Abstract
Cyprinidae is the biggest family of freshwater fish, but the phylogenetic relationships among its higher-level taxa are not yet fully resolved. In this study, we used the nuclear recombination activating gene 2 and the mitochondrial 16S ribosomal RNA and cytochrome b genes to reconstruct cyprinid phylogeny. Our aims were to (i) demonstrate the effects of partitioned phylogenetic analyses on phylogeny reconstruction of cyprinid fishes; (ii) provide new insights into the phylogeny of cyprinids. Our study indicated that unpartitioned strategy was optimal for our analyses; partitioned analyses did not provide better-resolved or -supported estimates of cyprinid phylogeny. Bayesian analyses support the following relationships among the major monophyletic groups within Cyprinidae: (Cyprininae, Labeoninae), ((Acheilognathinae, ((Leuciscinae, Tincinae), Gobioninae)), Xenocyprininae). The placement of Danioninae was poorly resolved. Estimates of divergence dates within the family showed that radiation of the major cyprinid groups occurred during the Late Oligocene through the Late Miocene. Our phylogenetic analyses improved our understanding of the evolutionary history of this important fish family.
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References
Nelson J S, ed. Fishes of the World. New York: John Wiley and Sons Inc., 2006
Howes G J. Systematics and biogeography: an overview. In: Winfield I J, Nelson J S, eds. Cyprinid Fishes: Systematics, Biology and Exploitation. London: Chapman and Hall, 1991. 1–33
Hensel K. Review of the classification and of the opinions on the evolution of Cyprinoidei (Eventognathi) with an annotated list of genera and subgenera described since 1921. Annot Zool Bot, 1970, 57: 1–45
Chen Y Y, ed. Fauna Sinica, Osteichthys: Cypriniformes (Part II). Beijing: Science Press, 1998
Gosline W A. Unbranched dorsal-fin rays and subfamily classification in the fish family Cyprinidae. Occas Pap Mus Zool Univ Mich, 1978, 684: 1–21
Chu Y T. Comparative studies on the scales and on the pharyngeals and their teeth in Chinese Cyprinids, with particular reference to taxonomy and evolution. Biol Bull St John’s Univ (Shanghai), 1935, 2: 1–225
Wu X, ed. The Cyprinid Fishes of China (in Chinese). Shanghai: Shanghai Science and Technology Press, 1964
Chen X L, Yue P Q, Lin R D. Major groups within the family Cyprinidae and their phylogenetic relationships. Acta Zootaxon Sin, 1984, 9: 424–440
Cavender T M, Coburn M M. Phylogenetic relationships of North American Cyprinidae. In: Mayden R L, ed. Systematics, Historical Ecology and North American Freshwater Fishes. Stanford, California: Stanford University Press, 1992. 293–327
Zardoya R, Doadrio I. Molecular evidence on the evolutionary and biogeographical patterns of European Cyprinids. J Mol Evol, 1999, 49: 227–237
Briolay J, Galtier N, Brito R M, et al. Molecular phylogeny of Cyprinidae inferred from cytochrome b DNA sequences. Mol Phylogenet Evol, 1998, 9: 100–108
Gilles A, Lecointre G, Faure E, et al. Mitochondrial phylogeny of the European Cyprinids: implications for their systematics, reticulate evolution, and colonization time. Mol Phylogenet Evol, 1998, 10: 132–143
Gilles A, Lecointre G, Miquelis A, et al. Partial combination applied to phylogeny of European Cyprinids using the mitochondrial control region. Mol Phylogenet Evol, 2001, 19: 22–33
Zardoya R, Doadrio I. Phylogenetic relationships of Iberian Cyprinids: systematic and biogeographical implications. Proc R Soc B Biol Sci, 1998, 265: 1365–1372
Durand J D, Tsigenopoulos C S, Unlu E, et al. Phylogeny and biogeography of the family Cyprinidae in the Middle East inferred from cytochrome b DNA-evolutionary significance of this region. Mol Phylogenet Evol, 2002, 22: 91–100
Hanfling B, Brandl R. Phylogenetics of European Cyprinids: insights from allozymes. J Fish Biol, 2000, 57: 265–276
Fu C Z, Wu J H, Chen J K, et al. Freshwater fish biodiversity in the Yangtze River Basin of China: patterns, threats and conservation. Biodivers Conserv, 2003, 12: 1649–1685
Cunha C, Mesquita N, Dowling T E, et al. Phylogenetic relationships of Eurasian and American Cyprinids using cytochrome b sequences. J Fish Biol, 2002, 61: 929–944
He S, Liu H, Chen Y, et al. Molecular phylogenetic relationships of Eastern Asian Cyprinidae (Pisces: Cypriniformes) inferred from cytochrome b sequences. Sci China Ser C-Life Sci, 2004, 47: 130–138
Liu H, Chen Y. Phylogeny of the East Asian Cyprinids inferred from sequences of the mitochondrial DNA control region. Can J Zool, 2003, 81: 1938–1946
Ronquist F, Huelsenbeck J P. Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 2003, 19: 1572–1574
Stamatakis A. Raxml-Vi-Hpc: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 2006, 22: 2688–2690
McGuire J A, Witt C C, Altshuler D L, et al. Phylogenetic systematics and biogeography of hummingbirds: Bayesian and maximum likelihood analyses of partitioned data and selection of an appropriate partitioning strategy. Syst Biol, 2007, 56: 837–856
Fink S V, Fink W L. Interrelationships of the ostariophysan fishes (Teleostei). Zool J Linn Soc, 1981, 72: 297–353
Wang X, Wang J, He S, et al. The complete mitochondrial genome of the Chinese hook snout carp Opsariichthys bidens (Actinopterygii: Cypriniformes) and an alternative pattern of mitogenomic evolution in vertebrate. Gene, 2007, 399: 11–19
Sambrook J, Fritsch E, Maniatis T, ed. Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press, 1989
Xiao W H, Zhang Y P, Liu H Z. Molecular systematics of Xenocyprinae (Teleostei: Cyprinidae): taxonomy, biogeography, and coevolution of a special group restricted in East Asia. Mol Phylogenet Evol, 2001, 18: 163–173
Li J, Wang X, Kong X, et al. Variation patterns of the mitochondrial 16s rRNA gene with secondary structure constraints and their application to phylogeny of Cyprinine fishes (Teleostei: Cypriniformes). Mol Phylogenet Evol, 2008, 47: 472–487
Lovejoy N R, Collette B B. Phylogenetic relationships of new world needlefishes (Teleostei: Belonidae) and the biogeography of transitions between marine and freshwater habitats. Copeia, 2001, 2: 324–338
Thompson J D, Gibson T J, Plewniak F, et al. The Clustal X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res, 1997, 25: 4876–4882
De Rijk P, Wuyts J, Van de Peer Y, et al. The European large subunit ribosomal RNA database. Nucleic Acids Res, 2000, 28: 177–178
Gutell R R, Gray M W, Schnare M N. A compilation of large subunit (23s and 23s-like) ribosomal RNA structures. Nucleic Acids Res, 1993, 21: 3055–3074
Gutell R R, Fox G E. A compilation of large subunit RNA sequences presented in a structural format. Nucleic Acids Res, 1988, 16: r175–269
Swofford D L. Paup*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0b10. 2003
Posada D, Crandall K A. Modeltest: testing the model of DNA substitution. Bioinformatics, 1998, 14: 817–818
Posada D, Buckley T R. Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol, 2004, 53: 793–808
Lemmon A R, Moriarty E C. The importance of proper model assumption in Bayesian phylogenetics. Syst Biol, 2004, 53: 265–277
Huelsenbeck J, Rannala B. Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Syst Biol, 2004, 53: 904–913
Wilgenbusch J, Warren D, Swofford D. Awty: A System for Graphical Exploration of Mcmc Convergence in Bayesian Phylogenetic Inference. 2004
Kass R E, Raftery A E. Bayes factors. J Am Stat Assoc, 1995, 90: 773–795
Nylander J A A, Ronquist F, Huelsenbeck J P, et al. Bayesian phylogenetic analysis of combined data. Syst Biol, 2004, 53: 47–67
Schwarz G. Estimating the dimension of a model. Ann Stat, 1978, 6: 461–464
Minin V, Abdo Z, Joyce P, et al. Performance-based selection of likelihood models for phylogeny estimation. Syst Biol, 2003, 52: 674–683
Abdo Z, Minin V N, Joyce P, et al. Accounting for uncertainty in the tree topology has little effect on the decision-theoretic approach to model selection in phylogeny estimation. Mol Biol Evol, 2005, 22: 691–703
Sullivan J, Abdo Z, Joyce P, et al. Evaluating the performance of a successive-approximations approach to parameter optimization in maximum-likelihood phylogeny estimation. Mol Biol Evol, 2005, 22: 1386–1392
Raftery A. Hypothesis testing and model selection. In: Gilks W R, Spiegelhalter D J, Richardson S, eds. Markov Chain Monte Carlo in Practice. London: Chapman and Hall, 1996. 163–187
Castoe T A, Sasa M M, Parkinson C L. Modeling nucleotide evolution at the mesoscale: the phylogeny of the neotropical pitvipers of the Porthidium group (Viperidae: Crotalinae). Mol Phylogenet Evol, 2005, 37: 881–898
Castoe T A, Parkinson C L. Bayesian mixed models and the phylogeny of pitvipers (Viperidae: Serpentes). Mol Phylogenet Evol, 2006, 39: 91–110
Brandley M C, Schmitz A, Reeder T W. Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Syst Biol, 2005, 54: 373–390
Shimodaira H. An approximately unbiased test of phylogenetic tree selection. Syst Biol, 2002, 51: 492–508
Sanderson M J. A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol Biol Evol, 1997, 14: 1218–1231
Sanderson M J. R8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics, 2003, 19: 301–302
Felsenstein J. Phylip (Phylogeny Inference Package) Version 3.5 C. 1993
Cavender T M. The fossil record of the Cyprinidae. In: Winfield I J, Nelson J S, eds. Cyprinid Fishes: Systematics, Biology and Exploitation. London: Chapman and Hall, 1991. 34–54
Hierholzer E, Mörs T. Cypriniden-Schlundzähne (Osteichthyes: Teleostei) aus dem Tertiär von Hambach (Niederrheinische Bucht, Nw-Deutschland). Palaeontographica, Abteilung A, 2003, 269: 1–38
Sytchevskaya E. Freshwater Ichthyofauna of the Neogene of Mongolia. Tr Sovm Sovets-Mongol Paleontol Eksped, 1989, 39: 1–144
Schulz-Mirbach T, Reichenbacher B. Reconstruction of oligocene and neogene freshwater fish faunas-an actualistic study on cypriniform otoliths. Acta Palaeontol Pol, 2006, 51: 283–304
Liu H, Su T. Pliocene fishes from the Yushe Basin, Shanxi. Vertebr Palasiat, 1962, 6: 1–25
Tang K L, Agnew M K, Hirt M V, et al. Systematics of the subfamily Danioninae (Teleostei: Cypriniformes: Cyprinidae). Mol Phylogenet Evol, 2010, 57: 189–214
Chen W J, Mayden R L. Molecular systematics of the Cyprinoidea (Teleostei: Cypriniformes), the world’s largest clade of freshwater fishes: further evidence from six nuclear genes. Mol Phylogenet Evol, 2009, 52: 544–549
Wang X, Li J, He S. Molecular evidence for the monophyly of East Asian groups of Cyprinidae (Teleostei: Cypriniformes) derived from the nuclear recombination activating gene 2 sequences. Mol Phylogenet Evol, 2007, 42: 157–170
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Wang, X., Gan, X., Li, J. et al. Cyprinid phylogeny based on Bayesian and maximum likelihood analyses of partitioned data: implications for Cyprinidae systematics. Sci. China Life Sci. 55, 761–773 (2012). https://doi.org/10.1007/s11427-012-4366-z
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DOI: https://doi.org/10.1007/s11427-012-4366-z