Environmental Biology of Fishes

, Volume 38, Issue 1–3, pp 175–185 | Cite as

Ovarian steroid synthesis and the hormonal control of the elasmobranch reproductive tract

  • Ian P. Callard
  • Lisa A. Fileti
  • Thomas J. Koob


The reproductive biology of the chondricthyan fishes is remarkably sophisticated. Using both oviparous and viviparous reproductive modes, the group has generally adapted the style of bringing forth relatively few young at one time, each representing the investment of a great deal of maternal energy. The oviparous species foreshadow the situation common in oviparous reptiles and universal in birds. On the other hand, viviparous species range from simple internal incubators, in which large yolked eggs are retained, to other species in which the complexity of placentation and yolk reduction approach the eutherian condition. Further, in certain viviparous elasmobranchs the phenomenon of histotrophic nutrition attains an importance and complexity not seen in any other vertebrate group including mammals. Internal fertilization and amniote patterns of reproductive tract development also operate in virtually all elasmobranchs. The summary of work presented here suggests that these female reproductive styles are associated with a reproductive endocrinology which is the archetype for amniote vertebrates.

Key words

Oviparity Viviparity Yolk Placentation Amniote Endocrinology 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References cited

  1. Bedarkar, S., T. Blundell, L. Gowan, K. McDonald & C. Schwabe.1982. On the three-dimensional structure of relaxin. pp. 22–33. In: B. Steinetz, C. Schwabe & G. Weiss (ed.) Relaxin: Structure, Function and Evolution, Ann. N.Y Acad. Sci. 380.Google Scholar
  2. Bullesbach, E.E., L.K. Gowan, C. Schwabe, B.G. Steinetz, E. O"Bryne & I.P. Callard. 1986. Isolation, purification, and the sequence of relaxin from the spiny dogfish (Squalus acanthias). Eur. J. Biochem. 161: 335–341.Google Scholar
  3. Bullesbach, E.E., C. Schwabe & I.P. Callard. 1987. Relaxin from an oviparous species, the skate (Raja erinacea). Biochem. Biophys. Res. Commun. 143: 273–280.Google Scholar
  4. Callard, G.V. & P. Mak. 1985. Exclusive nuclear location of estrogen receptors in Squalus testis. Proc. Natl. Acad. Sci. U.S.A. 82: 1336–1340.Google Scholar
  5. Callard, I.P., G.V. Callard & V. Lance. 1979. Lower vertebrate animal models in reproduction research. pp. 346–359. In: N.J. Alexander (ed.) Animal Models for Research on Contraception and Fertility, Harper and Row, New York.Google Scholar
  6. Callard, I.P. & L. Klosterman. 1987. Reproductive physiology. pp. 277–291. In: T. Shuttleworth (ed.) The Physiology of Elasmobranchs Fishes, Springer-Verlag, Berlin.Google Scholar
  7. Callard, I.P., L.L. Klosterman, L.A. Sorbera, L.A. Fileti & J.C. Reese. 1989. Endocrine regulation of reproduction in elasmobranchs: archetype for terrestrial vertebrates. J. Exp. Zool. Suppl. 2: 12–22.Google Scholar
  8. Callard, I.P. & T.J. Koob.1982. Relaxin: speculations on its physiologic importance in some non-mammalian species. pp. 163–173. In: B. Steinetz, C. Schwabe & G. Weiss (ed.) Relaxin: Structure, Function and Evolution, Ann. N.Y. Acad. Sci. 380.Google Scholar
  9. Chieffi, G. 1961. La luteogenesi nei Selacei ovovivipari. Ricerche istologiche e istochimiche in Torpedo marmorata e Torpedo ocellata. Publ. Staz. Zool. Napoli 32: 145–166.Google Scholar
  10. Cox, D.L. & T.J. Koob. 1990. Latent egg capsule catechol oxidase in the little skate (Raja erinacea). Comp. Biochem. Physiol. 95B: 767–771.Google Scholar
  11. Dodd, J.M. & C.K. Goddard. 1961. Some effects of oestradiol benzoate on the reproductive ducts of the female dogfish Scyliorhinus caniculus. Proc. Zool. Soc. London 137: 325–331.Google Scholar
  12. Dodd, J.M. & P.J. Sumpter. 1984. Fishes. pp. 1–126. In: G.E. Lamming (ed.) Marshall"s Physiology of Reproduction, 4th Edition, Churchill Livingston, Edinburgh.Google Scholar
  13. Fileti, L.A. 1993. Regulation of ovarian steroidogenesis in the little skate, Raja erinacea. Ph.D. Thesis, Boston University, Boston. (in press).Google Scholar
  14. Fileti, L.A. & I.P. Callard. 1988. Corpus luteum function and regulation in the skate, Raja erinacea. The Bulletin, Mt.Desert Isl. Biol. Lab. 27: 37–39.Google Scholar
  15. Fileti, L.A. & I.P. Callard. 1990. Regulation of in vitro ovarian steroidogenesis in the little skate, Raja erinacea. The Bulletin, Mt. Desert Isl. Biol. Lab. 29: 129–130.Google Scholar
  16. Gilmore, R.G., J.W. Dodrill & P.A. Linley. 1983. Reproduction and embryonic development of the sand tiger shark, Odontaspis taurus (Rafinesque). U.S. Fish. Bull. 81: 201–225.Google Scholar
  17. Hamlett, W.C. 1987. Comparative morphology of the elasmobranch placental barrier. Arch. Biol. 98: 135–162.Google Scholar
  18. Hamlett, W.C. 1989. Evolution and morphogenesis of the placenta in sharks. J. Exp. Zool. Suppl. 2: 35–52.Google Scholar
  19. Hamlett, W.C. & J.P. Wourms. 1984. Ultrastructure of the preimplantation shark yolk sac placenta. Tissue Cell 16: 613–625.Google Scholar
  20. Hamlett, W.C., J.P. Wourms & J.W. Smith. 1985. Stingray placental analogues: structure of trophonemata in Rhinoptera bonasus. J. Submicrosc. Cytol. 17: 541–550.Google Scholar
  21. Harkness, M.L.R. & R.D. Harkness. 1959. Changes in the physical properties of the uterine cervix of the rat during pregnancy. J. Physiol. 148: 524–547.Google Scholar
  22. Hisaw, L. & A. Abramowitz. 1939. Physiology of reproduction in the dogfishes Mustelus canis and Squalus acanthias. Rep. Woods Hole Oceanor. Inst. 1938: 22.Google Scholar
  23. Koob, T.J. & I.P. Callard. 1991. Reproduction in female elasmobranchs. pp. 155–210.In: R. Kinne (ed.) Comparative Physiology. vol. 4, Oocytes and Reproduction, Karger, New York.Google Scholar
  24. Koob, T.J., J.J. Laffan, B. Elger & I.P. Callard. 1983. Effects of estradiol on the Verschlussvorrichtung of Squalus acanthias. The Bulletin, Mt. Desert Isl. Biol. Lab. 23: 67–68.Google Scholar
  25. Koob, T.J., J.J. Laffan & I.P. Callard. 1984. Effects of relaxin and insulin on reproductive tract size and early fetal loss in Squalus acanthias. Biol. Reprod. 31: 231–238.Google Scholar
  26. Koob, T.J., P. Tsang & I.P. Callard. 1986. Plasma estradiol, testosterone and progesterone levels during the ovulatory cycle of the skate (Raja erinacea). Biol. Reprod. 35: 267–275.Google Scholar
  27. Koob, T.J. & D.L. Cox. 1988. Egg capsule catechol oxidase from the little skate Raja erinacea Mitchill,1825. Biol. Bull. Woods Hole 175: 202–211.Google Scholar
  28. Koob, T.J. & D.L. Cox, 1993. Introduction and oxidation of catechols during the formation of the skate (Raha erinacea) egg capsule. J. Mar. Biol. Ass. U.K. 70 (in press).Google Scholar
  29. Metten H. 1939. Studies on the reproduction of the dogfish. Phil. Trans. Royal Soc. London 230: 217–238.Google Scholar
  30. Olefsky, J., M. Saekow & R.L. Kroc.1982. Potentiation of insulin binding and insulin action by purified relaxin. pp. 200–216. In: B. Steinetz, C. Schwabe & B. Weiss (ed.) Relaxin: Structure, Function and Evolution, Ann. N.Y. Acad. Sci. 380.Google Scholar
  31. Reese J.C. & I.P. Callard. 1991. Characterization of a specific estrogen receptor in the oviduct of the little skate, Raja erinacea. Gen. Comp. Endocrinol. 84: 170–181.Google Scholar
  32. Reinig, J.W., L.N. Daniel, C. Schwabe, L.K. Gowan, B.G. Steinetz & E. O"Bryne. 1981. Isolation and characterization of relaxin from the sand tiger shark (Odontaspis taurus). Endocrinology 109: 537–543.Google Scholar
  33. Rusaouen, M. 1976. The dogfish shell gland, a histochemical study. J. Exp. Mar. Biol. Ecol. 23: 267–283.Google Scholar
  34. Rusaouen, M. 1978. Etude ultrastructurale des zones á sécréetions protéiques et glycoprotdiques de la glande nidamentaire de la rousette á maturité. Arch. Anat. Microscp. 67: 107–119.Google Scholar
  35. Rusaouen, M., J.-P. Pujol, J. Jocquet, A. Veillard & J.-P. Borel. 1976. Evidence of collagen in the egg capsule of the dogfish, Scyliorhinus canicula. Comp. Biochem. Physiol. 53B: 539–543.Google Scholar
  36. Sorbera, L.A., C. Schwabe & I.P. Callard. 1986. The effect of homologous relaxin and neurointermediate lobe extracts on in vivo and in vitro myometrial activity in the viviparous dogfish, Squalus acanthias. The Bulletin, Mt. Desert Isl. Biol. Lab. 26: 133–135.Google Scholar
  37. Tsang, P. & I.P. Callard. 1987a. Morphological and endocrine correlates of the reproductive cycle of the aplacental viviparous dogfish, Squalus acanthias. Gen. Comp. Endocrinol. 66: 182–189.Google Scholar
  38. Tsang, P. & I.P. Callard. 1987b. Luteal progesterone and regulation in the viviparous dogfish, Squalus acanthias. J. Exp. Zool. 241: 377–382.Google Scholar
  39. Tsang, P. & I.P. Callard. 1992. Regulation of in vitro ovarian steroidogenesis in the viviparous dogfish,Squalus acanthias. J. Exp. Zool. 261: 97–104.Google Scholar
  40. Wourms, J.P. 1977. Reproduction and development in chondrichthyan fishes. Amer. Zool. 17. 379–410.Google Scholar
  41. Wourms, J.P. 1981. Viviparity: the maternal-fetal relationships of fishes. Amer. Zool. 21: 473–515.Google Scholar
  42. Wourms, J.P, B.V. Grove & J.H. Lombardi.1988. The maternal-embryonic relationship in viviparous fishes. pp. 1–134. In: W.S. Hoar & D.J. Randall (ed.) Fish Physiology, Vol. 11b, Academic Press, San Diego.Google Scholar

Copyright information

© Kluwer Academic Publishers 1993

Authors and Affiliations

  • Ian P. Callard
    • 1
  • Lisa A. Fileti
    • 1
  • Thomas J. Koob
    • 2
    • 3
  1. 1.Department of BiologyBoston UniversityBostonU.S.A.
  2. 2.Department of BiologyUniversity of New MexicoAlbuquerqueU.S.A.
  3. 3.Mount Desert Island Biological LaboratorySalsbury CoveU.S.A.

Personalised recommendations