Morphology, development, and evolution of fetal membranes and placentation in squamate reptiles

Abstract

Current studies on fetal membranes of reptiles are providing insight into three major historical transformations: evolution of the amniote egg, evolution of viviparity, and evolution of placentotrophy. Squamates (lizards and snakes) are ideal for such studies because their fetal membranes sustain embryos in oviparous species and contribute to placentas in viviparous species. Ultrastructure of the fetal membranes in oviparous corn snakes (Pituophis guttatus) shows that the chorioallantois is specialized for gas exchange and the omphalopleure, for water absorption. Transmission and scanning electron microscopic studies of viviparous thamnophine snakes (Thamnophis, Storeria) have revealed morphological specializations for gas exchange and absorption in the intra-uterine environment that represent modifications of features found in oviparous species. Thus, fetal membranes in oviparous species show morphological differentiation for distinct functions that have been recruited and enhanced under viviparous conditions. The ultimate in specialization of fetal membranes is found in viviparous skinks of South America (Mabuya) and Africa (Trachylepis, Eumecia), in which placentotrophy accounts for nearly all of the nutrients for development. Ongoing research on these lizards has revealed morphological specializations of the chorioallantoic placenta through which nutrient transfer is accomplished. In addition, African Trachylepis show an invasive form of implantation, in which uterine epithelium is replaced by invading chorionic cells. Ongoing analysis of these lizards shows how integration of multiple lines of evidence can provide insight into the evolution of developmental and reproductive specializations once thought to be confined to eutherian mammals.

The evolution of viviparity: molecular and genomic data from squamate reptiles advance understanding of live birth in amniotes

“…(Stewart & Thompson 2004. Although they lack a placentome, the highly placentotrophic skinks of the genera Eumecia and Trachylepis appear to transport nutrients across both chorioallantoic and yolk-sac placentae (Flemming & Branch 2001, Blackburn & Flemming 2009). …”

“…The highly placentotrophic Eumecia sp., Mabuya sp., and Trachylepis sp. also appear to transport nutrients across yolk-sac placentae (Flemming & Branch 2001, Jerez & Ramirez-Pinilla 2001, Blackburn & Flemming 2009). In contrast, the genera Eulamprus, Thamnophis, and Virginia are not placentotrophic, which suggests that uterine epithelial hypertrophy in the yolk-sac placenta is not always associated with organic nutrient transport , Thompson et al 2001a.…”

The corn snake yolk sac becomes a solid tissue filled with blood vessels and yolk-rich endodermal cells

“…There are however, significant differences in the extraembryonic membranes of chickens and those of lizards, turtles and snakes [3][4][5]. Most of these investigations have centred on the chorion and allantois, with little attention paid to the yolk sac.…”

Portal hypertension-related inflammatory phenotypes: From a vitelline and amniotic point of view

“…Its acquisition, that is, the "amniotic egg" was one of the main causes that enabled amniotes to escape the bonds that confined their ancestors to aquatic environments [178,188]. If so, it could be proposed that there this is no better method to escape the sea than taking the sea with us, as an amniotic-mesothelial structure full of saline trophic fluid [188,189]. Since this ability would be associated in the post-natal life with mesothelial cells, its major spread through the body is not surprising, coating cavities, i.e.…”