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Histological and ultrastructural evidence for the role of gonadal steroid hormones in sex change in the protogynous wrasse Thalassoma duperrey

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The process of sex change in the protogynous wrasse, Thalassoma duperrey, was investigated through histological and ultrastructural observations on the gonads of females changing sex to male. Changes in plasma steroid levels concomitant with structural changes were measured by radioimmunoassay. The process of sex change from ovary to testis was divided into six stages on the basis of changes in the structure of the germinal and somatic elements. Ovaries of females were filled with vitellogenic oocytes during the breeding season, but contained no spermatogenic tissue (Stage 1). At the commencement of sex change (Stage 2), vitellogenic oocytes began to degenerate, and were ingested by macrophagous cells. This stage was accompanied by a rapid drop in plasma levels of estradiol-17β. Thereafter, previtellogenic oocytes (Stage 3) also began to degenerate, and aggregations of stromal tissue, and loose connective tissue were observed in the central region of the lamellae. Steroid producing cells (Leydig cells), developed at the border of this loose connective tissue. Presumed spermatogonia proliferated on the periphery of the lamellae, and Leydig cells increased in size and number (Stage 4). Spermatogonia formed cysts, and underwent spermatogenesis (Stage 5). Finally, sex change to male was considered complete, with the beginning of active spermatogenesis and spermiation (Stage 6). Plasma levels of testosterone remained low throughout the sex change, but a second androgen, 11-ketotestosterone increased gradually in parallel to the increased numbers of Leydig cells and spermatogonia. Preliminary in vitro incubation of gonads with salmon gonadotropin, revealed that sex-changed males had higher levels of 11-ketotestosterone production than did females, while females had higher levels of estradiol-17β production than did males. Production of both these steroids increased in a dose-related fashion with increasing doses of gonadotropin.

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References cited

  • Atz, J.W. 1964. Intersexuality in fishes. pp. 145–232. In: C.N. Armstrong & A.J. Marshall (ed.) Intersexuality in Vertebrates Including Man, Academic Press, London.

    Google Scholar 

  • Billard, R., B. Breton, A. Fostier, B. Jalabert & C. Weil. 1978. Endocrine control of the teleost reproductive cycle and its relation to external factors: salmonid and cyprinid models. pp. 37–48. In: P.T. Gaillard & H.H. Boer (ed) Comparative Endocrinology, Elsevier North Holland Biomedical Press, Amsterdam..

    Google Scholar 

  • Bretschneider, L.H. & J.J. Duyvené de Wit. 1947. Sexual endocrinology of non-mammalian vertebrates. Elsevier, Amsterdam. 146 pp..

    Google Scholar 

  • Brusle, S. 1983. Contribution to the sexuality of a hermaphroditic teleost, Serranus hepatus L. J. Fish Biol. 22: 283–292.

    Google Scholar 

  • Brusle, S. & J. Brusle. 1978. An ultrastructural study of early germ cells in Mugil auratus Risso (Teleostei: Mugilidae). Ann. Biol. Anim. Bioch. Biophys. 18: 1141–1153.

    Google Scholar 

  • Chan, S.T.H. & J.G. Phillips. 1967. The structure of the gonad during natural sex reversal in Monopterus albus. J. Zool. Lond. 153: 129–141.

    Google Scholar 

  • Chan, S.T.H., W.S. O & S.W.B. Hui. 1975. The gonadal and adenohypophysial functions of natural sex reversal. pp. 201–221. In: R. Reinboth (ed.) Intersexuality in the Animal Kingdom, Springer Verlag, New York. .

    Google Scholar 

  • Chan, S.T.H., T.B. Ng, W.S. O & S.W.B. Hui. 1977. Hormones and natural sex succession in Monopterus. pp. 101–120. In: B. Lofts & S.T.H. Chan (ed.) Biological Research in Southeast Asia, University of Hong Kong, Hong Kong..

    Google Scholar 

  • Chan, S.T.H., A. Wright & J.G. Phillips. 1967. The atretic structures in the gonads of the rice-field eel (Monopterus albus) during natural sex reveral. J. Zool. Lond. 151: 129–141.

    Google Scholar 

  • Chan, S.T.H. & W.S.B. Yeung. 1983. Sex control and sex reversal in fish under natural conditions. pp. 171–222. In: W.S. Hoar, D.J. Randall & E.M. Donaldson (ed.) Fish Physiology, Volume 9B, Academic Press, New York.

  • Charnov, E.L. 1982. The theory of sex allocation. Monogr. Pop. Biol. 18, Princeton Univ. Press, Princeton. 355 pp.

    Google Scholar 

  • Christensen, A.K. & S.W. Gillim. 1969. The correlation of fine structure and function in steroid-secreting cells with emphasis on those of the gonad. Part 2: Steroid secreting cell. pp. 415–490. In: K.W. McKerns (ed.) The Gonad, North-Holland Co., Amsterdam..

    Google Scholar 

  • Crim, L.W., R.E. Peter & R. Billard. 1981. Onset of gonadotropic hormone accumulation in the immature trout pituitary gland in response to estrogen or aromatizable androgen steroid hormones. Gen. Comp. Endocrinol. 44: 374–381.

    Google Scholar 

  • DeMartini, E.E. & R.K. Fountain 1981. Ovarian cycling frequency and batch fecundity in the queenfish, Seriphus politus: attributes representative of serial spawning fishes. U.S. Fish. Bull. 79: 547–560.

    Google Scholar 

  • Dildine, G.C. 1936. Studies on teleostean reproduction. I. Embryonic hermaphroditism in Lebistes reticulatus. J. Morph. 60: 261–277.

    Google Scholar 

  • Demski, L.S. 1987. Diversity in reproductive patterns and behavior in teleost fishes. pp. 1–27. In: D. Crews (ed.)Psychobiology of Reproductive Behavior: An Evolutionary Perspective, Prentice Hall, Inc. Englewood Cliffs..

    Google Scholar 

  • Dipper, F.A. & R.S.V. Pullin. 1979. Gonochorism and sex-inversion in British Labridae (Pisces). J. Zool. Lond. 187: 97–112.

    Google Scholar 

  • Dodd, J.M., P.A.C. Stuart-Kregor, J.P. Sumpter, L.W. Crim & R.E. Peter. 1978. Premature sexual maturation in the Atlantic salmon (Salmo salar). pp. 37–48. In: P.T. Gaillard & H.H. Boer (ed.) Comparative Endocrinology, Elsevier North Holland Biomedical Press, Amsterdam..

    Google Scholar 

  • Fishelson, L. 1975. Ecology and physiology of sex reversal in Anthias squamipinnis (Teleostei, Anthiidae). pp. 284–294. In: R. Reinboth (ed.) Intersexuality in the Animal Kingdom, Springer Verlag, New York..

    Google Scholar 

  • Flores, J.A., J.R. Burns & K.D. Kallman. 1985. Ultrastructural study of the primary spermatogonia and oogonia of the platyfish. Amer. Zool. 25: 97. (Abstract).

    Google Scholar 

  • Fostier, A., B. Jalabert, R. Billard, B. Breton & Y. Zohar. 1983. The gonadal steroids. pp. 227–372. In: W.S. Hoar, D.J. Randall & E.M. Donaldson (ed.) Fish Physiology, Volume 9A, Academic Press, New York.

    Google Scholar 

  • Fostier, A., R. Billard, B. Breton, M. Legendre & S. Marlot. 1981. Plasma 11-oxotestosterone and gonadotropin during the beginning of spermiation in rainbow trout (Salmo gairdneri L.). Gen. Comp. Endocrinol. 46: 428–434.

    Google Scholar 

  • Grier, H.J. 1988. Brown bodies in the gonads of the black sea bass, Centropristis striatus. In: D.R. Idler, L.W. Crim & J.M. Walsh (ed.) Proceedings of the 3rd International Symposium on Reproductive Physiology of Fish, St. Johns. (In press).

  • Gresik, E.W. 1973. Fine structural evidence for the presence of nerve terminals in the testis of the teleost, Oryzias latipes. Gen. Comp. Endocrinol. 21: 210–213.

    Google Scholar 

  • Hishida, T. & N. Kawamoto. 1970. Androgenic and male-inducing effects of 11-ketotestosterone on a teleost, the medaka (Orizias latipes). J. Exp. Zool. 173: 79–284.

    Google Scholar 

  • Hourigan, T.F. & C.D. Kelley. 1985. Histology of the gonads and observations on the social behavior of the Caribbean angelfish, Holacanthus tricolor. Mar. Biol. 88: 311–322.

    Google Scholar 

  • Hourigan, T.F. & E.S. Reese. 1987. Mid-ocean isolation and the evolution of Hawaiian reef fishes. Trends Ecol. Evol. 2: 187–191.

    Google Scholar 

  • Idler, D.R., R. Reinboth, J.M. Walsh & B. Truscott. 1973. A comparison of 11-hydroxytestosterone and 11-ketotestosterone in blood of ambisexual and gonochoristic teleosts. Gen. Comp. Endocrinol. 30: 517–521.

    Google Scholar 

  • Jones, G.P. 1980. Growth and reproduction in the protogynous hermaphrodite Pseudolabrus celidotus (Pisces: Labridae) in New Zealand. Copeia 1980: 660–675.

  • Kagawa, H., K. Takano & Y. Nagahama. 1981. Correlation of plasma estradiol-17β and progesterone levels with ultrastructure and histochemistry of ovarian follicles in the white-spotted char, Salvelinus leucomaenis. Cell Tissue Res. 218: 315–329.

    Google Scholar 

  • Kagawa, H., G. Young, S. Adachi & Y. Nagahama. 1982. Estradiol-17β production in amago salmon (Oncorhynchus rhodurus) ovarian follicles: role of the thecal and granulosa cells. Gen. Comp. Endocrinol. 47: 440–448.

    Google Scholar 

  • Karnovsky, M.J. 1965. A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J. Cell Biol. 27: 137.

    Google Scholar 

  • Liley, N.R. & N.E. Stacey. 1983. Hormones, pheromones and reproductive behavior in fish. pp. 1–63. In: W.S. Hoar, D.J. Randall & E.M. Donaldson (ed.) Fish Physiology, Volume 9B, Academic Press, New York.

  • MacLusky, N.J. & F. Naftolin. 1981. Sexual differentiation of the central nervous system. Science 211: 1294–1303.

    Google Scholar 

  • Mehl, J.A.P. 1973. Ecology, osmoregulation and reproductive biology of the white steenbras, Lithognathus lithognathus (Teleostei: Sparidae). Zool. Africana 8: 157–230.

    Google Scholar 

  • Moyer, J.T. & A. Nakazono. 1978. Population structure, reproductive behavior and protogynous hermaphroditism in the angelfish Centropyge interruptus at Miyake-jima, Japan. Jap. J. Ichthyol. 25: 25–39.

    Google Scholar 

  • Nagahama, Y. 1983. The functional morphology of teleost gonads. pp. 181–226. In: W.S. Hoar, D.J. Randall & E.M. Donaldson (ed.) Fish Physiology, Volume 9A, Academic Press, New York.

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

    Google Scholar 

  • Nakamura, M. 1978. Morphological and experimental studies on sex differentiation of the gonad in several teleost fishes. Ph.D. Dissertation, Hokkaido University. Hakodate. 115 pp.

  • Ozon, R. 1972. Androgens in fishes, amphibians, reptiles and birds. pp. 329–389. In: D.R. Idler (ed.)Steroids in Non-mammalian Vertebrates, Academic Press, New York..

    Google Scholar 

  • Policansky, D. 1982. Sex change in plants and animals. Ann. Rev. Ecol. Syst. 13: 471–495.

    Google Scholar 

  • Reinboth, R. 1962. Morphologische und funktionelle Zweigeschlechtlichtkeit bei marinen Teleostiern (Serranidae, Sparidae, Centracanthidae, Labridae). Zool. Jahrb., Abt. Allg. Zool. Physiol. Tiere 69: 405–480.

    Google Scholar 

  • Reinboth, R. 1970. Intersexuality in fishes. Mem. Soc. Endocrinol. 18: 516–543.

    Google Scholar 

  • Reinboth, R. 1973. Dualistic reproductive behavior in the protogynous wrasse Thalassoma bifasciatum and some observations on its day/night changeover. Helgoländer wiss. Meeresunters. 24: 174–191.

    Google Scholar 

  • Reinboth, R. 1975. In vitro studies on steroid metabolism of testicular tissue in ambisexual teleost fish. J. Steroid Biochem. 6: 341–344.

    Google Scholar 

  • Reinboth, R. 1979. On steroidogenic pathways in ambisexual fishes. Proc. Indian Natl. Sci. Acad. B45: 421–428.

    Google Scholar 

  • Reinboth, R. 1980. Can sex inversion be environmentally induced? Biol. Reprod. 22: 49–59.

    Google Scholar 

  • Reinboth, R. 1982. The problem of sexual bipotentiality as exemplified by teteosts. Reprod. Nutr. Dev. 22: 39–403.

    Google Scholar 

  • Robertson, D.R. 1972. Social control of sex reversal in a coral reef fish. Science 177: 1007–1009.

    Google Scholar 

  • Robertson, D.R. 1974. A study of the ethology and reproductive biology of the labrid fish, Labroides dimidiatus at Heron Is., Great Barrier Reef. Ph.D. Dissertation, University of Queensland, Brisbane. 295 pp.

  • Ross, R.M. 1981. Experimental evidence for stimulation and inhibition of sex change in the Hawaiian reef fish Thalassoma duperrey. Proc. 4th Internatl. Coral Reef Symp. 2: 571–577.

    Google Scholar 

  • Ross, R.M. 1982. Sex change in the endemic Hawaiian labrid Thalassoma duperrey: a behavioral and ecological analysis. Ph.D. Dissertation, University of Hawaii, Honolulu. 171 pp.

  • Ross, R.M. 1983. Annual, semilunar and diel reproductive rhythms in the Hawaiian labrid Thalassoma duperrey. Mar. Biol. 72: 311–318.

    Google Scholar 

  • Ross, R.M. 1984a. Growth and sexual strategies in the fish Thalassoma duperrey(Labridae), a protogynous hermaphrodite. Env. Biol. Fish. 10: 253–259.

    Google Scholar 

  • Ross, R.M. 1984b. Catheterization: a non-harmful method of sex identification for sexually monomorphic fishes. Prog. Fish Cult. 46: 151–152.

    Google Scholar 

  • Ross, R.M. 1984c. Anatomical changes associated with sex reversal in the fish Thalassoma duperrey. Copeia 1984: 245–248.

  • Ross, R.M., G.S. Losey & M. Diamond. 1983. Sex change in a coral reef fish: dependence of stimulation and inhibition on relative size. Science 221: 574–575.

    Google Scholar 

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

    Google Scholar 

  • Sadovy, Y. & D.Y. Shapiro. 1987. Criteria for the diagnosis of hermaphroditism in fishes. Copeia 1987: 136–156.

  • Schmidt, P.J. & D.R. Idler. 1962. Steroid hormones in the plasma of salmon at various stages of maturation. Gen. Comp. Endocrinol. 2: 204–214.

    Google Scholar 

  • Shpigel, M. & L. Fishelson. 1986. Behavior and physiology of coexistence in two species of Dascyllus (Pomacentridae, Teleostei). Env. Biol. Fish. 17: 253–265.

    Google Scholar 

  • Smith, C.L. 1965. The patterns of sexuality and the classification of serranid fishes. Amer. Mus. Novit. 2207: 1–20.

    Google Scholar 

  • Stenger, A.H. 1959. A study of the structure and development of certain reproductive structures of Mugil cephalus. Zoologica 44: 53–70.

    Google Scholar 

  • Stuart-Kregor, P.A.C., J.P. Sumpter & J.M. Dodd. 1981. The involvement of gonadotropin and sex steroids in the control of reproduction in the parr and adults of Atlantic salmon, Salmo salar. J. Fish Biol. 18: 59–72.

    Google Scholar 

  • Takahashi, H. 1975. Process of functional sex reversal of the gonad in the female guppy, Poecilia reticulatus treated with androgen before birth. Develop. Growth Differen. 17: 167–175.

    Google Scholar 

  • Tang, F., S.T.H. Chan & B. Lofts. 1974. Effect of steroid hormones on the process of natural sex reversal in the ricefield eel, Monopterus albus. Gen. Comp. Endocrinol. 24: 227–241.

    Google Scholar 

  • Tang, F., S.T.H. Chan & B. Lofts. 1975. A study on the 3β- and 17β-hydroxysteroid dehydrogenase activities in the gonads of Monopterus albus at various sexual phases during natural sex reversal. J. Zool. Lond. 175: 571–580.

    Google Scholar 

  • Thresher, R.E. 1984. Reproduction in reef fishes. T.F.H. Publications Inc., Neptune City. 399 pp.

    Google Scholar 

  • Tricas, T.C. 1986. Life history, foraging ecology and territorial behavior of the Hawaiian butterflyfish, Chaetodon multicinctus. Ph.D. Dissertation, University of Hawaii, Honolulu. 248 pp..

  • Ueda, H., A. Kambegawa & Y. Nagahama. 1985. Involvement of gonadotropin and steroid hormones in spermiation in the Amago salmon, Oncorhynchus rhodurus, and goldfish Carassius auratus. Gen. Comp. Endocrinol. 59: 24–30.

    Google Scholar 

  • Van den Hurk, R., J. Meek & J. Peute. 1974. Ultrastructural study of the testes of the black molly (Mollienisia latipinna). II. Sertoli cells and Leydig cells. Proc. Kon. Ned. Akad. Wetensch. Serie C, 77: 470–476.

    Google Scholar 

  • Warner, R.R. 1975. The reproductive biology of the protogynous hermaphrodite Pimelometopon pulchrum (Pisces: Labridae). U.S. Fish. Bull. 73: 262–283.

    Google Scholar 

  • Warner, R.R. 1978. The evolution of hermaphroditism and unisexuality in aquatic and terrestrial vertebrates. pp. 77–101. In: E.S. Reese & F. Lighter (ed.) Contrasts in Behavior, Wiley Interscience, New York..

    Google Scholar 

  • Warner, R.R. 1984. Mating behavior and hermaphroditism in coral reef fishes. Amer. Sci. 72: 128–136.

    Google Scholar 

  • Warner, R.R. & D.R. Robertson 1978. Sexual patterns of the labroid fishes of the western Caribbean: I. The wrasses (Labridae). Smithson. Contrib. Zool. 254: 1–27.

    Google Scholar 

  • Wilson, J.D., F.W. George & J.E. Griffin. 1981. The hormonal control of sexual development. Science 211: 1278–1284.

    Google Scholar 

  • Yaron, Z. 1971. Observations on the granulosa cells of Acanthobrama terrea-sanctae and Tilapia nilotica (Teleostei). Gen. Comp. Endocrinol. 17: 247–252.

    Google Scholar 

  • Yamamoto, T. 1969. Sex differentiation. pp. 117–175. In: W.S. Hoar & D.J. Randall (ed.) Fish Physiology, Volume 3A, Academic Press, New York.

  • Yamazaki, F. & E.M. Donaldson. 1969. Involvement of gonadotropin and steroid hormones in the spermiation of the goldfish (Carassius auratus). Gen. Comp. Endocrinol. 12: 491–497.

    Google Scholar 

  • Yeung, W.S.B., M.N. Adal, S.W.B. Hui & S.T.H. Chan. 1985. The ultrastructural and biosynthetic characteristics of steroidogenic cells in the gonad of Monopterus albus (Teleostei) during natural sex reversal. Cell Tissue Res. 239: 383–394.

    Google Scholar 

  • Yeung, W.S.B. & S.T.H. Chan. 1987. The plasma steroid profiles in the freshwater, sex-reversing teleost fish, Monopterus albus (Zuiew). Gen. Comp. Endocrinol. 65: 233–242.

    Google Scholar 

  • Yoshikawa, H. & M. Oguri. 1978. Sex differentiation in a cichlid Tilapia zillii. Bull. Japan Soc. Sci. Fish. 44: 313–318.

    Google Scholar 

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Nakamura, M., Hourigan, T.F., Yamauchi, K. et al. Histological and ultrastructural evidence for the role of gonadal steroid hormones in sex change in the protogynous wrasse Thalassoma duperrey . Environ Biol Fish 24, 117–136 (1989). https://doi.org/10.1007/BF00001282

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