The macroevolutionary dynamics of pharyngognathy in fishes fail to support the key innovation hypothesis

Abstract

Abstract Key innovations, traits that provide species access to novel niches, are thought to be a major generator of biodiversity. One commonly cited example of key innovation is pharyngognathy, a set of modifications to the pharyngeal jaws found in some highly species-rich fish clades such as cichlids and wrasses. Here, using comparative phylogenomics and phylogenetic comparative methods, we investigate the genomic basis of pharyngognathy and the impact of this innovation on diversification. Whole genomes resolve the relationships of fish clades with this innovation and their close relatives, but high levels of topological discordance suggest the innovation may have evolved fewer times than previously thought. Closer examination of the topology of noncoding elements accelerated in clades with the pharyngognathy innovation reveals hidden patterns of shared ancestry across putatively independent transitions to pharyngognathy. When our updated phylogenomic relationships are used alongside large-scale phylogenetic and ecological datasets, we find no evidence pharyngognathy consistently modifies the macroevolutionary landscape of trophic ecology nor does it increase diversification. Our results highlight the necessity of incorporating genomic information in studies of key innovation.