Complete Ichthyornis skull illuminates mosaic assembly of the avian head

The homologies of jaw muscles among archosaurs and other sauropsids have been unclear, confounding interpretation of adductor chamber morphology and evolution. Relevant topological patterns of muscles, nerves, and blood vessels were compared across a large sample of extant archosaurs (birds and crocodylians) and outgroups (e.g., lepidosaurs and turtles) to test the utility of positional criteria, such as the relative position of the trigeminal divisions, as predictors of jaw muscle homology. Anatomical structures were visualized using dissection, sectioning, computed tomography (CT), and vascular injection. Data gathered provide a new and robust view of jaw muscle homology and introduce the first synthesized nomenclature of sauropsid musculature using multiple lines of evidence. Despite the great divergences in cephalic morphology among birds, crocodylians, and outgroups, several key sensory nerves (e.g., n. anguli oris, n. supraorbitalis, n. caudalis) and arteries proved useful for muscle identification, and vice versa. Extant crocodylians exhibit an apomorphic neuromuscular pattern counter to the trigeminal topological paradigm: the maxillary nerve runs medial, rather than lateral to M. pseudotemporalis superficialis. Alternative hypotheses of homology necessitate less parsimonious interpretations of changes in topology. Sensory branches to the rictus, external acoustic meatus, supraorbital region, and other cephalic regions suggest conservative dermatomes among reptiles. Different avian clades exhibit shifts in some muscle positions, but maintain the plesiomorphic, diapsid soft-tissue topological pattern. Positional data suggest M. intramandibularis is merely the distal portion of M. pseudotemporalis separated by an intramuscular fibrocartilaginous sesamoid. These adductor chamber patterns indicate multiple topological criteria are necessary for interpretations of soft-tissue homology and warrant further investigation into character congruence and developmental connectivity. Copyright (c) 2007 Wiley-Liss, Inc.

Significance Studies reconstructing morphological evolution have long relied on simple representations of organismal form or on limited sampling of species, hindering a comprehensive understanding of the factors shaping biological diversity. Here, we combine high-resolution 3D quantification of skull shape with dense taxonomic sampling across a major vertebrate clade, birds, to demonstrate that the avian skull is formed of multiple semi-independent regions that epitomize mosaic evolution, with cranial regions and major lineages evolving with distinct rates and modes. We further show that the evolvability of different cranial regions reflects their disparate embryonic origins. Finally, we present a hypothetical reconstruction of the ancestral bird skull using this high-resolution shape data to generate a detailed estimate of extinct forms in the absence of well-preserved three-dimensional fossils.