How do embryonic turtles process yolk? Evidence from the Snapping Turtle, Chelydra serpentina (Chelydridae)

Abstract

Compared with amphibians, oviparous reptiles and birds lay large eggs that contain abundant yolk. Because the yolk is extracellular, it must be taken up by cells of the yolk sac and metabolized so that products of yolk digestion can be transported to the embryo to fuel development. In birds, the yolk is processed by cells that line the inside of the yolk sac. A very different developmental pattern recently has been demonstrated in lizards and snakes in which the yolk sac cavity is converted to a compact mass of blood vessels lined by endodermal cells. In this study, we used scanning electron microscopy to determine which of these developmental patterns (if either) occurs in a representative chelonian, the North American Snapping Turtle (Chelydra serpentina (Linnaeus, 1758)). Our observations reveal that yolk-filled endodermal cells progressively fill the yolk sac cavity. These cells become organized around anastomosing blood vessels, forming elongated strands that are morphologically well suited for yolk digestion and vascular transport of nutrients. This developmental pattern shares features with that of squamates, but it differs markedly from that of birds. These observations indicate that mechanisms of yolk processing in lizards and snakes have an evolutionary history that pre-dates the squamate clade.