Abstract
The order Cypriniformes and family Catostomidae, the Holarctic suckers, have received considerable phylogeneticattention in recent years. These studies have provided contrasting phylogenies and classifications to historical,morphology-based phylogenetic and prephylogenetic hypotheses of relationships of species and the naturalness ofhypothesized genera, tribes, and subfamilies. To date, nearly all molecular work on catostomids has been done using DNAsequence variation of mitochondrial genes. In this study, we add to our previous investigations to identify single-copynuclear gene markers for diploid and polyploid cypriniforms, and to expand sequences of nuclear IRBP2 gene to 1,933 bpfor 23 catostomid species. This effort expands our previous studies using only partial sequences of 849 bp. The extendedgene fragment consists of nearly the complete gene across exon1 to exon 4 and is used in two analyses to inferphylogenetic relationships of the currently, or formerly, recognized genera, tribes, and subfamilies. One analysis includes23 ingroup species for which the larger fragment of IRBP2 could be obtained; these taxa were also included in a secondanalysis of 67 samples of 52 species for the shorter fragment. As is typical of other nuclear genes examined to date forcypriniform species, variation in IRBP2 provided strong nodal support for some supra-specific groupings and speciesrelationships. The two analyses revealed slightly different relationships, yet are largely consistent with one another. Theresulting tree from variation in the shorter fragment for 52 species is somewhat inferior to the tree derived using theextended fragment in that not as many nodes were resolved, and few have strong support. Relationships from the latteranalysis are, however, consistent with inferred relationships that are more robustly supported in the smaller taxon analysisusing the larger fragment, lending credence to the use of more complete sequence data of genes in phylogenetic analyses.The current classification of the family (e.g., Nelson 2006) is not fully supported herein. The Ictiobinae is monophyletic,but some ambiguity exists as to relationship of this group relative to Cycleptinae and Myxocyprininae, as well as the needto recognize the latter two subfamilies. Catostominae is monophyletic. Catostomus is clearly not monophyletic;unnaturalness of the genus is supported herein as well as in multiple, consistently repeated and highly supported studiesresolving Deltistes, Chasmistes, and Xyrauchen within Catostomus. We herein synonymize the former three genera intothe latter genus; their recognition as distinct genera has been based on historical methods of classification based strictlyon “distinctiveness” or anagenesis of each lineage alone and not phylogenetic relationships relative to species ofCatostomus. The monophyly of Erimyzonini is strongly supported within the analysis of the longer sequence data set. Themonophyly of Thoburniini is ambiguous, but Moxostomatini, including “Scartomyzon,” is monophyletic in both analyses.The proposed recognition of Scartomyzon as a monophyletic group separate from Moxostoma is again falsified but with evidence from the nuclear gene IRBP2.References
Amores, A., Force, A., Yan, Y.L., Joly, L., Amemiya, C., Fritz, A., Ho, R.K., Langeland, J., Prince, V., Wang, Y.L., Westerfield, M., Ekker, M., & Postlethwait, J.H. (1998) Zebrafish hox clusters and vertebrate genome evolution. Science, 282, 1711–1714.
Bart, H.L., Reneau, P.C., Doosey, M.H. & Bell, C.D. (2010) Evolutionary divergence of duplicate copies of the growth hormone gene in suckers (Actinopterygii: Catostomidae). International Journal of Molecular Sciences, 11, 1090–1102.
Bruner, J.C. (1991) Comments on the genus Amyzon (family Catostomidae). Journal of Paleontology, 65, 678–686.
Burr, B.M. & Mayden, R.L. (1999) A new species of Cycleptus (Cypriniformes: Catostomidae) from Gulf Slope drainages of Alabama, Mississippi, and Louisiana, with a review of distribution, biology and conservation status of the genus. Bulletin Alabama Museum of Natural History, 20, 19–57.
Chen, W.-J., Lheknim, V. & Mayden, R.L. (2009) Molecular phylogeny of the Cobitoidea (Teleostei: Cypriniformes) revisited: position of enigmatic loach Ellopostoma Vaillant resolved with six nuclear genes. Journal of Fish Biology, 75, 2197–2208.
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, W.-J. & Mayden, R.L. (2010) A phylogenomic perspective on the new era of ichthyology. BioScience, 60, 421–432.
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.
Christoffels, A., Koh, E.G., Chia, J.M., Brenner, S., Aparicio, S. & Venkatesh, B. (2004) Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes. Molecular Biology and Evolution, 21, 1146–1151.
Clements, M.D., Bart, H.L. & Hurley, D.L. (2012) A different perspective on the phylogenetic relationships of the Moxostomatini (Cypriniformes: Catostomidae) based on cytochrome-b and Growth Hormone intron sequences. Molecular Phylogenetics and Evolution, 63, 159–167.
DeBry, R.W. & Sagel, R.M. (2001) Phylogeny of Rodentia (Mammalia) inferred from the nuclear-encoded gene IRBP. Molecular Phylogenetics and Evolution, 19, 290–301.
Dettaï, A. (2004) La phylogénie des Acanthomorpha (Teleostei) inférée par l'étude de la congruence taxinomique,PhD Dissertation. Université Paris 6, Paris, 347 pp.
Dettaï, A. & Lecointre, G. (2008) New insights into the organization and evolution of vertebrate IRBP genes and utility of IRBP gene sequences for the phylogenetic study of the Acanthomorpha (Actinopterygii : Teleostei). Molecular Phylogenetics and Evolution, 48, 258–269.
Doosey, M.H., Bart, H.L., Saitoh, K. & Miya, M. (2010) Phylogenetic relationships of catostomid fishes (Actinopterygii: Cypriniformes) based on mitochondrial ND4/ND5 gene sequences. Molecular Phylogenetics and Evolution, 54, 1028–1034.
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791.
Ferris, S.D. (1984) Tetraploidy and the evolution of the catostomid fishes. In: Turner, B. J. (Ed), Evolutionary Genetics of Fishes. Plenum, New York, pp. 55–93.
Ferris, S.D. & Whitt, G. S. (1978) Phylogeny of tetraploid catostomid fishes based on loss of duplicate gene-expression. Systematic Zoology, 27, 189–206.
Fong, S.L., Fong, W. B., Morris, T. A., Kedzie, K. M. & Bridges, C. D. (1990) Characterization and comparative structural features of the gene for human interstitial retinol-binding protein. Journal of Biological Chemistry, 265, 3648–3653.
Fowler, H.W. (1913) Notes on catostomid fishes. Proceedings of the Academy of Natural Sciences Philadelphia, 6558, 45–60.
Fuiman, L.A. (1985) Contributions of developmental characters to a phylogeny of catostomid fishes, with comments on heterochrony. Copeia, 1985, 833–846.
Gaubert, P. & Cordeiro-Estrela, P. (2006) Phylogenetic systematics and tempo of evolution of the Viverrinae (Mammalia, Carnivora, Viverridae) within feliformians: Implications for faunal exchanges between Asia and Africa. Molecular Phylogenetics and Evolution, 41, 266–278.
Harris, P.M. & Mayden, R.L. (2001) Phylogenetic relationships of major clades of Catostomidae (Teleostei : Cypriniformes) as inferred from mitochondrial SSU and LSU rDNA sequences. Molecular Phylogenetics and Evolution, 20, 225–237.
Harris, P.M., Mayden, R.L., Perez, H.S.E. & De Leon, F.G. (2002) Phylogenetic relationships of Moxostoma and Scartomyzon (Catostomidae) based on mitochondrial cytochrome b sequence data. Journal of Fish Biology, 61, 1433–1452.
Hennig, W. (1966) Phylogenetic Systematics. University of Illinois Press, Urbana, Illinois, 263 pp.
Hillis, D.M. & Bull, J.J. (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology, 42, 182–192.
Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES. Bayesian inference of phylogeny. Bioinformatics, 17, 754–755.
Jansa, S.A. & Weksler, M. (2004) Phylogeny of muroid rodents: relationships within and among major lineages as determined by IRBP gene sequences. Molecular Phylogenetics and Evolution, 31, 256–276.
Schneider, H., Sampaio, I., Harada, M.L., Barroso, C.M., Schneider, M.P., Czelusniak, J. & Goodman, M. (1996) Molecular phylogeny of the New World monkeys (Platyrrhini, Primates) based on two unlinked nuclear genes: IRBP intron 1 and ε-globin sequences. American Journal of Physical Anthropology, 100, 153–179.
Le Comber, S.C. & Smith, C. (2004) Polyploidy in fishes: patterns and processes. Biological Journal of the Linnean Society, 82, 431–442.
Lee, D.S., Gilbert, C.R., Hocutt, C.H., Jenkins, R.E., McAllister, D.E. & Stauffer, J.R., Jr. (1981) Atlas of North American freshwater fishes. North Carolina Museum of Natural History, Raleigh, NC, 867 pp.
Leggatt, R.A. & Iwama, G.K. (2003) Occurrence of polyploidy in fishes. Reviews in Fish Biology and Fisheries, 13, 237–246.
Martin, A.P. & Burg, T.M. (2002) Perils of paralogy: using HSP70 genes for Inferring organismal phylogenies. Systematic Biology, 51, 570–587.
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., 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.
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.
Meyer, A. & Van de Peer, Y. (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). BioEssays, 27, 937–945.
Miller, R.R. (1959) Origin and affinities of the freshwater fish fauna of western North America. In: Hubbs, C.L. (Ed), Zoogeography. American Association for the Advancement of Science, Washington D.C., pp. 187–222.
Miller, R.R. & Smith, G.R. (1981) Distribution and evolution of Chasmistes (Pises: Catostomidae) in western North America. Occasional Papers of the Museum of Zoology University of Michigan, 696, 1–46.
Nelson, J.S. (2006) Fishes of the World, 4th Edition. John Wiley & Sons, Inc., Hoboken, NJ, 601 pp.
Nickerson, J.M., Frey, R.A., Ciavatta, V.T. & Stenkamp, D.L. (2006) Interphotoreceptor retinoid-binding protein gene structure in tetrapods and teleost fish. Molecular Vision, 12, 1565–1585.
Ohno, S. (1970) Evolution by gene duplication. Springer-Verlag, New York, 160 pp.
Palandacic, A., Zupancic, P. & Snoj, A. (2010) Revised classification of former genus Phoxinellus using nuclear DNA sequences. Biochemical Systematics and Ecology, 38, 1069–1073.
Pepperberg, D.R., Okajima, T.L., Wiggert, B., Ripps, H., Crouch, R.K. & Chader, G.J. (1993) Interphotoreceptor retinoid-binding protein (IRBP). Molecular biology and physiological role in the visual cycle of rhodopsin. Molecular Neurobiology, 7, 61–85.
Rajendran, R.R., Van Niel, E.E., Stenkamp, D.L., Cunningham, L.L., Raymond, P.A. & Gonzalez-Fernandez, F. (1996) Zebrafish interphotoreceptor retinoid-binding protein: differential circadian expression among cone subtypes. The Journal of Experimental Biology, 199, 2775–2787.
Rambaut, A. (1996) Sequence alignment editor version 1.0 α1, University of Oxford, Oxford, UK. Available from http://evolve.zoo.ox.ac.uk/Se-Al/Se-Al.html.
Saitoh, K. & Chen, W.-J. (2008) Reducing cloning artifacts for recovery of allelic sequences by T7 endonuclease I cleavage and single re-extension of PCR products — a benchmark. Gene, 423, 92–95.
Saitoh, K., Chen, W.-J. & Mayden, R.L. (2010) Extensive hybridization and tetrapolyploidy in spined loach fish. Molecular Phylogenetics and Evolution, 56, 1001–1010.
Saitoh, K., Sado, T., Mayden, R.L., Hanzawa, N., Nakamura, K., Nishida, M. & Miya, 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.
Schneider, C.J., Cunningham, M., Moritz, C. (1998) Comparative phylogeography and the history of endemic vertebrates in the Wet Tropics rainforests of Australia. Molecular Ecology, 7, 487–498.
Siebert, P.D., Chenchik, A., Kellogg, D.E., Lukyanov, K.A. & Lukyanov, S.A. (1995) An improved PCR method for walking in uncloned genomic DNA. Nucleic Acids Research, 23, 1087–1088.
Silvestro, D. & Michalak, I. (2011) RaxmlGUI: a graphical front-end for RAxML. Organisms Diversity & Evolution, http://dx.doi.org/10.1007/s13127-13011-10056-13120.
Smith, G.R. (1992) Phylogeny and biogeography of the Catostomidae, freshwater fishes of North America and Asia. In: Mayden, R.L. (Ed), Systematics, historical ecology and North American freshwater fishes. Standford University Press, Stanford, pp. 778–813.
Stamatakis, A. (2006) RAxML-VI-HPC: Maximum Likelihood-based Phylogenetic Analyses with Thousands of Taxa and Mixed Models. Bioinformatics, 22, 2688–2690.
Stanhope, M.J., Smith, M.R., Waddell, V.G., Porter, C.A., Shivji, M.S. & Goodman, M. (1996) Mammalian evolution and the interphotoreceptor retinoid binding protein (IRBP) gene: convincing evidence for several superordinal clades. Journal of Molecular Evolution, 43, 83–92.
Swofford, D.L. (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. (4 ed.). Sinauer Associates, Sunderland, Massachusetts.
Tang, K.L., Agnew, M.K., Chen, W.-J., Raley, M.E., Sado, T., Schneider, L.M. Yang, L., Bart, H. L., He, S., Liu, H., Miya, M., Saitoh, K., Simon, A. M., Wood, R. M. & Mayden, R. L. (2011) Phylogeny of the gudgeons (Teleostei: Cyprinidae: Gobioninae). Molecular Phylogenetics and Evolution, 61, 103–124.
Tao, W.J., Zou, M., Wang, X.Z., Gan, X.N., Mayden, R.L. & He, S.P. (2010) Phylogenomic analysis resolves the formerly intractable adaptive diversification of the endemic clade of East Asian Cyprinidae (Cypriniformes). PLoS ONE, 5 (10): e13508. http://dx.doi.org/10.1371/journal.pone.0013508.
Tsigenopoulos, C.S., Ráb, P., Naran, D. & Berrebi, P. (2002) Multiple origins of polyploidy in the phylogeny of southern African barbs (Cyprinidae) as inferred from mtDNA markers. Heredity, 88, 466–473.
Uyeno, T. & Smith, G.R. (1972) Tetraploid origin of the karyotype of catostomid fishes. Science, 175, 644–646.
Wilson, M.V.H. (1977) Middle Eocene freshwater fishes from British Columbia. Royal Ontario Museum, Life Sciences Contributions, 113, 1–61.
Yang, L., Arunachalam, M., Sado, T., Levin, B.A., Golubtsov, A.S., Freyhof, J., Friel, J.P., Chen, W.-J., Hirt, M.V., Manickam, R., Agnew, M.K., Simons, A.M., Saitoh, K., Miya, M., Mayden, R.L. & He, S. (2012) Molecular phylogeny of the cyprinid tribe Labeonini (Teleostei: Cypriniformes). Molecular Phylogenetics and Evolution, 65, 362–379.
Zwickl, D.J. & Hillis, D.M. (2002) Increased taxon sampling greatly reduces phylogenetic error. Systematic Biology, 51, 588–598.