Ecological drivers of jaw morphological evolution in lepidosaurs

Abstract

Ecology is a key driver of morphological evolution during adaptive radiations, but alternative factors like phylogeny and allometry can have a strong influence on morphology. Lepidosaurs, the most diverse clade of tetrapods, including lizards and snakes, have evolved a remarkable variety of forms and adapted to disparate ecological niches, representing an ideal case study to understand drivers of morphological evolution. Here, we quantify morphological variation in the lower jaw using three-dimensional geometric morphometrics on a broad sample of 153 lepidosaur species. Our results suggest that phylogeny has significantly influenced mandibular shape evolution, and snakes have diverged from a lizard-like jaw morphology during their evolution. Allometry and ecological factors like diet, foraging mode and substrate also appear to drive the diversification of mandibular forms. Ecological groups differ in patterns of disparity, convergence and rates of evolution, indicating that divergent evolutionary mechanisms are responsible for the acquisition of different diets and habitats. Our analyses support that lepidosaurs ancestrally use their jaws to capture prey, contrary to the traditional view favouring lingual prehension as ancestral. Specialized or ecologically diverse lineages show high rates of jaw shape evolution, suggesting that morphological innovation in the mandible has contributed to the spectacular ecomorphological diversification of lepidosaurs.

Keywords: Lepidosauria; disparity; ecomorphology; evolution; evolutionary rates; geometric morphometrics.

Figure 1.

Phylomorphospace of lower jaw shape in Lepidosauria. Top panel shows the PC1–PC2 phylomorphospace; bottom panel shows the PC1–PC3 phylomorphospace. Extreme jaw morphologies are represented at the positive and negative ends of the three principal coordinate (PC) axes. Convex hulls indicate different lepidosaur clades. Within Serpentes, dashed hulls represent Colubroidea, and dotted hulls represent Viperidae. Silhouettes from PhyloPic.org.

Figure 2.

Phylogenetic regression of allometry of jaw shape on size. Regression lines represent allometric trends in lizards and snakes. Within Serpentes, dashed hulls represent Colubroidea, and dotted hulls represent Viperidae. Silhouettes from PhyloPic.org.

Figure 3.

Morphological disparity and rates of evolution of the lower jaw per clade and ecological category. (a) Disparity per clade and ecological group as sum of variances. (b) Evolutionary rates per ecological group. Boxes represent the median with confidence intervals, white circles represent the mean.

Figure 4.

Rates of evolution of mandibular morphology in Lepidosauria. Branch-specific evolutionary rates (log-transformed) represented by a colour gradient, where red represents high rates and blue, low rates.

Figure 5.

Ancestral state reconstruction of prehension mechanisms. Pie charts represent the probability of each character state at each node, as the consensus of a leave-one-out cross-validation on four different models of character state transition. Abbreviations: Ig, Iguania; Le, Lepidosauria; Sq, Squamata; To, Toxicofera. Prehension mode icons modified from [18].