Development of the extraembryonic membranes and histology of the placentae in Virginia striatula (Squamata: Serpentes)

Abstract

Development of the extraembryonic membranes and their structural alignment in the formation of the four placental categories that occur in Virginia striatula is similar to that of other Serpentes. The vascularized trilaminar omphalopleure contacts the uterine epithelium early in development to form the choriovitelline placenta, which subsequently extends over the surface of the yolk to its limit at the margin of the isolated yolk mass. As in other squamates, the isolated yolk mass is separated from the yolk sac by the growth of intravitelline cells into the yolk. The bilaminar omphalopleure (ectoderm, endoderm) of the isolated yolk mass contributes the fetal epithelium of the omphaloplacenta. During formation of the omphidoplacenta, the allantois makes its initial contact with the chorion dorsal to the embryo. As the allantois expands, the chorioallantoic placenta gradually replaces the choriovitelline placenta. The terminal placental stage is defined by an extensive chorioallantoic placenta and an omphalallantoic placenta associated with the isolated yolk mass. Although similar in most aspects to the omphalallantoic placentae of other snakes, a secondary yolk cleft develops in V. striatula. This structure, which separates the outer allantoic membrane from the isolated yolk mass, has not been described in other squamates. The choriovitelline placenta and most of the surface of the chorioallantoic placenta are characterized by close vascular apposition, whereas the omphaloplacenta and omphalallantoic placenta feature uterine and fetal epithelial cell hypertrophy in the absence of fetal vascular support. A narrow zone within the chorioallantoic placenta, lying on either side of the omphalallantoic placenta, contains hypertrophied epithelial cells with supporting capillaries on both fetal and maternal aspects.