Bee venom genes predominately originated in ancestors of sawfly hymenopterans before the aculeate stinger evolved

To study convergent trait evolution, venoms that evolved multiple times in animals are ideal models. However, only few animal groups are studied in detail at the genomic level to understand toxin gene evolution. Hyper-diverse hymenopterans are the most speciose venomous animals, but the origin of their toxin genes has been largely overlooked despite their adaptive significance. We combined genomics with proteo-transcriptomics to compile an up-to-date list of core bee venom proteins and investigated the origin of 11 toxin genes in 30 hymenopteran genomes. We found that bee venom toxins originated predominantly by single gene co-option combined with gene duplication. Only melittin and the new venom protein family anthophilin appear unique to the bee lineage. Other toxins already existed in earliest hymenopterans before aculeates evolved their stinger. We elucidate here toxin gene origin at the genomic level during the mega-radiation of hymenopterans with general implications on the evolution of gene function.