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Validating venom variation and evolution in solitary and eusocial aculeate hymenopterans by comparative genomics, transcriptomics, and proteomics

Applicant Professor Dr. Ingo Ebersberger, since 1/2022
Subject Area Evolution, Anthropology
Ecology and Biodiversity of Animals and Ecosystems, Organismic Interactions
Systematics and Morphology (Zoology)
Term from 2018 to 2023
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 399287429
 
Final Report Year 2024

Final Report Abstract

Hymenoptera is one of the most species-rich insect groups, playing a significant role in both ecology and the economy. Despite the fact that they are renowned for their numerous venomous species, there is still a paucity of knowledge regarding the origin and evolution of their venom genes. The diversity of venom systems within Hymenoptera, which evolve from an ovipositor to a stinger, makes them ideal for studying the co-evolution of toxin genes linked to venom apparatuses. It is surprising that, despite recent advances in proteo-transcriptomics and genomics, large-scale studies on the genomic origins of toxin genes are generally scarce and focused on only a few taxa. Furthermore, such studies are lacking for hymenopterans. This project addresses this knowledge gap by examining venom variation between solitary and eusocial aculeates and investigating the origin and evolution of venom genes within these taxa. The project commenced with an initial focus on bees, encompassing the first comprehensive proteo-transcriptomic analyses on solitary bees. This highlighted the importance of comparing venom glandexpressed versus injected venom proteins. The initial findings indicate that the secreted venom components of solitary bees are largely analogous to those of eusocial bees. However, there is a notable difference in the expression levels of these components, with only a few distinctive components identified in both groups. In order to identify the genes responsible for the synthesis of bee venom proteins, a workflow combining proteomic, transcriptomic and genomic data was developed. In order to predict orthology and phylogenetic relationships of gene families, micro-syntenic patterns, tree reconstruction and a novel machine learning approach using deep learning-based large language models were employed. The results indicate that the majority of dominant bee venom genes were already present in early hymenopteran lineages prior to the evolution of the aculeate stinger, thereby suggesting the existence of a core set of venom genes across Hymenoptera. In bees sensu lato, toxins such as melittin and the novel gene family anthophilin originate in this clade. In contrast, toxins from other groups, such as ants, wasps and solitary wasps, are not found. Our findings suggest that hymenopterans possess a core venom that is adapted by different lineages and complemented with specific toxins. We can reject the hypothesis of a family of aculeatoxins that occur in all aculeates, including melittin and apamin. Interestingly, phylogenetically older melittin variants from solitary bees demonstrated in a translational study, promising effects on cancer cells, exhibiting reduced and thus more applicable toxicity to healthy cells compared to honeybee melittin.

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