Evolutionary dynamics of collective behavior across the tree of ray-finned fishes

Abstract Trait evolution and lineage diversification are thought to be driven by selection on the phenotypes of individuals. However, many important phenotypes are only manifested when individuals interact. Collective behavior is one such phenotype. During collective behavior, interactions among individuals lead to emergent group-level phenotypes that can govern individual fitness. Yet, whether collective behaviors exhibit similar patterns of trait evolution to individual traits and whether these group phenotypes have influenced macroevolutionary diversification is unknown. In ray-finned fishes, the most species-rich of all vertebrate classes, many species exhibit striking displays of collective behavior in the form of collective movement. Here, we use state-of-the-art machine learning methods for text and image analysis to quantify collective movement phenotypes for 2,839 Actinopterygian fishes, comprising nearly 10% of all extant species. We find that collective movement is highly evolutionarily stable in some clades and extremely labile in others, exhibiting over 300 evolutionary transitions. Consistent with theoretical predictions, collective movement is associated with more patchy diets and higher predation pressure. Finally, we find that the evolution of collective movement coincides with an increase in net macroevolutionary diversification rate. Our analyses reveal that collective behavior is deeply intertwined with ecological and evolutionary dynamics across a vast phylogenetic scale, unlocking new questions about the role of collective phenotypes in shaping the diversity of life on Earth. Significance Collective behavior is thought to contribute to the fitness of individuals that live in groups, but we still do not understand why some species exhibit collective behavior and others do not. We developed machine learning methods to quantify collective phenotypes for thousands of species spanning the phylogeny of ray-finned fishes and found collective behavior to be widespread and consistently correlated with experiencing higher predation pressure and foraging for grouping prey. Lineages that evolve collective movement show a higher net diversification rate. Our results illustrate that collective behavior is foundational to the broad-scale patterns of evolution and diversification in the largest vertebrate class.