Extraordinary case of matrotrophy in the African skink Eumecia anchietae

The viviparous African skink, Eumecia anchietae, exhibits a matrotrophic fetal nutritional pattern. Until well after the limb bud stage, extravitelline nutritional provision is in the form of holocrine secretion originating from the stratified uterine epithelium of the uterine incubation chambers. Uterine secretions are absorbed by a specialized yolk sac ectoderm and chorioallantois through histotrophy. The yolk sac is not in close contact with the uterine lining from the limb bud stage onwards. The yolk sac ectoderm forms invaginations filled with uterine secretion and consists of a single layer of vacuolated hypertrophied cells bearing microvilli. The chorioallantois at the limb bud stage is extensive, well-vascularized, and not intimately associated with the uterine epithelium. Where the uterus is folded, the chorioallantois may interdigitate loosely. Chorionic cells are low to high columnar, clearly vacuolated, and bear microvilli. The allantoic layer consists primarily of squamous cells exhibiting villous projections. By the time embryos have well-defined digits, the specialized yolk sac ectoderm has regressed and the yolk sac lumen has been invaded by vitelline cells. The chorioallantois is very extensive and in areas greatly folded. Where it contacts the uterine epithelium, a proper chorioallantoic placenta is formed. Cell layers of the chorioallantois and uterine epithelium are thin and cuboidal to squamous in appearance. The chorioallantoic placenta is simple in structure, occurs throughout the incubation chamber, and is epitheliochorial in arrangement. It is unknown whether the placentome observed in other highly matrotrophic scincids is formed in late stage embryos of this species.     

Blastocyst implantation in the Chinese hamster (Cricetulus griseus)

Embryonic development of the Chinese hamster (Cricetulus griseus) was studied from the onset of implantation to the formation of the parietal yolk sac placenta. Implantation began on day 6 of pregnancy, when the embryo became fixed to the uterine luminal epithelium. At this time there was no zona pellucida, and microvilli of the trophoblast and uterine epithelium were closely apposed. Stromal cells immediately adjacent to the implantation chamber began to enlarge and accumulate glycogen. By day 7 the mural trophoblast penetrated the luminal epithelium in discrete area. The trophoblast appeared to phagocytize uterine epithelial cells, although epithelium adjoining the points of penetration was normal. In other areas nascent apical protrusions from the uterine epithelium indented the surface of the trophoblast. The epiblast had enlarged and both visceral and parietal endoderm cells were present. The well-developed decidual cells were epithelioid and completely surrounded the implantation chamber. On day 8 the uterine epithelium had disappeared along the mural surface of the embryo. The embryonic cell mass was elongated and filled the yolk sac cavity. Reichert's membrane was well developed. The uterine epithelial basal lamina was largely disrupted, and the trophoblast was in direct contact with decidual cells. Primary and secondary giant trophoblast cells were present and in contact with extravasated maternal blood. The mural trophoblast formed channels in which blood cells were found in close proximity to Reichert's membrane. Decidual cells were in contact with capillary epithelium and in some cases formed part of the vessel wall. Structural changes occurring in the embryo and endometrium during implantation in the Chinese hamster are described for the first time in this report and are compared to those described for some other myomorph rodents.     

Placental Type Interactions and Evolutionary Trends of Development of Uterus in Cestodes

In Proteocephalus thymalli and P. torulosus, a contact of the placental type in uterus was shown to be formed at two different levels. At the first level an interaction occurs between outgrowths of uterine epithelium and thin capsule of embryos closely adjacent to uterine wall. The next level is formation of contact between neighboring egg capsules, which allows distributing nutrients among fetuses present in the uterine cavity. Placental interactions in Clestobothrium acheilognathi are limited in time and space. First, a relatively small number of eggs are involved in interaction of the placental type in the uterine sac, while uterine duct is filled with freely lying eggs. Second, the closest contact is observed in eggs with non-sclerosed egg shell. One of the main evolutionary tendencies in cestodes has been shown to be a modification of uterus for formation of close interrelations with embryonic membranes in the course of transition from the extrauterine to the intrauterine type of embryonic development. Uterus in parasites with a polylecital type of the egg is suggested to serve to the greater extent as a reservoir, whereas in cestodes with oligolecital eggs, uterus performs its direct function—supply of developing embryos with nutrients. As a result, modifications of uterine epithelium are formed: from the appearance of the placental type interactions formed repeatedly in phylogenetically distant groups of cestodes to formation of branched outgrowths separating the uterine space into units or disintegration to actively functioning uterine capsules.     

Position of the embryos of American mink in the fetal chamber at different stages of development]

The spacial position of American mink embryos is characterized by regular changes and is associated with the development and formation of provisory embryonic organs and the uterus. After the implantation the longitudinal axis of the embryo's body lies perpendicularly towards the long axis of the uterus horn. From the end of the 22nd day till birth the embryo moves along the antimesometral side of the fetal chamber by rotation counter clockwise relative to the point of attachment of the alantois stalk. On the 20th day prior to delivery the embryo's body bent as a coil takes a vertical position its fore-part is disposed in the yolk sac cavity, and the hinder part is in the exocoelom. During 17 days before birth the embryo "rolls out" from the yolk sac cavity and occupies the low position in the longitudinal posture of the body. During the following 6 days the prefetus moves towards the opposite side wall of the fetal chamber, takes the upper position and keeps a longitudinal position till the end of the embryonic life.     

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.     

Morphometry of implantation in sheep. I. Trophoblast attachment, modification of the uterine lining, conceptus size and embryo location

The degree of trophoblastic attachment, modification of the uterine lining epithelium during implantation, possible differences in size of the conceptus, and preferential zones of nidation were evaluated. Eight ewes at 14 (n=3), 17 (n=2), 20 (n=1), and 24 (n=2) d of gestation were used, and 6 to 8 equidistant samples of either uterine o uterine plus embryonic membranes tissues were taken from each uterine horn for histomorphometric analysis. Trophoblastic attachment varied from 1.5 to 100% at 14 and 24 d of gestation, respectively. Modification of the uterine lining epithelium ranged from 0% at 14 d to 90% at 24 d. The conceptuses occupied a variable area of the uterine cavity; 15.1% at 14 d, 100% at 17 d, 70.6% at 20 d and 100% at 24 d of gestation. All the embryos were located caudal to the center of the uterine horn. Attachment of the trophoblast and modification of the uterine lining epithelium occurred in the area surrounding the embryos. Implantation was a gradual and long-lasting process which commenced near the embryo and extended peripherally. Morphological variations need to be considered when evaluating embryonic viability.     

Some aspects of segment formation and post-placental development in Peripatus acacioi marcus and marcus (Onychophora)

The surface morphology of the anterior-to-posterior sequence of segment formation in embryos of a viviparous neotropical onychophoran and aspects of post-placental development seen using scanning electron microscopy are described. When all the segments have formed and the walking legs have completed their elongation, the body surface becomes covered with an embryonic cuticle that does not exhibit the hydrofuge properties seen in the adult cuticle. As soon as the walking legs have reached their full length, barbed projections are formed at their distal extremities. These projections are extensions of single cells and are covered by the embryonic cuticle. Transmission electron microscopy reveals that the cells at the distal ends of the legs and their projections have many pinocytotic vesicles at their surfaces. The cytoplasm of these cells and their projections is rich in mitochondria, rough endoplasmic reticulum, glycogen, and granules of storage material. There are minor differences in the surface morphology of the projections found at the ends of the walking legs in embryos of Peripatus acacioi and those of Peripatus biolleyi. The projections and the embryonic cuticle persist thoughout postplacental development. The role of the projections in the uptake of material by the embryo from the uterus is discussed and the possible phylogenetic significance of these projections is suggested.     

Uterine morphology during the annual cycle in Chalcides ocellatus tiligugu (Gmelin) (Squamata: scincidae)

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.     

Uterine epithelial changes during placentation in the viviparous skink Eulamprus tympanum

We used scanning electron microscopy (SEM) and transmission electron microscopy (TEM) to describe the complete ontogeny of simple placentation and the development of both the yolk sac placentae and chorioallantoic placentae from nonreproductive through postparturition phases in the maternal uterine epithelium of the Australian skink, Eulamprus tympanum. We chose E. tympanum, a species with a simple, noninvasive placenta, and which we know, has little net nutrient uptake during gestation to develop hypotheses about placental function and to identify any difference between the oviparous and viviparous conditions. Placental differentiation into the chorioallantoic placenta and yolk sac placenta occurs from embryonic Stage 29; both placentae are simple structures without specialized features for materno/fetal connection. The uterine epithelial cells are not squamous as previously described by Claire Weekes, but are columnar, becoming increasingly attenuated because of the pressure of the impinging underlying capillaries as gestation progresses. When the females are nonreproductive, the luminal uterine surface is flat and the microvillous cells that contain electron-dense vesicles partly obscure the ciliated cells. As vitellogenesis progresses, the microvillous cells are less hypertrophied than in nonreproductive females. After ovulation and fertilization, there is no regional differentiation of the uterine epithelium around the circumference of the egg. The first differentiation, associated with the chorioallantoic placentae and yolk sac placentae, occurs at embryonic Stage 29 and continues through to Stage 39. As gestation proceeds, the uterine chorioallantoic placenta forms ridges, the microvillous cells become less hypertrophied, ciliated cells are less abundant, the underlying blood vessels increase in size, and the gland openings at the uterine surface are more apparent. In contrast, the yolk sac placenta has no particular folding with cells having a random orientation and where the microvillous cells remain hypertrophied throughout gestation. However, the ciliated cells become less abundant as gestation proceeds, as also seen in the chorioallantoic placenta. Secretory vesicles are visible in the uterine lumen. All placental differentiation and cell detail is lost at Stage 40, and the uterine structure has returned to the nonreproductive condition within 2 weeks. Circulating progesterone concentrations begin to rise during late vitellogenesis, peak at embryonic Stages 28-30, and decline after Stage 35 in the later stages of gestation. The coincidence between the time of oviposition and placental differentiation demonstrates a similarity during gestation in the uterus between oviparous and simple placental viviparous squamates.     

Ultrastructure of the placentae of the natricine snake,Virginia striatula (Reptilia: Squamata)

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.     

Morphology and ultrastructure of the uterus of Lineolepis scutigera (Dujardin, 1845) Karpenko, 1985 (Cestoda,Cyclophyllidea, Hymenolepididae) in formation of uterine capsules

The microanatomy and ultrastructure of the uterus in different stages of ontogenesis were studied in a cyclophyllidean cestode Lineolepis scutigera. In the early stages, developing embryos lie freely in the cavity of a single unbroken uterus, which is later fragmented into separate compartments. As a result, numerous spherical uterine capsules are formed; each of them contains one formed egg. Capsules represent a fragmented but actively functioning uterus. Muscular cells containing numerous lipid inclusions are located around them. In the final stages, placenta-like relationships are formed between eggs and the epithelium of capsules. A comparative morphofunctional analysis of uterine capsules in cestodes is presented. Attention is paid to the formation of close interactions between the uterine epithelium and developing eggs.     

An examination of surface epithelium structures of the embryo across the genus Poeciliopsis (Poeciliidae)

In viviparous, teleost fish, with postfertilization maternal nutrient provisioning, embryonic structures that facilitate maternal‐fetal nutrient transfer are predicted to be present. For the family Poeciliidae, only a handful of morphological studies have explored these embryonic specializations. Here, we present a comparative morphological study in the viviparous poeciliid genus, Poeciliopsis . Using microscopy techniques, we examine the embryonic surface epidermis of Poeciliopsis species that vary in their level of postfertilization maternal nutrient provisioning and placentation across two phylogenetic clades and three independent evolutionary origins of placentation. We focus on surface features of the embryo that may facilitate maternal‐fetal nutrient transfer. Specifically, we studied cell apical‐surface morphology associated with the superficial epithelium that covers the body and sac (yolk and pericardial) of embryos at different developmental stages. Scanning electron microscopy revealed common surface epithelial cells across species, including pavement cells with apical‐surface microridges or microvilli and presumed ionocytes and/or mucus‐secreting cells. For three species, in the mid‐stage embryos, the surface of the body and sac were covered in microvillus epithelium. The remaining species did not display microvillus epithelium at any of the stages examined. Instead, their epithelium of the body and sac were composed of cells with apical‐surface microridges. For all species, in the late stage embryos, the surface of the body proper was composed of apical‐surface microridges in a “fingerprint‐like arrangement.” Despite the differences in the surface epithelium of embryos across Poeciliopsis species and embryonic developmental stages, this variation was not associated with the level of postfertilization maternal nutrient provisioning. We discuss these results in light of previous morphological studies of matrotrophic, teleost fish, phylogenetic relationships of Poeciliopsis species, and our earlier comparative microscopy work on the maternal tissue of the Poeciliopsis placenta.     

Mechanisms regulating toxicant disposition to the embryo during early pregnancy: an interspecies comparison

The dose of toxicant reaching the embryo is a critical determinant of developmental toxicity, and is likely to be a key factor responsible for interspecies variability in response to many test agents. This review compares the mechanisms regulating disposition of toxicants from the maternal circulation to the embryo during organogenesis in humans and the two species used predominantly in regulatory developmental toxicity testing, rats and rabbits. These three species utilize fundamentally different strategies for maternal-embryonic exchange during early pregnancy. Early postimplantation rat embryos rely on the inverted visceral yolk sac placenta, which is in intimate contact with the uterine epithelium and is equipped with an extensive repertoire of transport mechanisms, such as pinocytosis, endocytosis, and specific transporter proteins. Also, the rat yolk sac completely surrounds the embryo, such that the fluid-filled exocoelom survives through most of the period of organogenesis, and can concentrate compounds such as certain weak acids due to pH differences between maternal blood and exocelomic fluid. The early postimplantation rabbit conceptus differs from the rat in that the yolk sac is not closely apposed to the uterus during early organogenesis and does not completely enclose the embryo until relatively later in development (approximately GD13). This suggests that the early rabbit yolk sac might be a relatively inefficient transporter, a conclusion supported by limited data with ethylene glycol and one of its predominant metabolites, glycolic acid, given to GD9 rabbits. In humans, maternal-embryo exchange is thought to occur via the chorioallantoic placenta, although it has recently been conjectured that a supplemental route of transfer could occur via absorption into the yolk sac. Knowledge of the mechanisms underlying species-specific embryonic disposition, factored together with other pharmacokinetic characteristics of the test compound and knowledge of critical periods of susceptibility, can be used on a case-by-case basis to make more accurate extrapolations of test animal data to the human.     

Formation of the hindgut cuticular lining during embryonic development of Porcellio scaber (Crustacea,Isopoda)

The hindgut and foregut in terrestrial isopod crustaceans are ectodermal parts of the digestive system and are lined by cuticle, an apical extracellular matrix secreted by epithelial cells. Morphogenesis of the digestive system was reported in previous studies, but differentiation of the gut cuticle was not followed in detail. This study is focused on ultrastructural analyses of hindgut apical matrices and cuticle in selected intramarsupial developmental stages of the terrestrial isopod Porcellio scaber in comparison to adult animals to obtain data on the hindgut cuticular lining differentiation. Our results show that in late embryos of stages 16 and 18 the apical matrix in the hindgut consists of loose material overlaid by a thin intensely ruffled electron dense lamina facing the lumen. The ultrastructural resemblance to the embryonic epidermal matrices described in several arthropods suggests a common principle in chitinous matrix differentiation. The hindgut matrix in the prehatching embryo of stage 19 shows characteristics of the hindgut cuticle, specifically alignment to the apical epithelial surface and a prominent electron dense layer of epicuticle. In the preceding embryonic stage – stage 18 – an electron dense lamina, closely apposed to the apical cell membrane, is evident and is considered as the first epicuticle formation. In marsupial mancae the advanced features of the hindgut cuticle and epithelium are evident: a more prominent epicuticular layer, formation of cuticular spines and an extensive apical labyrinth. In comparison to the hindgut cuticle of adults, the hindgut cuticle of marsupial manca and in particular the electron dense epicuticular layer are much thinner and the difference between cuticle architecture in the anterior chamber and in the papillate region is not yet distinguishable. Differences from the hindgut cuticle in adults imply not fully developed structure and function of the hindgut cuticle in marsupial manca, possibly related also to different environments, as mancae develop in marsupial fluid. Bacteria, evenly distributed within the homogenous electron dense material in the hindgut lumen, were observed only in one specimen of early marsupial manca. The morphological features of gut cuticle renewal are evident in the late marsupial mancae, and are similar to those observed in the exoskeleton.     

Placentation in the opossum, Didelphis virginiana

For the first 9 days of gestation, opossum embryos float in uterine secretions, separated from maternal tissues by a shell membrane. Each embryo is part of the wall of its hollow embryonic sphere. By the 10th day of development, the embryo becomes enveloped by both the amnion and yolk-sac. The yolk-sac consists of vascular and non-vascular portions and, together with the surrounding trophectoderm (trophoblast), forms the yolk-sac placenta of the opossum: the allantois does not contribute to formation of the placenta. The vascular portion of the yolk-sac placenta establishes an intimate relationship with the uterine epithelium soon after loss of the shell membrane. The yolk-sac placenta is non-invasive. Cells of the trophoblast exhibit numerous microvilli, an apical endocytic complex and the lateral and basal cell membrane are elaborately folded. These features suggest a cell that is active in the transport of materials. Junctional complexes between cells of the trophoblast and uterine epithelium were not observed. The uterine epithelium changes from ciliated pseudostratified columnar with few infoldings of lateral and basal cell membranes, to non-ciliated simple columnar in which these membranes show elaborate infoldings. The cells show numerous inclusions and mitochondria are polarized to the basal half of the cell. These features suggest a cell that also is active in the transport of materials.     

Uterine asynchrony: a cause of embryonic loss

During early gestation, hormonal events associated with corpora lutea formation and embryonic synthesis of proteins, prostaglandins, and steroids result in synthesis and release of endometrial secretory products into the uterine lumen. The embryo, inherently and in response to secretory products of the uterus, develops and grows. However, considerable embryonic mortality occurs when uterine secretions become altered in such a manner that they are asynchronous to the developing embryo. Factors that advance or retard development of the uterus and embryo have been utilized to document utero-embryonic asynchrony, and it has been observed that the uterus will not "wait" for embryos to become synchronous. However, the reverse is possible: embryonic development can be accelerated or decelerated. Furthermore within the uterus, localized areas might also exist that favor development of some embryos at the expense of others. This review will consider causes of utero-embryonic asynchrony and offer models of embryonic loss associated with an asynchronous environment in cattle, sheep, and swine.     

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.     

Non‐invasive placentation in the marsupials Macropus eugenii (Macropodidae) and Trichosurus vulpecula (Phalangeridae) involves redistribution of uterine Desmoglein‐2

In mammalian pregnancy, the uterus is remodeled to become receptive to embryonic implantation. Since non‐invasive placentation in marsupials is likely derived from invasive placentation, and is underpinned by intra‐uterine conflict between mother and embryo, species with non‐invasive placentation may employ a variety of molecular mechanisms to maintain an intact uterine epithelium and to prevent embryonic invasion. Identifying such modifications to the uterine epithelium of marsupial species with non‐invasive placentation is key to understanding how conflict is mediated during pregnancy in different mammalian groups. Desmoglein‐2, involved in maintaining lateral cell–cell adhesion of the uterine epithelium, is redistributed before implantation to facilitate embryo invasion in mammals with invasive placentation. We identified localization patterns of this cell adhesion molecule throughout pregnancy in two marsupial species with non‐invasive placentation, the tammar wallaby (Macropus eugenii; Macropodidae), and the brushtail possum (Trichosurus vulpecula; Phalangeridae). Interestingly, Desmoglein‐2 redistribution also occurs in both M. eugenii and T. vulpecula, suggesting that cell adhesion, and thus integrity of the uterine epithelium, is reduced during implantation regardless of placental type, and may be an important component of uterine remodeling. Desmoglein‐2 also localizes to the mesenchymal stromal cells of M. eugenii and to epithelial cell nuclei in T. vulpecula, suggesting its involvement in cellular processes that are independent of adhesion and may compensate for reduced lateral adhesion in the uterine epithelium. We conclude that non‐invasive placentation in marsupials involves diverse and complementary strategies to maintain an intact epithelial barrier.     

Branchial placenta in the viviparous teleost Ilyodon whitei (Goodeidae)

Intraluminal gestation, as it occurs in viviparous goodeids, allows a wide diversity of embryo‐maternal metabolic exchanges. The branchial placenta occurs in embryos developing in intraluminal gestation when ovarian folds enter through the operculum, into the branchial chamber. The maternal ovarian folds may extend to the embryonic pharyngeal cavity. A branchial placenta has been observed in few viviparous teleosts, and there are not previous histological analyses. This study analysis the histological structure in the goodeid Ilyodon whitei. The moterno ovarian folds extend through the embryonic operculum and reach near the gills, occupying part of the branchial chamber. These folds extend also into the pharyngeal cavity. In some regions, the epithelia of the ovarian folds and embryo were in apposition, developing a placental structure in which, maternal and embryonic capillaries lie in close proximity. The maternal epithelium has desquamated cells which may enter through the branchial chamber to the pharyngeal cavity and the alimentary tract. The complex processes that occur in the ovaries of viviparous teleosts, and its diverse adaptations for viviparity, as the presence of branchial placenta, are relevant in the study of the evolution of vertebrate viviparity. J. Morphol. 275:1406–1417, 2014. © 2014 Wiley Periodicals, Inc.