A synthetic review: natural history of amniote reproductive modes in light of comparative evolutionary genomics

Abstract

There is a current lack of consensus on whether the ancestral parity mode was oviparity (egg-laying) or viviparity (live-birth) in amniotes and particularly in squamates (snakes, lizards, and amphisbaenids). How transitions between parity modes occur at the genomic level has primary importance for how science conceptualises the origin of amniotes, and highly variable parity modes in Squamata. Synthesising literature from medicine, poultry science, reproductive biology, and evolutionary biology, I review the genomics and physiology of five broad processes (here termed the ‘Main Five’) expected to change during transitions between parity modes: eggshell formation, embryonic retention, placentation, calcium transport, and maternal–fetal immune dynamics. Throughout, I offer alternative perspectives and testable hypotheses regarding proximate causes of parity mode evolution in amniotes and squamates. If viviparity did evolve early in the history of lepidosaurs, I offer the nucleation site hypothesis as a proximate explanation. The framework of this hypothesis can be extended to amniotes to infer their ancestral state. I also provide a mechanism and hypothesis on how squamates may transition from viviparity to oviparity and make predictions about the directionality of transitions in three species. After considering evidence for differing perspectives on amniote origins, I offer a framework that unifies (i) the extended embryonic retention model and (ii) the traditional model which describes the amniote egg as an adaptation to the terrestrial environment. Additionally, this review contextualises the origin of amniotes and parity mode evolution within Medawar's paradigm. Medawar posited that pregnancy could be supported by immunosuppression, inertness, evasion, or immunological barriers. I demonstrate that this does not support gestation or gravidity across most amniotes but may be an adequate paradigm to explain how the first amniote tolerated internal fertilization and delayed egg deposition. In this context, the eggshell can be thought of as an immunological barrier. If serving as a barrier underpins the origin of the amniote eggshell, there should be evidence that oviparous gravidity can be met with a lack of immunological responses in utero. Rare examples of two species that differentially express very few genes during gravidity, suggestive of an absent immunological reaction to oviparous gravidity, are two skinks Lampropholis guichenoti and Lerista bougainvillii. These species may serve as good models for the original amniote egg. Overall, this review grounds itself in the historical literature while offering a modern perspective on the origin of amniotes. I encourage the scientific community to utilise this review as a resource in evolutionary and comparative genomics studies, embrace the complexity of the system, and thoughtfully consider the frameworks proposed.