Prevalent bee venom genes evolved before the aculeate stinger and eusociality

Abstract

Background 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. Results Utilizing a combination of genomic and proteo-transcriptomic data, we investigated the origin of 11 toxin genes in 29 published and 3 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. Conclusions Most Hymenoptera venom genes are shared by all members of the clade and only melittin and the new venom protein family anthophilin1 appear unique to the bee lineage. Most venom proteins thus predate the mega-radiation of hymenopterans and the evolution of the aculeate stinger.

The genome of the ant Tetramorium bicarinatum reveals a tandem organization of venom peptides genes allowing the prediction of their regulatory and evolutionary profiles

“…The global vpg organization is consistent with a common ancestor in each precursor family and diversification by local tandem duplication. Genomic studies in other venomous animals such as snake [ 32 , 33 ], sea anemones [ 34 ], spider [ 35 ], cone [ 36 ], and Apidae [ 10 ] showed also tandem duplication of some genes coding venom peptide toxins. The number of paralogous genes within A1 and C1 families may indicate an ancient origin of these vpg or a high frequency of duplication.…”

“…However, these proteo-transcriptomic studies rarely include genomic data yet being essential for understanding the evolution of toxins. For instance, the inclusion of genomic data has revealed that venom toxins undergo various genetic mechanisms in different insect lineages such asilid flies [ 8 ], parasitoid wasps [ 9 ], and recently bees [ 10 ].…”

“…Robinson and colleagues noted that most of the venom peptide sequences described in aculeate Hymenoptera vary widely in their mature parts but shared similar pre-pro sequences suggesting a common origin and proposed to group these toxins into a single gene family called Aculeatoxins [ 13 ]. However, evolutionary analyses performed by Koladorov et al on a dataset containing bee, wasp and ant venom peptides do not support this hypothesis, as ant venom peptides clustered differently from the others [ 10 ]. Thus, the evolution of Hymenoptera venoms appears to be much more complex than originally thought and warrants further investigations.…”

The genome sequence of the Violet Carpenter Bee, Xylocopa violacea (Linnaeus, 1785): a hymenopteran species undergoing range expansion.

“…We generated 149,032,417, 107,159,638, 116,609,061, and 148,189,077 Illumina RNA-seq short reads respectively for the head, thorax, abdomen, and legs. Additional RNA-seq reads, from X. violacea venom gland, were downloaded from SRA (SRR14690757, Koludarov et al, 2023). The same extractions were also used to generate 790,150; 717,956; 977,170, and 999,264 PacBio Iso-Seq long reads for the head, thorax, abdomen, and legs respectively.…”

“…X. violacea also exhibits lineage specific traits such as its microbiome (Alberoni et al, 2019;Holley et al, 2022;Handy et al, 2023) and a distinctive venom profile with novel melittin variants that show potential for anticancer applications (von Reumont et al, 2022;Erkoc et al, 2022). There is only a contig-level assembly of the X. violacea genome currently available (Koludarov et al, 2023).…”