Evolution of placental specializations in viviparous African and South American lizards

Abstract

Phylogenetic information offers an important resource in analyses of reproductive diversity, including interpretations of fetal membrane evolution. In this paper, we draw upon ongoing studies of South American and African lizards to consider the value of combining phylogenetic and reproductive evidence in the construction of evolutionary interpretations. South American lizards of the genus Mabuya exhibit several reproductive specializations that are convergent on those of eutherian mammals, including viviparity, long gestation periods, ovulation of tiny eggs, and placental supply of the nutrients for development. Studies of placental morphology and development indicate that New World Mabuya share several other derived features, including chorionic areolae and a "Type IV" epitheliochorial placenta with a villous, mesometrial placentome. Some characteristics of these lizards are shared by two African skinks, M. ivensii and Eumecia anchietae, including minuscule eggs, placentotrophy, an absorptive chorioallantois, and features of the yolk sac. Available evidence is consistent with two explanations: (1) placentotrophy originated in Africa, predating a trans-Atlantic colonization by Mabuya of the New World; and (2) placentotrophy arose two or three separate times among these closely related skinks. As illustrated by analysis of these animals, not only can data on fetal membrane morphology yield phylogenetic information, but phylogenetic evidence in turn provides a valuable way to reconstruct the evolution of fetal membranes in a biogeographic context. When appropriately interpreted, morphological and phylogenetic evidence can be combined to yield robust evolutionary conclusions that avoid the pitfalls of circular reasoning.

A single origin of extreme matrotrophy in African mabuyine skinks

“…Skeletal data have long been recognized to support close affinities between Eumecia and the Mabuya group [27] and more recently have been interpreted to support a close relationship between Eumecia and T. ivensii [8,28]. Our results corroborate this and explicitly support their sister relationship.…”

“…Extreme matrotrophy, in which maternally supplied nutrients account for virtually all nutrients used for embryonic development, is found in at least three different mabuyine lineages: Neotropical Mabuyinae (63 species), Eumecia (2 species; Africa) and Trachylepis ivensii (Africa) [8]. Nutrient transfer is best understood for several species of Neotropical Mabuyinae that transport large amounts of water, ions, lipids and proteins to the embryo via the placenta and have tiny ovulated eggs indicative of little or no lecithotrophy [7,11,12].…”

Morphology, development, and evolution of fetal membranes and placentation in squamate reptiles

“…Thus far, species of New World Mabuya appear to share placental specializations, although other species deserve to be studied in detail. Given the widespread distribution of placentotrophy in New World Mabuya, this pattern is probably ancestral for the group (Blackburn and Vitt, '92;Flemming and Blackburn, 2003). On that basis, we need to seek elsewhere to discover where and when that remarkable reproductive pattern originated.…”

“…In theory, three main interpretations are possible: (1) the three placentotrophic taxa discussed herein are derived from a common placentotrophic ancestor; (2) New World Mabuya and T. ivensi stem from one origin of placentotrophy and Eumecia from another; and (3) the taxa are derived from three independent origins of placentotrophy (Flemming and Blackburn, 2003). The suggested relationship of T. ivensi and allied African forms to New World Mabuya (Greer et al, 2000) could be taken as evidence for one of the first two explanations.…”

“…The suggested relationship of T. ivensi and allied African forms to New World Mabuya (Greer et al, 2000) could be taken as evidence for one of the first two explanations. Accordingly, one could postulate a trans-Atlantic migration of a placentotrophic species from Africa to South America (Flemming and Blackburn, 2003). Likewise, suggestions that Eumecia is allied with African ''Mabuya'' [sensu lato] (Greer,'67,'77) leaves open the possibility that they stem from a common placentotrophic ancestor.…”