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Morphology, endocrinology, and environmental modulation of gonadal sex differentiation in teleost fishes

Abstract

Successful reproduction by an adult depends on the normal ontogenesis of the gonads, a complex process of cellular and histological differentiation that starts early in life. This process is theoretically predetermined by genetic factors and includes sensitisation of the bipotential gonads to endogenous endocrine factors prior to, during and even after commitment to maleness or femaleness. However, young fish are relatively vulnerable to a host of environmental (physical and chemical) factors that can affect this endogenous endocrine axis, disturbing or even overriding the putative developmental pathway. This sexually lability can be exploited to our advantage for the production of monosex fish populations of the most valuable sex for food production or aquarium fish trade. On the other hand, it represents also a potential path for undesirable influences from endocrine-disrupting chemicals and climatic factors, particularly environmental temperature. This paper provides a detailed account of the early histological process of gonadal sex differentiation, with special reference to gonochoristic species, and reviews the criteria employed to positively identify ovarian and testicular differentiation. It also reviews the development of endocrine competence and sensitivity of the differentiating gonads to exogenous influences in the context of the relative stability of genotypic sex determination in various fish species. Sex differentiation in some species seems to be under strong genetic control and may not require endogenous sex steroid production. Conversely, reliance on endogenous sex steroids for gonadal differentiation is observed in other species and this phenomenon is apparently associated with a higher incidence of environment (mainly temperature)-labile sex differentiation.

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References

  • Afonso, L.O.B., Wassermann, G.J. and Oliveira, R.T. 2001. Sex reversal in Nile tilapia (Oreochromis niloticus) using a nonsteroidal aromatase inhibitor. J. Exp. Zool. 290: 177–181.

    Article  PubMed  CAS  Google Scholar 

  • Akhundov. M.M. 2000. The ecological plasticity of sturgeons sex differentiation. In: Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. pp. 267. Edited by B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson and S.O. Stefansson. Fish Symp 99, Bergen, Norway.

  • Arai, K. 2001. Genetic improvement of aquaculture finfish species by chromosome manipulation techniques in Japan. Aquaculture 197: 205–228.

    Article  CAS  Google Scholar 

  • Baroiller, J.-F. and D'Cotta, H. 2001. Environment and sex determination in farmed fish. Comp. Biochem. Physiol. 130C: 399–409.

    CAS  Google Scholar 

  • Baroiller, J.-F., Guiguen, Y. and Fostier, A. 1999. Endocrine and environmental aspects of sex differentiation in fish. Cell. Mol. Life Sci. 55: 910–931.

    Article  CAS  Google Scholar 

  • Beardmore, J.A., Mair, G.C. and Lewis, R.I. 2001. Monosex male production in finfish as exemplified by tilapia: Applications, problems, and prospects. Aquaculture 197: 283–301.

    Article  Google Scholar 

  • Chang, C.F., Hung, C.Y., Chiang, M.C. and Lan, S.C. 1999. The concentrations of plasma sex steroids and gonadal aromatase during controlled sex differentiation in grey mullet, Mugil cephalus. Aquaculture 177: 37–45.

    Article  CAS  Google Scholar 

  • Chieffi, G. 1957. The reproductive system of elasmobranchs: development and endocrinological aspects. In: Sharks, skates and ray. pp. 553–589. Edited by P.W. Gilbert, R.F. Mathewson and D.P. Rall. John Hopkins Press, Baltimore, Maryland.

    Google Scholar 

  • Colombo, G. and Grandi, G. 1996. Histological study of the development and sex differentiation of the gonad in the European eel. J. Fish Biol. 48: 493–512.

    Article  Google Scholar 

  • Crews, D. 1996. Temperature-dependent sex determination: the interplay of steroid hormones and temperature. Zool. Sci. 13: 1–13.

    Article  PubMed  CAS  Google Scholar 

  • D'Cotta, H., Fostier, A., Guiguen, Y., Govoroun, M. and Baroiller, J.-F. 2001. Search for genes involved in the temperature-induced gonadal sex differentiation in the tilapia, Oreochromis niloticus. J. Exp. Zool. 290: 574–585.

    Article  PubMed  Google Scholar 

  • D'Cotta, H., Guiguen, Y., Govoroun, M., McMeel, O. and Baroiller, J.-F. 2000. Aromatase gene expression in temperature-induced gonadal sex differentiation of tilapia Oreochromis niloticus. In: Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. pp. 197–199. Edited by B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson and S.O. Stefansson. Fish Symp 99, Bergen, Norway.

  • Devlin, R.H. and Nagahama, Y. 2002. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208: 191–364.

    Article  CAS  Google Scholar 

  • Fedorov, K.E., Zubova, S.E., Semenov, V.V. and Burlakov, A.B. 1990. Secretory cells in the gonads of the young sterlet Acipenser ruthenus during sex differentiation. J. Ichthyol. 30: 65–75.

    Google Scholar 

  • Feist, G., Schreck, C.B., Fitzpatrick, M.S. and Redding, J.M. 1990. Sex steroid profiles of coho salmon (Oncorhynchus kisutch) during early development and sexual differentiation. Gen. Comp. Endocrinol. 80: 299–313.

    Article  PubMed  CAS  Google Scholar 

  • Fitzpatrick, M.S., Pereira, C.B. and Schreck, C.B. 1993. In vitro steroid secretion during early development of mono-sex rainbow trout: sex differences, onset of pituitary control, and effects of dietary steroid treatment. Gen. Comp. Endocrinol. 91: 199–215.

    Article  PubMed  CAS  Google Scholar 

  • Francis, R.C. 1992. Sexual lability in teleosts: developmental factors. Quart. Rev. Biol. 67: 1–18.

    Article  Google Scholar 

  • Govoroun, M., McMeel, O.M., D'Cotta, H., Ricordel, M.-J., Smith, T.J., Fostier, A. and Guiguen, Y. 2001a. Steroid enzyme gene expressions during natural and androgen-induced gonadal differentiation in the rainbow trout, Oncorhynchus mykiss. J. Exp. Zool. 290: 558–566.

    Article  PubMed  CAS  Google Scholar 

  • Govoroun, M., McMeel, O.M., Mecherouki, H., Smith, T.J. and Guiguen, Y. 2001b. 17β-estradiol treatment decreases steroidogenic enzyme messenger ribonuclei acid levels in the rainbow trout testis. Endocrinology 142: 1841–1848.

    Article  PubMed  CAS  Google Scholar 

  • Green, B.W. and Teichert-Coddington, D.R. 2000. Human food safety and environmental assessment of the use of 17α-methyltestosterone to produce male tilapia in the United States. J. World Aquaculture Soc. 31: 337–357.

    Article  Google Scholar 

  • Guiguen, Y., Baroiller, J.-F., Ricordel, M.-J., Iseki, K., McMeel, O.M., Martin, S.A.M. and Fostier, A. 1999. 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. Develop. 54: 154–162.

    Article  CAS  Google Scholar 

  • Guiguen, Y., Govoroun, M., D'Cotta, H.D., McMeel, O.M. and Fostier, A. 2000. Steroids and gonadal sex differentiation in the rainbow trout, Oncorhynchus mykiss. In: Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. pp. 241–243. Edited by B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson and S.O. Stefansson. Fish Symp 99, Bergen, Norway.

  • Hann, H.W. 1927. The history of the germ cells of Cottus bairdie Girard. J. Morphol. Physiol. 43: 427–498.

    Article  Google Scholar 

  • Harder, W. 1975. Anatomy of Fishes. E. Schweizerbart'sche Verlagsbuchhandlung, Stuttgart.

    Google Scholar 

  • Hayes, T.B. 1998. Sex determination and primary sex differentiation in amphibians: genetic and developmental mechanisms. J. Exp. Zool. 281: 373–399.

    Article  PubMed  CAS  Google Scholar 

  • Hunter, G.A. and Donaldson, E.M. 1983. Hormonal sex control and its application to fish culture. In: Fish Physiology Vol. IX, Part B Behaviour and Fertility Control. pp. 223–303. Edited by W.S. Hoar, J.D. Randall and E.M. Donaldson. Academic Press, New York.

    Google Scholar 

  • Hoar, W.S. 1969 Reproduction. In: Fish Physiology, Vol. III. Reproduction and Growth, Bioluminescence, Pigments, and Poisons. pp. 1–72. Edited by W.S. Hoar and D.J. Randall. Academic Press, New York

    Google Scholar 

  • Hyodo, Y., Tuzuki, E. and Egami, N. 1966. Multiplication of primordial germ cells and initiation of meiosis in the medaka, Oryzias latipes. Japan. J. Exp. Morphol. 20: 98.

    Google Scholar 

  • Ito, L.S., Yamashita, M. and Strüssmann, C.A. 2002. Dynamics of heat-induced germ cell loss in pejerrey, Odontesthes bonariensis. Fish. Sci. 68S: in press.

  • Jensen, G.L. and Shelton, W.L. 1983. Gonadal differentiation in relation to sex control of grass carp, Ctenopharyngodon idella (Pisces: Cyprinidae). Copeia 1983: 749–755.

    Article  Google Scholar 

  • Kallman, K.D. 1984. A new look at sex determination in Poeciliid fishes. In: Evolutionary genetics of fishes. pp. 95–171. Edited by B.J. Turner. Plenum Press, New York.

    Google Scholar 

  • Kanamori, A., Nagahama, Y. and Egami, N. 1985 Development of the tissue architecture in the gonads of the medaka Oryzias latipes. Zool. Sci. 2: 695–706.

    Google Scholar 

  • Karube, M. 2001. Cloning and expression of cytochrome P450 aromatase and estrogen receptors α and β genes during the critical period of thermolabile sex determination in pejerrey Odontesthes bonariensis. M.Sc. Thesis. Tokyo University of Fisheries, Tokyo, Japan.

    Google Scholar 

  • Kawahara, T. and Yamashita, I. 2000. Estrogen-independent ovary formation in the medaka fish, Oryzias latipes. Zool. Sci. 17: 65–68.

    Article  CAS  PubMed  Google Scholar 

  • Kitano, T., Takamune, K., Kobayashi, T., Nagahama, Y. and Abe, S. 1999. Suppression of P450 aromatase gene expression in sexreversed 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.

    Article  PubMed  CAS  Google Scholar 

  • Kitano, T., Takamune, K., Nagahama, Y. and Abe, S. 2000. 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. Develop. 56: 1–5.

    Article  CAS  Google Scholar 

  • Korpelainen, H. 1990. Sex ratios and conditions required for environmental sex determination in animals. Biol. Rev. 65: 147–184.

    PubMed  CAS  Google Scholar 

  • Kwon, J., Haghpanah, V., Kogson-Hurtado, L.M., McAndrew, B.J. and Penman, D.J. 2000. Masculinization of genetic female Nile tilapia (Oreochromis niloticus) by dietary administration of an aromatase inhibitor during sexual differentiation. J. Exp. Zool. 287: 46–53.

    Article  PubMed  CAS  Google Scholar 

  • Kwon, J., McAndrew, B.J. and Penman, D.J. 2000. Inhibition of aromatase activity suppresses high-temperature feminisation of genetic male Nile tilapia, Oreochromis niloticus). In: Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. pp. 268. Edited by B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson and S.O. Stefansson. Fish Symp 99, Bergen, Norway.

  • Kurita, M. 1999. Effects of water temperature on the process of gonadal sex differentiation in pejerrey. M.Sc. Thesis. Tokyo University of Fisheries, Tokyo, Japan.

    Google Scholar 

  • Lebrun, C., Billard, R. and Jalabert, B. 1982. Changes in the number of germ cells in the gonads of the rainbow trout (Salmo gairdneri) during the first 10 post-hatching weeks. Reprod. Nutr. Dev. 22: 405–412.

    PubMed  CAS  Google Scholar 

  • Liu, S., Govoroun, M., D'Cotta, H.D., Ricordel, M.-J., Lareyre, J.-J., McMeel, O.M., Smith, T., Nagahama, Y. and Guiguen, Y. 2000. Expression of cytochrome P45011β. (11β-hydroxylase) gene during gonadal differentiation and spermatogenesis in rainbow trout, Oncorhynchus mykiss. J. Steroid Biochem. Mol. Biol. 75: 291–298.

    Article  PubMed  CAS  Google Scholar 

  • Lofts, B. and Bern, H.B. 1972. The functional morphology of steroidogenic tissue. In: Steroids in nonmammalian vertebrates. pp. 37–125. Edited by D.R. Idler. Academic Press, New York.

    Google Scholar 

  • Marchand, O., Govoroun, M., D'Cotta, H.D., McMeel, O.M., Lareyre, J.-J., Bernot, A., Laudet, V. and Guiguen, Y. 2000. DMRT1 expression during gonadal differentiation and spermatogenesis in the rainbow trout, Oncorhynchus mykiss. Biochem. Biophys. Acta 1493: 180–187.

    PubMed  CAS  Google Scholar 

  • Matsuda, M., Nagahama, Y., Shinomiya, A., Satoh, T., Matsuda, C., Kobayashi, T., Morrey, C.E., Shibata, N., Asakawa, S., Shimizu, N., Hori, H., Hamaguchi, S. and Sakaizumi, M. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417: 559–562.

  • Miranda, L.A., Strüssmann, C.A. and Somoza, G.M. 2001. Immunocytochemical identification of GtH1 and GtH2 cells during the temperature-sensitive period for sex determination in pejerrey, Odontesthes bonariensis. Gen. Comp. Endocrinol. 124: 45–52.

    Article  PubMed  CAS  Google Scholar 

  • Nagahama, Y. 2000. Gonadal steroid hormones: major regulators of gonadal sex differentiation and gametogenesis in fish. In: Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. pp. 211–222. Edited by B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson and S.O. Stefansson. Fish Symp 99, Bergen, Norway.

  • Nagahama, Y., Kagawa, H. and Young, G. 1982. Cellular sources of sex steroids in teleost gonads. Can. J. Fish. Aquat. Sci. 39: 56–64.

    Article  CAS  Google Scholar 

  • Nakamura, M. 1978. Morphological and experimental studies on sex differentiation of the gonad in several teleost fishes. Ph.D. Thesis. Hokkaido University, Hokkaido, Japan.

    Google Scholar 

  • Nakamura, M. 1982. Gonadal sex differentiation in whitespotted char, Salvelinus leucomaenis. Japan. J. Ichthyol. 28: 431–436.

    Google Scholar 

  • Nakamura, M. 1984. Effects of estradiol-17β on gonadal sex differentiation in two species of salmonids, the masu salmon, Oncorhynchus masou, and the chum salmon, O. keta. Aquaculture 43: 83–90.

    Article  CAS  Google Scholar 

  • Nakamura, M., Kobayashi, T., Chang, X.-T. and Nagahama, Y. 1998. Gonadal sex differentiation in teleost fish. J. Exp. Zool. 281: 362–372.

    Article  Google Scholar 

  • Nakamura, M., Kobayashi, T., Yoshiura, Y. and Nagahama, Y. 2000. Role of endogenous steroid hormones on gonadal sex differentiation in fish. In: Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. pp. 247–249. Edited by B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson and S.O. Stefansson. Fish Symp 99, Bergen, Norway.

  • Nakamura, M. and Nagahama, Y. 1985. Steroid producing cells during ovarian differentiation of the tilapia Sarotherodon niloticus. Dev. Growth. Differ. 27: 701–708.

    Article  Google Scholar 

  • Nakamura, M. and Nagahama, Y. 1989. Differentiation and development of Leydig cells, and changes of testosterone levels during testicular differentiation in tilapia Oreochromis niloticus. Fish Physiol. Biochem. 7: 211–219.

    CAS  Google Scholar 

  • Nakamura, M. and Nagahama, Y. 1993. Ultrastructural study on the differentiation of steroid-producing cells during ovarian differentiation in the amago salmon, Oncorhynchus rhodurus. Aquaculture 112: 237–251.

    Article  CAS  Google Scholar 

  • Nakamura, M. and Takahashi, H. 1973. Gonadal sex differentiation in tilapia, with special regard to the time of estrogen treatment effective in inducing complete feminization of genetic males. Bull. Fac. Fish. Hokkaido Univ. 24: 1–13.

    Google Scholar 

  • Nakamura, M., Takahashi, H. and Hiroi, O. 1974. Sex differentiation in the masu salmon (Oncorhynchus masou). Sci. Rep. Hokkaido Salmon Hatchery 28: 1–8.

    Google Scholar 

  • Onitake, K. 1972. Morphological studies of normal sexdifferentiation and induced sex-reversal process of gonads in the medaka, Oryzias latipes. Annot. Zool. Japan. 45: 159–169.

    Google Scholar 

  • Pandian, T.J. and Koteeswaran, R. 1999. Lability of sex differentiation in fish. Current Science 76: 580–583.

    Google Scholar 

  • Pandian T.J. and Sheela, S.G. 1995. Hormonal induction of sex reversal in fish. Aquaculture 138: 1–22

    Article  CAS  Google Scholar 

  • Pandian, T.J., Venugopal, T. and Koteeswaran, R. 1999. Problems and prospects of hormone, chromosome and gene manipulations in fish. Current Science 76: 369–386.

    CAS  Google Scholar 

  • Parhar, I.S. 1997. GnRH in Tilapia: three genes, three origins and their roles. In: GnRH neurons: gene to behavior, pp. 99–122. Edited by I.S. Parhar and Y. Sakuma. Brain Shuppan, Tokyo.

    Google Scholar 

  • Patiño, R. 1997. Manipulations of the reproductive system of fishes by means of exogenous chemicals. Prog. Fish-Cult. 59: 118–128.

    Article  Google Scholar 

  • Patiño, R. Davis, K.B., Schoore, J.E., Uguz, C., Strüssmann, C.A., Parker, N.C., Simco, B.A. and Goudie, C.A. 1996. Sex differentiation of channel catfish gonads: normal development and effects of temperature. J. Exp. Zool. 276: 209–218.

    Article  Google Scholar 

  • Patiño, R. and Takashima, F. 1995. In: An Atlas of fish histology, normal and pathological features (2nd edition), pp. 128–153. Edited by F. Takashima and T. Hibiya. Kodansha/Gustav Fischer Verlag, Tokyo/Stuttgart.

    Google Scholar 

  • Pieau, C. 1996. Temperature variation and sex determination in reptiles. BioEssays 18: 19–26.

    Article  CAS  Google Scholar 

  • Piferrer, F. 2001. Endocrine sex control strategies for the feminization of teleost fish. Aquaculture 197: 229–281.

    Article  CAS  Google Scholar 

  • Piferrer, F., Zanuy, S., Carrillo, M., Solar, I.I., Devlin, R.H., and Donaldson, E.M. 1994. Brief treatment with an aromatase inhibitor during sex differentiation causes chromosomally female salmon to develop as normal, functional females. J. Exp. Zool. 270: 255–262.

    Article  Google Scholar 

  • Rothbard, S., Moav, B. and Yaron, Z. 1987. Changes in steroid concentrations during sexual ontogenesis in tilapia. Aquaculture 61: 59–74.

    Article  CAS  Google Scholar 

  • Satoh, N. 1974. An ultrastructural study of sex differentiation in the teleost Oryzias latipes. J. Embryol. Exp. Morphol. 32: 195–215.

    PubMed  CAS  Google Scholar 

  • Satoh, N. and Egami, N. 1972. Sex differentiation of germ cells in the teleost, Oryzias latipes, during normal embryonic development. J. Embryol. Exp. Morphol. 28: 385–395.

    PubMed  CAS  Google Scholar 

  • Scholz, S. and Gutzeit, H.O. 2000. 17α-ethinylestradiol affects reproduction, sexual differentiation and aromatase gene expression of the medaka (Oryzias latipes). Aquat. Toxicol. 50: 367–373.

    Article  Google Scholar 

  • Schreck, C.B. 1974. Hormonal treatment and sex manipulation in fishes. In: Control of sex in fishes. pp. 84–106. Edited by C.B. Schreck. Virginia Polytechnic Institute and State University, Blacksburg.

    Google Scholar 

  • Schreibman, M.P., Berkowitz, E.J. and Van den Hurk, R. 1982. Histology and histochemistry of the testis and ovary of the platy-fish, Xiphophorus maculatus, from birth to sexual maturity. Cell Tissue Res. 224: 81–87.

    Article  CAS  Google Scholar 

  • Shimizu, M. and Takahashi, H. 1980. Process of sex differentiation of the gonad and gonoduct of the three-spined stickleback, Gasterosteus aculeatus L. Bull. Fac. Fish. Hokkaido Univ. 31: 137–148 (in Japanese).

    Google Scholar 

  • Shinomiya, A., Hamaguchi, S. and Shibata, N. 2001. Sexual differentiation of germ cell deficient gonads in the medaka, Oryzias latipes. J. Exp. Zool. 290: 402–410.

    Article  PubMed  CAS  Google Scholar 

  • Strüssmann, C.A., Karube, M., Miranda, L.A., Patiño, R., Somoza, G.M., Uchida, D. and Yamashita, M. 2002. Methods of sex control in fishes and an overview of novel hypotheses concerning the mechanisms of sex differentiation. In: Fish genetics and aquaculture biotechnology. In press. Edited by T.J. Pandian, C.A. Strüssmann and M.P. Marian. Oxford & IBH Publishing/Science Publishers, New Delhi, India/Enfield, USA.

    Google Scholar 

  • Strüssmann, C.A., Moriyama, S., Hanke, E.F., Calsina Cota, J.C. and Takashima, F. 1996b. Evidence of thermolabile sex determination in pejerrey. J. Fish Biol. 48: 643–651.

    Article  Google Scholar 

  • Strüssmann, C.A. and Patiño, R. 1995. Temperature manipulation of sex differentiation in fish. In: Proceedings of the Fifth International Symposium on the Reproductive Physiology of Fish. pp. 153–160. Edited by F.W. Goetz and P. Thomas. Fish Symp 95, Austin, Texas.

  • Strüssmann, C.A. and Patiño, R. 1999. Sex determination, environmental. In: Encyclopedia of reproduction. Vol. 4, pp. 402–409. Edited by E. Knobil and J.D. Neill. Academic Press.

  • Strüssmann, C.A.; Saito, T., Usui, M., Yamada, H. and Takashima, F. 1997. Thermal thresholds and critical period of thermolabile sex determination in two atherinid fishes, Odontesthes bonariensis and Patagonina hatcheri. J. Exp. Zool. 278: 167–177.

    Article  Google Scholar 

  • Strüssmann, A., Takashima, F. and Toda, K. 1996a. Sex differentiation and hormonal feminisation in pejerrey Odontesthes bonariensis. Aquaculture 139: 31–45.

    Article  Google Scholar 

  • Sumpter, J.P. 1997. Environmental control of fish reproduction: a different perspective. Fish Physiol. Biochem. 17: 25–31.

    Article  CAS  Google Scholar 

  • Takahashi, H. 1977. Juvenile hermaphroditism in the zebrafish, Brachydanio rerio. Bull. Fac. Fish. Hokkaido Univ. 28: 57–65.

    Google Scholar 

  • Takahashi, H. and Iwasaki, Y. 1973. The occurrence of histochemical activity of 3β-hydroxysteroid dehydrogenase in the developing testes of Poecilia reticulata. Dev. Growth Differ. 15: 241–253.

    Article  Google Scholar 

  • Takahashi, H. and Shimizu, M. 1983. Juvenile intersexuality in a cyprinid fish, the Sumatra barb, Barbus tetrazona tetraxona. Bull. Fac. Fish. Hokkaido Univ. 34: 69–78.

    Google Scholar 

  • Thorgaard, G.H. 1983. Chromosome set manipulation and sex control in fish. In: Fish Physiology, Vol. IX, Part B, Behavior and Fertility Control. pp. 405–434. Edited by W.S. Hoar, D.J. Randall and E.M. Donaldson. Academic Press, New York.

    Google Scholar 

  • Trant, J.M., Gavasso, S., Ackers, J., Chung, B.-C. and Place, A.R. 2001. Developmental expression of cytochrome P450 aromatase genes (CYP19a and CYP19b) in zebrafish fry (Danio rerio). J. Exp. Zool. 290: 475–483.

    Article  PubMed  CAS  Google Scholar 

  • Tuzuki, E., Egami, N. and Hyodo, Y. 1966. Multiplication and sex differentiation of germ cells during development in the medaka, Oryzias latipes. Japan. J. Ichthyol. 13: 176–182.

    Google Scholar 

  • Uchida, D., Yamashita, M., Kitano, T. and Iguchi, T. 2002. Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. J. Exp. Biol. 205: 711–718.

    PubMed  Google Scholar 

  • Van den Hurk, R. 1974. Steroidogenesis in the testis and gonadotropic activity in the pituitary during postnatal development of the black molly (Mollienesia latipinna). Proc. Kon. Ned. Akad. Wet. C77: 193–200.

    Google Scholar 

  • Van den Hurk, R., Lambert, J.G.D. and Peute, J. 1982. Steroidogenesis in the gonads of rainbow trout fry (Salmo gairdneri) before and after the onset of gonadal sex differentiaton. Reprod. Nutr. Dev. 22: 413–425.

    PubMed  CAS  Google Scholar 

  • Witschi, E. 1957. The inductor theory of sex differentiation. J. Fac. Hokkaido Univ. Ser. VI Zool. 13: 428–439.

    Google Scholar 

  • Yamamoto, T. 1953. Artificially induced sex reversal in genotypic males of the medaka (Oryzias latipes). J. Exp. Zool. 123: 571–594.

    Article  Google Scholar 

  • Yamamoto, T. 1969. Sex differentiation. In: Fish Physiology Vol. III, Reproduction and Growth, Bioluminescence, Pigments, and Poisons. pp. 117–175. Edited by W.S. Hoar and D.J. Randall. Academic Press, New York.

    Google Scholar 

  • Yamazaki, F. 1983. Sex control and manipulation of fish. Aquaculture 33: 329–354.

    Article  Google Scholar 

  • Yoshikawa, H. and Oguri, M. 1978. Gonadal sex differentiation in the medaka, Oryzias latipes, with special regard to the gradient of the differentiation of testes. Bull. Japan. Fish. Sci. Soc. 45: 1115–1121.

    Google Scholar 

  • Yoshizaki, G., Takeuchi, Y., Kobayashi, T., Ihara, S. and Takeuchi, T. 2002. Primordial germ cells: the blueprint for a piscine life. Fish Physiol. Biochem. 26: 3–12.

    Article  CAS  Google Scholar 

  • Zanuy, S., Carrillo, M., Felip, A., Rodríguez, L., Blázquez, M., Ramos, J. and Piferrer, F. 2001. Genetic, hormonal and environmental approaches for the control of reproduction in the European sea bass (Dicentrarchus labrax L.). Aquaculture 202: 187–203.

    Article  CAS  Google Scholar 

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Strüssmann, C.A., Nakamura, M. Morphology, endocrinology, and environmental modulation of gonadal sex differentiation in teleost fishes. Fish Physiology and Biochemistry 26, 13–29 (2002). https://doi.org/10.1023/A:1023343023556

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  • DOI: https://doi.org/10.1023/A:1023343023556

  • environment
  • fish
  • sex determination
  • sex differentiation
  • steroidogenesis