Ultrastructural evidence for loss of the trophoblastic layer in the chorioallantoic placenta of Australian Bandicoots (Marsupialia: Peramelidae)

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Abstract
In most marsupials, placentation involves only the yolk sac; however, in the bandicoot family, Peramelidae, a functional chorioallantoic placentation develops in addition (Hill, 1895, 1897, 1900; Flynn, ′22, ′23). This duality is viewed as having evolutionary significance because most eutheria have both placentae. Furthermore, the bandicoot trophoblast was reported to vanish from the chorioallantoic site in late gestation (Hill, 1897; Flynn, ′23); whereas, the eutherian trophoblast is identifiable throughout later pregnancy and may act as an immunological barrier between maternal and fetal genotypes (Kirby, ′68). Thus we have re‐examined this singular chorioallantoic placenta of the bandicoot in plastic sections with light and electron microscopy.A distinctive feature of bandicoot placentation is the transformation of the uterine simple columnar luminal epithelium into a highly vascular lining composed almost entirely of discrete syncytial masses (homokaryons). Endometrial blood vessels penetrate among the homokaryons to create a rich network of large diameter capillaries at extremely superficial locations near the maternal surface.In the chorioallantoic placenta (7 mm to 10–11 mm crown‐rump embryos) the microvillous surface of the maternal homokaryons interdigitates with the microvillous border of the fetal trophoblast with desmosomal interaction. This trophoblast consists of a single layer of tall columnar undifferentiated cells rich in ribosomes‐polysomes, poor in cytoplasmic membranes, and with large nuclei that have distinct clumps of heterochromatin and conspicuous nucleoli. It is thus remarkable that these undifferentiated cells disappear as a recognizable layer later in gestation (12 mm crown‐rump embryos).Flynn's hypothesis that the trophoblastic cells disapppear by fusing with maternal syncytia gains support from the existence of two populations of nuclei in the syncytial masses only at the chorioallantoic site. One population is comparable to that occurring in the homokaryons of the yolk sac placenta, i.e., pale staining nuclei with little heterochromatin and small peripheral nucleoli. However, the other nuclei resemble those of the trophoblast cells. Since the trophoblastic cells before their disappearance as a layer possess properties associated with potential for further differentiation, the possibility of fusion between the maternal homokaryons and the fetal trophoblastic cells to form heterokaryons composed of two genotypes merits further consideration.The disappearance of the trophoblastic layer and the superficial positioning of the maternal capillaries bring the maternal and fetal bloodstreams into closest proximity near term (12 mm crown‐rump embryo). The thinnest parts of the barrier consist of delicate cytoplasmic extensions from the syncytial masses (that may be maternal in origin or jointly maternal and fetal) and a layer of maternal stroma intervening between the maternal and fetal endothelia. Thus the chorioallantoic placental barrier of the marsupial bandicoot is unlike any thus far described for eutherian mammals.

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