Adaptive variation in the development of extraembryonic membranes of gekkotan embryos: A meta-analytical approach

Highly mineralized rigid-shelled eggs characterize one lineage of gekkotans. In contrast, poorly mineralized flexible-shelled eggs characterize basal lineages of gekkotans and all other squamates. Low oxygen permeability of rigid-shelled eggs is associated with small eggs and hatchlings, and long incubation lengths compared to flexible-shelled gekkotan eggs. These features represent a demographic cost for species with rigid-shelled eggs. This cost is offset, at least in part, because mortality due to desiccation and predation is reduced for rigid-shelled eggs relative to flexible-shelled eggs. Developmental traits may also compensate for the low oxygen permeability of rigid-shelled eggs. Oviposition, for example, occurs at earlier developmental stages for gekkotans with rigid- versus flexible-shelled eggs. Such early oviposition facilitates development because eggs move from the relatively hypoxic oviduct to the much better oxygenated nest environment. In this study, I tested the hypothesis that the growth of the yolk sac (YS) and chorioallantoic membrane (CAM) of gekkotans with rigid-shelled eggs is initiated and completed earlier than those of gekkotans with flexible-shelled eggs. I measured the surface area of eggs covered by the YS and CAM from oviposition to hatching and determined which of four nonlinear models provide the best fit for growth curves. I also compiled a data set on embryonic metabolism of gekkotans and other lizards in order to place growth of the YS and CAM in the context of energy utilization of lizard embryos overall. Growth of the YS and CAM of gekkotans with rigid-shelled eggs is accelerated relative to that of gekkotans with flexible-shelled eggs and may serve to separate the cost of YS and CAM development from that of the embryo itself. Adaptive variation in YS and CAM development may extend to birds, crocodilians, and turtles as they also exhibit life history variation that affects oxygen availability to embryos during development.