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

Abstract

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.

The evolution of viviparity: molecular and genomic data from squamate reptiles advance understanding of live birth in amniotes

“…Placental transport of iron has only been reported in highly placentotrophic Mabuya skinks (Ramirez-Pinilla 2006, Ramirez-Pinilla et al 2011), does not occur in lecithotrophic Thamnophis snakes (Hoffman 1970), but has not been investigated in other species (Thompson 1982. The mechanisms of inorganic ion transport are largely unknown in viviparous squamates, but in snakes of the genus Thamnophis, sodium may be transported by the yolk-sac placenta to increase osmolarity of the embryo and to facilitate water absorption , Blackburn & Lorenz 2003 Brandley et al 2012). Thus, nutrient transport is controlled by a large suite of genes, yet we still lack information whether these same genes are also used by other viviparous or oviparous squamates.…”

“…1C; Stewart 1992, Blackburn & Lorenz 2003, Stewart & Thompson 2004. The yolk-sac placenta has been associated with histotrophic nutrient R20 J U Van Dyke and others transport in Pseudemoia sp.…”

Stable isotope tracer reveals that viviparous snakes transport amino acids to offspring during gestation

“…We fed [ 15 N]leucine-labeled diets to gestating females of four viviparous snake species (Boidae: Boa constrictor, Linnaeus; Natricidae: Nerodia sipedon, Linnaeus and Thamnophis sirtalis, Linnaeus; Viperidae: Agkistrodon contortrix, Linnaeus) during gestation, and compared resulting 15 N content of offspring with that of control groups that were not fed tracer. Thamnophis sirtalis has previously been reported to be capable of placental transport of amino acids (Blackburn and Lorenz, 2003a;Blackburn and Lorenz, 2003b;Hoffman, 1970), but placental transport of organic nutrients has not been documented in the other species we tested. Because viviparity is thought to have arisen independently in all three families studied here (Blackburn, 1992), we used a phylogenetic approach to test for differences in tracer transport among species.…”

“…Because the opposing uterine epithelium also appears to be specialized for secretion in some species, particularly natricid snakes, some authors have suggested that the omphalallantoic placenta (i.e. yolk-sac placenta) may be a site of histotrophic organic nutrient transport (Blackburn and Lorenz, 2003a;Hoffman, 1970;Stewart, 1992;Stewart and Brasch, 2003). In addition to maternal and embryonic tissues, many viviparous reptiles retain a reduced shell membrane (reviewed by Guillette, 1982), which exists as an acellular layer between the embryo and uterine lining (Hoffman, 1970).…”

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

“…In T. ordinoides, pregnant females provide sodium, calcium, amino acids, and water to their embryos (Hoffman,'70;Stewart et al,'90). The omphaloplacenta is inferred from ultrastructural observations to be a site of sodium-coupled water transport and may also function in maternal secretion and fetal absorption Blackburn and Lorenz, 2003b).…”