Journal of Molecular Evolution

, Volume 63, Issue 6, pp 826–841 | Cite as

Mitogenomic Evolution and Interrelationships of the Cypriniformes (Actinopterygii: Ostariophysi): The First Evidence Toward Resolution of Higher-Level Relationships of the World’s Largest Freshwater Fish Clade Based on 59 Whole Mitogenome Sequences

  • K. Saitoh
  • T. Sado
  • R. L. Mayden
  • N. Hanzawa
  • K. Nakamura
  • M. Nishida
  • M. MiyaEmail author


Fishes of the order Cypriniformes are almost completely restricted to freshwater bodies and number > 3400 species placed in 5 families, each with poorly defined subfamilies and/or tribes. The present study represents the first attempt toward resolution of the higher-level relationships of the world’s largest freshwater-fish clade based on whole mitochondrial (mt) genome sequences from 53 cypriniforms (including 46 newly determined sequences) plus 6 outgroups. Unambiguously aligned, concatenated mt genome sequences (14,563 bp) were divided into 5 partitions (first, second, and third codon positions of the protein-coding genes, rRNA genes, and tRNA genes), and partitioned Bayesian analyses were conducted, with protein-coding genes being treated in 3 different manners (all positions included; third codon positions converted into purine [R] and pyrimidine [Y] [RY-coding]; third codon positions excluded). The resultant phylogenies strongly supported monophyly of the Cypriniformes as well as that of the families Cyprinidae, Catostomidae, and a clade comprising Balitoridae + Cobitidae, with the 2 latter loach families being reciprocally paraphyletic. Although all of the data sets yielded nearly identical tree topologies with regard to the shallower relationships, deeper relationships among the 4 major clades (the above 3 major clades plus Gyrinocheilidae, represented by a single species Gyrinocheilus aymonieri in this study), were incongruent depending on the data sets. Treatment of the rapidly saturated third codon–position transitions appeared to be a source of such incongruities, and we advocate that RY-coding, which takes only transversions into account, effectively removes this likely “noise” from the data set and avoids the apparent lack of signal by retaining all available positions in the data set.


Evolutionary genomics Partitioned Bayesian analysis RY-coding Third codon position Treeness/RCV 



This study has been conducted as a part of the Cypriniformes Tree of Life (CToL) Project ( For donation of the study materials, we sincerely thank T. Asahida, H. L. Bart Jr., J. Bohlen, T. Eros, Y. Fujimoto, H. Imai, Y. P. Kartavtsev, K. Katsura, S. Lavoué, N. E. Mandrak, M. Matsuda, T. Mukai, J. Nakajima, H. Persat, P. Rab, V. V. Sviridov, K. Takahashi, T. Ueda, T. Urano, A. A. Varaksin, E. O. Wiley, and T. Yokoyama. We also thank Y. Kumazawa for advice on data analysis. Critical comments from 2 anonymous reviewers were helpful to improve the manuscript. This study was supported by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology, Japan, and Japan Science for the Promotion of Science (Grants No. 12NP0201, 13556028, 15570090, 15380131, and 17207007).


  1. Adachi J, Hasegawa M (1996) Model of amino acid substitution in proteins encoded by mitochondrial DNA. J Mol Evol 42:459–468PubMedGoogle Scholar
  2. Alves MJ, Collares-Pereira MJ, Dowling TE, Coelho MM (2002) The genetics of maintenance of an all-male lineage in the Squalius alburnoides complex. J Fish Biol 60:649–662Google Scholar
  3. Arai R (1982) A chromosome study on two cyprinid fishes Acrossocheilus labiatus and Psuedorasbora pumila pumila, with notes on Eurasian cyprinids and their karyotypes. Bull Nat Sci Mus Tokyo Ser A (Zool) 8:131–152Google Scholar
  4. Asahida T, Kobayashi T, Saitoh K, Nakayama I (1996) Tissue preservation and total DNA extraction from fish stored at ambient temperature using buffers containing high concentration of urea. Fish Sci 62:727–730Google Scholar
  5. Baird IG, Inthaphaisy V, Kisouvannalath P, Phylavanh B, Mounsouphom B (1999) The fishes of southern Lao. Lao Community Fisheries and Dolphin Protection Project. Ministry of Agriculture and Forestry, Lao PDR, 161 ppGoogle Scholar
  6. Berra T (2001) Freshwater fish distribution. Academic, London, UKGoogle Scholar
  7. Briolay J, Galtier N, Brito RM, Bouvet Y (1998) Molecular phylogeny of Cyprinidae inferred from cytochrome b DNA sequences. Mol Phylogenet Evol 9:100–108PubMedCrossRefGoogle Scholar
  8. Broughton RE, Milam JE, Roe BA (2001) The complete sequence of the zebrafish (Danio rerio) mitochondrial genome and evolutionary patterns in vertebrate mitochondrial DNA. Genome Res 11:1958–1967PubMedGoogle Scholar
  9. Cavender TM, Coburn MM (1992) Phylogenetic relationships of North American Cyprinidae. In: Mayden RL (ed) Systematics historical ecology and North American freshwater fishes. Stanford University Press, Palo Alto, CA, pp 293–327Google Scholar
  10. Chen WJ, Bonillo C, Lecointre G (2003) Repeatability of clades as a criterion of reliability: A case study for molecular phylogeny of Acanthomorpha (Teleostei) with larger number of taxa. Mol Phylogenet Evol 26:262–288PubMedCrossRefGoogle Scholar
  11. Chen X-L, Yue P-Q, Lin R-D (1984) Major groups within the family Cyprinidae and their phylogenetic relationships. Acta Zootaxon Sinica 9:424–440Google Scholar
  12. Chen Y-Y, et al. (1997) Fauna Sinica. Osteichthyes: Cypriniformes II. Science Press, Beijing, ChinaGoogle Scholar
  13. Cheng S, Chang S-Y, Gravitt P, Respess R (1994) Long PCR. Nature 369:684–685PubMedCrossRefGoogle Scholar
  14. Clements MD, Bart HL Jr, Herley DL (2004) Isolation and characterization of two distinct growth hormone cDNAs from the tetraploid smallmouth buffalofish (Ictiobus bubalus). Gen Comp Endocrinol 136:411–418PubMedCrossRefGoogle Scholar
  15. Coburn MM, Cavender TM (1992) Interrelationships of North American cyprinid fishes. In: Mayden RL (ed) Systematics historical ecology and North American freshwater fishes. University Press, Palo Alto, CA, pp 328–373Google Scholar
  16. Cunha C, Mesquita N, Dowling TE, Gilles A, Coelho MM (2002) Phylogenetic relationships of Eurasian and American cyprinids using cytochrome b sequences. J Fish Biol 61:929–944CrossRefGoogle Scholar
  17. Delsuc F, Phillips MJ, Penny D (2003) Technical comment on “Hexapod origins: Monophyletic or paraphyletic?” Science 301:1482PubMedCrossRefGoogle Scholar
  18. Dettai A, Lecointre G (2005) Further support for the clades obtained by multiple molecular phylogenies in the acanthomorph bush. CR Biol 328:674–689Google Scholar
  19. De Rijk P, Caers A, Van de Peer Y, De Wachter R (1998) Database of the structure of large ribosomal subunit RNA. Nucleic Acids Res 26:183–186PubMedCrossRefGoogle Scholar
  20. Durand J-D, Tsigenopoulos CS, Ünlü E, Berrebi P (2002) Phylogeny and biogeography of the family Cyprinidae in the Middle East inferred from cytochrome b DNA: Evolutionary significance of this region. Mol Phylogenet Evol 22:91–100PubMedCrossRefGoogle Scholar
  21. Duyk G, Schmitt K (2001) Fish x 3. Nat Genet 27:8–9PubMedCrossRefGoogle Scholar
  22. Fink SV, Fink WL (1981) Interrelationships of the ostariophysan fishes. Zool J Linn Soc 72:297–353Google Scholar
  23. Fink SV, Fink WL (1996) Interrelationships of ostariophysan fishes. In: Stiassny MLJ, Parenti LR, Johnson GD (eds) Interrelationships of fishes. Academic, San Diego, CA, pp 209–249Google Scholar
  24. Gilles A, Lecointre G, Faure E, Chappaz R, Brun G (1998) Mitochondrial phylogeny of the European cyprinids: implications for their systematics, reticulate evolution, and colonization time. Mol Phylogenet Evol 19:22–33CrossRefGoogle Scholar
  25. Gilles A, Lecointre G, Miquelis A, Loerstcher M, Chappaz R, Brun G (2001) Partial combination applied to phylogeny of European cyprinids using the mitochondrial control region. Mol Phylogenet Evol 19:22–33PubMedCrossRefGoogle Scholar
  26. Hänfling B, Brandl R (2000) Phylogenetics of European cyprinids: Insights from allozymes. J Fish Biol 57:265–276CrossRefGoogle Scholar
  27. Harris PM, Mayden RL (2001) Phylogenetic relationships of major clades of Catostomidae (Teleostei: Cypriniformes) as inferred from mitochondrial SSU and LSU rDNA sequences. Mol Phylogenet Evol 20:225–237PubMedCrossRefGoogle Scholar
  28. Harrison GL, McLenachan PA, Phillips MJ, Slack KE, Cooper A, Penny D (2004) Four new avian mitochondrial genomes help get to basic evolutionary questions in the late Cretaceous. Mol Biol Evol 21:974–983PubMedCrossRefGoogle Scholar
  29. He D, Chen Y, Chen Y, Chen Z (2004a) Molecular phylogeny of the specialized schizothoracine fishes (Teleostei: Cyprinidae), with their implications for the uplift of the Qinghai-Tibetan Plateau. Chinese Sci Bull 49:39–48CrossRefGoogle Scholar
  30. He S, Liu H, Chen Y, Kuwahara M, Nakajima T, Zhong Y (2004b) Molecular phylogenetic relationships of Eastern Asian Cyprinidae (Pisces: Cypriniformes) inferred from cytochrome b sequences. Sci China Ser C Life Sci 47:130–138CrossRefGoogle Scholar
  31. Hillis DM (1998) Taxonomic sampling, phylogenetic accuracy, and investigator bias. Syst Biol 47:3–8PubMedCrossRefGoogle Scholar
  32. Howes GJ (1991) Systematics and biogeography: An overview. In: Winfield IJ, Nelson JS (eds) Cyprinid fishes: Systematics biology and exploitation. Chapman & Hall, London, UK, pp 1–33Google Scholar
  33. Inoue JG, Miya M, Tsukamoto K, Nishida M (2000) Complete mitochondrial DNA sequence of the Japanese sardine, Sardinops melanostictus. Fish Sci 66:924–932CrossRefGoogle Scholar
  34. Inoue JG, Miya M, Aoyama J, Ishikawa S, Tsukamoto K, Nishida M (2001a) Complete mitochondrial DNA sequence of the Japanese eel, Anguilla japonica. Fish Sci 67:118–125CrossRefGoogle Scholar
  35. Inoue JG, Miya M, Tsukamoto K, Nishida M (2001b) Complete mitochondrial DNA sequence of Conger myriaster (Teleostei: Anguilliformes): Novel gene order for vertebrate mitochondrial genomes and the phylogenetic implications for anguilliform families. J Mol Evol 52:311–320Google Scholar
  36. Inoue JG, Miya M, Tsukamoto K, Nishida M (2001c) A mitogenomic perspective on the basal teleostean phylogeny: Resolving higher-level relationships with longer DNA sequences. Mol Phylogenet Evol 20:275–285CrossRefGoogle Scholar
  37. Inoue JG, Miya M, Tsukamoto K, Nishida M (2001d) Complete mitochondrial DNA sequence of the Japanese anchovy, Engraulis japonicus. Fish Sci 67:828–835CrossRefGoogle Scholar
  38. Inoue JG, Miya M, Tsukamoto K, Nishida M (2003) Evolution of the deep-sea gulper eel mitochondrial genomes: Large-scale gene rearrangements originated within the eels. Mol Biol Evol 20:1911–1917Google Scholar
  39. Inoue JG, Miya M, Tsukamoto K, Nishida M (2004) Mitogenomic evidence for the monophyly of elopomorph fishes (Teleostei) and the evolutionary origin of the leptocephalus larva. Mol Phylogenet Evol 32:274–286PubMedCrossRefGoogle Scholar
  40. Ishiguro NB, Miya M, Nishida M (2001) Complete mitochondrial DNA sequence of ayu, Plecoglossus altivelis. Fish Sci 67:474–481CrossRefGoogle Scholar
  41. Ishiguro NB, Miya M, Nishida M (2003) Basal euteleostean relationships: A mitogenomic perspective on the phylogenetic reality of the “Protacanthopterygii.” Mol Phylogenet Evol 27:476–488PubMedCrossRefGoogle Scholar
  42. Ishiguro NB, Miya M, Inoue JG, Nishida M (2005) Sundasalanx (Sundasalangidae) is a progenetic clupeiform, not a closely-related group of salangids (Osmeriformes): Mitogenomic evidence. J Fish Biol 67:561–569CrossRefGoogle Scholar
  43. Johnson GD, Patterson C (1993) Percomorph phylogeny: A survey of acanthomorphs and a new proposal. Bull Mar Sci 52:554–626Google Scholar
  44. Kawaguchi A, Miya M, Nishida M (2001) Complete mitochondrial DNA sequence of Aulopus japonicus (Teleostei: Aulopiformes), a basal Eurypterygii: Longer DNA sequences and higher-level relationships. Ichthyol Res 48:213–223CrossRefGoogle Scholar
  45. Kimmel CB (1989) Genetics and early development of zebrafish. Trends Genet 5:283–288PubMedCrossRefGoogle Scholar
  46. Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J Mol Evol 29:170–179PubMedCrossRefGoogle Scholar
  47. Kottelat M, Britz R, Hui TH, Witte KE (2005) Paedocypris, a new genus of Southeast Asian cyprinid fish with a remarkable sexual dimorphism, comprises the world’s smallest vertebrate. Proc R Soc Lond B Biol Sci 273:895–899CrossRefGoogle Scholar
  48. Kumazawa Y, Nishida M (1993) Sequence evolution of mitochondrial tRNA genes and deep-branch animal phylogenetics. J Mol Evol 37:380–398PubMedCrossRefGoogle Scholar
  49. Kumazawa Y, Azuma Y, Nishida M (2004) Tempo of mitochondrial gene evolution: Can mitochondrial DNA be used to date old divergence? Endocytobiosis Cell Res 15:136–142Google Scholar
  50. Lanyon S (1988) The stochastic mode of molecular evolution: What consequences for systematic investigators? Auk 105:565–573Google Scholar
  51. Larget B, Simon DL (1999) Markov Chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16:750–759Google Scholar
  52. Lavoué S, Miya M, Inoue JG, Saitoh K, Ishiguro NB, Nishida M (2005) Molecular systematics of the gonorynchiform fishes (Teleostei) based on whole mitochondrial genome sequences: Implications for higher-level relationships within the Otocephala. Mol Phylogenet Evol 37:165–177PubMedCrossRefGoogle Scholar
  53. Lê HLV, Lecointre G, Perasso R (1993) A 28S rRNA based phylogeny of the gnathostomes: First steps in the analysis of conflict and congruence with morphologically based cladograms. Mol Phylogenet Evol 2:31–51PubMedCrossRefGoogle Scholar
  54. Leggatt RA, Iwama GK (2003) Occurrence of polyploidy in the fishes. Rev Fish Biol Fish 13:237–246CrossRefGoogle Scholar
  55. Li J, Wan X, He S, Chen Y (2005) Phylogenetic studies of Chinese labeonine fishes (Teleostei: Cyprinidae) based on the mitochondrial 16S rRNA gene. Prog Nat Sci 15:213–219Google Scholar
  56. Liu H, Chen Y (2003) Phylogeny of the East Asian cyprinids inferred from sequences of the mitochondrial DNA control region. Can J Zool 81:1938–1946CrossRefGoogle Scholar
  57. Lôpez JA, Chen W-J, Ortí G (2004) Esociform phylogeny. Copeia 2004:449–464CrossRefGoogle Scholar
  58. Mabuchi K, Miya M, Senou H, Suzuki T, Nishida M (2006) Complete mitochondrial DNA sequence of the Lake Biwa wild strain of common carp (Cyprinus carpio L.): Further evidence for an ancient origin. Aquaculture 257:68–77CrossRefGoogle Scholar
  59. Martin AP, Burg TM (2002) Perils of paralogy: Using HSP70 genes for inferring organismal phylogenies. Syst Biol 51:570–587PubMedCrossRefGoogle Scholar
  60. Mau B, Newton MA, Larget B (1999) Bayesian phylogenetic inference via Markov Chain Monte Carlo methods. Biometrics 55:1–12PubMedCrossRefGoogle Scholar
  61. Miller RE, Buckley TR, Manos PS (2002) An examination of the monophyly of morning glory taxa using Bayesian phylogenetic inference. Syst Biol 51:740–753PubMedCrossRefGoogle Scholar
  62. Minegishi Y, Aoyama J, Inoue JG, Miya M, Nishida M, Tsukamoto K (2005) Molecular phylogeny and evolution of the freshwater eels genus Anguilla based on the whole mitochondrial genome sequences. Mol Phylogenet Evol 34:134–146PubMedCrossRefGoogle Scholar
  63. Mirza RS, Chivers DP (2003) Fathead minnows learn to recognize heterospecific alarm cues they detect in the diet of a known predator. Behaviour 140:1359–1369CrossRefGoogle Scholar
  64. Miya M, Nishida M (1999) Organization of the mitochondrial genome of a deep-sea fish Gonostoma gracile (Teleostei: Stomiiformes): First example of transfer RNA gene rearrangements in bony fishes. Mar Biotechnol 1:416–426PubMedCrossRefGoogle Scholar
  65. Miya M, Nishida M (2000) Use of mitogenomic information in teleostean molecular phylogenetics: A tree-based exploration under the maximum-parsimony optimality criterion. Mol Phylogenet Evol 17:437–455PubMedCrossRefGoogle Scholar
  66. Miya M, Kawaguchi A, Nishida M (2001) Mitogenomic exploration of higher teleostean phylogenies: A case study for moderate-scale evolutionary genomics with 38 newly determined complete mitochondrial DNA sequences. Mol Biol Evol 18:1993–2009PubMedGoogle Scholar
  67. Miya M, Takeshima H, Endo H, Ishiguro NB, Inoue JG, Mukai T, Satoh TP, Yamaguchi M, Kawaguchi A, Mabuchi K, Shirai SM, Nishida M (2003) Major patterns of higher teleostean phylogenies: A new perspective based on 100 complete mitochondrial DNA sequences. Mol Phylogenet Evol 26:121–138PubMedCrossRefGoogle Scholar
  68. Miya M, Saitoh K, Wood R, Nishida M, Mayden RL (2006, in press) New primers for amplifying and sequencing the mitochondrial ND4/ND5 gene region of the Cypriniformes (Actinopterygii: Ostariophysi). Ichthyol Res 53:75–81CrossRefGoogle Scholar
  69. Miya M, Satoh TP, Nishida M (2005) The phylogenetic position of toadfishes (order Batrachoidiformes) in the higher ray-finned fish as inferred from partitioned Bayesian analysis of 102 whole mitochondrial genome sequences. Biol J Linn Soc 85:289–306CrossRefGoogle Scholar
  70. Murakami J, Yamashita Y, Fujitani H (1998) The complete sequence of mitochondrial genome from a gynogenetic triploid “ginbuna” (Carassius auratus longsdorfi). Zool Sci 15:335–337CrossRefGoogle Scholar
  71. Nelson JS (1994) Fishes of the world, third ed. Wiley, NYGoogle Scholar
  72. Okazaki M, Naruse K, Shima A, Arai R (2001) Phylogenetic relationships of bitterings based on mitochondrial 12S ribosomal DNA sequences. J Fish Biol 58:89–106CrossRefGoogle Scholar
  73. Phillips MJ, Penny D (2003) The root of the mammalian tree inferred from whole mitochondrial genomes. Mol Phylogenet Evol 28:171–185PubMedCrossRefGoogle Scholar
  74. Rannala B, Yang Z (1996) Probability distribution of molecular evolutionary trees: A new method of phylogenetic inference. J Mol Evol 43:304–311PubMedGoogle Scholar
  75. Roberts TR (1989) The freshwater fishes of western Borneo (Kalimantan Barat Indonesia). Mem Calif Acad Sci 14:i–xii, 1–210Google Scholar
  76. Roberts TR, Warren TJ (1994) Observations of fishes and fisheries in southern Laos and northeastern Cambodia October 1993–February 1994. Nat Hist Bull Siam Soc 42:87–115Google Scholar
  77. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  78. Saitoh K, Kim I-S, Lee E-H (2004) Mitochondrial gene introgression between spined loaches via hybridogenesis. Zool Sci 21:795–798PubMedCrossRefGoogle Scholar
  79. Saitoh K, Miya M, Inoue JG, Ishiguro NB, Nishida M (2003) Mitochondrial genomics of ostariophysan fishes: Perspectives on phylogeny and biogeography. J Mol Evol 56:464–472PubMedCrossRefGoogle Scholar
  80. Sawada Y (1982) Phylogeny and zoogeography of the superfamily Cobitoidea (Cyprinoidei: Cypriniformes). Mem Fact Fish Hokkaido Univ 28:65–223Google Scholar
  81. Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: Maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504PubMedCrossRefGoogle Scholar
  82. Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116Google Scholar
  83. Siebert DJ (1987) Interrelationships among families of the order Cypriniformes (Teleostei). Doctoral dissertation, The City University of New York, New York, NYGoogle Scholar
  84. Simmons MP, Miya M (2004) Efficiently resolving the basal clades of a phylogenetic tree using Bayesian and parsimony approach: A case study using mitogenomic data from 100 higher teleost fishes. Mol Phylogenet Evol 31:351–362PubMedCrossRefGoogle Scholar
  85. Simons AM, Berentzen P, Mayden RM (2003) Molecular systematics of North American phoxinin genera (Actinopterygii: Cyprinidae) inferred from mitochondrial 12S and 16S ribosomal RNA sequences. Zool J Linn Soc 139:63–80CrossRefGoogle Scholar
  86. Smith GR (1992) Phylogeny and biogeography of the Catostomidae, freshwater fishes of North America and Asia. In: Mayden RL (ed) Systematics historical ecology and North American freshwater fishes. Stanford University Press, Palo Alto, CA, pp 778–826Google Scholar
  87. Smith WL, Wheeler WC (2004) Polyphyly of the mail-cheeked fishes (Teleostei: Scorpaeniformes): evidence from mitochondrial and nuclear sequence data. Mol Phylogenet Evol 32:627–646PubMedCrossRefGoogle Scholar
  88. Swofford DL (2001) PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4.0. Sinauer Associates, MAGoogle Scholar
  89. Talwar PK, Jhingran AG (1991) Inland fishes of India and adjacent countries. Volume 1. Balkema, Rotterdam, The NetherlandsGoogle Scholar
  90. Tang Q, Xiong B, Yang X, Liu H (2005) Phylogeny of the East Asian botiine loaches (Cypriniformes Botiidae) inferred from mitochondrial cytochrome b gene sequences. Hydrobiologia 544:249–258CrossRefGoogle Scholar
  91. Tzeng CS, Hui CF, Shen SC, Huang PC (1992) The complete nucleotide sequence of the Crossostoma lacustre mitochondrial genome: conservation and variations among vertebrates. Nucleic Acids Res 20:4853–4858PubMedGoogle Scholar
  92. Van de Peer Y, Caers A, De Rijk P, De Wachter R (1998) Database on the structure of small ribosomal subunit RNA. Nucleic Acids Res 26:179–182PubMedCrossRefGoogle Scholar
  93. Vrijenhoek RC, Dawley RM, Cole CJ, Bogart JP (1989) A list of the known unisexual vertebrates. In: Dawley RM, Bogart JP (eds) Evolution and ecology of unisexual vertebrates. Bull 466. New York State Museum, New York, NY, pp 19–23Google Scholar
  94. Wiley EO, Johnson GD, Dimmick WW (2000) The interrelationships of acanthomorph fishes: A total evidence approach using molecular and morphological data. Biochem Syst Ecol 28:319–350PubMedCrossRefGoogle Scholar
  95. Wu X, Chen Y, Chen X-L, Chen J-X (1981) Classification and phylogenetic interrelationships among families of suborder Cyprinoidei. Sci China 3:369–376Google Scholar
  96. Yamanoue Y, Miya M, Matsuura K, Katoh M, Sakai H, Nishida M (2004) Mitochondrial genomes and phylogeny of the ocean sunfishes (Tetraodontiformes: Molidae). Ichthyol Res 51:269–273CrossRefGoogle Scholar
  97. Yang Z (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: Approximate methods. J Mol Evol 39:306–314PubMedCrossRefGoogle Scholar
  98. Yang Z, Rannala B (1997) Bayesian phylogenetic inference using DNA sequences: A Markov Chain Monte Carlo method. Mol Biol Evol 14:717–724PubMedGoogle Scholar
  99. Xiao W, Zhang Y, Liu H (2001) Molecular systematics of Xenocyprinae (Teleostei: Cyprinidae): Taxonomy, biogeography, and coevolution of a special group restricted in East Asia. Mol Phylogenet Evol 18:163–173PubMedCrossRefGoogle Scholar
  100. Zaragueta-Bagils R, Lavoué S, Tillier A, Bonillo C, Lecointre G (2002) Assessment of otocephalan and protacanthopterygian concepts in the light of multiple molecular phylogenies. CR Biol 325:1191–1207Google Scholar
  101. Zardoya R, Doadrio I (1998) Phylogenetic relationships of Iberian Cyprinidae: Systematic and biogeographical implications. Proc Roy Soc Lond Ser B 265:1365–1372CrossRefGoogle Scholar
  102. Zardoya R, Doadrio I (1999a) Molecular evidence on the evolutionary and biogeographical patterns of European cyprinids. J Mol Evol 49:227–237CrossRefGoogle Scholar
  103. Zardoya R, Doadrio I (1999b) Phylogenetic relationships of Greek Cyprinidae: Molecular evidence for at least two independent origins of the Greek cyprinid fauna. Mol Phylogenet Evol 13:122–131CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • K. Saitoh
    • 1
  • T. Sado
    • 2
  • R. L. Mayden
    • 3
  • N. Hanzawa
    • 4
  • K. Nakamura
    • 4
  • M. Nishida
    • 5
  • M. Miya
    • 2
    Email author
  1. 1.Tohoku National Fisheries Research InstituteMiyagiJapan
  2. 2.Natural History Museum and InstituteChibaJapan
  3. 3.Department of BiologySaint Louis UniversitySt. LouisUnited States
  4. 4.Department of BiologyYamagata UniversityYamagataJapan
  5. 5.Ocean Research InstituteUniversity of TokyoTokyoJapan

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