Histomorphometric comparison of the gravid and non-gravid uterus at the time of birth in the tammar wallaby (Macropus eugenii): insights into the embryo-maternal interface.

Abstract

Context Tammar wallabies have a very short gestation which does not exceed the length of the estrus cycle. Direct contact between embryo and mother is established via a short-lived yolk sac placenta only in the last third of gestation. Therefore, an efficient embryo-maternal interface is required to ensure rapid embryonic growth. However, the morphology of the placenta at the time of birth is not well described in marsupials. Aims To study the morphology of the embryo-maternal interface, to compare the gravid and the non-gravid uterus at the time of birth and to examine the presence of polyploid trophoblast cells. Methods Histomorphometrical analysis of the uteri from light microscopic images. Quantification of the endometrial vascularization in samples stained with CD31 using AI machine learning. DNA content estimations of the giant trophoblast cell nuclei by Feulgen Image Analysis Densitometry. Key results In histological sections of the gravid endometrium, more tissue area was occupied by blood vessels than in the non-gravid endometrium, with subepithelial capillaries making up one-fourth of the vessel area in the gravid endometrium. The gravid uterus exhibited a 2.75-fold increase in surface area due to winding folds. Polyploidy of the giant trophoblast cells was confirmed. Giant trophoblast cells showed signs of degeneration. Conclusions The adaptations of the gravid uterus and the polyploidy of the trophoblast cells ensure sufficient embryo-maternal exchange. However, they seem to be self-limiting. Implications Morphology of the tammar wallaby trophoblast and endometrium prior birth is optimized for rapid embryonic growth during the brief interaction between maternal and fetal cells but the placenta seemingly cannot persist after the designated due time.