Macroevolutionary role reversals in the earliest radiation of bony fishes

The evolution of jaws is hypothesized to have fueled radiations among vertebrates, contributing to their overwhelming success in the present day. Past work shows rapid early expansion of diversity in jaw structure in many lineages; however, the evolutionary dynamics underlying this pattern are unclear and hindered by the lack of a robust comparative framework. Here, using a macroevolutionary approach, we explore the diversification of lower jaws in early bony fishes, a major contributor to this initial radiation. Using newly generated three-dimensional mandibular shape data from 86 species, we find evidence of adaptive radiation in jaws during the earliest interval of bony fish evolutionary history (423–359 Ma). These patterns are principally driven by early lungfishes and coelacanths, which display high rates of jaw diversification, rapid shifts into novel functional regions of trait space, and substantial innovation in jaw morphology and feeding ecology, standing in contrast to their “living fossil” descendants of today. Conversely, ray-finned fishes and tetrapodomorphs, morphologically diverse groups in the present day, show little indication of their future success, possessing slow rates of jaw evolution and low functional diversity. This profound inversion of patterns in modern taxa highlights the significance of paleontological data in understanding drivers of evolutionary diversification and the limitations of approaches using only living species. Overall, our findings provide insight into the evolutionary dynamics associated with the evolution of jaws and provide context for the role of jaws in vertebrate success.