Mechanisms Underlying the Development of Pattern in Marsupial Embryos
Department of Zoology La Trobe University Bundoora, 3083 Victoria, Australia
Since the development of the inside-outside hypothesis (Tarkowski and Wroblewska, 1967) and its subsequent experimental analysis (for review, see Denker, 1976; Johnson, 1981; Gardner, 1983; Pedersen, 1986) of how the cells of a mammalian embryo could receive and respond to positional signals (re- viewed by Johnson and Maro, 1986) the marsupial embryo has presented a paradox to developmental biologists because of the external position of the embryoblast (Hill, 1910; Hartman, 1916; McCrady, 1938; Selwood and Young, 1983; Selwood, 1986a,b). The embryoblast of the marsupial appears in a blastocyst in which all cells are superficial and apparently identical. This caused McCrady (1938) to call the blastocyst epithelium a “protoderm” because of the apparent totipotency of the cells. Marsupial embryos are not unique in possessing a unilaminar blastocyst with no inner cell mass. Such a structure is also found in a number of other mammals including the elephant shrew, Elephantulus (van der Horst, 1942), and the tenrec, Hemicentetes (Bluntschli, 1938; Goetz, 1939; see Wimsatt, 1975, for review). Of course, in the monotremes Ornithorynchus and Tachyglossus, which have meroblastic cleavage (see Griffiths, 1978, for review) embryonic and extraembryonic cells are also generated from an initially unilaminar structure, the blastoderm.
Eutherian mammalian embryos such as the mouse have considerable capacity to regulate for loss or addition of blastomeres (Tarkowski, 1961; Mintz, 1965). Specification of cell fate is due largely, if not entirely, to positional effects (Pedersen, 1986; Johnson and Maro, 1986) and maternal determinants are thought to play a minimal role (Johnson et al., 1986). These positional effects are derived from environmental stimuli, not so much from diffusable components unique to an inside or outside location, but because inside or outside cells have particular relationships with their neighbouring cells (Pedersen and Spindle, 1980). In eutherian mammals, in which some cells (the inner cell mass, ICM) are enclosed by others (the trophectoderm, TE), the cellular positional signals act in a three-dimensional framework within the morula. In marsupials, cellular positional signals may act instead in the two-dimensional framework of an epithelial sheet because of the unilaminar structure of the blastocyst. Any three-dimension- al signals acting on early marsupial differentiation would have to be derived from the outside environment (the investments and factors in the uterine lumen) and the inside environment (the blastocoel) acting in concert with cell-cell interactions. It is difficult, however, to envision how outside and inside information could lead to specialization of some blastocyst epithelial cells at the embryonic pole (destined to form the primary endoderm cells) because all blastocyst epi- thelial cells appear to be exposed to the same external and internal environments.
This review provides an outline of marsupial embryonic development during preimplantation stages up to the trilaminar blastocyst stage. Because the developing polarity of the marsupial embryo is initiated during oogenesis, the review also covers oogenesis and fertilization in marsupials. It does not deal with re- productive physiology of marsupials, which has been comprehensively reviewed in recent years (Tyndale-Biscoe and Renfree, 1987). It also does not deal with embryonic development past the trilaminar blastocyst stage, and so does not include organogenesis. [In most marsupials the embryo is implanted after neural tube and somite formation have begun (Selwood, 1989a) when the embryo has about 15-25 somites.]
Accordingly, the major theme of this review will be to explore the idea that the marsupial embryo acquires a polarized state that is initially related to the position of the nucleus and the pattern of distribution of cytoplasmic organelles, especially yolky storage products, in oocytes and zygotes. The particular nature of this polarized state generates a particular and highly specific pattern of cleavage. This in turn ensures that blastomeres during cleavage end up occupying a particular part of the blastocyst wall. The potential role of positional signals, the order of cell division and maternal determinants operating at a two-dimensional level in specifying cell fate, and early steps in determination will be examined.