Fetal Membrane Ultrastructure and Development in the Oviparous Milksnake Lampropeltis triangulum (Colubridae) with Reference to Function and Evolution in Snakes

J Exp Zool B Mol Dev Evol. 2016 Jul;326(5):290-302. doi: 10.1002/jez.b.22684. Epub 2016 Jul 4.

Abstract

In eggs of oviparous reptiles, fetal membranes maintain developing embryos through the exchange of respiratory gases and provision of water and calcium. As part of a survey of reptilian fetal membranes, we used scanning electron microscopy to study fetal membrane morphology in the oviparous Pueblan milksnake, Lampropeltis triangulum campbelli. The chorioallantois initially is an avascular structure lined by enlarged chorionic and allantoic epithelia. Upon vascularization, the chorionic epithelium becomes greatly attenuated, enhancing the potential for gas exchange; the allantoic epithelium also flattens. The bilaminar omphalopleure of the yolk sac lacks blood vessels, but it becomes vascularized by allantoic capillaries and transformed into an omphalallantois. Upon regression of the isolated yolk mass, this membrane is converted to chorioallantois, equipping it for gas exchange. Allantoic fluid serves as a water reservoir, and we postulate that it facilitates water uptake by establishing an osmotic gradient. Early in development, epithelia of both the chorion and the omphalopleure show apical microvilli that greatly increase the cell surface area available for water uptake. However, these features are incompatible with gas exchange and are lost as oxygen needs take precedence. A comparison of the fetal membranes to those of other squamate species (both oviparous and viviparous) reveals characteristics that are probably ancestral for snakes, some of which are plesiomorphic for Squamata. The widespread phylogenetic distribution of these features reflects their utility as adaptations that serve functional requirements of squamate embryos.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Allantois / embryology
  • Allantois / ultrastructure
  • Animals
  • Biological Evolution
  • Chorioallantoic Membrane / blood supply
  • Chorioallantoic Membrane / embryology
  • Chorioallantoic Membrane / ultrastructure*
  • Colubridae / embryology*
  • Extraembryonic Membranes / embryology
  • Extraembryonic Membranes / ultrastructure*
  • Oviparity
  • Ovum / growth & development
  • Ovum / ultrastructure
  • Yolk Sac / embryology
  • Yolk Sac / ultrastructure