New insight into the anatomy of the hyolingual apparatus of Alligator mississippiensis and implications for reconstructing feeding in extinct archosaurs

J Anat. 2015 Jul;227(1):45-61. doi: 10.1111/joa.12320. Epub 2015 May 28.

Abstract

Anatomical studies of the cranium of crocodilians motivated by an interest in its function in feeding largely focused on bite force, the jaw apparatus and associated muscles innervated by the trigeminal nerve. However, the ossified and cartilaginous elements of the hyoid and the associated hyolingual muscles, innervated by the facial, hypoglossal and glossopharyngeal nerves, received much less attention. Crocodilians are known to retain what are ancestrally the 'Rhythmic Hyobranchial Behaviors' such as buccal oscillation, but show diminished freedom and movement for the hyobranchial apparatus and the tongue in food transport and manipulation. Feeding among crocodilians, generally on larger prey items than other reptilian outgroups, involves passive transport of the food within the mouth. The tongue in extant crocodilians is firmly attached to the buccal floor and shows little movement during feeding. Here, we present a detailed anatomical description of the myology of the hyolingual apparatus of Alligator mississippiensis, utilizing contrast-enhanced micro-computed tomography and dissection. We construct the first three-dimensional (3D) description of hyolingual myology in Alligator mississippiensis and discuss the detailed implications of these data for our understanding of hyolingual muscle homology across Reptilia. These anatomical data and an evaluation of the fossil record of hyoid structures also shed light on the evolution of feeding in Reptilia. Simplification of the hyoid occurs early in the evolution of archosaurs. A hyoid with only one pair of ceratobranchials and a weakly ossified or cartilaginous midline basihyal is ancestral to Archosauriformes. The comparison with non-archosaurian reptilian outgroup demonstrates that loss of the second set of ceratobranchials as well as reduced ossification in basihyal occurred prior to the origin of crown-clade archosaurs, crocodilians and birds. Early modification in feeding ecology appears to characterize the early evolution of the clade. Hyoid simplification has been linked to ingestion of large prey items, and this shift in hyoid-related feeding ecology may occur in early archosauriform evolution. A second transformation in hyoid morphology occurs within the crocodilian stem lineage after the split from birds. In Crocodyliformes, deflections in the ceratobrachials become more pronounced. The morphology of the hyoid in Archosauriformes indicates that aspects of the hyolingual apparatus in extant crocodilians are derived, including a strong deflection near the midpoint of the ceratobranchials, and their condition should not be treated as ancestral for Archosauria.

Keywords: Alligator; computed tomography; feeding; fossil; hyolingual apparatus; muscles; tongue.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alligators and Crocodiles / anatomy & histology*
  • Animals
  • Biological Evolution
  • Extinction, Biological
  • Feeding Behavior / physiology
  • Hyoid Bone / anatomy & histology*
  • Muscles / anatomy & histology*
  • Tongue / anatomy & histology*
  • X-Ray Microtomography