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

Abstract

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.

Uterine Gene Expression in the Live-Bearing Lizard, Chalcides ocellatus, Reveals Convergence of Squamate Reptile and Mammalian Pregnancy Mechanisms

“…Uterine downregulation of MHC Class I expression also occurs in cattle, pigs, and sheep, species with noninvasive epitheliochorial placentae, but in these cases, trophoblast cells merge with those of the uterine epithelia to form binucleate syncytia of embryonic and maternal origin (Davies et al 2000; Choi et al 2003; Joyce et al 2008); downregulation of MHC Class I expression may be a mechanism by which the maternal immune system ignores these allograft cells in mammals. However, there is no evidence of syncytia formation in C. ocellatus (but they may form in the very late stages in pregnancy in C. chalcides [Blackburn et al 1998] and some Mabuya group skinks [Ramírez-Pinilla et al 2006; Vieira et al 2007; Blackburn and Flemming 2011]), and thus, the function of uterine MHC downregulation in C. ocellatus remains unclear.…”

“…These studies have described a continuum of placental complexity, ranging from simple placentae formed by the apposition of uterine and embryonic tissue (e.g., most Eulamprus quoyii group skinks; Murphy et al 2012) to highly complex placentae characterized by extensive folding of the uterus associated with blood vessels and containing enlarged uterine and chorionic epithelial cells (e.g., some Mabuya group skinks; Jerez and Ramírez-Pinilla 2001; Ramírez-Pinilla et al 2006; Vieira et al 2007; Blackburn and Flemming 2011). For the purposes of this discussion, we refer to these ends of the morphological complexity spectrum as “simple” and “complex,” although we note these categories are an oversimplification of the true underlying diversity (see Blackburn 1993).…”

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

“…In an excellent series of studies on another species, M. mabouya, Ramírez-Pinilla (2001, 2003) have described placentation and development by means of light and electron microscopy (also see Ramírez-Pinilla et al, 2006). These studies have done much to advance our understanding of placental morphology and development in members of the group.…”

Desmosomes in the Uterine Epithelium of Noninvasive Skink Placentae

“…Unlike in the African lizard Trachylepis ivensi (Blackburn and Flemming, 2009) where uterine epithelium is replaced by invading chorionic cells and in the South American Mabuya genus (Ramirez-Pinilla, 2006;Vieira et al, 2007) which exhibited a localized endotheliochorial placenta, Australian viviparous skinks exhibit epitheliochorial placentation, where there is no invasion or breaching of the uterine epithelium (Amoroso, 1952;Mossman, 1974;Blackburn 1993;Adams et al, 2005). In epitheliochorial placentation, the maternal and fetal capillaries are separated by six distinct layers, three from the maternal component and three from the fetal component (Grosser, 1927).…”

“…This is a form of placentotrophy whereby the developing embryo receives most of its nutrients from maternal placentotrophic transfer. The omphaloplacenta, which is formed by apposition between fetal and maternal tissue, is situated at the abembryonic pole of the egg and consists of tall, hypertrophied uterine epithelial cells that exhibit secretory properties, whereas membranes associated with gaseous exchange occur in the chorioallantoic placental region of the paraplacentome, where the uterine epithelium is attenuated and overlies an extensive vascular network (Blackburn, 1993;Corso et al, 2000;Flemming and Branch, 2001;Jerez and Ramirez-Pinilla, 2001;Adams et al, 2005;Ramirez-Pinilla et al, 2006). Highly placentotrophic skinks also contain a placentome, which is comprised of interdigitations between the chorioallantoic membranes of the embryonic tissue and uterine epithelium, which exhibits similar morphology and ultrastructure as the omphaloplacenta Thompson, 1998, 2000;Corso et al, 2000;Jerez and Ramirez-Pinilla, 2001;Blackburn and Vitt, 2002) with a unique case of syncytial formation in the Mabuya species (Blackburn and Vitt, 1992).…”