Extensive hybridization and tetrapolyploidy in spined loach fish

Molecular Phylogenetics and Evolution

Volumn 56, Issue 3, 2010, Pages 1001-1010

  Saitoh, Kenji ^a   Chen, Wei Jen ^b   Mayden, Richard L ^c  

^a FISHERIES RESEARCH AGENCY   (Japan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c SAINT LOUIS UNIVERSITY   (United States)

Author keywords

Cypriniformes; Early growth response protein; Gene duplication; Interphotoreceptor retinoid binding protein; MtDNA; Polyploidy; Recombination activating gene; Rhodopsin; Teleostean fish

Indexed keywords

MITOCHONDRIAL DNA;

ALLELE; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CELL NUCLEUS; CLASSIFICATION; CYPRINIFORMES; DNA SEQUENCE; GENETICS; HYBRIDIZATION; JAPAN; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYPLOIDY; SEQUENCE ALIGNMENT; STATISTICAL MODEL;

ALLELES; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL NUCLEUS; CYPRINIFORMES; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; HYBRIDIZATION, GENETIC; JAPAN; LIKELIHOOD FUNCTIONS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYPLOIDY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

COBITIDAE; COBITIS; COBITIS BIWAE; COBITIS STRIATA; COBITIS TAENIA; CYPRINIFORMES; TELEOST FISH;

EID: 77954458250     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2010.04.021     Document Type: Article

References (83)

1. Adachi J., Hasegawa M. MOLPHY version 2.3: programs for molecular phylogenetics based on maximum likelihood. Comput. Sci. Monogr. 1996, 28:1-150.
2. Allendorf F.W., Thorgaard G.A. Tetraploidy and the evolution of salmonid fishes. Evolutionary Genetics of Fishes 1984, 1-53. Plenum, New York. B.J. Turner (Ed.).
3. Alves M.J., Coelho M.M., Collares-Pereira M.J. Diversity in the reproductive modes of females of the Rutilus alburnoides complex (Teleostei, Cyprinidae): a way to avoid the genetic constraints of uniparentalism. Mol. Biol. Evol. 1998, 15:1233-1242.
4. Alves M.J., Coelho M.M., Prospero M.I., Collares-Pereira M.J. Production of fertile unreduced sperm by hybrid males of the Rutilus alburnoides complex (Teleostei, Cyprinidae): an alternative route to genome tetraploidization in unisexuals. Genetics 1999, 151:277-283.
5. Alves M.J., Collares-Pereira M.J., Dowling T.E., Coelho M.M. The genetics of maintenance of an all-male lineage in the Squalius alburnoides complex. J. Fish Biol. 2002, 60:649-662.
6. Arai K. Genetics of the loach, Misgurnus anguillicaudatus: recent progress and perspecte. Folia Biol. (Krakow) 2003, 51(Supp. 1):107-117.
7. Asahida T., Kobayashi T., Saitoh K., Nakayama I. Tissue preservation and total DNA extraction from fish stored at ambient temperature using buffers containing high concentration of urea. Fish. Sci. 1996, 62:727-730.
8. Binet M.C., Angers B. Genetic identification of members of the Phoxinus eos-neogaeus hybrid complex. J. Fish Biol. 2005, 67:1169-1177.
9. Chapman M.A., Burke J.M. Genetic divergence and hybrid speciation. Evolutiion 2007, 61:1773-1780.
10. Chen W.J., Bonillo C., Lecointre G. Repeatability of clades as a criterion of reliability: a case study for molecular phylogeny of acanthomorph (Teleostei) with larger number of taxa. Mol. Phylogenet. Evol. 2003, 26:262-288.
11. Chen W.-J., Miya M., Saitoh K., Mayden R.L. Phylogenetic utility of two existing and four novel nuclear loci in reconstructing tree of life of ray-finned fishes: the order Cypriniformes (Ostariophysi) as a case study. Gene 2008, 423:125-134.
12. Choleva L., Apostolou A., Rab P., Janko K. Making it on their own: sperm-dependent hybrid fishes (Cobitis) switch the sexual hosts and expand beyond the ranges of their original sperm donors. Phil. Trans. R. Soc. [B] 2008, 363:2911-2919.
13. Cunha C., Doadrio I., Coelho M.M. Speciation towards tetraploidization after intermediate processes of non-sexual reproduction. Phil. Trans. R. Soc. [B] 2008, 363:2921-2929.
14. Danzmann R.G., Cairney M., Davidson W.S., Ferguson M.M., Gharbi K., Guyomard R., Holm L.-E., Leder E., Okamoto N., Ozaki A., Rexroad C.E., Sakamoto T., Taggart J.B., Woram R.A. A comparative analysis of the rainbow trout genome with 2 other species of fish (Arctic charr and Atlantic salmon) within the tetraploid derivative Salmonidae family (subfamily: Salmoninae). Genome 2005, 48:1037-1051.
15. David L., Blum S., Feldman M.W., Lavi U., Hillel J. Recent duplication of the common carp (Cyprinus carpio L.) genome as revealed by analyses of microsatellite loci. Mol. Biol. Evol. 2003, 20:1425-1434.
16. R 3100 genetic analyzer. BioTechniques 2004, 36:932-933.
17. Ferris S.D. Tetraploidy and the evolution of the catostomid fishes. Evolutionary Genetics of Fishes 1984, 55-93. Plenum, New York. B.J. Turner (Ed.).
18. Flajshans M., Kvasnicka P., Rab P. Genetic studies in Tench (Tinca tinca L.): high incidence of spontaneous triploidy. Aquaculture 1993, 110:243-248.
19. Golubtsov A.S., Krysanov E.Y. Karyological study of some cyprinid species from Ethiopia - the ploidy differences between large and small Barbus of Africa. J. Fish Biol. 1993, 42:445-455.
20. Gromicho M., Coelho M.M., Alves M.J., Collares-Pereira M.J. Cytogenetic analysis of Anaecypris hispanica and its relationship with the paternal ancestor of the diploid-polyploid Squalius alburnoides complex. Genome 2006, 49:1621-1628.
21. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
22. Hasegawa M., Kishino H. Accuracies of the simple methods for estimating the bootstrap probability of a maximum likelihood tree. Mol. Biol. Evol. 1994, 11:142-145.
23. Hiramatsu K., Hosoya K. Thermotaxis and selection of a wintering site in the Ajime-loach, Niwaella delicata. Ichthyol. Res. 2007, 54:238-245.
24. Huelsenbeck J.P., Rannala B. Phylogenetic methods come of age: testing hypotheses in an evolutionary context. Science 1997, 276:227-232.
25. Janko K., Flajshans M., Choleva L., Bohlen J., Slechtova V., Rabova M., Lajbner Z., Slechta V., Ivanova P., Dobrovolov I., Culling M., Persat H., Kotusz J., Rab P. Diversity of European spined loaches (genus Cobitis L.): an update of the geographic distribution of the Cobitis taenia hybrid complex with a description of new molecular tools for species and hybrid determination. J. Fish Biol. 2007, 71(Suppl. C):387-408.
26. Kilic Demurok N., Unlu E. Karyotypes of cyprinid fish Capoeta trutta and Capoeta capoeta umbla (Cyprinidae) from the Tigris River. Turk. J. Zool. 2001, 25:389-393.
27. Kim I.-S., Lee J.-H. Diploid-triploid hybrid complex of the spined loach Cobitis sinensis and C. Longicorpus (Pisces, Cobitidae). Kor. J. Ichthyol. 1990, 2:203-210.
28. Kim I.-S., Lee E.-H. Hybridization experiment of diploid-triploid cobitid fishes, Cobitis sinensis-longicorpus complex (Pisces: Cobitidae). Folia Zool. 2000, 49(Suppl. 1):17-22.
29. Kim S.-Y., Park J.-Y., Kim I.-S. Chromosome of spined loach, Iksookimia yondokensis. Kor. J. Ichthyol. 1999, 11:172-176.
30. Kimizuka Y., Kobayasi H. Geographic distributions of karyological races of Cobitis biwae (Cobitididae). Jpn. J. Ichthyol. 1983, 30:308-312.
31. Kitagawa E., Nakajima J., Hoshino K., Kitagawa T. Geographic distribution and biogeographical origin of the spined loach genus Cobitis in north-eastern Kyushu Island, Japan. Jpn. J. Ichthyol. 2009, 56:7-19.
32. Kitagawa T., Jeon S.R., Kitagawa E., Yoshioka M., Kashiwagi M., Okazaki T. Genetic relationships among the Japanese and Korean striated spined loach complex (Cobitidae: Cobitis) and their phylogenetic positions. Ichthyol. Res. 2005, 52:111-122.
33. Kitagawa T., Watanabe M., Kitagawa E., Yoshioka M., Kashiwagi M., Okazaki T. Phylogeography and the maternal origin of the tetraploid form of the Japanese spined loach, Cobitis biwae, revealed by mitochondrial DNA analysis. Ichthyol. Res. 2003, 50:318-325.
34. Kobayasi H. A cytological study on gynogenesis of the triploid ginbuna (Carassius auratus langsdorfi). Zool. Mag. Tokyo 1971, 80:316-322.
35. Kumazawa Y., Nishida M. Sequence evolution of mitochondrial tRNA genes and deep-branch animal phylogenetics. J. Mol. Evol. 1993, 37:380-398.
36. Kusunoki T., Arai K., Suzuki R. Production of viable gynogens without chromosome duplication in the spinous loach Cobitis biwae. Aquaculture 1994, 119:11-23.
37. Lanave C., Preparata G., Saccone C., Serio G. A new method for calculating evolutionary substitution rates. J. Mol. Evol. 1984, 20:86-93.
38. Leggatt R.A., Iwama G.K. Occurrence of polyploidy in the fishes. Rev. Fish Biol. Fish. 2003, 13:237-246.
39. Lopez J.A., Chen W.-J., Orti G. Esociform phylogeny. Copeia 2004, 2004:449-464.
40. Ludwig A., Belfiore N.M., Pitra C., Svirsky V., Jenneckens I. Genome duplication events and functional reduction of ploidy levels in sturgeon (Acipenser, Huso and Scaphirhynchus). Genetics 2001, 158:1203-1215.
41. Mable B.K. Breaking down taxonomic barriers in polyploidy research. Trends Plant Sci. 2003, 8:582-590.
42. Mallet J. Hybrid speciation. Nature 2007, 446:279-283.
43. 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. 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. Mol. Phylogenet. Evol. 2009, 51:500-514.
44. Mezhzherin S.V., Pavlenko L.I. Genetic structure of diploid-polyploid complex of spined loach genus Cobitis (Cypriniformes, Cobitidae) in the lower Danube. Cytol. Genet. 2007, 41:49-56.
45. Minamori S. Hybridization and classification in spinous loaches. Jpn. J. Ichthyol. 1951, 1:215-225.
46. Minamori S. Local races of spinous loaches. Bull. Biogeogr. Soc. Jpn. 1955, 16-19:278-282.
47. Minamori S. Physiological isolation in Cobitidae. IV. Speciation of two sympatric races of Lake Biwa of the striated spinous loaches. Jpn. J. Zool. 1956, 12:89-104.
48. Miya M., Saitoh K., Wood R., Nishida M., Mayden R.L. New primers for amplifying and sequencing the mitochondrial ND4/ND5 gene region of the Cypriniformes (Actinopterygii: Ostariophysi). Ichthyol. Res. 2006, 53:75-81.
49. Morishima K., Nakamura-Shiokawa Y., Bando E., Li Y.J., Boron A., Khan M.M., Arai K. Cryptic clonal lineages and genetic diversity in the loach Misgurnus anguillicaudatus (Teleostei: Cobitidae) inferred from nuclear and mitochondrial DNA analyses. Genetica 2008, 132:159-171.
50. Nelson J.S. Fishes of the world 2006, John Wiley, Sons, New Jersey. 4th ed.
51. Niwa H. A new species of Cobitidae from Japan (Cobitis delicata). Zool. Mag. Tokyo 1937, 49:71-74.
52. Ohno S. Evolution by Gene Duplication 1970, Springer, Berlin.
53. Otto S.P. The evolutionary consequences of polyploidy. Cell 2007, 131:452-462.
54. Raicu P., Taisescu E. Misgurnus fossilis, a tetraploid fish species. J. Hered. 1972, 63:92-94.
55. Saitoh K. Multiple sex-chromosome system in a loach fish. Cytogenet. Cell Genet. 1989, 52:62-64.
56. Saitoh K. Mitotic and meiotic analyses of the 'large race' of Cobitis striata, a polyploid spined loach of hybrid origin. Folia Biol. (Krakow) 2003, 51(Suppl. 1):101-105.
57. Saitoh K., Aizawa H. Local differentiation within the striated spined loach (the striata type of Cobitis taenia complex). Jpn. J. Ichthyol. 1987, 34:334-345.
58. Saitoh K., Chen W.-J. Reducing cloning artifacts for recovery of allelic sequences by T7 endonuclease I cleavage and single re-extension of PCR products - a benchmark. Gene 2008, 423:92-95.
59. Saitoh K., Kim I.-S., Lee E.-H. Mitochondrial gene introgression between spined loaches via hybridogenesis. Zool. Sci. 2004, 21:795-798.
60. Saitoh K., Kobayashi T., Ueshima R., Numachi K. Analyses of mitochondrial and satellite DNAs on spined loaches of the genus Cobitis from Japan have revealed relationships among populations of three diploid-tetraploid complexes. Folia Zool. 2000, 49(Suppl. 1):9-16.
61. Saitoh K., Matsuda M. An introduction to the spined loaches in the Lake Biwa Basin. Ann. Rep. Biwako-Bunkakan 1990, 8:19-23.
62. Saitoh K., Sado T., Mayden R.L., Hanzawa N., Nakamura K., Nishida M., Miya M. 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. J. Mol. Evol. 2006, 63:826-841.
63. Saitoh, K., Sado, T., Doosey, M., Bart Jr., H.L., Inoue, J.G., Nishida, M., Mayden, R.L., Miya, M., in press. Evidence from mitochondrial genomics supports the lower Mesozoic of South Asia as the time and place of basal divergence of cypriniform fishes (Actinopterygii: Ostariophysi). Zool. J. Linn. Soc.
64. Shimizu T. Life history of a Japanese spinous loach, Cobitis takatsuensis in Shikoku Island. Jpn. J. Ichthyol. 2002, 49:33-40.
65. Shimodaira H., Hasegawa M. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 2001, 17:1246-1247.
66. Shimodaira H. An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 2002, 51:492-508.
67. Slechtova V., Bohlen J., Perdices A. Molecular phylogeny of the freshwater fish family Cobitidae (Cypriniformes: Teleostei): delimitation of genera, mitochondrial introgression and evolution of sexual dimorphism. Mol. Phylogenet. Evol. 2008, 47:812-831.
68. Suzawa Y. A new loach, Cobitis shikokuensis (Teleostei: Cobitidae), from Shikoku Island. Ichthyol. Res. 2006, 53:315-322.
69. Suzuki A. Chromosomal evolution of the suborder Cyprinoidei, with special reference to topical problems of phylogenetic relationships of their families. Cytobios 1996, 87:169-179.
70. Tamura K., Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 1993, 10:512-526.
71. Ueno K. Karyotypes in loaches with special reference to polymorphism and polyploidy. Mar. Sci. Mon. 1981, 13:60-70.
72. Ueno K., Iwai S., Ojima Y. Karyotypes and geographic distribution in the genus Cobitis (Cobitidae). Bull. Jpn. Soc. Sci. Fish. 1980, 46:9-18.
73. Uyeno T., Smith G.R. Tetraploid origin of karyotype of catostomid fishes. Science 1972, 175:644-646.
74. Van de Peer Y., Maere S., Meyer A. The evolutionary significance of ancient genome duplications. Nat. Rev. Genet. 2009, 10:725-732.
75. Vasil'ev V.P., Akimova N.V., Emel'yanova N.G., Pavlov D.A., Vasil'eva E.D. Reproductive capacities in the polyploid males of spined loaches from the unisexual-bisexual complex, occurred in the Moscow River. Folia Biol. (Krakow) 2003, 51(Suppl. 1):67-73.
76. Vasil'ev V.P., Lebedeva E.B., Vasil'eva E.D., Ryskov A.P. Monoclonal and de novo arising tetraploid forms of the genus Cobitis (Cobitidae) from different clonal-bisexual complexes. Dokl. Biol. Sci. 2007, 416:559-562.
77. Vasil'ev V.P., Vasil'eva K.D., Osinov A.G. Evolution of a diploid-triploid-tetraploid complex in fishes of the genus Cobitis (Pisces, Cobitidae). Evolution and Ecology of Unisexual Vertebrates. Bull 1989, vol. 466:135-169. NY State Museum, Albany.
78. Willett C.E., Cherry J.J., Steiner L.A. Characterization and expression of the recombination activating genes (rag1 and rag2) of zebrafish. Immunogenetics 1997, 45:394-404.
79. Yamauchi A., Hosokawa A., Nagata H., Shimoda M. Triploid bridge and role of parthenogenesis in the evolution of autopolyploidy. Am. Nat. 2004, 164:101-112.
80. Yang Z. Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J. Mol. Evol. 1994, 39:306-314.
81. Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. CABIOS 1997, 13:555-556.
82. Yu Q., Zhou R. Analyses of genetic diversities in Chinese freshwater fishes. Chin. Biodiv. 1996, 4(Suppl):1-5.
83. Yu X., Zhou T., Li K., Li Y., Zhou M. On the karyosystematics of cyprinid fishes and a summary of fish chromosome studies in China. Genetica 1987, 72:225-236.