A Novel Pattern of Yolk Processing in Developing Snake Eggs (Colubridae: Lampropeltini) and its Functional and Evolutionary Implications. Issue 5 (24th May 2017)

• Record Type: Journal Article
• Authors: Powers, Kathryn G.; Blackburn, Daniel G.
• Is Part Of: Journal of experimental zoology. Volume 328:Issue 5(2017)
• Page Start: 462
• Page End: 475
• Publication Date: 2017-05-24
• Subjects: Cleavage -- Oviparity -- Reptilia -- Yolk -- Yolk sac; Developmental biology -- Periodicals; Evolution (Biology) -- Periodicals; Molecular evolution -- Periodicals; Zoology -- Periodicals; Evolution, Molecular -- Periodicals; Developmental Biology -- Periodicals; Zoology -- Periodicals; 591
• DOI: 10.1002/jez.b.22750
• Languages: English
• ISSNs: 1552-5007

Abstract

GRAPHICAL ABSTRACT: In lampropeltine snakes, yolk cellularization and provision to the embryo differ dramatically from these processes in birds. Proliferating endodermal cells invade the yolk sac cavity, phagocytose yolk material, and become arranged around invading capillaries. This pattern has significant functional and evolutionary implications. ABSTRACT: 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.