The Evolution of the Antorbital Cavity of Archosaurs: A Study in Soft-Tissue Reconstruction in the Fossil Record with an Analysis of the Function of Pneumaticity

ABSTRACT

The most commonly cited apomorphy of Archosauriformes is an opening in the snout known as the antorbital cavity. Despite the ubiquity and prominence of the antorbital cavity, its function and importance in craniofacial evolution have been problematic. Discovering the significance of the antorbital cavity is a two step process: first, establishing the function of the bony cavity (that is, its soft-tissue relations), and second, determining the biological role of the enclosed structure. The first step is the most fundamental, and hence is examined at length. Three hypotheses for the function of the antorbital cavity have been advanced, suggesting that it housed (1) a gland, (2) a muscle, or (3) a paranasal air sinus. Thus, resolution is correctly viewed as a “soft-tissue problem,” and is addressed within the context of the extant phylogenetic bracket (EPB) approach for reconstructing the unpreserved features of fossil organisms. The soft-anatomical relations of the antorbital cavity (or any bony structure) are important because (1) soft tissues generally have morphogenetic primacy over bony tissues and (2) inferences about soft tissues are the foundation for a cascading suite of paleobiological inferences. The EPB approach uses the shared causal associations between soft tissues and their osteological correlates (i.e., the signatures imparted to the bones by the soft tissues) that are observed in the extant outgroups of the fossil taxon of interest to infer the soft-anatomical attributes of the fossil; based on the assessment at the outgroup node, a hierarchy characterizing the strength of the inference can be constructed. This general approach is applied to the problem of the function of the antorbital cavity, taking each hypothesized soft-tissue candidate—gland, muscle, and air sac—in turn, (1) establishing the osteological correlates of each soft-tissue system in the EPB of any fossil archosaur (i.e., extant birds and crocodilians), (2) formulating a hypothesis of homology based on similarities in these causal associations between birds and crocodilians, (3) testing this hypothesis by surveying fossil archosaurs for the specified osteological correlates, and (4) accepting or rejecting the hypothesis based on its phylogenetic congruence. Using this approach, fossil archosaurs can be reliably reconstructed with a Glandula nasalis, M. pterygoideus, pars dorsalis, and Sinus antorbitalis that are homologous with those of extant archosaurs; however, the osteological correlates of only the antorbital paranasal air sinus involve the several structures associated with the antorbital cavity. Additional evidence for the pneumatic nature of the antorbital cavity comes from the presence of numerous accessory cavities (especially in theropod dinosaurs) surrounding the main antorbital cavity. To address the origin of the antorbital cavity, the EPB approach was applied to basal archosauriforms; the data are not as robust, but nevertheless suggest that the cavity appeared as a housing for a paranasal air sinus. The second step in discovering the evolutionary significance of the antorbital cavity is to assess the function of the enclosed paranasal air sac. In fact, the function of all pneumaticity is investigated here. Rather than the enclosed volume of air (i.e., the empty space) being functionally important, better explanations result by focusing on the pneumatic epithelial diverticulum itself. It is proposed here that the function of the epithelial air sac is simply to pneumatize bone in an opportunistic manner within the constraints of a particular biomechanical loading regime. Trends in facial evolution in three clades of archosaurs (crocodylomorphs, ornithopod dinosaurs, and theropod dinosaurs) were examined in light of this new perspective. Crocodylomorphs and ornithopods both show trends for reduction and enclosure of the antorbital cavity (but for different reasons), whereas theropods show a trend for relatively poorly constrained expansion. These findings are consistent with the view of air sacs as opportunistic pneumatizing machines, with weight reduction and design optimality as secondary effects.