Yolk sac development in lizards (Lacertilia: Scincidae): New perspectives on the egg of amniotes

Stewart, James R.; Thompson, Michael B.

doi:10.1002/jmor.20656

Cited by 17 publications

(63 citation statements)

References 34 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…However, these descriptions did not consider the progressive spread of germ layers around the yolk and the timing of its vascularization. For such details, descriptions of many other squamates are available, including both snakes and lizards and oviparous as well as viviparous species (see Stewart, , ; Stewart and Thompson, , ; Blackburn and Stewart, ; Stewart and Blackburn, ). From these studies, a widely‐shared pattern is evident.…”

Section: Discussionmentioning

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

View full text Add to dashboard Cite

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.

show abstract

Section: Discussionmentioning

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

View full text Add to dashboard Cite

show abstract

“…Descriptions with detailed diagrams are widely available (e.g., Blackburn & Stewart, 2011;Stewart, 1985Stewart, , 1990Stewart, , 1993Stewart & Blackburn, 2015;Stewart & Thompson, 2017). Descriptions with detailed diagrams are widely available (e.g., Blackburn & Stewart, 2011;Stewart, 1985Stewart, , 1990Stewart, , 1993Stewart & Blackburn, 2015;Stewart & Thompson, 2017).…”

Section: Early Developmentmentioning

confidence: 99%

“…One hypothesis is that the yolk cleft provides a site for development of small granulocyte-like cells, migratory cells that assist in yolk digestion or that are part of the yolk or embryonic immunity system (Hrabowski, 1926;Stewart & Florian, 2000;Stewart & Thompson, 2017;Stewart et al, 2012). One hypothesis is that the yolk cleft provides a site for development of small granulocyte-like cells, migratory cells that assist in yolk digestion or that are part of the yolk or embryonic immunity system (Hrabowski, 1926;Stewart & Florian, 2000;Stewart & Thompson, 2017;Stewart et al, 2012).…”

Section: Possible Functionsmentioning

confidence: 99%

“…Subsequent research has revealed that a YC-IYM complex does in fact develop in several species of Sceloporus (Anderson et al, 2011;Blackburn et al, 2010;Villagrán, Mendez, & Stewart, 2005;Villagrán Santa Cruz, 1989), and in three species of Liolaemus (Aguilar et al, 2015;Crocco, Ibargüengoytía, & Cussac, 2008). )* Weekes (1927bWeekes ( , 1935 Eulamprus quoyi* Weekes (1927a) Eulamprus (4 species)* Murphy, Brandley, Murphy, and Thompson (2012) Lampropholis guichenoti Stewart and Thompson (2017) Mabuya mabouya* Jerez and Ramírez-Pinilla Acritoscincus ("Bassiana") duperreyi Stewart and Thompson (1996) Carinascincus ("Niveoscincus") (6 species)* Stewart and Thompson (1994, 1998, 2009a Chalcides chalcides* Blackburn and Callard (1997) and Blackburn (1993) C. ocellatus * Corso, Delitala, and Carcupino (2000) and Ibrahim (1977) Egernia (3 spp.…”

Section: Over Squamate Interrelationshipsmentioning

confidence: 99%

“…Morethia adelaidensis Stewart and Thompson (2017) Oligosoma lichenigerum Stewart et al (2012) (Continues) MacAvoy (1976) Plestiodon fasciatus Stewart and Florian (2000) Pseudemoia entrecasteauxii* Thompson (1996, 2009b) and Weekes (1930) P. pagenstecheri* Stewart and Thompson (1996) and Stinnett et al (2012) P. spenceri* Thompson (1998, 2003) Saproscincus mustelinus Stewart and Thompson (2017) Tiliqua (2 spp. )* Weekes (1927bWeekes ( , 1935 Trachylepis vittata* Nassar (2017) Xantusiidae Xantusia vigilis* Stewart and Presch (1992) and Yaron (1985) Anguidae Hrabowski (1926) Elgaria coerulea* Stewart (1985) E. multicarinata Stewart and Mendez de la Cruz (2019) and Stewart (1985) Mesaspis viridiflava* Stewart and Mendez de la Cruz (2019)…”

Section: Over Squamate Interrelationshipsmentioning

confidence: 99%

See 2 more Smart Citations

A developmental synapomorphy of squamate reptiles

Stewart

Blackburn

2019

Evolution and Development

Self Cite

View full text Add to dashboard Cite

The reptilian clade Squamata is defined primarily by osteological synapomorphies, few of which are entirely unambiguous. Studies of developing squamate eggs have revealed a uniquely specialized feature not known to occur in any other amniotes. This feature-the yolk cleft/isolated yolk mass complex-lines the ventral hemisphere of the egg. During its formation, extraembryonic mesoderm penetrates the yolk and an exocoelom (the yolk cleft [YC]) forms in association with it, cutting off a thin segment of yolk (the "isolated yolk mass" [IYM]) from the main body of the yolk. The YC-IYM complex has been observed and described in more than 65 squamate species in 12 families. In viviparous species, it contributes to the "omphaloplacenta," a type of yolk sac placenta unique to squamates. The only squamates known to lack the IYM are a few highly placentotrophic skinks with minuscule eggs, viviparous species in which it clearly has been lost. Given its absence in mammals, chelonians, crocodylians, and birds, the YC-IYM complex warrants recognition as a developmental synapomorphy of the squamate clade. As in extant viviparous lizards and snakes, the YC-IYM complex presumably contributed to the placenta of extinct viviparous squamates. K E Y W O R D Sisolated yolk mass, lizards, snakes, yolk cleft Daniel G. Blackburn and James R. Stewart contributed equally and should be considered joint senior authors.

show abstract

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

et al. 2019

View full text Add to dashboard Cite

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.

show abstract

Yolk sac development in lizards (Lacertilia: Scincidae): New perspectives on the egg of amniotes

Cited by 17 publications

References 34 publications

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

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

A developmental synapomorphy of squamate reptiles

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

Contact Info

Product

Resources

About