Yolk sac placentation in reptiles: Structural innovation in a fundamental vertebrate fetal nutritional system

Abstract

AbstractThe extraembryonic membranes of amniote vertebrates are shared structures that have a brief, yet substantive role in the ontogeny of the organism. The yolk sac, which is the first of these structures to develop, has an important function in regulation and mobilization of nourishment to embryos of oviparous species and additionally contributes to maternal‐fetal exchange in many viviparous species. Yolk sac placentation has been described in all major taxa of viviparous amniotes. The yolk sac of viviparous reptiles contributes to three categories of placentation, the choriovitelline placenta, which also occurs in marsupial and eutherian mammals, and the omphaloplacenta and omphalallantoic placenta, which occur only among squamate reptiles (lizards and snakes). The fetal contribution to the omphaloplacenta includes a structure termed the isolated yolk mass, which forms in all Squamata independent of reproductive mode, and is produced by a morphogenesis of extraembryonic mesoderm that is unique to this reptilian order. For some viviparous squamates, the allantois contributes to the inner margin of the isolated yolk mass and this structural arrangement constitutes the omphalallantoic placenta. The isolated yolk mass is bordered externally by a bilaminar omphalopleure. Epithelial cells of the bilaminar omphalopleure of the omphaloplacenta and omphalallantoic placenta are hypertrophied. The apposed uterine epithelium likewise contains enlarged cuboidal or columnar shaped cells and the underlying lamina propria is richly vascularized. This epithelial cell structure suggests that the region of the isolated yolk mass is a site of placental specialization in viviparous reptiles. Further, since these features of omphaloplacentation or omphalallantoic placentation commonly occur in species without apparent morphological specialization in other areas of fetal‐uterine contact, it is likely that the bilaminar omphalopleure of the isolated yolk mass is evolutionarily the initial site of placental specialization among viviparous reptiles. © 1993 Wiley‐Liss, Inc.