Evolution of Viviparity in Sceloporine Lizards: In Utero Po₂as a Developmental Constraint during Egg Retention

Abstract

Reptilian viviparity evolves through selection for increasingly prolonged egg retention within the oviduct. In the majority of sceloporine lizard species, however, egg retention past the normal time of oviposition results in retarded or arrested embryonic development. In this study, we tested the hypothesis that the amount of embryonic development normally attained in utero is directly related to in utero oxygen partial pressure (PO(2)). The three species of sceloporine lizards we used are characterized by developmental arrest (Urosaurus ornatus), retarded development (Sceloporus virgatus), and normal development (Sceloporus scalaris) when eggs are retained. We incubated eggs of these species for 10 d under conditions that simulated retention in the oviduct at a range of experimental oxygen partial pressures (PO(2)). We estimated in utero PO(2) from a standard curve generated from the stage and dry mass of experimental embryos incubated for 10 d at known PO(2). The standard curve was then used to predict the PO(2) associated with the observed rate of development of embryos retained in utero. The results of this study showed that the degree of embryonic development attained in utero during egg retention was positively associated with in utero PO(2). The results indicate that oxygen availability in utero is associated with interspecific differences in the capacity to support intrauterine development in sceloporine lizards.

Angiogenesis of the uterus and chorioallantois in the eastern water skinkEulamprus quoyii

“…If viviparity evolves as a gradual increase in the duration of egg retention in oviparous species (Packard et al, 1977;Shine, 1983;Shine, 1985), then the uterus must develop the capacity to support the metabolic demands of the embryo during such a prolonged period in utero (Parker and Andrews, 2006;Parker et al, 2010a). As the embryo and its extra-embryonic membranes grow and differentiate during pregnancy, changes in vascular density occur in the surrounding uterine tissue to support embryonic growth (Guillette and Jones, 1985;Parker et al, 2010a;Parker et al, 2010b).…”

Obligate costs of parental care to offspring: egg brooding-induced hypoxia creates smaller, slower and weaker python offspring

“…However, in at least one study, experimenters determined the detrimental effects of developmental hypoxia (e.g. reduced embryonic growth rate and survival) on embryos by creating an artificial oxygen tension (PO 2) environment that models in vivo developmental PO2 (Parker & Andrews, 2006). Similarly, in this study we used previously quantified intraclutch oxygen tensions (PO2clutch) in Children's pythons (Antaresia childreni, Gray 1842 to determine the hypoxia-related costs of egg brooding to A. childreni embryos.…”

Unusual angiogenic factor plays a role in lizard pregnancy but is not unique to viviparity

“…The uterus presents a significant barrier to respiratory gas diffusion in internally incubated embryos compared to eggs incubated in the external environment. As low oxygen conditions constrain embryonic development in squamates and other taxa (e.g., Black and Snyder, ; Seymour et al, ; Andrews, ; Woods and Hill, ; Parker and Andrews, ), increasing egg retention must be accompanied by adaptations to facilitate gas exchange, such as reduced thickness of egg coverings, haemoglobin with high oxygen affinity, and increased uterine vascularisation (Guillette and Jones, ; Andrews, ; Parker and Andrews, ). If increased vascularization of the uterus is essential to the evolution of viviparity, it is possible that VEGF 111 expression is a key adaptation allowing the evolution of viviparity in S. equalis .…”