Hypoxia and hypothermia as rival agents of selection driving the evolution of viviparity in lizards

Aim: The evolution of key innovations promotes adaptive radiations by opening access to new ecological opportunity. The acquisition of viviparity (live-bearing reproduction) has emerged as one such innovation explaining reptile proliferations into extreme climates. By evolving viviparity, females provide embryos with internally stable environments to complete development. The classical hypothesis suggests that natural selection for viviparity arises from low temperatures in cold climates, which promote prolonged egg retention in the mother's body. An alternative hypothesis proposes that declines in atmospheric oxygen at high elevations create natural selection for embryo retention to provide them with optimal oxygen levels during development. However, although experimental studies support the negative effects of low oxygen on egg development, this ‘hypoxia’ hypothesis has never been tested quantitatively. Here, we compete the hypoxia hypothesis against the ‘cold-climate’ hypothesis, using a highly diverse lizard genus. Location: South America. Major taxa: Liolaemus lizards. Methods: We use a multivariate dataset covering 121 species varying extensively in geographical and climatic distribution (including extreme thermal and oxygen gradients) and parity mode. Based on a new molecular phylogeny for the genus, we use phylogenetic logistic regressions to generate a range of models ranking environmental factors as a function of their effects on parity mode transitions. Results: Elevation and oxygen declines were almost perfectly correlated, and both were identified as the dominant predictors of oviparity-to-viviparity transitions, whereas the role for temperature (dominated by the coldest winter temperatures and daily fluctuations) was significant but secondary. Overall, we showed that oxygen deprivation and low temperatures both play a role in the evolution of viviparity. Main conclusions: Our findings support the role for selection from declines in oxygen concentrations as the primary driver behind viviparity. However, selection arising from cold temperatures and from reduced fluctuations in daily temperatures contributes to the evolution of these transitions by creating multivariate selection on parity mode.