Marine Biology

, Volume 147, Issue 2, pp 367–379 | Cite as

Genetic divergence between two morphologically similar varieties of the kuruma shrimp Penaeus japonicus

Research Article

Abstract

The kuruma shrimp Penaeus japonicus is widely distributed throughout the Indo-West Pacific. Two morphologically similar varieties, I and II, are recognized from the South China Sea. The two varieties are characterized by different color banding patterns on the carapace, but there are no distinct differences in morphometric traits between them based on measurement of 13 characters. Sequence data and restriction profiles of the mitochondrial genes reveal that these two varieties represent distinct clades, with sequence divergences of about 1% (473 bp) in 16S rRNA, 6–7% (504 bp) in cytochrome oxidase I, and 16–19% (470 bp) in the control region. Analysis of amplified fragment length polymorphism confirms that the two varieties are genetically distinct. We also investigated the geographical distribution of the two varieties in the western Pacific by analyzing specimens collected from Japan and Singapore. Shrimps from Japan and Singapore have been found to belong to varieties I and II, respectively, suggesting that the two varieties have different geographical distribution. Phylogenetic study reveals that the two varieties are more closely related to each other than to the other phylogenetically related Penaeus species. Results from this study suggest the occurrence of two cryptic species in the kuruma shrimp P. japonicus.

Keywords

Amplify Fragment Length Polymorphism Amplify Fragment Length Polymorphism Marker Amplify Fragment Length Polymorphism Analysis Kuruma Shrimp Rostrum Length 
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

Acknowledgements

Sincere thanks are extended to P.K.L. Ng (National University of Singapore), K. Tanaka (Kyorin University, Japan), Y.H. Yung (The Chinese University of Hong Kong), J. Wong and P.H. Wong (Princess Margaret Hospital, Hong Kong) for collecting specimens. We are indebted to T.Y. Chan (National Taiwan Ocean University) for examination of the specimens and discussion on this project. We also thank J. Tong (Institute of Hydrobiology, Chinese Academy of Sciences), Y.K. Tam, C.P. Li, and W. Lau (The Chinese University of Hong Kong) for technical assistance, and C.K. Wong (The Chinese University of Hong Kong) and an anonymous reviewer for constructive comments on the manuscript. The work described in this article was fully supported by a grant from the Research Grants Council, Hong Kong Special Administrative Region (HKSAR), China (Project no. CUHK4157/01 M). The experiments complied with the current laws of HKSAR.

References

  1. Adams DC, Rohlf FJ (2000) Ecological character displacement in Plethodon: biomechanical differences found from a geometric morphometric study. Proc Natl Acad Sci U S A 97:4106−4111Google Scholar
  2. Aubert H, Lightner DV (2000) Identification of genetic populations of the Pacific blue shrimp Penaeus stylirostris of the Gulf of California, Mexico. Mar Biol 137:875−885CrossRefGoogle Scholar
  3. Avise JC, Ball RM Jr (1990) Principles of genealogical concordance in species concepts and biological taxonomy. Oxford Surv Evol Biol 7:45−67Google Scholar
  4. Avsar D (1994) A stock differentiation study of the sprat (Sprattus sprattus phalericus Risso) off the southern coast of the Black Sea. Fish Res 19:363−378Google Scholar
  5. Benzie JAH (1998) Penaeid genetics and biotechnology. Aquaculture 164:23−47Google Scholar
  6. Benzie JAH, Ballment E, Forbes AT, Demetriades NT, Sugama K, Haryanti Moria S (2002) Mitochondrial DNA variation in Indo-Pacific populations of the giant tiger prawn, Penaeus monodon. Mol Ecol 11:2553–2569Google Scholar
  7. Birky CW Jr, Maruyama T, Fuerst P (1983) An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics 103:513−527PubMedGoogle Scholar
  8. Bouchon D, Souty-Grosset C, Raimond R (1994) Mitochondrial DNA variation and markers of species identity in two penaeid shrimp species: Penaeus monodon Fabricus and P. japonicus Bate. Aquaculture 127:131−144Google Scholar
  9. Bruce AJ (1978) The evolution and zoogeography of shallow-water tropical shrimps. Informative Series, Department of Scientific and Industrial Research, New Zealand 137:337−355Google Scholar
  10. Camin JH, Sokal RR (1965) A method for deducing branching sequences in phylogeny. Evolution 19:311−326Google Scholar
  11. Chan TY (1998) Shrimps and prawns. In: Carpenter KE, Niem VH (eds) The living marine resources of the western central Pacific, vol 2. Food and Agriculture Organization of the United Nations, Rome, pp 851−917Google Scholar
  12. Chassard-Bouchaud C (1965) L’adaptation chromatiwue chez les Natantia (crustacés decapods). Cah Biol Mar 6:469−576Google Scholar
  13. Chu KH, Li CP, Tam YK, Lavery S (2003) Application of mitochondrial control region in population genetic studies of the shrimp Penaeus. Mol Ecol Notes 3:120−122Google Scholar
  14. Cracraft J (1983) Species concepts and speciation analysis. Current Ornithol 1:159−187Google Scholar
  15. Cracraft J (1987) Species concepts and the ontology of evolution. Biol Philos 2:329−346Google Scholar
  16. Duda TF Jr, Palumbi SR (1999) Population structure of the black tiger prawn, Penaeus monodon, among western Indian Ocean and western Pacific populations. Mar Biol 134:705−710Google Scholar
  17. Farris JS, Kallersjo M, Kluge AG, Bult C (1995) Constructing a significant test for incongruence. Syst Biol 44:570−572Google Scholar
  18. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368−376PubMedGoogle Scholar
  19. Felsenstein J (2002) Phylogeny inference package (PHYLIP) v3.6a3. University of Washington, SeattleGoogle Scholar
  20. Fukami H, Budd AF, Levitan DR, Jara J, Kersanach R, Knowlton N (2004) Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution 58:324−337Google Scholar
  21. Futuyma DJ (1998) Evolutionary biology, 3rd edn. Sinauer, Sunderland, MAGoogle Scholar
  22. Gusmão J, Lazoski C, Solé-Cava AM (2000) A new species of Penaeus (Crustacea: Penaeidae) revealed by allozyme and cytochrome oxidase I analysis. Mar Biol 137:435−446Google Scholar
  23. Hetzel DJS, Crocos PJ, Davis GP, Moore SS, Preston NC (2000) Response to selection and heritability for growth in the kuruma prawn, Penaeus japonicus. Aquaculture 181:215−223Google Scholar
  24. Hualkasin W, Sirimontaporn P, Chotigeat W, Querci J, Phongdara A (2003) Molecular phylogenetic analysis of white prawns species and the existence of two clades in Penaeus merguiensis. J Exp Mar Biol Ecol 296:1–11Google Scholar
  25. Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132:583–589PubMedGoogle Scholar
  26. Jerry DR, Preston NP, Crocos PJ, Keys S, Meadows JRS, Li Y (2004) Parentage determination of kuruma shrimp Penaeus (Marsupenaeus) japonicus using microsatellite markers (Bate). Aquaculture 235: 237–247Google Scholar
  27. Keiper FJ, McConchie R (2000) An analysis of genetic variation in natural populations of Sticherus flabellatus [R. Br. (St John)] using amplified fragment length polymorphism (AFLP) markers. Mol Ecol 9:571−581Google Scholar
  28. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111−120PubMedGoogle Scholar
  29. Klinbunga S, Penman DJ, McAdrew BJ, Tassanakajon A (1999) Mitochondrial DNA diversity in three populations of the giant tiger shrimp Penaeus monodon. Mar Biotechnol 1:113−121Google Scholar
  30. Knowlton N (1986) Cryptic and sibling species among the decapod Crustacea. J Crustac Biol 6:356−363Google Scholar
  31. Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Syst 24:189−216Google Scholar
  32. Knowlton N, Keller BD (1983) A new, sibling species of snapping shrimp associated with the Caribbean sea anemone Bartholomea annulata. Bull Mar Sci 33:353−362Google Scholar
  33. Knowlton N, Weigt LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proc R Soc Lond B Biol Sci 265:2257−2263CrossRefGoogle Scholar
  34. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetic analysis software. Bioinformatics 17:1244−1245CrossRefPubMedGoogle Scholar
  35. Lavery S, Chan TY, Tam YK, Chu KH (2004) Phylogenetic relationships and evolutionary history of the shrimp genus Penaeus s. l. derived from mitochondrial DNA. Mol Phylogenet Evol 31:39–49Google Scholar
  36. Li Y, Byrne K, Miggiano E, Whan V, Moore S, Keys S, Crocos P, Preston N, Lehnert S (2003) Genetic mapping of the kuruma prawn Penaeus japonicus using AFLP markers. Aquaculture 219:143–156CrossRefGoogle Scholar
  37. Mayr E (1942) Systematics and the origin of species from the viewpoint of a zoologist. New York, Columbia University PressGoogle Scholar
  38. McElroy D, Moran P, Bermingham E, Kornfield I (1991) REAP: the restriction enzyme analysis package, ver 4.0. Department of Zoology, University of Maine, OronoGoogle Scholar
  39. McMillen-Jackson AL, Bert TM (2004) Genetic diversity in the mtDNA control region and population structure in the pink shrimp Farfantepenaeus duorarum. J Crustac Biol 24:101−109Google Scholar
  40. Merril CR, Switzer RC, Keuren ML van (1979) Trace polypeptides in cellular extracts and human body fluid detected by two-dimensional electrophoresis and a highly sensitive silver stain. Proc Natl Acad Sci U S A 76:4335−4339Google Scholar
  41. Mink DG, Sites JW Jr (1996) Species limits, phylogenetic relationships, and origins of viviparity in the Scalaris complex of the lizard genus Sceloporus (Phrynosomatidae). Herpetologica 52:551−557Google Scholar
  42. Nei M (1977) F-statistics and analysis of gene diversity in subdivided populations. Ann Hum Genet 41:225−233Google Scholar
  43. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  44. Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonuclease. Proc Natl Acad Sci U S A 76:5269−5273Google Scholar
  45. Nei M, Tajima F (1981) DNA polymorphism detectable by restriction endonucleases. Genetics 97:145−163PubMedGoogle Scholar
  46. Palumbi SR, Benzie J (1991) Large mitochondrial DNA differences between morphologically similar penaeid shrimp. Mol Mar Biol Biotechnol 1:27−34Google Scholar
  47. Pérez Farfante I (1969) Western Atlantic shrimp of genus Penaeus. Fish Bull U S 67:461−591Google Scholar
  48. Pérez Fartante I, Kensley B (1997) Penaeoid and sergestoid shrimps and prawns of the world. Keys and diagnoses for the families and genera. Mém Mus Natl Hist Nat Paris 175:1−233Google Scholar
  49. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817−818CrossRefPubMedGoogle Scholar
  50. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280−1283Google Scholar
  51. Rodríguez F, Oliver JL, Marín A, Medina JR (1990) The general stochastic model of nucleotide substitution. J Theor Biol 142:485–501PubMedGoogle Scholar
  52. Roff DA, Bentzen P (1989) The statistical analysis of mitochondrial DNA polymorphism: χ2 and the problems of small samples. Mol Biol Evol 6:539−545PubMedGoogle Scholar
  53. Rosenberry B (2001) World shrimp farming 2001. Shrimp News International, San DiegoGoogle Scholar
  54. Rzhetsky A, Nei M (1992) A simple method for estimating and testing minimum-evolution trees. Mol Biol Evol 9:945−967Google Scholar
  55. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406−425PubMedGoogle Scholar
  56. Salini JP, Moore LE (1985) Taxonomy of the greentail prawn, Metapenaeus bennettae, and the western school prawn, M. dalli. In: Rothlisberg PC, Hill BJ, Staples DJ (eds) Second Australian national prawn seminar. Cleveland, pp 95−103Google Scholar
  57. Salmon M, Ferris SD, Johnston D, Hyatt G, Whitt GS (1979) Behavioral and biochemical evidence for species distinctiveness in the fiddler crabs. Uca speciosa and U. spinicarpa. Evolution 33:182−191Google Scholar
  58. Sbordoni V, DeMatthaeis E, Cobolli Sbordoni M, La Rosa G, Mattoccia M (1986) Bottleneck effects and the depression of genetic variability in hatchery stocks of Penaeus japonicus (Crustacea, Decapoda). Aquaculture 57:239−251Google Scholar
  59. Schneider S, Roessli O, Excoffier L (2000) Arlequin ver 2.000: a software for genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  60. Seki S, Agresti JJ, Gall GAE, Taniguchi N, Bernie M (1999) AFLP analysis of genetic diversity in three populations of ayu Plecoglossus altivelis. Fish Sci 65:888−892Google Scholar
  61. Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:652–701Google Scholar
  62. Sturmbauer C, Levinton J, Christy J (1996) Molecular phylogeny analysis of fiddler crabs: test of the hypothesis of increasing behavioral complexity in evolution. Proc Natl Acad Sci U S A 93:10855–10857Google Scholar
  63. Sugaya T, Ikeda M, Mori H, Taniguchi N (2002) Inheritance mode of microsatellite DNA markers and their use for kinship estimation in kuruma prawn Penaeus japonicus. Fish Sci 68:299−305Google Scholar
  64. Supungul P, Sootanan P, Klinbunga S, Kamonrat W, Jarayabhand P, Tassanakajon A (2000) Microsatellite polymorphism and the population structure of the black tiger shrimp (Penaeus monodon) in Thailand. Mar Biotechnol 2:339–347Google Scholar
  65. Swofford DL (2000) PAUP*: phylogenetic analysis using parsimony (*and other methods), ver 4. Sinauer, Sunderland, MAGoogle Scholar
  66. Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Proc Natl Acad Sci U S A 22:4673–4680Google Scholar
  67. Tirmizi NW (1971) Marsupenaeus, a new subgenus of Penaeus Fabricius, 1798 (Decapoda, Natantia). Pak J Zool 3:193–194Google Scholar
  68. Tong JG, Chan TY, Chu KH (2000) A preliminary phylogenetic analysis of Metapenaeopsis (Decapoda: Penaeidae) based on mitochondrial DNA sequences of selected species form the Indo-West Pacific. J Crustac Biol 20:543–551Google Scholar
  69. Tzeng TD, Yeh SY (1999) Analysis of the morphometric characters of the kuruma shrimp (Penaeus japonicus) in the East China Sea and the Taiwan Strait. J Fish Soc Taiwan 26:203−212Google Scholar
  70. Vos P, Hogers R, Bleeker M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407−4414PubMedGoogle Scholar
  71. Wang ZY, Jayasankar P, Khoo SK (2000) AFLP fingerprinting reveals genetic variability in common carp stocks from Indonesia. Asian Fish Sci 13:139−147Google Scholar
  72. Wang ZY, Tsoi KH, Chu KH (2004) Application of AFLP technology in genetic and phylogenetic analysis of penaeid shrimp. Biochem Syst Ecol 32:399−407Google Scholar
  73. Yu HP, Chan TY (1986) The illustrated penaeoid prawns of Taiwan. Southern Materials Center, TaiwanGoogle Scholar
  74. Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice Hall, LondonGoogle Scholar
  75. Tzeng TD, Yeh SY (2002) Multivariate allometric comparisons for kuruma shrimp (Penaeus japonicus) off Taiwan. Fish Res 59:279–288Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Department of BiologyThe Chinese University of Hong KongHong KongChina
  2. 2.Fisheries CollegeJimei UniversityXiamen, FujianChina

Personalised recommendations