Phylogenomics reveals the evolutionary relationships between nesting and brooding behaviours and morphological structures in vespid wasps

Abstract

Vespid wasps (family Vespidae) exhibit remarkable behavioural and ecological diversity, making them an ideal model for studying the evolution of insect adaptations, particularly regarding nesting and brooding habits. To elucidate the evolutionary mechanisms underlying these traits, we reconstructed the phylogeny of Vespidae using 5820 universal single‐copy orthologues (USCOs) and 2467 ultraconserved elements (UCEs). Our dataset integrated 32 newly sequenced low‐coverage whole genomes from the subfamily Eumeninae with public genomic and transcriptomic data. The resulting phylogenomic framework, Stenogastrinae + (Masarinae + (Eumeninae + (Zethinae + (Polistinae + Vespinae)))), is consistent with mitochondrial and anchored hybrid enrichment (AHE) phylogenies. Within Eumeninae, our results suggest a reclassification into at least four distinct tribes. Divergence time estimation indicates that the radiation of nesting and brooding strategies in vespids coincided with the diversification of angiosperms and key prey groups, such as lepidopteran larvae. Ancestral state reconstruction reveals that the evolution of specialized mandibles and metasomal structures closely mirrors the phylogenetic transitions in brooding and nesting behaviours. Specifically, larval food provisioning and nest security appear to be associated with these morphological adaptations. These findings highlight the synergistic evolution of morphology and behaviour in Vespidae and provide a robust framework for further exploring the drivers of social and ecological diversification in wasps.