Untangling the Evolutionary Dynamics of the Phenome in Megadiverse Hymenoptera

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Abstract
Hymenoptera is a megadiverse insect order, yet the drivers of its massive radiation remain poorly understood. Here, we employ novel comparative phylogenetic methods that integrate computational ontologies with ancestral state reconstructions of 346 discrete morphological characters to investigate the tempo and mode of phenome evolution in Hymenoptera across both adults and larvae. We examine the interplay between phenotypic rates, selection, modularity, and lineage diversification over deep time. Our analyses reveal that both larval and adult phenomes experienced an early burst scenario during the Late Permian – Triassic. However, their evolution appears decoupled, which enhanced the overall evolvability of Hymenoptera. Moreover, major phenotypic transitions in the order are complex, multifaceted processes driven by directional selection. One such event—the emergence of the wasp waist— involved a fundamental reorganization of the adult phenome. This dramatic transformation shifted net diversification from negative to positive during the Triassic, thereby enabling the subsequent survival and explosive diversification of the apocritan lineage.

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