Evolution of novel jaw joints promote trophic diversity in coral reef fishes

Abstract

We investigated the functional morphology and ecology of biting among the squamipinnes, an assemblage of nine successful and distinctive reef fish families. We demonstrate that an intramandibular joint (IMJ) may have evolved at least three and possibly five times in this assemblage and discuss the impact of this recurring innovation in facilitating prey-capture by biting. Using character mapping on a supertree for the squamipinnes, we reveal up to seven gains or losses of intramandibular flexion, all associated with trophic transitions between free-living and attached prey utilization. IMJs are basal in six of the studied families whereas the origin of intramandibular flexion in the Chaetodontidae (butterflyfishes) coincides with a transition from ram-suction feeding to benthic coral feeding, with flexion magnitude reaching its peak (49 ± 2.7°) in the coral scraping subgenus Citharoedus. Although IMJs generally function to augment vertical gape expansion during biting behaviours to remove small invertebrates, algae or coral from the reef, the functional ecology of IMJs in the Pomacanthidae (angelfishes) stands in contrast. Pomacanthid IMJs exhibit over 35° of flexion, permitting gape closure when the jaws are fully protruded. We demonstrate the widespread IMJ occurrence among extant biters to result from a complex convergent evolutionary history, indicating that the IMJ is a major functional innovation that enhances biting strategies in several prominent reef fish groups.