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Viviparity and the maternal-embryonic relationship in the coelacanth Latimeria chalumnae

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The biology of Latimeria chalumnae and evolution of coelacanths

Part of the book series: Developments in environmental biology of fishes ((DEBF,volume 12))

Abstract

Embryos of Latimeria chalumnae develop in well-vascularized compartments in the uterine region of the right oviduct. Compartments conform to the shape of their embryos and yolksacs; they represent a stable, gestation-induced oviductal modification. Late-term pups possess large, flaccid, vascular yolksacs almost devoid of yolk. The sac is in close contact with, but does not adhere to, the lumenal uterine surface. A massive vascular plexus occurs in the wall of the compartment at the site of contact with the yolksac ; together they constitute a non-adherent, transposable placenta. The exterior surface of the yolksac is bounded by an attenuated, single-layered, squamous epithelium that surrounds an intercommunicating bed of cortical sinuses. The cortex of the sac is composed mostly of connective tissue stroma. The inner surface is bounded by a layer of yolk-digesting merocytes. Residual yolk occurs as yolk platelets that include yolk crystals. The interior surface of the sac is invested by an uniquely specialized vitelline circulation; no connection seems to exist between the interior of the yolksac and gut. The uterine wall consists of : (1) a lumenal surface composed of an anastomosing network of capillaries with a layer of attenuated, very thin, squamous epithelium, (2) a well-vascularized connective tissue stroma, (3) alternating transverse and longitudinal layers of smooth muscle, also well-vascularized, and (4) an external epithelial layer. Comparison of egg dry weight (184 g) with the estimated dry weights of a late-term pup (171 to 239 g) and a neonate (200 to 280 g) reveals a weight change of − 7 to + 30% and + 9 to + 52%, respectively. This is indicative of matrotrophy. In one female specimen, 19 remarkably large ovulated eggs were found and in another about 30 somewhat smaller ovarian ones. These are many more than ever could be accommodated in the uterine space. During the early and middle phases of development, embryos must be lecithotrophic, using their yolk reserves, with oophagy of fragmented supernumerary eggs as the most probable source of additional nutrients. The well-developed embryonic gut contains brown, amorphous yolk-like material. The limited amount of metachromatic secretory product of the uterine glands can play little or no role in embryonic nutrition.

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References cited

  • Amoroso, E.C. 1981. Viviparity. pp. 3–25. In: S.R. Glasser & D.W. Bullock (ed.) Cellular and Molecular Aspects of Implantation, Plenum Press, News York.

    Chapter  Google Scholar 

  • Anthony, J. & J. Millot. 1972. Première capture d’une femelle de coelacanthe en état de maturité sexuelle. C.R. Acad. Sc. Paris Sér. D 274: 1925–1926.

    Google Scholar 

  • Anthony, J. & D. Robineau. 1976. Sur quelques caractères juvéniles de Latimeria chalumnae Smith (Pisces, Crossopterygii, Coelacanthidae). C.R. Acad. Sc. Paris Sér. D 283: 1739–1742.

    Google Scholar 

  • Atz, J.W. 1976. Latimeria babies are born, not hatched. Underwater Naturalist 9(4): 4–7.

    Google Scholar 

  • Balon, E.K. 1984. Patterns in the evolution of reproductive styles in fishes. pp. 35–53. In: G.W. Potts & R.J. Wootton (ed.) Fish Reproduction: Strategies and Tactics, Academic Press, London.

    Google Scholar 

  • Balon, E.K. 1985. The theory of saltatory ontogeny and life history models revisited. pp. 13–30. In: E.K. Balon (ed.) Early Life History of Fishes: New Developmental, Ecological and Evolutionary Perspectives, Developments in Env. Biol. Fish. 5, Dr W. Junk Publishers, Dordrecht.

    Chapter  Google Scholar 

  • Balon, E.K. 1986. Types of feeding in the ontogeny of fishes and the life-history model. Env. Biol. Fish. 16: 11–24.

    Article  Google Scholar 

  • Balon, E.K. 1991. Probable evolution of the coelacanth’s reproductive style: lecithotrophy and orally feeding embryos in cichlid fishes and in Latimeria chalumnae. Env. Biol. Fish. 32: 249–265. (this volume)

    Article  Google Scholar 

  • Balon, E.K., M.N. Bruton & H. Fricke. 1988. A fiftieth anniversary reflection on the living coelacanth, Latimeria chalumnae: some new interpretations of its natural history and conservation status. Env. Biol. Fish. 23: 241–280.

    Article  Google Scholar 

  • Bemis, W.E. & R.G. Northcutt. 1991. Innervation of the basicranial muscle of Latimeria chalumnae. Env. Biol. Fish. 32: 147–158. (this volume)

    Article  Google Scholar 

  • Compagno, L.J.V. 1984. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. FAO Fish. Synop. No. 125 (4, Pt. 1) viii+ 249.

    Google Scholar 

  • Devys, M., A. Thierry, M. Barbier & M.M. Janot. 1972. Premières observations sur les lipides de l’ovocyte du coelacanthe (Latimeria chalumnae). C.R. Acad. Sc. Paris Sér. D 275: 2085–2087.

    CAS  Google Scholar 

  • Fricke, H., O. Reinicke, H. Hofer & W. Nachtigall. 1987. Locomotion of the coelacanth Latimeria chalumnae in its natural environment. Nature 329: 331–333.

    Article  Google Scholar 

  • Fritzsch, B. 1987. Inner ear of the coelacanth fish Latimeria has tetrapod affinities. Nature 327: 153–154.

    Article  PubMed  CAS  Google Scholar 

  • Gilbert, P.W. & D.A. Schlernitzauer. 1966. The placenta and gravid uterus of Carcharhinus falciformis. Copeia 1966: 451–457.

    Article  Google Scholar 

  • Grodziñski, Z. 1972. The yolk of Latimeria chalumnae Smith. Folia histochem. cytochem. 10: 11–18.

    Google Scholar 

  • Hamlett, W.C., J.P. Wourms & J.W. Smith. 1985. Sting-ray placental analogue: structure of the trophonemata in Rhinoptera bonasus. J. submicrosc. Cytol. 17: 31–40.

    PubMed  CAS  Google Scholar 

  • Hensel, K. 1986. Morphologie et interprétation des canaux et canalicules sensoriels céphaliques de Latimeria chalumnae Smith, 1939 (Osteichthyes, Crossopterygii, Coelacanthiformes). Bull. Mus. natn. Hist. nat. Paris Sér. 4, 8: 379–407.

    Google Scholar 

  • Hoar, W.S. 1969. Reproduction. pp. 1–72. In: W.S. Hoar & DJ. Randall (ed.) Fish Physiology, Volume 3, Academic Press, New York.

    Google Scholar 

  • Jollie, W.P. & L.G. Jollie. 1967. Electron microscopic observations on accommodations to pregnancy in the uterus of the spiny dogfish, Squalus acanthias. J. Ultrastruct. Res. 20: 161–178.

    Article  PubMed  CAS  Google Scholar 

  • Kessel, R.G. & R.H. Kardon. 1979. Tissues and organs. W.H. Freeman and Co., San Francisco. 317 pp.

    Google Scholar 

  • Knight, F.M., J. Lombardi, J.P. Wourms & J.R. Burns. 1985. Follicular placenta and embryonic growth of the viviparous four-eyed fish (Anableps). J. Morph. 185: 131–142.

    Article  Google Scholar 

  • Lange, R.H. 1983. Les cristaux de lipovitelline-phosvitine dans l’ovocyte de Latimeria chalumnae Smith 1939 (Coelacanthidae, Pisces). Étude comparative. C.R. Acad. Sc. Paris Sér. III 297: 393–396.

    Google Scholar 

  • Locket, N.A. 1976. A future for the coelacanth? New Scientist 70: 456–458.

    Google Scholar 

  • Locket, N.A. 1980. Some advances in coelacanth biology. Proc. R. Soc. Lond. B208: 265–307.

    Article  PubMed  CAS  Google Scholar 

  • McAllister, D.E. & C.L. Smith. 1978. Mensurations morphologiques, dénombrements méristiques et taxonomie du coelacanth, Latimeria chalumnae. Naturaliste can. 105: 63–76.

    Google Scholar 

  • McCosker, J.E. & M.D. Lagios (ed.) 1979. The biology and physiology of the living coelacanth. Occ. Pap. Calif. Acad. Sci. 134. 17

    Google Scholar 

  • Millot, J. & J. Anthony. 1974. Les oeufs du coelacanthe. Science et Nature 121: 3–4 (+ color cover photograph).

    Google Scholar 

  • Millot, J., J. Anthony & D. Robineau. 1978. Anatomie de Latimeria chalumnae, Vol. 3, Appareil digestif, appareil respiratoire, appareil urogénital, glandes endocrines, appareil circulatoire, téguments, écailles, conclusions générales. C.N.R.S., Paris. 198 pp.

    Google Scholar 

  • Mossman, H.W. 1937. Comparative morphogenesis of the fetal membranes and accessory uterine structures. Contrib. Embryol. Carnegie Inst. 26: 129–246.

    Google Scholar 

  • Mossman, H.W. 1987. Vertebrate fetal membranes. Rutgers University Press, New Brunswick. 383 pp.

    Google Scholar 

  • Myking, L.M. 1977. Old four legs: the living fossil. Sea Frontiers 23: 334–341.

    Google Scholar 

  • Needham, J. 1942. Biochemistry and morphogenesis. Cambridge University Press, London. 785 pp.

    Google Scholar 

  • Ranzi, S. 1932. The physio-morphological basis of embryonic development in sharks. (Le basi fisio-morfologische dello sviluppo embrionale dei selaci.) Parti I. Pubbl. St. Zool. Napoli 13: 209–290. (In Italian).

    Google Scholar 

  • Ranzi, S. 1934. The physio-morphological basis of embryonic development in sharks. i(Le basi fisio-morfologische dello sviluppo embrionale dei selaci.) Parti II, III. Pubbl. St. Zool. Napoli 13: 331–437. (In Italian).

    Google Scholar 

  • Schultze, H.-P. 1980. Eier legende und lebend gebärende Quastenflosser. Natur und Museum 110: 101–108. (English translation from the Department of Geology, Field Museum of Natural History, Chicago).

    Google Scholar 

  • Schultze, H.-P. 1985. Reproduction and spawning sites of Rhabdoderma (Pisces, Osteichthyes, Actinistia) in Pennsylvanian deposits of Illinois, USA. Neuvième Congr. Internat. Stratigr. Geol. Carbonifère, Washington, Compte Rendu 5: 326–330.

    Google Scholar 

  • Smith, C.L., C.S. Rand, B. Schaeffer & J.W. Atz. 1975. Latimeria, the living coelacanth, is ovoviviparous. Science 190: 1105–1106.

    Article  Google Scholar 

  • Suyehiro, Y., T. Uyeno & N. Suzuki. 1982. Coelacanth: dissecting a living fossil. Newton graphic Science Magazine 2(8): 82–93. (In Japanese).

    Google Scholar 

  • Suzuki, N., Y. Suyehiro & T. Hamada. 1985. Initial report of expeditions for coelacanth — Part I-Field studies in 1981 and 1983. Sci. Pap. Coll. Arts Sci. Univ. Tokyo 35: 37–79.

    Google Scholar 

  • Tanaka, S. 1989. Extant frilled sharks. Collecting and Breeding 51: 50, 61-63. (In Japanese).

    Google Scholar 

  • Watson, D.M.S. 1927. The reproduction of the coelacanth fish, Undina. Proc. Zool. Soc. Lond. 1927: 453–457.

    Google Scholar 

  • Wourms, J.P. 1977. Reproduction and development of chondrichthyan fishes. Amer. Zool. 17: 379–410.

    Google Scholar 

  • Wourms, J.P. 1981. Viviparity: the maternal-fetal relationship in fishes. Amer. Zool. 21: 473–515.

    Google Scholar 

  • Wourms, J.P. & A.B. Bodine. 1984. Structure and function of trophonemata, a placental analogue, during early gestation of the butterfly ray. p. 407. In: S. Seno & Y. Orada (ed.) International Cell Biology 1984, Academic Press, Orlando. (Abstract)

    Google Scholar 

  • Wourms, J.P. & D.M. Cohen. 1975. Trophotaeniae, embryonic adaptations in the viviparous ophidioid fish, Oligopus long-hursti: a study of museum specimens. J. Morph. 147: 385–401.

    Article  Google Scholar 

  • Wourms, J.P., B.D. Grove & J. Lombardi. 1988. The maternal-embryonic relationship in viviparous fishes. pp. 1–134. In: W.S. Hoar & D.J. Randall (ed.) Fish Physiology, Volume 11B, Academic Press, San Diego.

    Google Scholar 

  • Wourms, J.P., M.D. Stribling & J.W. Atz. 1980. Maternal fetal nutrient relationships in the coelacanth, Latimeria. Amer. Zool. 20: 962. (Abstract)

    Google Scholar 

  • Hecmstra, P.C. & L.J.V. Compagno. 1989. Uterine cannibalism and placental viviparity in the coelacanth? A skeptical view. S. Afr. J. Sci. 85: 485–486.

    Google Scholar 

  • Yano, K. 1989. Comments on the reproductive mode of the false cat shark Pseudotriakis microdon. Program and Abstracts. 69th Annual Meeting Amer. Soc. Ichthyol. Herpetol: 164.

    Google Scholar 

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Authors and Affiliations

  1. Department of Biological Sciences, Clemson University, Clemson, SC, 29634, USA

    John P. Wourms & M. Dean Stribling

  2. Department of Herpetology and Ichthyology, American Museum of Natural History, New York, NY, 10024, USA

    James W. Atz

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  1. John P. Wourms
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  2. James W. Atz
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  3. M. Dean Stribling
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John A. Musick Michael N. Bruton Eugene K. Balon

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Wourms, J.P., Atz, J.W., Stribling, M.D. (1991). Viviparity and the maternal-embryonic relationship in the coelacanth Latimeria chalumnae . In: Musick, J.A., Bruton, M.N., Balon, E.K. (eds) The biology of Latimeria chalumnae and evolution of coelacanths. Developments in environmental biology of fishes, vol 12. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-3194-0_15

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  • DOI: https://doi.org/10.1007/978-94-011-3194-0_15

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-0-7923-1289-5

  • Online ISBN: 978-94-011-3194-0

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