Developmental and evolutionary origins of the crocodylian snout and amniote face

Abstract

Crocodylians (alligators, crocodiles, and gharial) are instantly recognizable by their flattened skulls and tooth-filled jaws, adaptations which aid in capturing prey in shallow water and along riverbanks. A popular perception is that crocodylians have remained unchanged since the time non-avian dinosaurs roamed the Earth and that all species are anatomically very similar. However, this group has a rich fossil record which reveals an impressive variation in skull anatomy and ecology, including terrestrial ancestors that superficially resemble later evolving dinosaurs, marine forms with incredibly elongated snouts (region in front of the eyes) and tail fins, and short, pug-faced herbivores with mammal-like molars. Within their semi-aquatic habitat, living species also display substantial variation in snout shape and dietary ecology, including ‘slender’ forms with long snouts that specialize on fish, ‘moderate’ forms like Alligator which have generalized diets, and ‘blunt’ snouted forms which process more tough, shelled prey. Arguably, crocodylians and their extinct relatives display the greatest variation in snout proportions of all amniotes (mammals, reptiles, and birds). These different snout shapes are often used as examples of adaptation because they convergently evolved many times in both living forms and their extinct relatives. Although the phylogenetic relationships, anatomy, biomechanics, and post-hatching growth of crocodylians have been previously studied, the developmental origins of the crocodylian skull remain poorly understood. In this dissertation, I explore the embryonic development of the crocodylian skull to assess mechanisms of snout shape evolution in living crocodylians, their stem lineage, and amniotes more generally.

In chapter 1, I use micro-computed tomography and digital photography to assemble the first comprehensive geometric morphometric (GMM) dataset of embryonic and post-hatching crocodylian skull shape, quantify species-specific developmental patterns, and reconstruct the evolution of development within Crocodylia. This analysis reveals that most species develop from a conserved embryonic shape (highlighting a developmental constraint) and that changes in the relative timing and rate of snout elongation and widening (i.e., heterochrony) were key mechanisms in the diversification of crocodylian snout shape and convergent evolution. In chapter 2, I expand this GMM dataset to include extinct stem crocodylians, implement a new method to quantify patterns of skull shape variation in stem crocodylians, and assess ecological and developmental mechanisms across more than 200 million years of crocodylian evolution. While skull shape disparity of the earliest stem crocodylians was highly distinct, within Crocodylomorpha patterns are consistent with evolution along modern crocodylian developmental ‘lines of least resistance’. This suggests crocodylian-like skull development likely evolved by the Jurassic. In chapter 3, I review the processes involved in the pre-skeletal developmental origins of the amniote face, present preliminary data on the role of cellular proliferation in crocodylian snout development, and hypothesize a common mechanism generates facial variation across amniotes. Although more data are needed to assess molecular mechanisms underlying the origins of facial disparity, in this dissertation I identify important cellular and anatomical components in the evolution of new facial proportions and integrate developmental and macroevolutionary perspectives to understand how similar forms can arise convergently.