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

Abstract

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.

Fig. 1. .

Parity mode (a) and substrate use (b) predict optimal (θ) body size shifts in Liolaemus lizards. a Viviparous (purple) species have a larger optimal (θ) body size than oviparous species (green). b Saxicolous (pink) species have a larger optimal (θ) body size than their saxicolous (blue) relatives. Evolutionary optimal body size was inferred from an Ornstein-Uhlenbeck (OU) model-fitting procedure (see Methods). The plots display the distribution of the estimated optimal body sizes, where the line is the median, box indicate lower and upper quartiles, and whiskers are minimum and maximum values. Each point within the plots represents a different stochastic character map (n = 500) across the ultrametric tree. Source data are provided as a Source Data file.

Fig. 2. Changes in the thermal environment drive body size evolution in Liolaemus lizards.

a Average of the five best-fitting models show that viviparity has an indirect effect (through its association with mean annual temperature (MAT)) on the body size of Liolaemus lizards. Solid arrows (and asterisk) represent significant associations and dashed arrows denote relationships that were not significant. Thicker arrows indicate stronger effects. Within parentheses we show the confidence interval of each association. This average model was supported from a Phylogenetic Path analysis (Supplementary Table 10), and the confidence intervals were obtained from 500 bootstrap replicates. b At lower environmental temperatures, Liolaemus lizards tend to be larger. Viviparous species (purple) are larger and common in colder habitats than their oviparous (green) counterparts. Solid line represents evolutionary regression (log₁₀ body size = −0.0048*MAT + 1.8316, n = 132) and dashed line represents optimal regression (log₁₀ body size = −0.0072*MAT + 1.8316, n = 132). Both regressions (evolutionary and optimal) were simultaneously estimated in an Ornstein-Uhlenbeck framework (Supplementary Table 11). Source data are provided as a Source Data file.