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Prevalent bee venom genes evolved before the aculeate stinger and eusociality

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 investigati...

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Autores principales: Koludarov, Ivan, Velasque, Mariana, Senoner, Tobias, Timm, Thomas, Greve, Carola, Hamadou, Alexander Ben, Gupta, Deepak Kumar, Lochnit, Günter, Heinzinger, Michael, Vilcinskas, Andreas, Gloag, Rosalyn, Harpur, Brock A., Podsiadlowski, Lars, Rost, Burkhard, Jackson, Timothy N. W., Dutertre, Sebastien, Stolle, Eckart, von Reumont, Björn M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10591384/
https://www.ncbi.nlm.nih.gov/pubmed/37867198
http://dx.doi.org/10.1186/s12915-023-01656-5
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author Koludarov, Ivan
Velasque, Mariana
Senoner, Tobias
Timm, Thomas
Greve, Carola
Hamadou, Alexander Ben
Gupta, Deepak Kumar
Lochnit, Günter
Heinzinger, Michael
Vilcinskas, Andreas
Gloag, Rosalyn
Harpur, Brock A.
Podsiadlowski, Lars
Rost, Burkhard
Jackson, Timothy N. W.
Dutertre, Sebastien
Stolle, Eckart
von Reumont, Björn M.
author_facet Koludarov, Ivan
Velasque, Mariana
Senoner, Tobias
Timm, Thomas
Greve, Carola
Hamadou, Alexander Ben
Gupta, Deepak Kumar
Lochnit, Günter
Heinzinger, Michael
Vilcinskas, Andreas
Gloag, Rosalyn
Harpur, Brock A.
Podsiadlowski, Lars
Rost, Burkhard
Jackson, Timothy N. W.
Dutertre, Sebastien
Stolle, Eckart
von Reumont, Björn M.
author_sort Koludarov, Ivan
collection PubMed
description 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01656-5.
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spelling pubmed-105913842023-10-24 Prevalent bee venom genes evolved before the aculeate stinger and eusociality Koludarov, Ivan Velasque, Mariana Senoner, Tobias Timm, Thomas Greve, Carola Hamadou, Alexander Ben Gupta, Deepak Kumar Lochnit, Günter Heinzinger, Michael Vilcinskas, Andreas Gloag, Rosalyn Harpur, Brock A. Podsiadlowski, Lars Rost, Burkhard Jackson, Timothy N. W. Dutertre, Sebastien Stolle, Eckart von Reumont, Björn M. BMC Biol Research Article 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01656-5. BioMed Central 2023-10-23 /pmc/articles/PMC10591384/ /pubmed/37867198 http://dx.doi.org/10.1186/s12915-023-01656-5 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Koludarov, Ivan
Velasque, Mariana
Senoner, Tobias
Timm, Thomas
Greve, Carola
Hamadou, Alexander Ben
Gupta, Deepak Kumar
Lochnit, Günter
Heinzinger, Michael
Vilcinskas, Andreas
Gloag, Rosalyn
Harpur, Brock A.
Podsiadlowski, Lars
Rost, Burkhard
Jackson, Timothy N. W.
Dutertre, Sebastien
Stolle, Eckart
von Reumont, Björn M.
Prevalent bee venom genes evolved before the aculeate stinger and eusociality
title Prevalent bee venom genes evolved before the aculeate stinger and eusociality
title_full Prevalent bee venom genes evolved before the aculeate stinger and eusociality
title_fullStr Prevalent bee venom genes evolved before the aculeate stinger and eusociality
title_full_unstemmed Prevalent bee venom genes evolved before the aculeate stinger and eusociality
title_short Prevalent bee venom genes evolved before the aculeate stinger and eusociality
title_sort prevalent bee venom genes evolved before the aculeate stinger and eusociality
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10591384/
https://www.ncbi.nlm.nih.gov/pubmed/37867198
http://dx.doi.org/10.1186/s12915-023-01656-5
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