Variation in eggshell characteristics and in intrauterine egg retention between two oviparous clades of the lizard Lacerta vivipara: insight into the oviparity-viviparity continuum in squamates

Abstract

The concept of the oviparity-viviparity continuum refers to the wide range in the length of intrauterine egg retention and, hence, in the stage of embryonic development at oviposition existing in squamates. The evolutionary process underlying this continuum may involve not only a lengthening of egg retention in utero, but also a marked reduction in the thickness of the eggshell. The idea that there may exist a negative correlation between the developmental stage reached by the embryo at oviposition and the eggshell thickness within squamates, although supported by the comparison of oviparous vs. viviparous species, has seldom been evaluated by comparing eggshell thickness of oviparous forms with different lengths of intrauterine egg retention. Eggs of two distinct oviparous clades of the lizard Lacerta vivipara were compared. The eggs laid by females from Slovenian and Italian populations have thicker eggshells, contain embryos on average less developed at the time of oviposition, and require a longer incubation period before hatching than the eggs laid by females from French oviparous populations. Our data and several other examples available from the literature support the idea that the lengthening of intrauterine retention of eggs and the shortening of the subsequent external incubation of eggs are associated with reduction in the thickness of the eggshell, at least in some lineages of oviparous squamates. The current hypotheses that may account for this correlation are presented and a few restrictions and refinements to those hypotheses are discussed. In particular, other changes, such as increased vascularization of the oviduct and of the extraembryonic membranes, may play the same role as the decrease of eggshell thickness in facilitating prolonged intrauterine egg retention in squamates. Future studies should also consider the hypothesis that the length of intrauterine retention might directly depend on the extent of maternal-fetal chemical communication through the eggshell barrier.