Article

Extraembryonic Membranes and Placentation in the Mexican Snake Conopsis lineata

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  • Facultad de Ciencias, UNAM
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Abstract

Extraembryonic membranes provide protection, oxygen, water, and nutrients to developing embryos, and their study generates information on the origin of the terrestrial egg and the evolution of viviparity. In this research, the morphology of the extraembryonic membranes and the types of placentation in the viviparous snake Conopsis lineata are described through optical microscopy during early and late gestation. When embryos develop inside the uterus, they become surrounded by a thin eggshell membrane. In early gestation, during stages 16 and 18, the embryo is already surrounded by the amnion and the chorion, and in a small region by the chorioallantois, which is product of the contact between the chorion and the growing allantois. A trilaminar omphalopleure covers the yolk sac from the embryonic hemisphere to the level of the equator where the sinus terminalis is located, and from there a bilaminar omphalopleure extends into the abembryonic hemisphere. Thus, according to the relationship of these membranes with the uterine wall, the chorioplacenta, the choriovitelline placenta, and the chorioallantoic placenta are structured at the embryonic pole, while the omphaloplacenta is formed at the abembryonic pole. During late gestation (stages 35, 36, and 37), the uterus and allantois are highly vascularized. The allantois occupies most of the extraembryonic coelom and at the abembryonic pole, it contacts the omphaloplacenta and form the omphalallantoic placenta. This is the first description of all known placenta types in Squamata for a snake species member of the subfamily Colubrinae; where an eggshell membrane with 2.9 μm in width present throughout development is also evident. The structure of extraembryonic membranes in C. lineata is similar to that of other oviparous and viviparous squamate species. The above indicates not only homology, but also that the functional characteristics have been maintained throughout the evolution of the reproductive type.

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Chapter
Viviparity and placentation have evolved convergently in numerous lineages of snakes, and are found in 14 families and in species of every utilized habitat. Viviparity can confer significant costs to female snakes, including reduced mobility, decreased feeding behavior, and constraints on litter size and frequency of reproduction. However, viviparity also confers thermal benefits, and permits exploitation of environments where nesting sites are lacking. Circumstantial and experimental evidence indicates that thermal benefits have acted as selective pressures in the origin of snake viviparity. Placentation evolves simultaneously with viviparity in snakes, in association with a change in composition and thinning of the eggshell and the consequent increased proximity of fetal membranes to the oviductal lining. Physiological studies on North American thamnophines (Natricidae) reveal that placentae are responsible for transfer of oxygen, water, and nutrients from pregnant females to embryos. Histological and ultrastructural studies of thamnophines from 6 genera and 9 species have revealed the morphological basis for these functions. The chorioallantoic placenta is primarily responsible for gas exchange and shows specializations that enhance its functions. Placentae derived from the yolk sac omphalopleure show cellular specializations for maternal nutrient secretion and fetal absorption. Based on evidence from thamnophines, we detail a model for the evolution of placentation in which the fetal membranes maintain and extend their original oviparous functions. Thus, during prolonged uterine egg retention and viviparity, the choriovitelline membrane and chorioallantois assume functions in intrauterine respiration, and the omphalopleure, in absorption. Subsequent specializations for nutrient transfer evolve in fetal and maternal components of both the chorioallantoic and yolk sac placentae. This model is testable in the many clades of viviparous snakes, and therefore offers a valuable framework for future research on placental function and evolution.
Article
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.
Article
The structure and seasonal changes of the oviductal-cloacal junction remain poorly understood in most squamates. This study was undertaken to describe the histology of the oviductal-cloaca junction of a female viviparous snake Toluca lineata, during gestation, previtellogenesis, and vitellogenesis. The oviductal-cloacal junction exhibits a wider lumen and thicker layers of connective tissue, smooth muscle layers, and total wall width compared to the posterior vagina. The lining is characterized by thick, short longitudinal mucosal folds. The luminal epithelia differ morphologically from anterior to posterior portions of the oviductal-cloacal junction. The anterior portion is lined with a simple columnar epithelium composed of nonciliated cells. The middle portion is lined with stratified epithelium that contains an apical columnar cell layer that undergoes morphological changes coincident with the reproductive cycle. The posterior portion is lined with a stratified squamous epithelium. The connective tissue underlying the epithelium contains numerous ovoid cells having abundant acidophilic cytoplasmic granules—eosinophils. Copulation occurs during the previtellogenic stage, as evidenced by the presence of abundant spermatozoa in the lumen of the anterior portion and of a copulatory plug in the middle and posterior portion of the oviductal-cloacal junction. J. Morphol. 237:91–100, 1998. © 1998 Wiley-Liss, Inc.
Article
Development of the extraembryonic membranes and their structural alignment in the formation of the four placental categories that occur in Virginia striatula is similar to that of other Serpentes. The vascularized trilaminar omphalopleure contacts the uterine epithelium early in development to form the choriovitelline placenta, which subsequently extends over the surface of the yolk to its limit at the margin of the isolated yolk mass. As in other squamates, the isolated yolk mass is separated from the yolk sac by the growth of intravitelline cells into the yolk. The bilaminar omphalopleure (ectoderm, endoderm) of the isolated yolk mass contributes the fetal epithelium of the omphaloplacenta. During formation of the omphidoplacenta, the allantois makes its initial contact with the chorion dorsal to the embryo. As the allantois expands, the chorioallantoic placenta gradually replaces the choriovitelline placenta. The terminal placental stage is defined by an extensive chorioallantoic placenta and an omphalallantoic placenta associated with the isolated yolk mass. Although similar in most aspects to the omphalallantoic placentae of other snakes, a secondary yolk cleft develops in V. striatula. This structure, which separates the outer allantoic membrane from the isolated yolk mass, has not been described in other squamates. The choriovitelline placenta and most of the surface of the chorioallantoic placenta are characterized by close vascular apposition, whereas the omphaloplacenta and omphalallantoic placenta feature uterine and fetal epithelial cell hypertrophy in the absence of fetal vascular support. A narrow zone within the chorioallantoic placenta, lying on either side of the omphalallantoic placenta, contains hypertrophied epithelial cells with supporting capillaries on both fetal and maternal aspects.
Article
The extraembryonic membranes of amniote vertebrates are shared structures that have a brief, yet substantive role in the ontogeny of the organism. The yolk sac, which is the first of these structures to develop, has an important function in regulation and mobilization of nourishment to embryos of oviparous species and additionally contributes to maternal-fetal exchange in many viviparous species. Yolk sac placentation has been described in all major taxa of viviparous amniotes. The yolk sac of viviparous reptiles contributes to three categories of placentation, the choriovitelline placenta, which also occurs in marsupial and eutherian mammals, and the omphaloplacenta and omphalallantoic placenta, which occur only among squamate reptiles (lizards and snakes). The fetal contribution to the omphaloplacenta includes a structure termed the isolated yolk mass, which forms in all Squamata independent of reproductive mode, and is produced by a morphogenesis of extraembryonic mesoderm that is unique to this reptilian order. For some viviparous squamates, the allantois contributes to the inner margin of the isolated yolk mass and this structural arrangement constitutes the omphalallantoic placenta. The isolated yolk mass is bordered externally by a bilaminar omphalopleure. Epithelial cells of the bilaminar omphalopleure of the omphaloplacenta and omphalallantoic placenta are hypertrophied. The apposed uterine epithelium likewise contains enlarged cuboidal or columnar shaped cells and the underlying lamina propria is richly vascularized. This epithelial cell structure suggests that the region of the isolated yolk mass is a site of placental specialization in viviparous reptiles. Further, since these features of omphaloplacentation or omphalallantoic placentation commonly occur in species without apparent morphological specialization in other areas of fetal-uterine contact, it is likely that the bilaminar omphalopleure of the isolated yolk mass is evolutionarily the initial site of placental specialization among viviparous reptiles. © 1993 Wiley-Liss, Inc.
Article
Despite a great deal of work in recent years on the structure of reptilian eggshells, few studies have examined the structure and regulation of the female reproductive tract in the formation of eggshell components, and none have examined the entire process from ovulation to oviposition. In this study, we examined oviductal structure in the oviparous lizard, Sceloporus woodi, followed changes in oviductal structure during gravidity, and determined uterine function in the formation of eggshell components. The endometrial glands of the uterus produce the proteinaceous fibers of the eggshell membrane mainly during the first 24 hours following ovulation, and the fibers are secreted intact and subsequently wrapped around the in utero eggs. Eggshell fibers of different thicknesses are layered around each egg, ranging from an inner layer of thick fibers that gradually become thinner medially and finally forms an outer layer of densely packed particulate matter. These changes in the fibrous layer are reflected by the thickness and length of fibers released from the endometrial glands. Calcium deposition occurs from 3 days following ovulation through day 14 (oviposition) and is accompanied by cellular changes in the luminal epithelium suggestive of secretory activity. Deposition of the eggshell components within the uterus occurs on all eggs simultaneously, rather than sequentially. © 1993 Wiley-Liss, Inc.
Article
The morphology of the female reproductive tract and corpus luteum is examined in Sphenomorphus fragilis, a lizard from the lowland regions of New Guinea exhibiting incipient viviparity. Females oviposit eggs that hatch either immediately or within a few hours. Corpora lutea form from ovulated follicles and decrease in diameter as embryonic development progresses. The oviduct from vitellogenic females is sparsely populated with well developed uterine glands containing secretory granules. The eggs are covered with a relatively thin shell (10 μm thick) composed of an inner boundary layer and proteinacous fibers. The secreted shell is complete by early neurulation. Shell morphology does not change throughout the remainder of the in utero incubation period. A well vascularized uterus and chorioallantoic membrane provide simple placentation. These findings suggest that the reduction in shell thickness associated with the evolution of a placenta is due to a decrease in the number of shell glands in the uterus and is not a delay or inhibition of the shelling process per se. This hypothesis further suggests that the selective forces favoring shell gland loss act on the vitellogenic female during gland recruitment which occurs prior to ovulation and not on the pregnant female. © 1992 Wiley-Liss, Inc.
Article
S ummary This is a reveiw of reptilian placentation and other phenomena in the reptilian reproductive cycle concerned with viviparity. There are three distinct types of placentation so far decribed for reptiles:‐ Type (i). A simple where the partial degneration of maternal and embryonic epithelium allows for a close apposition of maternal and embryonic blood streams. The lizards with this type of placents have no apparent reduction in the yolk‐content of thier eggs at the time of ovulation. These Lizards are Lygosoma (Hinulia) quoyi, L. (Hemiergis) quadridigitatum, Tiliqua scincoides, t. nigrolutea , and from Giacomini's decription Chalcides ocellatus , as well as the snakes Denisonia superba and D.suta. Type (ii.). A simple type where the maternal capillaries are raised into small folds. Ther grooves between the folds are lined with glandular epithelium, but the cdapillaries themselves are exporsed at the surface of the folods. The underlying chorionic ectoderm may be thickened and glandular. No early stages were available for and examination of the yolk‐content of the eggs. The lizards with this type of placenta are Lygosoma (Liolepisma) pretiosum, L. (L.) ocellatum, and L. (L.) metallicum. Type (iii.). The most specialized placenta so far described for reptiles, where the uterine wall, over a distinct elliptical area beneth the main longitudinal utering blood‐vessels, is raised into a series of folds filled with capillaries and lined with thickened glandular epithelium and is underlain by an elliptical embryonic area of much thickened chorionie ectoderm. The Lizards with this type of placements have a reduced yolk‐content at the time of ovualion. Thes lizards are Chalcides tridactylus, Lygosoma (Liolepisma) entrecasteauxi, and L. (L.) weekesæ. It is suggested that (α) in reptiles with and obvious reduction in the yolk‐content of their eggs at the time of ovulation, and its invaribale accompaniment by a speciallized folded glandular area of allanto‐placentation, the function of this specialized placenta, is nutrition; that (b) the funciton of the yolk‐sao placenta is possibly to supply water to the developing egg: and that (c) the function of the simple placenta, so consistently present in lizards with eggs with an apparently yolk‐content, is respiration. The condition of the large yolk‐laden egg held tighly in a stretched utersu is obviously the most primitive expression of viviparity among repitles. The condition of a samll egge with a reduced yolk‐content is more advanced, and is obviously but a step behind the yolkless egg, such as occures among the eutherian mammals. Hence it is suggested that the function of fixation, although one of the first concerns of the trophoblast of the small mammalian egg to‐day, has probably originated secondariyly to some other funciton, presumably respiration. It is suggested that with a decrease in the yolk‐content of the egg the yolk‐sac placenta would gradually lose significance as a water absorbing organ, but the virture of its extra‐embryonic circulation, a placenta to funciton for respirtion or nutrition, or both, could be evolved, and it is conceivable that the mammalian yolk‐sac placenta could have been evolved along lines similar to theses. The specialized placenta. type (iii.) is considered to have evolved from the simple conditon described as type (ii.), and it is thought that the placenta in ungulates (the mammalian non‐deciducte plancenta) may have had origin form some such simple type as type (i.), through a stage in placentation similar to type (iii.), which Giacomini likened to a cow's cotyledon in early stages of development. The facts are condsidered to justify the conclusion that among reptiles placentation has arisen independently development of similar types of placentas is common. It ws found that the proportion of viviparous to oviparous reptiles on the Great Dividing Range and the inland plain of south‐easten Australia was extradinarily high, and that the number of oviparous species only approached the number of viviparsous speices on the lower slopes of the Dividing Range, and on the coastal plain. In the Pyrenees and the French Alps by far the majority of lizards found at high altitudes were viviparous. the oviparous species were practically confined to the mountaind slopes up to about 3000‐4000 feet above sea‐level. It is suggested that the failure of oviparous species to establish themselves at 4000 feet and over above sea‐level amy be caused by cold interfering with development of the eggs in the nest. All viviparous speices found on, or recorded from, the inland plain, the mountain slopes, ro the coastal plain of south‐eastern Australia also occur at least 4000 feet above sea‐level on the Great Dividing Range. Two viviparous speices with teh most highly specialized allanto‐placeta and reproductive cycle yet recorded for reptiles in Australia, and only equlled by the lizard C. tridactylus in Italy, are restricted to 4000‐7000 feet above sea‐level. Therefore, it is suggested that in south‐eastern Australia, at least, the factros determining the adoption of viviparity may be either (α) definitely associated with the altitudes to which these lizards are restricted or (b) may work most efficently under the conditons existing at such altitudes. Cold is suggested as the most likely external factor associated with high altitudes that may influence either directly or indircectly the adoption of viviparity.
Article
In reptiles, the evolutionary transition from egg-laying to live-bearing is thought to involve a gradual increase in the duration of egg retention, with progressively more development occurring prior to oviposition, and culminating in the birth of fully developed offspring. However, prolonging the retention of fully-shelled eggs within the oviducts may pose serious gas-exchange problems for the embryos. Thus, evolutionary increases in the period of intrauterine retention may require correlated decreases in the thickness of eggshells and/or their degree of calcification to allow for adequate embryonic gas exchange. To test this evolutionary model, eggs of three distinct reproductive forms of the scincid lizard Lerista bougainvillii were examined to determine the evolutionary relationships between the thickness of the shell membrane, degree of eggshell calcification, and the duration of uterine egg retention. These comparisons revealed the predicted pattern of correlated shifts in eggshell morphology and embryonic stage at oviposition. Evolutionary increases in the duration of egg retention were accompanied by decreases in the thickness of the eggshell membrane and degree of eggshell calcification. This evolutionary model suggests that there may be a tradeoff between the advantages of extended egg retention and the disadvantages of a thinner eggshell. On the basis of this tradeoff, I propose that oviparous taxa with relatively thin eggshells may be preadapted to evolve viviparity. Comparative examination of the limited data available on eggshell thickness in lizards supports this possibility. © 1996 Wiley-Liss, Inc.
Article
Morphological changes occurring in the oviduct and epithelial cells of the lizards Crotaphytus collaris and Eumeces obsoletus during the natural reproductive cycle were examined and quantified. Additionally, development of the eggshell at different stages of gravidity was described. The anterior uterus of each species has a distinct glandular type which differs between species: in E. obsoletus, the glands are tubular and in C. collaris, branched saccular. The branched saccular glands in the anterior uterus of C. collaris produce collagen-like material that forms the fibers of the shell membranes. However, fibers from the eggshell of E. obsoletus did not stain for collagen. The shell of both species is composed of a multilayered inner boundary covered externally by fibers of varying thickness. Initial layers are composed of thick fibers all lying along the same general axis. Outer layers of fibers are progressively thinner and an external surface layer composed of glycosaminoglycans (GAGs) is also present. In C. collaris, calcium, which is deposited in relatively small amounts on the shell surface, appears to be secreted by the epithelium of the anterior uterus. The nonciliated secretory epithelial cells covering the villi-like folds of the posterior infundibulum secrete GAGs. Epithelial cell height of the infundibular villi is greatest during early gravidity. A functional relationship may exist between luteal activity and oviductal secretory activity because the activity of the glandular epithelium varied as gravidity progressed.
Article
The placental memebranes and uterus of the garter snake, Thamnophis sirtalis, were studied using histological, histochemical, electron microscopic, dye transfer, and radioisotopic techniques. The conceptuses are completely enclosed throughout gestation by a transparent shell membrane which is produced by glandular epithelia in the uterine segment of the oviduct. Both chorio-allantoic and omphalo (yolk-sac) placentation are observed in this snake. The growth of the extra-embryonic mesoderm takes place in a manner peculiar to placental reptiles, and results in the isolation of the omphaloplacenta from the yolk-sac wall. On the basis of morphology, enzyme histochemistry, and phagocytosis of Trypan blue particles, this structure is interpreted as a site of histiotrophic absorption. The chorio-allantoic region of placentation is simple in structure. Fetal and maternal capillaries are closely apposed but always separated by layers of uterine and chorionic epithelium and the thin shell membrane. The placental membranes of the garter snake are similar in many respects to those of other live-bearing snakes, but less specialized than most lizard placentate. Isotopically labelled sodium and glycine are passed to the fetus following maternal injection, the latter at least apparently via the omphaloplacenta. The permeability to iron and phospate is extremely low. On the basis of these results and the selective transfer of certain dyestuffs, it appears that the shell membrane functions as a dialyzing membrane.
Article
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.
Article
The eggshell of lizards is a complex structure composed of organic and inorganic molecules secreted by the oviduct, which protects the embryo by providing a barrier to the external environment and also allows the exchange of respiratory gases and water for life support. Calcium deposited on the surface of the eggshell provides an important nutrient source for the embryo. Variation in physical conditions encountered by eggs results in a tradeoff among these functions and influences eggshell structure. Evolution of prolonged uterine egg retention results in a significant change in the incubation environment, notably reduction in efficiency of gas exchange, and selection should favor a concomitant reduction in eggshell thickness. This model is supported by studies that demonstrate an inverse correlation between eggshell thickness and length of uterine egg retention. One mechanism leading to thinning of the eggshell is reduction in size of uterine shell glands. Saiphos equalis is an Australian scincid lizard with an unusual pattern of geographic variation in reproductive mode. All populations retain eggs in the uterus beyond the embryonic stage at oviposition typical for lizards, and some are viviparous. We compared structure and histochemistry of the uterus and eggshell of two populations of S. equalis, prolonged egg retention, and viviparous to test the hypotheses: 1) eggshell thickness is inversely correlated with length of egg retention and 2) eggshell thickness is positively correlated with size of shell glands. We found support for the first hypothesis but also found that eggshells of both populations are surprisingly thick compared with other lizards. Our histochemical data support prior conclusions that uterine shell glands are the source of protein fiber matrix of the eggshell, but we did not find a correlation between size of shell glands and eggshell thickness. Eggshell thickness is likely determined by density of uterine shell glands in this species.
Article
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.
Article
Lizards of the viviparous genus Niveoscincus contributed importantly to a classic model for the evolution of placentation of squamate reptiles. This model predicts that: (1) placental function is correlated with placental structural complexity and (2) the type of chorioallantoic placenta attributed to three species of Niveoscincus (N. metallicus, N. ocellatus, N. pretiosus) is intermediate in complexity to a highly placentotrophic type of placenta. Recent studies of two of these species (N. metallicus, N. ocellatus) revealed additional variation in placental structure, as well as variation in the level of placentotrophy; N. metallicus is predominantly lecithotrophic, while N. ocellatus is highly placentotrophic. We used light microscopy to study placental ontogeny in two biennially reproducing species of Niveoscincus (N. greeni, N. microlepidotus) and placental morphology in late stage embryos of N. pretiosus. These data, in combination with prior studies, provide descriptions of placental structure for six of the eight species assigned to this lineage. The genus Niveoscincus has greater variation in placental structure than any other squamate lineage. We recognize four distinct groupings among these six species based on placental structure. The most highly placentotrophic species, N. ocellatus, has a complex placental morphology, yet shares these structures with a predominantly lecithotrophic species, N. microlepidotus. Thus, among species of Niveoscincus, placental structural complexity is not an infallible predictor of overall placental function.
Article
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.
Article
The uterus of the viviparous skink Chalcides ocellatus tiligugu was studied by SEM and LM during the annual cycle. Three functional phases were identified: preovulatory (spring), gestatory (summer), and quiescent (autumn-winter), characterized by changes in the uterine wall (mainly the endometrial layer). In the preovulatory phase, the uterine wall increases in thickness; its luminal epithelium has ciliated cells and two types of unciliated secretory cells. The first type secretes sulfated glycosaminoglycans (GAGs), which form the amorphous inner layer of the eggshell membrane; the second type secretes acidic glycoproteins that form the intrafibrillar matrix of the outer layer of the eggshell membrane. The lamina propria contains simple alveolar glands that secrete the collagen fibers of the eggshell membrane. During the gestatory phase, the glycoproteins produced by secretory cells of the second type have histotrophic activity for the developing embryo. The uterus widens to form incubation chambers with two hemispheres, one embryonic and the other abembryonic. Both a chorioallantoic placenta and an omphaloplacenta with histotrophic activity are present in late gestation. The chorioallantoic placenta, with aspects of a Weekes (1935) Type III placenta, develops in the embryonic hemisphere. The omphaloplacenta forms at the vegetative pole of the egg and shows cellular hypertrophy of the bilaminar omphalopleure and uterus. During the quiescent phase, the uterus gradually decreases in thickness and activity; its luminal epithelium does not show secretory activity. The annual variations in the myometrial layer involved the inner circular and the outer longitudinal muscle layers.
Article
Squamate reptiles are uniquely suited to study of evolution of reproductive mode and pattern of embryonic nutrition. Viviparous species have evolved from oviparous ancestors on numerous occasions, patterns of nutritional provision to embryos range widely from lecithotrophy, at one end of a continuum, to placentotrophy at the other, and structure and function of the maternal-embryonic relationship is highly constrained resulting in parallel evolutionary trajectories among taxa. Embryos of oviparous species primarily receive nourishment from yolk, but also mobilize a significant quantity of calcium from the eggshell. Most viviparous species also are predominantly lecithotrophic, yet all viviparous species are placentotrophic to some degree. Similarities in embryonic development and nutritional pattern between oviparous species and most viviparous species suggest that the pattern of nutrition of oviparous squamates is an exaptation for the evolution of viviparity and that placentotrophy and viviparity evolve concomitantly. The few species of squamates that rely substantially on placentotrophy have structural modifications of the interface between the embryo and mother that are interpreted as adaptations to enhance nutritional exchange. Recent studies have extended understanding of the diversity of embryonic nutrition and placental structure and have resulted in hypotheses for transitions in the evolution of placentotrophy, yet data are available for few species. Indirect tests of these hypotheses, by comparison of structural-functional relationships among clades in which viviparity has evolved, awaits further study of the reproductive biology of squamates.
Article
Virginia striatula is a viviparous snake with a complex pattern of embryonic nutrition. Nutrients for embryonic development are provided by large, yolked eggs, supplemented by placental transfer. Placentation in this species is surprisingly elaborate for a predominantly lecithotrophic squamate reptile. The embryonic-maternal interface consists of three structurally distinct areas, an omphalallantoic placenta and a regionally diversified chorioallantoic placenta. The chorioallantoic placenta over the embryonic hemisphere (paramesometrial region) of the egg, features close apposition of embryonic and uterine blood vessels because of the attenuate form of the interceding epithelial cells. The periphery of the chorioallantoic placenta, which is adjacent to the omphalallantoic placenta, is characterized by a simple cuboidal uterine epithelium apposed to a stratified cuboidal chorionic epithelium. There are no sites with attenuate epithelial cells and close vascular apposition. The morphology of the omphalallantoic placenta is similar to that of the peripheral chorioallantoic placenta, except that the height of uterine epithelial cells is greater and allantoic blood vessels are not associated with the embryonic epithelium. The functional capabilities of the three placental regions are not known, but structural characteristics suggest that the omphalallantoic placenta and peripheral zone of the chorioallantoic placenta are sites of nutritional provision via histotrophy. The paramesometrial region of the chorioallantoic placenta is also nutritive, in addition to functioning as the primary embryonic respiratory system. The structure of the chorioallantoic placenta of V. striatula is a new placental morphotype for squamate reptiles that is not represented by a classic model for the evolution of reptilian placentation.
Article
An understanding of the evolutionary morphology of extraembryonic membranes in reptiles requires information about oviparous as well as viviparous species. We are studying histology and ultrastructure of the extraembryonic membranes of snakes to clarify the evolutionary history of reptilian fetal membranes, including determination of basal (ancestral) ophidian and squamate patterns. Microscopic anatomy of the membranes of oviparous corn snakes (Elaphe guttata) was examined using light and electron microscopy. At mid-development the inner surface of the eggshell is lined by two extraembryonic membranes, the chorioallantois and the omphalallantoic membrane. The chorioallantois consists of a bilayered cuboidal epithelium that overlies the allantoic blood vessels. During development, allantoic capillaries become more abundant, and the chorionic epithelium thins, decreasing the diffusion distance for respiratory gas exchange. The abembryonic pole of the egg is delimited by a bilaminar omphalopleure and isolated yolk mass, the latter of which is lined on its inner face by the allantois. The isolated yolk mass regresses developmentally, and patches of yolk droplets become isolated and surrounded by allantoic blood vessels. By late development, the abembryonic hemisphere has been fully vascularized by allantoic vessels, forming a "secondary chorioallantois." With regard to its extraembryonic membranes, Elaphe gutatta is similar to viviparous snakes. However, this species exhibits features that have not previously been reported among squamates, perhaps reflecting its oviparous reproductive habits. Morphological evidence for the uptake of eggshell material by epithelia of the chorion and omphalopleure suggests that the potential for absorption by extraembryonic membranes predates the origin of viviparity.
Article
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.
Article
Fetal membranes (such as the chorioallantois and yolk sac) are essential to embryonic development, and have contributed importantly to the evolutionary and ecological diversity of vertebrates. Since the mid-19th century, many scientific careers have been devoted to investigations of their structure, function, and development. However, significant gaps remain in our understanding of the diversity and evolution of fetal membranes. This symposium volume focuses on the use of cladistic principles and phylogenetic relationships to reconstruct the evolutionary morphology of fetal membranes. The main goal of the present paper is to introduce the application of such methods to the evolution of vertebrate fetal membranes, as well as to provide the reader with background information on relevant concepts and terminology. Contributions within this journal issue draw upon studies of metatherian and eutherian mammals, as well as sauropsid reptiles (notably squamates). Particular attention is given to historical transformations of fetal membranes associated with the evolution of such phenomena as placentation and matrotrophy, and reproductive strategies such as viviparity. What emerges from the contributed papers is a broad sampling of contemporary research on fetal membranes, and an overview of how these membranes have evolved to support embryonic life in diverse terrestrial and intra-uterine environments.
Article
Topological and histological analyses of Mabuya mabouya embryos at different developmental stages showed an extraembryonic membrane sequence as follows: a bilaminar omphalopleure and progressive mesodermal expansion around the whole yolk sac at gastrula stages; mesodermal split and formation of an exocoelom in the entire embryonic chamber at neurula stages; beginning of the expansion of the allantois into the exocoelom to form a chorioallantoic membrane at pharyngula stages; complete extension of the allantois into the exocoelom between limb-bud to preparturition stages. Thus, a placental sequence could be enumerated: bilaminar yolk sac placenta; chorioplacenta; allantoplacenta. All placentas are highly specialized for nutrient absorption from early developmental stages. The bistratified extraembryonic ectoderm possesses an external layer with cuboidal cells and a microvillar surface around the whole yolk sac, which absorbs uterine secretions during development of the bilaminar yolk sac placenta and chorioplacenta. During gastrulation, with mesodermal expansion a dorsal absorptive plaque forms above the embryo and several smaller absorptive plaques develop antimesometrially. Both structures are similar histologically and are active in histotrophic transfer from gastrula stages until the end of development. The dorsal absorptive plaque will constitute the placentome and paraplacentome during allantoplacental development. At late gastrula-early neurula stages some absorptive plaques form chorionic concavities or chorionic bags that are penetrated by a long uterine fold and seem to have a specialized histotrophic and/or metabolic role. The extraembryonic mesoderm does not ingress into the yolk sac and neither an isolated yolk mass nor a yolk cleft are formed. This derived pattern of development may be related to the drastic reduction of the egg size and obligatory placentotrophy from early developmental stages. Our results show new specialized placentotrophic structures and a novel arrangement of extraembryonic membrane morphogenesis for Squamata.
Article
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.