Invasive implantation and intimate placental associations in a placentotrophic african lizard, Trachylepis ivensi (scincidae)

Abstract

In the viviparous lizard Trachylepis ivensi (Scincidae) of central Africa, reproducing females ovulate tiny ∼1 mm eggs and supply the nutrients for development by placental means. Histological study shows that this species has evolved an extraordinary placental pattern long thought to be confined to mammals, in which fetal tissues invade the uterine lining to contact maternal blood vessels. The vestigial shell membrane disappears very early in development, allowing the egg to absorb uterine secretions. The yolk is enveloped precocially by the trilaminar yolk sac and no isolated yolk mass or yolk cleft develops. Early placentas are formed from the chorion and choriovitelline membranes during the neurula through pharyngula stages. During implantation, cells of the chorionic ectoderm penetrate between uterine epithelial cells. The penetrating tissue undergoes hypertrophy and hyperplasia, giving rise to sheets of epithelial tissue that invade beneath the uterine epithelium, stripping it away. As a result, fetal epithelium entirely replaces the uterine epithelium, and lies in direct contact with maternal capillaries and connective tissue. Placentation is endotheliochorial and fundamentally different from that of all other viviparous reptiles known. Further, the pattern of fetal membrane development (with successive loss and re-establishment of an extensive choriovitelline membrane) is unique among vertebrates. T. ivensi represents a new extreme in placental specializations of reptiles, and is the most striking case of convergence on the developmental features of viviparous mammals known. J. Morphol. 2011. © 2011 Wiley Periodicals, Inc.