Placentation in watersnakes II: Placental ultrastructure in Nerodia erythrogaster (Colubridae: Natricinae)

Abstract

Ultrastructure of the placental tissues from redbelly watersnakes (Nerodia erythrogaster) was analyzed during late pregnancy to provide insight into placental development and function. Examination of the chorioallantoic placenta with transmission electron microscopy reveals that chorionic and uterine epithelia are extremely attenuated but intact and that the eggshell membrane is vestigial and lacks a calcareous layer. These features minimize the interhemal diffusion distance across the placenta. Scanning electron microscopy reveals that fetal and maternal components of the placentas are richly vascularized by dense networks of capillaries. Although the yolk sac omphalopleure has largely been replaced by chorioallantois by late gestation, it retains patches of yolk droplets and regions of absorptive cells with microvilli and abundant mitochondria. Transmission electron microscopy reveals that yolk material is taken up for digestion by endodermal cells. As yolk is removed, allantoic capillaries invade to occupy positions just beneath the epithelium, forming regions of chorioallantoic placentation. Ultrastructural features indicate that the chorioallantoic placenta is specialized for gas exchange, while the omphalallantoic ("yolk sac") placenta shows evidence of functions in yolk digestion and maternal-fetal nutrient transfer. Placental features of this species are consistent with those of other thamnophines, and are evolutionarily convergent on snakes of other viviparous clades.

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*…”

“…Specializations include novel epithelial cell structure and enhanced vascular support for the omphalopleure. At the placental interface of several species, the maternal epithelium is secretory and the fetal component is absorptive (Anderson, Blackburn, & Dunlap, 2011;Blackburn & Lorenz 2003b;Blackburn, Anderson, Lo, Marquez, & Callard, 2017b;Blackburn, Gavelis, Anderson, Johnson, & Dunlap, 2010;Blackburn, Stewart, Baxter, & Hoffman, 2002;Stewart & Brasch 2003;Stewart & Mendez de la Cruz, 2019). However, as in oviparous species, specific functional roles played by the yolk cleft and isolated yolk mass are unclear.…”

Developmental morphology and evolution of extraembryonic membranes of lizards and snakes (Reptilia, Squamata)

“…Colubridae-Tissue composition of the epithelium of the egg of viviparous colubrid snakes, N. erythrogaster, N. rhombifer, N. sipedon, N. taxispolita, S. dekayi, T. ordinoides, T. radix, T. sirtalis, and H. striatula, is similar to the oviparous species; a bilayer of cells surrounds the egg (Blackburn et al, 2002(Blackburn et al, , 2009Blackburn, Anderson, Aronson, et al, 2017;Blackburn, Anderson, Lo, et al, 2017;Blackburn & Lorenz, 2003a, 2003bHoffman, 1970;Stewart, 1990;Stewart & Brasch, 2003). These species differ from oviparous colubrids in that the outer epithelium is regionally differentiated; cells of the chorioallantoic placenta differ morphologically from those of the yolk sac placenta.…”

“…Two cell types are present also in the outer epithelium of the omphalopleure of the yolk sac placenta of H. striatula, each with long microvilli (Stewart & Brasch, 2003). The outer epithelial cells of N. erythrogaster also have microvilli (Blackburn, Anderson, Lo, et al, 2017). Although the isolated yolk mass is reduced in thickness and in breadth later in development, the omphalopleure is retained throughout gestation and cells of the epithelium of the (Blackburn, Anderson, Aronson, et al, 2017) and the cytoplasm of the large cells of N. erythrogaster is thinned where they overlie blood vessels (Blackburn, Anderson, Lo, et al, 2017).…”

Uterine and eggshell modifications associated with the evolution of viviparity in South American water snakes (Helicopsspp.)

“…Saiphos equalis and Z. vivipara are monotypic genera and there is no information on the shell membrane of L. microtus, the other viviparous species of Lerista (Shine, 1985). However, several viviparous squamates exhibit only a vestigial shell membrane throughout pregnancy comparable to that of the viviparous H. carinicaudus and H. infrataeniatus (e.g., Blackburn, Anderson, Lo, Marquez, & Callard, 2017;Hoffman, 1970;Stewart, 1985;Stewart & Brasch, 2003). In many cases, the shell membranes are barely seen or degenerate at late stages of development (e.g., Blackburn & Flemming, 2012;Jerez & Ramírez-Pinilla, 2003;Murphy et al, 2012).…”