Morphogenesis of placental membranes in the viviparous, placentotrophic lizard Chalcides chalcides (Squamata: Scincidae)

Abstract

In the scincid lizard Chalcides chalcides, females ovulate small ova and supply most of the nutrients for development by placental means. The yolk is enveloped precocially by extraembryonic ectoderm and endoderm during the gastrula stage, establishing a simple bilaminar yolk sac placenta. The shell membrane begins to degenerate at this time, resulting in apposition of extraembryonic and maternal tissues. A true chorioplacenta has developed by the early pharyngula stage, as has a choriovitelline placenta and the first stages of an omphaloplacenta. Although the choriovitelline membrane disappears rapidly, the omphaloplacenta spreads to occupy the entire abembryonic pole. The yolk cleft is not confluent with the exocoelom, and no omphalallantoic placenta develops. By the limb-bud stage, an allantoplacenta has been established, with a mesometrial placentome composed of interdigitating ridges of chorioallantois and uterine mucosa. The discovery of five distinct placental arrangements in this species, three of which are transitory and two of which have not previously been recorded in reptiles, emphasizes the need for accounts that specify ontogenetic stages and the precise identity and composition of squamate placental membranes. Contrary to previous interpretations, the pattern of extraembryonic membrane development in C. chalcides is evolutionarily conservative, despite the presence of a reduced yolk mass and cytological specializations for nutrient transfer. Our observations indicate that substantial placentotrophy can evolve in squamates without major modifications of morphogenetic patterns.

Extraordinary case of matrotrophy in the African skinkEumecia anchietae

“…It is unknown, however, if they form large quantities of uterine secretions, as is evident in Eumecia anchietae. Cellular debris of uterine epithelial origin was occasionally noted in the uterine lumen of these lizards (Blackburn, 1993b;Stewart and Thompson, 1996;Blackburn and Callard, 1997), although not in the quantities evident in E. anchietae. Blackburn (1995) considered all squamates inherently placental as the oviduct and extraembryonic membranes lie in close contact from the onset of embryonic development and incipient nutrient transfer is evident in every squamate he knew about.…”

“…Blackburn and Callard (1997), for instance, noted that the surface epithelium of the avascular bilaminar omphalopleure of Chalcides chalcides, prior to the invasion of intravitelline mesoderm, transforms from squamous to columnar cells. The surrounding uterine lumen at this stage does contain eosinophilic secretory material, mixed with degenerating cells presumed to be of uterine origin.…”

“…The surrounding uterine lumen at this stage does contain eosinophilic secretory material, mixed with degenerating cells presumed to be of uterine origin. A mass of detritus, intermixed with fragments of acellular shell membrane, may still collect at the abembryonic pole between the omphalopleure and uterine epithelium well after the limb bud stage (Blackburn, 1993b;Blackburn and Callard, 1997). They therefore suggested that extraembryonic ectoderm is not only involved in absorption of cellular debris, but perhaps through phagocytosis may take an active role in the breakdown of the shell membrane in this species.…”

“…As in most other viviparous squamates (e.g., Yaron, 1985;Guillette, 1992;Blackburn, 1993a), the shell membrane in E. anchietae eggs is thin. Chalcides chalcides and highly matrotrophic New World Mabuya ovulate small ova expanding enormously in volume during gestation; thus, stretching by the egg may lead to loss of the shell membrane (Vitt and Blackburn, 1983;Blackburn et al, 1984;Blackburn and Vitt, 1992;Blackburn and Callard, 1997). A consequence of this early loss of the shell membrane is that extraembryonic and uterine tissues are in direct contact for most of gestation.…”

Histología de las membranas extraembrionarias durante la retención intrauterina en Sceloporus aeneus (Squamata: Phrynosomatidae)

“…La membrana coriovitelina se forma muy temprano en el desarrollo embrionario y típicamente es transitoria tanto en especies ovíparas como en vivíparas (Blackburn & Callard 1997, Villagrán et al 2005. En S. aeneus, esta membrana es sustituida por la membrana corioalantoidea en el estadio 30, mientras que esta membrana en E. fasciatus es reemplazada en el estadio 33 ó 34 (Stewart & Florian 2000) Thompson 1996).…”