Uterine and chorioallantoic angiogenesis and changes in the uterine epithelium during gestation in the viviparous lizard,niveoscincus conventryi(squamata: scincidae)

Abstract

We used immunofluorescent confocal microscopy and scanning electron microscopy to quantify uterine vascularity and to describe uterine surface morphology during gestation in pregnant females of the lecithotrophic lizard Niveoscincus coventryi. As uterine angiogenesis and epithelial cell morphology are thought to be under progesterone control, we studied the effect of a progesterone receptor antagonist (mifepristone) on uterine and chorioallantoic microvasculature and features of the uterine epithelial surfaces. Although intussuceptive angiogenesis was observed in both, uterine and chorioallantoic, vascular beds during gestation, the only significant increases were in the diameters of the uterine vessels. An ellipsoid vessel-dense area grows in the mesometrial hemisphere of the developing conceptus, which parallels the expansion of the allantois to form the chorioallantoic placenta. Uterine surface topography changed during gestation. In particular, uterine blood vessels bulge over the luminal surface to form marked ridges on the uterine embryonic hemisphere, especially during the last stage of pregnancy, and ciliated cells are maintained in the embryonic and abembryonic hemispheres but disappear in both the mesometrial and antimesometrial poles. This distinct regionalization of uterine ridges and ciliated cells in the uterine surface and in the shape of the epithelial component of the chorion might be related to the function of both chorioallantoic and yolk sac placentae during gestation. There was no significant difference between females treated with or without mifepristone, which may be related to the partial function of mifepristone as a progestin antagonist and/or with the function and time of action of progesterone in the uterus during gestation in N. coventryi. Differences in the pattern of angiogenesis and uterine surface morphology during gestation among squamates may be related to the functional diversity of the uterine component of the different placentae and probably reflect its diverse evolutionary history.

Uterine Epithelial Morphology and Progesterone Receptors in a Mifepristone‐treated Viviparous Lizard Pseudemoia entrecasteauxii (Squamata: Scincidae) During Gestation

“…The expansion of the placentome increased throughout pregnancy and followed similar changes to those previously documented in P. entrecasteauxii (Adams et al, ). The results of the present study contrast with those of Ramirez‐Pinilla et al (), where mifepristone treatment did not affect uterine epithelial surface morphology or vascular microarchitecture in the skink Niveoscincus coventryi at any stage of embryonic development.…”

Evolution of viviparity in squamate reptiles: Reversibility reconsidered

“…For example, numerous specializations enhance maternal‐fetal gas exchange in the intrauterine environment (summarized by Blackburn, , ). One set of specializations is the increased vascularity of the pregnant uterus and of the chorioallantois (Murphy et al, ; Parker et al, 2010a, b; Ramírez‐Pinilla et al, ). Another is represented by the attenuated chorionic and/or uterine epithelia that reduce the interhemal distance (Blackburn and Lorenz, ; Stewart and Brasch, ; Blackburn, ; Adams et al, ).…”

Viviparous placentotrophy in reptiles and the parent–offspring conflict

“…Chorioallantoic placentas of lecithotrophic squamates share multiple features that enhance gas exchange. These include: a) well‐vascularized fetal and uterine components (Yaron, ; Blackburn, ; Parker et al, , ; Murphy et al, ; Ramírez‐Pinilla et al, ; b) a vestigial eggshell remnant that thins or disappears during gestation (Blackburn, ; Thompson et al, ), and c) extremely attenuated uterine and chorionic epithelia between the maternal and fetal blood vessels (Blackburn, , ; Stewart and Blackburn, ). As a consequence of these features, the diffusion distance between maternal and fetal capillaries commonly is thinned to a few micrometers or less (Blackburn and Lorenz, ; Stewart and Brasch, ; Adams et al, ; Blackburn et al, , ; Thompson et al, ).…”

“…Placental morphology also has been studied extensively in Niveoscincus (Stewart and Thompson, , , , 2009a, 2009b; Ramírez‐Pinilla et al, ; Wu et al, ). Although most Niveoscincus are relatively lecithotrophic, the Australian N. ocellatus exhibits a modest degree of placentotrophy equivalent to that of some Pseudemoia (Thompson et al, , ).…”

“…As noted above, even species with incipient placentotrophy can show enlarged secretory uterine cells and specializations of the fetal membranes for nutrient uptake (Blackburn and Lorenz, ; Stewart and Brasch, ; Blackburn et al, ; Thompson et al, ; Anderson et al, ). In fact, in relatively lecithotrophic viviparous squamates, yolk sac placentas with microscopic evidence of maternal secretion and fetal absorption are common (e.g., Boyd, ; Villagrán et al, ; Adams et al, ; Ramírez‐Pinilla et al, ) although not universal (Stewart, ; Stewart et al, ).…”