Limited Oxygen Availability In Utero May Constrain the Evolution of Live Birth in Reptiles

Abstract

Although viviparity (live birth) has evolved from oviparity (egg laying) at least 140 times in vertebrates, nearly 120 of these independent events occurred within a single reptile taxon. Surprisingly, only squamate reptiles (lizards and snakes) are capable of facilitating embryonic development to increasingly advanced stages inside the mother during extended periods of oviducal egg retention. Viviparity has never evolved in turtle lineages, presumably because embryos enter and remain in an arrested state until after eggs are laid, regardless of the duration of egg retention. Until now, the limiting factor that initiates and maintains developmental arrest has remained elusive. Here, we show that oviducal hypoxia arrests embryonic development. We demonstrate that hypoxia can maintain developmental arrest after oviposition and that subsequent exposure of arrested embryos to normoxia triggers resumption of their development. We discovered remarkably low oxygen partial pressure in the oviducts of gravid turtles and found that secretions produced by the oviduct retard oxygen diffusion. Our results suggest that an extremely hypoxic environment in the oviduct arrests embryonic development and may constrain the evolution of viviparity in turtles, with the reduced diffusive capacity of oviducal secretions possibly creating or contributing to this hypoxia. We anticipate that these findings will allow us to better understand the mechanisms underlying the evolutionary transition between reproductive modes.

Are we working towards global research priorities for management and conservation of sea turtles?

“…We know the necessary conditions for oviposition and incubation (Mortimer 1990, Ackerman 1997, we recognize that some anthropogenic activities can disrupt nesting (Miller et al 2003) and have identified that delays to nesting can increase embryonic death (Rafferty et al 2011(Rafferty et al , 2013. However, we still lack a deeper understanding of how sea turtles select nest sites at intra-and inter-beach levels.…”

The Impact of Extended Preovipositional Arrest on Embryonic Development and Hatchling Fitness in the Flatback Sea Turtle

“…2). Hypoxia is known to prolong preovipositional arrest, allowing us to compare embryonic development in this treatment to the hyperoxic and normoxic treatments (Rafferty et al 2013). Five or six days is about the longest period that can elapse between the expected oviposition date and the actual oviposition date in natural populations of leatherback turtles (Reina et al 2002;Rafferty et al 2011), so we used it to represent a period of extended preovipositional arrest.…”

“…An extremely low-oxygen (hypoxic) environment in the oviducts of gravid female turtles is known to maintain embryonic preovipositional arrest in utero. Active embryonic development only recommences following exposure to atmospheric oxygen levels after eggs are laid (Rafferty et al 2013). There is an ongoing influence of the environment on the subsequent completion of development of embryos, as well as on the fitness of emerged hatchlings (Lee and Hays 2004), through factors such as temperature (Booth 2006;Rafferty and Reina 2014), concentrations of respiratory gases (Wallace et al 2004), egg location within the nest (Ralph et al 2005), and sand moisture (Wallace et al 2004).…”

“…Early embryonic death is a serious problem for this species of critically endangered sea turtle, which has an extremely low average global hatching success of approximately 50% (Bell et al 2004). Extended periods of preovipositional arrest have also been shown to increase mortality during the initial stages of development, following oviposition, in species of both freshwater turtles (western oblong turtle Chelodina oblonga) and sea turtles (green turtles Chelonia mydas; Rafferty et al 2013). If extended periods of hypoxia in utero can result in a failure of embryos to recommence development after oviposition, it is possible that a remedial management strategy may be to expose nests of turtles to elevated concentrations of oxygen shortly after egg laying is completed.…”

Evolution of viviparous reproduction in Paleozoic and Mesozoic reptiles

“…In fact, the capacity for maternal-fetal gas exchange is thought to constrain the evolution of viviparity (Andrews and Mathies, 2000;Andrews, 2002;Parker et al, 2004;Parker and Andrews, 2006). Furthermore, in chelonians, limitations on gas exchange arrest development of the oviductal egg, with the result that the egg is laid at a very early stage of development (Rafferty et al, 2013).…”