Ontogeny of Amniote Fetal Membranes and Their Application to Phylogeny

  • W. Patrick Luckett
Part of the NATO Advanced Study Institutes Series book series (NSSB, volume 14)


The extraembryonic or fetal membranes of vertebrates play an important functional role in the nutrition, respiration, excretion, and protection of the embryo and fetus during prenatal life. They are auxiliary structures which develop in continuity with the tissues of the embryo proper, and both embryo and fetal membranes are derived from the same three basic germ layers (ectoderm, mesoderm, and endoderm). The fetal membranes are transitory structures which persist for only a relatively brief period during the ontogeny of the individual; nevertheless, their functional differentiation is essential for the normal development of the embryo during prenatal life. The functional life of the fetal membranes is terminated at the time of birth or hatching; they may become partially resorbed into the body of the newborn, or, more commonly, they become disrupted and degenerate.


Shell Membrane Somite Stage Yolk Mass Embryonic Mass Chorioallantoic Placenta 
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  1. Agassiz, L., 1857, Embryology of the turtle. Contrib. Nat. Hist. USA 2: 451–644.Google Scholar
  2. Amoroso, E.C., 1952, Placentation, in: “Marshall’s Physiology of Reproduction,” (A.S. Parkes, ed.), 3rd ed., Vol. II. pp. 127–311. Longmans, Green and Co., London.Google Scholar
  3. Amoroso, E.C.and Perry, J.S., 1975, The existence during gestation of an immunological buffer zone at the interface between maternal and foetal tissues. Phil. Trans. Roy. Soc., Ser. B. 271: 343–361.CrossRefGoogle Scholar
  4. Bauchot, R., 1965, La placentation chez les reptiles. Ann. Biol. 4: 547–575.Google Scholar
  5. Bellairs, R., 1971, Developmental Processes in Higher Vertebrates. Logos Press, London.Google Scholar
  6. Bertin, L., 1952, Oviparite, ovoviviparite, viviparite. Bull. Soc. Zool. Fr. 77: 84–88.Google Scholar
  7. Boyd, M.M., 1942, The oviduct, foetal membranes, and placentation in Hoplodactylus maculatus Gray. Proc. Zool. Soc. Lond., Ser. A. 112: 65–104.Google Scholar
  8. Boyden, E.A., 1924, An experimental study of the development of the avian cloaca, with special reference to a mechanical factor in the growth of the allantois. J. Exp. Zool. 40: 437–472.CrossRefGoogle Scholar
  9. Brambell, F.W.R., 1970, The transmission of passive immunity from mother to young. North-Holland, Amsterdam.Google Scholar
  10. Caldwell, W.H., 1887, The embryology of Monotremata and Mar- supialia. Phil. Trans. Roy. Soc., 178: 463–486.CrossRefGoogle Scholar
  11. Cate-Hoedemaker, N.J. ten., 1933, Beitrage zur Kenntnis der Plazentation bei Haien und Reptilien. Zeit. Zellforsch. 18: 299–345.CrossRefGoogle Scholar
  12. Dalcq, A., 1937, Les plans d’ebauches chez les Vertebres et la signification morphologique des annexes foetales. Ann. Soc. Roy. Zool. Belg., 68: 69–76.Google Scholar
  13. Dalcq, A., 1949, L’apport de l’embryologie causale au probleme de l’evolution. Portug. Acta Biol., Ser. A., 367–400.Google Scholar
  14. Dendy, A., 1899, Outlines of the development of the tuatara, Sphenodon. Quart. J. Micr. Sci., 42: 1–87.Google Scholar
  15. Dufaure, J.P. and Hubert, J., 1961, Table de developpement du lezard vivipare: Lacerta (Zootoca) vivipara Jacquin. Arch. Anat. Micr. Morph. Exp., 50: 309–327.Google Scholar
  16. Enders, A.C. and Enders, R.K., 1969, The placenta of the foureyed opossum (Philander opossum). Anat. Rec., 165: 431–450.PubMedCrossRefGoogle Scholar
  17. Farris, J.S., 1966, Estimation of conservatism of characters by constancy within biological populations. Evolution 20: 587–591.CrossRefGoogle Scholar
  18. Fisk, A. and Tribe, M., 1949, The development of the amnion and chorion of reptiles. Proc. Zool. Soc. Lond., 119: 83–114.Google Scholar
  19. Flynn, T.T., 1922, The phylogenetic significance of the marsupial allanto-placenta. Proc. Linn. Soc. NSW 47: 541–544.Google Scholar
  20. Flynn, T.T., 1923, The yolk-sac and allantoic placenta in Perameles. Quart. J. Micr. Sci., 67: 123–182.Google Scholar
  21. Flynn, T.T. and Hill, J.P., 1939, The development of the Monotremata. Part IV. Growth of the ovarian ovum, maturation, fertilisation, and early cleavage. Trans. Zool. Soc. Lond., 24: 445–623.CrossRefGoogle Scholar
  22. Flynn, T.T. and Hill, J.P., 1947, The development of the Monotremata. Part VI. The later stages of cleavage and the formation of the primary germ-layers. Trans. Zool. Soc. Lond., 26: 1–151.Google Scholar
  23. Giacomini, E., 1891, Materiaux pour l’etude du developpement Seps chalcides. Arch. Ital. Biol., 16: 332–359.Google Scholar
  24. Gingerich, P.D., 1974, Cranial anatomy and evolution of early Tertiary Plesiadapidae (Mammalia, Primates). Unpublished Ph.D. Thesis, Yale Univ.Google Scholar
  25. Glenister, T.W., 1954, The emperor penguin Aptenodytes forsteri Gray. II. Embryology. Falkland Islands Dependencies Survey, Sci. Repts., 10: 1–19.Google Scholar
  26. Goin, C.J., 1960, Amphibians, pioneers of terrestrial breeding habits. Ann. Rep. Smithsonian Inst., 1959: 427–445.Google Scholar
  27. Grosser, 0., 1909, Vergleichende Anatomie und Entwicklungsgeschichte der Eihaute und der Placenta. Wilhelm Braumuller, Vienna.Google Scholar
  28. Grosser, 0. and Tandler, J., 1909, Normentafel zur Entwicklungsgeschichte der Keibitzes (Vanellus cristatus Meyer), in: “Normentafeln zur Entwicklungsgeschichte der Wirbeltiere,” ( F. Keibel, ed.), Vol. 9. pp. 1–58, G. Fischer, Jena.Google Scholar
  29. Hamilton, H.L., 1952, Lillie’s Development of the Chick, 3rd ed. Henry Holt and Co., New York.Google Scholar
  30. Harrison, L. and Weekes, H.C., 1925, On the occurrence of placentation in the scincid lizard Lygosoma entrecasteauxi. Proc. Linn. Soc. NSW 50: 470–486.Google Scholar
  31. Hartman, C.G., 1916, Studies in the development of the opossum Didelphys virginiana L. I. History of the early cleavage. II. Formation of the blastocyst. J. Morph., 27: 1–83.CrossRefGoogle Scholar
  32. Hartman, C.G., 1919, Studies in the development of the opossum Didelphys virginiana L. III. Description of new material on maturation, cleavage and entoderm formation. IV. The bilaminar blastocyst. J. Morph., 32: 1–142.CrossRefGoogle Scholar
  33. Hartman, C.G., 1928, The breeding season of the opossum (Didelphis virginiana) and the rate of the intra-uterine and postnatal development. J. Morph., 46: 143–215.CrossRefGoogle Scholar
  34. Haswell, W.A., 1887, Observations on the early stages in the development of the emu (Dromaeus novae-hollandiae). Proc. Linn. Soc. NSW 2: 577–600.Google Scholar
  35. Hennig, W., 1966, Phylogenetic Systematics. University of Illinois Press, Urbana.Google Scholar
  36. Hill, J.P., 1895, Preliminary note on the occurrence of a placental connection in Perameles obesula and on the foetal membranes of certain macropods. Proc. Linn. Soc. NSW 10: 578–581.Google Scholar
  37. Hill, J.P., 1897, The placentation of Perameles. Quart. J. Micr. Sci., 40: 385–446.Google Scholar
  38. Hill, J.P., 1900, On the foetal membranes, placentation and parturition of the native cat (Dasyurus viverrinus). Anat. Anz., 18: 364–373.Google Scholar
  39. Hill, J.P., 1910, The early development of Marsupialia, with special reference to the native cat (Dasyurus viverrinus). Quart. J. Micr. Sci., 56: 1–134.Google Scholar
  40. Hill, J.P., 1932, The developmental history of the primates. Phil. Trans. Roy. Soc., Ser. B., 221: 45–178.CrossRefGoogle Scholar
  41. Hill, J.P., 1949, The allantoic placenta of Perameles. Proc. Linn. Soc. Lond., 161: 3–7.Google Scholar
  42. Hill, J.P. and Martin, C.J., 1894, On a platypus embryo from the intra-uterine egg. Proc. Linn. Soc. NSW 10: 43–74.Google Scholar
  43. Hoffman, L.H., 1970, Placentation in the garter snake Thamnophis sirtalis. J. Morph., 131: 57–88.PubMedCrossRefGoogle Scholar
  44. Hopson, J.A. and Crompton, A.W., 1969, Origin of mammals. Evol. Biol., 3: 15–72.Google Scholar
  45. Hrabowski, H., 1926, Das Dotterorgan der Eidechsen. Z. Wiss. Zool., 128: 305–382.Google Scholar
  46. Hubrecht, A.A.W., 1908, Early ontogenetic phenomena in mammals and their bearing on our interpretation of the phylogeny of the vertebrates. Quart. J. Micr. Sci., 53: 1–181.Google Scholar
  47. Hughes, R.L., 1974, Morphological studies on implantation in marsupials. J. Reprod. Fert., 39: 173–186.CrossRefGoogle Scholar
  48. Jollie, W.P. and Jollie, L.G., 1967, Electron microscopic observations on the yolk sac of the spiny dogfish, Squalus acanthias. J. Ultra. Res., 18: 102–126.CrossRefGoogle Scholar
  49. Kerr, J.G., 1919, Textbook of Embryology. H. Vertebrata. Macmillan, London.Google Scholar
  50. King, B.F. and Enders, A.C., 1970, Protein absorption and transport by the guinea pig visceral yolk sac placenta. Am. J. Anat., 129: 261–288.PubMedCrossRefGoogle Scholar
  51. Krull, J., 1906, Die Entwicklung der Ringelnatter (Tropoidonotus natrix Boie) vom ersten Aufstreten des Proamnios bis zum Schlusse des Amnios. Z. Wiss. Zool., 85: 107–155.Google Scholar
  52. Lambson, R.O., 1970, An electron microscopic study of the entodermal cells of the yolk sac of the chick during incubation and after hatching. Am. J. Anat., 129: 1–20.PubMedCrossRefGoogle Scholar
  53. Lemus, D., 1967, Contribution al estudio de la embriologia de reptiles chilenos. H. Tabla de desarrollo de la lagartija vivipara Liolaemus gravenhorti (Reptilia-Squamata-Iguanidae). Biologica, 40: 39–61.PubMedGoogle Scholar
  54. Lemus, D. and Duvauchelle, R., 1966, Desarollo intrauterino de Liolaemus tenuis tenuis (Dumeril y Bibron). Biologica, 39: 80–98.PubMedGoogle Scholar
  55. Luckett, W.P., 1971, The development of the chorio-allantoic placenta of the African scaly-tailed squirrels (family Anomaluridae). Am. J. Anat., 130: 159–178.PubMedCrossRefGoogle Scholar
  56. Luckett, W.P., 1974, Comparative development and evolution of the placenta in primates, in: “Reproductive Biology of the Primates, Contributions to Primatology,” (W.P. Luckett, ed.), Vol. 3., pp. 142–234. S. Karger, Basel.Google Scholar
  57. Luckett, W.P., 1975, Ontogeny of the fetal membranes and placenta: Their bearing on primate phylogeny, in: “Phylogeny of the Primates,” ( W.P. Luckett and F.S. Szalay, eds.), pp. 157–182. Plenum Press, New York.CrossRefGoogle Scholar
  58. Luckett, W.P., 1976, Cladistic relationships among primate higher categories: Evidence of the fetal membranes and placenta. Folia Primat, 25: 245–276.CrossRefGoogle Scholar
  59. Luckett, W.P. and Szalay, F.S., (in press), Clades versus grades in primate phylogeny, in: Proceedings 6th International Congress of Primatology, Cambridge, England. Academic Press, London and New York.Google Scholar
  60. Mahmoud, I.Y., Hess, G.L., and Klucka, J., 1973, Normal embryonic stages of the western painted turtle, Chrysemys pitta bellii. J. Morph., 141: 269–280.PubMedCrossRefGoogle Scholar
  61. McCrady, E., Jr., 1938, The embryology of the opossum. Am. Anat. Mem., 16: 1–233.Google Scholar
  62. Mitsukuri, K., 1891, On the foetal membranes of Chelonia. J. Coll. Sci., Imp. Univ. Japan, 4: 1–53.Google Scholar
  63. Mossman, H.W., 1937, Comparative morphogenesis of the fetal membranes and accessory uterine structures. Contrib. Embryol. Carneg. Inst., 26: 129–246.Google Scholar
  64. Mossman, H.W., 1953, The genital system and the fetal membranes as criteria for mammalian phylogeny and taxonomy. J. Mammal., 34: 289–298.CrossRefGoogle Scholar
  65. Mossman, H.W., 1967, Comparative biology of the placenta and fetal membranes, in: “Fetal Homeostasis,” (R.M. Wynn, ed.),Vol. 2, pp. 13–977-New York Academy of Science, New York.Google Scholar
  66. Mossman, H.W., 1971, Orientation and site of attachment of the blastocyst, in: “The Biology of the Blastocyst,” ( R.J.Blandau, ed.), pp. 49–57. University of Chicago Press, Chicago.Google Scholar
  67. Needham, J., 1942, Biochemistry and Morphogenesis. Cambridge University Press, London.Google Scholar
  68. Nelsen, O.E., Comparative Embryology of the Vertebrates. The Blakiston Company, New York.Google Scholar
  69. Noble, G.K., 1931, The Biology of the Amphibia. McGraw-Hill, New York.Google Scholar
  70. Padykula, H.A. and Taylor, J.M., 1974, Cytological observations on marsupial placentation: The Australian bandicoots (Perameles and Isoodon). Anat. Rec., 178: 434.Google Scholar
  71. Padykula, H.A. and Taylor, J.M. (in press), Ultrastructural evidence for loss of the trophoblastic layer in the chorioallantoic placenta of Australian bandicoots (Marsupialia: Peramelidae). Anat. Rec.Google Scholar
  72. Panigel, M., 1951, Rapports anatomo-histologiques etablis au cours de la gestation entre l’oeuf et l’oviducte maternel chez le lezard ovovivipare Zootoca vivipara W. Bull. Soc. Zool. Fr., 76: 163–170.Google Scholar
  73. Panigel, M., 1956, Contribution a l’etude de l’ovoviviparite chez les reptiles: Gestation et parturition chez le lezard vivipare Zootoca vivipara. Ann. Sci. Nat., Zool., 18: 569–668.Google Scholar
  74. Parameswaran, K.N., 1963, The foetal membranes and placentation of Enhydris dussumieri (Smith). Proc. Ind. Acad. Sci. B. 56: 302–327.Google Scholar
  75. Pasteels, J.J., 1957a, Une table analytique du developpement des reptiles. I. Stades de gastrulation chez les cheloniens et les lacertiliens. Ann. Soc. Roy. Zool. Belg., 87: 217–241.Google Scholar
  76. Pasteels, J.J., 1957b, La formation de l’amnios chez les cameleons. Ann. Soc. Roy. Zool. Belg., 87: 243–246.Google Scholar
  77. Pasteels, J.J., 1970, Developpement embryonnaire, in: “Traite de Zoologie,” (P.P. Grasse, ed.), Vol. 14, Part 3, pp. 893–971. Masson et Cie, Paris.Google Scholar
  78. Pearson, J., 1949, Placentation of the Marsupialia. Proc. Linn. Soc. London, 161: 1–3.CrossRefGoogle Scholar
  79. Peter, K., 1904, Normentafel eur Entwicklungsgeschichte der Zauneidechse (Lacerta agilis), in: “Normentafeln zur Entwicklungsgeschichte der Wirbeltiere,” (F. Keibel, ed.), Vol. 4. G. Fischer, Jena.Google Scholar
  80. Peter, K., 1934, Die erste Entwicklung des Chamaleons (Chamaeleo vulgaris), verglichen mit der Eidechse (Ei, Keimbildung, Furchung, Entodermbildung). Z. Anat. Entwg., 103: 147–188.CrossRefGoogle Scholar
  81. Peter, K., 1935, Die innere Entwicklung des Chamaleonkeimes nach der Furchung bis zum Durchbruch des Urdarms. Z. Anat. Entwg., 104: 1–60.CrossRefGoogle Scholar
  82. Reese, A.M., 1908, The development of the American alligator(A. mississippiensis). Smithsonian Misc. Coll., 6: 1–66.Google Scholar
  83. Reese, A.M., 1915, The Alligator and its Allies. Putnam, New York.Google Scholar
  84. Renfree, M.B., 1973, The composition of fetal fluids of the marsupial Macropus eugenii. Develop. Biol., 33: 63–79.Google Scholar
  85. Romanoff, A.L., 1960, The Avian Embryo. The Macmillan Company,New York.Google Scholar
  86. Romanoff, A.L. and Romanoff, A.J., 1949, The Avian Egg. John Wiley and Sons, New York.Google Scholar
  87. Romer, A.S., 1957, Origin of the amniote egg. Sci. Monthly, 85: 57–63.Google Scholar
  88. Romer, A.S., 1967, Major steps in vertebrate evolution. Science, 158: 1629–1637.PubMedCrossRefGoogle Scholar
  89. Schaeffer, B., Hecht, M.K., and Eldredge, N., 1972, Phylogeny and paleontology. Evol. Biol., 6: 31–46.CrossRefGoogle Scholar
  90. Schauinsland, H., 1899, Beitrage zur Biologie und Entwickelung der Hatteria nebst Bemerkungen uber die Entwickelung der Sauropsiden. Anat. Anz., 15: 309–334.Google Scholar
  91. Schauinsland, H., 1903, Beitrage zur Entwickelungsgeschichte und Anatomie der Wirbeltiere. I. Sphenodon, Callorhynchus, Chamaeleo. Zoologica, 16: 1–98.Google Scholar
  92. Schauinsland, H., 1906, Die Entwickelung der Eihaute der Reptilien und der Vogel, in: “Handbuch der Vergleichenden und experimentellen Entwickelungslehre der Wirbeltiere,” (0. Hertwig, ed.), Vol. 1, Pt. 2, pp. 177–234. G. Fischer, Jena.Google Scholar
  93. Schlafke, S. and Enders, A.C., 1975, Cellular basis of interaction between trophoblast and uterus at implantation. Biol. Reprod., 12: 41–65.PubMedCrossRefGoogle Scholar
  94. Selenka, E., 1887, Studien uber Entwickelungsgeschichte der Tiere. I V. Das Opossum (Didelphys virginiana). C.W. Kreidel’s Verlag. Wiesbaden.Google Scholar
  95. Semon, R., 1894a, Die Embryonalhullen der Monotremen und Marsupialier. Denkschr. Med. Naturwiss. Ges. Jena, 5: 19–58.Google Scholar
  96. Semon, R., 1894b, Zur Entwickelungsgeschichte der Monotremen. Denkschr. Med. Naturwiss. Ges. Jena, 5: 61–74.Google Scholar
  97. Sharman, G.B., 1961, The embryonic membranes and placentation in five genera of diprotodont marsupials. Proc. Zool. Soc. Lond., 137: 197–220.Google Scholar
  98. Simons, E.L., (in press), The fossil record of primate phylogeny, in: “Molecular Anthropology,” (M. Goodman and R.E. Tashian, eds.), Plenum Press, New York.Google Scholar
  99. Starch, D., 1959, Ontogenie und Entwicklungsphysiologie der Saugetiere. Handb. Zool., 8: 1–276.Google Scholar
  100. Tarkowski, A.K. and Wroblewska, J., 1967, Development of blastomeres of mouse eggs isolated at the 4- and 8-celled stage. J. Embryol. Exp. Morph., 18: 155–180.PubMedGoogle Scholar
  101. Turner, W., 1877, Some general observations on the placenta,with special reference to the theory of evolution. J. Anat. Physiol., 11: 33–53.Google Scholar
  102. Tyndale-Biscoe, H., 1973, Life of Marsupials. Arnold, London.Google Scholar
  103. Tyndale-Biscoe, C.H., Hearn, J.P., and Renfree, M.B., 1974, Control of reproduction in macropodid marsupials. J. Endocr., 63: 589–614.PubMedCrossRefGoogle Scholar
  104. Valen, L., 1967, New Paleocene insectivores and insectivore classification. Bull. Am. Mus. Nat. Hist., 135: 217–284.Google Scholar
  105. Virchow, H., 1892, Das Dotterorgan der Wirbeltiere (Fortsetzung). Arch. Mikr. Anat., 40: 39–101.CrossRefGoogle Scholar
  106. Voeltzkow, A., 1902, Beitrage zur Entwicklungsgeschichte der Reptilien. I. Biologie und Entwicklung der ausseren Korperform von Crocodilus madagascariensis Grant. Abh. Senckenberg. Naturf. Ges., 26: 1–150.Google Scholar
  107. Weekes, H.C., 1927, Placentation and other phenomena in the scincid lizard Lygosoma (Hinulia) quoyi. Proc. Linn. Soc. NSW 52:499–554.Google Scholar
  108. Weekes, H.C., 1929, On placentation in reptiles I. Proc. Linn. Soc. NSW 54: 34–60.Google Scholar
  109. Weekes, H.C., 1935, A review of placentation among reptiles, with particular regard to the function and evolution of the placenta. Proc. Zool. Soc. Lond., Part 2: 625–645.Google Scholar
  110. Wild, A.E., 1971, Transmission of proteins from mother to conceptus in the grey squirrel (Sciurus carolinensis). Immunology, 20: 789–797.Google Scholar
  111. Will, L., 1893, Beitrage zur Entwicklungsgeschichte der Reptilien.I. Die Anlage der Keimblatter beim Gecko (Platydactylus facetanus Schreib.). Zool. Jahrb., 6: 1–160.Google Scholar
  112. Wilson, J.T. and Hill, J.P., 1907, Observations on the development of Ornithorhynchus. Phil. Trans. Roy. Soc. Lond., Ser.B., 199: 31–168.CrossRefGoogle Scholar
  113. Wilson, J.T. and Hill, J.P., 1915, The embryonic area and so-called “primitive knot” in the early monotreme egg. Quart. J. Micr. Sci., 61: 15–25.Google Scholar
  114. Wislocki, G.B., 1929, On the placentation of primates, with a consideration of the phylogeny of the placenta. Contrib. Embryol. Carneg. Inst., 20: 51–80.Google Scholar
  115. Witschi, E., 1956 Development of Vertebrates. W.B. Saunders Company, Philadelphia.Google Scholar
  116. Yntema, C.L., 1968, A series of stages in the embryonic development of Chelydra serpentina. J. Morph., 125: 219–252.PubMedCrossRefGoogle Scholar
  117. Zehr, D.R., 1962, Stages in the normal development of the common garter snake, Thamnophis sirtalis sirtalis. Copeia, 1962: 322–329.CrossRefGoogle Scholar

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© Plenum Press, New York 1977

Authors and Affiliations

  • W. Patrick Luckett
    • 1
  1. 1.Dept. of AnatomyCreighton Univ. School of MedicineOmahaUSA

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