Wild sex in zebrafish: Loss of the natural sex determinant in domesticated strains

Genetics

Volumn 198, Issue 3, 2014, Pages 1291-1308

  Wilson, Catherine A ^a   High, Samantha K ^a   McCluskey, Braedan M ^a   Amores, Angel ^a   Yan, Yi Lin ^a   Titus, Tom A ^a   Anderson, Jennifer L ^b   Batzel, Peter ^a   Carvan, Michael J ^c   Schartl, Manfred ^d   Postlethwait, John H ^a  

^a UNIVERSITY OF OREGON   (United States)

^b INSERM   (France)

^c UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^d UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA; DNA;

ALLELE; ARTICLE; CHROMOSOME 4; CLADISTICS; DNA BASE COMPOSITION; DOMESTICATION; ENVIRONMENTAL TEMPERATURE; FEMALE; GENE LINKAGE DISEQUILIBRIUM; GENETIC VARIABILITY; GENOMICS; GENOTYPE; HAPLOGROUP; HETEROZYGOTE; MALE; MATING; MITOCHONDRIAL GENOME; MONOPHYLY; NATURAL POPULATION; NONHUMAN; ORYZIAS LATIPES; PHENOTYPE; PHYLOGENOMICS; PHYLOGENY; POPULATION GENETICS; SEX; SEX CHROMOSOME; SEX DETERMINATION; SEX DIFFERENTIATION; SEX TRANSFORMATION; SINGLE NUCLEOTIDE POLYMORPHISM; SRY GENE; TELOMERE; Y CHROMOSOME; ZEBRA FISH; ANIMAL; CHROMOSOME MAP; CHROMOSOME SEGREGATION; CROSS BREEDING; GENE LOCUS; GENETICS; GENOME; ORYZIAS; REPRODUCIBILITY; RESTRICTION MAPPING; SEX DETERMINATION PROCESS;

ANIMALS; CHROMOSOME MAPPING; CHROMOSOME SEGREGATION; CROSSES, GENETIC; DNA; FEMALE; GENETIC LOCI; GENOME; GENOTYPE; MALE; ORYZIAS; PHENOTYPE; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; REPRODUCIBILITY OF RESULTS; RESTRICTION MAPPING; SEX CHROMOSOMES; SEX DETERMINATION PROCESSES; ZEBRAFISH;

EID: 84908627899     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.169284     Document Type: Article

References (115)

1. Abozaid, H., S. Wessels, and G. Horstgen-Schwark, 2011 Effect of rearing temperatures during embryonic development on the phenotypic sex in zebrafish (Danio rerio). Sex Dev. 5: 259-265.
2. Abozaid, H., S. Wessels, and G. Horstgen-Schwark, 2012 Elevated temperature applied during gonadal transformation leads to male bias in zebrafish (Danio rerio). Sex Dev. 6: 201-209.
3. Amores, A., and J. H. Postlethwait, 1999 Banded chromosomes and the zebrafish karyotype. Methods Cell Biol. 60: 323-338.
4. Amores, A., J. Catchen, A. Ferrara, Q. Fontenot, and J. H. Postlethwait, 2011 Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted gar, an outgroup for the teleost genome duplication. Genetics 188: 799-808.
5. Anderson, J. L., A. Rodriguez-Mari, I. Braasch, A. Amores, P. Hohenlohe et al., 2012 Multiple sex-associated regions and a putative sex chromosome in zebrafish revealed by RAD mapping and population genomics. PLoS ONE 7: e40701.
6. Atwell, S., Y. S. Huang, B. J. Vilhjalmsson, G. Willems, M. Horton et al., 2010 Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465: 627-631.
7. Bachtrog, D., J. E. Mank, C. L. Peichel, M. Kirkpatrick, S. P. Otto et al., 2014 Sex determination: Why so many ways of doing it? PLoS Biol. 12: e1001899.
8. Baird, N. A., P. D. Etter, T. S. Atwood, M. C. Currey, A. L. Shiver et al., 2008 Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3: e3376.
9. Benjamini, Y., and Y. Hochberg, 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc., B 57: 289-300.
10. Braasch, I., Y. Guiguen, R. Loker, J. H. Letaw, A. Ferrara et al., 2014 Connectivity of vertebrate genomes: paired-related homeobox (Prrx) genes in spotted gar, basal teleosts, and tetrapods. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 163: 24-36.
11. Bradley, K. M., J. P. Breyer, D. B. Melville, K. W. Broman, E. W. Knapik et al., 2011 An SNP-based linkage map for zebrafish reveals sex determination loci. G3 (Bethesda) 1: 3-9.
12. Brown, A. R., L. K. Bickley, T. A. Ryan, G. C. Paull, P. B. Hamilton et al., 2012a Differences in sexual development in inbred and outbred zebrafish (Danio rerio) and implications for chemical testing. Aquat. Toxicol. 112-113: 27-38.
13. Brown, K. H., K. P. Dobrinski, A. S. Lee, O. Gokcumen, R. E. Mills et al., 2012b Extensive genetic diversity and substructuring among zebrafish strains revealed through copy number variant analysis. Proc. Natl. Acad. Sci. USA 109: 529-534.
14. Bull, J. J., 1983 Evolution of Sex Determining Mechanisms. Benjamin/Cummings, Menlo Park, CA.
15. Catchen, J. M., A. Amores, P. Hohenlohe, W. Cresko, and J. H. Postlethwait, 2011 Stacks: building and genotyping Loci de novo from short-read sequences. G3 (Bethesda) 1: 171-182.
16. Catchen, J., P. A. Hohenlohe, S. Bassham, A. Amores, and W. A. Cresko, 2013 Stacks: an analysis tool set for population genomics. Mol. Ecol. 22: 3124-3140.
17. Chakrabarti, S., G. Streisinger, F. Singer, and C. Walker, 1983 Frequency of gamma-ray induced specific locus and recessive lethal mutations in mature germ cells of the zebrafish, Brachydanio rerio. Genetics 103: 109-123.
18. Charlesworth, B., 1996 The evolution of chromosomal sex determination and dosage compensation. Curr. Biol. 6: 149-162.
19. Charlesworth, D., B. Charlesworth, and G. Marais, 2005 Steps in the evolution of heteromorphic sex chromosomes. Heredity 95: 118-128.
20. Charnier, M., 1966 Action of temperature on sex-ratio in agama agamas embryo (Agamidae lacertilien). C. R. Seances Soc. Biol. Fil. 160: 620-622.
21. Chen, S., G. Zhang, C. Shao, Q. Huang, G. Liu et al., 2014 Wholegenome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat. Genet. 46: 253-260.
22. Cheung, C. H., J. M. Chiu, and R. S. Wu, 2014 Hypoxia turns genotypic female medaka fish into phenotypic males. Ecotoxicology 23: 1260-1269.
23. Daga, R. R., G. Thode, and A. Amores, 1996 Chromosome complement, C-banding, Ag-NOR and replication banding in the zebrafish Danio rerio. Chromosome Res. 4: 29-32.
24. Dranow, D. B., R. P. Tucker, and B. W. Draper, 2013 Germ cells are required to maintain a stable sexual phenotype in adult zebrafish. Dev. Biol. 376: 43-50.
25. Engeszer, R. E., L. B. Patterson, A. A. Rao, and D. M. Parichy, 2007 Zebrafish in the wild: a review of natural history and new notes from the field. Zebrafish 4: 21-40.
26. Gornung, E., I. Gabrielli, S. Cataudella, and L. Sola, 1997 CMA3-banding pattern and fluorescence in situ hybridization with 18S rRNA genes in zebrafish chromosomes. Chromosome Res. 5: 40-46.
27. Gornung, E., S. De Innocentiis, F. Annesi, and L. Sola, 2000 Zebrafish 5S rRNA genes map to the long arms of chromosome 3. Chromosome Res. 8: 362.
28. Hattori, R. S., R. J. Gould, T. Fujioka, T. Saito, J. Kurita et al., 2007 Temperature-dependent sex determination in Hd-rR medaka Oryzias latipes: gender sensitivity, thermal threshold, critical period, and DMRT1 expression profile. Sex Dev. 1: 138-146.
29. Hayashi, Y., H. Kobira, T. Yamaguchi, E. Shiraishi, T. Yazawa et al., 2010 High temperature causes masculinization of genetically female medaka by elevation of cortisol. Mol. Reprod. Dev. 77: 679-686.
30. Heule, C., W. Salzburger, and A. Bohne, 2014 Genetics of sexual development: an evolutionary playground for fish. Genetics 196: 579-591.
31. Hohenlohe, P. A., S. Bassham, P. D. Etter, N. Stiffler, E. A. Johnson et al., 2010 Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 6: e1000862.
32. Houwing, S., L. M. Kamminga, E. Berezikov, D. Cronembold, A. Girard et al., 2007 A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in zebrafish. Cell 129: 69-82.
33. Howe, K., M. D. Clark, C. F. Torroja, J. Torrance, C. Berthelot et al., 2013 The zebrafish reference genome sequence and its relationship to the human genome. Nature 496: 498-503.
34. Johnson, S. L., M. A. Gates, M. Johnson, W. S. Talbot, S. Horne et al., 1996 Centromere-linkage analysis and consolidation of the zebrafish genetic map. Genetics 142: 1277-1288.
35. Kakioka, R., T. Kokita, H. Kumada, K. Watanabe, and N. Okuda, 2013 A RAD-based linkage map and comparative genomics in the gudgeons (genus Gnathopogon, Cyprinidae). BMC Genomics 14: 32.
36. Kamiya, T., W. Kai, S. Tasumi, A. Oka, T. Matsunaga et al., 2012 A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu). PLoS Genet. 8: e1002798.
37. Kasahara, M., K. Naruse, S. Sasaki, Y. Nakatani, W. Qu et al., 2007 The medaka draft genome and insights into vertebrate genome evolution. Nature 447: 714-719.
38. Kelly, P. D., F. Chu, I. G. Woods, P. Ngo-Hazelett, T. Cardozo et al., 2000 Genetic linkage mapping of zebrafish genes and ESTs. Genome Res. 10: 558-567.
39. Kikuchi, K., and S. Hamaguchi, 2013 Novel sex-determining genes in fish and sex chromosome evolution. Dev. Dyn. 242: 339-353.
40. Kirchen, R. V., and W. R. West, 1976 The Japanese Medaka: Its Care and Development. Carolina Biological Supply Co., Burlington, NC.
41. Kitano, T., Y. Hayashi, E. Shiraishi, and Y. Kamei, 2012 Estrogen rescues masculinization of genetically female medaka by exposure to cortisol or high temperature. Mol. Reprod. Dev. 79: 719-726.
42. Knapik, E. W., A. Goodman, O. S. Atkinson, C. T. Roberts, M. Shiozawa et al., 1996 A reference cross DNA panel for zebrafish (Danio rerio) anchored with simple sequence length polymorphisms. Development 123: 451-460.
43. Knapik, E. W., A. Goodman, M. Ekker, M. Chevrette, J. Delgado et al., 1998 A microsatellite genetic linkage map for zebrafish (Danio rerio). Nat. Genet. 18: 338-343.
44. Kobayashi, Y., Y. Nagahama, and M. Nakamura, 2013 Diversity and plasticity of sex determination and differentiation in fishes. Sex Dev. 7: 115-125.
45. Kondo, M., U. Hornung, I. Nanda, S. Imai, T. Sasaki et al., 2006 Genomic organization of the sex-determining and adjacent regions of the sex chromosomes of medaka. Genome Res. 16: 815-826.
46. Kondo, M., I. Nanda, M. Schmid, and M. Schartl, 2009 Sex determination and sex chromosome evolution: insights from medaka. Sex Dev. 3: 88-98.
47. Lang, J. W., and H. V. Andrews, 1994 Temperature-dependent sex determination in crocodilians. J. Exp. Zool. 270: 28-44.
48. Larney, C., T. L. Bailey, and P. Koopman, 2014 Switching on sex: transcriptional regulation of the testis-determining gene Sry. Development 141: 2195-2205.
49. Lawrence, C., J. P. Ebersole, and R. V. Kesseli, 2008 Rapid growth and out-crossing promote female development in zebrafish (Danio rerio). Environ. Biol. Fishes 81: 239-246.
50. Liew, W. C., and L. Orban, 2014 Zebrafish sex: a complicated affair. Brief Funct Genomics 13: 172-187.
51. Liew, W. C., R. Bartfai, Z. Lim, R. Sreenivasan, K. R. Siegfried et al., 2012 Polygenic sex determination system in zebrafish. PLoS ONE 7: e34397.
52. Loucks, E., and M. J. Carvan, 2004 Strain-dependent effects of developmental ethanol exposure in zebrafish. Neurotoxicol. Teratol. 26: 745-755.
53. Matsuda, M., Y. Nagahama, A. Shinomiya, T. Sato, C. Matsuda et al., 2002 DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417: 559-563.
54. Mayden, R. L., K. L. Tang, K. W. Conway, J. Freyhof, S. Chamberlain et al., 2007 Phylogenetic relationships of Danio within the order cypriniformes: a framework for comparative and evolutionary studies of a model species. J. Exp. Zoolog. B Mol. Dev. Evol. 308B: 642-654.
55. Merchant-Larios, H., and V. Diaz-Hernandez, 2013 Environmental sex determination mechanisms in reptiles. Sex Dev. 7: 95-103.
56. Mills, M. G., R. J. Nuckels, and D. M. Parichy, 2007 Deconstructing evolution of adult phenotypes: genetic analyses of kit reveal homology and evolutionary novelty during adult pigment pattern development of Danio fishes. Development 134: 1081-1090.
57. Ming, R., A. Bendahmane, and S. S. Renner, 2011 Sex chromosomes in land plants. Annu. Rev. Plant Biol. 62: 485-514.
58. Mork, L., M. Czerwinski, and B. Capel, 2014 Predetermination of sexual fate in a turtle with temperature-dependent sex determination. Dev. Biol. 386: 264-271.
59. Mullins, M. C., M. Hammerschmidt, P. Haffter, and C. NussleinVolhard, 1994 Large-scale mutagenesis in the zebrafish: in search of genes controlling development in a vertebrate. Curr. Biol. 4: 189-202.
60. Myosho, T., H. Otake, H. Masuyama, M. Matsuda, Y. Kuroki et al., 2012 Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis. Genetics 191: 163-170.
61. Nanda, I., M. Kondo, U. Hornung, S. Asakawa, C. Winkler et al., 2002 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.
62. Nanda, I., U. Hornung, M. Kondo, M. Schmid, and M. Schartl, 2003 Common spontaneous sex-reversed XX males of the medaka Oryzias latipes. Genetics 163: 245-251.
63. Orban, L., R. Sreenivasan, and P. E. Olsson, 2009 Long and winding roads: testis differentiation in zebrafish. Mol. Cell. Endocrinol. 312: 35-41.
64. Ota, S., and A. Kawahara, 2014 Zebrafish: a model vertebrate suitable for the analysis of human genetic disorders. Congenit. Anom. 54: 8-11.
65. Parnell, N. F., and J. T. Streelman, 2013 Genetic interactions controlling sex and color establish the potential for sexual conflict in Lake Malawi cichlid fishes. Heredity 110: 239-246.
66. Peichel, C. L., J. A. Ross, C. K. Matson, M. Dickson, J. Grimwood et al., 2004 The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome. Curr. Biol. 14: 1416-1424.
67. Pelegri, F., and S. Schulte-Merker, 1999 A gynogenesis-based screen for maternal-effect genes in the zebrafish, Danio rerio. Methods Cell Biol. 60: 1-20.
68. Phillips, R. B., A. Amores, M. R. Morasch, C. Wilson, and J. H. Postlethwait, 2006 Assignment of zebrafish genetic linkage groups to chromosomes. Cytogenet. Genome Res. 114: 155-162.
69. Pijnacker, L. P., and M. A. Ferwerda, 1995 Zebrafish chromosome banding. Genome 38: 1052-1055.
70. Postlethwait, J. H., S. Johnson, C. N. Midson, W. S. Talbot, M. Gates et al., 1994 A genetic linkage map for the zebrafish. Science 264: 699-703.
71. Postlethwait, J. H., I. G. Woods, P. Ngo-Hazelett, Y. L. Yan, P. D. Kelly et al., 2000 Zebrafish comparative genomics and the origins of vertebrate chromosomes. Genome Res. 10: 1890-1902.
72. Pradhan, A., H. Khalaf, S. A. Ochsner, R. Sreenivasan, J. Koskinen et al., 2012 Activation of NF-kappaB protein prevents the transition from juvenile ovary to testis and promotes ovarian development in zebrafish. J. Biol. Chem. 287: 37926-37938.
73. Rauch, G. J., M. Granato, and P. Haffter, 1997 A polymorphic zebrafish line for genetic mapping using SSLPs on high-percentage agarose gels. Tech. Tips Online 2: 148-150.
74. Roberts, R. B., J. R. Ser, and T. D. Kocher, 2009 Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes. Science 326: 998-1001.
75. Rodríguez-Marí, A., and J. H. Postlethwait, 2011 The role of Fanconi anemia/BRCA genes in zebrafish sex determination. Methods Cell Biol. 105: 461-490.
76. Rodríguez-Marí, A., Y. L. Yan, R. A. Bremiller, C. Wilson, C. Cañestro et al., 2005 Characterization and expression pattern of zebrafish anti-Müllerian hormone (amh) relative to sox9a, sox9b, and cyp19a1a, during gonad development. Gene Expr. Patterns 5: 655-667.
77. Rodriguez-Mari, A., and C. Canestro, R. A. Bre-Miller, A. Nguyen-Johnson, K. Asakawa et al., 2010 Sex reversal in zebrafish fancl mutants is caused by Tp53-mediated germ cell apoptosis. PLoS Genet. 6: e1001034.
78. Rodriguez-Mari, A., C. Wilson, T. A. Titus, and C. Canestro, R. A. Bre-Miller et al., 2011 Roles of brca2 (fancd1) in oocyte nuclear architecture, gametogenesis, gonad tumors, and genome stability in zebrafish. PLoS Genet. 7: e1001357.
79. Ross, J. A., J. R. Urton, J. Boland, M. D. Shapiro, and C. L. Peichel, 2009 Turnover of sex chromosomes in the stickleback fishes (gasterosteidae). PLoS Genet. 5: e1000391.
80. Saitoh, K., T. Sado, M. H. Doosey, H. L. Bart, J. G. Inoue et al., 2011 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. 161: 633-662.
81. Sato, T., T. Endo, K. Yamahira, S. Hamaguchi, and M. Sakaizumi, 2005b Induction of female-to-male sex reversal by high temperature treatment in Medaka, Oryzias latipes. Zoolog. Sci. 22: 985-988.
82. Schreeb, K. H., G. Groth, W. Sachsse, and K. J. Freundt, 1993 The karyotype of the zebrafish (Brachydanio rerio). J. Exp. Anim. Sci. 36: 27-31.
83. Selim, K. M., A. Shinomiya, H. Otake, S. Hamaguchi, and M. Sakaizumi, 2009 Effects of high temperature on sex differentiation and germ cell population in medaka, Oryzias latipes. Aquaculture 289: 340-349.
84. Ser, J. R., R. B. Roberts, and T. D. Kocher, 2010 Multiple interacting loci control sex determination in lake Malawi cichlid fish. Evolution 64: 486-501.
85. Seth, A., D. L. Stemple, and I. Barroso, 2013 The emerging use of zebrafish to model metabolic disease. Dis. Model. Mech. 6: 1080-1088.
86. Shang, E. H., R. M. Yu, and R. S. Wu, 2006 Hypoxia affects sex differentiation and development, leading to a male-dominated population in zebrafish (Danio rerio). Environ. Sci. Technol. 40: 3118-3122.
87. Sharma, K. K., O. P. Sharma, and N. K. Tripathi, 1998 Female heterogamety in Danio rerio (Cypriniformes: Cyprinidae). Proc. Nat. Acad. Sci. India 68B: 123-126.
88. Siegfried, K. R., 2010 In search of determinants: gene expression during gonadal sex differentiation. J. Fish Biol. 76: 1879-1902.
89. Siegfried, K. R., and C. Nusslein-Volhard, 2008 Germ line control of female sex determination in zebrafish. Dev. Biol. 324: 277-287.
90. Slanchev, K., J. Stebler, G. de la Cueva-Mendez, and E. Raz, 2005 Development without germ cells: the role of the germ line in zebrafish sex differentiation. Proc. Natl. Acad. Sci. USA 102: 4074-4079.
91. Smith, C. A., K. N. Roeszler, T. Ohnesorg, D. M. Cummins, P. G. Farlie et al., 2009 The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461: 267-271.
92. Sola, L., and E. Gornung, 2001 Classical and molecular cytogenetics of the zebrafish, Danio rerio (Cyprinidae, Cypriniformes): an overview. Genetica 111: 397-412.
93. Stamatakis, A., 2014 RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313.
94. Storey, J., and R. Tibshirani, 2003 Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. USA 100: 9440-9445.
95. Streisinger, G., C. Walker, N. Dower, D. Knauber, and F. Singer, 1981 Production of clones of homozygous diploid zebra fish (Brachydanio rerio). Nature 291: 293-296.
96. Takahashi, H., 1977 Juvenile hermaphroditism in the zebrafish, Brachydanio rerio. Bull. Fac. Fish. Hokkaido Univ. 28: 57-65.
97. Takehana, Y., M. Matsuda, T. Myosho, M. L. Suster, K. Kawakami et al., 2014 Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena. Nat. Commun. 5: 4157.
98. Takehana, Y., K. Naruse, S. Hamaguchi, and M. Sakaizumi, 2007 Evolution of ZZ/ZW and XX/XY sex-determination systems in the closely related medaka species, Oryzias hubbsi and O. dancena. Chromosoma 116: 463-470.
99. Tang, K. L., M. K. Agnew, M. V. Hirt, T. Sado, L. M. Schneider et al., 2010 Systematics of the subfamily Danioninae (Teleostei: Cypriniformes: Cyprinidae). Mol. Phylogenet. Evol. 57: 189-214.
100. Tong, S. K., H. J. Hsu, and B. C. Chung, 2010 Zebrafish monosex population reveals female dominance in sex determination and earliest events of gonad differentiation. Dev. Biol. 344: 849-856.
101. Traut, W., and H. Winking, 2001 Meiotic chromosomes and stages of sex chromosome evolution in fish: zebrafish, platyfish and guppy. Chromosome Res. 9: 659-672.
102. Uchida, D., M. Yamashita, T. Kitano, and T. Iguchi, 2002 Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. J. Exp. Biol. 205: 711-718.
103. Villamizar, N., L. Ribas, F. Piferrer, L. M. Vera, and F. J. SanchezVazquez, 2012 Impact of daily thermocycles on hatching rhythms, larval performance and sex differentiation of zebrafish. PLoS ONE 7: e52153.
104. Walker-Durchanek, R. C., 1980 Induction of germ line mutations by gamma-irradiation of zebrafish embryos, p. 96. Ph.D. thesis, Department of Biology, University of Oregon, Eugene, OR.
105. Wang, X., R. Bartfai, I. Sleptsova-Freidrich, and L. Orban, 2007 The timing and extent of ‘juvenile ovary’ phase are highly variable during zebrafish testis differentiation. J. Fish Biol. 70: 33-44.
106. Westerfield, M., 2007 The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish Danio (Brachydanio) rerio, Ed. 5. M. Westerfield, Eugene
107. Whiteley, A. R., A. Bhat, E. P. Martins, R. L. Mayden, M. Arunachalam et al., 2011 Population genomics of wild and laboratory zebrafish (Danio rerio). Mol. Ecol. 20: 4259-4276.
108. Wilkinson, R. N., C. Jopling, and F. J. van Eeden, 2014 Zebrafish as a model of cardiac disease. Prog. Mol. Biol. Transl. Sci. 124: 65-91.
109. Woods, I. G., P. D. Kelly, F. Chu, P. Ngo-Hazelett, Y. L. Yan et al., 2000 A comparative map of the zebrafish genome. Genome Res. 10: 1903-1914.
110. Woods, I. G., C. Wilson, B. Friedlander, P. Chang, D. K. Reyes et al., 2005 The zebrafish gene map defines ancestral vertebrate chromosomes. Genome Res. 15: 1307-1314.
111. Wu, T. D., and S. Nacu, 2010 Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26: 873-881.
112. Yano, A., R. Guyomard, B. Nicol, E. Jouanno, E. Quillet et al., 2012 An immune-related gene evolved into the master sexdetermining gene in rainbow trout, Oncorhynchus mykiss. Curr. Biol. 22: 1423-1428.
113. Yoshimoto, S., and M. Ito, 2011 A ZZ/ZW-type sex determination in Xenopus laevis. FEBS J. 278: 1020-1026.
114. Yoshimoto, S., E. Okada, H. Umemoto, K. Tamura, Y. Uno et al., 2008 A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc. Natl. Acad. Sci. USA 105: 2469-2474.
115. Yoshimoto, S., N. Ikeda, Y. Izutsu, T. Shiba, N. Takamatsu et al., 2010 Opposite roles of DMRT1 and its W-linked paralogue, DM-W, in sexual dimorphism of Xenopus laevis: implications of a ZZ/ZW-type sex-determining system. Development 137: 2519-2526.