Diversity and Convergence of Sex-Determination Mechanisms in Teleost Fish

Literature Cited

1. 1.

   Beukeboom LW, Perrin N. 2014. The Evolution of Sex Determination Oxford, UK: Oxford Univ. Press
2. 2.

   Bachtrog D, Mank JE, Peichel CL, Kirkpatrick M, Otto SP et al. 2014. Sex determination: Why so many ways of doing it?. PLOS Biol. 12:7e1001899
   [Google Scholar]
3. 3.

   Kirkpatrick M, Jenkins CD. 1989. Genetic segregation and the maintenance of sexual reproduction. Nature 339:6222300–1
   [Google Scholar]
4. 4.

   Kondrashov AS. 1988. Deleterious mutations and the evolution of sexual reproduction. Nature 336:6198435–40
   [Google Scholar]
5. 5.

   Hamilton WD. 1980. Sex versus non-sex versus parasite. Oikos 35:2282–90
   [Google Scholar]
6. 6.

   Hamilton WD, Axelrod R, Tanese R. 1990. Sexual reproduction as an adaptation to resist parasites (a review). PNAS 87:93566–73
   [Google Scholar]
7. 7.

   Parker GA, Baker RR, Smith VG. 1972. The origin and evolution of gamete dimorphism and the male-female phenomenon. J. Theor. Biol. 36:3529–53
   [Google Scholar]
8. 8.

   Lehtonen J, Kokko H. 2011. Two roads to two sexes: unifying gamete competition and gamete limitation in a single model of anisogamy evolution. Behav. Ecol. Sociobiol. 65:3445–59
   [Google Scholar]
9. 9.

   Maynard Smith J. 1978. The Evolution of Sex Cambridge, UK: Cambridge Univ. Press
10. 10.

    Nagahama Y, Chakraborty T, Paul-Prasanth B, Ohta K, Nakamura M 2021. Sex determination, gonadal sex differentiation, and plasticity in vertebrate species. Physiol. Rev. 101:31237–308
    [Google Scholar]
11. 11.

    Kikuchi K, Hamaguchi S. 2013. Novel sex-determining genes in fish and sex chromosome evolution. Dev. Dyn. 242:4339–53
    [Google Scholar]
12. 12.

    Mank JE, Avise JC. 2009. Evolutionary diversity and turn-over of sex determination in teleost fishes. Sex Dev. 3:2–360–67
    [Google Scholar]
13. 13.

    Godwin J. 2009. Social determination of sex in reef fishes. Semin. Cell Dev. Biol. 20:3264–70
    [Google Scholar]
14. 14.

    Gemmell NJ, Todd EV, Goikoetxea A, Ortega-Recalde O, Hore TA. 2019. Natural sex change in fish. Curr. Top. Dev. Biol. 134:71–117
    [Google Scholar]
15. 15.

    Ortega-Recalde O, Goikoetxea A, Hore TA, Todd EV, Gemmell NJ. 2020. The genetics and epigenetics of sex change in fish. Annu. Rev. Anim. Biosci. 8:47–69
    [Google Scholar]
16. 16.

    Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK, Sakamoto T et al. 2012. A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. PNAS 109:82955–59
    [Google Scholar]
17. 17.

    Peichel CL, McCann SR, Ross JA, Naftaly AFS, Urton JR et al. 2020. Assembly of the threespine stickleback Y chromosome reveals convergent signatures of sex chromosome evolution. Genome Biol. 21:177
    [Google Scholar]
18. 18.

    Li M, Sun Y, Zhao J, Shi H, Zeng S et al. 2015. A tandem duplicate of anti-Müllerian hormone with a missense SNP on the Y chromosome is essential for male sex determination in Nile tilapia, Oreochromis niloticus. PLOS Genet. 11:11e1005678
    [Google Scholar]
19. 19.

    Pan Q, Feron R, Yano A, Guyomard R, Jouanno E et al. 2019. Identification of the master sex determining gene in Northern pike (Esox lucius) reveals restricted sex chromosome differentiation. PLOS Genet. 15:8e1008013
    [Google Scholar]
20. 20.

    Hattori RS, Kumazawa K, Nakamoto M, Nakano Y, Yamaguchi T et al. 2022. Y-specific amh allele, amhy, is the master sex-determining gene in Japanese flounder Paralichthys olivaceus. Front. Genet. 13:1007548
    [Google Scholar]
21. 21.

    Kamiya T, Kai W, Tasumi S, Oka A, Matsunaga T et al. 2012. A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu). PLOS Genet. 8:7e1002798
    [Google Scholar]
22. 22.

    Nacif CL, Kratochwil CF, Kautt AF, Nater A, Machado-Schiaffino G et al. 2023. Molecular parallelism in the evolution of a master sex-determining role for the anti-Mullerian hormone receptor 2 gene (amhr2) in Midas cichlids. Mol. Ecol. 32:61398–410
    [Google Scholar]
23. 23.

    Wen M, Pan Q, Jouanno E, Montfort J, Zahm M et al. 2022. An ancient truncated duplication of the anti-Müllerian hormone receptor type 2 gene is a potential conserved master sex determinant in the Pangasiidae catfish family. Mol. Ecol. Resour. 22:62411–28
    [Google Scholar]
24. 24.

    Jasonowicz AJ, Simeon A, Zahm M, Cabau C, Klopp C et al. 2022. Generation of a chromosome-level genome assembly for Pacific halibut (Hippoglossus stenolepis) and characterization of its sex-determining genomic region. Mol. Ecol. Resour. 22:72685–700
    [Google Scholar]
25. 25.

    Imarazene B, Du K, Beille S, Jouanno E, Feron R et al. 2021. A supernumerary “B-sex” chromosome drives male sex determination in the Pachón cavefish, Astyanax mexicanus. Curr. Biol. 31:214800–9.e9
    [Google Scholar]
26. 26.

    Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C et al. 2002. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417:6888559–63
    [Google Scholar]
27. 27.

    Zhang W, Wang H, Brandt DYC, Hu B, Sheng J et al. 2022. The genetic architecture of phenotypic diversity in the Betta fish (Betta splendens). Sci. Adv. 8:38eabm4955
    [Google Scholar]
28. 28.

    Chen S, Zhang G, Shao C, Huang Q, Liu G et al. 2014. Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat. Genet. 46:3253–60
    [Google Scholar]
29. 29.

    Takehana Y, Matsuda M, Myosho T, Suster ML, Kawakami K 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
    [Google Scholar]
30. 30.

    Myosho T, Takehana Y, Hamaguchi S, Sakaizumi M. 2015. Turnover of sex chromosomes in celebensis group medaka fishes. G3 5:122685–91
    [Google Scholar]
31. 31.

    Martínez P, Robledo D, Taboada X, Blanco A, Moser M et al. 2021. A genome-wide association study, supported by a new chromosome-level genome assembly, suggests sox2 as a main driver of the undifferentiatiated ZZ/ZW sex determination of turbot (Scophthalmus maximus). Genomics 113:41705–18
    [Google Scholar]
32. 32.

    Koyama T, Nakamoto M, Morishima K, Yamashita R, Yamashita T et al. 2019. A SNP in a steroidogenic enzyme is associated with phenotypic sex in Seriola fishes. Curr. Biol. 29:111901–9.e8
    [Google Scholar]
33. 33.

    Catanach A, Ruigrok M, Bowatte D, Davy M, Storey R et al. 2021. The genome of New Zealand trevally (Carangidae: Pseudocaranx georgianus) uncovers a XY sex determination locus. BMC Genom. 22:785
    [Google Scholar]
34. 34.

    Nakamura Y, Higuchi K, Kumon K, Yasuike M, Takashi T et al. 2021. Prediction of the sex-associated genomic region in tunas (Thunnus fishes). Int. J. Genom. 2021:7226353
    [Google Scholar]
35. 35.

    Bao L, Tian C, Liu S, Zhang Y, Elaswad A et al. 2019. The Y chromosome sequence of the channel catfish suggests novel sex determination mechanisms in teleost fish. BMC Biol. 17:6
    [Google Scholar]
36. 36.

    Yano A, Guyomard R, Nicol B, Jouanno E, Quillet E et al. 2012. An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Curr. Biol. 22:151423–28
    [Google Scholar]
37. 37.

    Yano A, Nicol B, Jouanno E, Quillet E, Fostier A et al. 2013. The sexually dimorphic on the Y-chromosome gene (sdY) is a conserved male-specific Y-chromosome sequence in many salmonids. Evol. Appl. 6:3486–96
    [Google Scholar]
38. 38.

    Bertho S, Herpin A, Branthonne A, Jouanno E, Yano A et al. 2018. The unusual rainbow trout sex determination gene hijacked the canonical vertebrate gonadal differentiation pathway. PNAS 115:5012781–86
    [Google Scholar]
39. 39.

    Kirubakaran TG, Andersen Ø, De Rosa MC, Andersstuen T, Hallan K et al. 2019. Characterization of a male specific region containing a candidate sex determining gene in Atlantic cod. Sci. Rep. 9:116
    [Google Scholar]
40. 40.

    Dan C, Lin Q, Gong G, Yang T, Xiong S et al. 2018. A novel PDZ domain-containing gene is essential for male sex differentiation and maintenance in yellow catfish (Pelteobagrus fulvidraco). Sci. Bull. 63:211420–30
    [Google Scholar]
41. 41.

    de la Herrán R, Hermida M, Rubiolo JA, Gómez-Garrido J, Cruz F et al. 2023. A chromosome-level genome assembly enables the identification of the follicule stimulating hormone receptor as the master sex-determining gene in the flatfish Solea senegalensis. Mol. Ecol. Resour. 23:4886–904
    [Google Scholar]
42. 42.

    Tao W, Xu L, Zhao L, Zhu Z, Wu X et al. 2021. High-quality chromosome-level genomes of two tilapia species reveal their evolution of repeat sequences and sex chromosomes. Mol. Ecol. Resour. 21:2543–60
    [Google Scholar]
43. 43.

    Kobayashi T, Matsuda M, Kajiura-Kobayashi H, Suzuki A, Saito N et al. 2004. Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes. Dev. Dyn. 231:3518–26
    [Google Scholar]
44. 44.

    Shibata Y, Paul-Prasanth B, Suzuki A, Usami T, Nakamoto M et al. 2010. Expression of gonadal soma derived factor (GSDF) is spatially and temporally correlated with early testicular differentiation in medaka. Gene Expr. Patterns 10:6283–89
    [Google Scholar]
45. 45.

    Masuyama H, Yamada M, Kamei Y, Fujiwara-Ishikawa T, Todo T et al. 2012. Dmrt1 mutation causes a male-to-female sex reversal after the sex determination by Dmy in the medaka. Chromosome Res. 20:163–76
    [Google Scholar]
46. 46.

    Imai T, Saino K, Matsuda M, Matsuda M. 2015. Mutation of gonadal soma-derived factor induces medaka XY gonads to undergo ovarian development. Biochem. Biophys. Res. Commun. 467:1109–14
    [Google Scholar]
47. 47.

    Horie Y, Myosho T, Sato T, Sakaizumi M, Hamaguchi S, Kobayashi T. 2016. Androgen induces gonadal soma-derived factor, Gsdf, in XX gonads correlated to sex-reversal but not Dmrt1 directly, in the teleost fish, northern medaka (Oryzias sakaizumii). Mol. Cell. Endocrinol. 436:141–49
    [Google Scholar]
48. 48.

    Morinaga C, Saito D, Nakamura S, Sasaki T, Asakawa S et al. 2007. The hotei mutation of medaka in the anti-Müllerian hormone receptor causes the dysregulation of germ cell and sexual development. PNAS 104:239691–96
    [Google Scholar]
49. 49.

    Kurokawa H, Saito D, Nakamura S, Katoh-Fukui Y, Ohta K et al. 2007. Germ cells are essential for sexual dimorphism in the medaka gonad. PNAS 104:4316958–63
    [Google Scholar]
50. 50.

    Sato T, Suzuki A, Shibata N, Sakaizumi M, Hamaguchi S. 2008. The novel mutant scl of the medaka fish, Oryzias latipes, shows no secondary sex characters. Zool. Sci. 25:3299–306
    [Google Scholar]
51. 51.

    Nishimura T, Sato T, Yamamoto Y, Watakabe I, Ohkawa Y et al. 2015. foxl3 is a germ cell-intrinsic factor involved in sperm-egg fate decision in medaka. Science 349:6245328–31
    [Google Scholar]
52. 52.

    Nakamoto M, Matsuda M, Wang D-S, Nagahama Y, Shibata N. 2006. Molecular cloning and analysis of gonadal expression of Foxl2 in the medaka, Oryzias latipes. Biochem. Biophys. Res. Commun. 344:1353–61
    [Google Scholar]
53. 53.

    Suzuki A, Tanaka M, Shibata N, Nagahama Y. 2004. Expression of aromatase mRNA and effects of aromatase inhibitor during ovarian development in the medaka, Oryzias latipes. J. Exp. Zool. A 301:3266–73
    [Google Scholar]
54. 54.

    Yamamoto Y, Zhang Y, Sarida M, Hattori RS, Strüssmann CA. 2014. Coexistence of genotypic and temperature-dependent sex determination in pejerrey Odontesthes bonariensis. PLOS ONE 9:7e102574
    [Google Scholar]
55. 55.

    Fernandino JI, Hattori RS, Shinoda T, Kumura H, Strobl-Mazzulla PH et al. 2008. Dimorphic expression of dmrt1 and cyp19a1 (ovarian aromatase) during early gonadal development in pejerrey, Odontesthes bonariensis. Sex Dev. 2:6316–24
    [Google Scholar]
56. 56.

    Zhang Y, Hattori RS, Sarida M, García EL, Strüssmann CA, Yamamoto Y. 2018. Expression profiles of amhy and major sex-related genes during gonadal sex differentiation and their relation with genotypic and temperature-dependent sex determination in pejerrey Odontesthes bonariensis. Gen. Comp. Endocrinol. 265:196–201
    [Google Scholar]
57. 57.

    Valenzuela N, Lance VA, eds. 2005. Temperature-Dependent Sex Determination in Vertebrates Washington, DC: Smithsonian Books
58. 58.

    Bull JJ. 1980. Sex determination in reptiles. Q. Rev. Biol. 55:13–21
    [Google Scholar]
59. 59.

    Sarre SD, Georges A, Quinn A. 2004. The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. BioEssays 26:6639–45
    [Google Scholar]
60. 60.

    Valenzuela N, Adams DC, Janzen FJ. 2003. Pattern does not equal process: Exactly when is sex environmentally determined?. Am. Nat. 161:4676–83
    [Google Scholar]
61. 61.

    Baroiller J-F, D'Cotta H. 2016. The reversible sex of gonochoristic fish: insights and consequences. Sex Dev. 10:5–6242–66
    [Google Scholar]
62. 62.

    Ospina-Álvarez N, Piferrer F. 2008. Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change. PLOS ONE 3:7e2837
    [Google Scholar]
63. 63.

    Conover DO, Kynard BE. 1981. Environmental sex determination: interaction of temperature and genotype in a fish. Science 213:4507577–79
    [Google Scholar]
64. 64.

    Honeycutt JL, Deck CA, Miller SC, Severance ME, Atkins EB et al. 2019. Warmer waters masculinize wild populations of a fish with temperature-dependent sex determination. Sci. Rep. 9:6527
    [Google Scholar]
65. 65.

    Miyoshi K, Hattori RS, Strüssmann CA, Yokota M, Yamamoto Y. 2020. Phenotypic/genotypic sex mismatches and temperature-dependent sex determination in a wild population of an Old World atherinid, the cobaltcap silverside Hypoatherina tsurugae. Mol. Ecol. 29:132349–58
    [Google Scholar]
66. 66.

    Yamamoto Y, Hattori RS, Patiño R, Strüssmann CA. 2019. Environmental regulation of sex determination in fishes: insights from Atheriniformes. Curr. Top. Dev. Biol. 134:49–69
    [Google Scholar]
67. 67.

    Sato T, Endo T, Yamahira K, Hamaguchi S, Sakaizumi M. 2005. Induction of female-to-male sex reversal by high temperature treatment in Medaka, Oryzias latipes. . Zool. Sci. 22:9985–88
    [Google Scholar]
68. 68.

    Hayashi Y, Kobira H, Yamaguchi T, Shiraishi E, Yazawa T et al. 2010. High temperature causes masculinization of genetically female medaka by elevation of cortisol. Mol. Reprod. Dev. 77:8679–86
    [Google Scholar]
69. 69.

    Kitano T, Hayashi Y, Shiraishi E, Kamei Y. 2012. Estrogen rescues masculinization of genetically female medaka by exposure to cortisol or high temperature. Mol. Reprod. Dev. 79:10719–26
    [Google Scholar]
70. 70.

    Hara S, Sawamura R, Kitano T. 2021. Cortisol induces masculinization of XX medaka through gonadal soma-derived growth factor (GSDF) and anti-Müllerian hormone receptor type 2 (AMHR2). Fish. Sci. 87:185–91
    [Google Scholar]
71. 71.

    Fernandino JI, Hattori RS, Kishii A, Strüssmann CA, Somoza GM. 2012. The cortisol and androgen pathways cross talk in high temperature-induced masculinization: the 11β-hydroxysteroid dehydrogenase as a key enzyme. Endocrinology 153:126003–11
    [Google Scholar]
72. 72.

    Hattori RS, Castañeda-Cortés DC, Arias Padilla LF, Strobl-Mazzulla PH, Fernandino JI. 2020. Activation of stress response axis as a key process in environment-induced sex plasticity in fish. Cell. Mol. Life Sci. 77:214223–36
    [Google Scholar]
73. 73.

    Piferrer F. 2021. Epigenetic mechanisms in sex determination and in the evolutionary transitions between sexual systems. Philos. Trans. R. Soc. Lond. B 376:183220200110
    [Google Scholar]
74. 74.

    Navarro-Martín L, Viñas J, Ribas L, Díaz N, Gutiérrez A et al. 2011. DNA methylation of the gonadal aromatase (cyp19a) promoter is involved in temperature-dependent sex ratio shifts in the European sea bass. PLOS Genet. 7:12e1002447
    [Google Scholar]
75. 75.

    Shao C, Li Q, Chen S, Zhang P, Lian J et al. 2014. Epigenetic modification and inheritance in sexual reversal of fish. Genome Res. 24:4604–15
    [Google Scholar]
76. 76.

    Stern DL. 2013. The genetic causes of convergent evolution. Nat. Rev. Genet. 14:11751–64
    [Google Scholar]
77. 77.

    Gompel N, Prud'homme B. 2009. The causes of repeated genetic evolution. Dev. Biol. 332:136–47
    [Google Scholar]
78. 78.

    Christin P-A, Weinreich DM, Besnard G. 2010. Causes and evolutionary significance of genetic convergence. Trends Genet. 26:9400–5
    [Google Scholar]
79. 79.

    Arendt J, Reznick D. 2008. Convergence and parallelism reconsidered: What have we learned about the genetics of adaptation?. Trends Ecol. Evol. 23:126–32
    [Google Scholar]
80. 80.

    Martin A, Orgogozo V. 2013. The loci of repeated evolution: a catalog of genetic hotspots of phenotypic variation. Evolution 67:51235–50
    [Google Scholar]
81. 81.

    Kopp A. 2009. Metamodels and phylogenetic replication: a systematic approach to the evolution of developmental pathways. Evolution 63:112771–89
    [Google Scholar]
82. 82.

    Orr HA. 2005. The probability of parallel evolution. Evolution 59:1216–20
    [Google Scholar]
83. 83.

    Marshall Graves JA, Peichel CL. 2010. Are homologies in vertebrate sex determination due to shared ancestry or to limited options?. Genome Biol. 11:4205
    [Google Scholar]
84. 84.

    Pan Q, Kay T, Depincé A, Adolfi M, Schartl M et al. 2021. Evolution of master sex determiners: TGF-β signalling pathways at regulatory crossroads. Philos. Trans. R. Soc. Lond. B 376:183220200091
    [Google Scholar]
85. 85.

    Adolfi MC, Herpin A, Schartl M. 2021. The replaceable master of sex determination: bottom-up hypothesis revisited. Philos. Trans. R. Soc. Lond. B 376:183220200090
    [Google Scholar]
86. 86.

    Long M, VanKuren NW, Chen S, Vibranovski MD. 2013. New gene evolution: little did we know. Annu. Rev. Genet. 47:307–33
    [Google Scholar]
87. 87.

    Ohno S. 1970. Evolution by Gene Duplication Berlin: Springer
88. 88.

    Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C et al. 2002. A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. PNAS 99:1811778–83
    [Google Scholar]
89. 89.

    Herpin A, Braasch I, Kraeussling M, Schmidt C, Thoma EC et al. 2010. Transcriptional rewiring of the sex determining dmrt1 gene duplicate by transposable elements. PLOS Genet. 6:2e1000844
    [Google Scholar]
90. 90.

    Ogita Y, Mawaribuchi S, Nakasako K, Tamura K, Matsuda M et al. 2020. Parallel evolution of two dmrt1-derived genes, dmy and dm-w, for vertebrate sex determination. iScience 23:1100757
    [Google Scholar]
91. 91.

    Bertho S, Herpin A, Schartl M, Guiguen Y. 2021. Lessons from an unusual vertebrate sex-determining gene. Philos. Trans. R. Soc. Lond. B 376:183220200092
    [Google Scholar]
92. 92.

    Myosho T, Otake H, Masuyama H, Matsuda M, Kuroki Y et al. 2012. Tracing the emergence of a novel sex-determining gene in medaka. Oryzias luzonensis. Genetics 191:1163–70
    [Google Scholar]
93. 93.

    Kabir A, Ieda R, Hosoya S, Fujikawa D, Atsumi K et al. 2022. Repeated translocation of a supergene underlying rapid sex chromosome turnover in Takifugu pufferfish. PNAS 119:23e2121469119
    [Google Scholar]
94. 94.

    Bull JJ, Charnov EL. 1977. Changes in the heterogametic mechanism of sex determination. Heredity 39:1–14
    [Google Scholar]
95. 95.

    van Doorn GS. 2014. Evolutionary transitions between sex-determining mechanisms: a review of theory. Sex Dev. 8:1–37–19
    [Google Scholar]
96. 96.

    van Doorn GS, Kirkpatrick M. 2007. Turnover of sex chromosomes induced by sexual conflict. Nature 449:7164909–12
    [Google Scholar]
97. 97.

    van Doorn GS, Kirkpatrick M. 2010. Transitions between male and female heterogamety caused by sex-antagonistic selection. Genetics 186:2629–45
    [Google Scholar]
98. 98.

    Charlesworth B, Wall JD. 1999. Inbreeding, heterozygote advantage and the evolution of neo-X and neo-Y sex chromosomes. Proc. R. Soc. Lond. B 266:141451–56
    [Google Scholar]
99. 99.

    Úbeda F, Patten MM, Wild G. 2015. On the origin of sex chromosomes from meiotic drive. Proc. Biol. Sci. 282:179820141932
    [Google Scholar]
100. 100.

     Jayakar SD. 1987. Some two locus models for the evolution of sex-determining mechanisms. Theor. Popul. Biol. 32:2188–215
     [Google Scholar]
101. 101.

     Burt A, Trivers R. 2006. Genes in Conflict: The Biology of Selfish Genetic Elements Cambridge, MA: Harvard Univ. Press
102. 102.

     Blaser O, Grossen C, Neuenschwander S, Perrin N. 2013. Sex-chromosome turnovers induced by deleterious mutation load. Evolution 67:3635–45
     [Google Scholar]
103. 103.

     Saunders PA, Neuenschwander S, Perrin N. 2019. Impact of deleterious mutations, sexually antagonistic selection, and mode of recombination suppression on transitions between male and female heterogamety. Heredity 123:3419–28
     [Google Scholar]
104. 104.

     Charlesworth B, Charlesworth D. 2000. The degeneration of Y chromosomes. Philos. Trans. R. Soc. Lond. B 355:14031563–72
     [Google Scholar]
105. 105.

     Blaser O, Neuenschwander S, Perrin N. 2014. Sex-chromosome turnovers: the hot-potato model. Am. Nat. 183:1140–46
     [Google Scholar]
106. 106.

     Veller C, Muralidhar P, Constable GWA, Nowak MA. 2017. Drift-induced selection between male and female heterogamety. Genetics 207:2711–27
     [Google Scholar]
107. 107.

     Saunders PA, Neuenschwander S, Perrin N. 2018. Sex chromosome turnovers and genetic drift: a simulation study. J. Evol. Biol. 31:91413–19
     [Google Scholar]
108. 108.

     Kallman KD. 1984. A new look at sex determination in poeciliid fishes. Evolutionary Genetics of Fishes BJ Turner 95–171. New York: Springer
     [Google Scholar]
109. 109.

     Ser JR, Roberts RB, Kocher TD. 2010. Multiple interacting loci control sex determination in Lake Malawi cichlid fish. Evolution 64:2486–501
     [Google Scholar]
110. 110.

     Lee B-Y, Hulata G, Kocher TD. 2004. Two unlinked loci controlling the sex of blue tilapia (Oreochromis aureus). Heredity 92:6543–49
     [Google Scholar]
111. 111.

     Kitano J, Ansai S, Fujimoto S, Kakioka R, Sato M et al. 2023. A cryptic sex-linked locus revealed by the elimination of a master sex-determining locus in medaka fish. Am. Nat. 202:2231–40
     [Google Scholar]
112. 112.

     Shinomiya A, Otake H, Togashi K-I, Hamaguchi S, Sakaizumi M. 2004. Field survey of sex-reversals in the medaka, Oryzias latipes: genotypic sexing of wild populations. Zool. Sci. 21:6613–19
     [Google Scholar]
113. 113.

     Sharma KK, Sharma OP, Tripathi NK. 1998. Female heterogamety in Danio rerio (Cypriniformes: Cyprinidae). Proc. Natl. Acad. Sci. India B 68:123–26
     [Google Scholar]
114. 114.

     Wilson CA, High SK, McCluskey BM, Amores A, Yan T-l et al. 2014. Wild sex in zebrafish: loss of the natural sex determinant in domesticated strains. Genetics 198:31291–308
     [Google Scholar]
115. 115.

     Liew WC, Bartfai R, Lim Z, Sreenivasan R, Siegfried KR, Orban L. 2012. Polygenic sex determination system in zebrafish. PLOS ONE 7:4e34397
     [Google Scholar]
116. 116.

     Kitano J, Peichel CL. 2012. Turnover of sex chromosomes and speciation in fishes. Environ. Biol. Fish. 94:3549–58
     [Google Scholar]
117. 117.

     Sember A, Nguyen P, Perez MF, Altmanová, Ráb P, de Bello Cioffi M. 2021. Multiple sex chromosomes in teleost fishes from a cytogenetic perspective: state of the art and future challenges. Philos. Trans. R. Soc. Lond. B 376:183320200098
     [Google Scholar]
118. 118.

     White MJD. 1973. Animal Cytology and Evolution Cambridge, UK: Cambridge Univ. Press
119. 119.

     Charlesworth D, Charlesworth B. 1980. Sex differences in fitness and selection for centric fusions between sex-chromosomes and autosomes. Genet. Res. 35:2205–14
     [Google Scholar]
120. 120.

     Matsumoto T, Kitano J. 2016. The intricate relationship between sexually antagonistic selection and the evolution of sex chromosome fusions. J. Theor. Biol. 404:97–108
     [Google Scholar]
121. 121.

     Matsumoto T, Yoshida K, Kitano J. 2017. Contribution of gene flow to the evolution of recombination suppression in sex chromosomes. J. Theor. Biol. 431:25–31
     [Google Scholar]
122. 122.

     Yoshida K, Kitano J. 2012. The contribution of female meiotic drive to the evolution of neo-sex chromosomes. Evolution 66:103198–208
     [Google Scholar]
123. 123.

     Pokorná M, Altmanová M, Kratochvíl L. 2014. Multiple sex chromosomes in the light of female meiotic drive in amniote vertebrates. Chromosome Res. 22:135–44
     [Google Scholar]
124. 124.

     Pennell MW, Kirkpatrick M, Otto SP, Vamosi JC, Peichel CL et al. 2015. Y fuse? Sex chromosome fusions in fishes and reptiles. PLOS Genet. 11:5e1005237
     [Google Scholar]
125. 125.

     Charnov EL, Bull J. 1977. When is sex environmentally determined?. Nature 266:5605828–30
     [Google Scholar]
126. 126.

     Conover DO. 1984. Adaptive significance of temperature-dependent sex determination in a fish. Am. Nat. 123:3297–313
     [Google Scholar]
127. 127.

     Bull JJ. 1981. Evolution of environmental sex determination from genotypic sex determination. Heredity 47:2173–84
     [Google Scholar]
128. 128.

     Geffroy B, Douhard M. 2019. The adaptive sex in stressful environments. Trends Ecol. Evol. 34:7628–40
     [Google Scholar]
129. 129.

     Fisher RA. 1930. The Genetical Theory of Natural Selection Oxford, UK: Oxford Univ. Press
130. 130.

     Bulmer MG, Bull JJ. 1982. Models of polygenic sex determination and sex ratio control. Evolution 36:113–26
     [Google Scholar]
131. 131.

     Grossen C, Neuenschwander S, Perrin N. 2011. Temperature-dependent turnovers in sex-determination mechanisms: a quantitative model. Evolution 65:164–78
     [Google Scholar]
132. 132.

     Ramos L, Antunes A. 2022. Decoding sex: elucidating sex determination and how high-quality genome assemblies are untangling the evolutionary dynamics of sex chromosomes. Genomics 114:2110277
     [Google Scholar]
133. 133.

     Rhie A, Nurk S, Cechova M, Hoyt SJ, Taylor DJ et al. 2023. The complete sequence of a human Y chromosome. Nature 621:344–54
     [Google Scholar]
134. 134.

     Ansai S, Kitano J. 2022. Speciation and adaptation research meets genome editing. Philos. Trans. R. Soc. Lond. B 377:185520200516
     [Google Scholar]
135. 135.

     Jeffries DL, Gerchen JF, Scharmann M, Pannell JR. 2021. A neutral model for the loss of recombination on sex chromosomes. Philos. Trans. R. Soc. Lond. B 376:183220200096
     [Google Scholar]
136. 136.

     Lenormand T, Roze D. 2022. Y recombination arrest and degeneration in the absence of sexual dimorphism. Science 375:6581663–66
     [Google Scholar]
137. 137.

     Jay P, Tezenas E, Véber A, Giraud T. 2022. Sheltering of deleterious mutations explains the stepwise extension of recombination suppression on sex chromosomes and other supergenes. PLOS Biol. 20:7e3001698
     [Google Scholar]
138. 138.

     Charlesworth D. 2017. Evolution of recombination rates between sex chromosomes. Philos. Trans. R. Soc. Lond. B 372:173620160456
     [Google Scholar]
139. 139.

     Abbott JK, Nordén AK, Hansson B. 2017. Sex chromosome evolution: historical insights and future perspectives. Proc. Biol. Sci. 284:185420162806
     [Google Scholar]
140. 140.

     Kratochvíl L, Stöck M, Rovatsos M, Bullejos M, Herpin A et al. 2021. Expanding the classical paradigm: what we have learnt from vertebrates about sex chromosome evolution. Philos. Trans. R. Soc. Lond. B 376:183320200097
     [Google Scholar]
141. 141.

     Kitano J, Ross JA, Mori S, Kume M, Jones FC et al. 2009. A role for a neo-sex chromosome in stickleback speciation. Nature 461:72671079–83
     [Google Scholar]
142. 142.

     Roberts RB, Ser JR, Kocher TD. 2009. Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes. Science 326:5955998–1001
     [Google Scholar]
143. 143.

     Dagilis AJ, Sardell JM, Josephson MP, Su Y, Kirkpatrick M, Peichel CL. 2022. Searching for signatures of sexually antagonistic selection on stickleback sex chromosomes. Philos. Trans. R. Soc. Lond. B 377:185620210205
     [Google Scholar]
144. 144.

     Matsunaga T, Ieda R, Hosoya S, Kuroyanagi M, Suzuki S et al. 2014. An efficient molecular technique for sexing tiger pufferfish (fugu) and the occurrence of sex reversal in a hatchery population. Fish. Sci. 80:5933–42
     [Google Scholar]
145. 145.

     Bertho S, Herpin A, Jouanno E, Yano A, Bobe J et al. 2022. A nonfunctional copy of the salmonid sex-determining gene (sdY) is responsible for the “apparent” XY females in Chinook salmon, Oncorhynchus tshawytscha. G3 12:2jkab451
     [Google Scholar]
146. 146.

     Wang H, Piferrer F, Chen S, Shen Z-G, eds. 2018. Sex Control in Aquaculture Hoboken, NJ: John Wiley & Sons
147. 147.

     Geffroy B, Wedekind C. 2020. Effects of global warming on sex ratios in fishes. J. Fish Biol. 97:3596–606
     [Google Scholar]
148. 148.

     McKenzie DJ, Geffroy B, Farrell AP. 2021. Effects of global warming on fishes and fisheries. J. Fish Biol. 98:61489–92
     [Google Scholar]
149. 149.

     Hattori RS, Somoza GM, Fernandino JI, Colautti DC, Miyoshi K et al. 2019. The duplicated Y-specific amhy gene is conserved and linked to maleness in silversides of the genus Odontesthes. Genes 10:9679
     [Google Scholar]
150. 150.

     Bej DK, Miyoshi K, Hattori RS, Strüssmann CA, Yamamoto Y. 2017. A duplicated, truncated amh gene is involved in male sex determination in an Old World silverside. G3 7:82489–95
     [Google Scholar]
151. 151.

     Matsuda M, Sato T, Toyazaki Y, Nagahama Y, Hamaguchi S, Sakaizumi M. 2003. Oryzias curvinotus has DMY, a gene that is required for male development in the medaka, O. latipes. Zool. Sci. 20:2159–61
     [Google Scholar]
152. 152.

     Ansai S, Montenegro J, Masengi KWA, Nagano AJ, Yamahira K, Kitano J. 2022. Diversity of sex chromosomes in Sulawesian medaka fishes. J. Evol. Biol. 35:121751–64
     [Google Scholar]
153. 153.

     Purcell CM, Seetharam AS, Snodgrass O, Ortega-García S, Hyde JR, Severin AJ. 2018. Insights into teleost sex determination from the Seriola dorsalis genome assembly. BMC Genom. 19:31
     [Google Scholar]
154. 154.

     Li M, Xu X, Liu S, Fan G, Zhou Q, Chen S. 2022. The chromosome-level genome assembly of the Japanese yellowtail jack Seriola aureovittata provides insights into genome evolution and efficient oxygen transport. Mol. Ecol. Resour. 22:72701–12
     [Google Scholar]
155. 155.

     Rafati N, Chen J, Herpin A, Pettersson ME, Han F et al. 2020. Reconstruction of the birth of a male sex chromosome present in Atlantic herring. PNAS 117:3924359–68
     [Google Scholar]
156. 156.

     Reichwald K, Petzold A, Koch P, Downie BR, Hartmann N et al. 2015. Insights into sex chromosome evolution and aging from the genome of a short-lived fish. Cell 163:61527–38
     [Google Scholar]
157. 157.

     Štundlová J, Hospodářská M, Lukšíková K, Voleníková A, Pavlica T et al. 2022. Sex chromosome differentiation via changes in the Y chromosome repeat landscape in African annual killifishes Nothobranchius furzeri and N. kadleci. Chromosome Res. 30:4309–33
     [Google Scholar]
158. 158.

     Pan Q, Feron R, Jouanno E, Darras H, Herpin A et al. 2021. The rise and fall of the ancient northern pike master sex-determining gene. eLife 10:e62858
     [Google Scholar]
159. 159.

     Nakamoto M, Uchino T, Koshimizu E, Kuchiishi Y, Sekiguchi R et al. 2021. A Y-linked anti-Müllerian hormone type-II receptor is the sex-determining gene in ayu, Plecoglossus altivelis. PLOS Genet. 17:8e1009705
     [Google Scholar]
160. 160.

     Adolfi MC, Du K, Kneitz S, Cabau C, Zahm M et al. 2021. A duplicated copy of id2b is an unusual sex-determining candidate gene on the Y chromosome of arapaima (Arapaima gigas). Sci. Rep. 11:21544
     [Google Scholar]
161. 161.

     Feron R, Zahm M, Cabau C, Klopp C, Roques C et al. 2020. Characterization of a Y-specific duplication/insertion of the anti-Mullerian hormone type II receptor gene based on a chromosome-scale genome assembly of yellow perch, Perca flavescens. Mol. Ecol. Resour. 20:2531–43
     [Google Scholar]
162. 162.

     Sardell JM, Josephson MP, Dalziel AC, Peichel CL, Kirkpatrick M. 2021. Heterogeneous histories of recombination suppression on stickleback sex chromosomes. Mol. Biol. Evol. 38:104403–18
     [Google Scholar]
163. 163.

     Jeffries DL, Mee JA, Peichel CL. 2022. Identification of a candidate sex determination gene in Culaea inconstans suggests convergent recruitment of an Amh duplicate in two lineages of stickleback. J. Evol. Biol. 35:121683–95
     [Google Scholar]
164. 164.

     Rondeau EB, Laurie CV, Johnson SC, Koop BF. 2016. A PCR assay detects a male-specific duplicated copy of anti-Müllerian hormone (amh) in the lingcod (Ophiodon elongatus). BMC Res. Notes. 9:230
     [Google Scholar]
165. 165.

     Herpin A, Schartl M, Depincé A, Guiguen Y, Bobe J et al. 2021. Allelic diversification after transposable element exaptation promoted gsdf as the master sex determining gene of sablefish. Genome Res. 31:81366–80
     [Google Scholar]
166. 166.

     Song W, Xie Y, Sun M, Li X, Fitzpatrick CK et al. 2021. A duplicated amh is the master sex-determining gene for Sebastes rockfish in the Northwest Pacific. Open Biol. 11:7210063
     [Google Scholar]
167. 167.

     Holborn MK, Einfeldt AL, Kess T, Duffy SJ, Messmer AM et al. 2022. Reference genome of lumpfish Cyclopterus lumpus Linnaeus provides evidence of male heterogametic sex determination through the AMH pathway. Mol. Ecol. Resour. 22:41427–39
     [Google Scholar]
168. 168.

     Jiang D-N, Huang Y-Q, Zhang J-M, Mustapha UF, Peng Y-X et al. 2022. Establishment of the Y-linked Dmrt1Y as the candidate sex determination gene in spotbanded scat (Selenotoca multifasciata). Aquacult. Rep. 23:101085
     [Google Scholar]
169. 169.

     Edvardsen RB, Wallerman O, Furmanek T, Kleppe L, Jern P et al. 2022. Heterochiasmy and the establishment of gsdf as a novel sex determining gene in Atlantic halibut. PLOS Genet. 18:2e1010011
     [Google Scholar]
170. 170.

     Zheng S, Tao W, Yang H, Kocher TD, Wang Z et al. 2022. Identification of sex chromosome and sex-determining gene of southern catfish (Silurus meridionalis) based on XX, XY and YY genome sequencing. Proc. Biol. Sci. 289:197120212645
     [Google Scholar]
171. 171.

     Qu M, Liu Y, Zhang Y, Wan S, Ravi V et al. 2021. Seadragon genome analysis provides insights into its phenotype and sex determination locus. Sci. Adv. 7:34eabg5196
     [Google Scholar]
172. 172.

     Ieda R, Hosoya S, Tajima S, Atsumi K, Kamiya T et al. 2018. Identification of the sex-determining locus in grass puffer (Takifugu niphobles) provides evidence for sex-chromosome turnover in a subset of Takifugu species. PLOS ONE 13:1e0190635
     [Google Scholar]
173. 173.

     Ramee SW, Lipscomb TN, DiMaggio MA. 2020. Evaluation of the effect of larval stocking density, salinity, and temperature on stress response and sex differentiation in the Dwarf Gourami and Rosy Barb. Aquacult. Rep. 16:100287
     [Google Scholar]
174. 174.

     Corona-Herrera GA, Tello-Ballinas JA, Hattori RS, Martínez-Palacios CA, Strüssmann CA et al. 2016. Gonadal differentiation and temperature effects on sex determination in the freshwater pike silverside Chirostoma estor Jordan 1880. Environ. Biol. Fish. 99:5463–71
     [Google Scholar]
175. 175.

     Brown EE, Baumann H, Conover DO. 2014. Temperature and photoperiod effects on sex determination in a fish. J. Exp. Mar. Biol. Ecol. 461:39–43
     [Google Scholar]
176. 176.

     Shen Z-G, Wang H-P, Yao H, O'Bryant P, Rapp D, Zhu K-Q. 2016. Sex determination in bluegill sunfish Lepomis macrochirus: effect of temperature on sex ratio of four geographic strains. Biol. Bull. 230:3197–208
     [Google Scholar]
177. 177.

     Li X-Y, Liu X-L, Zhu Y-J, Zhang J, Ding M et al. 2018. Origin and transition of sex determination mechanisms in a gynogenetic hexaploid fish. Heredity 121:164–74
     [Google Scholar]
178. 178.

     Fujioka Y. 2002. Effects of hormone treatments and temperature on sex-reversal of Nigorobuna Carassius carassius grandoculis. Fish. Sci. 68:4889–93
     [Google Scholar]
179. 179.

     Biswas C, Chakraborty S, Munilkumar S, Gireesh-Babu P, Sawant PB et al. 2021. Effect of high temperature during larval and juvenile stages on masculinization of common carp (Cyprinus carpio, L). Aquaculture 530:735803
     [Google Scholar]
180. 180.

     Sfakianakis DG, Leris I, Mylonas CC, Kentouri M. 2012. Temperature during early life determines sex in zebrafish, Danio rerio (Hamilton, 1822). J. Biol. Res. 17:68–73
     [Google Scholar]
181. 181.

     Fujioka Y. 2006. Patterns of sex ratio response to water temperature during sex determination in honmoroko Gnathopogon caerulescens. Fish. Sci. 72:51034–41
     [Google Scholar]
182. 182.

     Kim S-S, Kim DN-J, Lee C-J, Yoo H-K, Byun S-G et al. 2020. The potential sex determination genes, Sox9a and Cyp19a, in walleye pollock (Gadus Chalcogrammus) are influenced by water temperature. J. Mar. Sci. Eng. 8:7501
     [Google Scholar]
183. 183.

     Huynh TB, Fairgrieve WT, Hayman ES, Lee JSF, Luckenbach JA. 2019. Inhibition of ovarian development and instances of sex reversal in genotypic female sablefish (Anoplopoma fimbria) exposed to elevated water temperature. Gen. Comp. Endocrinol. 279:88–98
     [Google Scholar]
184. 184.

     Montalvo AJ, Faulk CK, Holt GJ. 2012. Sex determination in southern flounder, Paralichthys lethostigma, from the Texas Gulf Coast. J. Exp. Mar. Biol. Ecol. 432–33:186–90
     [Google Scholar]
185. 185.

     Colburn HR, Nardi GC, Borski RJ, Berlinsky DL. 2009. Induced meiotic gynogenesis and sex differentiation in summer flounder (Paralichthys dentatus). Aquaculture 289:1175–80
     [Google Scholar]
186. 186.

     Haffray P, Lebègue E, Jeu S, Guennoc M, Guiguen Y et al. 2009. Genetic determination and temperature effects on turbot Scophthalmus maximus sex differentiation: an investigation using steroid sex-inverted males and females. Aquaculture 294:130–36
     [Google Scholar]
187. 187.

     Viñas J, Asensio E, Cañavate JP, Piferrer F. 2013. Gonadal sex differentiation in the Senegalese sole (Solea senegalensis) and first data on the experimental manipulation of its sex ratios. Aquaculture 384–87:74–81
     [Google Scholar]
188. 188.

     Cole KS, Noakes DLG, Thompson N, Blouin M, Morrison B, Schreck CB. 2013. Exposure to elevated temperature during early development affects sexual development in Oncorhynchus mykiss. North Pac. Anadromous Fish Comm. Tech. Rep. 9:104–6
     [Google Scholar]
189. 189.

     Omoto N, Koya Y, Chin B, Yamashita Y, Nakagawa M, Noda T. 2010. Gonadal sex differentiation and effect of rearing temperature on sex ratio in black rockfish (Sebastes schlegeli). Ichthyol. Res. 57:2133–38
     [Google Scholar]
190. 190.

     Santi S, Gennotte V, Toguyeni A, Mélard C, Antoine N, Rougeot C. 2016. Thermosensitivity of the sex differentiation process in the African catfish, Clarias gariepinus: determination of the thermosensitive period. Aquaculture 455:73–80
     [Google Scholar]
191. 191.

     Yu Y, Chen M, Qi P-P, Chang L-Y, Wang T et al. 2021. High temperature-induced masculinization in yellow catfish Tachysurus fulvidraco: a potential approach for environmental-friendly mono-sex production. Aquaculture 534:736263
     [Google Scholar]
192. 192.

     Zhou H, Zhuang Z, Zhang R, Xu Q, Liang Y et al. 2019. Temperature-control-induced masculinization in tiger puffer Takifugu rubripes. J. Oceanol. Limnol. 37:31125–35
     [Google Scholar]
193. 193.

     Rabosky DL, Chang J, Title PO, Cowman PF, Sallan L et al. 2018. An inverse latitudinal gradient in speciation rate for marine fishes. Nature 559:7714392–95
     [Google Scholar]