UC Davis

More than 35,000 fish species dominate diverse aquatic settings due, in part, to the evolution of functional innovations. Such traits enable novel interactions with the environment, often promoting increased diversification within the lineage that it evolved. As several of these innovative traits are morphological modifications that impact prey capture and manipulation, the feeding apparatus is a rich system to examine the macroevolutionary impacts of functional novelties. My dissertation leverages functional morphology, kinematics, and phylogenetic comparative methods to explore how key functional innovations, specifically oral jaw protrusion and a major pharyngeal jaw modification, have affected the evolution and function of the fish feeding system.

Most fishes use suction feeding to capture their food, expanding the oral cavity to draw in water and prey. Protrusion of the oral jaws, an innovation among ray-finned fishes, is essential to this feeding mechanism as it increases flow forces into the mouth. Though a common mechanism in suction feeding fishes, the magnitude and direction of jaw protrusion vary greatly phylogenetically. In my first chapter, I explored the anatomical basis of oral jaw protrusion directionality in ponyfishes (Leiognathidae), a family comprised of 52 species that exhibit striking diversity in this functional trait. Using cleared and stained specimens of 20 ponyfish species representing every major lineage within the family, I measured eight traits associated with the size and positioning of oral jaw bones. Species fell into three nonoverlapping clusters with respect to directionality including dorsal, rostral, and ventral protruders. I found that the anterior–posterior position of the articular-quadrate jaw joint is a key correlate of protrusion direction. As the joint position moves from a posterior to a more anterior location, the orientation of the relaxed mandible rotates from an almost horizontal resting position to an upright vertical posture. Thus, the abduction of the mandible from the horizontal position results in ventrally directed protrusion, while the more upright mandible rotates to a position that maintains dorsal orientation. The position of the lower jaw joint may be a widespread anatomical mechanism for adjusting the directionality of jaw protrusion in ray-finned fishes, but it remains to be seen whether other groups have evolved different traits to facilitate this underappreciated aspect of diversity in fish feeding functional morphology.

In addition to the functional capacity of the oral jaws, fishes also have pharyngeal jaws – a second jaw system located posterior to the mouth cavity that chews, tears, and/or crushes prey before swallowing. This prey capture and processing sequence is generally conserved across suction feeding fishes. However, some species have evolved a novel pharyngeal jaw configuration, termed “pharyngognathy”, where several musculoskeletal modifications enable fishes to process more robust prey. Thus, the MPJ is widely considered a key innovation as it enhanced trophic diversification within several prominent fish clades. Seen in cichlids, damselfishes, wrasses, and a few other groups, these musculoskeletal alterations are believed to have increased the evolutionary independence of the oral and pharyngeal jaw systems, enabling greater diversification of the feeding system. Though aspects of this hypothesis have received considerable attention, we lack comparative analyses contrasting the evolutionary patterns and feeding functions in species with and without the MPJ. Thus, we lack a complete understand of how this novel trait impacts the fish feeding apparatus overall.

In my second chapter, I conducted comparative phylogenetic analyses of integration, disparity, and rate of evolution on feeding-related, skeletal structures in 85 Neotropical cichlid species and 30 North American centrarchid species, which lack the specialized pharyngeal jaw. Contrasting evolutionary patterns in these two continental radiations, I tested a classic decoupling hypothesis. Specifically, I asked whether the modified pharyngeal jaws in cichlids resulted in enhanced evolutionary independence of the oral and pharyngeal jaws, leading to increased morphological diversification of feeding structures. Contrary to this prediction, I found significantly stronger evolutionary integration between the oral and pharyngeal jaws in cichlids compared to centrarchids, although the two groups did not differ in patterns of integration within each jaw system. Further, though I found no significant differences in disparity, centrarchids showed faster rates of morphological evolution. These results suggest that while the modified pharyngeal jaw enhances feeding performance, the novelty does not prompt increased morphological diversification within the feeding apparatus, as has long been thought.

In my third chapter, I conducted comparative phylogenetic analyses to assess the effects of the pharyngeal jaw novelty on diversification of feeding morphology and kinematics across a phylogenetically diverse sample of spiny-rayed fishes. I quantified movements of the oral jaws and other craniofacial structures during suction feeding strikes using 689 high speed videos collected from 228 species with and without the modified pharyngeal jaw. In line with my Chapter 2 findings, I found significantly greater disparity in oral jaw functions and craniofacial shapes in fishes without the MPJ. Further, fishes lacking the specialized trait showed faster rates of oral jaw functional evolution. In light of these findings in my 2nd and 3rd chapters, a reinterpretation of the macroevolutionary consequences of the MPJ is urgently needed. 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, the novelty also restricts the overall diversification of the feeding system, revealing that the impact of this novel trait is more nuanced than previously thought.