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Prevalent bee venom genes evolved before the aculeate stinger and eusociality Ivan Koludarov 1390163 2881201-1390163 https://orcid.org/0000-0002-9073-4758 Mariana Velasque 3169383-0 Tobias Senoner 3169384-0 Thomas Timm 1497719-0 Carola Greve 809790 2299072-809790 https://orcid.org/0000-0003-4993-1378 Alexander Ben Hamadou 2781871-0 Deepak Kumar Gupta 2089509-0 Günter Lochnit 2343246-0 Michael Heinzinger 1476116 2922184-1476116 https://orcid.org/0000-0002-9601-3580 Andreas Vilcinskas cdb723b56b5623f2a65648dce4368ed9 agrar.uni-giessen.de 867583 444665-867583 https://orcid.org/0000-0001-8276-4968 Rosalyn Gloag c11e6410dbba4a6a6a1c4fc89b22f0cf sydney.edu.au 1069408 1841130-1069408 https://orcid.org/0000-0002-2037-4267 Brock A. Harpur b8c7354a6ae77a8d404455824256f574 purdue.edu 1124749 1037388-1124749 https://orcid.org/0000-0001-8722-272X Lars Podsiadlowski 1813379-0 Burkhard Rost 1202752 1228485-1202752 https://orcid.org/0000-0003-0179-8424 Timothy N W Jackson 505bc55723e3d25d17224ab620fdc2d3 unimelb.edu.au 1054918 1658700-1054918 Sébastien Dutertre bb73ab3a7cb4f31e3fd37b45b69c574c univ-montp2.fr sebastien-dutertre 1117559 814854-1117559 https://orcid.org/0000-0002-2945-1484 https://www.idref.fr/185528236 Eckart Stolle 3169386-0 Björn Marcus von Reumont 1413942 1665460-1413942 https://orcid.org/0000-0002-7462-8226 Camille Dubernet 059deec6c579cc8bd11b0348d9426f5a umontpellier.fr BMvR and IK thank the German Science Foundation (DFG) for funding this work by a grant to BMvR (DFG RE3454/6–1). BMvR and AV acknowledge generous funding obtained by AV from the Hessian Ministry of Higher Education, Research, and the Arts for the group “Animal Venomics”, which was coordinated by BMvR until end of 2021 at the Institute for Insectbiotechnology at the Justus Liebig University, embedded in the LOEWE Centre for Translational Biodiversity Genomics. 2024-12-12 11:02:28 2026-05-05 16:37:44 2024-12-16 15:49:41 2023-10-23 2024-12-12 contributor Camille Dubernet 059deec6c579cc8bd11b0348d9426f5a umontpellier.fr CCSD hal-04605047 https://hal.umontpellier.fr/hal-04605047 koludarov:hal-04605047 <i>BMC Biology</i>, 2023, 21 (1), pp.229. <a target="_blank" href="https://dx.doi.org/10.1186/s12915-023-01656-5">⟨10.1186/s12915-023-01656-5⟩</a> BMC Biology, 2023, 21 (1), pp.229. ⟨10.1186/s12915-023-01656-5⟩ CC BY 4.0 - Attribution Sciences De l'Environnement CNRS - Centre national de la recherche scientifique Ecole Nationale Supérieure de Chimie de Montpellier Institut des Biomolécules Max Mousseron GIP Bretagne Environnement Institut de Chimie du CNRS Chimie Université de Montpellier Université de Montpellier (2015-2021) Université de Montpellier - EPE Publications linked to dataset and software International No Yes Prevalent bee venom genes evolved before the aculeate stinger and eusociality Ivan Koludarov 1390163 2881201-1390163 https://orcid.org/0000-0002-9073-4758 Mariana Velasque 3169383-0 Tobias Senoner 3169384-0 Thomas Timm 1497719-0 Carola Greve 809790 2299072-809790 https://orcid.org/0000-0003-4993-1378 Alexander Ben Hamadou 2781871-0 Deepak Kumar Gupta 2089509-0 Günter Lochnit 2343246-0 Michael Heinzinger 1476116 2922184-1476116 https://orcid.org/0000-0002-9601-3580 Andreas Vilcinskas cdb723b56b5623f2a65648dce4368ed9 agrar.uni-giessen.de 867583 444665-867583 https://orcid.org/0000-0001-8276-4968 Rosalyn Gloag c11e6410dbba4a6a6a1c4fc89b22f0cf sydney.edu.au 1069408 1841130-1069408 https://orcid.org/0000-0002-2037-4267 Brock A. Harpur b8c7354a6ae77a8d404455824256f574 purdue.edu 1124749 1037388-1124749 https://orcid.org/0000-0001-8722-272X Lars Podsiadlowski 1813379-0 Burkhard Rost 1202752 1228485-1202752 https://orcid.org/0000-0003-0179-8424 Timothy N W Jackson 505bc55723e3d25d17224ab620fdc2d3 unimelb.edu.au 1054918 1658700-1054918 Sébastien Dutertre bb73ab3a7cb4f31e3fd37b45b69c574c univ-montp2.fr sebastien-dutertre 1117559 814854-1117559 https://orcid.org/0000-0002-2945-1484 https://www.idref.fr/185528236 Eckart Stolle 3169386-0 Björn Marcus von Reumont 1413942 1665460-1413942 https://orcid.org/0000-0002-7462-8226 313 1741-7007 1741-7007 BMC Biology BioMed Central 21 1 229 2023-10-23 10.1186/s12915-023-01656-5 37867198 PMC10591384 English Hymenoptera venom Bee toxins Proteo-transcriptomics Solitary bee venom Genomics Venom gene evolution Machine learning Melittin Apamin Aculeatoxins Environmental Sciences/Biodiversity and Ecology Life Sciences [q-bio]/Animal biology Journal articles Journal articles Journal articles

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.

Justus-Liebig-Universität Gießen = Justus Liebig University JLU 2017-01-24

Ludwigstraße 23, 35390 Gießen

http://www.uni-giessen.de/index.html 031660150 0000000123369749 https://ror.org/02kkvpp62 Q157808 Technische Universität Munchen = Technical University Munich = Université Technique de Munich TUM 1868-01-01

Arcisstrasse 21, D- 80333 München

https://www.tum.de https://ror.org/02qg15b79 Okinawa Institute of Science and Technology Graduate University OIST

1919-1 Tancha, Onna-son, Kunigami-gunOkinawa, Japan 904-0495

https://www.oist.jp/ LOEWE Centre for Translational Biodiversity Genomics (LOEWE-TBG)

Fraunhofer Institute for Molecular Biology and Applied Ecology Fraunhofer IME

https://www.ime.fraunhofer.de/en.html The University of Sidney

https://www.sydney.edu.au/ https://ror.org/02dqehb95 Purdue University [West Lafayette]

Hovde Hall, 610 Purdue Mall, West Lafayette, IN 47907

https://www.purdue.edu/ https://ror.org/00wz4b049 Zoologisches Forschungsmuseum Alexander Koenig

Adenauerallee 16053113 Bonn

https://www.zfmk.de/de Leibniz Institute for the Analysis of Biodiversity Change LAB

Adenauerallee 127, 53113 Bonn, Germany

https://ror.org/01ej9dk98 University of Melbourne

Parkville VIC 3010

http://www.unimelb.edu.au/ 200711912X https://ror.org/05d1e6v30 Institut des Biomolécules Max Mousseron [Pôle Chimie Balard] IBMM 2022-01-01

CNRS - 1919 Route de Mende34293 Montpellier cedex 5

http://www.ibmm.univ-montp1.fr 0000 0004 1936 9721 https://ror.org/04cvxnb49 Goethe University Frankfurt = Goethe-Universität Frankfurt am Main 1914-01-01

Theodor-W.-Adorno-Platz 1 , 60323 Frankfurt am Main

http://www.goethe-university-frankfurt.de/en? Partenaires INRAE

Cette structure regroupe l'ensemble des structures créées pour la reprise des données ProdInra

0000 0000 9261 3939 https://ror.org/05hkkdn48 Fraunhofer Fraunhofer-Gesellschaft

Hansastraße 27c, 80686 München

https://www.fraunhofer.de/en.html 232435103 000000010626358X https://ror.org/02cte4b68 Institut de Chimie - CNRS Chimie INC-CNRS 2009-10-01

CENTRE NATIONAL DE LA RECHERCHE SCIENTIFIQUE3 rue Michel-Ange75794 PARIS CEDEX 16 - France

http://www.cnrs.fr/inc 02636817X 0000000122597504 https://ror.org/02feahw73 Centre National de la Recherche Scientifique CNRS 1939-10-19

https://www.cnrs.fr/ https://ror.org/051escj72 Université de Montpellier UM 2022-01-01

163 rue Auguste Broussonnet - 34090 Montpellier

http://www.umontpellier.fr/ https://ror.org/03sgyqj04 Ecole Nationale Supérieure de Chimie de Montpellier ENSCM 2022-01-01

8 Rue de l'Ecole Normale 34296 Montpellier Cedex 5

http://www.enscm.fr