Mitochondrial capture and incomplete lineage sorting in the diversification of balitorine loaches (Cypriniformes, Balitoridae) revealed by mitochondrial and nuclear genes

Zoologica Scripta

Volumn 41, Issue 3, 2012, Pages 233-247

  Tang, Qiong Ying ^a   Liu, Si Qing ^a   Yu, Dan ^a   Liu, Huan Zhang ^a   Danley, Patrick D ^b  

^a INSTITUTE OF HYDROBIOLOGY   (China)

^b BAYLOR UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABBREVIATA; BALITORIDAE; COBITIDAE; CYPRINIFORMES; JINSHAIA; JINSHAIA SINENSIS; LEPTURICHTHYS; LEPTURICHTHYS DOLICHOPTERUS; LEPTURICHTHYS FIMBRIATA;

EID: 84862831107     PISSN: 03003256     EISSN: 14636409     Source Type: Journal    
DOI: 10.1111/j.1463-6409.2011.00530.x     Document Type: Article

References (70)

1. Aboim, M. A., Mavarez, J., Bernatchez, L. & Coelho, M. M. (2010). Introgressive hybridization between two Iberian endemic cyprinid fish: a comparison between two independent hybrid zones. Journal of Evolutionary Biology, 23, 817-828.
2. 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.
3. Avise, J. C. (2000). Phylogeography, the History and Formation of Species. England: Harvard University.
4. Bandelt, H. J., Forster, P. & Rohl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37-48.
5. Barbanera, F., Zuffi, M. A. L., Guerrini, M., Gentilli, A., Tofanelli, S., Fasola, M. & Dini, F. (2009). Molecular phylogeography of the asp viper Vipera aspis (Linnaeus, 1758) in Italy: evidence for introgressive hybridization and mitochondrial DNA capture. Molecular Phylogenetics and Evolution, 52, 103-114.
6. Birky, C. W. J. (1991). Evolution and population genetics of organelle genes: mechanisms and models. In R. K. Selander, A. G. Clark & T. S. Whittam (Eds) Evolution at the molecular level (pp. 112-134). Sunderland, MA: Sinauer Associates.
7. Chan, K. M. A. & Levin, S. A. (2005). Leaky prezygotic isolation and porous genomes: rapid introgression of maternally inherited DNA. Evolution, 59, 720-729.
8. Chang, H. W. (1945). Comparative study on the girdles and their adjacent structures in Chinese Homalopterid fishes with special reference to the adaptation to torrential stream. Sinensia, 16, 9-26.
9. Chen, Y. Y. (1980). Systematic studies on the fishes of the family Homalopteridae of China III. Phyletic studies of the Homalopterid fishes. Acta Zootaxonomica Sinica, 5, 200-211.
10. Chen, Y. Y. & Tang, W. Q. (2000). Homalopteridae. In P. Q. Yue (Ed.) Fauna sinica. Osteichthyes. Cypriniformes (pp. 438-567). Beijing: Sciences Press.
11. Dai, D. Y. (1985). A new species of the genus Lepturichthys from China. Acta Zotaxonomica Sinica, 10, 221-223.
12. Demarais, B. D. & Minckley, W. L. (1992). Hybridization in native cyprinid fishes, Gila ditaenia and Gila sp in Northwestern Mexico. Copeia, 69, 7-703.
13. Demarais, B. D., Dowling, T. E., Douglas, M. E., Minckley, W. L. & Marsh, P. C. (1992). Origin of Gilaseminuda (Teleostei:Cyprinidae) through introgressive hybridization: implications for evolution and conservation. Proceedings of the National Academy of Sciences of the United States of America, 89, 2747-2751.
14. Dowling, T. E. & DeMarais, B. D. (1993). Evolutionary significance of introgressive hybridization in cyprinid fishes. Nature, 362, 444-446.
15. Dowling, T. E. & Secor, C. L. (1997). The role of hybridization and introgression in the diversification of animals. Annual Review of Ecology and Systematics, 28, 593-619.
16. Drummond, A. J. & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
17. Durand, J. D., Tsigenopoulos, C. S., Ünlü, E. & Berrebi, P. (2002). Phylogeny and biogeography of the family Cyprinidae in the Middle East inferred from Cytochrome b DNA-- evolutionary significance of this region. Molecular Phylogenetics and Evolution, 22, 91-100.
18. Egger, B., Koblmueller, S., Sturmbauer, C. & Sefc, K. M. (2007). Nuclear and mitochondrial data reveal different evolutionary processes in the Lake Tanganyika cichlid genus Tropheus. BMC Evolutionary Biology, 7, 137.
19. Excoffier, L., Laval, G. & Schneider, S. (2005). Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47-50.
20. Ferris, S. D., Sage, R. D., Huang, C. M., Nielsen, J. T., Ritte, U. & Wilson, A. C. (1983). Flow of mitochondrial DNA across a species boundary. Proceedings of the National Academy of Sciences of the United States of America, 80, 2290-2294.
21. 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, 294-299.
22. Freyhof, J., Lieckfeldt, D., Pitra, C. & Ludwig, A. (2005). Molecules and morphology: evidence for introgression of mitochondrial DNA in Dalmatian cyprinids. Molecular Phylogenetics and Evolution, 37, 347-354.
23. Froese, R. & Pauly, D. (2011). FishBase. World Wide Web electronic publication. Available via, version (06/2011).
24. Funk, D. J. & Omland, K. E. (2003). Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology Evolution and Systematics, 34, 397-423.
25. Galtier, N. & Daubin, V. (2008). Dealing with incongruence in phylogenomic analyses. Philosophical Transactions of the Royal Society B-Biological Sciences, 363, 4023-4029.
26. Galtier, N., Gouy, M. & Gautier, C. (1996). SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Bioinformatics, 12, 543-548.
27. Genner, M. J. & Turner, G. F. (2011). Ancient hybridization and phenotypic novelty within lake Malawi's cichlid fish radiation. Molecular Biology and Evolution, 29, 195-206.
28. Gilles, A., Costedoat, C., Barascud, B., Voisin, A., Banarescu, P., Bianco, P. G., Economidis, P. S., Marić, D. & Chappaz, R. (2010). Speciation pattern of Telestes souffia complex (Teleostei, Cyprinidae) in Europe using morphological and molecular markers. Zoologica Scripta, 39, 225-242.
29. Gompert, Z., Forister, M. L., Fordyce, J. A. & Nice, C. C. (2008). Widespread mito-nuclear discordance with evidence for introgressive hybridization and selective sweeps in Lycaeides. Molecular Ecology, 17, 5231-5244.
30. Good, J. M., Hird, S., Reid, N., Demboski, J. R., Steppan, S. J., Martin-Nims, T. R. & Sullivan, J. (2008). Ancient hybridization and mitochondrial capture between two species of chipmunks. Molecular Ecology, 17, 1313-1327.
31. Grant, P. R. & Grant, B. R. (1992). Hybridization of bird species. Science, 256, 193-197.
32. Grant, P. R. & Grant, B. R. (1994). Phenotypic and genetic effects of hybridization in Darwin's finches. Evolution, 48, 297-316.
33. Heckman, K. L., Mariani, C. L., Rasoloarison, R. & Yoder, A. D. (2007). Multiple nuclear loci reveal patterns of incomplete lineage sorting and complex species history within western mouse lemurs (Microcebus). Molecular Phylogenetics and Evolution, 43, 353-367.
34. Kane, N. C., King, M. G., Barker, M. S., Raduski, A., Karrenberg, S., Yatabe, Y., Knapp, S. J. & Rieseberg, L. H. (2009). Comparative genomic and population genetic analyses indicate highly porous genomes and high levels of gene flow between divergent Helianthus species. Evolution, 63, 2061-2075.
35. Ketmaier, V., Bianco, P. G., Cobolli, M., Krivokapic, M., Caniglia, R. & De Matthaeis, E. (2004). Molecular phylogeny of two lineages of Leuciscinae cyprinids (Telestes and Scardinius) from the peri-Mediterranean area based on Cytochrome b data. Molecular Phylogenetics and Evolution, 32, 1061-1071.
36. Koblmüller, S., Nord, M., Wayne, R. K. & Leonard, J. A. (2009). Origin and status of the Great Lakes wolf. Molecular Ecology, 18, 2313-2326.
37. Koblmüller, S., Egger, B., Sturmbauer, C. & Sefc, K. M. (2010). Rapid radiation, ancient incomplete lineage sorting and ancient hybridization in the endemic Lake Tanganyika cichlid tribe Tropheini. Molecular Phylogenetics and Evolution, 55, 318-334.
38. Kocher, T. D., Thomas, W. K., Meyer, A., Edwards, S. V., Paabo, S., Villablanca, F. X. & Wilson, A. C. (1989). Dynamics of mitochondrial-DNA evolution in animals - amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences of the United States of America, 86, 6196-6200.
39. Kottelat, M. & Chu, X. L. (1988). A synopsis of Chinese balitorine loaches (Osteichthyes: Homalopteridae) with comments on their phylogeny and description of a new genus. Revue Suisse de Zoologie, 95, 181-201.
40. Lewontin, R. C. & Birch, L. C. (1966). Hybridization as a source of variation for adaptation to new environments. Evolution, 20, 315-336.
41. Librado, P. & Rozas, J. (2009). Dnasp v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
42. Linnen, C. R. & Farrell, B. D. (2007). Mitonuclear discordance is caused by rampant mitochondrial introgression in Neodiprion (Hymenoptera: Diprionidae) sawflies. Evolution, 61, 1417-1438.
43. López, J. A., Chen, W. J. & Orti, G. (2004). Esociform phylogeny. Copeia, 3, 449-464.
44. Meyer, A. (1993). Evolution of mitochondrial DNA in fishes. In P. W. Hochachka & T. P. Mommsen (Eds) Biochemistry and Molecular Biology of Fishes (pp. 1-38). Amsterdam: Elsevier Science Publishers.
45. Nelson, J. S. (2006). Fishes of the World. New York: Wiley.
46. Nevado, B., Koblmüller, S., Sturmbauer, C., Snoeks, J., Usano-Alemany, J. & Verheyen, E. (2009). Complete mitochondrial DNA replacement in a Lake Tanganyika cichlid fish. Molecular Ecology, 18, 4240-4255.
47. Palumbi, S. R., Cipriano, F. & Hare, M. P. (2001). Predicting nuclear gene coalescence from mitochondrial data: the three-times rule. Evolution, 55, 859-868.
48. Peters, J. L., Zhuravlev, Y., Fefelov, I., Logie, A. & Omland, K. E. (2007). Nuclear loci and coalescent methods support ancient hybridization as cause of mitochondrial paraphyly between gadwall and falcated duck (Anas spp.). Evolution, 61, 1992-2006.
49. Posada, D. & Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817-818.
50. Rabosky, D. L., Talaba, A. L., Donnellan, S. C. & Lovette, I. J. (2009). Molecular evidence for hybridization between two Australian desert skinks, Ctenotus leonhardii and Ctenotus quattuordecimlineatus (Scincidae: Squamata). Molecular Phylogenetics and Evolution, 53, 368-377.
51. Rambaut, A. (2010). FigTree. Available via
52. Rambaut, A. & Drummond, A. J. (2007). Tracer v1.4. Available via
53. Redenbach, Z. & Taylor, E. B. (2002). Evidence for historical introgression along a contact zone between two species of char (Pisces: Salmonidae) in northwestern North America. Evolution, 56, 1021-1035.
54. Regan, C. T. (1911). Classification of Teleostean fishes of the Order Ostariophysi. I. Cyprinoidea. Annals and Magazine of Natural History, 8, 31-32.
55. Rheindt, F. E., Christidis, L. & Norman, J. A. (2009). Genetic introgression, incomplete lineage sorting and faulty taxonomy create multiple cases of polyphyly in a montane clade of tyrant-flycatchers (Elaenia, Eyrannidae). Zoologica Scripta, 38, 143-153.
56. Ronquist, F. & Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574.
57. Saitoh, K., Kim, I. S. & Lee, E. H. (2004). Mitochondrial gene introgression between spined loaches via hybridogenesis. Zoological Science, 21, 795-798.
58. Saitoh, K., Chen, W. J. & Mayden, R. L. (2010). Extensive hybridization and tetrapolyploidy in spined loach fish. Molecular Phylogenetics and Evolution, 56, 1001-1010.
59. Šlechtová, V., Bohlen, J. & Perdices, A. (2008). Molecular phylogeny of the freshwater fish family Cobitidae (Cypriniformes: Teleostei): delimitation of genera, mitochondrial introgression and evolution of sexual dimorphism. Molecular Phylogenetics and Evolution, 47, 812-831.
60. Swofford, D. L. (2002). PAUP*: Phylogenetic Analysis Using Parsimony (* and Other Methods), Version 4. Sunderland, MA: Sinauer Associates.
61. Takezaki, N., Rzhetsky, A. & Nei, M. (1995). Phylogenetic tests of the molecular clock and linearized trees. Molecular Biology and Evolution, 12, 823-833.
62. Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596-1599.
63. Tang, Q. Y., Liu, H. Z., Mayden, R. & Xiong, B. X. (2006). Comparison of evolutionary rates in the mitochondrial DNA Cytochrome b gene and control region and their implications for phylogeny of the Cobitoidea (Teleostei: Cypriniformes). Molecular Phylogenetics and Evolution, 39, 347-357.
64. Tang, Q. Y., Freyhof, J., Xiong, B. X. & Liu, H. Z. (2008). Multiple invasions of Europe by east Asian Cobitid loaches (Teleostei: cobitidae). Hydrobiologia, 605, 17-28.
65. 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, 25, 4876-4882.
66. Willis, B. L., van Oppen, M. J. H., Miller, D. J., Vollmer, S. V. & Ayre, D. J. (2006). The role of hybridization in the evolution of reef corals. Annual Review of Ecology Evolution and Systematics, 37, 489-517.
67. Wirtz, P. (1999). Mother species-father species: unidirectional hybridization in animals with female choice. Animal Behaviour, 58, 1-12.
68. Xiao, W. & Zhang, Y. (2000). Genetics and evolution of mitochondrial DNA in fish. Acta Hydrobiologica Sinica, 24, 384-391.
69. Xiao, W., Zhang, Y. & Liu, H. (2001). Molecular systematics of Xenocyprinae (Teleostei: Cyprinidae): taxonomy, biogeography, and coevolution of a special group restricted in East Asia. Molecular Phylogenetics and Evolution, 18, 163-173.
70. Zhang, L., Tang, Q. Y. & Liu, H. Z. (2008). Phylogeny and speciation of the eastern Asian cyprinid genus Sarcocheilichthys. Journal of Fish Biology, 72, 1122-1137.