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

Elinson, Richard P.; Stewart, James R.

doi:10.1098/rsbl.2013.0870

Cited by 18 publications

(27 citation statements)

References 13 publications

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“…These hatchlings contrast markedly with the small aquatic larvae that commonly emerge from amphibian eggs. However, the macrolecithal condition of reptiles also required a series of mechanisms by which yolk nutrients could be processed for embryonic use (Elinson, ; Elinson & Stewart, ). In amphibians, cleavage is holoblastic, and yolk material lies within each of the dividing blastomeres from early stages of development onwards.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2019

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Evolution of the large‐yolked, amniotic egg required mechanisms by which extracellular yolk could be made available for embryonic development. In birds, the endodermal lining of the yolk sac absorbs and digests the yolk. In contrast, recent studies on lizards and snakes (squamates) have revealed that yolk is processed by means of a proliferating mass of “spaghetti‐like” strands formed by endodermal cells attached to anastomosing blood vessels. To clarify the method of yolk processing in chelonians, we applied electron microscopy to an extensive series of embryos of the pond slider turtle, Trachemys scripta. Our findings demonstrate that proliferating endodermal cells phagocytose yolk spheres. These cells remain attached to one another following mitosis, thereby forming clumps that progressively occupy the yolk sac cavity. Upon invasion of blood vessels, the cells become organized into elongated, vascularized “spaghetti‐like” strands of cells like those found in squamates. Residual yolk found in the body cavity of new hatchlings chiefly consists of these vascularized strands. Such strands of cells also develop in the false map turtle, Graptemys pseudographica (Emydidae). We infer that the developmental pattern by which yolk is processed is ancestral for both Chelonia and Reptilia, and therefore must have been modified or abandoned in birds or their archosaur ancestors.

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Section: Introductionmentioning

confidence: 99%

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

et al. 2019

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“…The yolk material itself is an extracellular liquid that is contained within the extraembryonic “yolk sac”. This yolk sac must somehow absorb and digest the yolk and send its products to the embryo to fuel its development (Elinson and Stewart, ).…”

Section: Introductionmentioning

confidence: 99%

“…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.…”

Section: Introductionmentioning

confidence: 99%

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

Powers

Blackburn

2017

J Exp Zool Pt B

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Early amniotic vertebrates evolved large-yolked eggs that permitted production of well-developed, terrestrial hatchlings. This reproductive pattern required new mechanisms for cellularizing the yolk and mobilizing it for embryonic use. In birds, cells that line the yolk sac cavity phagocytose and digest the yolk material, a pattern that is commonly assumed to be universal among oviparous amniotes. However, recent evidence challenges the assumption that all squamate reptiles conform to the avian developmental pattern. In this paper, scanning electron microscopy and histology were used to study mechanisms of yolk processing in two colubrid snakes, the kingsnake Lampropeltis getula and the milksnake L. triangulum. Endodermal cells from the yolk sac splanchnopleure proliferate massively as they invade the yolk sac cavity, forming elaborate chains of interlinked cells. These cells grow in size as they phagocytose yolk material. Subsequently, vitelline capillaries invade the masses of yolk-laden cells and become coated with the endodermal cells, forming an elaborate meshwork of cell-coated strands. The close association of cells, yolk, and blood vessels allows yolk material to be cellularized, digested, and transported for embryonic use. The overall pattern is like that of the corn snake Pantherophis guttatus, but contrasts markedly with that of birds. Given recent evidence that this developmental pattern may also occur in certain lizards, we postulate that it is ancestral for squamates. Studies of lizards, crocodilians, and turtles are needed to clarify the evolutionary history of this pattern and its implications for the evolution of the amniotic (terrestrial) vertebrate egg.

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“…That may not be the case. Elinson and Stewart (2014) recently reported that the yolk sac of the corn snake (Pantherophis guttatus) (Colubridae) eventually becomes a mass of spaghetti-like blood vessels coated by large endodermal cells (Fig. 1).…”

Section: B a B C A Yolk Sacs In Reptiles 891mentioning

confidence: 99%

“…A recent discovery that the yolk of the corn snake, Pantherophis guttatus, becomes cellularized and forms a solid, vascularized tissue (Elinson and Stewart, 2014) reveals a dramatic contrast to the development of the yolk sac of the chicken that raises questions regarding appropriate models for the egg of early amniotes. We will consider the relevance of development of the corn snake yolk sac to other squamates, and amniotes generally, and suggest a new scenario for the evolution of the yolk sac of oviparous amniotes.…”

Section: Introductionmentioning

confidence: 99%

Amniote yolk sacs: diversity in reptiles and a hypothesis on their origin

Elinson¹,

Stewart²,

Bonneau³

et al. 2014

Int. J. Dev. Biol.

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Oviparous amniotes produce a large yolky egg that gives rise to a free-living hatchling. Structural characteristics and functional attributes of the egg are best known for birds, which have a large mass of fluid yolk surrounded by an extraembryonic yolk sac. Yolk nutrients are delivered to the embryo via the vascular yolk sac. This developmental pattern and nutrient transport mechanism is thought to be representative of all other lineages of amniotes. Recent discovery of a snake with cellularized yolk organized around a meshwork of blood vessels reveals an additional pattern for yolk mobilization, which may also occur in other squamate reptiles (lizards and snakes). This complex yolk sac raises interesting questions about developmental mechanisms and suggests a possible model for the transition between the egg of anamniotes and that of amniotes.

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

Cited by 18 publications

References 13 publications

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

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

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

Amniote yolk sacs: diversity in reptiles and a hypothesis on their origin

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