Heterochronic shifts and conserved embryonic shape underlie crocodylian craniofacial disparity and convergence

Abstract

The distinctive anatomy of the crocodylian skull is intimately linked with dietary ecology, resulting in repeated convergence on blunt- and slender-snouted ecomorphs. These evolutionary shifts depend upon modifications of the developmental processes which direct growth and morphogenesis. Here we examine the evolution of cranial ontogenetic trajectories to shed light on the mechanisms underlying convergent snout evolution. We use geometric morphometrics to quantify skeletogenesis in an evolutionary context and reconstruct ancestral patterns of ontogenetic allometry to understand the developmental drivers of craniofacial diversity within Crocodylia. Our analyses uncovered a conserved embryonic region of morphospace (CER) shared by all non-gavialid crocodylians regardless of their eventual adult ecomorph. This observation suggests the presence of conserved developmental processes during early development (before Ferguson stage 20) across most of Crocodylia. Ancestral state reconstruction of ontogenetic trajectories revealed heterochrony, developmental constraint, and developmental systems drift have all played essential roles in the evolution of ecomorphs. Based on these observations, we conclude that two separate, but interconnected, developmental programmes controlling craniofacial morphogenesis and growth enabled the evolutionary plasticity of skull shape in crocodylians.

Keywords: Crocodylia; embryonic ontogeny; evolutionary developmental biology; geometric morphometrics; heterochrony; skull.

Figure 1.

Ontogenetic morphospace of extant crocodylian dorsal skull shape, showing differences among blunt (yellow), moderate (green) and slender (blue) ecomorphs. The conserved embryonic region (CER) is shaded in red, late-skeletal period embryos of non-gavialids are contained within the black, unshaded polygon. Gavialis gangeticus and Tomistoma schlegelii embryos occupy a unique region (shaded purple); within, the red outlined symbol represents the single mid-skeletal period embryo of Gavialis. Silhouettes are from the lettered specimens in the morphospace and the size of symbol is scaled by ontogenetic period. See electronic supplementary material, figures S5 and S6 to view morphospace labelled by species and developmental period.

Figure 2.

Comparison of PC1 (a,b) and PC2 (c,d) ontogenetic trajectories for blunt and slender ecomorphs reveals more distinct ontogenies for slender forms while blunt species are nearly indistinguishable. For moderate ecomorph comparisons, see electronic supplementary material, figure S8. (Online version in colour.)

Figure 3.

Reconstructed evolution of PC1 ontogenies of exemplar slender (a,b), blunt (a,c), and moderate (c) species. Theoretical heterochronic shifts (d) are displayed for comparison. In all plots, dashed lines are reconstructed ancestral ontogenies (numbers correspond to nodes in molecular phylogeny as shown in figure 4) while solid lines are extant species' ontogenies. (Online version in colour.)

Figure 4.

Reconstructed heterochronic modifications to PC1 ontogenetic trajectories across the crocodylian phylogeny (a). Shifts that change adult ecomorph are shown in colour of novel ecomorph. Reconstructed embryonic and adult shapes for key ancestral ontogenies are shown (b) with arrows on the adult shape depicting changes from the embryonic shape. Reconstructed heterochronic modification to PC2 ontogenies can be found in electronic supplementary material, figure S12. A list of heterochrony statements can be found in electronic supplementary material, table S13. (Online version in colour.)