Histology and ultrastructure of the placental membranes of the viviparous brown snake, Storeria dekayi (Colubridae: Natricinae)

Abstract

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.

A developmental synapomorphy of squamate reptiles

“…Haldea ("Virginia") striatula* Stewart and Brasch (2003) and Stewart (1990) Pantherophis guttatus Blackburn et al, (2003) and Knight and Blackburn (2008) Lampropeltis getula Kim and Blackburn (2015) L. triangulum Kim and Blackburn (2016) Nerodia (three species)* Blackburn, Anderson, Aronson, et al (2017a) Nerodia erythrogaster* Blackburn, Anderson, Lo, et al (2017b) Regina septemvitatta* Attaway (2000) Storeria dekayi* Blackburn, Anderson, Johnson, Knight, and Gavelis (2009) Thamnophis sirtalis* Blackburn et al (2002), Blackburn and Lorenz, (2003b) and Hoffman (1970) T. radix* Blackburn and Lorenz (2003b) T. ordinoides* Blackburn et al (2002) Tropidoclonion lineatum* Baxter (1987) and Jones and Baxter (1991) Homalopsidae Dieurostus ("Enhydris") dussumieri*…”

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;.…”

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

“…In thamnophine snakes of the genera Storeria and Thamnophis, placental membranes have been studied by means of both SEM and TEM Blackburn and Lorenz, 2003a,b;Johnson, 2003;Blackburn et al, 2008). As in the oviparous snakes, regions associated with the chorioallantois and omphalopleure are morphologically distinct (Figs.…”