Abstract
Embryogenetic pathways differ markedly among monotremes, marsupials, and placentals, and their analysis provides information of fundamental importance to recognition of mammalian evolutionary directions. The cap of cuboidal cells of the marsupial late unilaminar blastocyst, generally known as the “embryonic area,” probably is induced to form (prior to origin of Hensen's node) by signals from earliest hypoblastic cells (“anterior visceral endoderm”). The thickened cap is a “medullary plate” of sauropsid terminology because it includes epiblastic cells presumptive to neurectoderm (including neural crest), Hensen's node, primitive streak, and gut endoderm. The remainder of the definitive embryo (i.e., parts of epidermal origin, including ectodermal placodes) derives from squamous ectoderm (surrounding the medullary plate) of the blastocyst's ill-named “trophoblastic area.” Amniotic ectoderm develops farther distally within the “trophoblastic area.” The autapomorphic inner cell mass (ICM) of placental mammals is homologous to medullary plate of the marsupial blastocyst plus morphologically undefined, proximal parts of surrounding ectoderm (of the “trophoblastic area”). Considerations of early cell lineages in marsupials are greatly affected by recognition that the boundary between future embryonic and extra-embryonic tissues does not match the margin of the medullary plate (i.e., “embryonic area”). Marsupials and monotremes largely conform to sauropsid early embryogenesis, but placentals express, at earliest developmental stages, innovations unique within Amniota that are linked to early establishment of the brain. Neonatal marsupials and hatchling monotremes are extremely altricial and closely comparable anatomically/physiologically; they share a temporal pattern in combining early morphogenesis of craniofacial features (related to suckling) with deferral of telencephalic completion into postnatal/posthatching life. Placentals contrast greatly in establishing the central nervous system prior to rudiments of the cranial skeleton and associated musculature, and they complete essentials of forebrain development before birth. Comparative evidence from transitory periderm suggests that primordial eutherians had extremely altricial hatchlings or newborns, whichever was the mode of early development. Details remain unknown about the origin of the unique specialization of ICM plus encapsulating trophoblast from the more generalized blastula of ancestral synapsids.
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Archibald, J. D., and Deutschman, D. H. (2001). Quantitative analysis of the timing of the origin and diversification of extant placental orders. J. Mammal. Evol. 8: 107–124.
Beer, G. R. de, and Fell, W. A. (1936). The development of the Monotremata. Part III. The development of the skull of Ornithorhynchus. Zool. Soc. Lond. Trans. 23: 1–43.
Beneden, E. van (1875). La maturation de lœuf, la fécondation, et les premières phases du développement embryonnaire des mammifères d'après des recherches faites chez le Lapin. Acad. Roy. Belg. Bull. Cl. Sci. 2ième ser. 40: 686–736.
Billington, W. D., and Bell, S. C. (1983). Immunobiology of mouse trophoblast. In: Biology of Trophoblast, Y. W. Loke and A. Whyte, eds., pp. 571–595, Elsevier, Amsterdam.
Blackburn, D. G. (1992). Convergent evolution of viviparity, matrotrophy, and specializations for fetal nutrition in reptiles and other vertebrates. Amer. Zool. 32: 313–321.
Blackburn, D. G. (1998). Viviparity and oviparity: Evolution and reproductive strategies. In: Encyclopedia of Reproduction, Vol. 4, E. Knobil and J. D. Neill, eds., pp. 994–1003, Academic Press, San Diego, CA.
Blackburn, D. G., Hayssen, V., and Murphy, C. J. (1989). The origins of lactation and the evolution of milk: A review with new hypotheses. Mammal. Rev. 19: 1–26.
Blackburn, D. G., Taylor, J. M., and Padykula, H. A. (1988). Trophoblast concept as applied to therian mammals. J. Morphol. 196: 127–136.
Bluntschli, H. (1938). Le développement primaire et l'implantation chez un centetiné (Hemicentetes). C. R. Assoc. Anat. 33: 39–46.
Caldwell, W. H. (1887). Embryology of Monotremata and Marsupialia. Part I. Roy. Soc. Lond. Philos. Trans. 178B: 463–486.
Carroll, R. L. (2001). The origin and early radiation of terrestrial vertebrates. J. Paleontol. 75: 1202–1213.
Cedard, L., and Firth, A. (eds.) (1992). Placental Signals: Autocrine and Paracrine Control of Pregnancy, Trophoblast Research Vol. 6, University of Rochester Press, Rochester, NY.
Cifelli, R. L. (2001). Early mammalian radiations. J. Paleontol. 75: 1214–1226.
Clark, C. T., and Smith, K. K. (1993). Cranial osteogenesis in Monodelphis domestica (Didelphidae) and Macropus eugenii (Macropodidae). J. Morphol. 215: 119–149.
Coulam, C. B., Faulk, W. P., and McIntyre, J. A. (1992). Immunological Obstetrics W. W. Norton, New York.
Cruz, Y. P., Yousef, A., and Selwood, L. (1996). Fate-map analysis of the epiblast of the dasyurid marsupial Sminthopsis macroura (Gould). Reprod. Fertil. Dev. 8: 779–788.
Denker, H.-W. (1983). Cell lineage, determination and differentiation in earliest developmental stages in mammals. In: Bibliotheca Anatomica, Vol. 24, W. Lierse, ed., pp. 22–58, Karger, Basel.
Edwards, R. G., Howe, C. W. S., and Johnson, M. H. (1975). Immunobiology of Trophoblast, Cambridge University Press, Cambridge, UK.
Foley, A. C., Skromne, I., and Stern, C. D. (2000). Reconciling different models of forebrain induction and patterning: A dual role for the hypoblast. Development 127: 3839–3854.
Flynn, T. T., and Hill, J. P. (1939). The development of the Monotremata. IV: Growth of the ovarian ovum, maturation, fertilisation, and early cleavage. Zool. Soc. Lond. Trans. 24: 445–623.
Flynn, T. T., and Hill, J. P. (1947). The development of the Monotremata. VI: The later stages of cleavage and the formation of the primary germ-layers. Zool. Soc. Lond. Trans. 26: 1–151 + 27 pls.
Frankenberg, S., and Selwood, L. (1998). An ultrastructural study of the role of an extracellular matrix during normal cleavage in a marsupial, the brushtail possum. Mol. Reprod. Dev. 50: 420–433.
Fraser, R. C. (1954). Studies on the hypoblast of the young chick embryo. J. Exp. Zool. 126: 349–399.
Garcia-Martinez, V., Alvarez, I. S., and Schoenwolf, G. C. (1993). Locations of the ectodermal and nonectodermal subdivisions of the epiblast at stages 3 and 4 of avian gastrulation and neurulation. J. Exp. Zool. 267: 431–446.
Gaupp, E. (1908). Zur Entwicklungsgeschichte und vergleichenden Morphologie des Schädels von Echidna aculeata var. typica. Denkschr. Med. Naturwiss. Ges. Jena (Semon. Zool. Forschungsreisen in Australien) 6 (Pt. 2): 539–788.
Gilbert, S. F. (1994). Developmental Biology, Sinauer Associates, Sunderland, MA.
Goetz, R. H. (1938). On the early development of the Tenrecoidea (Hemicentetes semispinosus). Biomorphosis 1: 67–79.
Gribnau, A. A. M., and Geijsberts, L. G. M. (1981). Developmental stages in the rhesus monkey (Macaca mulatta). Adv. Anat. Embryol. Cell Biol. 68: vi, 1–84.
Gribnau, A. A. M., and Geijsberts, L. G. M. (1985). Morphogenesis of the brain in staged rhesus monkey embryos. Adv. Anat. Embryol. Cell Biol. 91: viii, 1–69.
Griffiths, M. (1968). Echidnas, Pergamon Press, Oxford.
Griffiths, M. (1978). The Biology of the Monotremes. Academic Press, New York.
Griffiths, M., McIntosh, D. L., and Coles, R. E. A. (1969). The mammary gland of the echidna, Tachyglossus aculeatus, with observations on the incubation of the egg and on the newly-hatched young. J. Zool. 158: 371–386.
Harder, J. D., Stonerook, M. J., and Pondy, J. (1993). Gestation and placentation in two New World opossums: Didelphis virginiana and Monodelphis domestica. J. Exp. Zool. 266: 463–479.
Hartman, C. G. (1916). Studies in the development of the opossum Didelphis virginiana L. I. History of the early cleavage. II: Formation of the blastocyst. J. Morphol. 27: 1–83.
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. Morphol. 32: 1–142.
Hartman, C. G. (1928). The breeding season of the opossum (Didelphis virginiana) and the rate of intrauterine and postnatal development. J. Morphol. 46: 143–215.
Hatada, Y., and Stern, C. D. (1994). A fate map of the epiblast of the early chick embryo. Development 120: 2879–2889.
Hill, J. P. (1910). Contributions to the embryology of the Marsupialia, IV: The early development of the Marsupialia, with special reference to the native cat (Dasyurus viverrinus). Q. J. Microsc. Sci. 56: 1–134 + pls. 1–9.
Hill, J. P. (1918). Contributions to the embryology of the Marsupialia. V: Some observations on the early development of Didelphys aurita. Q. J. Microsc. Sci. 63: 91–139 + pls. 6–9.
Hill, J. P., and de Beer, G. R. (1949). Development of the Monotremata. Part VII: The development and structure of the egg-tooth and the caruncle in the monotremes and on the occurrence of vestiges of the egg-tooth and caruncle in marsupials. Zool. Soc. Lond. Trans. 26: 503–544 + 10 pls.
Hine, R. (ed.) (1999). The Facts on File Dictionary of Biology, 3rd edn., Checkmark Books, Facts on File, Inc., New York.
Hopson, J. A. (1994). Synapsid evolution and the radiation of non-eutherian mammals. In: Major Features of Vertebrate Evolution, Short Courses in Paleontology 7, D. R. Prothero and R. M. Schoch, eds., pp. 190–219, The Paleontological Society, Lawrence, KS.
Hubrecht, A. A. W. (1889). Studies in mammalian embryology. I: The placentation of Erinaceus europaeus, with remarks on the phylogeny of the placenta. Q. J. Microsc. Sci. 30: 283–404 + pls. XV–XXVII.
Hubrecht, A. A. W. (1908). Early ontogenetic phenomena in mammals and their bearing on our interpretation of the phylogeny of the vertebrates. Q. J. Microsc. Sci. 53: 1–181.
Hughes, R. L. (1984). Structural adaptations of the eggs and the fetal membranes of monotremes and marsupials for respiration and metabolic exchange. In: Respiration and Metabolism of Embryonic Vertebrates, R. S. Seymour, ed., pp. 389–421, Dr W. Junk Publishers, Boston.
Hughes, R. L. (1993). Monotreme development with particular reference to the extraembryonic membranes. J. Exp. Zool. 266: 480–494.
Hughes, R. L., and Hall, L. S. (1988). Structural adaptations of the newborn marsupial. In: The Developing Marsupial: Models for Biomedical Research, C. H. Tyndale-Biscoe and P. A. Janssens, eds., pp. 8–27, Springer-Verlag, Berlin.
Hughes, R. L., and Hall, L. S. (1998). Early development and embryology of the platypus. Roy. Soc. Lond. Philos. Trans., Ser. B 353: 1101–1114.
Janke, A., Magnell, O., Wieczorek, G., Westerman, M., and Arnason, U. (2002). Phylogenetic analysis of 18S rRNA and the mitochondrial genomes of the wombat, Vombatus ursinus, and the spiny anteater, Tachyglossus aculeatus: Increased support for the Marsupionta hypothesis. J. Mol. Evol. 54: 71–80.
Jeffery, J. E., Bininda-Emonds, O. R. P., Coates, M. I., and Richardson, M. K. (2002). Analyzing evolutionary patterns in amniote embryonic development. Evol. Dev. 4: 292–302.
Ji, Q., Luo, Z.-X., Yuan, C.-X., Wible, J. R., Zhang, J.-P., and Georgi, J. A. (2002). The earliest known eutherian mammal. Nature 416: 816–822.
Johnson, M. H. (1996). Origins of pluriblast and trophoblast in the eutherian conceptus. Reprod. Fertil. Dev. 8: 699–709.
Johnson, M. H., and Selwood, L. (1996). Nomenclature of early development in mammals. Reprod. Fertil. Dev. 8: 759–764.
Kerr, T. (1935). Notes on the development of the germ-layers in diprotodont marsupials. Q. J. Microsc. Sci. 77: 305–315.
Kerr, T. (1936). On the primitive streak and associated structures in the marsupial Bettongia cuniculus. Q. J. Microsc. Sci. 78: 687–715.
Kielan-Jaworowska, Z., Cifelli, R. L., and Luo, Z.-X. (eds.) (2004). Mammals from the Age of Dinosaurs: Origins, Evolution and Structure, Columbia University Press, New York.
Killian, J. K., Buckley, T. R., Stewart, N., Munday, B. L., and Jirtle, R. L. (2001). Marsupials and eutherians reunited: Genetic evidence for the Theria hypothesis of mammalian evolution. Genome 12: 513–517.
Kirsch, J. A. W., and Mayer, G. C. (1998). The platypus is not a rodent: DNA hybridization, amniote phylogeny and the palimpsest theory. Roy. Soc. Lond. Philos. Trans., Ser. B 353: 1221–1237.
Knoetgen, H., Teichmann, U., and Kessel, M. (1999a). Head-organizing activities of endodermal tissues in vertebrates. Cell. Mol. Biol. 45: 481–492.
Knoetgen, H., Viebahn, C., and Kessel, M. (1999b). Head induction in the chick by primitive endoderm of mammalian, but not avian origin. Development 126: 815–825.
Knoetgen, H., Teichmann, U., Wittler, L., Viebahn, C., and Kessel, M. (2000). Anterior neural induction by nodes from rabbits and mice. Dev. Biol. 225: 370–380.
Krause, W. J. (1998). A review of histogenesis/organogenesis in the developing North American opossum (Didelphis virginiana). Adv. Anat. Embryol. Cell Biol. 143: 1–143.
Kuhn, H.-J. (1971). Die Entwicklung und Morphologie des Schädels von Tachyglossus aculeatus. Abh. senkenb. naturforsch. Ges. 528: 1–192 + pls. 1–32.
Kuhn, H.-J., and Zeller, U. (1987). The cavum epiptericum in monotremes and therian mammals. In: Morphogenesis of the Mammalian Skull, H.-J. Kuhn and U. Zeller, eds., pp. 51–70, Verlag Paul Parey, Hamburg.
Lillegraven, J. A. (1975). Biological considerations of the marsupial–placental dichotomy. Evolution 29: 707–722.
Lillegraven, J. A. (1985). Use of the term "trophoblast" for tissues in therian mammals. J. Morphol. 183: 293–299.
Lillegraven, J. A., Thompson, S. D., McNab, B. K., and Patton, J. L. (1987). The origin of eutherian mammals. Biol. J. Linn. Soc. 32: 281–336.
Loke, Y. W., and Whyte, A. (1983). Biology of Trophoblast, Elsevier, Amsterdam.
Luckett, W. P., and Zeller, U. (1989). Developmental evidence for dental homologies in the monotreme Ornithorhynchus and its systematic implications. Z. Säugetierkunde 54: 193–204.
Luo, Z.-X., Kielan-Jaworowska, Z., and Cifelli, R. L. (2002). In quest for a phylogeny of Mesozoic mammals. Acta Palaeontol. Pol. 47: 1–78.
Lyne, A. G., and Hollis, D. E. (1977). The early development of marsupials, with special reference to bandicoots. In: Reproduction and Evolution, J. H. Calaby and C. H. Tyndale-Biscoe, eds., pp. 293–302, Australian Academy of Science, Canberra City.
Maier, W. (1993). Cranial morphology of the therian common ancestor, as suggested by the adaptations of neonate marsupials. In: Mammal Phylogeny: Vol. 2. Mesozoic Differentiation, Multituberculates, Monotremes, Early Therians, and Marsupials, F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds., pp. 165–181, Springer-Verlag, New York.
Mate, K. E., Robinson, E. S., VandeBerg, J. L., and Pedersen, R. A. (1994). Timetable of in vivo embryonic development in the grey short-tailed opossum (Monodelphis domestica). Mol. Reprod. Dev. 39: 365–374.
McCrady, E., Jr. (1938). The embryology of the opossum. Am. Anat. Mem., Wistar Inst. Anat. Biol. 16: 233p.
McCrady, E., Jr. (1944). The evolution and significance of the germ layers. J. Tenn. Acad. Sci. 19: 240–251.
McKenna, M. C., and Bell, S. K. (1997). Classification of Mammals Above the Species Level, Columbia University Press, New York.
Morton, H. (1998). Early pregnancy factor: An extracellular chaperonin 10 homologue. Immunol. Cell Biol. 76: 483–496.
Morton, H., Rolfe, B. E., McNeill, L., Clarke, P., Clarke, F. M., and Clunie, G. J. A. (1980). Early pregnancy factor: Tissues involved in its production in the mouse. J. Reprod. Immunol. 2: 73–82.
Müller, F. (1968). Die transitorischen Verschlüsse in der postnatalen Entwicklung der Marsupialia. Acta Anat. 71: 581–624.
Nelson, J. E. (1988). Growth of the brain. In: The Developing Marsupial: Models for Biomedical Research, C. H. Tyndale-Biscoe and P. A. Janssens, eds., pp. 87–100, Springer-Verlag, Berlin.
Novacek, M. J., Rougier, G. W., Wible, J. R., McKenna, M. C., Dashzeveg, D., and Horovitz, I. (1997). Epipubic bones in eutherian mammals from the Late Cretaceous of Mongolia. Nature 389: 483–486.
Nunn, C. L., and Smith, K. K. (1998). Statistical analyses of developmental sequences: The craniofacial region of marsupial and placental mammals. Amer. Nat. 152: 82–101.
Packard, G. C., Elinson, R. P., Gavaud J., Guillette, L. J., Jr., Lombardi, J., Schindler, J., Shine, R., Tyndale-Biscoe, H. C., Wake, M. H., Xavier, F. D. J., and Yaron, Z. (1989). Group report: How are reproductive systems integrated and how has viviparity evolved? In: Complex Organismal Functions: Integration and Evolution in Vertebrates, D. B. Wake and G. Roth, eds., pp. 281–293, Wiley, New York.
Patten, B. M. (1948). Embryology of the Pig, McGraw-Hill, New York.
Patten, B. M. (1964). Foundations of Embryology, McGraw-Hill, New York.
Penny, D., Hasegawa, M., Waddell, P. J., and Hendy, M. D. (1999). Mammalian evolution: Timing and implications from using the LogDeterminant transform for proteins of differing amino acid composition. Syst. Biol. 48: 76–93.
Renfree, M. B. (1993). Ontogeny, genetic control, and phylogeny of female reproduction in monotreme and therian mammals. In: Mammal Phylogeny: Vol. 2. Mesozoic Differentiation, Multituberculates, Monotremes, Early Therians, and Marsupials, F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds., pp. 4–20, Springer-Verlag, New York.
Renfree, M. B. (1995). Monotreme and marsupial reproduction. Reprod. Fertil. Dev. 7: 1003–1020.
Rich, T. H., Flannery, T. F., Trusler, P., Kool, L., van Klaveren, N. A., and Vickers-Rich, P. (2002). Evidence that monotremes and ausktribosphenids are not sistergroups. J. Vert. Paleontol. 22: 466–469.
Richardson, M. K. (1995). Heterochrony and the phylotypic period. Dev. Biol. 172: 412–421.
Richardson, M. K., Hanken, J., Gooneratne, M. L., Pieau, C., Raynaud, A., Selwood, L., and Wright, G. M. (1997). There is no highly conserved embryonic stage in the vertebrates: Implications for current theories of evolution and development. Anat. Embryol. 196: 91–106.
Roberts, C. T., and Breed, W. G. (1996). The marsupial shell membrane: An ultrastructural and immunogold localization study. Cell Tissue Res. 284: 99–110.
Roberts, C. T., Breed, W. G., and Mayrhofer, G. (1994). Origin of the oocyte shell membrane of a dasyurid marsupial: An immunohistochemical study. J. Exp. Zool. 270: 321–331.
Rose, R. W. (1989). Embryonic growth rates of marsupials with a note on monotremes: J. Zool. 218: 11–16.
Rougier, G. W., Wible, J. R., and Novacek, M. J. (1998). Implications of Deltatheridium specimens for early marsupial history. Nature 396: 459–463.
Sánchez-Villagra, M. R., Gemballa, S., Nummela, S., Smith, K. K., and Maier, W. (2002). Ontogenetic and phylogenetic transformations of the ear ossicles in marsupial mammals. J. Morphol. 251: 219–238.
Schmidt, W. (1992). The amniotic fluid compartment: The fetal habitat. Adv. Anat. Embryol. Cell Biol. 127: 1–100.
Schoenwolf, G. C. (1991). Cell movements in the epiblast during gastrulation and neurulation in avian embryos. In: Gastrulation: Movements, Patterns, and Molecules, R. Keller, W. H. Clark, Jr., and F. Griffin, eds., pp. 1–28, Plenum Press, New York.
Schoenwolf, G. C. (1995). Laboratory Studies of Vertebrate and Invertebrate Embryos: Guide and Atlas of Descriptive and Experimental Development, Prentice-Hall, Englewood Cliffs, NJ.
Schoenwolf, G. C., and Sheard, P. (1990). Fate mapping the avian epiblast with focal injections of a fluorescent-histochemical marker: Ectodermal derivatives. J. Exp. Zool. 255: 323–339.
Selenka, E. (1887). Studien über Entwicklungsgeschichte der Theire. Bd. 4. Das Opossum (Didelphys virginiana). C. W. Kreidels Verlag, Wiesbaden.
Selwood, L. (1986). The marsupial blastocyst—A study of the blastocysts in the Hill Collection. Aust. J. Zool. 34: 177–187.
Selwood, L. (1992). Mechanisms underlying the development of pattern in marsupial embryos. In: Current Topics in Developmental Biology, Vol. 27, R. A. Pedersen, ed., pp. 175–233, Academic Press, San Diego, CA.
Selwood, L. (1994). Development of early cell lineages in marsupial embryos: An overview. Reprod. Fertil. Dev. 6: 507–527.
Selwood, L. (1996). The blastocyst epithelium is not a protoderm in dasyurid marsupials: A review of the evidence. Reprod. Fertil. Dev. 8: 711–723.
Selwood, L. (2000). Marsupial egg and embryo coats. Cells Tissues Organs 166: 208–219.
Selwood, L., and Sathananthan, A. H. (1988). Ultrastructure of early cleavage and yolk extrusion in the marsupial Antechinus stuartii. J. Morphol. 195: 327–344.
Selwood, L., and Woolley, P. A. (1991). A timetable of embryonic development, and ovarian and uterine changes during pregnancy, in the stripe-faced dunnart, Sminthopsis macroura (Marsupialia: Dasyuridae). J. Reprod. Fertil. 91: 213–227.
Smith, K. K. (1994). Development of craniofacial musculature in Monodelphis domestica (Marsupialia, Didelphidae). J. Morphol. 222: 149–173.
Smith, K. K. (1997). Comparative patterns of craniofacial development in eutherian and metatherian mammals. Evolution 51: 1663–1678.
Smith, K. K. (2001a). Early development of the neural plate, neural crest and facial region of marsupials. J. Anat. 199: 121–131.
Smith, K. K. (2001b). The evolution of mammalian development. Bull. Mus. Comp. Zool. Harv. Univ. 156: 119–135.
Smith, K. K. (2001c). Heterochrony revisited: The evolution of developmental sequences. Biol. J. Linn. Soc. 73: 169–186.
Souza, F. S. J. de, and Niehrs, C. (2000). Anterior endoderm and head induction in early vertebrate embryos. Cell Tissue Res. 300: 207–217.
Springer, M. S., Murphy, W. J., Eizrik, E., and O'Brien, S. J. (2003). Placental mammal diversification and the Cretaceous–Tertiary boundary. Proc. Natl. Acad. Sci. U.S.A. 100: 1056–1061.
Stern, C. D. (1991). Mesoderm formation in the chick embryo, revisited. In: Gastrulation: Movements, Patterns, and Molecules, R. Keller, W. H. Clark Jr., and F. Griffin, eds., pp. 29–41, Plenum Press, New York.
Tyndale-Biscoe, H., and Renfree, M. (1987). Reproductive Physiology of Marsupials, Cambridge University Press, Cambridge, UK.
Ulinski, P. S. (1984). Thalamic projections to the somatosensory cortex of the echidna, Tachyglossus aculeatus. J. Comp. Neurol. 229: 153–170.
Velhagen, W. A., Jr. (1997). Analyzing developmental sequences using sequence units. Syst. Biol. 46: 204–210.
Viebahn, C., Mayer, B., and Habré de Angelis, M. (1995). Signs of the principle [sic] body axes prior to primitive streak formation in the rabbit embryo. Anat. Embryol. 192: 159–169.
Voyle, R. B., Haines, B. P., Loffler, K. A., Hope, R. M., Rathjen, P. D., and Breed, W. G. (1999). Isolation and characterisation of zona pellucida A (ZPA) cDNAs from two species of marsupial: Regulated oocyte-specific expression of ZPA transcripts. Zygote 7: 239–248.
Waddington, C. H. (1952). The Epigenetics of Birds, Cambridge University Press, Cambridge, UK.
Wood, G. W. (1994). Is restricted antigen presentation the explanation for fetal allograft survival?. Immunol. Today 15: 15–18.
Woodburne, M. O., Rich, T. H., and Springer, M. S. (2003). The evolution of tribospheny and the antiquity of mammalian clades. Mol. Phylogenet. Evol. 28: 360–385.
Yousef, A., and Selwood, L. (1993). Embryonic development in culture of the marsupials Antechinus stuartii (Macleay) and Sminthopsis macroura (Spencer) during preimplantation stages. Reprod. Fertil. Dev. 5: 445–458.
Zeller, U. (1999a). Mammalian reproduction: Origin and evolutionary transformations. Zool. Anz. 238: 117–130.
Zeller, U. (1999b). Phylogeny and systematic relations of the Monotremata: Why we need an integrative approach. Cour. Forschungsinst. Senckenb. 215: 227–232.
Zeller, U., and Freyer, C. (2001). Early ontogeny and placentation of the grey short-tailed opossum, Monodelphis domestica (Didelphidae: Marsupialia): Contribution to the reconstruction of the marsupial morphotype. J. Zool. Syst. Evol. Res. 39: 137–158.
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Lillegraven, J.A. Polarities in Mammalian Evolution Seen Through Homologs of the Inner Cell Mass. Journal of Mammalian Evolution 10, 277–333 (2003). https://doi.org/10.1023/B:JOMM.0000019774.11018.22
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DOI: https://doi.org/10.1023/B:JOMM.0000019774.11018.22