Pharyngeal biting mechanics in centrarchid and cichlid fishes: Insights into a key evolutionary innovation

This study compares the pharyngeal biting mechanism of the Cichlidae, a family of perciform fishes that is characterized by many anatomical specializations, with that of the Centrarchidae, a family that possesses the generalized perciform anatomy. Our objective was to trace the key structural and functional changes in the pharyngeal jaw apparatus that have arisen in the evolution from the generalized to derived (cichlid) perciform condition. We propose a mechanical model of pharyngeal biting in the Centrarchidae and compare this with an already existing model for pharyngeal biting in the family Cichlidae. Central to our centrarchid model is a structural coupling between the upper and lower pharyngeal jaws. This coupling severely limits independent movement of the pharyngeal jaws, in contrast to the situation in the speciose Cichlidae, in which the upper and fewer pharyngeal jaw movements are to a large extent independent. We tested both models by electrically stimulating nine muscles of the branchial and hyoid apparatuses in three centrarchid and three cichlid species. The results confirmed the coupled movement of the upper and lower pharyngeal jaws in the Centrarchidae and the independence of these movements in the Cichlidae. We suggest that the key structural innovation in the development of the functionally versatile cichlid (labroid) pharyngeal jaw apparatus was the decoupling of epibranchials 4 from the upper pharyngeal jaws. This structural decoupling implies the decoupling of the movements of the upper and lower pharyngeal jaws and leads to a cichlid (labroid) type of pharyngeal bite. The initial decoupling facilitated a cascade of changes, each leading to improved biting effectiveness and/or to increased mobility and mechanical flexibility of the pharyngeal jaws. The shift of insertion of the m. levator externus 4 which has been considered the primary innovation in the transformation probably arose secondarily. The transformation of the pharyngeal biting mechanism in the perciforms is an excellent example of decoupling of structures associated with diversification of form and function and with increased speciation rates.