Viviparity imparts a macroevolutionary signature of ecological opportunity in the body size of female Liolaemus lizards.

Viviparity evolved ~115 times across squamate reptiles, facilitating the colonization of cold habitats, where oviparous species are scarce or absent. Whether the ecological opportunity furnished by such colonization reconfigures phenotypic diversity and accelerates evolution is unclear. We investigated the association between viviparity and patterns and rates of body size evolution in female Liolaemus lizards, the most species-rich tetrapod genus from temperate regions. Here, we discover that viviparous species evolve ~20% larger optimal body sizes than their oviparous relatives, but exhibit similar rates of body size evolution. Through a causal modeling approach, we find that viviparity indirectly influences body size evolution through shifts in thermal environment. Accordingly, the colonization of cold habitats favors larger body sizes in viviparous species, reconfiguring body size diversity in Liolaemus. The catalyzing influence of viviparity on phenotypic evolution arises because it unlocks access to otherwise inaccessible sources of ecological opportunity, an outcome potentially repeated across the tree of life.

Exceptional parallelisms characterize the evolutionary transition to live birth in phrynosomatid lizards.

Viviparity, an innovation enhancing maternal control over developing embryos, has evolved >150 times in vertebrates, and has been proposed as an adaptation to inhabit cold habitats. Yet, the behavioral, physiological, morphological, and life history features associated with live-bearing remain unclear. Here, we capitalize on repeated origins of viviparity in phrynosomatid lizards to tease apart the phenotypic patterns associated with this innovation. Using data from 125 species and phylogenetic approaches, we find that viviparous phrynosomatids repeatedly evolved a more cool-adjusted thermal physiology than their oviparous relatives. Through precise thermoregulatory behavior viviparous phrynosomatids are cool-adjusted even in warm environments, and oviparous phrynosomatids warm-adjusted even in cool environments. Convergent behavioral shifts in viviparous species reduce energetic demand during activity, which may help offset the costs of protracted gestation. Whereas dam and offspring body size are similar among both parity modes, annual fecundity repeatedly decreases in viviparous lineages. Thus, viviparity is associated with a lower energetic allocation into production. Together, our results indicate that oviparity and viviparity are on opposing ends of the fast-slow life history continuum in both warm and cool environments. In this sense, the 'cold climate hypothesis' fits into a broader range of energetic/life history trade-offs that influence transitions to viviparity.