Abstract
The power of comparative phylogenomic analyses also depends on the amount of data that are included in such studies. We used expressed sequence tags (ESTs) from fish model species as a proof of principle approach in order to test the reliability of using ESTs for phylogenetic inference. As expected, the robustness increases with the amount of sequences. Although some progress has been made in the elucidation of the phylogeny of teleosts, relationships among the main lineages of the derived fish (Euteleostei) remain poorly defined and are still debated. We performed a phylogenomic analysis of a set of 42 of orthologous genes from 10 available fish model systems from seven different orders (Salmoniformes, Siluriformes, Cypriniformes, Tetraodontiformes, Cyprinodontiformes, Beloniformes, and Perciformes) of euteleostean fish to estimate divergence times and evolutionary relationships among those lineages. All 10 fish species serve as models for developmental, aquaculture, genomic, and comparative genetic studies. The phylogenetic signal and the strength of the contribution of each of the 42 orthologous genes were estimated with randomly chosen data subsets. Our study revealed a molecular phylogeny of higher-level relationships of derived teleosts, which indicates that the use of multiple genes produces robust phylogenies, a finding that is expected to apply to other phylogenetic issues among distantly related taxa. Our phylogenomic analyses confirm that the euteleostean superorders Ostariophysi and Acanthopterygii are monophyletic and the Protacanthopterygii and Ostariophysi are sister clades. In addition, and contrary to the traditional phylogenetic hypothesis, our analyses determine that killifish (Cyprinodontiformes), medaka (Beloniformes), and cichlids (Perciformes) appear to be more closely related to each other than either of them is to pufferfish (Tetraodontiformes). All 10 lineages split before or during the fragmentation of the supercontinent Pangea in the Jurassic.
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References
Abascal F, Zardoya R, Posada D (2005) ProtTest: Selection of best-fit models of protein evolution. Bioinformatics 21:2104–2015
Aparicio S, Chapman J, Stupka E, Putnam N, Chia JM, Dehal P, Christoffels A, Rash S, Hoon S, Smit A, Gelpke MD, Roach J, Oh T, Ho IY, Wong M, Detter C, Verhoef F, Predki P, Tay A, Lucas S, Richardson P, Smith SF, Clark MS, Edwards YJ, Doggett N, Zharkikh A, Tavtigian SV, Pruss D, Barnstead M, Evans C, Baden H, Powell J, Glusman G, Rowen L, Hood L, Tan YH, Elgar G, Hawkins T, Venkatesh B, Rokhsar D, Brenner S (2002) Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297:1283–1285
Arratia G (1999) The monophyly of teleostei and stem-group teleosts. In: Arratia G, Schultze HP (eds) Mesozoic fish 2: Systematics and fossil record. Pfeil, Munich
Benton MJ (1993). The fossil record, vol. 2. Chapman and Hall, London
Berg LS (1958) System der rezenten und fossilen Fischartigen und Fische. Verlag der Wissenschaften, Berlin
Cavender (1991) The fossile record of the Cyprinidae. In: Winfield IJ, Nelson JS (eds) Cyprinid fish: Systematics, biology and exploitation. Fish and Fisheries Series 3. Chapman and Hall, London
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 26:262–288
Chen WJ, Orti G, Meyer A (2004) Novel evolutionary relationship among four fish model systems. Trends Genet 20:424–431
Collette BB (2003) Family Belonidae Bonaparte 1832—needlefish. Calif Acad Sci Annot Checklists Fish 16:1–22
Cummings MP, Meyer A (2005) Magic bullets and golden rules: data sampling in molecular phylogenetics. Zoology 108:329–336
Cummings MP, Otto SP, Wakeley J (1995) Sampling properties of DNA sequence data in phylogenetic analysis. Mol Biol Evol 12:814–822
De Pinna MCC (1996) Teleostean monophyly. In: Stiassny MLJ, Parenti LR, Johnson GD (eds) Interrelationships of fish. Academic Press, San Diego
Felsenstein J, (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Felsenstein J (1989) Phylogenetic inference programs (PHYLIP). University of Washington, Seattle, and University Herbarium, University of California, Berkeley
Fink SV, Fink WL (1996) Interrelationships of ostariophysan fish (Teleostei). In: Stiassny MLJ, Parenti LR, Johnson GD (eds) Interrelationships of fish. Academic Press, San Diego
Gadagkar SR, Rosenberg MS, Kumar S (2005) Inferring species phylogenies from multiple genes:Concatenated sequence tree versus consensus gene tree. Mol Dev Evol 304B:64–74
Gerhold D, Caskey CT (1996) It’s the genes! EST access to human genome content. Bioessays 18:973–981
Greenwood PH, Rosen DE, Weitzman SH, Mayers GS (1966) Phyletic studies of teleostean fish, with a provisional classification of living forms. Bull Am Mus Nat Hist 131:339–455
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Helfman GS, Collette BB, Facey DE (1997) The diversity of fish. Blackwell Science, Cambridge, MA
Hillis DM (1998) Taxonomic sampling, phylogenetic accuracy, and investigator bias. Syst Biol 47:3–8
Hillis DM, Pollock DD, McGuire JA, Zwickl DJ (2003) Is sparse taxon sampling a problem for phylogenetic inference? Syst Biol 52:124–126
Hoegg S, Brinkmann H, Taylor JS, Meyer A (2004) Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J Mol Evol 59:190–203
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755
Hughes J, Longhorn SJ, Papadopoulou A, Theodorides K, de Riva A, Mejia-Chang M, Foster PG, Vogler AP (2006) Dense taxonomic EST sampling and its applications for molecular systematics of the Coleoptera (beetles). Mol Biol Evol 23:268–278
Inoue JG, Miya M, Tsukamoto K, Nishida M (2004) Mitogenomic evidence for the monophyly of elopomorph fish (Teleostei) and the evolutionary origin of the leptocephalus larva. Mol Phylogenet Evol 32:274–286
Inoue JG, Miya M, Venkatesh B, Nishida M (2005) The mitochondrial genome of Indonesian coelacanth Latimeria menadoensis (Sarcopterygii: Coelacanthiformes) and divergence time estimation between the two coelacanths. Gene 349:227–235
Ishiguro NB, Miya M, Nishida M (2003) Basal euteleostean relationships: a mitogenomic perspective on the phylogenetic reality of the “Protacanthopterygii.” Mol Phylogenet Evol 27:476–488
Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard V, Jubin C, Castelli V, Katinka M, Vacherie B, Biemont C, Skalli Z, Cattolico L, Poulain J, De Berardinis V, Cruaud C, Duprat S, Brottier P, Coutanceau JP, Gouzy J, Parra G, Lardier G, Chapple C, McKernan KJ, McEwan P, Bosak S, Kellis M, Volff JN, Guigo R, Zody MC, Mesirov J, Lindblad-Toh K, Birren B, Nusbaum C, Kahn D, Robinson-Rechavi M, Laudet V, Schachter V, Quetier F, Saurin W, Scarpelli C, Wincker P, Lander ES, Weissenbach J, Roest Crollius H (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946–957
Johnson GD, Patterson C (1993) Percomorph phylogeny: a survey of acanthomorphs and a new proposal. Bull Mar Sci 52:554–626
Johnson GD, Patterson C (1996) Relationships of lower euteleostean fish. In: Stiassny MLJ, Parenti LR, Johnson GD (eds) Interrelationships of fish. Academic Press, San Diego
Kruiswijk CP, , Hermsen TT, Westphal AH, Savelkoul FJ, Steti RJM (2002). A novel functional class I cineage in Zebrafish (Danio rerio), Carp (Cyprinus carpio), and large Barbus (Barbus intermedius) showing an unusual conservation of the peptide binding domains. J Immunol 169:1936–1947
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5:150–163
Kumar S, Gadagkar SR (2000) Efficiency of the neighborjoining method in reconstructing deep and shallow evolutionary relationships in large phylogenies. J Mol Evol 51:544–553
Kumazawa Y, Yamaguchi M, Nishida M (1999). Mitochondrial molecular clocks and the origin of euteleostean biodiversity: familial radiation of Perciforms may have predated the Cretaceous/Tertiary boundary. In: Kato M (ed) The biology of biodiversity. Springer, Hong Kong
Lake LA, Moore JE (1998) Phylogenetic analysis and comparative genomics. Trends guide to Bioinformatics, Trends Supplement 1998:22–23
Larget B, Simon DL (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16:750–759
Mitchell A, Mitter C, Regier JC (2000) More taxa or more characters revisited: combining data from nuclear protein-encoding genes for phylogenetic analyses of Noctuoidea (Insecta: Lepidoptera). Syst Biol 49:202–224
Miya M, Nishida M (2000) Use of mitogenomic information in teleostean molecular pyhlogenetics: a tree-based exploration under the maximum-parsimony optimality criterion. Mol Phylogenet Evol 17:437–455
Miya M, Takeshima H, Endo H, Ishiguro NB, Inoue JG, Mukai T, Satoh TP, Yamaguchi M, A. Kawaguchi, K. Mabuchi, Shirai SM, Nishida M (2003) Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Mol Phylogenet Evol 26:121–138
Mossel E, Vigoda E (2005) Phylogenetic MCMC algorithms are misleading on mixtures of trees. Science 309:2207–2209
Near TJ, Sanderson MJ (2004). Assessing the quality of molecular divergence time estimates by fossil calibrations and fossil-based model selection. Phil Trans R Soc Lond B Biol Sci 359:1477–1483
Near TJ, Meylan PA, Shaffer HB (2005) Assessing concordance of fossil calibration points in molecular clock studies: an example using turtles. Am Nat 165:137–146
Nelson J (1994) Fish of the world. Wiley, New York
Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217
Renn SCP, Aubin-Horth N, Hofmann HA (2004) Biologically meaningful expression profiling across species using heterologous hybridization to a cDNA microarray. BMC Genomics 5:42
Resetnikov JS (1988) Coregonid fish in recent conditions. Finnish Fish Res 9:11–16
Rokas A, Carroll SB (2005) More genes or more taxa? The relative contribution of gene number and taxon number to phylogenetic accuracy. Mol Biol Evol 22:1337–1344
Rokas A, William BL, King N, Carroll SB (2003) Genome scale approaches to resolving incongruence in molecular phylogenies. Nature 425:798–804
Rokas A, Kruger D, Carroll SB (2005) Animal evolution and the molecular signature of radiations compressed in time. Science 310:1933–1938
Rosen DE (1973) Interrelationships of higher teleostean fish. In: Greenwood PH, Miles RS, Patterson C (eds) Interrelationships of fish. Academic Press, London
Rosen DE, (1974) Phylogeny and zoogeography of salmoniform fish and relationships of Lepidogalaxias salamandroides. Bull Am Mus Nat Hist 153:265–326
Rosen DE, Greenwood PH (1970) Origin of the Weberian apparatus and the relationships of the ostariophysan and gonorynchiform fish. Am Mus Novit 2428:1–25
Rosen DE, Patterson C (1969) The structure and relationships of the paracanthopterygian fish. Bull Am Mus Nat Hist 141:357–474
Rosenberg MS, Kumar S (2001) Incomplete taxon sampling is not a problem for phylogenetic inference. Proc Natl Acad Sci USA 98:10751–10756
Rosenberg MS, Kumar S (2003) Taxon sampling, bioinformatics, and phylogenomics. Syst Biol 52:119–124
Saitoh K, Miya M, Inoue JG, Ishiguro NB, Nishida M (2003) Mitochondrial genomics of ostariophysan fish:Perspectives on phylogeny and biogeography. J Mol Evol 56:464–472
Sanderson MJ (2003) r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19:301–302
Santini F, Tyler JC (2003) A phylogeny of the families of fossil and extant tetraodontiform fish (Acanthomorpha, Tetraodontiformes), Upper Cretaceous to Recent. Zool J Linn Soc 139:565–617
Shevchuk NA, Allard MW (2001) Sources of incongruence among mammalian mitochondrial sequences: COII, COIII, and ND6 genes are main contributors. Mol Phylogenet Evol 21:43–54
Shimodaira H (2002) An approximately unbiased test of phylogenetic tree selection. Syst Biol 51:492–508
Shimodaira H, Hasegawa M (2001) CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17:1246–1247
Simmons MP, Miya M (2004) Efficiently resolving the basal clades of a phylogenetic tree using Bayesian and parsimony approaches: a case study using mitogenomic data from 100 higher teleost fish. Mol Phylogenet Evol 31:351–362
Steinke D, Salzburger W, Meyer A (2004) EverEST—A phylogenomic EST database approach. Phyloinformatics 6:1–4
Stepien CA, Kocher TD (1997) Molecules and morphology in studies of fish evolution. In: Kocher TD, Stepien CA (eds) Molecular systematics of fish. Academic Press, San Diego
Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4.10b. Sinauer Associates, Sunderland, MA
Takezaki N, Figueroa F, Zaleska-Rutczynska Z, Klein J (2003) Molecular phylogeny of early vertebrates: monophyly of the Agnathans as revealed by sequences of 35 genes. Mol Biol Evol 20:287–292
Takezaki N, Figueroa F, Zaleska-Rutczynska Z, Takahata N, Klein J (2004) The phylogenetic relationship of tetrapod, coelacanth, and lungfish revealed by the sequences of forty-four nuclear genes. Mol Biol Evol 21:1512–1524
Taylor JS, Braasch I, Frickey T, Meyer A, van de Peer Y (2003) Genome duplication, a trait shared by 22,000 species of ray-finned fish. Genome Res 13:382–390
Watanabe M, Kobayashi N, Shin-i T, Horiike T, Tateno Y, Kohara Y, Okada N (2004) Extensive analysis of ORF sequences from two different cichlid species in Lake Victoria provides molecular evidence for a recent radiation event of the Victoria species flock identity of EST sequences between Haplochromis chilotes and Haplochromis sp. “Redtailsheller.” Gene 343:263–269
Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699
Wiley EO, Johnson GD, Dimmick WW (2000) The interrelationships of Acantomorph fish: a total evidence approach using molecular and morphological data. Biochem Syst Ecol 28:319–350
Acknowledgments
Support for this study came from the Deutsche Forschungsgemeinschaft (DFG) to A.M., and from the European Community, the Landesstiftung Baden-Württemberg GmbH, and the Center for Junior Research Fellows at the University of Konstanz to W.S. The authors also would like to thank Simone Hoegg, Masaki Miya, Rafael Zardoya, and two anonymous referees for valuable comments on the manuscript.
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Steinke, D., Salzburger, W. & Meyer, A. Novel Relationships Among Ten Fish Model Species Revealed Based on a Phylogenomic Analysis Using ESTs. J Mol Evol 62, 772–784 (2006). https://doi.org/10.1007/s00239-005-0170-8
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DOI: https://doi.org/10.1007/s00239-005-0170-8