Placental specializations of the mountain spiny lizard Sceloporus jarrovi

Abstract

The lizard Sceloporus jarrovi (Phrynosomatidae) is one of the most widely studied viviparous reptiles of North America. Past research has assumed that placentation in this species is relatively simple and functions mainly in gas exchange. Our examination of the late stage placenta via transmission electron microscopy reveals that S. jarrovi has a unique combination of placental characteristics, with unusual specializations for secretion and absorption. In the chorioallantoic placenta, chorionic and uterine tissues are directly apposed through eggshell loss, and their epithelia are greatly attenuated, enhancing gas exchange; this placenta shows evidence of both nutrient transfer and endocrine function. Contrary to past inferences, a yolk sac placenta forms from the avascular omphalopleure and persists through the end of gestation. The uterine epithelium is enlarged and secretory, and the fetal omphalopleure shows branching absorptive channels and other specializations for uptake. Elsewhere, the omphalopleure develops elongated folds that protrude into a coagulum of degenerating shell membrane and other organic material. Uterine tissue in this region shows specializations for absorption. Placental features in S. jarrovi have unexpected functional implications, and challenge assumptions that specializations for nutrient transfer are confined to matrotrophic species.

Scanning electron microscopy of the placental interface in the viviparous lizard Sceloporus jarrovi (Squamata: Phrynosomatidae)

“…As shown elsewhere (Blackburn et al, 2010), the yolk sac placenta contains two distinct regions, an appositional region (which occupies most of the abembryonic hemisphere) and a specialized region (which is confined to the abembryonic pole). In the appositional region, the omphalopleure and uterus are apposed with little or no space between them.…”

“…The overall composition of fetal membranes in Sceloporus jarrovi is consistent with that of typical squamates (see Blackburn, 1993a; Stewart, 1993; Thompson and Speake, 2006). The point is significant, given different reports about Sceloporus in earlier literature (Goldberg, 1970; Guillette et al, 1981; Guillette and Jones, 1985) and more recent studies (Villagrán et al, 2005; Blackburn et al, 2010). The chorioallantois is a duplex membrane consisting of vascularized allantois fused to the chorion and occupies the dorsal hemisphere of the egg (Figs.…”

“…In the absence of detailed information on placental morphology, S. jarrovi and its congeners were previously considered to exhibit a simple form of placentation (Guillette et al, 1981; Guillette and Jones, 1985), implying a departure from fetal membrane characteristics found in other species (Stewart and Blackburn, 1988; Stewart 1993). However, recent study of late‐stage placentation in S. jarrovi has revealed basic similarities with other squamates over which have been superimposed unusual specializations for fetal nutrition (Blackburn et al, 2010).…”

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

“…The epithelia of uterine and chorioallantoic tissues are also attenuated in some viviparous reptiles to bring capillaries closer together and reduce diffusion distances for respiratory gases ( Fig. 1A; Adams et al 2005, Blackburn et al 2010. In taxa with chorioallantoic placentae that differentiate into a placentome and paraplacentome, the paraplacentome is the region of the chorioallantoic placenta that is primarily responsible for gas exchange ( Fig.…”

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;.…”