Ecological Limits on the Decoupling of Prey Capture and Processing in Fishes

Abstract

Synopsis Ray-finned fishes have two jaw systems, the oral and pharyngeal jaws, which perform functions associated with prey capture and processing, respectively. The structural independence of the jaw systems is recognized as having broad implications for the functional and ecological diversity of the radiation. Cichlids (and a few other lineages) possess a modified pharyngeal jaw system that enhances prey processing versatility and capacity. This innovation, pharyngognathy, is hypothesized to have freed the oral jaws to diversify in terms of prey capture. We test the relative role of prey capture properties (e.g., evasiveness) and prey processing (e.g., crushing) in driving divergent selection in the oral and pharyngeal jaws using a macroevolutionary model fitting framework. Evolutionary outcomes were asymmetric. All transitions between different properties of prey capture had a corresponding transition in properties of prey processing. In contrast, fewer than half the transitions in the properties of prey processing had a corresponding prey capture transition. This discrepancy was further highlighted by multi-peak models that reflect the opposing function of each jaw system, which fit better than null models for oral jaw traits, but not pharyngeal jaw traits. These results suggest that pharyngeal jaw function can change independently from the function of the oral jaws, but not vice versa. This finding highlights the possibility of ecological limits to the evolutionary decoupling of jaw systems. The independent actions of prey capture and processing may be decoupled, but their respective functional demands (and evolution) are not. Therefore, prey likely impose some degree of coordinated evolution between acquisition and processing functional morphology, even in decoupled jaw systems.