Scanning electron microscopy of the placental interface in the viviparous lizard Sceloporus jarrovi (Squamata: Phrynosomatidae)

Placental membranes mediate maternal‐fetal exchange in all viviparous reptilian sauropsids. We used scanning electron microscopy to examine the placental interface in the mountain spiny lizard, Sceloporus jarrovi (Phrynosomatidae). From the late limb bud stage until birth, the conceptus is surrounded by placental membranes formed from the chorioallantois and yolk sac omphalopleure. The chorioallantois lies directly apposed to the uterine lining with no intervening shell membrane. Both fetal and maternal sides of the chorioallantoic placenta are lined by continuous layers of flattened epithelial cells that overlie dense capillary networks. The chorioallantoic placenta shows specializations that enhance respiratory exchange, as well as ultrastructural evidence of maternal secretion and fetal absorption. The yolk sac placenta contains enlarged fetal and maternal epithelia with specializations for histotrophic nutrient transfer. This placenta lacks intrinsic vascularity, although the vascular allantois lies against its inner face, contributing to an omphallantoic placenta. In a specialized region at the abembryonic pole, uterine and fetal tissues are separated by a compact mass of shed shell membrane, yolk droplets, and cellular debris. The omphalopleure in this region develops elongate folds that may contribute to sequestration and absorption of this material. Fetal membrane morphogenesis and composition in S. jarrovi are consistent with those of typical squamates. However, this species exhibits unusual placental specializations characteristic of highly placentotrophic lizards. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Morphology, development, and evolution of fetal membranes and placentation in squamate reptiles

Current studies on fetal membranes of reptiles are providing insight into three major historical transformations: evolution of the amniote egg, evolution of viviparity, and evolution of placentotrophy. Squamates (lizards and snakes) are ideal for such studies because their fetal membranes sustain embryos in oviparous species and contribute to placentas in viviparous species. Ultrastructure of the fetal membranes in oviparous corn snakes (Pituophis guttatus) shows that the chorioallantois is specialized for gas exchange and the omphalopleure, for water absorption. Transmission and scanning electron microscopic studies of viviparous thamnophine snakes (Thamnophis, Storeria) have revealed morphological specializations for gas exchange and absorption in the intra-uterine environment that represent modifications of features found in oviparous species. Thus, fetal membranes in oviparous species show morphological differentiation for distinct functions that have been recruited and enhanced under viviparous conditions. The ultimate in specialization of fetal membranes is found in viviparous skinks of South America (Mabuya) and Africa (Trachylepis, Eumecia), in which placentotrophy accounts for nearly all of the nutrients for development. Ongoing research on these lizards has revealed morphological specializations of the chorioallantoic placenta through which nutrient transfer is accomplished. In addition, African Trachylepis show an invasive form of implantation, in which uterine epithelium is replaced by invading chorionic cells. Ongoing analysis of these lizards shows how integration of multiple lines of evidence can provide insight into the evolution of developmental and reproductive specializations once thought to be confined to eutherian mammals.     

Histology of the late-stage placentae in the matrotrophic skink Chalcides chalcides (Lacertilia; Scincidae)

Examination of late-stage placental material of the lizard Chalcides chalcides from the Hubrecht Laboratorium (Utrecht, The Netherlands) reveals several cytological and histological specializations that appear to have been superimposed over a morphological pattern that is typical for squamates. The chorioallantoic placenta is highly vascularized and consists of a single mesometrial placentome and a generalized paraplacentomal region, both of which are epitheliochorial. The placentome is deciduate, and contains deeply interdigitating folds of hypertrophied uterine and chorioallantoic tissue. Chorionic epithelium lining the placentome comprises enlarged, microvilliated cells, a small proportion of which are diplokaryocytes. The placentomal uterine epithelium is not syncytial and consists of enlarged cells bearing microvilli. The yolk sac placenta is a true omphaloplacenta (sensu stricto), being formed by juxtaposition of uterine tissues to an avascular, bilaminar omphalopleure. Epithelium of the omphalopleure is stratified and is hypertrophied into papillae that project into detritus of the uterine lumen. The omphalopleure is separated from the yolk sac proper by a yolk cleft that is not confluent with the exocoelom and is not invaded by the allantois. Neither an omphalallantoic placenta nor a true choriovitelline placenta is present in late gestation. Morphologically, the mature placentae of C. chalcides are among the most specialized to have been described in reptiles, reflecting the substantial maternal-fetal nutrient transfer that occurs in this species. © 1993 Wiley-Liss, Inc.     

Placentation in garter snakes: scanning EM of the placental membranes of Thamnophis ordinoides and T. sirtalis

Surface topography and cross-sections of the placental membranes were examined by scanning electron microscopy in two species of Thamnophis. The chorionic epithelium of the chorioallantoic placenta consists of broad, squamous cells that lack surface specializations. The apposed uterine epithelium contains ciliated cells and larger, nonciliated cells. Neither the epithelium of the chorion nor that of the uterus is eroded; thus, underlying capillaries are not exposed to the luminal surface. In both the omphaloplacenta and the omphalallantoic placenta, epithelium of the omphalopleure consists of brush-border cells bearing prominent microvilli, interspersed with cells bearing minuscule microvilli. These surface epithelial cells are joined at their apices and their lateral surfaces are extensively sculpted by intercellular channels, presenting the appearance of an epithelium specialized for absorption. Deep to the epithelium lie the yolk spheres of the isolated yolk mass, interspersed with endodermal cells. Surface topography of the uterine epithelia of the omphaloplacenta and omphalallantoic placenta is relatively unspecialized. The acellular shell membrane separates maternal and fetal tissues in each of the three placental types. Marked differences in surface features of the chorioallantois and omphalopleure probably reflect different roles of these membranes in gas exchange and transfer of water and nutrients.     

Placentation in garter snakes. III. Transmission EM of the omphalallantoic placenta of Thamnophis radix and T. sirtalis

The omphalallantoic placenta is a complex organ that is unique to viviparous squamates. Using transmission EM and light microscopy, we examined this placenta in garter snakes in order to understand its structural organization and functional capabilities. The omphalallantoic placenta is formed from the uterine lining and the bilaminar omphalopleure, the latter of which is associated with the isolated yolk mass and allantois. A thin shell membrane separates the fetal and maternal tissues throughout gestation. The uterine epithelium contains cuboidal cells with large droplets or granules and appears to be secretory. Epithelium of the omphalopleure is specialized for absorption and contains cells with prominent microvilli and others with large cytoplasmic droplets or granules. The brush-border cells are rich in mitochondria and Golgi bodies and interdigitate extensively with adjacent cells, forming elaborate intercellular canaliculi. Their morphology is consistent with their proposed role in sodium-coupled water movement. During development, the isolated yolk mass becomes depleted as yolk droplets are digested by cells of the omphalopleure and allantois. However, the allantois does not fuse to or vascularize the inner face of the omphalopleure. Consequently, the distance between fetal and maternal circulatory systems remains large (about 250-300 microm), precluding efficient gas exchange and hemotrophic transfer. The morphology of the omphalallantoic placenta strongly suggests that it functions in nutrient transfer through uterine secretion and fetal absorption.     

Histology and ultrastructure of the placental membranes of the viviparous brown snake,Storeria dekayi (Colubridae: Natricinae)

The placental membranes of the viviparous brown snake Storeria dekayi were examined following mid‐gestation by means of light microscopy, scanning electron microscopy, and transmission electron microscopy to reveal their structural organization and cytological composition. By Zehr stage 32, the chorioallantoic placenta (allantoplacenta) is established around much of the egg, and a well‐developed omphalallantoic placenta occurs in the abembryonic hemisphere. The allantoplacenta exhibits multiple features that enhance interhemal exchange: the uterus and allantois are well vascularized, the chorionic and uterine epithelia are attenuated, and the shell membrane is vestigial and has begun to degenerate. In the omphalallantoic placenta, the uterine epithelium is enlarged and appears to be secretory. The omphalopleure contains two distinct populations of cells, and shows cytological evidence for absorption. In intermediate areas, regions of omphalallantoic placenta are being transformed into allantoplacenta, through depletion of the isolated yolk mass and reduction in epithelial height of both uterus and omphalopleure. Morphological evidence suggests that the allantoplacenta is specialized for gas exchange, and the omphalallantoic placenta, for maternal secretion and fetal absorption. On the basis of the available evidence, we postulate that this pattern is characteristic of the thamnophine radiation of snakes. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

Placentation in watersnakes II: Placental ultrastructure in Nerodia erythrogaster (Colubridae: Natricinae)

Ultrastructure of the placental tissues from redbelly watersnakes (Nerodia erythrogaster ) was analyzed during late pregnancy to provide insight into placental development and function. Examination of the chorioallantoic placenta with transmission electron microscopy reveals that chorionic and uterine epithelia are extremely attenuated but intact and that the eggshell membrane is vestigial and lacks a calcareous layer. These features minimize the interhemal diffusion distance across the placenta. Scanning electron microscopy reveals that fetal and maternal components of the placentas are richly vascularized by dense networks of capillaries. Although the yolk sac omphalopleure has largely been replaced by chorioallantois by late gestation, it retains patches of yolk droplets and regions of absorptive cells with microvilli and abundant mitochondria. Transmission electron microscopy reveals that yolk material is taken up for digestion by endodermal cells. As yolk is removed, allantoic capillaries invade to occupy positions just beneath the epithelium, forming regions of chorioallantoic placentation. Ultrastructural features indicate that the chorioallantoic placenta is specialized for gas exchange, while the omphalallantoic (“yolk sac”) placenta shows evidence of functions in yolk digestion and maternal‐fetal nutrient transfer. Placental features of this species are consistent with those of other thamnophines, and are evolutionarily convergent on snakes of other viviparous clades.     

Placentation in watersnakes I: Placental histology and development in North American Nerodia (Colubridae: Natricinae)

As part of a broad survey of placental structure, function, and evolution in reptilian sauropsids paraffin‐section histology was used to study microscopic anatomy of the uterus and fetal membranes of three species of North American watersnakes (Nerodia : Colubridae). The pre‐ovulatory uterus is poorly vascularized with inactive shell glands. These shell glands are activated during vitellogenesis but regress during pregnancy. Two placentas develop through apposition of the uterine lining to the chorioallantois and the yolk sac omphalopleure. Fetal and maternal components of the chorioallantoic placenta are progressively vascularized during development. Their epithelia are attenuated, but (contrary to a previous report), epithelia of neither the uterus nor the chorion are eroded. The fetal portion of the yolk sac placenta is an omphalallantois, formed of avascular omphalopleure, isolated yolk mass, and allantois. This placenta is progressively replaced by chorioallantoic placenta during mid‐ to late‐development through depletion of the isolated yolk mass. The chorioallantoic placenta is anatomically specialized for maternal–fetal gas exchange, and its expansion during development reflects the growing needs of the fetus for gas exchange. The yolk sac placenta is morphologically unsuited for gas exchange, but may serve other functions in maternal‐fetal exchange.     

Scanning electron microscopy of the fetal membranes of an oviparous squamate,the corn snake Pituophis guttatus (Colubridae)

Although the fetal membranes of viviparous squamates have received much study, morphology of their homologues among oviparous reptiles is poorly understood. The scarcity of information about these membranes in egg‐laying reptiles hampers attempts to distinguish specializations for viviparity from ancestral oviparous features. We used scanning electron microscopy to examine fetal membranes of an oviparous snake (Pituophis guttatus) throughout the developmental period from oviposition to hatching. The external surface of the chorion contains broad, flattened cells that lack surface features; these cells form a continuous layer over the allantoic capillaries and offer a minimal barrier to respiratory exchange. In contrast, the surface epithelium of the omphalopleure bears elaborate surface ridges suggestive of absorptive capabilities. These ridges are prominent in the first few weeks after oviposition, but diminish thereafter. During development, the isolated yolk mass (IYM) of the omphalopleure becomes depleted, and the tissue becomes heavily vascularized by allantoic vessels. Surface features of the omphalopleure progressively take on the appearance of the chorioallantois, but the changes are not synchronous with loss of the IYM or membrane vascularization. Previous studies on viviparous snakes suggest that the chorioallantois and omphalopleure are respectively specialized for gas exchange and absorption in the intrauterine environment. Our studies of fetal membranes in P. guttatus offer evidence that cytological specializations for these functions originated under oviparous conditions, reflecting functional capacities that predate viviparity. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Ultrastructure of the fetal membranes of the oviparous kingsnake,Lampropeltis getula (Colubridae) as revealed by scanning electron microscopy

In reptilian sauropsids, fetal (extraembryonic) membranes that line the eggshell sustain developing embryos by providing for gas exchange and uptake of water and eggshell calcium. However, a scarcity of morphological studies hinders an understanding of functional specializations and their evolution. In kingsnakes (Lampropeltis getula), scanning electron microscopy reveals two major fetal membranes: the chorioallantois and yolk sac omphalopleure. In early development, the chorioallantois contains tall chorionic epithelial cells, avascular connective tissue, and enlarged allantoic epithelial cells. During its maturation, the chorionic and allantoic epithelia thin dramatically and become underlain by a rich network of allantoic capillaries, yielding a membrane ideally suited for respiratory gas exchange. Yolk sac development initially is like that of typical lizards and snakes, forming an avascular omphalopleure, isolated yolk mass (IYM), and yolk cleft. However, unlike the situation in most squamates studied, the omphalopleure becomes transformed into a “secondary chorioallantois” via three asynchronous events: flattening of the epithelium, regression of the IYM, and vascularization by the allantois. Progressive expansion of chorioallantois parallels growing embryonic needs for gas exchange. In early through mid‐development, external surfaces of both the chorionic and omphalopleure epithelium show an abundance of irregular surface protrusions that possibly increase surface area for water absorption. We postulate that the hypertrophied allantoic epithelial cells produce allantoic fluid, a viscous substance that facilitates water uptake and storage. Our findings are consistent with a previous study on the corn snake Pantherophis guttatus, but include new observations and novel functional hypotheses relevant to a reconstruction of basal squamate patterns. J. Morphol. 276:1467–1481, 2015. © 2015 Wiley Periodicals, Inc.     

Allantoplacental ultrastructure of an Andean population of Mabuya (Squamata, Scincidae)

Mabuya species are highly matrotrophic viviparous lizards with Type IV epitheliochorial allantoplacenta. The allantoplacenta of an Andean population of this genus, currently assigned to Mabuya sp., possesses specializations related to histotrophic nutrition at the embryonic hemisphere (placentome, paraplacentome, and chorionic areolas), while at the abembryonic hemisphere it has a mixed function: histotrophic transfer (absorptive plaques) and hemotrophic nutrition (gas exchange in respiratory segments). These placental specializations were studied using high-resolution light microscopy and transmission electron microscopy, and were compared with those found in other squamate reptiles and eutherian mammals. Cytological features of the placentome suggest that this is an important region for nutritional provision; the paraplacentome also shows characteristics for nutrient transfer, especially lipids. Chorionic areolas allow the absorption of glandular products, as well as uterine and chorionic cellular debris produced by lysis of some cells of both epithelia during areola formation. In the absorptive plaques both uterine and chorionic epithelia are firmly attached and their cellular apices exhibit electron-dense granules that could be related to autocrine and paracrine functions. The short interhemal distance found in the respiratory segments confirms their role in gas exchange. A common feature of all regional specializations in the Mabuya sp. allantoplacenta is the presence of lipids in the interacting chorionic and uterine epithelia, suggesting that lipids are transferred throughout the entire embryonic chamber; placental transfer of lipids may be the principal fetal energy and lipid source in this species. In spite of this feature, each one of the specialized areas of the allantoplacenta has different features suggesting particular functions in the transfer of nutrients (as ions, lipids, proteins, amino acids, sugar, water, and gases), and in the possible synthesis of hormones and proteins. The placental complexity observed in this species of Mabuya is greater than in any other reptile, and resembles that of eutherian mammals: Each one of these specializations of the placental membranes in Mabuya sp. is similar to those found among different eutherian mammals, indicating a very impressive evolutionary convergence at the histological and cytological levels between both clades. However, no eutherian mammal species simultaneously displays all of these specializations in the embryonic chamber as does Mabuya sp.     

Placentation in the lizard Gerrhonotus coeruleus with a comparison to the extraembryonic membranes of the oviparous Gerrhonotus multicarinatus (Sauria,Anguidae)

Paraffin sections of an ontogenetic series of embryos of the viviparous lizard Gerrhonotus coeruleus and the oviparous congener G. multicarinatus reveal that although general features of the development of the chorioallantoic and yolk sac membranes are similar, differences are evident in the distribution of the chorioallantoic membrane in late stage embryos. An acellular shell membrane surrounds the egg throughout gestation in both species although the thickness of this structure is much reduced in G. coeruleus over that of G. multicarinatus. The initial vascular membrane to contact the shell membrane in both species is a trilaminar omphalopleure (choriovitelline membrane) composed of ectoderm, mesoderm of the area vasculosa, and endoderm. This transitory membrane is replaced by the vascularized chorioallantois as the allantois expands to contact the inner surface of the chorion. Prior to the establishment of the chorioallantois at the embryonic pole, a membrane begins to form within the yolk ventral to the sinus terminalis. This membrane, which becomes vascularized, extends across the entire width of the abembryonic region and isolates a mass of yolk ventral to the yolk mass proper. The outer membrane of the yolk pole is a nonvascular bilaminar omphalopleure (chorionic ectoderm and yolk endoderm). In G. multicarinatus the bilaminar omphalopleure is supported internally by the vascularized allantoic membrane, whereas in G. coeruleus the allantois does not extend beyond the margin of the isolated yolk mass and the bilaminar omphalopleure is supported by the vascularized intravitelline membrane. Both the chorioallantoic placenta (uterine epithelium, chorionic ectoderm and mesoderm, and allantoic mesoderm and endoderm) and the yolk sac placenta at the abembryonic pole (uterine epithelium, chorionic ectoderm, and yolk sac endoderm) persist to the end of gestation in G. coeruleus.     

Placental morphology in two sympatric Andean lizards of the genus Liolaemus (Reptilia: Liolaemidae)

Viviparity is a remarkable feature in squamate sauropsids and it has evolved multiple times in parallel with the formation of a placenta. One example of this repeated evolution of viviparity and placentation occurs in the species‐rich South American genus Liolaemus with at least six independent origins of viviparity. However, evolutionary studies of placentation in this genus are limited by a lack of data on placental morphology. The aim of this study is to describe and compare the microanatomy and vessel diameter (Dv, a function of blood flow) of the placenta using scanning electron microscopy (SEM) and confocal laser scanning microscopy (cLSM) in two sympatric Andean viviparous but highly divergent species, Liolaemus robustus and Liolaemus walkeri. We found interspecific differences in cell types in the chorion, allantois, and omphalopleure that may be explained by divergent phylogenetic history. Time elapsed since divergence may also explain the pronounced interspecific differences in vessel diameter, and within each species, there are strong differences in Dv between tissue locations. Both species show features to improve gas exchange in the chorioallantoic placenta including absence of eggshell, large Dv in the allantois (L. robustus) or embryonic side of the uterus (L. walkeri), and when present, microvillous cells in the allantois (L. walkeri). Both species also show features that suggest transfer of nutrients or water in the omphaloplacenta, including an almost complete reduction of the eggshell, secretive material (L. robustus), or vesicles (L. walkeri) on cell surface uterus, and when present specialized cells in the omphalopleure (L. walkeri). No statistical differences in Dv were found among stages 32–39 in each species, suggesting that a different mechanism, other than enhanced blood flow, might satisfy the increased oxygen demand of the developing embryos in the hypoxic environments of the high Andes. J. Morphol. 276:1205–1217, 2015. © 2015 Wiley Periodicals, Inc.     

Evolutionary transformations of the fetal membranes of viviparous reptiles: a case study of two lineages

The reptilian placenta is a composite structure formed by a functional interaction between extraembryonic membranes and the maternal uterus. Study of placental structure of squamate reptiles over the past century has established that each of the multiple independent origins of placentation, which characterize the reproductive diversity of squamates, has resulted from the evolutionary transformation of these homologous structures. Because each evolutionary transformation is an independent novel relationship between maternal and embryonic tissues, the resulting placentae are not homologous, even though the individual components may be. The evolution of reptilian placentation should reveal much about evolutionary patterns and mechanisms because similar structural-functional systems have been transformed along parallel trajectories on multiple occasions. We compared extraembryonic membrane and placental development and pattern of embryonic nutrition in thamnophiine snakes and Pseudemoia lizards in the context of recent hypotheses of phylogenetic relationships. Two primary types of placentation, chorioallantoic and yolk sac, evolved in each lineage. Smooth, highly vascular regions of chorioallantoic placentation are indistinguishable homoplasies that evolved in parallel, likely to facilitate respiratory exchange. The yolk sac placenta of each lineage is specialized for histotrophic nutrient transfer, yet composition of these structures differs because of variation in the ancestral snakes and lizards. In addition, the omphalopleure that contributes to yolk sac placentation persists to later embryonic stages compared to oviparous outgroups, but the two lineages have evolved different structures that prevent replacement of the omphalopleure by the allantois. Each lineage has also evolved unique structural specializations of the chorioallantoic placenta.     

Maximization of evolutionary trends for placental viviparity in the spadenose shark,Scoliodon taticaudus

Synopsis Placental viviparity has evolved inScoliodon taticaudus to a degree that rivals some eutherian mammals. Its eggs are the smallest known of any shark. They have a diameter of 1 mm, a dry weight of 0.0654 ± 0.0100 mg and are nearly yolk-free. Implantation takes place at an early (3 mm) stage of development, and gestation is short (5–6 months). Comparison of the dry weight of the egg (0.065 mg) with the estimated dry weights of a mid-late term 90 mm embryo (910 mg) and a 152 mm neonate (3815.4 mg) reveals weight changes of 14219 × and 58338 ×, respectively. Its normalized brood weight, a measure of maternal nutrient investment, is 49.5 g · kg^–1 female body weight for a six-month gestation. Comparisons with other species of placental and nonplacental sharks show thatS. laticaudus has a highly advanced form of matrotrophy. Maternal nutrients appear to be acquired by placental transport and by imbibition of uterine fluid. Hemotrophic placental nutrient transfer occurs across a unique uterine implantation site, termed the trophonematous cup, in which maternal blood appears to bathe the outer epithelium of the embryonic yolksac placenta. The latter is solid and filled with a three-dimensional network of capillaries and many free interstitial cells. The umbilical stalk contains the vitelline vessels but lacks a yolk duct. Its surface is amplified by many long, villous appendiculae, which consist of a vascular core that ramifies into a massive surface capillary network invested by a simple squamous epithelium. The appendiculae ofS. laticaudus most likely are sites of gas exchange and possibly the uptake of small molecules. They are unlike the appendiculae described in any other placental shark and exhibit design principles similar to those of the uterine trophonemata of matrotrophic rays.     

Placental development and expression of calcium transporting proteins in the extraembryonic membranes of a placentotrophic lizard

Pseudemoia pagenstecheri is a viviparous Australian scincid lizard in which the maternal–embryonic placental interface is differentiated into structurally distinct regions. The chorioallantoic placenta contains an elliptical‐shaped region, the placentome, characterized by hypertrophied uterine and embryonic epithelial cells supported by dense vascular networks. The remainder of the chorioallantoic placenta, the paraplacentome, is also highly vascularized but uterine and chorionic epithelia are thin. An omphaloplacenta with hypertrophied epithelia is located in the abembryonic hemisphere of the egg. There is extensive placental transport of organic and inorganic nutrients, e.g., 85–90% of neonatal calcium is received via placental transfer. Calcium uptake by extraembryonic membranes of squamates correlates with expression of the intracellular calcium binding protein, calbindin‐D_28K, and plasma membrane calcium ATPase (PMCA) is a marker for active calcium transport. We estimated expression of calbindin‐D_28K and PMCA in the chorioallantoic membrane in a developmental series of embryos using immunoblotting and used immunohistochemistry to define the cellular localization of calbindin‐D_28K to test the hypotheses that 1) expression of calcium transporting proteins is coincident with placental transport of calcium and 2) the placenta is functionally specialized for calcium transport in regions of structural differentiation. Calbindin‐D_28K and PMCA were detected at low levels in early stages of development and increased significantly prior to birth, when embryonic calcium uptake peaks. These data support the hypothesis that placental calcium secretion occurs over an extended interval of gestation, with increasing activity as embryonic demand escalates in late development. In addition, calbindin‐D_28K expression is localized in chorionic epithelial cells of the placentome and in the epithelium of the omphalopleure of the omphaloplacenta, which supports the hypothesis that regional structural differentiation in the placenta reflects functional specializations for calcium transport. J. Morphol. 2012. © 2011 Wiley Periodicals, Inc.     

Morphogenesis of placental membranes in the viviparous,placentotrophic lizard Chalcides chalcides (Squamata: Scincidae)

In the scincid lizard Chalcides chalcides, females ovulate small ova and supply most of the nutrients for development by placental means. The yolk is enveloped precocially by extraembryonic ectoderm and endoderm during the gastrula stage, establishing a simple bilaminar yolk sac placenta. The shell membrane begins to degenerate at this time, resulting in apposition of extraembryonic and maternal tissues. A true chorioplacenta has developed by the early pharyngula stage, as has a choriovitelline placenta and the first stages of an omphaloplacenta. Although the choriovitelline membrane disappears rapidly, the omphaloplacenta spreads to occupy the entire abembryonic pole. The yolk cleft is not confluent with the exocoelom, and no omphalallantoic placenta develops. By the limb-bud stage, an allantoplacenta has been established, with a mesometrial placentome composed of interdigitating ridges of chorioallantois and uterine mucosa. The discovery of five distinct placental arrangements in this species, three of which are transitory and two of which have not previously been recorded in reptiles, emphasizes the need for accounts that specify ontogenetic stages and the precise identity and composition of squamate placental membranes. Contrary to previous interpretations, the pattern of extraembryonic membrane development in C. chalcides is evolutionarily conservative, despite the presence of a reduced yolk mass and cytological specializations for nutrient transfer. Our observations indicate that substantial placentotrophy can evolve in squamates without major modifications of morphogenetic patterns. J Morphol 232:35–55, 1997. © 1997 Wiley-Liss, Inc.     

Specializations of the chorioallantoic placenta in the Brazilian scincid lizard,Mabuya heathi: a new placental morphotype for reptiles

New World skinks of the genus Mabuya exhibit a unique form of viviparity that involves ovulation of tiny (1 mm) eggs and provision of virtually all of the nutrients for embryonic development by placental means. Studies of the Brazilian species M. heathi reveal that the chorioallantoic placenta is unlike those reported in any other squamate genus and exhibits striking specializations for maternal-fetal nutrient transfer. The uterine lining is intimately apposed to the chorioallantois, with no trace of an intervening shell membrane or of epithelial erosion; thus, the placenta is epitheliochorial. The uterus exhibits multicellular glands that secrete organic material into the uterine lumen. Opposite the openings of these glands, the chorion develops areolae, invaginated pits that are lined by absorptive, columnar epithelium. A single, mesometrial placentome develops, formed by radially oriented uterine folds that project into a deep invagination of the chorion. Uterine epithelium of the placentome appears to be syncytial and secretory and overlies a rich vascular supply. The apposed chorionic epithelium is absorptive in morphology and contains giant binucleated cells that bear microvilli. Several specializations of the placental membranes of M. heathi are found among eutherian mammals, signifying evolutionary convergence that extends to histological and cytological levels. The chorioallantoic placenta of M. heathi and its relatives warrants recognition as a new morphotype for reptiles, defined here as the "Type IV" placenta. This is the first new type of chorioallantoic placenta to be defined formally for reptiles in over half a century.     

Structural changes to the uterus of the dwarf ornate wobbegong shark (Orectolobus ornatus) during pregnancy

Embryos of the viviparous dwarf ornate wobbegong shark (Orectolobus ornatus) develop without a placenta, unattached to the uterine wall of their mother. Here, we present the first light microscopy study of the uterus of O. ornatus throughout pregnancy. At the beginning of pregnancy, the uterine luminal epithelium and underlying connective tissue become folded to form uterine ridges. By mid to late pregnancy, the luminal surface is extensively folded and long luminal uterine villi are abundant. Compared to the nonpregnant uterus, uterine vasculature is increased during pregnancy. Additionally, as pregnancy progresses the uterine epithelium is attenuated so that there is minimal uterine tissue separating large maternal blood vessels from the fluid that surrounds developing embryos. We conclude that the uterus of O. ornatus undergoes an extensive morphological transformation during pregnancy. These uterine modifications likely support developing embryos via embryonic respiratory gas exchange, waste removal, water balance, and mineral transfer.