Phenome-wide adaptive radiation drives lineage diversification in hyperdiverse Hymenoptera

Abstract

How complex phenotypes evolve across the Tree of Life remains poorly understood because phenotypic evolution unfolds across multiple hierarchical and developmental scales. Hymenoptera (ants, wasps, and bees) represent one of the largest animal radiations (>150,000 species), yet the origin of their remarkable phenotypic diversity remains unclear. Here, we reconstruct the evolution of the hymenopteran skeletomuscular phenome and analyze its dynamics across anatomical hierarchies and developmental stages. We show that hymenopteran adaptive radiation was a phenome-wide process facilitated by evolutionary decoupling between adults and larvae and the semi-independent evolution of adult anatomical systems. Phenotypic and lineage diversification was driven not simply by key innovations or elevated phenomic rates, but by the partitioning of evolutionary innovation across anatomical systems, generating a broader repertoire of adaptive solutions. These findings extend the classical view of adaptive radiation from individual key innovations to phenome-wide reorganization.