Environmental effects on fish sex determination and differentiation

Sexual Development

Volumn 3, Issue 2-3, 2009, Pages 118-135

  Baroiller, J F ^a   D'Cotta, H ^a   Saillant, E ^b  

^a CIRAD   (France)

^b UNIVERSITY OF SOUTHERN MISSISSIPPI   (United States)

Author keywords

ESD; Fish; Genes; Gonads; Growth rate; GSD; Hypoxia; Sex determination differentiation; Temperature

Indexed keywords

AROMATASE;

APOPTOSIS; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; CORRELATION ANALYSIS; ENVIRONMENTAL FACTOR; ENZYME INDUCTION; ENZYME REGULATION; ENZYME REPRESSION; EUROPEAN SEA BASS; GENETIC VARIABILITY; GERM CELL; GROWTH RATE; HEAT SENSITIVITY; HYPOXIA; IN VITRO STUDY; NATURAL POPULATION; NUCLEAR REACTOR; PH; PHENOTYPE; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; REVIEW; SEX DETERMINATION; SEX DIFFERENTIATION; SOCIAL STATUS; TEMPERATURE SENSITIVITY; TILAPIA; XX MALE;

ANIMALS; ENVIRONMENT; FISHES; GENETIC VARIATION; SEX DETERMINATION PROCESSES; SEX DIFFERENTIATION; TEMPERATURE;

MENIDIA; OREOCHROMIS NILOTICUS; SERRANIDAE; TILAPIA;

EID: 69249144154     PISSN: 16615425     EISSN: 16615433     Source Type: Journal    
DOI: 10.1159/000223077     Document Type: Review

References (139)

1. Abucay JS, Mair GC, Skibinski DO, Beardmore JA: Environmental sex determination: the effect of temperature and salinity on sex ratio in Oreochromis niloticus L. Aquaculture 173: 219-234 (1999).
2. Altena A, Hörstgen-Schark G: Effects of rearing temperatures on sex ratios in tilapia, Oreochromis niloticus L., investigations on a local population from the Lake Victoria in Kenya. In: Challenge to Organic Farming and Sustainable Land Use in the Tropics and Subtropics. Deutscher Tropentag, Witzenhausen (2002).
3. Baroiller JF, D'Cotta H: Environment and sex determination in farmed fish. Comp Biochem Physiol C Toxicol Pharmacol 130: 399-409 (2001).
4. Baroiller JF, Jalabert B: Contribution of research in reproductive physiology to the culture of tilapias. Aquat Living Resour 2: 105-116 (1989).
5. Baroiller JF, Chourrout D, Fostier A, Jalabert B: Temperature and sex chromosomes govern sex ratios on the mouthbrooding cichlid fish Oreochromis niloticus. J Exp Zool 273: 216-223 (1995).
6. Baroiller JF, Guiguen Y, Fostier A: Endocrine and environmental aspects of sex differentiation in fish. Cell Mol Life Sci 55: 910-931 (1999). (Pubitemid 29304446)
7. Baroiller JF, D'Cotta H, Wessels S, Bezault E, Hoerstgen-Schwark G: Temperature effects on tilapia sex differentiation. In: Proceedings of the 6th International Symposium on Fish Endocrinology, June 22-27, Calgary, Canada (2008).
8. Baroiller JF, D'Cotta H, Bezault E, Wessels S, Hoerstgen-Schwark G: Tilapia sex determination: Where temperature and genetics meet. Comp Biochem Physiol A Mol Integr Physiol 153: 30-38 (2009).
9. Barón BS, Bückle FS, Espina S: Environmental factors and sexual differentiation in Poecilia sphenops Valenciennes (Pisces: Poeciliidae). Aquac Res 33: 615-619 (2002).
10. Berishvili G, D'Cotta H, Baroiller JF, Segner H, Reinecke M: Differential expression of IGF-I mRNA and peptide in the male and female gonad during early development of a bony fish, the tilapia Oreochromis niloticus . Gen Comp Endocrinol 146: 204-210 (2006).
11. Bezault E, Clota F, Derivaz M, Chevassus B, Baroiller JF: Sex determination and temperature-induced sex differentiation in three natural populations of Nile tilapia (Oreochromis niloticus) adapted to extreme temperature conditions. Aquaculture 272:S3-S16 (2007).
12. Blázquez M, Zanuy S, Carrillo M, Piferrer F: Effects of rearing temperature on sex differentiation in the European sea bass ( Dicentrarchus labrax L.). J Exp Zool 281: 207-216 (1998). (Pubitemid 28259750)
13. Blázquez M, González A, Papadaki M, Mylonas C, Piferrer F: Sex-related changes in estrogen receptors and aromatase gene expression and enzymatic activity during early development and sex differentiation in the European sea bass (Dicentrarchus labrax) . Gen Comp Endocrinol 158: 95-101 (2008).
14. Bull JJ: Sex determination in reptiles. Quart Rev Biol 55: 3-21 (1980).
15. Bull JJ: Sex determination: are two mechanisms better than one? J Biosci 33: 5-8 (2008).
16. Cnaani A, Lee BY, Zilberman N, Ozouf-Costaz C, Hulata G, et al: Genetics of sex determination in tilapiine species. Sex Dev 2: 43-54 (2008). (Pubitemid 351555909)
17. Colburn HR, Nardi GC, Borski RJ, Berlinsky DL: Induced meiotic gynogenesis and sex determination in summer flounder (Paralichthys dentatus) . Aquaculture 289: 175-180 (2009).
18. Conover DO: Adaptative significance of temperature-dependent sex determination in a fish. Am Nat 123: 298-313 (1984).
19. Conover DO: Temperature-dependent sex determination in fishes, in Valenzuela N, Lance V (eds): Temperature-Dependent Sex Determination in Vertebrates, pp 11-20 (Smithsonian Books, Washington 2004).
20. Conover DO, Heins SW: The environmental and genetic components of sex-ratio in Menidia menidia (Pisces: Atherinidae). Copeia 1987: 732-743 (1987).
21. Conover DO, Kynard BE: Environmental sex determination: interaction of temperature and genotype in a fish. Science 213: 577-579 (1981).
22. Conover DO, Van Vorhees DA, Ehtisham A: Sexratio selection and the evolution of sex determination in laboratory population of Meni dia menidia . Evolution 46: 1722-1730 (1992).
23. 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).
24. Davey AJH, Jellyman DJ: Sex determination in freshwater eels and management options for manipulation of sex. Rev Fish Biol Fisheries 15: 37-52 (2005).
25. D'Cotta H, Fostier A, Guiguen Y, Govoroun M, Baroiller JF: Search for the molecular mechanisms implicated in the thermosensitivity of sex gonadal differentiation of tilapia fish: differential approach and expression of candidate genes. J Exp Zool 290: 574-585 (2001a).
26. D'Cotta H, Guiguen Y, Govoroun MS, McMeel O, Baroiller JF: Aromatase plays a key role during normal and temperature-induced sex differentiation of tilapia Oreochromis niloticus. Mol Reprod Dev 59: 265-276 (2001b). (Pubitemid 32525433)
27. D'Cotta H, Pepey E, Pfennig F, Bienvenu D, Gutzeit HO, et al: Sox9a, Sox9b and Amh are up-regulated in the gonads during natural and temperature-induced tilapia male differentiation. In: Proceedings of the 8th International Symposium on Reproductive Physiology of Fish, June 3-8, Saint-Malo (2007).
28. D'Cotta H, Pepey E, Wessels S, Poonlaphdecha S, Reinelt B, et al: Temperature-induced male differentiation in the Nile tilapia: gonad gene expression using female monosex populations and divergent thermo-sensitive lines. In: Proceedings of the 20th International Congress of Zoology, S10 Sex determination & differentiation, August 26-29, Paris (2008).
29. Devlin RH, Nagahama Y: Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208: 191-364 (2002).
30. DiNapoli L, Capel B: SRY and the standoff in sex determination. Mol Endocrinol 22: 1-9 (2008).
31. Ezaz T, Quinn AE, Miura I, Sarre SD, Georges A, Marshall Graves JA: The dragon lizard Pogona vitticeps has ZZ/ZW micro-sex chromosomes. Chromosome Res 13: 763-776 (2005).
32. Fernandino JI, Hattori RS, Kimura H, Strüssmann CA, Somoza GM: Expression profile and estrogenic regulation of anti-Müllerian hormone during gonadal development in pejerrey Odontesthes bonariensis , a teleost fish with strong temperature-dependent sex determination. Dev Dyn 237: 3192-3199 (2008a).
33. Fernandino JI, Hattori RS, Shinoda H, Strobl- Mazzulla PH, Strüssmann C, Somoza GM: Dimorphic expression of dmrt1 and cyp19a1 (ovarian aromatase) during early gonadal development in pejerrey, Odontesthes bonariensis. Sex Dev 2: 316-324 (2008b).
34. Forlano PM, Deitcher DL, Myer DA, Bass AH: Anatomical distribution and cellular basis for high levels of aromatase activity in the brain of teleost fish: aromatase enzyme and mRNA expression identify glia as source. J Neurosci 22: 8943-8955 (2001).
35. Francis RC: The effects of bidirectional selection for social dominance on agonistic behaviour and sex ratios in the Paradise fish (Macropodus opercularis) . Behaviour 9025-9045 (1984).
36. Francis RC: Temperament in a fish: a longitudinal study of the development of individual differences in aggression and social rank in the Midas cichlid. Ethology 86: 311-325 (1990).
37. Francis RC, Barlow GW: Social control of primary sex differentiation in the Midas cichlid. Proc Natl Acad Sci USA 90: 10673-10675 (1993).
38. Fujioka Y: Thermolabile sex determination in honmoroko. J Fish Biol 59: 851-861 (2001).
39. Fujioka Y: Effects of hormone treatments and temperature on sex-reversal of nigorobuna Carassius carassius grandoculis . Fish Sci 68: 889-893 (2002).
40. Fujioka Y: Patterns of sex ratio response to water temperature during sex determination in honmoroko Gnathopogon caerulescens . Fish Sci 72: 1034-1041 (2006).
41. Galay-Burgos M, Gealy C, Navarro-Martín L, Piferrer F, Zanuy S, Sweeney GE: Cloning of the promoter from the gonadal aromatase gene of the European sea bass and identification of single nucleotide polymorphisms. Comp Biochem Physiol A Mol Integr Physiol 145: 47-53 (2006). (Pubitemid 44251191)
42. Godwin J: Social determination of sex in reef fishes. Semin Cell Dev Biol 20: 264-270 (2009).
43. Goto R, Mori T, Kawamata K, Matsubara T, Mizuno S, et al: Effects of temperature on gonadal sex determination in barfin flounder Verasper moseri . Fish Sci 65: 884-887 (1999). (Pubitemid 129692546)
44. Goto R, Kayaba T, Adachi S, Yamauchi K: Effects of temperature on sex determination in marbled sole Limanda yokohamae . Fish Sci 66: 400-402 (2000).
45. Haffray P, Lebègue E, Jeu S, Guennoc M, Guiguen Y, et al: Genetic determination and temperature effects on turbot Scophthalmus maximus sex differentiation: an investigation using steroid sex-inverted males and females. Aquaculture, in press (2009). doi:10.1016/j. aquaculture.2009.05.004.
46. Halm S, Rocha A, Miura T, Prat F, Zanuy S: Anti-Müllerian hormone (AMH/AMH) in the European sea bass: its gene structure, regulatory elements, and the expression of alternatively-spliced isoforms. Gene 388: 148-158 (2007).
47. Hattori RS, Gould RJ, Fujioka T, Saito T, Kurita J, et al: 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 (2007). (Pubitemid 46714641)
48. He F, Wen HS, Dong SL, Shi B, Chen CF, et al: Identification of single nucleotide polymorphism cytochrome P450-c19a and its relation to reproductive traits in Japanese flounder (Paralichthys olivaceus) . Aquaculture 279: 177-181 (2008).
49. Helfman GS, Collette BB, Facey DE, Bowen B: The Diversity of Fishes. Biology, Evolution, and Ecology, 2nd ed. (Blackwell Science, Malden 2009).
50. Herpin A, Schindler D, Kraiss A, Hornung U, Winkler C, Schartl M: Inhibition of primordial germ cell proliferation by the medaka male determining gene dmrt1bY . BMC Dev Biol 7: 99 (2007). (Pubitemid 47606704)
51. Holmgren K, Mosegaard H: Implications of individual growth status on the future sex of the European eel. J Fish Biol 49: 910-925 (1996). (Pubitemid 27012136)
52. Ijiri S, Kaneko H, Kobayashi T, Wang DS, Sakai F, et al: Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol Reprod 78: 333-341 (2008). (Pubitemid 351159989)
53. Ito LS, Yamashita M, Strüssmann CA: Histological process and dynamics of germ cell degeneration in pejerrey Odontesthes bonariensis larvae and juveniles during exposure to warm water. J Exp Zool A Comp Exp Biol 297: 169-179 (2003).
54. Ito LS, Cornejo AM, Yamashita M, Strüssmann CA: Thermal threshold and histological process of heat-induced sterility in adult pejerrey (Odontesthes bonariensis) : a comparative analysis of laboratory and wild specimens. Physiol Biochem Zool 81: 775-784 (2008a).
55. Ito LS, Takahashi C, Yamashita M, Strüssmann CA: Warm water induces apoptosis, gonadal degeneration, and germ cell loss in subadult pejerrey Odontesthes bonariensis (Pisces, Atheriniformes). Physiol Biochem Zool 81: 762-774 (2008b).
56. Karube M, Fernandino JI, Strobl-Mazzulla PH, Strüssmann CA, Yoshizaki G, et al: Characterization and expression profile of the ovarian cytochrome P-450 (CYP19A1) gene during the thermolabile sex determination period in pejerrey, Odontesthes bonariensis . J Exp Zool 307A:625-636 (2007). (Pubitemid 350057040)
57. Kettlewell JR, Raymond CS, Zarkower D: Temperature-dependent expression of turtle Dmrt1 prior to sexual differentiation. Genesis 26: 174-178 (2000).
58. Kim Y, Capel B: Balancing the bipotential gonad between alternative organ fates: a new perspective on an old problem. Dev Dyn 235: 2292-2300 (2006). (Pubitemid 44325247)
59. Kitano T, Takamune K, Kobayashi T, Nagahama Y, Abe S: Suppression of P450 aromatase gene expression in sex-reversed males produced by rearing genetically female larvae at a high water temperature during a period of sex differentiation in the Japanese flounder (Paralichthys olivaceus) . J Mol Endocrinol 23: 167-176 (1999). (Pubitemid 29503095)
60. Kitano T, Takamune K, Nagahama Y, Abe S: Aromatase inhibitor and 17α-methyltestosterone cause sex-reversal from genetical females to phenotypic males and suppression of P450 aromatase gene expression in Japanese flounder (Paralichthys olivaceus) . Mol Reprod Dev 56: 1-5 (2000). (Pubitemid 30193856)
61. Komen J, De Boer P, Richter CJJ: Male sex reversal in gynogenetic XX females of common carp ( Cyprinus carpio L.) by a recessive mutation in a sex determining gene. J Hered 83: 431-434 (1992). (Pubitemid 23100612)
62. Kondo M, Nanda I, Hornung U, Asakawa S, 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).
63. Koumoundouros G, Pavlidis M, Anezaki L, Kokkari C, Sterioti A, et al: Temperature sex determination in the European sea bass, Dicentrarchus labrax (L., 1758) (Teleostei, Perciformes, Moronidae): critical sensitive ontogenetic phase. J Exp Zool 292: 573-579 (2002).
64. Kraak SBM, de Looze EMA: A new hypothesis on the evolution of sex determination in vertebrates: big females ZW, big males XY. Neth J Zoo 43: 260-273 (1993).
65. Krueger WH, Oliveira K: Evidence for environmental sex determination in the American eel, Anguilla rostrata . Env Biol Fish 55: 381-389 (1999).
66. Kurokawa H, Saito D, Nakamura S, Katoh-Fukui Y, Ohta K, et al: Germ cells are essential for sexual dimorphism in the medaka gonad. Proc Natl Acad Sci USA 104: 16958-16963 (2007). (Pubitemid 350210972)
67. Kwon JY, Haghpanah V, Kogson-Hurtado LM, McAndrew BJ, Penman DJ: Masculinization of genetic female Nile tilapia (Oreochromis niloticus) by dietary administration of an aromatase inhibitor during sexual differentiation. J Exp Zool 287: 46-53 (2000).
68. Kwon JY, Mc Andrew BJ, Penman DJ: Cloning of brain aromatase gene and expression of brain and ovarian aromatase genes during sexual differentiation in genetic male and female Nile tilapia Oreochromis niloticus . Mol Reprod Dev 59: 359-370 (2001).
69. Kwon JY, Mc Andrew BJ, Penman DJ: Treatment with an aromatase inhibitor suppresses high-temperature feminization of genetic male (YY) Nile tilapia. J Fish Biol 60: 625-636 (2002).
70. Lampert KP: Facultative parthenogenesis in vertebrates: reproductive error or chance? Sex Dev 2: 290-301 (2008).
71. Lawrence C, Ebersole JP, Kesseli RV: Rapid growth and out-crossing promote female development in zebrafish (Danio rerio) . Environ Biol Fish 81: 239-246 (2008). (Pubitemid 350234083)
72. Lewis ZR, McClellan MC, Postlethwait JH, Cresko WA, Kaplan RH: Female-specific increase in primordial germ cells marks sex differentiation in threespine stickleback (Gasterosteus aculeatus) . J Morphol 269: 909-921 (2008).
73. Loffler KA, Zarkower D, Koopman P: Etiology of ovarian failure in blepharophimosis ptosis epicanthus inversus syndrome: FOXL2 is a conserved, early-acting gene in vertebrate ovarian development. Endocrinology 144: 3237-3243 (2003).
74. Luckenbach JA, Godwin J, Daniels HV, Borski RJ: Gonadal differentiation and effects of temperature on sex determination in southern flounder (Paralichthys lethostigma) . Aquaculture 216: 315-327 (2003).
75. Luckenbach JA, Borski RJ, Daniels HV, Godwin J: Sex determination in flatfishes: mechanisms and environmental influences. Semin Cell Dev Biol 20: 256-263 (2009).
76. Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, et al: A Y-specific, DM-domain gene, DMY , is required for male development in the medaka (Oryzias latipes). Nature 417: 559-563 (2002). (Pubitemid 34595924)
77. Miranda LA, Strobl-Mazzulla PH, Strüssmann CA, Parhar I, Somoza GM: Gonadotropinreleasing hormone neuronal development during the sensitive period of temperature sex determination in the pejerrey fish, Odontesthes bonariensis . Gen Comp Endocrinol 132: 444-453 (2003). (Pubitemid 36875733)
78. Morrison CM, Miyake T, Wright JR: Histological study of the development of the embryo and early larva of Oreochromis niloticus (Pisces: Cichlidae). J Morphol 247: 172-195 (2001).
79. Mylonas C, Anezaki L, Divanach P, Zanuy S, Piferrer F, et al: Influence of rearing temperature at two periods during early life on growth and sex differentiation of two strains of European sea bass. Fish Physiol Biochem 28: 167-168 (2003). (Pubitemid 39530376)
80. Nanda I, Kondo M, Hornung 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)
81. Nanda I, Hornung U, Kondo M, Schmid M, Schartl M: Common spontaneous sex-reversed XX males of the medaka Oryzias latipes . Genetics 163: 245-251 (2003).
82. Navarro-Martín L, Viñas J, Gutiérrez A, Di Croce L, Piferrer F: Sex-dependent differences in DNA-methylation levels in the promoter of the gonadal aromatase gene in a fish, the European sea bass (Dicentrarchus labrax) . In: Proceedings of the 8th International Symposium on Reproductive Physiology of Fish, June 3-8, Saint-Malo (2007).
83. Nusslein-Volhard C, Dahm R: Zebrafish: a Practical Approach (Oxford University Press, Oxford 2002).
84. Oldfield RG: Genetic, abiotic and social influences on sex differentiation in cichlid fishes and the evolution of sequential hermaphroditism. Fish and Fisheries 6:93-110 (2005).
85. Oldfield RG, McCrary J, McKaye KR: Habitat use, social behaviour and female and male size distributions of juvenile Midas cichlids, Amphilophus cf. citrinellus , in Lake Apoyo, Nicaragua. Carib J Sci 42: 197-207 (2006).
86. Ospina-Alvarez N, Piferrer F: Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change. PLoS ONE 3:e2837 (2008).
87. Oura M, Kimura H, Kinno T, Hattori RS, Yokota M, et al: Relation of apoptosis and sex steroid hormones during sex differentiation in pejerrey Odontesthes bonariensis , a species with temperature-dependent sex determination. In: Proceedings of the 6th International Symposium on Fish Endocrinology, p 136, June 22-27, Calgary, Canada (2008).
88. Pasmanik M, Callard GV: Aromatase and 5α-reductase in the teleost brain, spinal cord, and pituitary gland. Gen Comp Endocrinol 60: 244-251 (1985). (Pubitemid 16225274)
89. Patiño R, Davis KB, Schoore JE, et al: Sex differentiation of channel catfish gonads: normal development and effects of temperature. J Exp Zool 276: 209-218 (1996). (Pubitemid 26405241)
90. Pavlidis M, Koumoundouris G, Serioti A, Somarakis S, Divanach P, Kentouri M: Evidence of temperature-dependent sex determination in the European sea bass ( Dicentrarchus labrax L.). J Exp Zool 287: 225-232 (2000). (Pubitemid 30454116)
91. Piferrer F, Blázquez M, Navarro L, González A: Genetic, endocrine, and environmental components of sex determination and differentiation in the European sea bass ( Dicentrarchus labrax L.). Gen Comp Endocrinol 142: 102-110 (2005).
92. Quillet E, Aubard G, Quéau I: Mutation in a sex-determining gene in rainbow trout: detection and genetic analysis. J Hered 93: 91-99 (2002). (Pubitemid 34755390)
93. Quinn AE, Georges A, Sarre S, Guarino F, Ezaz T, Marshall Graves JA: Temperature sex reversal implies sex gene dosage in a reptile. Science 316: 411 (2007). (Pubitemid 46651484)
94. Radder RS, Quinn AE, Georges A, Sarre SD, Shine R: Genetic evidence for co-occurrence of chromosomal and thermal sex-determining systems in a lizard. Biol Lett 4: 176-178 (2008). (Pubitemid 351346295)
95. Römer U, Beisenherz W: Environmental determination of sex in Apistogramma (Cichlidae) and two other freshwater fishes (Teleostei). J Fish Biol 48: 714-725 (1996).
96. Rougeot C, Kanfitine SY, Prignon C, Gennotte V, Mélard C: Early sex reversal during the embryonic development in the Nile tilapia. In: Proceedings of the 8th International Symposium on Reproductive Physiology of Fish, p 161, June 3-8, Saint-Malo, France (2007).
97. Rougeot C, Prignon C, Ngouana Kengne CV, Mélard C: Effect of high temperature during embryogenesis on the sex differentiation process in the Nile tilapia, Oreochromis niloticus. Aquaculture 276: 205-208 (2008).
98. Rubin DA: Effect of pH on sex ratio in cichlids and a poeciliid (Teleostei). Copeia 1985: 233-235 (1985).
99. Ryskov AP: Genetically unstable microsatellitecontaining loci and genome diversity in clonally reproduced unisexual vertebrates. Int Rev Cell Mol Biol 270: 319-349 (2008).
100. Sadovy de Mitcheson Y, Liu M: Functional hermaphroditism in teleosts. Fish and Fisheries 9: 1-43 (2008).
101. Saillant E, Fostier A, Haffray P, Menu B, Thimonier J, et al: Temperature effects and genotype temperature interactions on sex-determination in the European sea bass ( Dicen -trarchus labrax L.). J Exp Zool 292: 494-505 (2002). (Pubitemid 34703270)
102. Saillant E, Chatain B, Menu B, Fauvel C, Vidal MO, Fostier A: Sexual differentiation and juvenile intersexuality in the European sea bass (Dicentrarchus labrax) . J Zool 260: 53-63 (2003a).
103. Saillant E, Fostier A, Haffray P, Menu B, Chatain B: Saline preferendum for the European sea bass, Dicentrarchus labrax , larvae and juveniles: effect of salinity on early development and sex determination. JEMBE 287: 103-117 (2003b).
104. Saillant E, Fostier A, Haffray P, Menu B, Laureau S, et al: Effects of rearing density, size grading and parental factors on sex ratios of the sea bass ( Dicentrarchus labrax L.) in intensive aquaculture. Aquaculture 221: 83-206 (2003c).
105. Sarre SD, Georges A, Quinn A: The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. Bioessays 26: 639-645 (2004). (Pubitemid 38758341)
106. Sato T, Endo T, Yamahira K, Hamaguchi S, Sakaizumi M: Induction of female-to-male sex reversal by high temperature treatment in medaka, Oryzias latipes. Zool Sci 22: 985-988 (2005). (Pubitemid 41566286)
107. Schartl M: Sex chromosome evolution in nonmammalian vertebrates. Curr Opin Genet Dev 14: 634-641 (2004).
108. Scott AG, Penman DJ, Beardmore JA, Skibinski DOF: The 'YY' supermale in Oreochromis niloticus (L.) and its potential in aquaculture. Aquaculture 78: 237-251 (1989).
109. Shang EH, Yu RM, Wu RS: Hypoxia affects sex differentiation and development, leading to a male-dominated population in zebrafish (Danio rerio) . Environ Sci Technol 40: 3118-3122 (2006).
110. Shine R, Elphick MJ, Donnellan S: Co-occurrence of multiple, supposedly incompatible modes of sex determination in a lizard population. Ecol Lett 5: 486-489 (2002). (Pubitemid 34824906)
111. Shoemaker C, Ramsey M, Queen J, Crews D: Expression of Sox9, Mis , and Dmrt1 in the gonad of a species with temperature-dependent sex determination. Dev Dyn 236: 1055-1063 (2007).
112. Shoemaker CM, Crews D: Analyzing the coordinated gene network underlying temperaturedependent sex determination in reptiles. Semin Cell Dev Biol 20: 293-303 (2009).
113. Siegfried KR, Nüsslein-Volhard C: Germ line control of female sex determination in zebrafish. Dev Biol 324: 277-287 (2008).
114. Socher SA, Yin Y, Dewolf WC, Morgentaler A: Temperature-mediated germ cell loss in the testis is associated with altered expression of the cell-cycle regulator p53. J Urol 157: 1986-1989 (1997).
115. Socorro S, Martins RS, Deloffre L, Mylonas CC, Canario AV: A cDNA for European sea bass (Dicentrachus labrax) 11beta-hydroxylase: gene expression during the thermosensitive period and gonadogenesis. Gen Comp Endocrinol 150: 164-173 (2007).
116. Strobl-Mazzulla PH, Lethimonier C, Gueguen MM, Karube M, Fernandino J, et al: Brain aromatase (Cyp19A2) and estrogen receptors, in larvae and adult pejerrey fish Odontesthes bonariensis : Neuroanatomical and functional relations. Gen Comp Endocrinol 158: 191-201 (2008).
117. Strüssmann CA, Patiño R: Sex determination, environmental, in Knobil E, Neill JD (eds): Encyclopedia of Reproduction, pp 402-409 (Academic Press, New York 1999).
118. Strüssmann CA, Moriyama S, Hanke EF, Calsina Cota JC, Takashima F: Evidence of thermolabile sex determination in pejerrey. J Fish Biol 48: 643-651 (1996). (Pubitemid 27048094)
119. Strüssmann CA, Saito T, Takashima F: Heat-induced germ cell deficiency in the teleosts Odontesthes bonariensis and Patagonina hatcheri . Comp Biochem Physiol A Mol Integr Physiol 119: 637-644 (1998).
120. Strüssmann CA, Oikawa T, Otake T, Kasuga S: Potential use of otolith microchemistry for field studies of temperature-dependent sex determination and gonadal degeneration in fish. Fish Physiol Biochem 28: 129-130 (2003). (Pubitemid 39530360)
121. Strüssmann CA, Kitahara A, Yamashita M: Role of apoptosis in temperature-dependent sex determination of pejerrey Odontesthes bonariensis. Cybium 32: 77-79 (2008).
122. Tessema M, Müller-Belecke A, Hörstgen- Schwark G: Effect of rearing temperatures on the sex ratios of Oreochromis niloticus populations. Aquaculture 258: 270-277 (2006).
123. Tong SK, Hsu HJ, Chung BC: Sex determination and gonad differentiation in zebrafish. In: Proceedings of the 5th International Symposium on the Biology of Vertebrate Sex Determination, p 104, April 20-24, Kona, Hawaii (2009).
124. Tsai CL, Chang SL, Wang LH, Chao TY: Temperature influences the ontogenetic expression of aromatase and oestrogen receptor mRNA in the developing tilapia (Oreochromis mossambicus) brain. J Neuroendocrinol 15: 97-102 (2003).
125. Uchida D, Yamashita M, Kitano T, Iguchi T: Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. J Exp Biol 205: 711-718 (2002). (Pubitemid 34861241)
126. Uchida D, Yamashita M, Kitano T, Iguchi T: An aromatase inhibitor or high water temperature induce oocyte apoptosis and depletion of P450 aromatase activity in the gonads of genetic female zebrafish during sex-reversal. Comp Biochem Physiol A Mol Integr Physiol 137: 11-20 (2004). (Pubitemid 38081282)
127. Valenzuela N: Evolution and maintenance of temperature-dependent sex determination, in Valenzuela N, Lance V (eds): Temperature- Dependent Sex Determination in Vertebrates, pp 131-147 (Smithsonian Books, Washington 2004).
128. Van Nes S, Andersen Ø: Temperature effects on sex determination and ontogenetic gene expression of the aromatases cyp19a and cyp19b , and the estrogen receptors esr1 and esr2 in atlantic halibut (Hippoglossus hippoglossus). Mol Reprod Dev 73: 1481-1490 (2006). (Pubitemid 44637100)
129. Vandeputte M, Dupont-Nivet M, Chavanne H, Chatain B: A polygenic hypothesis for sex determination of the European sea bass Dicentrarchus labrax . Genetics 176: 1049-1057 (2007).
130. Vrijenhoek RC: Unisexual fish: model systems for studying ecology and evolution. Annu Rev Ecol Systemat 25: 71-96 (1994).
131. Wang DS, Kobayashi T, Zhou LY, Paul-Prasanth B, Ijiri S, et al: Foxl2 up-regulates aromatase gene transcription in a female-specific manner by binding to the promoter as well as interacting with ad4 binding protein/steroidogenic factor 1. Mol Endocrinol 21: 712-725 (2007). (Pubitemid 46310192)
132. Wang LH, Tsai CL: Effects of temperature on the deformity and sex differentiation of tilapia, Oreochromis mossambicus. J Exp Zool 286: 534-537 (2000).
133. Warner DA, Shine R: The adaptive significance of temperature-dependent sex determination in a reptile. Nature 451: 566-568 (2008).
134. Wessels S, Hörstgen-Schwark G: Selection experiments to increase the proportion of males in Nile tilapia (Oreochromis niloticus) by means of temperature treatment. Aquaculture 272:S80-S87 (2007).
135. Western PS, Harry JL, Graves JAM, Sinclair AH: Temperature-dependent sex determination in the American alligator: AMH precedes SOX9 expression. Dev Dyn 216: 411-419 (1999).
136. Yamaguchi T, Yamaguchi S, Hirai T, Kitano T: Follicle-stimulating hormone signaling and Foxl2 are involved in transcriptional regulation of aromatase gene during gonadal sex differentiation in Japanese flounder, Paralichthys olivaceus . Biochem Biophys Res Comm 359: 935-940 (2007). (Pubitemid 46946907)
137. Yamamoto E: Studies on sex-manipulation and production of cloned populations in hirame, Paralichthys olivaceus (Temminck et Schlegel). Aquaculture 173: 235-246 (1999).
138. Yao HH, Capel B: Temperature, genes, and sex: a comparative view of sex determination in Trachemys scripta and Mus musculus . J Biochem 138: 5-12 (2005).
139. Yoshinaga N, Shiraishi E, Yamamoto T, Iguchi T, Abe S, Kitano T: Sexually dimorphic expression of a teleost homologue of Müllerian inhibiting substance during gonadal sex differentiation in Japanese flounder, Paralichthys olivaceus . Biochem Biophys Res Commun 322: 508-513 (2004). (Pubitemid 39490333)