Abstract
The catfish genus Pseudexostoma (Sisoridae) currently contains three species: P. yunnanensis from the upper Irrawaddy River (Dayingjiang), and P. brachysoma and P. longipterus from the upper Salween River (Nujiang). We adopted an integrative approach combining both morphology-based (traditional measurements, truss-based and geometric morphometrics, fin skeleton examination and X-ray photography) and molecular approaches (genetic distances, haplotype network, phylogenetic relationships) to reappraise species validity in Pseudexostoma. Our results showed that P. longipterus cannot be distinguished from P. brachysoma from either morphological or molecular analyses, and that the former name should thus be considered a junior synonym of the latter. The two remaining geographically isolated species, P. yunnanensis and P. brachysoma, showed a distinct genetic distance equated to the typical 2% sequence divergence threshold delineating different species of fishes, and with a divergence time dated to approximately 1.22–2.14 million years ago. Although P. yunnanensis and P. brachysoma share some morphological characters that appear gradually diverging (body depth at anus and interorbital distance), some degree of overlap still exists, we suggest the two species are distinct based on the total evidence.
References
April, J., Hanner, R.H., Dion-cote, A.M. & Bernatchez, L. (2013) Glacial cycles as an allopatric speciation pump in north-eastern American freshwater fishes. Molecular Ecology, 22 (2), 409–422.
http://dx.doi.org/10.1111/mec.12116Bandelt, H.J., Forster, P. & Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16 (1), 37–48.
http://dx.doi.org/10.1093/oxfordjournals.molbev.a026036Bartlett, M.S. (1954) A note on the multiplying factors for various chi square approximations. Journal of the Royal Statistical Society, Series B, 16, 296–298.
Chu, X.L. (1979) Systematics and evolutionary pedigree of the glyptosternoid fishes (family Sisoridae). Acta Zootaxonomica Sinica, 4 (1), 72–82.
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9 (8), 772–772.
http://dx.doi.org/10.1038/nmeth.2109de Pinna, M.C. (1996) Phylogenetic analysis of the Asian catfish families Sisoridae, Akysidae, and Amblycipitidae, with a hypothesis on the relationships of the neotropical Aspredinidae (Teleostei, Ostariophysi). Fieldiana Zoology, New Series, 84, 1–83.
Dowling, T.E., Martasian, D.P. & Jeffery, W.R. (2002) Evidence for multiple genetic forms with similar eyeless phenotypes in the blind cavefish, Astyanax mexicanus. Molecular Biology and Evolution, 19 (4), 446–455.
http://dx.doi.org/10.1093/oxfordjournals.molbev.a004100Ferraris, C.J. (2007) Checklist of catfishes, recent and fossil (Osteichthyes: Siluriformes), and catalogue of siluriform primary types. Zootaxa, 1418, 1–628.
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3 (5), 294–299.
Guo, X.G., He, S.P. & Zhang, Y.G. (2005) Phylogeny and biogeography of Chinese sisorid catfishes re-examined using mitochondrial cytochrome b and 16S rRNA gene sequences. Molecular Phylogenetics and Evolution, 35 (2), 344–362.
http://dx.doi.org/10.1016/j.ympev.2004.12.015Hardman, M. & Page, L.M. (2003) Phylogenetic relationships among bullhead catfishes of the genus Ameiurus (Siluriformes: Ictaluridae). Copeia, 2003 (1), 20–33.
http://dx.doi.org/10.1643/0045-8511(2003)003[0020:prabco]2.0.co;2He, D.K. & Chen, Y.F. (2006) Biogeography and molecular phylogeny of the genus Schizothorax (Teleostei: Cyprinidae) in China inferred from cytochrome b sequences. Journal of Biogeography, 33 (8), 1448–1460.
http://dx.doi.org/10.1111/j.1365-2699.2006.01510.xHe, S.P. (1996) The phylogeny of the glyptosternoid fishes (Teleostei: Siluriformes, Sisoridae). Cybium, 20 (2), 115–159.
Hebert, P.D.N., Cywinska, A., Ball, S.L. & Dewaard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of The Royal Society of London. Series B, Biological Sciences, 270, 313–321.
http://dx.doi.org/10.1098/rspb.2002.2218Hora, S.L. & Silas, E. (1952) Evolution and distribution of Glyptosternoid fishes of the family Sisoridae (Order: Siluroidea). In: Proceedings of the National Institute of Sciences of India, 1952, pp. 309–322.
Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17 (8), 754–755.
http://dx.doi.org/10.1093/bioinformatics/17.8.754Jiang, W.S., Ng, H.H., Yang, J.X. & Chen, X.Y. (2012) A taxonomic review of the catfish identified as Glyptothorax zanaensis (Teleostei: Siluriformes: Sisoridae), with the descriptions of two new species. Zoological Journal of the Linnean Society, 165 (2), 363–389.
http://dx.doi.org/10.1111/j.1096-3642.2011.00811.xJörger, K.M. & Schrödl, M. (2013) How to describe a cryptic species? Practical challenges of molecular taxonomy. Frontiers in Zoology, 10 (1), 1–27.
http://dx.doi.org/10.1186/1742-9994-10-59Kaiser, H. (1970) A second generation little jiffy. Psychometrika, 35 (4), 401–415.
http://dx.doi.org/10.1007/BF02291817Kang, Z.J., Chen, Y.X. & He, D.K. (2016) Pareuchiloglanis hupingshanensis, a new species of the glyptosternine catfish (Siluriformes: Sisoridae) from the middle Yangtze River, China. Zootaxa, 4083 (1), 109–125.
http://dx.doi.org/10.11646/zootaxa.4083.1.6Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16 (2), 111–120.
http://dx.doi.org/10.1007/BF01731581Klingenberg, C.P. (2011) MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11 (2), 353–357.
http://dx.doi.org/10.1111/j.1755-0998.2010.02924.xMa, X.H., Kang, J.L., Chen, W.T., Zhou, C.J. & He, S.P. (2015) Biogeographic history and high-elevation adaptations inferred from the mitochondrial genome of Glyptosternoid fishes (Sisoridae, Siluriformes) from the southeastern Tibetan Plateau. BMC Evolutionary Biology, 15 (233), 1–12.
http://dx.doi.org/10.1186/s12862-015-0516-9Mitteroecker, P. & Gunz, P. (2009) Advances in geometric morphometrics. Evolutionary Biology, 36 (2), 235–247.
http://dx.doi.org/10.1007/s11692-009-9055-xNg, H.H. & Jiang, W.S. (2015) Intrafamilial relationships of the Asian hillstream catfish family Sisoridae (Teleostei: Siluriformes) inferred from nuclear and mitochondrial DNA sequences. Ichthyological Exploration of Freshwaters, 26 (3), 229–240.
Ng, H.H. (2010) The monophyly and composition of the Asian hillstream catfish family Sisoridae (Teleostei: Siluriformes): evidence from morphology. Ichthyological Exploration of Freshwaters, 21 (3), 247–278.
Ng, H.H. (2015) Phylogenetic systematics of the Asian catfish family Sisoridae (Actinopterygii: Siluriformes). Ichthyological Exploration of Freshwaters, 26 (2), 97–157.
Ornelas-García, C.P., Domínguez-Domínguez, O. & Doadrio, I. (2008) Evolutionary history of the fish genus Astyanax Baird & Girard (1854) (Actinopterygii, Characidae) in Mesoamerica reveals multiple morphological homoplasies. BMC Evolutionary Biology, 8 (340), 1–17.
http://dx.doi.org/10.1186/1471-2148-8-340Parsons, K.J., Robinson, B.W. & Hrbek, T. (2003) Getting into shape: an empirical comparison of traditional truss-based morphometric methods with a newer geometric method applied to New World cichlids. Environmental Biology of Fishes, 67 (4), 417–431.
http://dx.doi.org/10.1023/A:1025895317253Peng, Z.G., Ho, S.Y., Zhang, Y.G. & He, S.P. (2006) Uplift of the Tibetan plateau: evidence from divergence times of glyptosternoid catfishes. Molecular Phylogenetics and Evolution, 39 (2), 568–572.
http://dx.doi.org/10.1016/j.ympev.2005.10.016Posada, D. & Buckley, T.R. (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology, 53 (5), 793–808.
http://dx.doi.org/10.1080/10635150490522304Regan, C.T. (1911) The classification of the teleostean fishes of the order Ostariophysi. 2. Siluroidea. Annals and Magazine of Natural History, Series 8, 8, 553–577.
http://dx.doi.org/10.1080/00222931108693067Rohlf, F.J. (2010) TPSDig version 2.17. Department of Ecology and Evolution, State University of New York, Stony Brook, New York.
Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular cloning: A Laboratory Manual. Vol. 2. Cold spring harbor laboratory press, New York, 1626 pp.
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22 (21), 2688–2690.
http://dx.doi.org/10.1093/bioinformatics/btl446Strecker, U., Faúndez, V.H. & Wilkens, H. (2004) Phylogeography of surface and cave Astyanax (Teleostei) from Central and North America based on cytochrome b sequence data. Molecular Phylogenetics and Evolution, 33 (2), 469–481.
http://dx.doi.org/10.1016/j.ympev.2004.07.001Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28 (10), 2731–2739.
http://dx.doi.org/10.1093/molbev/msr121Taylor, W.R. & Van Dyke, G. (1985) Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium, 9 (2), 107–119.
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22 (22), 4673–4680.
http://dx.doi.org/10.1093/nar/22.22.4673Thomson, A.W. & Page, L.M. (2006) Genera of the Asian catfish families Sisoridae and Erethistidae (Teleostei: Siluriformes). Zootaxa, 1345, 1–96.
Xiao, W.H., Zhang, Y.P. & Liu, H.Z. (2001) Molecular systematics of Xenocyprinae (Teleostei: Cyprinidae): taxonomy, biogeography, and coevolution of a special group restricted in East Asia. Molecular Phylogenetics and Evolution, 18 (2), 163–173.
http://dx.doi.org/10.1006/mpev.2000.0879Yang, J., Yang, J.X. & Chen, X.Y. (2012) A re-examination of the molecular phylogeny and biogeography of the genus Schizothorax (Teleostei: Cyprinidae) through enhanced sampling, with emphasis on the species in the Yunnan-Guizhou Plateau, China. Journal of Zoological Systematics and Evolutionary Research, 50 (3), 184–191.
http://dx.doi.org/10.1111/j.1439-0469.2012.00661.xYu, M.L. & He, S.P. (2012) Phylogenetic relationships and estimation of divergence times among Sisoridae catfishes. Science China Life Sciences, 55 (4), 312–320.
http://dx.doi.org/10.1007/s11427-012-4305-zZhou, W., Yang, Y., Li, X. & Li, M.H. (2007) A review of the catfish genus Pseudexostoma (Siluriformes: Sisoridae) with description of a new species from the upper Salween (Nujiang) basin of China. The Raffles Bulletin of Zoology, 55 (1), 147–155.