Generation gland morphology in cordylid lizards: an evolutionary perspective.

To elucidate the functional significance of the three distinct types of generation glands that have been identified among cordylid lizards, we mapped gland type to the terminal taxa in the most recent phylogenetic tree for the Cordylidae. We used the phylogenetic programme Mesquite and applied the principle of parsimony to infer character states for the ancestral nodes in the tree. For those species where information on gland type was not available from the literature, we conducted a histological investigation of generation gland morphology, using standard histological techniques. We included two species of the sister family Gerrhosauridae in the analysis to serve as outgroups. In both Gerrhosaurus typicus and G. flavigularis, scales immediately anterior to the femoral pores displayed glandular activity, but differed from generation glands of cordylids in the absence of mature glandular generations. Among the cordylids investigated, we identified a fourth type of generation gland in Pseudocordylus subviridis, P. spinosus, and in the two Hemicordylus species, one where the glands consistently comprise of two mature glandular generations. In H. capensis, both single- and two-layer type glands are present. Our reconstruction of ancestral character states suggests a minimum of six transformations from one gland type to another during the evolutionary history of the family. The reconstruction furthermore suggests that the single-layer type gland reappeared at least once (in Hemicordylus) in the Cordylinae after having been lost. The reconstruction also unequivocally shows that the pit-like multiple-layer type gland evolved directly from the single-layer type and not from the protruding multiple-layer type. The two-layer type gland appears to be an intermediary condition between the multiple-layer and single-layer types. The evolutionary transformation of generation gland type appears to be linked to changes in lifestyle and associated changes in degree of territoriality and the need for chemical communication.

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

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.

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

Current studies on fetal membranes of reptiles are providing insight into three major historical transformations: evolution of the amniote egg, evolution of viviparity, and evolution of placentotrophy. Squamates (lizards and snakes) are ideal for such studies because their fetal membranes sustain embryos in oviparous species and contribute to placentas in viviparous species. Ultrastructure of the fetal membranes in oviparous corn snakes (Pituophis guttatus) shows that the chorioallantois is specialized for gas exchange and the omphalopleure, for water absorption. Transmission and scanning electron microscopic studies of viviparous thamnophine snakes (Thamnophis, Storeria) have revealed morphological specializations for gas exchange and absorption in the intra-uterine environment that represent modifications of features found in oviparous species. Thus, fetal membranes in oviparous species show morphological differentiation for distinct functions that have been recruited and enhanced under viviparous conditions. The ultimate in specialization of fetal membranes is found in viviparous skinks of South America (Mabuya) and Africa (Trachylepis, Eumecia), in which placentotrophy accounts for nearly all of the nutrients for development. Ongoing research on these lizards has revealed morphological specializations of the chorioallantoic placenta through which nutrient transfer is accomplished. In addition, African Trachylepis show an invasive form of implantation, in which uterine epithelium is replaced by invading chorionic cells. Ongoing analysis of these lizards shows how integration of multiple lines of evidence can provide insight into the evolution of developmental and reproductive specializations once thought to be confined to eutherian mammals.

Evolution of placental specializations in viviparous African and South American lizards.

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.

Population fragmentation in the southern rock agama, Agama atra: more evidence for vicariance in Southern Africa.

Mitochondrial DNA sequence data derived from two genes were used to infer phylogeographical relationships between 13 Agama atra populations. Three distinct geographical assemblages were found among the lizard populations. The first occurs in southern Namibia, the second is restricted to the western dry arid regions of South Africa, whereas the third is distributed throughout the more mesic southern and eastern parts of the subcontinent. Geographically structured differences among populations within Agama clades are probably the result of dispersal and historic isolations among populations. At the broader scale, there were marked congruences between the Agama genetic discontinuities and those described previously in other rock-dwelling vertebrates such as Pronolagus rupestris and Pachydactylus rugosus. This suggests vicariance, probably as a response to natural climatic changes during the past three million years.

Active generation glands present in neonates of some Cordylid Lizards: A case study of Cordylus macropholis (Sauria: Cordylidae).

Generation glands are holocrine epidermal glands occurring on the ventral aspect of the thigh of cordylid lizards. In most species these glands seemingly start to differentiate with the onset of sexual maturity, but macroscopic signs of generation gland activity were noted in neonates of the large-scaled girdled lizard, Cordylus macropholis. The glands of neonatal, subadult, and adult individuals were examined microscopically using standard histological techniques. The glands of the five neonatal specimens examined, including both males and females, all had the same basic structure and displayed two layers of mature glandular material. In subadult and adult specimens, the number of layers varied from seven to nine. The structure of the generation glands of C. macropholis is similar to that of the few other Cordylus species that have been described to date. They are of the protruding kind with multiple mature glandular generations. Juveniles of an additional 12 cordylid species have been examined for the presence of active generation glands. Active glands were found to be present in neonates of C. tasmani and C. tropidosternum, both of which are, like C. macropholis, terrestrial species. In C. cordylus and C. coeruleopunctatus, active generation glands are absent in neonates, but differentiate soon after birth. In other cordylid species, generation glands apparently differentiate only with the onset of sexual maturity. J. Morphol. 235:177-182, 1998. © 1998 Wiley-Liss, Inc.