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Issue: Vol. 2877 No. 1: 13 May. 2011
Type: Articles
Published: 2011-05-13
DOI: 10.11646/zootaxa.2877.1.1
Page range: 1–40
Abstract views: 30
PDF downloaded: 2

Gill arch and hyoid arch diversity and cypriniform phylogeny: Distributed integration of morphology and web-based tools

University of South Dakota, Vermillion, SD 57069, USA
University of South Dakota, Vermillion, SD 57069, USA
University of Kansas, Lawrence, KS 66045, USA
Russian Academy of Sciences, St. Petersburg, Russian Federation
University of Warmia and Mazury, Faculty of Biology Olsztyn, Poland
John Carroll University, Cleveland, OH 44118, USA (deceased)
Saint Louis University, St. Louis, MO, USA. E-mail: kevin.conway@tamu.edu; current address: Texas A&M University, College Station, TX 77843, USA
Chinese Academy of Sciences, Wuhan, China
Russian Academy of Sciences, St. Petersburg, Russian Federation
Tulane University, New Orleans, LA 70037, USA
University of Minnesota, St. Paul, MN 55108, USA
University of Warmia and Mazury, Faculty of Biology Olsztyn, Poland
Chinese Academy of Sciences, Wuhan, China
Fish Branchial arches Hyoid arch Pharyngeal arches Ostariophysi Cypriniformes Skeleton Ontology

Abstract

Using the multiple tools available to support an online collaborative environment, we surveyed 62 morphological features from the hyoid arch and gill arches of 53 species of cypriniform fishes that matched those sampled in recent molecularanalyses and two sets of outgroup species (‘Saitoh outgroups’ and ‘Basal outgroups’). This is a skeletal region whose variation is considered historically significant within fishes and Cypriniformes in particular, and we review previous work in light of our own. The clarity of description of characters was enhanced by the use of a community reference ontology, the Teleost Anatomy Ontology. Terms, synonyms, and definitions for skeletal features from this region were contributed to this ontology, and links to these terms and relationships are included in our character descriptions. One thousand two hundred sixty-three images of features from this region were linked to ontology terms and deposited in a community image repository, Morphbank; these are linked to the characters described herein. Character data were analyzed using parsimony and Bayesian methods for two sets of outgroups, one of which matched that used in previous molecular analyses. The parsimony results, using either outgroup set, indicated similar higher-level relationships, including a sister group relationship between cyprinids and loaches. A basal trichotomy among Gyrinocheilus, catostomids and cyprinids + loaches was the result of Saitoh outgroup analysis in contrast to a sister group relationship between Gyrinocheilus and catostomids discovered in the Basal outgroup analysis. Interestingly, analyses including basal outgroups recovered a monophyletic Cyprinidae, consistent with all previous studies. Character evolution that supports higher-level nodes of interest in the consensus tree is described. In some respects, it might be a surprise that 62 morphological characters from a small skeletal region for only 53 cypriniform species (out of over 3,200 total species) could provide as much resolution as it does. We expect, however, further phylogenetic resolution as morphological data from across skeleton regions are combined, species sampling is increased, and molecular data are added.

References

  1. Ahnelt, H., Bauer, E., Loffler, J. & Mwebaza-Ndawula (2006) Rastrineobola argentea (Teleostei, Cyprinidae), a small African rasborine with four rows of pharyngeal teeth. Folia Zoologica, 55, 309–314.

    Alberts, B. (2010) Promoting scientific standards. Science, 327, 12.

    Altekar, G., Dwarkadas, S., Huelsenbeck, J.P. & Ronquist, F. (2004) Parallel Metropolis-coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics, 20, 407–415.

    Arratia, G. (1999) The monophyly of Teleostei and stem-group teleosts. Consensus and disagreements. In: G. Arratia & H.-P. Schultze (Eds), Mesozoic Fishes 2- Systematics and Fossil Record. Verlag Dr. F. Pfeil, Munchen, pp. 265–334.

    Arratia, G. (2003) Chapter 1. Catfish Head Skeleton. An Overview. In: G. Arratia, B. G. Kapoor, M. Chardon & R. Diogo (Eds), Catfishes. Science Publishers Inc., Enfield, NH, pp. 3–46.

    Arratia, G. & Schultze, H.P. (1990) The urohyal development and homology within osteichthyans. Journal of Morphology, 203, 247–282.

    Arratia, G. (2010) The Clupeocephala re-visited: Analysis of characters and homologies. Revista Biologia Marina and Oceanografia, 45, 635–657.

    Berra, T.M. (2007) Freshwater Fish Distribution. Chicago: The University of Chicago Press.

    Britz, R. & Conway, K.W. (2009) Osteology of Paedocypris, a miniature and highly developmentally truncated fish (Teleostei: Ostariophysi: Cyprinidae). Journal of Morphology, 270, 389–412.

    Cavender, T.M. & Coburn, M.M. (1992) Phylogenetic relationships of North American Cyprinidae. In: R. L. Mayden (Ed), Systematics, Historical Ecology, and North American Freshwater Fishes. Stanford University Press, Stanford, pp. 293–327.

    Chen, W.-J., Miya, M., Saitoh, K. & Mayden, R.L. (2008) Phylogenetic utility of two existing and four novel nuclear gene loci in reconstructing Tree of Life of ray-finned fishes: The order Cypriniformes (Ostariophysi) as a case study. Gene, 423, 125–134.

    Chen, W.J. & Mayden, R.L. (2009) Molecular systematics of the Cyprinoidea (Teleostei:Cypriniformes), the world’s largest clade of freshwater fishes: Further evidence from six nuclear genes. Molecular Phylogenetics and Evolution, 52, 544–549.

    Chen, Y. (1981) Investigation on the systematic position of Psilorhynchus (Cyprinoidei, Pisces). Acta Hydrobiologica Sinica, 7, 371–376.

    Chu, Y.T. (1935) Comparative studies on the scales and on the pharyngeals and their teeth in Chinese cyprinids, with particular reference to taxonomy and evolution. Biological Bulletin, St. John's University, 2, pp. x + 1–225, pl. I–XXX.

    Clarke, J.A. & Middleton, K.M. (2008) Mosaicism, modules, and the evolution of birds: Results from a Bayesian approach to the study of morphological evolution using discrete character data Systematic Biology, 57, 185–201.

    Coburn, M.M. & Cavender, T.M. (1992) Interrelationships of North American cyprinid fishes. In: R. L. Mayden (Ed), Systematics, Historical Ecology, and North American Freshwater Fishes. Stanford University Press, Stanford, California, pp. 328–373.

    Conway, K.W. (in press) Descriptive osteology of the Genus Psilorhynchus McClelland 1839 with a phylogenetic investigation of its position within the Order Cypriniformes (Teleostei: Ostariophysi: Psilorhynchidae). Zoological Journal of the Linnean Society.

    Conway, K.W., Hirt, M.V., Yang, L., Mayden, R.L. & Simons, A.M. (2010) Cypriniformes: Systematics and Paleontology. In: J. S. Nelson, H.-P. Schultze, M.V.H. Wilson (Eds), Origin and Phylogenetic Interrelationships of Teleosts. Verlag Dr. Freidrich Pfeil, München, pp. 295–316.

    Conway, K.W. & Mayden, R.L. (2007) The gill arches of Psilorhynchus (Ostariophysi: Psilorhynchidae) Copeia, 2007, 267–280.

    Conway, K.W. & Mayden, R.L. (2009) Gill-filament ossifications: a possible morphological synapomorphy uniting the families Balitoridae and Cobitidae (Ostariophysi: Cypriniformes). Journal of Fish Biology, 75, 2839–2844.

    Cubbage, C.C. & Mabee, P.M. (1996) Development of the cranium and paired fins in the zebrafish Danio rerio (Ostariophysi, Cyprinidae). Journal of Morphology, 229, 121–160.

    Dahdul, W.M., Lundberg, J.G., Midford, P.E., Balhoff, J.P., Lapp, H., Vision, T.J., Haendel, M.A., Westerfield, M. & Mabee, P.M. (2010) The Teleost Anatomy Ontology: Anatomical representation for the genomics age. Systematic Biology, 59, 369–383.

    de Pinna, M.C.C. (1993) Higher-level Phylogeny of Siluriformes (Teleostei: Ostariophysi), with a New Classification of the Order. City University of New York, New York.

    de Pinna, M. & di Dario, D. (2010) The branchial arches of the primitive clupeomorph Denticeps clupeoides, and their phylogenetic implication (Clupeiformes, Denticipitidae). In: J.S. Nelson, H.-P. Schultze, M.V.H. Wilson (Eds), Origin and Phylogenetic Interrelationships of Teleosts. Verlag Dr. Freidrich Pfeil, Muenchen, pp. 251–268.

    Dingerkus, G. & Uhler, D. (1977) Enzyme clearing of alcian blue stained whole small vertebrates for demonstration of cartilage. Stain Technology, 52, 229–232.

    Eastman, J.T. (1977) The pharyngeal bones and teeth of catostomid fishes. American Midland Naturalist, 97, 68–88.

    Egge, J.J.D. & Simons, A.M. (2009) Molecules, morphology, missing data and the phylogenetic position of a recently extinct madtom catfish (Actinopterygii: Ictaluridae). Zoological Journal of the Linnean Society, 155, 60–75.

    Engeman, J.M., Aspinwall, N. & Mabee, P.M. (2009) Development of the pharyngeal arch skeleton in Catostomus commersonii (Teleostei: Cypriniformes). Journal of Morphology, 270, 291–305.

    Fink, S.V. & Fink, W.L. (1981) Interrelationships of the ostariophysan fishes (Teleostei). Zoological Journal of the Linnean Society, 72, 297–353.

    Fink, S.V. & Fink, W.L. (1996) Interrelationships of ostariophysan fishes (Teleostei). In: M. L. J. Stiassny, L. R. Parenti & G. D. Johnson (Eds), Interrelationships of Fishes. Academic Press, San Diego, pp. 209–249.

    Golubtsov, A.S., Dzerjinskii, K.F. & Prokofiev, A.M. (2005) Four rows of pharyngeal teeth in an aberrant specimen of the small African barb Barbus paludinosus (Cyprinidae): novelty or atavistic alteration? Journal of Fish Biology, 67, 286–291.

    Harrington, R.W. (1955) The osteocranium of the American cyprinid fish Notropis bifrenatus, with an annotated synonymy of teleost skull bones. Copeia, 1955, 267–290.

    He, S., Mayden, R.L., Wang, X., Wang, W., Tang, K.L., Chen, W.J. & Chen, Y. (2008) Molecular phylogenetics of the family Cyprinidae (Actinopterygii: Cypriniformes) as evidenced by sequence variation in the first intron of S7 ribosomal protein-coding gene: further evidence from a nuclear gene of the systematic chaos in the family. Molecular Phylogenetics and Evolution, 46, 818–829.

    Hora, S.L. (1925) Notes on the fishes of the Indian Museum. XII. The systematic position of cyprinoid genus Psilorhynchus McClelland. Records of the Indian Museum, 27, 457–460.

    Howes, G.J. (1981) Anatomy and phylogeny of the Chinese major carps Ctenopharyngodon Steind., 1866 and Hypophthalmichthys Blkr.,1860. Bulletin of the British Museum of Natural History (Zoology), 41, 1–52.

    Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755.

    Johnson, G.D. & Patterson, C. (1996) Relationships of lower euteleostean fishes. In: M. L. J. Stiassny, L. R. Parenti & G. D. Johnson (Eds), Interrelationships of Fishes. Academic Press, San Diego, pp. 251–332.

    Johnson, G.D. & Patterson, C. (1997) The gill-arches of gonorynchiform fishes. South African Journal of Science, 93, 594–600.

    Maddison, W.P. & Maddison, D.R. (2009) Mesquite: a modular system for evolutionary analysis. Version 2.6.

    Mayden, R., Chen, W.J., Bart, H.L., Doosey, M.H., Simons, A.M., Tang, K.L., Wood, R.M., Agnew, M.K., Yang, L., Hirt, M. V., Clements, M.D., Saitoh, K., Sado, T., Miya, M. & Nishida, M. (2009) Reconstructing the phylogenetic relationships of the earth’s most diverse clade of freshwaterfishes–order Cypriniformes (Actinopterygii:Ostariophysi): A case study using multiple nuclear loci and the mitochondrial genome. Molecular Phylogenetics and Evolution, 51, 500–514.

    Mayden, R.L. & Chen, W.J. (2010) The world's smallest vertebrate species of the genus Paedocypris: a new family of freshwater fishes and the sister group to the world's most diverse clade of freshwater fishes (Teleostei: Cypriniformes). Molecular Phylogenetics and Evolution, 57, 152–175.

    Mayden, R.L., Tang, K.L., Wood, R.M., Chen, W.-J., Agnew, M.K., Conway, K.W., Yang, L., Simons, A.M., Bart, H.L., Harris, P.M., Li, J., Wang, X., Saitoh, K., He, S., Liu, H., Chen, Y., Nishida, M. & Miya, M. (2008) Inferring the Tree of Life of the order Cypriniformes the earth's most diverse clade of freshwater fishes: Implications of varied taxon and character sampling. Journal of Systematics and Evolution, 46, 424–438.

    McAllister, D.E. (1968) Evolution of branchiostegals and classification of teleostome fishes. Bulletin of the National Museum of Canada, Biological Series, 221, 1–239.

    Morphbank (2011) Biological Imaging (http://www.morphbank.net/, 11 February 2011). Florida State University, Department of Scientific Computing, Tallahassee, FL 32306-4026 USA.

    Nakajima, T. (1987) Development of pharyngeal dentition in the cobitid fishes, Misgurnus anguillicaudatus and Cobitis biwae, with a consideration of evolution of cypriniform dentitions. Copeia, 1987, 208–213.

    Nalbant, T.T. (2002) Sixty million years of evolution. Part one: Family Botiidae (Pisces: Ostariophysi: Cobitoidea). Travaux du Muséum National d'Histoire Naturelle "Grigore Antipa", 44, 309–344.

    Nelson, G.J. (1969) Gill arches and the phylogeny of fishes, with notes on the classification of vertebrates. Bulletin of the American Museum of Natural History, 141, 475–552.

    Nelson, J.S. (2006) Fishes of the World. Hoboken, NJ: John Wiley & Sons, Inc.

    O'Leary, M.A. & Kaufman, S.G. (2007) MorphoBank 2.5: Web application for morphological phylogenetics and taxonomy.

    Patterson, C. (1977) Cartilage bones, dermal bones and membrane bones, or the exoskeleton versus the endoskeleton. In: S. M. Andrews, R. S. Miles and A. D. Walker (Ed), Problems in Vertebrate Evolution. Academic Press, London, pp. 77–121.

    Potthoff, T. (1984) Clearing and staining techniques. In: H. G. Moser (Ed), Ontogeny and Systematics of Fishes. Special Publication 1, American Society of Ichthyologists and Herpetologists, Lawrence, Kansas, pp. 35–37.

    Ramaswami, L.S. (1952) Skeleton of cyprinoid fishes in relation to phylogenetic studies. II. The systematic position of Psilorhynchus McClelland. Proceedings of the National Institute of Sciences of India, 18, 141–150.

    Rojo, A.L. (1991) Dictionary of Evolutionary Fish Osteology: CRC Press.

    Ronquist, F. & Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.

    Rüber, L., Kottelat, M., Tan, H.H., Ng, P.K. & Britz, R. (2007) Evolution of miniaturization and the phylogenetic position of Paedocypris, comprising the world's smallest vertebrate. BMC Evolutionary Biology, 7.

    Saitoh, K., Sado, T., Mayden, R.L., Hanzawa, N., Nakamura, K. & Nishida, M. (2006) 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 Journal of Molecular Evolution, 63, 826–841.

    Sawada, Y. (1982) Phylogeny and zoogeography of superfamily Cobitoidea (Cyprinoidei, Cypriniformes). Memoirs of the Faculty of Fisheries, Hokkaido University, 28, 65–223.

    Siebert, D.H. (1987) Interrelationships among families of the order Cypriniformes (Teleostei). Unpublished Ph.D. dissertation.City University of New York, New York, New York.

    Šlechtová, V., Bohlen, J. & Tan, H.H. (2007) Families of Cobitoidea (Teleostei; Cypriniformes) as revealed from nuclear genetic data and the position of the mysterious genera Barbucca, Psilorhynchus, Serpenticobitis and Vaillantella. Molecular Phylogenetics and Evolution, 44, 1358–1365.

    Smith, G.R. (1992) Phylogeny and biogeography of the Catostomidae, freshwater fishes of North America and Asia. In: R. L. Mayden (Ed), Systematics, HIstorical Ecology, and North American Freshwater Fishes. Stanford University Press, Stanford, CA, pp. 778–826.

    Springer, V.G. & Johnson, G.D. (2004) Study of the dorsal gill-arch musculature of teleostome fishes, with special reference to the actinopterygii. Bulletin of the Biological Society of Washington, 1–260.

    Takahasi, N. (1925) On the homology of the cranial muscles of the cypriniform fishes. Journal of Morphology and Physiology, 40, 1–109.

    Tang, K.L., Agnew, M.K., Hirt, M.V., Sado, T., Schneider, L.M., Freyhof, J., Sulaiman, Z., Swartz, E., Vidthayanon, C., Miya, M., Saitoh, K., Simons, A.M., Wood, R.M. & Mayden, R.L. (2010) Systematics of the subfamily Danioninae (Teleostei: Cypriniformes: Cyprinidae). Molecular Phylogenetics and Evolution, 57, 189–214.

    Taylor, W. & Van Dyke, G. (1985) Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium, 9, 107–119.

    Wiens, J.J., Fetzner Jr., J.W., Parkinson, C.L. & Reeder, T.W. (2005) Hylid frog phylogeny and sampling strategies for speciose clades. Systematic Biology, 54, 778–807.

    Winterbottom, R. (1974) A Descriptive Synonymy of the Striated Muscles of the Teleostei. Journal of the Academy of Natural Sciences Philadelphia, 125, 225–317.

    Wu, X., Chen, Y., Chen, X. & Che, J. (1981) A taxonomic system and phylogenetic relationship of the families of suborder Cyprinoidei (Pisces). Scientia Sinica, 24, 563–572.