Ecomorphological diversification in squamates from conserved pattern of cranial integration

Abstract

Factors intrinsic and extrinsic to organisms dictate the course of morphological evolution but are seldom considered together in comparative analyses. Among vertebrates, squamates (lizards and snakes) exhibit remarkable morphological and developmental variations that parallel their incredible ecological spectrum. However, this exceptional diversity also makes systematic quantification and analysis of their morphological evolution challenging. We present a squamate-wide, high-density morphometric analysis of the skull across 181 modern and extinct species to identify the primary drivers of their cranial evolution within a unified, quantitative framework. Diet and habitat preferences, but not reproductive mode, are major influences on skull-shape evolution across squamates, with fossorial and aquatic taxa exhibiting convergent and rapid changes in skull shape. In lizards, diet is associated with the shape of the rostrum, reflecting its use in grasping prey, whereas snakes show a correlation between diet and the shape of posterior skull bones important for gape widening. Similarly, we observe the highest rates of evolution and greatest disparity in regions associated with jaw musculature in lizards, whereas those forming the jaw articulation evolve faster in snakes. In addition, high-resolution ancestral cranial reconstructions from these data support a terrestrial, nonfossorial origin for snakes. Despite their disparate evolutionary trends, lizards and snakes unexpectedly share a common pattern of trait integration, with the highest correlations in the occiput, jaw articulation, and palate. We thus demonstrate that highly diverse phenotypes, exemplified by lizards and snakes, can and do arise from differential selection acting on conserved patterns of phenotypic integration.

Keywords: Squamata; geometric morphometrics; integration and modularity; macroevolution; skull.

Fig. 1.

Cranial partitions in the lizard, snake, and combined datasets. (A) Skull of Sceloporus variabilis (FMNH 122866) reconstructed from µCT imaging in dorsal and ventral views. (B) Rate-through-time plot of each partition corrected by maximum rate value within each module for comparability.

Fig. 2.

Morphospace of skull shape constructed from first two PCs of combined extant and fossil skull-shape data. Data points color-coded by taxonomic group, as indicated by key. Brown polygon spans fossorial lizards sampled in this study. Morphospace with all taxonomic labels in SI Appendix, Figs. S2 and S3.

Fig. 3.

Estimated rates of cranial shape evolution mapped on time-calibrated phylogeny of squamates under best-supported model of trait evolution. (A) Evolutionary rates of overall skull shape of combined dataset under the OU model. Gray rings signify Jurassic–Cretaceous (J-K) and K-Pg boundaries. (B) Evolutionary rates of premaxilla bone under λ model. (C) Evolutionary rates of jaw joint under δ model. (D) Evolutionary rates of pterygoid bone under λ model. Color gradient on branches indicates the rate of shape evolution as indicated by histogram (Insets). Color of circular band denotes taxonomic group as specified in Fig. 2. Rates estimated by using BayesTraitsV3 (78).

Fig. 4.

Per-landmark Procrustes variance and mean evolutionary rates. Landmarks and sliding semilandmarks on skull reconstruction in dorsal (Top Left), ventral (Top Right), and lateral (Bottom) views indicating Procrustes variance in lizards (A) and snakes (B), where a warmer color indicates greater value. (C) Bivariate plot of within-landmark variance against rate for each landmark, where the black line and gray band denote the regression line and 95% CI. Blue line and band indicate expected correlation between within-landmark rate and variance given Brownian motion model of trait evolution and its 95% CI.

Fig. 5.

Plots of mean evolutionary rates for each partition colored by trait values. (A) Mean evolutionary rates of partitions in extant lizards colored by diet preference. (B) Mean evolutionary rates of partitions in extant squamates colored by habitat preference. Mean rates calculated with the compare.multi.evol.rates function in geomorph R package (79).