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Developmental Morphology and Evolution of Extraembryonic Membranes of Lizards and Snakes (Reptilia, Squamata)Stewart, James R. 01 July 2021 (has links)
Amniote embryos are supported and nourished by a suite of tissues, the extraembryonic membranes, that provide vascular connections to the egg contents. Oviparous reptiles share a basic pattern of development inherited from a common ancestor; a vascular chorioallantoic membrane, functioning as a respiratory organ, contacts the eggshell and a vascular yolk sac membrane conveys nutrients to the embryo. Squamates (lizards, snakes) have evolved a novel variation in morphogenesis of the yolk sac that results in a unique structure, the yolk cleft/isolated yolk mass complex. This structure is a source of phylogenetic variation in architecture of the extraembryonic membranes among oviparous squamates. The yolk cleft/isolated yolk mass complex is retained in viviparous species and influences placental architecture. The aim of this paper is to review extraembryonic membrane development and morphology in oviparous and related viviparous squamates to explore patterns of variation. The survey includes all oviparous species for which data are available (11 species; 4 families). Comparisons with viviparous species encompass six independent origins of viviparity. The comparisons reveal that both phylogeny and reproductive mode influence variation in extraembryonic membrane development and that phylogenetic variation influences placental evolution. Models of the evolution of squamate placentation have relied primarily on comparisons between independently derived viviparous species. The inclusion of oviparous species in comparative analyses largely supports these models, yet exposes convergent patterns of evolution that become apparent when phylogenetic variation is recognized.
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Developmental Morphology and Evolution of Extraembryonic Membranes of Lizards and Snakes (Reptilia, Squamata)Stewart, James R. 01 January 2020 (has links)
Amniote embryos are supported and nourished by a suite of tissues, the extraembryonic membranes, that provide vascular connections to the egg contents. Oviparous reptiles share a basic pattern of development inherited from a common ancestor; a vascular chorioallantoic membrane, functioning as a respiratory organ, contacts the eggshell and a vascular yolk sac membrane conveys nutrients to the embryo. Squamates (lizards, snakes) have evolved a novel variation in morphogenesis of the yolk sac that results in a unique structure, the yolk cleft/isolated yolk mass complex. This structure is a source of phylogenetic variation in architecture of the extraembryonic membranes among oviparous squamates. The yolk cleft/isolated yolk mass complex is retained in viviparous species and influences placental architecture. The aim of this paper is to review extraembryonic membrane development and morphology in oviparous and related viviparous squamates to explore patterns of variation. The survey includes all oviparous species for which data are available (11 species; 4 families). Comparisons with viviparous species encompass six independent origins of viviparity. The comparisons reveal that both phylogeny and reproductive mode influence variation in extraembryonic membrane development and that phylogenetic variation influences placental evolution. Models of the evolution of squamate placentation have relied primarily on comparisons between independently derived viviparous species. The inclusion of oviparous species in comparative analyses largely supports these models, yet exposes convergent patterns of evolution that become apparent when phylogenetic variation is recognized.
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Yolk Sac Development in Lizards (Lacertilia: Scincidae): New Perspectives on the Egg of AmniotesStewart, James R., Thompson, Michael B. 01 April 2017 (has links)
Embryos of oviparous reptiles develop on the surface of a large mass of yolk, which they metabolize to become relatively large hatchlings. Access to the yolk is provided by tissues growing outward from the embryo to cover the surface of the yolk. A key feature of yolk sac development is a dedicated blood vascular system to communicate with the embryo. The best known model for yolk sac development and function of oviparous amniotes is based on numerous studies of birds, primarily domestic chickens. In this model, the vascular yolk sac forms the perimeter of the large yolk mass and is lined by a specialized epithelium, which takes up, processes and transports yolk nutrients to the yolk sac blood vessels. Studies of lizard yolk sac development, dating to more than 100 years ago, report characteristics inconsistent with this model. We compared development of the yolk sac from oviposition to near hatching in embryonic series of three species of oviparous scincid lizards to consider congruence with the pattern described for birds. Our findings reinforce results of prior studies indicating that squamate reptiles mobilize and metabolize the large yolk reserves in their eggs through a process unknown in other amniotes. Development of the yolk sac of lizards differs from birds in four primary characteristics, migration of mesoderm, proliferation of endoderm, vascular development and cellular diversity within the yolk sac cavity. Notably, all of the yolk is incorporated into cells relatively early in development and endodermal cells within the yolk sac cavity align along blood vessels which course throughout the yolk sac cavity. The pattern of uptake of yolk by endodermal cells indicates that the mechanism of yolk metabolism differs between lizards and birds and that the evolution of a fundamental characteristic of embryonic nutrition diverged in these two lineages. Attributes of the yolk sac of squamates reveal the existence of phylogenetic diversity among amniote lineages and raise new questions concerning the evolution of the amniotic egg. J. Morphol. 278:574–591, 2017. © 2017 Wiley Periodicals, Inc.
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Amniote Yolk Sacs: Diversity in Reptiles and a Hypothesis on Their OriginElinson, Richard P., Stewart, James R., Bonneau, Laurie J., Blackburn, Daniel G. 08 July 2014 (has links)
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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Embryonic Mobilization of Calcium in a Viviparous Reptile: Evidence for a Novel Pattern of Placental Calcium SecretionFregoso, Santiago P., Stewart, James R., Ecay, Tom W. 01 January 2010 (has links)
Yolk reserves supply the majority of embryonic nutrition in squamate reptiles, including calcium. Embryos of oviparous squamates exploit the eggshell for supplemental calcium, while embryos of viviparous species may receive additional calcium via the placenta. Developmental uptake of calcium in oviparous snakes increases during the interval of greatest embryonic growth (stage 35 to parturition). However, the pattern of embryonic calcium acquisition is unknown for viviparous snakes. Furthermore, while the uterus of oviparous species transports calcium early in embryonic development during mineralization of the eggshell, the timing of uterine calcium secretion in viviparous snakes is unknown. We studied a viviparous snake, Virginia striatula, to determine the ontogenetic pattern of yolk and embryonic calcium content. The pattern of embryonic calcium uptake of V. striatula is similar to that of oviparous snakes but the sources of calcium differ. In contrast to oviparous species, embryos of V. striatula acquire half of total neonatal calcium via placental provision, of which 71% is mobilized between stage 35 and parturition. Furthermore, we report for the first time in a viviparous squamate an increase in yolk calcium content during early stages of embryonic development, indicating that uterine secretion of calcium occurs in V. striatula coincident with shelling in oviparous squamates. Thus, uterine calcium secretion in this viviparous species may either occur continuously or in two phases, coincident with the timing of shelling in oviparous species and again during the last stages of development. Whereas, the pattern of embryonic calcium acquisition in V. striatula is plesiomorphic for squamates, the pattern of uterine calcium secretion includes both retention of a plesiomorphic trait and the evolution of a novel trait.
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Development of the Uterine Shell Glands During the Preovulatory and Early Gestation Periods in Oviparous and Viviparous Lacerta ViviparaHeulin, Benoit, Stewart, James R., Surget-Groba, Yann, Bellaud, Patricia, Jouan, Florence, Lancien, Gérard, Deunff, Jean 01 October 2005 (has links)
The evolutionary process leading to the emergence of viviparity in Squamata consists of lengthening the period of egg retention in utero coupled with marked reduction in the thickness of the eggshell. We used light microscopy and scanning electron microscopy to study uterine structure during the reproductive cycle of oviparous and viviparous females of the reproductively bimodal Lacerta vivipara. We compared the structure of the uterine shell glands, which secrete components of the eggshell, during preovulatory and early gestation phases of the reproductive cycle and also compared histochemistry of the eggshells. The uterine glands of both reproductive forms undergo considerable growth within a period of a few weeks during folliculogenesis and vitellogenesis preceding ovulation. The majority of the proteinaceous fibers of the shell membrane are secreted early in embryonic development and the uterine glands regress shortly thereafter. This supports previous observations indicating that, in Squamata, secretion of the shell membrane occurs very rapidly after ovulation. The most striking differences between reproductive modes were larger uterine glands at late vitellogenesis in oviparous females, 101 μm compared to 60 μm in viviparous females, and greater thickness of the shell membrane during early gestation in oviparous females (52-73 μm) compared to viviparous females (4-8 μm). Our intraspecific comparison supports the conclusions of previous studies that, prior to ovulation, the uterine glandular layer is less developed in viviparous than in oviparous species, and that this is the main factor accounting for differences in the thickness of the shell membrane of the two reproductive forms of squamates.
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Facultative Mobilization of Eggshell Calcium Promotes Embryonic Growth in an Oviparous SnakeStewart, James R., Pyles, Rebecca A., Mathis, Kaitlyn A., Ecay, Tom W. 01 February 2019 (has links)
The mineralized eggshell of Reptilia was a major innovation in the evolution of the amniotic egg. Inorganic components strengthen the eggshell and are a potential source of nutrients to developing embryos. Embryos of oviparous reptiles do extract calcium from eggshells but vary interspecifically in exploitation of this resource. The pattern of embryonic calcium nutrition of the corn snake, Pantherophis guttatus, is similar to a diversity of squamate species: embryos obtain most calcium from yolk, yet also mobilize calcium from the eggshell. We tested the hypothesis that embryonic development is not dependent on eggshell calcium by manipulating calcium availability. We peeled away the outer calcareous layer of the eggshell of recently oviposited eggs; control eggs were left intact. Eggs were sampled periodically and calcium content of egg compartments (embryo, yolk, eggshell) was measured. We also analyzed skeletal development and size of hatchlings. There was no difference in survivorship or length of incubation between treatments. However, hatchlings from intact eggs contained more calcium and were larger in mass and length than siblings from peeled eggs. There were no observable differences in ossification but hatchlings from intact eggs had larger skeletal elements (skull, vertebrae). Our results indicate that mobilization of eggshell calcium is not a requirement for embryonic development of P. guttatus and that embryos augment yolk calcium by extracting calcium from the eggshell. This pattern of embryonic calcium nutrition would favor embryos with a greater capacity to mobilize calcium from the eggshell by promoting growth and thereby potentially enhancing hatchling fitness.
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Development of Yolk Sac and Chorioallantoic Membranes in the Lord Howe Island Skink, Oligosoma LichenigerumStewart, James R., Russell, Kylie J., Thompson, Michael B. 01 October 2012 (has links)
Development of the yolk sac of squamate reptiles (lizards and snakes) differs from other amniote lineages in the pattern of growth of extraembryonic mesoderm, which produces a cavity, the yolk cleft, within the yolk. The structure of the yolk cleft and the accompanying isolated yolk mass influence development of the allantois and chorioallantoic membrane. The yolk cleft of viviparous species of the Eugongylus group of scincid lizards is the foundation for an elaborate yolk sac placenta; development of the yolk cleft of oviparous species has not been studied. We used light microscopy to describe the yolk sac and chorioallantoic membrane in a developmental series of an oviparous member of this species group, Oligosoma lichenigerum. Topology of the extraembryonic membranes of late stage embryos differs from viviparous species as a result of differences in development of the yolk sac. The chorioallantoic membrane encircles the egg of O. lichenigerum but is confined to the embryonic hemisphere of the egg in viviparous species. Early development of the yolk cleft is similar for both modes of parity, but in contrast to viviparous species, the yolk cleft of O. lichenigerum is transformed into a tube-like structure, which fills with cells. The yolk cleft originates as extraembryonic mesoderm is diverted from the periphery of the egg into the yolk sac cavity. As a result, a bilaminar omphalopleure persists over the abembryonic surface of the yolk. The bilaminar omphalopleure is ultimately displaced by intrusion of allantoic mesoderm between ectodermal and endodermal layers. The resulting chorioallantoic membrane has a similar structure but different developmental history to the chorioallantoic membrane of the embryonic hemisphere of the egg.
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Patterns of Maternal Provision and Embryonic Mobilization of Calcium in Oviparous and Viviparous Squamate ReptilesStewart, James R., Ecay, Tom W. 29 October 2010 (has links) (PDF)
Embryos of oviparous squamate reptiles obtain all organic and most inorganic nutrients from yolk; yolk provides 19-86% of hatchling calcium content. The remaining calcium is extracted from the eggshell. Yolk calcium provision to viviparous embryos also is variable and includes three patterns. The contribution of yolk to embryonic development for most viviparous squamates is similar to oviparous species, but the attenuated eggshell of viviparous species is a poor source of calcium because it lacks an outer layer of calcium carbonate, and embryos supplement yolk calcium via placental transfer. In a second pattern, yolk provides all organic nutrients and calcium. The final pattern occurs in viviparous species that are substantially placentotrophic and placental transfer accounts for most organic and inorganic nutrients, including calcium. The many independent evolutionary transitions to viviparity among squamates have inspired interest in a possible link to patterns of embryonic calcium nutrition. A prominent model predicts that the pattern of maternal provision and embryonic uptake of calcium unique to squamates facilitates the evolution of viviparity. A primary assumption of the model is that the evolution of viviparity precedes the evolution of calcium placentotrophy. An alternative model predicts that viviparity and placentotrophy evolve concurrently because mechanisms for nutrient provision and mobilization are not dependent on reproductive mode. These hypotheses have not been tested directly but review of the literature indicates that neither fully explains the diversity of squamate embryonic calcium nutrition. Viviparous species differ from oviparous species primarily in the timing of uterine calcium secretion and structure of eggshell calcium. Future studies should focus on the mechanisms that promote these differences.
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Placental Calcium Provision in a Lizard With Prolonged Oviductal Egg RetentionLinville, Brent J., Stewart, James R., Ecay, Tom W., Herbert, Jacquie F., Parker, Scott L., Thompson, Michael B. 01 January 2010 (has links)
A prominent scenario for the evolution of viviparity and placentation in reptiles predicts a step-wise pattern with an initial phase of prolonged oviductal egg retention accompanied by progressive reduction in eggshell thickness culminating in viviparity; calcium placentotrophy evolves secondarily to viviparity. Saiphos equalis is an Australian scincid lizard with a reproductive mode that is uncommon for squamates because eggs are retained in the oviduct until late developmental stages, and the embryonic stage at oviposition varies geographically. We studied calcium mobilization by embryos in two populations with different oviductal egg retention patterns to test the hypothesis that the pattern of nutritional provision of calcium is independent of the embryonic stage at oviposition. Females from one population are viviparous and oviposit eggs containing fully formed embryos, whereas embryos in oviposited eggs of the second population are morphologically less mature, and these eggs hatch several days later. The reproductive mode of this population is denoted as prolonged oviductal egg retention. Yolk provided the highest proportion of calcium to hatchlings in both populations. Eggs of both populations were enclosed in calcified eggshells, but shells of the population with prolonged egg retention had twice the calcium content of the viviparous population and embryos recovered calcium from these eggshells. Placental transfer accounted for a substantial amount of calcium in hatchlings in both populations. Hatchling calcium concentration was higher in the population with prolonged egg retention because these embryos mobilized calcium from yolk, the eggshell and the placenta. This pattern of embryonic calcium provision in which both a calcified eggshell and placentotrophy contribute to embryonic nutrition is novel. The reproductive pattern of S. equalis illustrates that calcified eggshells are compatible with prolonged oviductal egg retention and that viviparity is not requisite to calcium placentotrophy.
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