A classic key innovation constrains oral jaw functional diversification in fishes

Abstract

Abstract Modifications to the pharyngeal jaws—a prey processing system located posterior to the mouth cavity—are widely considered a key innovation that enhanced diversification within several prominent fish clades. Seen in cichlids, damselfishes, wrasses, and a few other lineages, these musculoskeletal alterations are believed to increase the evolutionary independence and, thus, the diversification of the oral and pharyngeal jaw systems. To test this classic hypothesis, we conducted comparative phylogenetic analyses to assess the effect of the pharyngeal novelty on the diversification of feeding morphology and kinematics across a taxonomically diverse sample of spiny-rayed fishes. We quantified movements of the oral jaws and other craniofacial structures from 689 suction-feeding strikes using high-speed videos collected from 228 species with and without the pharyngeal jaw novelty. Contradicting long-held predictions, we find significantly greater disparity across all traits and faster rates of oral jaw functional evolution in fishes without the specialized prey processing system. The modified pharyngeal jaw is undoubtedly a functional innovation as it enhances the strength of the prey processing system, facilitating exceptional transition rates to feeding on hard and tough prey. However, it also restricts the diversification of the feeding system, revealing that the impact of pharyngognathy is more nuanced than previously thought. In light of these and other recent findings, a reinterpretation of the macroevolutionary consequences of the pharyngeal jaw novelty is needed.