A common venomous ancestor? Prevalent bee venom genes evolved before the aculeate stinger while few major toxins are bee-specific

Venoms, which have evolved numerous times in animals, are ideal models of convergent trait evolution. However, detailed genomic studies of toxin-encoding genes exist for only a few animal groups. The hyper-diverse hymenopteran insects are the most speciose venomous clade, but investigation of the origin of their venom genes has been largely neglected. Utilising a combination of genomic and proteo-transcriptomic data, we investigated the origin of 11 toxin genes in 29 published and three new hymenopteran genomes and compiled an up-to-date list of prevalent bee venom proteins. Observed patterns indicate that bee venom genes predominantly originate through single gene co-option with gene duplication contributing to subsequent diversification. Most Hymenoptera venom genes are shared by all members of the clade and only melittin and the new venom protein family anthophilin appear unique to the bee lineage. Most venom proteins thus predate the mega-radiation of hymenopterans and the evolution of the aculeate stinger.动物体内的毒液已独立演化多次，是趋同性状演化研究的理想模型。然而，目前仅针对少数动物类群开展了毒素编码基因的精细化基因组研究。高度多样化的膜翅目（Hymenoptera）昆虫是物种多样性最高的有毒演化支，但其毒液基因起源的相关研究长期遭到严重忽视。本研究结合基因组与蛋白质组-转录组联合数据，对29个已发表及3个新测序的膜翅目基因组中的11个毒素基因的起源展开了分析，并编制了涵盖常见蜜蜂毒液蛋白的最新名录。观测结果显示，蜜蜂毒液基因主要通过单基因共招募演化而来，基因复制事件为后续的功能多样化提供了重要支撑。绝大多数膜翅目毒液基因为该演化支的所有类群所共有，仅蜂毒肽（melittin）与新型毒液蛋白家族花青素（anthophilin）为蜜蜂谱系所特有。由此可见，多数毒液蛋白的起源早于膜翅目的大辐射演化以及针尾类（aculeate）螫刺的演化。