The role of mammalian foetal membranes in early embryogenesis: Lessons from marsupials

Abstract

Across mammals, early embryonic development is supported by uterine secretions taken up through the yolk sac and other foetal membranes (histotrophic nutrition). The marsupial conceptus is enclosed in a shell coat for the first two-thirds of gestation and nutrients pass to the embryo through the shell and the avascular bilaminar yolk sac. At around the time of shell rupture, part of the yolk sac is trilaminar and supplied with blood vessels. It attaches to the uterus and forms a choriovitelline placenta. Rapid growth of the embryo ensues, still supported by histotrophe as well as exchange of oxygen and nutrients between maternal and foetal blood vessels (haemotrophic nutrition). Few marsupials have a chorioallantoic placenta and the highly altricial newborn is delivered after a short gestation. Eutherian embryos pass through a similar sequence before there is a fully functional chorioallantoic placenta. In most orders, there is transient yolk sac placentation, but even before this, nutrients are transferred through an avascular yolk sac. Yolk sac placentation does not occur in rodents or catarrhine primates. Early embryonic development in the mouse is nonetheless dependent on histotrophic nutrition. In the first trimester of human pregnancy, uterine glands open to the intervillous space and secretion products are taken up by the trophoblast. Transfer of nutrients to the early human embryo also involves the yolk sac, which floats free in the exocoelom. Marsupials can therefore inform us about the role of foetal membranes and histotrophic nutrition in early embryogenesis, knowledge that can translate to eutherians.