeler DL, Chappey C, Lash AE, Leipe DD, Madden TL, Schuler GD, Tatusova TA, Rapp BA. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2000; 28: 10–14.PubMedCrossRefGoogle Scholar
  35. 35.
    Rozas J, Sánchez-Del Barrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003; 19: 2496–2497.PubMedCrossRefGoogle Scholar
  36. 36.
    Schneider S, Roessli D, Excoffier L. Arlequin (Version 2.000): A Software for Population Genetics Data Analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland. 2000.Google Scholar
  37. 37.
    Kumar S, Tamura K, Nei M. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 2004; 5: 150–163.PubMedCrossRefGoogle Scholar
  38. 38.
    Rogers DJ, Tanimoto TT. A computer program for classifying plants. Science 1960; 132: 1115–1118.PubMedCrossRefGoogle Scholar
  39. 39.
    Armstrong JS, Gibbs AJ, Peakall R, Weiller GF. The RAP Distance package Version 1.04 1994. (1 screen). [Cited 2005] Available at http://www.anu.edu.au/BoZo/software/index.html.Google Scholar
  40. 40.
    Hudson RR, Boos DD, Kaplan NL. A statistical test for detecting geographic subdivision. Mol. Biol. Evol. 1992; 9: 138–151.PubMedGoogle Scholar
  41. 41.
    Raymond M, Rousset F. An exact test for population differentiation. Evolution 1995; 49: 1280–1283.CrossRefGoogle Scholar
  42. 42.
    Excoffier L, Smouse PE, Quattro JM. Analysis of molecular variance inferred from metric distrances among DNA haplotypes: applications to human mitochondrial DNA restriction data. Genetics 1992; 13: 479–491.Google Scholar
  43. 43.
    Bandelt HJ, Forster P, Sykes BC, Richards MB. Mitochondrial portraits of human populations. Genetics 1995; 141: 743–753.PubMedGoogle Scholar
  44. 44.
    Polzin T, Daneschmand SV. On Steiner trees and minimum spanning trees in hypergraphs. Opera. Res. Lett. 2003; 31: 12–20.CrossRefGoogle Scholar
  45. 45.
    Fluxus Technology. Free Phylogenetic Network Software: Network 4.1. 2006; (1 screen). [Cited 2006.] Available from URL: http://www.fluxus-engineering.com/sharenet.htm.Google Scholar
  46. 46.
    Kovach WL. A Multivariate Statistical Package for Windows. v3.1 Kovach Computing Services, Pentraeth, UK. 1999.Google Scholar
  47. 47.
    Bandelt HJ, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 1999; 16: 37–48.PubMedGoogle Scholar
  48. 48.
    Beauchamp KA, Powers DA. Sequence variation of the first internal transcribed spacer (ITS-1) of ribosomal DNA in ahermatypic corals from California. Mol. Mar. Biol. Biotechnol. 1996; 5: 357–362.PubMedGoogle Scholar
  49. 49.
    Hedgecock D, Li G, Banks MA, Kain Z. Occurrence of the Kumamoto oyster Crassostrea sikamea in the Ariake Sea, Japan. Mar. Biol. 1999; 133: 65–68.CrossRefGoogle Scholar
  50. 50.
    Vollmer SV, Palumbi SR. Testing the utility of internally transcribed spacer sequences in coral phylogenetics. Mol. Ecol. 2004; 13: 2763–2772.PubMedCrossRefGoogle Scholar
  51. 51.
    Lopez JV, Kersanach R, Rehner SA, Knowlton N. Molecular determination of species boundaries in corals: genetic analysis of the Montastrea annularis complex using amplified length polymorphism and a microsatellite marker. Biol. Bull. (Woods Hole) 1999; 196: 80–93.CrossRefGoogle Scholar
  52. 52.
    Parsons YM, Shaw KL. Species boundaries and genetic diversity among Hawaiian crickets of the genus Laupala identified using amplified fragment length polymorphism. Mol. Ecol. 2001; 10: 1765–1772.PubMedCrossRefGoogle Scholar
  53. 53.
    Kai Y, Nakayama K, Nakabo T. Genetic differences among three colour morphotypes of the black rockfish, Sebastes inermis, inferred from mtDNA and AFLP analyses. Mol. Ecol. 2002; 11: 2591–2598.PubMedCrossRefGoogle Scholar
  54. 54.
    Albertson RC, Markert JA, Danley PD, Kocher TD. Phylogeny of a rapidly evolving clade: The cichlid fishes of Lake Malawi, East Africa. Proc. Natl. Acad. Sci. USA 1999; 96: 5107–5110.PubMedCrossRefGoogle Scholar

Copyright information

© The Japanese Society of Fisheries Science 2006

Authors and Affiliations

  1. 1.South China Sea Fisheries Research InstituteChinese Academy of Fishery SciencesGuangzhou, GuangdongHong Kong, China
  2. 2.Department of BiologyChinese University of Hong KongShatin, N.T.Hong Kong, China

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