Developmental and evolutionary origins of the crocodylian snout and amniote face
Committee: Stephanie Pierce (Advisor), Arkhat Abzhanov, James Hanken, Elena Kramer, Clifford Tabin
Abstract: Crocodylians (alligators, crocodiles, and gharial) are instantly recognizable by their flattened skulls and tooth-filled jaws, an adaptation which aids in capturing prey in shallow water and along riverbanks. A popular perception is that crocodylians have remained unchanged ever 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 with impressive variation in skull anatomy and ecology, including terrestrial ancestors that superficially resemble later evolving dinosaurs, marine lineages with incredibly elongated snouts (region of the face in front of the eyes) and tail fins, and short, pug-faced herbivores with mammal-like molars. Within their general semi-aquatic habitat, living species also display substantial variation in snout shape and dietary ecology, including ‘slender’ forms with long snouts that specialize on fast swimming fish, ‘moderate’ forms like Alligator which have a generalized diet, and ‘blunt’ snouted forms which process more tough, shelled prey. Arguably, crocodylians and their extinct relatives display the greatest variation in the proportions of the snout of all amniotes (mammals, reptiles, and birds). These different snout forms are often used as examples of adaptation because similar shapes have 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 geometric morphometric (GMM) dataset of embryonic and post-hatching crocodylian skull shape, quantify species-specific developmental patterns, and reconstruct the evolution of skull development within Crocodylia. This analysis reveals that most species develop from a conserved embryonic shape (highlighting a developmental constraint) and that changes in the timing and rate of snout elongation and widening (i.e., heterochrony) were key mechanisms in the convergent evolution of similar snout shapes. In Chapter 2, I expand this GMM dataset to include extinct relatives of crocodylians, implement a new method to quantify organization and patterns of skull shape in stem-crocodylians, and assess the ecological and developmental mechanisms driving patterns of skull shape across more than 200 million years of crocodylian evolution. While skull shape disparity of the earliest stem-crocodylians was highly distinct, skull evolution within Crocodylomorpha followed modern crocodylian developmental ‘lines of least resistance’, suggesting crocodylian-like skull development likely evolved by the Jurassic. In Chapter 3, I review the processes involved in the developmental formation of the amniote face and present preliminary data on the role of cellular proliferation in crocodylian snout development, which suggests current models for skull development cannot explain the origins of amniote facial disparity. Although more data are needed to understand the molecular mechanisms underlying the origins of facial disparity among and within amniote clades, in this dissertation I am able to identify anatomical and cellular components of development that were critical for the origin of the crocodylian skull and are key mechanisms underlying convergence.