Placentation in watersnakes I: Placental histology and development in North American Nerodia (Colubridae: Natricinae)

Abstract

As part of a broad survey of placental structure, function, and evolution in reptilian sauropsids paraffin-section histology was used to study microscopic anatomy of the uterus and fetal membranes of three species of North American watersnakes (Nerodia: Colubridae). The pre-ovulatory uterus is poorly vascularized with inactive shell glands. These shell glands are activated during vitellogenesis but regress during pregnancy. Two placentas develop through apposition of the uterine lining to the chorioallantois and the yolk sac omphalopleure. Fetal and maternal components of the chorioallantoic placenta are progressively vascularized during development. Their epithelia are attenuated, but (contrary to a previous report), epithelia of neither the uterus nor the chorion are eroded. The fetal portion of the yolk sac placenta is an omphalallantois, formed of avascular omphalopleure, isolated yolk mass, and allantois. This placenta is progressively replaced by chorioallantoic placenta during mid- to late-development through depletion of the isolated yolk mass. The chorioallantoic placenta is anatomically specialized for maternal-fetal gas exchange, and its expansion during development reflects the growing needs of the fetus for gas exchange. The yolk sac placenta is morphologically unsuited for gas exchange, but may serve other functions in maternal-fetal exchange.

A Novel Pattern of Yolk Processing in Developing Snake Eggs (Colubridae: Lampropeltini) and its Functional and Evolutionary Implications

“…First, the granular cells are much smaller than the endodermal cells; second the granular cells never contain yolk droplets; and third, no structural intermediates exist between the two populations. The cells appear to be equivalent to granulocyte‐like cells described in other squamates, including both lizards (Stewart and Florian, ; Stewart et al., ; Stewart and Thompson, ) and snakes (Blackburn et al., ; Powers and Blackburn, ; Stewart and Thompson, ).…”

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.…”

“…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). The large polymorphic cells of Thamnophis sp.…”

“…Colubridae —North American natricine snakes have been the focus of numerous studies of ecology, reproductive biology, and evolution. All members of this lineage are viviparous and placental development and structure have been described for 11 species, Nerodia erythrogaster, N. rhombifer, N. sipedon, N. taxispolita, Regina septemvittata, Storeria dekayi, Thamnophis ordinoides, T. radix, T. sirtalis, Tropidoclonion lineatum , and Haldea striatula (Attaway, 2000; Baxter, 1987; Blackburn et al, 2017; Blackburn, Anderson, Johnson, Knight, & Gavelis, 2009; Blackburn, Anderson, Lo, Marquez, & Callard, 2017; Blackburn & Lorenz, 2003a, 2003b; Blackburn, Stewart, Baxter, & Hoffman, 2002; Hoffman, 1970; Stewart, 1990; Stewart & Brasch, 2003). The clade is most closely related to Old World species that are oviparous (Figueroa, McKelvy, Grismer, Bell, & Lailvaux, 2016; McVay, Flores‐Villela, & Carstens, 2015), which unfortunately have not been studied.…”

“…A chorioallantoic membrane does not completely encircle the egg at any time in development because the omphalopleure occupies some of the abembryonic region of the egg. In addition to receding at the margins, the isolated yolk mass also thins gradually and by embryonic Stage 36, during the late phase of embryonic growth, only remnants persist (Blackburn & Lorenz, 2003b; Blackburn, Anderson, Lo, et al, 2017; Blackburn, Anderson, Aronson, et al, 2017; Figure 10a). The vascular outer allantoic membrane is positioned internal to the omphalopleure, yet does not fuse with the omphalopleure.…”