Synopsis
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.
Similar content being viewed by others
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.
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..
Bretschneider, L.H. & J.J. Duyvené de Wit. 1947. Sexual endocrinology of non-mammalian vertebrates. Elsevier, Amsterdam. 146 pp..
Brusle, S. 1983. Contribution to the sexuality of a hermaphroditic teleost, Serranus hepatus L. J. Fish Biol. 22: 283–292.
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.
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.
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. .
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..
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.
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.
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..
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.
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.
Dildine, G.C. 1936. Studies on teleostean reproduction. I. Embryonic hermaphroditism in Lebistes reticulatus. J. Morph. 60: 261–277.
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..
Dipper, F.A. & R.S.V. Pullin. 1979. Gonochorism and sex-inversion in British Labridae (Pisces). J. Zool. Lond. 187: 97–112.
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..
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..
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).
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.
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.
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.
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.
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.
Hourigan, T.F. & E.S. Reese. 1987. Mid-ocean isolation and the evolution of Hawaiian reef fishes. Trends Ecol. Evol. 2: 187–191.
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.
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.
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.
Karnovsky, M.J. 1965. A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J. Cell Biol. 27: 137.
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.
Mehl, J.A.P. 1973. Ecology, osmoregulation and reproductive biology of the white steenbras, Lithognathus lithognathus (Teleostei: Sparidae). Zool. Africana 8: 157–230.
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.
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.
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..
Policansky, D. 1982. Sex change in plants and animals. Ann. Rev. Ecol. Syst. 13: 471–495.
Reinboth, R. 1962. Morphologische und funktionelle Zweigeschlechtlichtkeit bei marinen Teleostiern (Serranidae, Sparidae, Centracanthidae, Labridae). Zool. Jahrb., Abt. Allg. Zool. Physiol. Tiere 69: 405–480.
Reinboth, R. 1970. Intersexuality in fishes. Mem. Soc. Endocrinol. 18: 516–543.
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.
Reinboth, R. 1975. In vitro studies on steroid metabolism of testicular tissue in ambisexual teleost fish. J. Steroid Biochem. 6: 341–344.
Reinboth, R. 1979. On steroidogenic pathways in ambisexual fishes. Proc. Indian Natl. Sci. Acad. B45: 421–428.
Reinboth, R. 1980. Can sex inversion be environmentally induced? Biol. Reprod. 22: 49–59.
Reinboth, R. 1982. The problem of sexual bipotentiality as exemplified by teteosts. Reprod. Nutr. Dev. 22: 39–403.
Robertson, D.R. 1972. Social control of sex reversal in a coral reef fish. Science 177: 1007–1009.
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.
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.
Ross, R.M. 1984a. Growth and sexual strategies in the fish Thalassoma duperrey(Labridae), a protogynous hermaphrodite. Env. Biol. Fish. 10: 253–259.
Ross, R.M. 1984b. Catheterization: a non-harmful method of sex identification for sexually monomorphic fishes. Prog. Fish Cult. 46: 151–152.
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.
Satoh, N. 1974. An ultrastructural study of sex differentiation in the teleost Oryzias latipes. J. Embryol. Exp. Morph. 32: 195–215.
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.
Shpigel, M. & L. Fishelson. 1986. Behavior and physiology of coexistence in two species of Dascyllus (Pomacentridae, Teleostei). Env. Biol. Fish. 17: 253–265.
Smith, C.L. 1965. The patterns of sexuality and the classification of serranid fishes. Amer. Mus. Novit. 2207: 1–20.
Stenger, A.H. 1959. A study of the structure and development of certain reproductive structures of Mugil cephalus. Zoologica 44: 53–70.
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.
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.
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.
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.
Thresher, R.E. 1984. Reproduction in reef fishes. T.F.H. Publications Inc., Neptune City. 399 pp.
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.
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.
Warner, R.R. 1975. The reproductive biology of the protogynous hermaphrodite Pimelometopon pulchrum (Pisces: Labridae). U.S. Fish. Bull. 73: 262–283.
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..
Warner, R.R. 1984. Mating behavior and hermaphroditism in coral reef fishes. Amer. Sci. 72: 128–136.
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.
Wilson, J.D., F.W. George & J.E. Griffin. 1981. The hormonal control of sexual development. Science 211: 1278–1284.
Yaron, Z. 1971. Observations on the granulosa cells of Acanthobrama terrea-sanctae and Tilapia nilotica (Teleostei). Gen. Comp. Endocrinol. 17: 247–252.
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.
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.
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.
Yoshikawa, H. & M. Oguri. 1978. Sex differentiation in a cichlid Tilapia zillii. Bull. Japan Soc. Sci. Fish. 44: 313–318.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00001282