Morphological specializations of the yolk sac for yolk processing in embryonic corn snakes (Pantherophis guttatus: Colubridae)

Abstract

Non-avian reptiles commonly are assumed to be like birds in their overall patterns of development. However, colubrid corn snakes (Pantherophis guttatus) have mechanisms of yolk cellularization and processing that are entirely different from the avian pattern. In birds, a vascular "yolk sac" surrounds and digests the liquid yolk. In contrast, in corn snakes, the yolk material is converted into vascularized cords of yolk-filled cells. In this study, we used stereomicroscopy, histology, and scanning electron microscopy to analyze this unusual developmental pattern in corn snakes. Our observations reveal that the yolk sac cavity is invaded by endodermal cells that proliferate, absorb yolk spheres, and form aggregates of interconnected cells within the liquid yolk mass. As development proceeds, small blood vessels arise from the yolk sac omphalopleure, penetrate into the yolk mass, and become tightly encased in the endodermal cells. The entire vitellus ultimately becomes converted into a mass of vascularized, "spaghetti-like" strands of yolk-laden cells. The resulting arrangement allows yolk to be digested intracellularly and yolk products to be transported to the developing embryo. Indirect evidence for this pattern in other species raises the possibility that it is ancestral for squamates and quite possibly Reptilia in general.

A Novel Pattern of Yolk Processing in Developing Snake Eggs (Colubridae: Lampropeltini) and its Functional and Evolutionary Implications

“…First, the granular cells are much smaller than the endodermal cells; second the granular cells never contain yolk droplets; and third, no structural intermediates exist between the two populations. The cells appear to be equivalent to granulocyte‐like cells described in other squamates, including both lizards (Stewart and Florian, ; Stewart et al., ; Stewart and Thompson, ) and snakes (Blackburn et al., ; Powers and Blackburn, ; Stewart and Thompson, ).…”

“…Our observations on the pattern of yolk processing in L. getula and L. triangulum reveal interesting similarities to some other squamates that have been appropriately studied. Not only is this pattern similar to that of the corn snake Pantherophis guttatus (Powers and Blackburn, ), but it appears to resemble that of certain lizards. Sparse information from light microscopy suggests that yolk‐filled endodermal cells surround small blood vessels in the eggs of two oviparous lizards (Romano et al., ; Stewart et al., ) and a viviparous one (Weekes, ) (see Elinson et al., ).…”

“…Recent observations on the corn snake Pantherophis guttatus (Colubridae) have revealed a pattern of yolk sac development that is dramatically different from that of birds (Elinson and Stewart, ; Elinson et al., ; Powers and Blackburn, ). This pattern results in conversion of the yolk material into vascularized, spaghetti‐like strands of yolk‐filled cells.…”

Ultrastructural analysis of the yolk processing pattern in embryonic pond slider turtles (Trachemys scripta: Emydidae)

“…This investigation is part of a research program focused on yolk processing patterns in developing reptile embryos, as called for in a recent review (Elinson et al, ). A subsequent series of papers demonstrated that lizard and snake embryos process yolk for development by an overall pattern that differs from that of birds (Blackburn et al, ; Powers & Blackburn, ; Stewart & Thompson, ). The present study on T. scripta reveals that chelonians have a pattern of yolk processing that is similar or identical to that of squamate reptiles, thereby corroborating preliminary observations on the snapping turtle C. serpentina (Blackburn et al, ).…”

“…Recent research has challenged these assumptions by revealing that some reptiles process yolk for embryonic development very differently than do birds (Elinson & Stewart, ; Elinson, Stewart, Bonneau, & Blackburn, ). Notably, in representative snakes and lizards, the yolk sac cavity becomes filled with a compact meshwork of elongated “spaghetti‐like” strands, each of which consists of yolk‐filled endodermal cells arranged in a monolayer around an anastomosing blood vessel (Blackburn, Lestz, Barnes, Powers, & Langkilde, ; Powers & Blackburn, ; Stewart & Thompson, ). By means of these unusual structures, yolk nutrients are cellularized, digested, and made available for transport back to the embryo.…”