The sex determining loci and sex chromosomes in the family salmonidae

Sexual Development

Volumn 3, Issue 2-3, 2009, Pages 78-87

  Davidson, W S ^a   Huang, T K ^a   Fujiki, K ^a   Von Schalburg, K R ^b   Koop, B F ^b  

^a SIMON FRASER UNIVERSITY   (Canada)

^b UNIVERSITY OF VICTORIA   (Canada)

Author keywords

Atlantic salmon; Candidate genes; Salmonids; Sex determination; Y chromosome

Indexed keywords

BIOLOGICAL MARKER; TRANSCRIPTION FACTOR;

ATLANTIC SALMON; DIFFERENTIATION; FLUORESCENCE IN SITU HYBRIDIZATION; GENE DUPLICATION; GENE LOCUS; GENE MAPPING; GENE SEQUENCE; GENETIC MARKER; GENOME; LINKAGE ANALYSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SALMONID; SEX CHROMOSOME; SEX DETERMINATION; SEX LINKAGE; X CHROMOSOME; Y CHROMOSOME;

ANIMALS; CHROMOSOME MAPPING; GENE DUPLICATION; IN SITU HYBRIDIZATION, FLUORESCENCE; SALMONIDAE; SEX CHROMOSOMES; SEX DETERMINATION PROCESSES;

SALMO SALAR; SALMONIDAE;

EID: 69249101339     PISSN: 16615425     EISSN: 16615433     Source Type: Journal    
DOI: 10.1159/000223073     Document Type: Review

References (96)

1. Alfaqih MA, Phillips RB, Wheeler PA, Thorgaard GH: The cutthroat trout Y chromosome is conserved with that of rainbow trout. Cytogenet Genome Res 121: 255-259 (2008).
2. Allendorf FW, Danzmann RG: Secondary tetrasomic segregation of MDH-B and preferential pairing of homeologues in rainbow trout. Genetics 145: 1083-1092 (1997).
3. Allendorf FW, Thorgaard GH: Tetraploidy and the evolution of salmonid fishes, in Turner BJ (ed): Evolutionary Genetics of Fishes, pp 1-53 (Plenum Publishing, New York 1984).
4. Allendorf FW, Gellman WA, Thorgaard GH: Sex-linkage of two enzyme loci in Oncorhynchus mykiss (rainbow trout). Heredity 72: 498-507 (1994).
5. Artieri CG, Mitchell LA, Ng SHS, Parisotto SE, Danzmann RG, et al: Identification of the sex determining locus of Atlantic salmon (Salmo salar) on chromosome 2. Cytogenet Genome Res 112: 152-159 (2006).
6. Azuma T, Takeda K, Doi T, Muto K, Akutsu M, et al: The influence of temperature on sex determination in sockeye salmon Oncorhynchus nerka. Aquaculture 234: 461-473 (2004).
7. Brunelli JP, Thorgaard GH: A new Y-chromosome-specific marker for the Pacific salmon. Trans Am Fisheries Soc 133: 10247-10253 (2004).
8. Brunelli JP, Wertzler KJ, Sundin K, Thorgaard GH: Y-specific sequences and polymorphisms in rainbow trout and Chinook salmon. Genome 51: 739-748 (2008).
9. Chevassus B, Devaux A, Chourrout D, Jalabert B: Production of YY rainbow trout males by self-fertilization of induced hermaphrodites. J Hered 79: 89-92 (1988).
10. Christoffels A, Koh EGL, Chia JM, Brenner S, Aparicio A, Venkatesh B: Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of rayfinned fishes. Mol Biol Evol 21: 1146-1151 (2004). (Pubitemid 38658222)
11. Craig JK, Foote CJ, Wood CC: Evidence for temperature-dependent sex determination in sockeye salmon (Oncorhynchus nerka). Can J Fish Aquat Sci 53: 141-147 (1996).
12. Danzmann RG, Davidson EA, Ferguson MM, Gharbi K, Koop BF, et al: Distribution of ancestral proto-Actinopterygian chromosome arms within the genomes of 4R-derivative salmonid fishes (rainbow trout and Atlantic salmon). BMC Genomics 9: 557 (2008).
13. Devlin RH, Nagahama Y: Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208: 191-364 (2002).
14. Devlin RH, McNeil BK, Groves TDD, Donaldson EM: Isolation of Y-chromosomal DNA probe capable of determining genetic sex in chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquatic Sci 48: 1606-1612 (1991).
15. Devlin RH, Stone GW, Smailus DE: Extensive direct tandem organization of a long repeat DNA sequence on the Y-chromosome of chinook salmon (Oncorhynchus tshawytscha). J Mol Evol 46: 277-287 (1998).
16. Devlin RH, Biagi CA, Smailus DE: Genetic mapping of Y-chromosomal DNA markers in Pacific salmon. Genetica 111: 43-58 (2001).
17. Devlin RH, Park L, Sakhrani DM, Baker JD, Marshall AR, et al: Variation of Y-chromosome DNA markers in Chinook salmon (Oncorhynchus tshawytscha) populations. Can J Fish Aquat Sci 62: 1386-1399 (2005).
18. Du SJ, Devlin RH, Hew CL: Genomic structure of growth hormone genes in chinook salmon (Oncorhynchus tshawytscha) : presence of two functional genes GH-I and GH-II, and a male-specific pseudogene, GH-psi. DNA Cell Biol 12: 739-751 (1993).
19. Felip A, Fujiwara A, Young WP, Wheeler PA, Noakes M, et al: Polymorphism and differentiation of rainbow trout Y-chromosomes. Genome 47: 1105-1113 (2004). (Pubitemid 40393958)
20. Fenske M, Segner H: Aromatase modulation alters gonadal differentiation in developing zebrafish (Danio rerio) . Aquat Toxicol 14: 105-126 (2004). (Pubitemid 38299338)
21. Forbes SH, Knudsen KL, North TW, Allendorf FW: One of two growth hormone genes in coho salmon is sex linked. Proc Natl Acad Sci USA 91: 1628-1631 (1994).
22. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J: Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531-1545 (1999). (Pubitemid 29177561)
23. Frolov SV: Sex chromosome differentiation in salmonid fish. Multiple sex chromosomes in least cisco. Citologiya 32: 659-663 (1990).
24. Fujiki K, Huang K, Lubrieniecki K, Chow W, Munzy DM, et al: Sequence analysis of eight BACs covering four microsatellite loci in the sex determining region of the Atlantic salmon genome. Plant and Animal Genome XVI: P597 (2008).
25. Gharbi K, Gautier A, Danzmann RG, Gharbi S, Sakamoto T, et al: A linkage map for brown trout (Salmo trutta): Chromosome homeologies and comparative genome organization with other salmonid fish. Genetics 172: 2405-2419 (2006).
26. Gilbey J, Verspoor E, McLay A, Houlihan D: A microsatellite linkage map for Atlantic salmon (Salmo salar). Anim Genet 35: 98-105 (2004).
27. Gregory TR, Nicol JA, Tamm H, Kullman B, Kullman K, et al: Eukaryotic genome size database. Nucleic Acids Res 35:D332-D338 (2007).
28. Guyomard R, Mauger S, Tabet-Canale K, Martineau S, Genet C, et al: A type I and type II microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) with presumptive coverage of all chromosome arms. BMC Genomics 7: 302 (2006).
29. Hoegg S, Brinkmann H, Taylor JS, Meyer A: Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J Mol Evol 59: 190-203 (2004). (Pubitemid 39128342)
30. Huang TK, Fujiki K, Li J, Boroevich KA, Koop BF, Davidson WS: Comparative genome analysis of the sex chromosome of Atlantic salmon (Salmo salar) with other teleosts. 8th Int Congress Fish Biol, P45 (2008).
31. Hunter GA, Donaldson EM, Goetz FW, Edgell PR: Production of all female and sterile coho salmon, and experimental evidence for heterogamety. Trans Am Fish Soc 111: 367-372 (1982).
32. Hunter GA, Donaldson EM, Stoss J, Baker II: Production of monosex female groups of chinook salmon (Oncorhynchus tshawytscha) by the fertilization of normal ova with sperm from sex-reversed females. Aquaculture 33: 355-364 (1983).
33. Inoue JG, Miya M, Tsukamoto K, Nishida M: Basal actinopterygian relationships: a mitogenomic perspective on the phylogeny of the ancient fish. Mol Phylogenet Evol 26: 110-120 (2003). (Pubitemid 36029258)
34. Iturra P, Medrano JF, Bagley M, Lam N, Vergara N, Marin JC: Identification of sex chromosome molecular markers using RAPDs and fluorescent in situ hybridization in rainbow trout. Genetica 101: 209-213 (1998). (Pubitemid 28329352)
35. Iturra P, Lam N, de la Fuente M, Vergara N: Characterization of sex chromosomes in rainbow trout and coho salmon using fluorescence in situ hybridization (FISH). Genetica 111: 125-131 (2001a). (Pubitemid 34115220)
36. Iturra P, Bagley M, Vergara N, Imbert P, Medrano JF: Development and characterization of DNA sequence OmyP9 associated with the sex chromosomes in rainbow trout. Heredity 86: 412-419 (2001b).
37. Jankun M, Rab P, Vuorinen J: A karyotype study of vendace, Coregonus albula (Pisces, Coregioninae). Hereditas 115: 291-294 (1991).
38. Johnstone R, Youngson AF: The progeny of sexinverted female Atlantic salmon ( Salmo salar L.). Aquaculture 37: 179-182 (1984).
39. Johnstone R, Simpson TH, Youngson AF, Whitehead C: Sex reversal in salmonid culture. Part II. The progeny of sex reversed rainbow trout. Aquaculture 18: 13-19 (1979).
40. Kikuchi K, Kai W, Hosokawa A, Mizuno N, Suetake H, et al: The sex-determining locus in the tiger pufferfish (Takifugu rubripes). Genetics 175: 2039-2042 (2007).
41. Kondo M, Nanda I, Hornburg U, Asakawa, Shimizu N, et al: Absence of the candidate male sex determining gene dmrt1b(Y) of medaka from other fish species. Curr Biol 13: 416-420 (2003).
42. Koop BF, von Schalburg KR, Leong J, Walker N, Lieph R, et al: A salmonid EST genomic study: genes duplications, phylogeny and micro arrays. BMC Genomics 9: 545 (2008).
43. Lee BY, Hulata G, Kocher TD: Two unlinked loci controlling the sex of blue tilapia (Oreochromis aureus). Heredity 92: 543-549 (2004).
44. Mank JE, Avise JC: Phylogentic conservation of chromosome number in Actinopterygian fishes. Genetica 127: 321-327 (2006).
45. Marshall AR, Knusden KL, Allendorf FW: Linkage disequilibrium between the pseudoautosomal PEPB-1 locus and the sex-determining region of chinook salmon. Heredity 93: 85-97 (2004).
46. Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, et al: DMY is a Y specific DMdomain gene required for male development in the medaka fish. Nature 417: 559-563 (2002).
47. May B, Johnson KR, Wright JE Jr: Sex linkage in salmonids: evidence from a hybridized genome of brook trout and Arctic charr. Biochem Genet 27: 291-301 (1989).
48. McClelland EA, Naish KA: A genetic linkage map for coho salmon (Oncorhynchus kisutch). Anim Genet 39: 169-179 (2008).
49. McGowan C, Davidson WS: The RAPD technique fails to detect a male-specific genetic marker in Atlantic salmon. J Fish Biol 53: 1134-1136 (1998).
50. McKay SJ, Devlin RH, Smith MJ: Phylogeny of Pacific salmon and trout based on growth hormone type-2 and mitochondrial NADH dehydrogenase subunit 3 DNA sequences. Can J Fish Aquat Sci 53: 1165-1176 (1996).
51. Moen T, Hoyheim B, Manuck H, Gomez-Raya L: A linkage map of Atlantic salmon (Salmo salar) reveals an uncommonly large difference in recombination rate between the sexes. Anim Genet 35: 81-92 (2004).
52. Moen T, Hayes B, Baranski M, Berg PR, Kjoglum S, et al: A linkage map of the Atlantic salmon (Salmo salar) based on EST-derived SNP markers. BMC Genomics 9: 223 (2008).
53. Moghadam HK, Ferguson MM, Danzmann RG: Evolution of Hox clusters in Salmonidae: a comparative study analysis between Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss). J Mol Evol 61: 636-649 (2005).
54. Moghadam HK, Ferguson MM, Danzmann RG: Linkage variation at the sex-determining locus within Fraser strain Arctic charr Salvelinus alpinus. J Fish Biol 71: 294-301 (2007).
55. Nagler JJ, Bouma J, Thorgaard GH, Duable DD: High incidence of a male-specific genetic marker in phenotypic female chinook salmon from the Columbia River. Environ Health Perspect 109: 67-69 (2001). (Pubitemid 32118028)
56. Nakayama I, Biagi CA, Koide N, Devlin RH: Identification of a sex-linked GH pseudogene in one of two species of Japanese salmon (Oncorhynchus masou and O. rhondurus). Aquaculture 173: 65-72 (1999). (Pubitemid 29158009)
57. Nanda I, Kondo M, Hornburg U, Asakawa S, Winkler C, et al: A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka (Oryzias latipes). Proc Natl Acad Sci USA 99: 11778-11783 (2002). (Pubitemid 34994475)
58. Nelson JS: Fishes of the World (Wiley, New York 2006).
59. Ng SHS, Artieri CG, Bosdet IE, Chiu R, Danzmann RG, et al: A physical map of the genome of Atlantic salmon (Salmo salar). Genomics 86: 396-404 (2005).
60. Nichols KM, Young WP, Danzmann RG, Robison BD, Rexroad C, et al: A consolidated linkage map for rainbow trout (Oncorhynchus mykiss). Anim Genet 34: 102-115 (2003).
61. Okada H, Matumoto H, Yamazaki F: Functional masculinisation of genetic females in rainbow trout. Bull Jpn Soc Fish 45: 413-419 (1979).
62. Olito C, Brock I: Sex reversal of rainbow trout: Creating an all-female population. Prog Fish Culturist 53: 41-44 (1991).
63. Peichel CL, Ross JA, Matson CK, Dickson M, Grimwood J, et al: The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome. Curr Biol 14: 1416-1424 (2004). (Pubitemid 39123739)
64. Phillips RB, Ihssen PE: Identification of sex chromosomes in lake trout (Salvelinus namaycush). Cytogenet Cell Genet 39: 14-18 (1985).
65. Phillips RB, Rab P: Chromosome evolution in the Salmonidae (Pisces): an update. Biol Rev 76: 1-25 (2001).
66. Phillips RB, Reed KM: Application of fluorescence in situ hybridization (FISH) techniques to fish genetics: a review. Aquaculture 140: 197-216 (1996).
67. Phillips RB, Konkol NR, Reed KM, Stein JD: Chromosome painting supports lack of homology among sex chromosomes in Oncorhynchus, Salmo, and Salvelinus (Salmonidae). Genetica 111: 119-123 (2001).
68. Phillips RB, Matsouka MP, Reed KM: Characterization of charr chromosomes using fluorescence in situ hybridization. Environ Biol Fish 64: 223-228 (2002).
69. Phillips RB, Morasch MR, Park LK, Naish KA, Devlin RH: Identification of the sex chromosome pair in coho salmon (Oncorhynchus kisutch): lack of conservation of the sex linkage group with chinook salmon (Oncorhynchus tshawytscha). Cytogenet Genome Res 111: 166-170 (2005).
70. Phillips RB, DeKoning J, Morasch MR, Park LK, Devlin RH: Identification of the sex chromosome pair in chum salmon (Oncorhynchus keta) and pink salmon (Oncorhynchus gorbuscha). Cytogenet Genome Res 116: 298-304 (2007).
71. Quillet E, Aubard G, Queau I: Mutation in a sex-determining gene in rainbow trout: detection and genetic analysis. Am Genet Assoc 93: 91-99 (2002). (Pubitemid 34755390)
72. Rashid H, Kitano H, Lee KH, Nii S, Shigematsu T, et al: Fugu (Takifugu rubripes) sexual differentiation: Cyp19 regulation and aromatase inhibitor induced testicular development. Sex Dev 1: 311-322 (2007).
73. Reed KM, Bohlander SK, Phillips RB: Microdissection of the Y chromosome and fluorescence in situ hybridization analysis of the sex chromosomes of lake trout, Salvelinus namaycush. Chromosome Res 3: 221-226 (1995).
74. Ross JA, Peichel CL: Molecular cytogenetic evidence of rearrangements on the Y chromosome of the threespine stickleback fish. Genetics 179: 2173-2182 (2008).
75. Sakamoto T, Danzmann RG, Gharbi K, Howard P, Oxaki A, et al: A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates. Genetics 155: 1331-1345 (2000).
76. Schultheis C, Zhou Q, Froschauer A, Nanda I, Selz Y, et al: Molecular analysis of the sexdetermining region of the platyfish Xiphophorus maculatus. Zebrafish 3: 299-309 (2006).
77. Stein J, Phillips RB, Devlin RH: Identification of the Y chromosome in chinook salmon (Oncorhynchus tshawytscha). Cytogenet Cell Genet 92: 108-110 (2001).
78. Stein J, Reed KM, Wilson CC, Phillips RB: A sexlinked microsatellite locus isolated from the Y chromosome of lake charr, Salvelinus namaycush. Environ Biol Fish 64: 211-216 (2002).
79. Steinke D, Salzburger W, Meyer A: Novel relationships among ten fish model species revealed based on a phylogenomic analysis using ESTs. J Mol Evol 62: 772-784 (2006). (Pubitemid 43847227)
80. Taggart TB, Prodohl PA, Ferguson A: Genetic markers for Atlantic salmon ( Salmo salar L.): single locus inheritance and joint segregation analyses of minisatellite (VNTR) DNA loci. Anim Genet 26: 13-20 (1995).
81. Taylor JS, Raes J: Duplication and divergence: the evolution of new genes and old ideas. Ann Rev Genet 38: 615-643 (2004).
82. Thorgaard GH: Heteromorphic sex chromosomes in male rainbow trout. Science 196: 900-902 (1977).
83. Thorgaard GH: Sex chromosomes in the sockeye salmon: a Y-autosome fusion. Can J Genet Cytol 20: 349-354 (1978).
84. Thorgaard GH: Chromosomal differences among rainbow trout populations. Copeia 1983: 650-662 (1983).
85. Thorgaard GH, Bailey GS, Williams D, Buhler DR, Kaattari SL, et al: Status and opportunities for genomics research with rainbow trout. Comp Biochem Physiol B Biochem Mol Biol 133: 609-646 (2002). (Pubitemid 35441085)
86. Thorsen J, Zhu B, Frengen E, Osoegawa K, de Jong PJ, et al: A highly redundant BAC library of Atlantic salmon (Salmo salar): an important tool for salmon projects. BMC Genomics 6: 50 (2005).
87. Volff JN, Nanda I, Schmid M, Schartl M: Governing sex determination in fish: regulatory putsches and ephemeral dictators. Sex Dev 1: 85-99 (2007). (Pubitemid 46714636)
88. von Hofsten J, Olsson PE: Zebrafish sex determination and differentiation: Involvement of FTZ-FI genes. Reprod Biol Endocrinol 3: 1-11 (2005). (Pubitemid 41662764)
89. Williamson KS, May B: Incidence of phenotypic female chinook salmon positive for the male Y-chromosome specific marker OtY1 in the Central Valley, California. J Aquat Anim Health 14: 175-183 (2002).
90. Williamson KS, Phillips R, May B: Characterization of a chromosomal rearrangement responsible for producing 'apparent' XY-female Chinook salmon in California. J Hered 99: 483-490 (2008).
91. Wolfe KH: Yesterdays polyploids and the mystery of diploidization. Nat Rev Genet 2: 333-341 (2001).
92. Woram RA, Gharbi K, Danzmann RG, Sakamoto T, Hoyheim B: Comparative genome analysis of the primary sex determining locus in salmonid fishes. Genome Res 13: 272-280 (2003). (Pubitemid 36575775)
93. Woram RA, McGown C, Stout JA, Gharbi K, Ferguson MM, et al: A genetic linkage map for Arctic charr (Salvelinus alpinus): evidence for higher recombination rates and segregation distortion in hybrid versus pure strain mapping parents. Genome 47: 304-315 (2004).
94. Wright JE, Johnson K, Hollister A, May B: Meiotic models to explain classical linkage, pseudolinkage, and chromosome pairing in tetraploid derivative salmonid genomes. Isozymes Curr Top Biol Med Res 10: 239-260 (1983).
95. Young WP, Wheeler PA, Coryell VH, Leim P, Thorgaard GH: A detailed linkage map of rainbow trout produced using doubled haploids. Genetics 148: 839-850 (1998).
96. Zhang Q, Nakayama I, Fujiwara A, Kobayashi T, Oohara I, et al: Sex identification by malespecific growth hormone pseudogene in Oncorhynchus masou complex and a related hybrid. Genetica 111: 111-118 (2001).