Skip to main content
SpringerLink
Log in

Gonadal development and sex determination in pulmonate molluscs

I. Arion circumscriptus

  • Published:
Zeitschrift für Zellforschung und Mikroskopische Anatomie Aims and scope Submit manuscript

Summary

A cytological study has been made, at the light- and electron-microscope levels, of gonadal development in Arion circumscriptus. The gonad appears to be ectodermal in origin and is composed of two cell lines—germinal and non-germinal. These two lineages are established in the embryo. The germinal line is first represented by primordial germ cells while the non-germinal line is first represented by auxiliary cells. The primordial germ cells differentiate into spermatogonia and oogonia, the auxiliary cells into Sertoli cells and follicular cells. Spermatogonia and oogonia differentiate about the time of hatching. All subsequent germ cells appear to differentiate from these initial populations of spermatogonia and oogonia. The concept of a germinal epithelium, as a cell layer in which germ cells differentiate from indeterminate germ cells throughout the life cycle, is not supported by this study.

A model for sex determination of the germ cells is proposed based on the hypothesis that sexually non-determined primordial germ cells are distributed into two physiologically isolated compartments (a male medullar compartment and a female cortical compartment). The spermatogonia and oogonia then differentiate in two different microenvironments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abdel-Malek, E. T.: Morphological studies on the family Planorbidae (Mollusca: Pulmonata). I. Genital organs of Helisoma trivolvis (Say) (Subfamily Helisomatinae F. C. Baker, 1945). Trans. Amer. micr. Soc. 73, 103–124 (1954).

    Google Scholar 

  • Ancel, P.: Histogenèse et structure de la glande hermaphrodite d'Helix pomatia. Arch. Biol. (Liège) 19, 389–652 (1903).

    Google Scholar 

  • Archie, V. E.: The histology and developmental history of the ovotestis of Lymnaea stagnalis. Thesis, University of Wisconsin 1942.

  • Armstrong, C. N., Marshall, A. J. (eds.): Intersexuality in vertebrates, including man, p. 479. New York: Academic Press 1964.

    Google Scholar 

  • Aubry, R.: La structure de l'acinus et la lignée femelle dans la glande hermaphrodite de Limnaea stagnalis adulte. C. R. Soc. Biol. (Paris) 148, 1498–1500 (1954a).

    Google Scholar 

  • Aubry, R.: Les éléments nourriciers dans la glande hermaphrodite de Limnaea stagnalis adulte. C. R. Soc. Biol. (Paris) 148, 1626–1629 (1954b).

    Google Scholar 

  • Aubry, R.: La lignée male dans la glande hermaphrodite de Limnaea stagnalis adulte. C. R. Soc. Biol. (Paris) 148, 1856–1858 (1954c).

    Google Scholar 

  • Aubry, R.: Sur le cycle d'élaboration sexuelle dans la glande hermaphrodite de Limnaea stagnalis adulte. C. R. Soc. Biol. (Paris) 148, 2075–2077 (1954d).

    Google Scholar 

  • Aubry, R.: Etude de l'hermaphrodisme et de l'action pharmacodynamique des hormones de vertébrés chez les gastéropodes pulmonés. Arch. Anat. micr. Morph. exp. 50 (Suppl.), 521–602 (1961).

    Google Scholar 

  • Bacci, G.: Sex determination, p. 293. New York: Pergamon Press 1965.

    Google Scholar 

  • Baker, J. R.: The structure and chemical composition of the Golgi element. Quart. J. micr. Sci. 85, 1–72 (1944).

    Google Scholar 

  • Bayne, C. J.: Observations on the composition of the layers of the egg of Agriolimax reticulatus, the grey field slug (Pulmonata, Stylommatophora). Comp. Biochem. Physiol. 19, 317–338 (1966).

    Google Scholar 

  • Berry, A. J., Chan, L. C.: Reproductive condition and tentacle extirpation in Malayan Achatina fulica (Pulmonata). Aust. J. Zool. 16, 849–855 (1968).

    Google Scholar 

  • Bounoure, L., Aubry, R.: La structure du canal hermaphrodite de Limnaea stagnalis et les possibilités de régénération germinale chez les gastéropodes pulmonés. C. R. Acad. Sci. (Paris) 243, 1453–1455 (1956).

    Google Scholar 

  • Bretschneider, L. H., Raven, C. P.: Structural and topochemical changes in the egg cells of Limnaea stagnalis L. during oogenesis. Arch. néerl. Zool. 10, 1–31 (1951).

    Google Scholar 

  • Brisson, P.: La castration chirurgicale chez Bulinus (contortus Michaud) truncatus (Audouin) (Mollusque Gastéropode Pulmoné). C. R. Acad. Sci. (Paris) 264, 131–133 (1967).

    Google Scholar 

  • Buresch, I.: Untersuchungen über die Zwitterdrüse der Pulmonaten. I. Die Differenzierung der Keimzellen bei Helix arbustorum. Arch. Zellforsch. 7, 314–343 (1912).

    Google Scholar 

  • Coggeshall, R. E.: A cytologic analysis of the bag cell control of egg laying in Aplysia. J. Morph. 132, 461–486 (1970).

    Google Scholar 

  • Demoll, R.: Die Spermatogenese von Helix pomatia L., ein Beitrag zur Kenntnis der Heterochromosomen. Zool. Jb. (Suppl. 15, (2)), 107–140 (1912).

  • DuPraw, E. J.: Cell and molecular biology, p. 739. New York: Academic Press 1968.

    Google Scholar 

  • Dym, M., Fawcett, D. W.: The blood testis barrier in the rat and the physiological compartmentalization of the seminiferous epithelium. Biol. Reprod. 3, 308–326 (1970).

    Google Scholar 

  • Eichardt, H.: Zur Kenntnis der cytologischen Vorgänge an den Geschlechtszellen von Arianta arbustorum während ihrer Reifungs- und Reifephase, unter besonderer Berücksichtigung des jahreszeitlichen Rhythmus. Z. Zellforsch. 35, 110–146 (1950).

    Google Scholar 

  • Fawcett, D. W., Leak, L. V., Heidger, P. M., Jr.: Electron microscopic observations on the structural components of the blood-testis barrier. J. Reprod. Fertil., Suppl. 10, 105–122 (1970).

    Google Scholar 

  • Franc, A.: Sous-classe des pulmonés. In: Traité de zoologie (P.-P. Grassé, ed.), tome V, frasc. III, p. 325–607. Paris: Masson & Cie. 1968.

    Google Scholar 

  • Fraser, L. A.: The embryology of the reproductive tract of Limnaea stagnalis appressa Say. Trans. Amer. micr. Soc. 65, 279–298 (1946).

    Google Scholar 

  • Gatenby, J. B.: The cytoplasmic inclusions of the germ cells. Part II. Helix aspersa. Quart. J. micr. Sci. 62, 556–611 (1917).

    Google Scholar 

  • Gatenby, J. B.: The cytoplasmic inclusions of the germ cells. Part III. The spermatogenesis of some other pulmonates. Quart. J. micr. Sci. 63, 197–258 (1918).

    Google Scholar 

  • Gatenby, J. B.: The cytoplasmic inclusions of the germ cells. Part IV. Notes on the dimorphic spermatozoa of Paludina and the giant germ-nurse cells of Testacella and Helix. Quart. J. micr. Sci. 63, 401–444 (1919a).

    Google Scholar 

  • Gatenby, J. B.: The cytoplasmic inclusions of the germ cells. Part V. The gametogenesis and early development of Limnaea stagnalis (L.), with special reference to the Golgi apparatus and the mitochondria. Quart. J. micr. Sci. 63, 445–492 (1919b).

    Google Scholar 

  • Goddard, C. K.: A study of the reproductive tract of Helix aspersa Muller after partial gonadectomy. Aust. J. biol. Sci. 13, 378–386 (1960).

    Google Scholar 

  • Gottfried, H., Dorfman, R. I.: Steroids of invertebrates. IV. On the optic tentacle-gonadal axis in the control of the male-phase ovotestis in the slug (Ariolimax californicus). Gen. comp. Endocr. 15, 101–119 (1970a).

    Google Scholar 

  • Gottfried, H., Dorfman, R. I.: Steroids of invertebrates. V. The in vitro biosynthesis of steroids by the male-phase ovotestis of the slug (Ariolimax californicus). Gen. comp. Endocr. 15, 120–138 (1970b).

    Google Scholar 

  • Gottfried, H., Dorfman, R. I.: Steroids of invertebrates. VI. Effect of tentacular homogenates in vitro upon post-androstenedione metabolism in the male phase of Ariolimax californicus ovotestis. Gen. comp. Endocr. 15, 139–142 (1970c).

    Google Scholar 

  • Greep, R. O.: Histology, p. 914. New York: McGraw-Hill Book Co. 1966.

    Google Scholar 

  • Guyard, A.: Aspects ultrastructuraux de la différenciation gonocytaire au début de l'organogénèse de la glande hermaphrodite d'Helix aspersa Müll. (Gasteropode Pulmoné). Bull. Soc. Zool. France 95, 471–474 (1970).

    Google Scholar 

  • Henderson, N. E., Pelluet, D.: The effect of visible light on the ovotestis of the slug Deroceras reticulatum (Muller). Canad. J. Zool. 38, 173–178 (1960).

    Google Scholar 

  • Hoffman, H.: Ueber die Entwicklung der Geschlechtsorgane bei Limax maximus. Z. wiss. Zool. 119, 493–536 (1922).

    Google Scholar 

  • Joosse, J., Boer, M. H., Cornelisse, C. J.: Gametogenesis and oviposition in Lymnaea stagnalis as influenced by γ-irradiation and hunger. Symp. Zool. Soc. Lond. 22, 213–235 (1968).

    Google Scholar 

  • Kugler, O. E.: A morphological and histochemical study of the reproductive system of the slug, Philomycus carolinianus (Bosc). J. Morph. 116, 117–132 (1965).

    Google Scholar 

  • Larambergue, M. de.: Étude de l'autofecondation chez les gastéropodes pulmonés. Recherches sur l'aphallie et la fecondation chez Bulinus (Isidora) contortus Michaud. Bull. Biol. France Belg. 73, 19–231 (1939).

    Google Scholar 

  • Laviolette, P.: Rôle de la gonade dans le déterminisme humarol de la maturité glandulaire du tractus génital chez quelques gastéropodes Arionidae et Limacidae. Bull. Biol. France Belg. 88, 310–332 (1954a).

    Google Scholar 

  • Laviolette, P.: Étude cytologique et expérimentale de la régénération germinale après castration chez Arion rufus L. (Gastéropode Pulmoné). Ann. Sci. Nat. Sci., Sér. 11, 16, 427–535 (1954b).

    Google Scholar 

  • Loomis, W. F.: Microenvironmental control of sexual differentiation in hydra. J. exp. Zool. 156, 289–306 (1964).

    Google Scholar 

  • Luchtel, D.: Cytology of gonadal development and gametogenesis in three species of pulmonate molluscs. p. 121. Ph. D. thesis. University of Washington 1969.

  • Luchtel, D.: Gonadal development and sex determination in pulmonate molluscs. II. Arion ater rufus and Deroceras reticulatum. Z. Zellforsch. 130, 302–311 (1972).

    Google Scholar 

  • Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).

    Google Scholar 

  • Lusis, O.: Post-embryonic changes in the reproductive system of the slug Arion ater rujus. Proc. Zool. Soc. Lond. 137, 433–468 (1961).

    Google Scholar 

  • Lusis, O.: Changes induced in the reproductive system of Arion ater rufus L. by varying environmental conditions. Proc. Malac. Soc. Lond. 37, 19–26 (1966).

    Google Scholar 

  • Martoja, M.: Devéloppement de l'appareil reproducteur chez les Gastéropodes Pulmonés. Ann. Biol. 3, 199–232 (1964).

    Google Scholar 

  • Masetti-Zannini, A.: Determinazione citosessuale e gametogenesis in Helix cincta. Bol. Zool. 26, 405–411 (1959).

    Google Scholar 

  • Masetti-Zannini, A.: La successione dei fenomeni di differenziamento citosessuala nella gonade giovanile di Helix cincta. Caryologia 13, 285–296 (1960).

    Google Scholar 

  • Merton, H.: Die Wanderungen der Geschlechtszellen in der Zwitterdrüse von Planorbis. Z. Zellforsch. 10, 527–551 (1930).

    Google Scholar 

  • Millonig, G.: A modified procedure for lead staining of thin sections. J. biophys. biochem. Cytol. 11, 736–739 (1961).

    Google Scholar 

  • Mittwoch, U.: Sex chromosomes, p. 306. New York: Academic Press 1967.

    Google Scholar 

  • Mol, J. J. van: Neurosecretory phenomena in the slug Arion rufus (Gastropoda: Pulmonata). Gen. comp. Endocr. 2, 616–617 (1962).

    Google Scholar 

  • Ohno, S.: Sex chromosomes and sex-linked genes, vol. 1, monographs on endocrinology, p. 192. New York: Springer 1967.

    Google Scholar 

  • Pabst, H.: Entwicklung des Genitalapparats von Arion empricorum Fèr. Zool. Jb., Abt. Anat. u. Ontog. 38, 465–508 (1914).

    Google Scholar 

  • Pelluet, D.: On the hormonal control of cell differentiation in the ovotestis of slugs (Gastropoda: Pulmonata). Canad. J. Zool. 42, 195–199 (1964).

    Google Scholar 

  • Pelluet, D., Lane, N. J.: The relation between neurosecretion and cell differentiation in the ovotestis of slugs (Gastropoda: Pulmonata). Canad. J. Zool. 39, 789–805 (1961).

    Google Scholar 

  • Pennypacker, M. I.: The germ-cells in the hermaphroditic gland of Polygra appressa. J. Morph. 49, 415–453 (1930).

    Google Scholar 

  • Perrot, J. L.: Chromosomes et hétérochromosomes chez les gastéropodes pulmonés. Rev. suisse Zool. 37, 397–434 (1930).

    Google Scholar 

  • Quattrini, D., Lanza, B.: Richerche sulla biologia dei Veronicellidae (Gastropoda soleolifera). II. Struttura della gonade, ovogenesi e spermatogenesi in Vaginulus borellianus (Colosi) e in Laevicaulis alte (Ferussac). Mon. Zool. Ital. 43, 3–60 (1965).

    Google Scholar 

  • Ranzoli, F.: Osservazioni sulla spermatogenesi di Helix lucorum. Bol. Zool. Ital. 23, 565–571 (1956)

    Google Scholar 

  • Ranzoli, F.: Osservazioni sull' ovogenesi di Helix lucorum e sui rapporti fra gametogenesi maschile o femminile e cellule nutrici. Bol. Zool. Ital. 24, 1–8 (1957).

    Google Scholar 

  • Richardson, K. C., Jarett, L., Finke, E. H.: Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol. 35, 313–323 (1960).

    Google Scholar 

  • Richter, E.: Der Bau der Zwitterdrüsen und der Entstehung der Geschlechtszellen bei Agriolimax agrestris. Jena. Z. Wiss. 69, 507–544 (1935).

    Google Scholar 

  • Roosen-Runge, E. C., Leik, J.: Gonocyte degeneration in the postnatal male rat. Amer. J. Anat. 122, 275–299 (1968).

    Google Scholar 

  • Rose, M., Hamon, M.: Sur l'influence des hormones sexuelles de synthèse chez le mollusque gastéropode pulmoné Milax gagates Draparnaud. C. R. Soc. Biol. (Paris) 131, 937–939 (1939).

    Google Scholar 

  • Rouzaud, H.: Recherches sur le developpement des organes génitaux de quelques gastéropodes hermaphrodites. J. roy. micr. Soc., Ser. 2, 6, 221–222 (1886).

    Google Scholar 

  • Simpson, L., Bern, H. A., Nishioko, R. S.: Examination of the evidence for neurosecretion in the nervous system of Helisoma tenue (Gastropoda Pulmonata). Gen. comp. Endocr. 7, 525–548 (1966a).

    Google Scholar 

  • Simpson, L., Bern, H. A., Nishioka, R. S.: Survey of evidence for neurosecretion in gastropod molluscs. Amer. Zool. 6, 123–138 (1966b).

    Google Scholar 

  • Smith, B. J.: Maturation of the reproductive tract of Arion ater (Pulmonata: Arionidae). Malacologia 4, 325–349 (1966).

    Google Scholar 

  • Stephenson, J. W.: A culture method for slugs. Proc. Malac. Soc. Lond. 35, 43–45 (1962).

    Google Scholar 

  • Tardy, M. J.: Organogenèse de l'appareil génital chez les mollusques. Bull. Soc. Zool. France 95, 407–428 (1970).

    Google Scholar 

  • Ubbels, G. A.: A cytochemical study of oogenesis in the pond snail Limnaea stagnalis. Thesis. Rijksuniv., Utrecht 1968.

  • Watts, H. H.: Spermatogenesis in the slug Arion subfuscus. J. Morph. 91, 53–77 (1952).

    Google Scholar 

  • Wautier, J., Hernandez, M.-L., Richardot, M.: Anatomie, histologie, et cycle vital de Gundlachia wautieri (Mirolli) Mollusque Basommatophore). Ann. Sci. Nat., Zool., Paris 8, 495–566 (1966).

    Google Scholar 

  • Weakley, B. S.: Electron microscopy of the oocyte and granulosa cells in the developing ovarian follicles of the golden hamster (Mesocricetus auratus). J. Anat. (Lond.) 100, 503–534 (1966).

    Google Scholar 

  • Weakley, B. S.: Light and electron microscopy of developing germ cells and follicle cells in the ovary of the golden hamster: twenty-four hours before birth to eight days post partum. J. Anat. (Lond.) 101, 435–459 (1967).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, University of Washington, Seattle, Washington, USA

    Daniel Luchtel

Authors
  1. Daniel Luchtel
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Supported in part by NSF Traineeship Grant GZ-198.1 and NIH Developmental Biology Training Grant, No. 5-T01-HD00266-01.

The author extends his thanks to Professors Alan J. Kohn, Edward C. Roosen-Runge, and W. Siang Hsu for their advice, suggestions, and encouragement.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Luchtel, D. Gonadal development and sex determination in pulmonate molluscs. Z.Zellforsch 130, 279–301 (1972). https://doi.org/10.1007/BF00306943

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00306943

Key words

Search

Navigation