Advertisement

Marine Biology

, Volume 153, Issue 4, pp 709–721 | Cite as

Molecular phylogenies help resolve taxonomic confusion with Asian Crassostrea oyster species

  • Kimberly S. Reece
  • Jan F. Cordes
  • Julie B. Stubbs
  • Karen L. Hudson
  • Elizabeth A. Francis
Research Article

Abstract

Identification of oyster species is still largely based on phenotypic characters that are highly plastic. Prompted by the proposed introduction of the Asian oyster species Crassostrea ariakensis into the Chesapeake Bay region of the U.S.A., this study uses molecular genetic information to understand the taxonomic framework surrounding C. ariakensis and to confidently distinguish among various sympatric oyster species. Putative samples of C. ariakensis and other species of cupped oysters from across Asia were collected and phylogenetic analyses were conducted on DNA sequences of both nuclear (ITS-1) and mitochondrial (COI) regions. Trees generated based on the two independent molecular datasets were highly congruent, and indicate that many oysters collected for this study as C. ariakensis were originally misidentified. Results also indicate that C. ariakensis, C. hongkongensis and C. nippona are distinct, but closely related species. There is strong support in both analyses for a close relationship between C. gigas and C. sikamea, as well as between C. belcheri and C. gryphoides, and between C. iredalei and C. madrasensis. The parsimony analyses based on these DNA markers, however, did not provide evidence to support C. angulata as a distinct species from C. gigas. Overall, the results emphasize the need for rigorous species identification, and additional extensive and intensive sampling to more accurately determine relationships among Crassostrea species, define their geographic distributions, and establish existing sympatry patterns.

Keywords

Monophyletic Clade Nest Clade Oyster Species Jackknife Support Crassostrea Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This research was supported by Virginia Sea Grant College Program award NA96RG0025, and NOAA/NMFS awards NA04NMF4570432, and NA03NMF4570379. The authors gratefully acknowledge the valuable contributions made by all of the individuals involved in collecting samples for this study including Q. Zhang, S. Allen, A. Wang, X. Wu, D. Bushek, X. Guo, I. Kornfeld, S. Klinbunga, A. Robinson, R. Carnegie, K. Johnson, H. Que, E. Burreson, F. O’Beirn, M. Luckenbach, B. Innes, J. Higano, H. An and X. Du. Numerous individuals made excellent technical contributions to this study including Q. Zhang, G. Scott, J. Xiao, W. Ribeiro and J. Moss. The translation of Lischke’s description of O. rivularis Gould was done by B.A. Cordes. We thank M. Siddall for valuable assistance in locating historical documents and for his very helpful critical reading of the document. These experiments were conducted in compliance with the laws of the USA and all collections were done in compliance with laws of the respective countries from which samples were obtained. This is VIMS contribution #2872.

References

  1. Ahmed M (1971) Oyster species of West Pakistan. Pakist J Zool 3:229–236Google Scholar
  2. Ahmed M (1975) Speciation in living oysters. Adv Mar Biol 13:357–397CrossRefGoogle Scholar
  3. Anderson TJ, Adlard RD (1994) Nucleotide sequence of a rDNA internal transcribed spacer supports synonymy of Saccostrea commercialis and S. glomerata. J Moll Stud 60:196–197CrossRefGoogle Scholar
  4. Banks MA, McGoldrick DJ, Borgeson W, Hedgecock D (1994) Gametic incompatibility and genetic divergence of Pacific and Kumamoto oysters, Crassostrea gigas and C. sikamea. Mar Biol 121:127–135CrossRefGoogle Scholar
  5. Bernard FR (1983) Catalogue of the living Bivalvia of the Eastern Pacific Ocean: Bering Strait to Cape Horn. Canadian Special Publication of Fisheries and Aquatic Sciences 61, 102 ppGoogle Scholar
  6. Boudry P, Heurtebise S, Collet B, Cornette F, Gérard A (1998) Differentiation between populations of the Portuguese oyster, Crassostrea angulata (Lamark) and the Pacific oyster, Crassostrea gigas (Thunberg), revealed by mtDNA RFLP analysis. J Exp Mar Biol Ecol 226:279–291CrossRefGoogle Scholar
  7. Boudry P, Heurtebise S, Lapègue S (2003) Mitochondrial and nuclear DNA sequence variation of presumed Crassostrea gigas and Crassostrea angulata specimens: a new oyster species in Hong Kong? Aquaculture 228:15–25CrossRefGoogle Scholar
  8. Brock V (1990) Intergeneric distances between Ostrea, Crassostrea, and Saccostrea, studied by means of crossed immunoelectrophoresis. Mar Ecol Prog Ser 68:59–63CrossRefGoogle Scholar
  9. Buroker NE, Hershberger WK, Chew KK (1979) Population genetics of the family Ostreidae. II. Interspecific studies of the genera Crassostrea and Saccostrea. Mar Biol 54:171–184CrossRefGoogle Scholar
  10. Carriker MR, Gaffney PM (1996) A catalogue of selected species of living oysters (Ostreacea) of the world. In: Kennedy VS, Newell RIE, Eble AF (eds) The eastern oyster Crassostrea virginica. Maryland Sea Grant College, College Park, MD, pp 1–18Google Scholar
  11. Coan EV, Valentich Scott PH, Bernard FR (2000) Superfamily Ostreoidea. In: Bivalve seashells of western North America: marine bivalve mollusks from Arctic Atlantic to Baja California. Santa Barbara Museum of Natural History, Santa Barbara, CA, pp 212–219Google Scholar
  12. Cordes JF, Stubbs JB, Reece KS (2005) Phylogenetics and species identification of Crassostrea oysters based on sequences and PCR-RFLP analyses of ITS-1 and COI markers. J Shellfish Res 24:647Google Scholar
  13. Dungan CF, Reece KS (2006) In vitro propagation of two Perkinsus spp. parasites from Japanese Manila clams Venerupis philippinarum, and description of Perkinsus honshuensis n. sp. J Eukaryot Microbiol 53:316–326CrossRefGoogle Scholar
  14. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299Google Scholar
  15. Fujita T (1913) Nihon suisan dobutsugaku (Japanese aquatic fisheries animals), vol 2. Shokabu, Tokyo, 292 pGoogle Scholar
  16. Gaffney PM, Allen SK Jr (1993) Hybridization among Crassostrea species: a review. Aquaculture 116:1–13CrossRefGoogle Scholar
  17. Glude, JB (1971) Identification of oysters of the South Pacific Islands. National Marine Fisheries Service, Seattle, WA: MimeoGoogle Scholar
  18. Gould AA (1861) Descriptions of shells collected in the North Pacific Exploring Expedition under Captains Ringgold and Rodgers. Proc Boston Soc Nat Hist 8:14–40Google Scholar
  19. Harry HW (1985) Synopsis of the supraspecific classification of living oysters (Bivlavia: Gryphaeidae and Ostreidae). Veliger 28:121–158Google Scholar
  20. Hedgecock D, Li G, Banks MA, Kain Z (1999) Occurence of the Kumamoto oyster Crassostrea sikamea in the Ariake Sea, Japan. Mar Biol 133:65–68CrossRefGoogle Scholar
  21. Huvet A, Lapègue S, Magoulas A, Boudry P (2000) Mitochondrial and nuclear DNA phylogeography of Crassostrea angulata, the Portuguese oyster endangered in Europe. Conserv Genet 1:252–262CrossRefGoogle Scholar
  22. Huvet A, Fabioux C, McCombie H, Lapègue S, Boudry P (2004) Natural hybridization between genetically differentiated populations of Crassostrea gigas and C. angulata highlighted by sequence variation in flanking regions of a microsatellite locus. Mar Ecol Prog Ser 272:141–152CrossRefGoogle Scholar
  23. ICES (2005) ICES code of practice on the introductions and transfers of marine organisms 2005. 30 ppGoogle Scholar
  24. Imai T, Sakai S (1961) Study of breeding of Japanese oysters. Tohoku J Agricul Res 12:125–171Google Scholar
  25. Klinbunga S, Ampayup P, Tassanakajon A, Jarayabhand P, Yoosukh W (2001) Genetic diversity and molecular markers of cupped oysters (genera Crassostrea, Saccostrea and Striostrea) in Thailand revealed by randomly amplified polymorphic DNA analysis. Mar Biotechnol 3:133–144CrossRefGoogle Scholar
  26. Klinbunga S, Khamnamtong N, Tassanakajon A, Puanglarp N, Jarayabhand P (2003) Molecular genetic identification tools for three commercially cultured oysters (Crassostrea belcheri, Crassostrea iredalei, and Saccostrea cucullata) in Thailand. Mar Biotechnol 5:27–36CrossRefGoogle Scholar
  27. Lam K, Morton B (2003) Mitochondrial DNA and morphological identification of a new species of Crassostrea (bivalvia: Ostreidae) cultured for centuries in the Pearl River Delta, Hong Kong, China. Aquaculture 228:1–13CrossRefGoogle Scholar
  28. Lam K, Morton B (2004) The oyster of Hong Kong (Bivlavia: Ostreidae and Gryphaeidae). Raffles Bull Zool 52:11–28Google Scholar
  29. Lapègue S, Boutet I, Leitao A, Heurtebise S, Garcia P, Thiriot-Quievreux C, Boudry P (2002) Trans-Atlantic distribution of a mangrove oyster species revealed by 16S mtDNA and karyological analyses. Biol Bull 202:232–242CrossRefGoogle Scholar
  30. Lapègue S, Batista FM, Heurtebise S, Yu Z, Boudry P (2004) Evidence for the presence of the Portuguese oyster, Crassostrea angulata, in northern China. J Shellfish Res 23:759–763Google Scholar
  31. Lawrence DR (1995) Diagnosis of the genus Crassostrea (Bivalvia, Ostreidae). Malacologia 36:185–202Google Scholar
  32. Lee SY, Park DW, An HS, Kim SH (2000) Phylogenetic relationship among four species of Korean oysters based on mitochondrial 16S rDNA and CO1 gene. Kor J Biol Sci 16:203–211Google Scholar
  33. Littlewood DTJ (1994) Molecular phylogenetics of cupped oysters based on partial 28S rRNA gene sequences. Mol Phylogenet Evol 3:211–229CrossRefGoogle Scholar
  34. Lischke CR (1869–1874) Ostrea rivularis Gould. In: Dunker W (ed) Japanische Meeres-Conchylien, mis besonderer Rücksicht aus die gegraphische Verbreitung derselben. Novitates Conchologicae Suppl 4, 3 pts in 1Google Scholar
  35. López-Flores I, de la Herrán R, Garrido-Ramos MA, Boudry P, Ruiz-Rejón C, Ruiz-Rejón M (2004) The molecular phylogeny of oysters based on satellite DNA related to transposons. Gene 339:181–188CrossRefGoogle Scholar
  36. Mathers NF, Wilkins NP, Walne PR (1974) Phosphoglucose isomerase and esterase phenotypes in Crassostrea angulata and C. gigas. Biochem Syst Ecol 2:93–96CrossRefGoogle Scholar
  37. Mattiucci S, Villani F (1983) Allozyme study in oysters classified as Crassostrea gigas (Thunberg, 1793) and Crassostrea angulata (Lamark, 1819) (Mollusca: Ostreidae). Parasitologia 25:21–27Google Scholar
  38. Menzel RW (1974) Portuguese and Japanese oysters are the same species. J Fish Res Board Can 31:453–456CrossRefGoogle Scholar
  39. Moss JA, Burreson EM, Cordes JF, Dungan CF, Brown GD, Wang A, Wu A, Reece KS (2007) Pathogens in Crassostrea ariakensis and other Asian oyster species: implications for non-native oyster introduction to Chesapeake Bay. Dis Aqua Org (in press)Google Scholar
  40. O’Foighil D, Gaffney PM Hilbish TJ (1995) Differences in mitochondrial 16S ribosomal gene sequences allow discrimination among American Crassostrea virginica (Gmelin) and Asian C. gigas (Thunberg), C. ariankensis (Wakiya). J Exp Mar Bio Ecol 192:221–220CrossRefGoogle Scholar
  41. O’Foighil D, Gaffney PM, Wilbur AE, Hilbish TJ (1998) Mitochondrial cytochrome oxidase I gene sequences support an Asian origin for the Portuguese oyster Crassostrea angulata. Mar Biol 131:497–503CrossRefGoogle Scholar
  42. O’Foighil D, Marshall BA, Hilbish TJ, Pino MA (1999) Trans-Pacific range extension by rafting is inferred for the flat oyster Ostrea chilensis. Biol Bull 196:122–126CrossRefGoogle Scholar
  43. Reece KS, Stokes NA (2003) Molecular analysis of a haplosporidian parasite from cultured New Zealand abalone (Haliotis iris Martyn, 1784). Dis Aquat Org 53:61–66CrossRefGoogle Scholar
  44. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467CrossRefGoogle Scholar
  45. Stenzel HB (1971) Oysters. In: Moore KK (ed) Treatise on invertebrate paleontology. Part N, vol. 3, Mollusca 6, Geol. America Inc. and the University of Kansas, Boulder, pp N953–N1224Google Scholar
  46. Sudradjat A, Yankson K, Moyse J, Skibinski DOF (1995) Genetic approach to taxonomy of oysters, Ostrea, Crassostrea, and Saccostrea. Proc Internat Sym Biotechnol: Appl Aquaculture 10:239–252CrossRefGoogle Scholar
  47. Swofford DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods). vs 4.0b10. Sinauer Associates, SunderlandGoogle Scholar
  48. Tack JF, Berghe E, Polk PH (1992) Ecomorphology of Crassostrea cucullata (Born, 1778) (Ostreidae) in a mangrove creek (Gazi, Kenya). Hydrobiologia 247:109–117CrossRefGoogle Scholar
  49. Thompson JD, Higgins DG, Gibson TJ (1994) Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  50. Torigoe K (1981) Oysters in Japan. J Science-Hiroshima University Series B Div 1 29:291–481Google Scholar
  51. Wang H, Guo X, Zhang G, Zhang F (2004) Classification of jinjiang oysters Crassostrea rivularis (Gould, 1861) from China, based on morphology and phylogenetic analysis. Aquaculture 242:137–155CrossRefGoogle Scholar
  52. Wang H, Guo X (2007) Identification of Crassostrea ariakensis and related oysters by multiplex species-specific PCR. J Shellfish Res (in press)Google Scholar
  53. Yu Z, Kong X, Zhang L, Guo X, Xiang J (2003) Taxonomic status of four Crassostrea oysters from China as inferred from mitochondrial DNA sequences. J Shellfish Res 22:31–38Google Scholar
  54. Zhang Q, Allen SK Jr, Reece KS (2005) Genetic variation in wild and hatchery stocks of the Suminoe oyster (Crassostrea ariakensis) assessed by PCR-RFLP and microsatellite markers. Mar Biotechnol 7:588–599CrossRefGoogle Scholar
  55. Zhou M, Allen Jr SK (2003) A review of published work on Crassostrea ariakensis. J Shellfish Res 22:1–20Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Kimberly S. Reece
    • 1
  • Jan F. Cordes
    • 1
  • Julie B. Stubbs
    • 1
  • Karen L. Hudson
    • 1
  • Elizabeth A. Francis
    • 1
  1. 1.Virginia Institute of Marine Science, School of Marine ScienceThe College of William and MaryGloucester PointUSA

Personalised recommendations