Skip to main content Skip to main navigation menu Skip to site footer
Type: Articles
Published: 2012-12-14
Page range: 281–303
Abstract views: 45
PDF downloaded: 59

Molecular systematics of western North American cyprinids (Cypriniformes: Cyprinidae)

Department of Biology, Saint Louis University, 3507 Laclede Avenue, St. Louis, MO 63103, USA
Department of Biology and Curator of Fishes, Monte L. Bean Life Science Museum, Brigham Young University, Provo, UT 84602, USA
School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501, USA
Department of Biology, Saint Louis University, 3507 Laclede Avenue, St. Louis, MO 63103, USA
Fish Western Clade Phoxinins sequence analyses Gila lineage controversial taxonomy

Abstract

The phylogenetic or evolutionary relationships of species of Cypriniformes, as well as their classification, is in a era offlux. For the first time ever, the Order, and constituent Families are being examined for relationships within aphylogenetic context. Relevant findings as to sister-group relationships are largely being inferred from analyses of bothmitochondrial and nuclear DNA sequences. Like the vast majority of Cypriniformes, due to an overall lack of anyphylogenetic investigation of these fishes since Hennig’s transformation of the discipline, changes in hypotheses ofrelationships and a natural classification of the species should not be of surprise to anyone. Basically, for most taxa noproperly supported phylogenetic hypothesis has ever been done; and this includes relationships with reasonable taxonand character sampling of even families and subfamilies. As such, like others, many western North American cyprinidgenera have had a controversial taxonomic and systematic history.Our effort to better understand the evolutionary history of this artificial geographic grouping of species (Western)surveyed taxa and characters broadly. We analyzed 127 taxa (71 species) from 36 genera, including representative taxafrom all 22 western genera hypothesized to form the Western Clade sensu Coburn and Cavender (1992). Our evaluationalso included additional sampling from a heterogeneous array of species from the western genera Algansea, Gila,Lepidomeda, Ptychocheilus and Siphateles. Resulting phylogenetic inferences, based on one mitochondrial and threenuclear genes (mtDNA: cytb; nDNA: Rag1, Rhod, S7), consistently resolved a well-supported Western Clade, but oneinclusive of Chrosomus erythrogaster. This taxon, always formed the sister group to the extant species of Gila plus 10other western genera. Our Western Clade is qualitatively different from that of prior studies and does not include thegenera Agosia, Algansea, Iotichthys, Lepidomeda, Meda, Mylocheilus, Plagopterus, Pogonichthys, Rhinichthys, Tiarogaor Yuriria. All of these taxa were, however, included in Coburn and Cavender´s (1992) Western Clade. Our broader-scalesurvey and increased character sampling were always resolved these latter taxa within one of two different major clades:the OPM Clade (sensu Mayden 1989) and the Creek Chub—Plagopterin Clade (sensu Simons et al. 2003). Ourhypothesized Western Clade places Orthodon sister to a Western Chub-Pikeminnow Clade also inclusive of Acrocheilus,Eremichthys, Gila, Hesperoleucus, Lavinia, Moapa, Mylopharodon, Ptychocheilus, Relictus and Siphateles. The lattertaxa have traditionally been recognized at the generic level, simply on the basis of their morphological distinctivenessand not on the basis of a phylogenetic evaluation of relationships. Composition of our Western Chub-Pikeminnow Cladealso reveals genetic divergences between species of some genera (Gila, Ptychocheilus, Siphateles) comparable to geneticdivergences documented between genera within the Western Clade. Relationships for these 10 genera also highlighttaxonomic inconsistencies relative to recent phylogenetic analysis and, in some cases, are in need of focused attentionusing morphology or additional molecular data to test relationships that will eventually establish a stable classification.Some of these genera are clearly unnatural relative to other genera and their classification or ranking is an obligatory change in modern science of phylogenetics.

References

  1. Aguilar, A. & Jones, W.J. (2009) Nuclear and mitochondrial diversification in two native California minnows: insights into taxonomic identity and regional phylogeography. Molecular Phylogenetics and Evolution, 51, 373–381.

    Arnold, M.L. (1997) Natural Evolution and Hybridization. Oxford University Press, Oxford, U.K., 232 pp.

    Avise, J.C. & Ayala, F.J. (1976) Genetic differentiation in speciose versus depauperate phylads: evidence from the California minnows. Evolution, 30, 46–58.

    Avise, J.C., Smith, J.J. & Ayala, F.J. (1975) Adaptive differentiation with little genetic change between two native California minnows. Evolution, 29, 411–426.

    Bailey, R.M. (1956) A revised list of the fishes of Iowa, with keys for identification. In: Harlan, J.R. & Speaker, E.B. (Eds), Iowa fish and fishing. State Conservation Commission, Des Moines, Iowa, pp. 327-377.

    Banarescu, P. (1964) Pisces-Osteichthys. Fauna Republicii Populare Romine. Editura Academiei Republicii Populare Romine, Bucuresti, Romine. 962 pp.

    Barbour, C.D. & Miller, R.R. (1978) A revision of the Mexican cyprinid fish genus Algansea. Miscellaneous publications Museum of Zoology, University of Michigan, 155, 1–72.

    Bernatchez, L. & Dodson, J. (1990) Allopatric origin of sympatric populations of lake whitefish (Coregonus clupeaformis) as revealed by mitochondrial-DNA restriction analysis. Evolution, 44, 1263–1271.

    Brown, L.R., Moyle, P.B., Bennett, W.A. & Quelvog, B.D. (1992) Implications of morphological variation among populations of California roach Lavinia symmetricus (Cyprinidae) for conservation policy. Biological Conservation, 62, 1–10.

    Bufalino, A.P. & Mayden, R.L. (2010a) Phylogenetic relationships of North American phoxinins (Actinopterygii: Cypriniformes: Leuciscidae) as inferred from S7 nuclear DNA sequences. Molecular Phylogenetics and Evolution, 5, 143–152.

    Bufalino, A.P. & Mayden, R.L. (2010b) Molecular Phylogenetics of North American phoxinins (Actinopterygii: Leuciscidae) based on RAG1 and S7 nuclear DNA sequence data. Molecular Phylogenetics and Evolution, 55, 274–283.

    Bufalino, A.P. & Mayden, R.L. (2010c) Phylogenetic evaluation of North American Leuciscidae (Actinopterygii: Cypriniformes: Cyprinoidea) as inferred from analyses of mitochondrial and nuclear DNA sequences. Systematics and Biodiversity, 8, 493–505.

    Burr, B.M. & Mayden, R.L. (1992) Phylogenetics and North American freshwater fishes. In: Mayden, R.L. (Ed), Systematics, historical ecology, and North American freshwater fishes. Stanford University Press, Stanford, California pp. 18–75.

    Carney, D.A. & Page, L.M. (1990) Meristic characteristics and zoogeography of the genus Ptychocheilus (Teleostei: Cyprinidae). Copeia, 1990, 171–181.

    Chen, W-J., 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. Molecular Phylogenetics and Evolution, 26, 262–288.

    Chow, S. & Hazama, K. (1998) Universal PCR primers for S7 ribosomal protein gene introns in fish. Molecular Ecology, 7, 1255–1256.

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

    Colosimo, P.F., Hosemann, K.E., Balabhadra, S., Villareal, G., Dickson, M., Grimwood, J., Schmutz, J., Myers, R.M., Schluter, D. & Kingsley, D.M. (2005) Widespread parallel evolution in Sticklebacks by repeated fixation of ectodysplasin alleles. Science, 307, 1928–1933.

    Dowling, T.E. & Secor, C.L. (1997) The role of hybridization and evolution in the diversification of animals. Annual Review of Ecology and Systematics, 28, 593–619.

    Dowling, T.E., Tibbets, A.C., Minckley W.L. & Smith, G.R. (2002) Evolutionary relationships of the Plagopterins (Teleostei: Cyprinidae). Copeia, 2002, 665–678.

    Estabrook, G.F., Smith, G.R. & Dowling, T.E. (2007) Body mass and temperature influence rates of mitochondrial DNA evolution in North American cyprinid fish. Evolution, 61, 1176–1187.

    Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791.

    Harris, P.M. (2000) Systematic studies of the genus Siphateles (Ostariophysi: Cyprinidae) from Western North America. Dissertation (Ph.D). Oregon State University, 189 pp.

    Heath, T.A., Zwickl, D.J., Kim, J. & Hillis, D.M. (2008) Taxon sampling affects inferences of macroevolutionary processes from phylogenetic trees. Systematic Biology, 57, 160–166.

    Hedtke, S.M., Townsend, T.M. & Hillis, D.M. (2006) Resolution of phylogenetic conflict in large data sets by increased taxon sampling. Systematic Biology, 55, 522–529.

    Hillis, D.M. (1998) Taxonomic sampling, phylogenetic accuracy, and investigator bias. Systematic Biology, 47, 3–8.

    Hillis, D.M., Pollock, D.D., McGuire, J.A. & Zwickl, D.J. (2003) Is sparse taxon sampling a problem for phylogenetic inference? Systematic Biology, 52, 124–126.

    Houston, D.D., Ogden, T.H., Whiting M.F. & Shiozawa, D.K. (2010a) Polyphyly of the Pikeminnows (Teleostei: Cyprinidae) inferred using mitochondrial DNA sequences. Transactions of the American Fisheries Society, 139, 303–315.

    Houston, D.D., Shiozawa, D.K. & Riddle, B.R. (2010b) Phylogenetic relationships of the western North American cyprinid genus Richardsonius, with an overview of phylogeographic structure. Molecular Phylogenetics and Evolution, 55, 259–273.

    Howes, G.J. (1984) Phyletics and biogeography of the aspinine cyprinid fishes. Bulletin of the British Museum of Natural History, 47, 283–303.

    Howes, G.J. (1985) A revised synonymy of the minnow genus Phoxinus Rafinesque, 1820 (Teleostei: Cyprinidae) with comments on its relationships and distribution. Bulletin of the British Museum of Natural History (Zoology), 48, 57–74.

    Hubbs, C.L. (1955) Hybridization between fish species in nature. Systematic Zoology, 4, 1–20.

    Hubbs, C.L. & Miller, R.R. (1977) Six distinctive cyprinid fish species referred to Dionda inhabiting segments of the Tampico embayment drainage of Mexico. Transactions on the San Diego Society of Natural History, 28, 267–335.

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

    Johnson, J.B., Dowling, T.E. & Belk, M.C. (2004) Neglected taxonomy of rare desert fishes: Congruent evidence for two species of Leaderside chub. Systematic Biology, 53, 841–855.

    Jones, W.J., Quelvog, B.D. & Bernardi, G. (2002) Morphological and genetic analysis of the Red Hills roach (Cyprinidae: Lavinia symmetricus). Conservation Genetics, 3, 261–276.

    Leviton, A.E. & Gibbs, R.H., Jr (1988) Standards in herpetology and ichthyology. Standard symbolic codes for institution resource collections in herpetology and ichthyology. Supplement No. 1: additions and corrections. Copeia, 1988, 280–282.

    Leviton, A.E., Gibbs, R.H. Jr., Heal, E. & Dawson, C.E. (1985) Standards in herpetology and ichthyology: Part I. Standard symbolic codes for institutional resource collections in herpetology and ichthyology. Copeia, 1985, 802–832.

    Lopez, J.A., Chen, W-J. & Orti, G. (2004) Esociform phylogeny. Copeia, 2004, 449–464.

    Lu, G. & Bernatchez, L. (1999) Correlated trophic specialization and genetic divergence in sympatric lake whitefish ecotypes (Coregonus clupeaformis): support for the ecological speciation hypothesis. Evolution, 53, 1491–1505.

    Mayden, R.L. (1989) Phylogenetic studies of North American minnows, with emphasis on the genus Cyprinella (Teleostei: Cypriniformes). Miscellaneous Publication Museum of Natural History, University of Kansas, 80, 1-189.

    Mayden, R.L. (1992) Explorations into the past and the dawn of systematics and historical ecology. In: Mayden, R.L. (Ed), Systematics, historical ecology, and North American freshwater fishes. Stanford University Press, Stanford, California, pp. 3–17.

    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., Rainboth, W.J. & Buth, D.G. (1991) Phylogenetic systematics of the cyprinid genera Mylopharodon and Ptychocheilus: comparative morphometry. Copeia 1991, 819–834.

    Mayden, R.L., Matson, R.H. & Hillis, D.M. (1992) Speciation in the North American genus Dionda (Teleostei: Cypriniformes). In: Mayden, R.L. (Ed), Systematics, historical ecology and North American freshwater fishes. Stanford University Press, Stanford, California, pp. 710–746.

    Mayden, R.L., Conway, K.W., Tang, K., Freyhof, J., Chamberlain, S., Haskins, M., Schneider, L., Sudkamp, M., Wood, R.M., Agnew, M., Bufalino, A., Sulaiman, Z., Miya, M., Saitoh, K., He, S. (2007) Phylogenetic Relationships of Danio within the Order Cypriniformes: A Framework for Comparative and Evolutionary Studies of a Model Species. Journal of Experimental Zoology, Molecular Development and Evolution, 308B, 642–654.

    Mayden, R.L., Tang, K.L., Wood, R.M., Chen, W.-J., Agnew, M.K., Conway, K.W., Yang, L., Li, J., Wang, X., Saitoh, K., Miya, M., He, S., Liu, H., Chen, Y. & Nishida, 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.

    Mayden, R.L., 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 freshwater fishes—order Cypriniformes (Actinopterygii: Ostariophysi): A case study using multiple nuclear loci and the mitochondrial genome. Molecular Phylogenetics and Evolution, 51, 500–514.

    Miller, R.R. (1945a) The status of Lavinia ardesiaca, a cyprinid fish from the Pajaro-Salinas River basin, California. Copeia, 1945, 197–204.

    Miller, R.R. (1945b) Snyderichthys, a new generic name for the leatherside chub of the Bonneville and Upper Snake drainages in western United States. Journal of the Washington Academy of Sciences, 35, 1–28.

    Miller, R.R. (1959) Origin and affinities of the fresh-water fish fauna of western North America. In: Hubbs, C.L. (Ed), Zoogeography. American Association for the Advancement of Science. Publication 51, Washington, D.C., pp. 187–222.

    Miller, R.R. (1965) Quaternary freshwater fishes of North America. In: Wright, H.E. & Frey, D.G. (Eds), Quaternary of the United States. Princeton University Press, Princeton, pp. 569–581.

    Miller, R.R. & Hubbs, C. (1960) The spiny-rayed cyprinid fishes (Plagopterini) of the Colorado River System. Miscellaneous Publications, Museum of Zoology, University of Michigan, 115, 5–39.

    Minckley, W.L., Hendrickson, D.A. & Bond, C.E. (1986) Geography of western North America fishes: description and relationships to intracontinental tectonism. In: Hocutt, C.H. & Wiley, E.O. (Eds), The zoogeography of North American freshwater fishes. John Wiley & Sons, New York, New York, pp. 519–614.

    Orti, G., Bell M.A., Reimchen, T.E. & Meyer, A. (1994) Global survey of mitochondrial DNA sequences in the threespine stickleback: Evidence for recent migrations. Evolution, 48 (3), 608–622.

    Perez-Rodriguez, R., Dominguez-Dominguez, O., Ponce de Leon G.P. & Doadrio, I. (2009) Phylogenetic relationships and biogeography of the genus Algansea Girard (Cypriniformes: Cyprinidae) on central Mexico inferred from molecular data. Biomedical Central Evolutionary Biology, 9, 223, doi:10.1186/1471-2148-9-223 (accessed May 2012).

    Pollock, D.D., Zwickl, D.J., McGuire, J.A. & Hillis, D.M. (2002) Increased taxon sampling is advantageous for phylogenetic inference. Systematic Biology, 51, 664–671.

    Posada, D., & Crandall, K.A. (1998) Modeltest: Testing the models of DNA substitution. Bioinformatics, 14, 817–818.

    Quattro, J.M., Jones, W.J., Grady, J.M, & Rhode, F.C. (2001) Gene-gene concordance and the phylogenetic relationships among rare and widespread pygmy sunfishes (genus Elassoma). Molecular Phylogenetics and Evolution, 18, 217–226.

    Ruber, L., Kottelat, M., Tan, H.H., Ng, P.K.L. & Britz, R. (2007) Evolution of miniaturization and the phylogenetic position of Paedocypris, comprising the world´s smallest vertebrate. Biomedical Central Evolutionary Biology, 7, doi:10.1186/1471-2148-7-38 (accessed May 2012).

    Schluter, D., Clifford, E.A., Nemethy, M. & McKinnon, F.S. (2004) Parallel evolution and inheritance of qualitative traits. The American Naturalist, 163 (6), 809–822.

    Schönhuth, S. & Doadrio, I. (2003) Phylogenetic relationships of Mexican minnows of the genus Notropis (Actinopterygii: Cyprinidae). Biological Journal of the Linnean Society, 80, 323–337.

    Schönhuth, S., Doadrio, I., Dominguez, O., Hillis, D. & Mayden, R.L. (2008) Molecular evolution of Southern North American Cyprinidae (Actinopterygii), with the description of the new genus Tampichthys from central Mexico. Molecular Phylogenetics and Evolution, 47, 729–756.

    Schönhuth, S. & Mayden, R.L. (2010) Phylogenetic relationships in the genus Cyprinella (Actinopterygii: Cyprinidae) based on mitochondrial and nuclear gene sequences. Molecular Phylogenetics and Evolution, 55, 77–98.

    Schönhuth, S., Blum, M.J., Lozano-Vilano, L., Neely, D.A., Romero-Varela, A., Espinosa, H., Perdices, A. & Mayden, R.L. (2011) Interbasin exchange and repeated headwater capture across the Sierra Madre Occidental inferred from the phylogeography of Mexican stonerollers. Journal of Biogeography, 38, 1406–1421.

    Schluter, D., Clifford, E.A., Nemethy, M. & McKinnon, F.S. (2004) Parallel evolution and inheritance of qualitative traits. The American Naturalist, 163, 809–822.

    SEDESOL. (1994) México: Informe de la situación general en material de equilibrio ecológico y protección al ambiente 19931994. Secretaria de Desarrollo Social (SEDESOL), México D.F., 376 pp.

    Simons, A.M. & Mayden, R.L. (1997) Phylogenetic relationships of the Creek Chubs and the Spine-Fins: an enigmatic group of North American cyprinid fishes (Actinopterygii: Cyprinidae). Cladistics, 13, 187–205.

    Simons, A.M. & Mayden, R.L. (1998) Phylogenetic relationships of the western North American phoxinins (Actinopterygii: Cyprinidae) as inferred from mitochondrial 12S and 16S ribosomal RNA sequences. Molecular Phylogenetics and Evolution, 9, 308–329.

    Simons, A.M. & Mayden, R.L. (1999) Phylogenetic relationships of North American cyprinids and assessment of homology of the Open Posterior Myodome. Copeia, 1999, 13–21.

    Simons, A.M., Berendzen, P.B. & Mayden, R.L. (2003) Molecular systematics of North American phoxinin genera (Actinopterygii: Cyprinidae) inferred from mitochondrial 12S and 16S ribosomal RNA sequences. Zoological Journal of the Linnean Society, 139, 63–80.

    Smith, G.R. (1981). Late Cenozoic freshwater fishes of North America. Annual Review of Ecology and Systematics, 12, 163–193.

    Smith, G.R., Dowling, T.E., Gobalet, K.W., Lugaski, T., Shiozawa, D.K. & Evans, R.P. (2002) Biogeography and timing of evolutionary events among Great Basin fishes. In: Hershler, R., Mansen, D. & Currey, D. (Eds), Great Basin aquatic systems history. Smithsonian Contributions to the Earth Sciences, 33. Smithsonian Institution Press, Washington, D.C., pp. 175–234.

    Smith, G.R., Miller R.R., & Sable, W.D. (1979) Species relationships among fishes of the genus Gila in the upper Colorado River drainage. Proceedings of the First Conference on Scientific Research in the National Parks, 1, 613–623.

    Stamatakis, A. (2006) RAxML-VI-HPC: Maximum Likelihood-based Phylogenetic Analyses with Thousands of Taxa and Mixed Models. Bioinformatics 22, 2688–2690.

    Stamatakis, A., Hoover, P. & Rougemont, J. (2008) A rapid bootstrap algorithm for the RaxML web-servers. Systematic Biology, 57, 758–771.

    Strange, R.M. & Mayden, R.L. (2009) Phylogenetic relationships and a revised taxonomy for North American cyprinids currently assigned to Phoxinus (Actinopterygii: Cyprinidae). Copeia, 2009, 494–501.

    Swofford, D.L. (2001) PAUP*: Phylogenetic Analysis using parsimony (* and other methods) Version 4.0b10. Sinauer, Sunderland, MA.

    Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 24, 634–640.

    U.S. Fish and Wildlife Service (2010) Listing status: http://www.fws.gov/species/ (accessed May 2012).

    Uyeno, T. (1960) Osteology and phylogeny of the American cyprinid fishes allied to the genus Gila. Unpublished Ph.D. dissertation, University of Michigan, Ann Arbor, Michigan, 174 pp.

    Wiley, E.O. (1981) Phylogenetics. The Theory and Practice of Phylogenetic Systematics. Wiley-Interscience, New York, 439 pp.

    Woodman, D.A. (1992) Systematic relationships within the cyprinid genus Rhinichthys. In: Mayden, R.L. (Ed), Systematics, historical ecology, and North American freshwater fishes. Stanford University Press, Stanford, California, pp. 374–391.

    Zwickle, D.J. & Hillis, D.M. (2002) Increased taxon sampling greatly reduces phylogenetic error. Systematic Biology, 51, 588–598.