Prevalent bee venom genes evolved before the aculeate stinger and eusociality

Ivan Koludarov; Mariana Velasque; Tobias Senoner; Thomas Timm; Carola Greve; Alexander Ben Hamadou; Deepak Kumar Gupta; Günter Lochnit; Michael Heinzinger; Andreas Vilcinskas; Rosalyn Gloag; Brock A Harpur; Lars Podsiadlowski; Burkhard Rost; Timothy N W Jackson; Sebastien Dutertre; Eckart Stolle; Björn M von Reumont

doi:10.1186/s12915-023-01656-5

Prevalent bee venom genes evolved before the aculeate stinger and eusociality

BMC Biol. 2023 Oct 23;21(1):229. doi: 10.1186/s12915-023-01656-5.

Authors

Ivan Koludarov^{1

2}, Mariana Velasque³, Tobias Senoner⁴, Thomas Timm⁵, Carola Greve⁶, Alexander Ben Hamadou⁶, Deepak Kumar Gupta⁶, Günter Lochnit⁵, Michael Heinzinger⁴, Andreas Vilcinskas^{7

8}, Rosalyn Gloag⁹, Brock A Harpur¹⁰, Lars Podsiadlowski¹¹, Burkhard Rost⁴, Timothy N W Jackson¹², Sebastien Dutertre¹³, Eckart Stolle¹¹, Björn M von Reumont^{14

15}

Affiliations

¹ Justus Liebig University of Gießen, Institute for Insect Biotechnology, Heinrich-Buff-Ring 58, 35392, Giessen, Germany. atjcoludar@gmail.com.
² Department of Informatics, Bioinformatics and Computational Biology, i12, Technical University of Munich, Boltzmannstr. 3, Garching, 85748, Munich, Germany. atjcoludar@gmail.com.
³ Genomics & Regulatory Systems Unit, Okinawa Institute of Science & Technology, Tancha, Okinawa, 1919, Japan.
⁴ Department of Informatics, Bioinformatics and Computational Biology, i12, Technical University of Munich, Boltzmannstr. 3, Garching, 85748, Munich, Germany.
⁵ Protein Analytics, Institute of Biochemistry, Justus Liebig University, Friedrichstrasse 24, 35392, Giessen, Germany.
⁶ LOEWE Centre for Translational Biodiversity Genomics (TBG), Senckenberganlage 25, 60325, Frankfurt, Germany.
⁷ Justus Liebig University of Gießen, Institute for Insect Biotechnology, Heinrich-Buff-Ring 58, 35392, Giessen, Germany.
⁸ Fraunhofer Institute for Molecular Biology and Applied Ecology, Department of Bioresources, Ohlebergsweg 12, 35392, Giessen, Germany.
⁹ Rosalyn Gloag - School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, 2006, Australia.
¹⁰ Brock A. Harpur - Department of Entomology, Purdue University, 901 W. State Street, West Lafayette, IN, 47907, USA.
¹¹ Leibniz Institute for the Analysis of Biodiversity Change, Zoological Research Museum Alexander Koenig, Centre of Molecular Biodiversity Research, Adenauerallee 160, 53113, Bonn, Germany.
¹² Australian Venom Research Unit, Department of Biochemistry and Pharmacology, University of Melbourne, Grattan Street, Parkville, Viktoria, 3010, Australia.
¹³ IBMM, Université Montpellier, CNRS, ENSCM, 34095, Montpellier, France.
¹⁴ LOEWE Centre for Translational Biodiversity Genomics (TBG), Senckenberganlage 25, 60325, Frankfurt, Germany. bmvr@reumont.net.
¹⁵ Faculty of Biological Sciences, Group of Applied Bioinformatics, Goethe University Frankfurt, Max-Von-Laue Str. 13, 60438, Frankfurt, Germany. bmvr@reumont.net.

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.

Keywords: Aculeatoxins; Apamin; Bee toxins; Genomics; Hymenoptera venom; Machine learning; Melittin; Proteo-transcriptomics; Solitary bee venom; Venom gene evolution.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Bee Venoms*
Bees / genetics
Gene Duplication
Gene Expression Profiling
Genomics
Transcriptome

Substances

Bee Venoms