Adaptive variation in the development of extraembryonic membranes of gekkotan lizards: 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 non-linear 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 reduce overlap in the costs of YS and CAM development from that of the embryo. Adaptive variation in YS and CAM development may also extend to birds, crocodilians, and turtles as they also exhibit life history variation that affects oxygen availability to embryos during development.硬壳卵（rigid-shelled eggs）的高矿化特性，是壁虎类（gekkotans）某一演化支的典型特征。与之形成鲜明对比的是，低矿化的软壳卵（flexible-shelled eggs）为壁虎类基部演化支以及所有其他有鳞类（squamates）所共有。相较于软壳卵的壁虎类，硬壳卵的氧气通透性更低，这与卵体及幼体体型偏小、孵化周期更长存在关联。这类特征为具有硬壳卵的物种带来了种群统计学层面的代价。不过该代价至少可部分得到抵消：相较于软壳卵，硬壳卵因干燥脱水与捕食导致的死亡率显著降低。发育相关性状或可弥补硬壳卵较低的氧气通透性缺陷。例如，相较于软壳卵的壁虎类，拥有硬壳卵的壁虎类会在更早期的发育阶段完成产卵。这类提前产卵行为可促进胚胎发育，因为卵体会从相对低氧的输卵管环境转移至氧气更为充足的巢区环境。本研究验证了如下假说：相较于软壳卵的壁虎类，拥有硬壳卵的壁虎类，其卵黄囊（yolk sac, YS）与尿囊绒膜（chorioallantoic membrane, CAM）的生长启动与完成时间均更早。本研究测量了从产卵到孵化全过程中，卵黄囊与尿囊绒膜所覆盖的卵表面积，并通过四种非线性模型拟合生长曲线，筛选出最优拟合模型。此外，本研究还汇编了壁虎类及其他蜥蜴的胚胎代谢数据集，以便将卵黄囊与尿囊绒膜的生长置于蜥蜴胚胎整体能量利用的框架下进行分析。相较于软壳卵的壁虎类，拥有硬壳卵的壁虎类，其卵黄囊与尿囊绒膜的生长速率更快，这或可减少卵黄囊、尿囊绒膜发育与胚胎发育之间的能量成本重叠。卵黄囊与尿囊绒膜发育的适应性变异或也存在于鸟类、鳄类及龟类类群中，因为这些类群同样存在影响胚胎发育期间氧气可用性的生活史变异。