Placentation in garter snakes. II. Transmission EM of the chorioallantoic placenta of Thamnophis radix and T. sirtalis

Abstract

Transmission electron microscopy was used to examine the ultrastructure of the allantoplacenta of garter snakes during the last half of gestation. This placenta occupies the dorsal hemisphere of the egg and is formed through apposition of the chorioallantois to the inner lining of the uterus. The uterine epithelium consists of flattened cells with short, irregular microvilli and others that bear cilia. The lamina propria is vascularized and its capillaries lie at the base of the uterine epithelial cells. The chorionic epithelium consists of a bilayer of squamous cells that are particularly thin superficial to the allantoic capillaries. Neither the chorionic epithelium nor the uterine epithelium undergoes erosion during development. Although a thin remnant of the shell membrane intervenes between fetal and maternal tissue at mid-gestation, it undergoes fragmentation by the end of gestation. Thus, uterine and chorionic epithelial are directly apposed in some regions of the allantoplacenta, forming continuous cellular boundaries at the placental interface. During development, capillaries proliferate in both the uterine and chorioallantoic tissues. By late gestation, the interhemal diffusion distance has thinned in some areas to less than 2 microm through attenuation of the uterine and chorionic epithelia. Morphologically, the allantoplacenta is well adapted for its function in gas exchange. However, the presence of cytoplasmic vesicles, ribosomal ER, and mitochondria in the chorionic and uterine epithelial cells are consistent with the possibility of additional forms of placental exchange.

Claudin‐5 is Restricted to the Tight Junction Region of Uterine Epithelial Cells in the Uterus of Pregnant/Gravid Squamate Reptiles

“…Additionally, there is a limit to the size of the molecule that can diffuse across these pores. Histotrophy is another mechanism where macromolecules and lipids are transported to the developing embryo by means of vesicle secretion in reptiles (Corso et al, 2000;Blackburn and Lorenz, 2003;Adams et al, 2005), and indeed occurs at the time when claudin-5 is present in the TJ region of the lateral plasma membrane. It may be that smaller ions and molecules are transported by means of the TJ pores, which are formed by claudin-5 and transcellular channels and larger molecules are transported by means of histotrophy.…”

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.…”

“…In species with simple placentae, the chorioallantois remains a highly vascularized membrane that surrounds the embryonic hemisphere of the egg. Chorioallantoic capillaries are closely aligned with maternal capillaries, so gas exchange is still thought to be its primary function in viviparous squamates, though transport of inorganic ions (Blackburn, 1993;Blackburn and Lorenz, 2003b) and histotrophic transfer (Stewart and Brasch, 2003) may also occur in natricid snakes. In squamates with complex placentae, such as the skink Mabuya heathi, the highly modified chorioallantois is also responsible for transport of organic nutrients (Blackburn and Vitt, 2002;Blackburn et al, 1984).…”

Evolution of viviparous reproduction in Paleozoic and Mesozoic reptiles

“…Several specializations facilitate maternal-fetal gas exchange (Blackburn, 2000b). These include the following: increased vascularity of the chorioallantois and pregnant oviduct (Murphy et al, 2010;Parker et al, 2010a, b;Ramírez-Pinilla et al, 2012); evolutionary loss or reduction of the eggshell and the glands that secrete it (Blackburn, 1998a;Heulin et al, 2002;Stewart et al, 2004a;Blackburn et al, 2009Blackburn et al, , 2010Anderson et al, 2011); a reduction in the interhemal diffusion distance through attenuation of intervening fetal and maternal epithelia (Blackburn, 1993b;Blackburn and Lorenz, 2003;Stewart and Brasch, 2003;Adams et al, 2005;Blackburn et al, 2010;Ramírez-Pinilla, 2014); and the development of higher oxygen affinity of fetal blood over maternal blood (Birchard et al, 1984;Berner and Ingermann, 1988;Ingermann, 1992;.…”