Tilapia sex determination: Where temperature and genetics meet

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 153, Issue 1, 2009, Pages 30-38

  Baroiller, J F ^a   D'Cotta, H ^a   Bezault, E ^a,b   Wessels, S ^c   Hoerstgen Schwark, G ^c  

^a CIRAD   (France)

^b UNIVERSITY OF BERN   (Switzerland)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Genes; GSD; Selection response; TSD; Wild populations

Indexed keywords

BRAIN; ENVIRONMENTAL TEMPERATURE; GENDER AND SEX; GENE EXPRESSION PROFILING; GENETIC REGULATION; GONAD; HEAT SENSITIVITY; NONHUMAN; OREOCHROMIS NILOTICUS; QUANTITATIVE TRAIT; REVIEW; SEX DIFFERENTIATION; SRY GENE; TILAPIA;

OREOCHROMIS NILOTICUS; TILAPIA;

EID: 64449088222     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2008.11.018     Document Type: Review

References (94)

1. Abucay J.S., Mair G.C., Skibinski D.O., and Beardmore J.A. Environmental sex determination: the effect of temperature and salinity on sex ratio in Oreochromis niloticus L. Aquaculture 173 (1999) 219-234
2. Altena A., and Hörstgen-Schwark G. Effects of rearing temperatures on sex ratios in tilapia, Oreochromis niloticus L., investigations on a local population from the Lake Victoria in Kenya. Challenge to Organic Farming and Sustainable Land Use in the Tropics and Subtropics (2002), Deutscher Tropentag, Witzenhausen
3. Baras E., Prignon C., Gohoungo G., and Mélard C. Phenotypic sex differentiation of blue tilapia under constant and fluctuating thermal regimes and its adaptive and evolutionary implications. J. Fish Biol. 57 (2000) 210-223
4. Baras E., Jacobs B., and Mélard C. Effect of water temperature on survival, growth and phenotypic sex of mixed (XX-XY) progenies of Nile tilapia Oreochromis niloticus. Aquaculture 192 (2001) 187-199
5. Baras E., Mpo'n'tcha A., Driouch H., Prignon C., and Mélard C. Ontogenetic variations of thermal optimum for growth, and its implication on thermolabile sex determination in blue tilapia. J. Fish Biol. 61 (2002) 645-660
6. Baroiller J.F., and Clota F. Interactions between temperature effects and genotype on Oreochromis niloticus sex determination. J. Exp. Zool. 281 (1998) 507
7. Baroiller J.F., and D'Cotta H. Environment and sex determination in farmed fish. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 130 (2001) 399-409
8. Baroiller J.F., and Jalabert B. Contribution of research in reproductive physiology to the culture of tilapias. Aquat. Living Resour. 2 (1989) 105-116
9. Baroiller J.F., and Toguyeni A. The Tilapiini tribe: environmental and social aspects of reproduction and growth. In: Safran P. (Ed). Fisheries and Aquaculture, Encyclopedia of Life Support Systems (EOLSS), Developed under the Auspices of the UNESCO (2004), Eolss Publishers, Oxford,UK. http://www.eolss.net [http://www.eolss.net]
10. Baroiller J.F., Chourrout D., Fostier A., and Jalabert B. Temperature and sex chromosomes govern sex ratios of the mouthbrooding cichlid fish Oreochromis niloticus. J. Exp. Zool. 273 (1995) 216-223
11. Baroiller J.F., Clota F., and Geraz E. Temperature sex determination in two tilapias species, Oreochromis niloticus and the red tilapia (Red Florida strain): effect of high or low temperatures. In: Goetz F.W., and Thomas P. (Eds). Proceedings of the 5th International Symposium on the Reproductive Physiology of Fish (1995), The University of Texas, Austin, Austin, Texas, USA 158-160 July2-8, 1995
12. Baroiller J.F., Nakayama I., Foresti F., and Chourrout D. Sex determination studies in two species of teleost fish, Oreochromis niloticus and Leporinus elongatus. Zool. Stud. 35 (1996) 279-285
13. Baroiller J.F., Guiguen Y., and Fostier A. Endocrine and environmental aspects of sex differentiation in fish. Cell. Mol. Life Sci. 55 (1999) 910-931
14. Baroiller J.F., D'Cotta H., Wessels S., Bezault E., and Hoerstgen-Schwark G. Temperature effects on tilapia sex differentiation. Proceeding of the 6th International Symposium on Fish Endocrinology, Calgary, Canada, June 22-27 (2008)
15. Baron D., Cocquet J., Xia X., Fellous M., Guiguen Y., and Veitia R.A. An evolutionary and functional analysis of FoxL2 in rainbow trout gonad differentiation. J. Mol. Endocrinol. 33 (2004) 705-715
16. Beardmore J.A., Mair G.C., and Lewis R.I. Monosex male production in finfish as exemplified by tilapia: applications, problems, and prospects. Aquaculture 197 (2001) 283-301
17. Bezault E. Etude du système de déterminisme du sexe au sein de populations naturelles de tilapia du Nil, Oreochromis niloticus: Importance des composantes génétiques et environnementales. Université Paris XI, Orsay, France (2005) 270
18. Bezault E., Ozouf-Costaz C., D'Hont A., Volff J.N., Rognon X., and Baroiller J.F. Structure and evolution of pure and hybrid genomes of Tilapia. Chromosom. Res. 9 suppl. 1 (2001) 30
19. Bezault E., Clota F., Derivaz M., Chevassus B., and Baroiller J.F. Sex determination and temperature-induced sex differentiation in three natural populations of Nile tilapia (Oreochromis niloticus) adapted to extreme temperature conditions. Aquaculture 272 (2007) S3-S16
20. Bruton M.N., and Boltt R.E. Aspects of the biology of Tilapia mossambica Peters (Pisces: Cichlidae) in a natural freshwater lake (Lake Sibaya, South Africa). J. Fish. Biol. 7 (1975) 423-445
21. Bull J.J. Sex determination in reptiles. Q. Rev. Biol. 55 (1980) 3-21
22. Bull J.J. Sex determination: are two mechanisms better than one?. J. Biosci. 33 (2008) 5-8
23. Carrasco L.A.P., Penman D.J., and Bromage N.R. Evidence for the presence of sex chromosomes in the Nile tilapia (Oreochromis niloticus) from synaptonemal complex analysis of XX, XY and YY genotypes. Aquaculture 173 (1999) 207-218
24. Chang X., Kobayashi T., Senthilkumaran B., Kobayashi-Kajura H., Sudhakumari C.C., and Nagahama Y. Two types of aromatase with different encoding genes, tissue distribution and developmental expression in Nile tilapia (Oreochromis niloticus). Gen. Comp. Endocrinol. 141 (2005) 101-115
25. Charnier M. Action de la temperature sur la sex-ratio chez l'embryon d'Agama agama (Agamidae, Lacertilien). Soc. Biol. Quest. Af. 160 (1966) 620-622
26. Charnov E.L., and Bull J.J. When is sex environmentally determined?. Nature 266 (1977) 828-830
27. Cnaani A., Zilberman N., Tinman S., Hulat G., and Ron M. Genome-scan analysis for quantitative trait loci in an F2 tilapia hybrid. Mol. Genet. Genomics 272 (2004) 162-172
28. Cnaani A., Lee B.Y., Zilberman N., Ozouf-Costaz C., Hulata G., Ron M., D'Hont A., Baroiller J.F., D'Cotta H., Penman D.J., Tomasino E., Coutanceau J.P., Pepey E., Shirak A., and Kocher T.D. Genetics of sex determination in tilapiine species. Sex. Dev. 2 (2008) 43-54
29. Conover D.O. Temperature-dependent sex determination in fishes. In: Valenzuela N., and Lance V. (Eds). Temperature-Dependent Sex Determination in Vertebrates (2004), Smithsonian Books, Washington, DC 11-20
30. Conover D.O., and Kynard B.E. Environmental sex determination-interaction of temperature and genotype in a fish. Science 213 (1981) 577-579
31. D'Cotta H., Guiguen Y., Govoroun M.S., McMeel O., and Baroiller J.F. Aromatase plays a key role during normal and temperature-induced sex differentiation of tilapia Oreochromis niloticus. Mol. Reprod. Dev. 59 (2001) 265-276
32. D'Cotta H., Fostier A., Guiguen Y., Govoroun M., and Baroiller J.F. 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 (2001) 574-585
33. D'Cotta H., Pepey E., Pfennig F., Bienvenu D., Gutzeit H.O., Volff J.N., Wenning M., and Baroiller J.F. Sox9a, Sox9b and Amh are up-regulated in the gonads during natural and temperature-induced tilapia male differentiation. Proceedings of the 8th International Symposium on Reproductive Physiology of Fish, June 3rd-8th, Saint-Malo, France (2007)
34. D'Cotta H., Pepey E., Wessels S., Poonlaphdecha S., Reinelt B., Hoerstgen-Schwark G., and Baroiller J.F. Temperature-induced male differentiation in the Nile tilapia: gonad gene expression using female monosex populations and divergent thermos-sensitive lines. Proceedings of the 20th International Congress of Zoology, S10 Sex determination & differentiation, Paris, August 26-29 (2008)
35. Desprez D., and Mélard C. Effect of ambient water temperature on sex determinism in the blue tilapia, Oreochromis aureus. Aquaculture 162 (1998) 79-84
36. Desprez D., Mélard C., Hoareau MC Bellemène Y., Bosc P., and Baroiller J.F. Inheritance of sex in two ZZ pseudofemale lines of tilapia Oreochromis aureus. Aquaculture 218 (2003) 131-140
37. Devlin R.H., and Nagahama Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208 (2002) 191-366
38. Ezaz T., Quinn A.E., Miura I., Sarre S.D., Georges A., and Marshall Graves J.A. The dragon lizard Pogona vitticeps has ZZ/ZW micro-sex chromosomes. Chromosom. Res. 13 (2005) 763-776
39. FAO Fisheries and Aquaculture Information and Statistics Service [FAO FIES], 2008.
40. Foresti F., Oliveira C., Galetti Jr. P.M., and Almeida Toledo L.F. Synaptonemal complex analysis in spermatocytes of tilapia, Oreochromis niloticus (Pisces, Cichlidae). Genome 36 (1993) 1124-1128 (che G10/P5)
41. Godwin J., Luckenbach J.A., and Borski R.J. Ecology meets endocrinology: environmental sex determination in fishes. Evol. Dev. 5 (2003) 40-49
42. Griffin D.K., Harvey S.C., Campos-Ramos R., Ayling L.J., Bromage N.R., Masabanda J.S., and Penman D.J. Early origins of the X and Y chromosomes: lessons from tilapia. Cytogenet. Genome Res. 99 (2002) 157-163
43. Guiguen Y., Baroiller J.F., Ricordel M.J., Iseki K., Mcmeel O.M., Martin S.A., and Fostier A. Involvement of estrogens in the process of sex differentiation in two fish species: the rainbow trout (Oncorhynchus mykiss) and a tilapia (Oreochromis niloticus). Mol. Reprod. Dev. 54 (1999) 154-162
44. Hammerman I.S., and Avtalion R.R. Sex determination in Sarotherodon (Tilapia). II. The sex ratio as a tool for the determination of genotype. A mathematical model of autosomal and gonosomal influence. Theor. Appl. Genet. 55 (1979) 177-187
45. Ijiri S., Kaneko H., Kobayashi T., Wang D.S., Sakai F., Paul-Prasanth B., Nakamura M., and Nagahama Y. Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol. Reprod. 78 (2008) 333-341
46. Jalabert B., Moreau J., Planquette P., and Billard R. Déterminisme du sexe chez Tilapia macrochir et Tilapia nilotica: action de la methyltestostérone dans l'alimentation des alevins sur la différenciation sexuelle; proportion des sexes dans la descendance des mâles "inversés". Ann. Biol. Anim. Biochim. Biophys. 14 4-B (1974) 729-739
47. Kwon J.Y., Haghpanah V., Kogson-Hurtado L.M., McAndrew B.J., and Penman D.J. Masculinization of genetic female Nile tilapia (Oreochromis niloticus) by dietary administration of an aromatase inhibitor during sexual differentiation. J. Exp. Zool. 287 (2000) 46-53
48. Kwon J.Y., Mc Andrew B.J., and Penman D.J. 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 (2001) 359-370
49. Lee B.Y., and Kocher T.D. Exclusion of Wilms tumor (WT1) and ovarian cytochrome P450 aromatase (CYP19A1) as candidates for sex determination genes in Nile tilapia (Oreochromis niloticus). Anim. Genet. 38 (2007) 85-86
50. Lee B.Y., Penman D.J., and Kocher T.D. Identification of a sex-determining region in Nile tilapia (Oreochromis niloticus) using bulked segregant analysis. Anim. Genet. 34 (2003) 379-383
51. Lee B.Y., Hulata G., and Kocher T.D. Two unlinked loci controlling the sex of blue tilapia (Oreochromis aureus). Heredity 92 (2004) 543-549
52. Loffler K.A., Zarkower D., and 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 (2003) 3237-3243
53. Mair G.C., Scott A.G., Penman D., Beardmore J.A., and Skibinski D.O. Sex determination in genus Oreochromis: 1-sex reversal, gynogenesis and triploidy in O. niloticus (L.). Theor. Appl. Genet. 82 (1991) 144-152
54. Mair G.C., Scott A., Penman D.J., Skibinski D.O.F., and Beardmore J.A. II. Sex reversal, hybridisation, gynogenesis and triploidy in O. aureus Steindachner. Theor. Appl. Genet. 82 (1991) 153-160
55. Mair G.C., Abucay J.S., Skibinski D.O.F., Abella T.A., and Beardmore J.A. Genetic manipulation of sex ratio for the large-scale production of all-male tilapia, Oreochromis niloticus. Can. J. Fish. Aquat. Sci. 54 (1997) 396-404
56. Majumdar K.C., and McAndrew B.J. Relative DNA content of somatic nuclei and chromosomal studies in three genera: Tilapia, Sarotherodon and Oreochromis of the tribe Tilapiini. Genetica 68 (1986) 165-168
57. Martins C., Oliveira C., Wasko A.P., and Wright J.M. Physical mapping of the Nile tilapia (Oreochromis niloticus) genome by fluorescent in situ hybridization of repetitive DNAs to metaphase chromosomes-a review. Aquaculture 231 (2004) 37-49
58. Matsuda M., Nagahama Y., Shinomiya A., Sato T., Matsuda C., Kobayashi T., Morrey C.E., Shibata N., Asakawa S., Shimizu N., Horik H., Hamaguchi S., and Sakaizumi M. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417 (2002) 559-563
59. Miyamoto Y., Taniguchi H., Hamel F., Silversides D.W., and Viger R.S. A GATA4/WT1 cooperation regulates transcription of genes required for mammalian sex determination and differentiation. BMC Mol. Biol. 9 (2008) 44
60. Morrison C.M., Miyake T., and Wright Jr. J.R. Histological study of the development of the embryo and early larva of Oreochromis niloticus (Pisces: Cichlidae). J. Morphol. 247 (2001) 172-195
61. Müller-Belecke A., and Hörstgen-Schwark G. Sex determination in tilapia (Oreochromis niloticus): sex ratios in homozygous gynogenetic progeny and their offspring. Aquaculture 137 (1995) 57-65
62. Nakamura M. Dosage-dependent changes in the effect of oral administration on gonadal sex differentiation in Tilapia mossambica. Bull. Fac. Fish Hokkaido Univ. 26 (1975) 99-108
63. Nakamura M., Kobayashi T., Chang X.T., and Nagahama Y. Gonadal sex differentiation in teleost fish. J. Exp. Zool. 281 (1998) 362-372
64. Nanda I., Kondo M., Hornung U., Asakawa S., Winkler C., Shimizu A., Shan Z., Haaf T., Shimizu N., Shima A., Schmid M., and Schartl M. 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 (2002) 11778-11783
65. Ohno S. Sex Chromosomes and Sex-Linked Genes (1967), Springer-Verlag, Berlin
66. Ospina-Alvarez N., and 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 7 (2008) e2837
67. Philippart J.C., and Ruwet J.C. Ecology and distribution of tilapias. In: Pullin R.S.V., and Lowe-McConnell R.H. (Eds). The Biology and Culture of Tilapias vol. 7 (1982), ICLARM, Manila, Philippines 15-60
68. Pieau C. Sur la proportion sexuelle chez les embryons de deux Cheloniens (Testudo graeca L. et Emys orbicularis L.) issus d'oeufs incubés artificiellement. C. R. Acad. Sci. Paris 272 (1971) 3071-3074
69. Pieau C. Effets de la température sur le développement des glandes génitales chez les embryons de deux Chéloniens, Emys orbicularis L. et. Testudo. graeca. L. C. R. Acad. Sci. Paris 274 (1972) 719-722
70. Quinn A.E., Georges A., Sarre S., Guarino F., Ezaz T., and Marshall Graves J.A. Temperature sex reversal implies sex gene dosage in a reptile. Science 316 (2007) 411
71. Radder R.S., Quinn A.E., Georges A., Sarre S.D., and Shine R. Genetic evidence for co-occurrence of chromosomal and thermal sex-determining systems in a lizard. Biol. Letts. 4 (2008) 176-178
72. Rougeot C., Kanfitine S.Y., Prignon C., Gennotte V., and Mélard C. Early sex reversal during the embryonic development in the Nile tilapia. In: Roudaut G., Labbé C., and Bobe J. (Eds). Proceedings of the 8th International Symposium on Reproductive Physiology of Fish, June 3-8, Saint-Malo, France (2007) 161
73. Rougeot C., Prignon C., Ngouana Kengne C.V., and Mélard C. Effect of high temperature during embryogenesis on the sex differentiation process in the Nile tilapia, Oreochromis niloticus. Aquaculture 276 (2008) 205-208
74. Sarre S.D., Georges A., and Quinn A. The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. Bioessays 26 (2004) 639-645
75. Scott A.G., Penman D.J., Beardmore J.A., and Skibinski D.O.F. The 'YY' supermale in Oreochromis niloticus (L.) and its potential in aquaculture. Aquaculture 78 (1989) 237-251
76. Shine R., Elphick M.J., and Donnellan S. Co-occurrence of multiple, supposedly incompatible modes of sex determination in a lizard population. Ecol. Lett. 5 (2002) 486-489
77. Shirak A., Seroussi E., Cnaani A., Howe A.E., Domokhovsky R., Zilberman N., Kocher T.D., Hulata G., and Ron M. Amh and dmrta2 genes map to tilapia (Oreochromis spp.) linkage group 23 within quantitative trait locus regions for sex determination. Genetics 174 (2006) 1573-1581
78. Shoemaker C., Ramsey M., Queen J., and Crews D. Expression of Sox9, Mis, and Dmrt1 in the gonad of a species with temperature-dependent sex determination. Dev. Dyn. 236 (2007) 1055-1063
79. Smith C.A., and Sinclair A.H. Sex determination: insights from the chicken. Bioessays 26 (2004) 120-132
80. Strüssmann C.A., and Patiño R. Sex determination, environmental. In: Knobil E., and Neill J.D. (Eds). Encyclopedia of Reproduction (1999), Academic Press, New York 402-409
81. Strüssmann C.A., Moriyama S., Hanke E.F., Calsina Cota J.C., and Takashima F. Evidence of thermolabile sex determination in pejerrey. J. Fish Biol. 48 (1996) 643-651
82. Tessema M., Müller-Belecke A., and Hörstgen-Schwark G. Effect of rearing temperatures on the sex ratios of Oreochromis niloticus populations. Aquaculture 258 (2006) 270-277
83. Toguyeni A., Fauconneau B., Fostier A., Abucay J., Mair G.C., and Baroiller J.F. Influence of sexual phenotype and genotype, and sex-ratio on growth performances in tilapia, Oreochromis niloticus. Aquaculture 207 (2002) 249-261
84. Trewavas E. Tilapiine Fishes of the Genera Sarotherodon, Oreochromis and Danakilia (1983), British Museum Natural History, London, UK
85. Valenzuela N. Evolution and maintenance of temperature-dependent sex determination. In: Valenzuela N., and Lance V. (Eds). Temperature-Dependent Sex Determination in Vertebrates (2004), Smithsonian Books, Washington, DC 131-147
86. Valenzuela N. Sexual development and the evolution of sex determination. Sex. Dev. 2 (2008) 64-72
87. Wang L.H., and Tsai C.L. Effects of temperature on the deformity and sex differentiation of tilapia, Oreochromis mossambicus. J. Exp. Zool. 286 (2000) 534-537
88. Wang D.S., Kobayashi T., Zhou L.Y., Paul-Prasanth B., Ijiri S., Sakai F., Okubo K., Morohashi K., and Nagahama Y. 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 (2007) 712-725
89. Warner D.A., and Shine R. The adaptive significance of temperature-dependent sex determination in a reptile. Nature 451 (2008) 566-568
90. Wessels S., and Hörstgen-Schwark G. Selection experiments to increase the proportion of males in Nile tilapia (Oreochromis niloticus) by means of temperature treatment. Aquaculture 272 (2007) S80-S87
91. Wessels S., and Hörstgen-Schwark G. The influence of rearing temperature and spawner's temperature responsiveness on progeny sex ratios in matings with Nile tilapia YY males. Proceedings of the 32nd Annual Larval Fish Conference, August 4-7, Kiel, Germany (2008)
92. Western P.S., Harry J.L., Graves J.A., and Sinclair A.H. Temperature-dependent sex determination in the American alligator: AMH precedes SOX9 expression. Dev. Dyn. 216 (1999) 411-419
93. Yamamoto T. Sex differentiation. Fish Physiol. 3 (1969) 117-175
94. Yao H.H., and Capel B. Temperature, genes, and sex: a comparative view of sex determination in Trachemys scripta and Mus musculus. J. Biochem. 138 (2005) 5-12