Untangling the Evolutionary Dynamics of the Phenome in Megadiverse Hymenoptera

Key innovations are traits that enable and/or facilitate the radiation of lineages often in association with the invasion of new adaptive zones. Despite their importance for understanding phenotypic macroevolutionary dynamics in megadiverse lineages, these traits are usually treated in isolation ignoring the context within organismal anatomy and potential trait synergies. Furthermore, what is often interpreted as a key innovation might represent an evolutionary singular event at the origin of a new body plan affecting multiple morphological traits at once. Here we argue that the formation of the typical “wasp waist” of apocritan Hymenoptera represents such a macroevolutionary singular event. We employed a set of newly developed ontology-informed comparative tools to assess the evolution of the phenome of Hymenoptera based on a dataset including adult and larval characters. We showed that the phenotypic diversification process in Hymenoptera simultaneously affected multiple anatomical complexes and was characterized by fast evolutionary rates and strong directional selection at branches leading to major lineages–—particularly Vespina and Apocrita—–during the Late Triassic (201∼237 Ma). Additionally, evolutionary rates of adult and larval phenomes were decoupled suggesting that distinct phenotypic diversification processes characterized different ontogenetic stages in Hymenoptera. Lastly, no clear association was recovered between phenotypic and lineage diversification rates for any morphological complex of the adult or the larval phenome. These results suggest that some key innovations might have a delayed effect on linage diversification, as observed in other recent studies.