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Venom chemistry underlying the painful stings of velvet ants (Hymenoptera: Mutillidae)

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Abstract

Velvet ants (Hymenoptera: Mutillidae) are a family of solitary parasitoid wasps that are renowned for their painful stings. We explored the chemistry underlying the stings of mutillid wasps of the genus Dasymutilla Ashmead. Detailed analyses of the venom composition of five species revealed that they are composed primarily of peptides. We found that two kinds of mutillid venom peptide appear to be primarily responsible for the painful effects of envenomation. These same peptides also have defensive utility against invertebrates, since they were able to incapacitate and kill honeybees. Both act directly on cell membranes where they directly increase ion conductivity. The defensive venom peptides of Dasymutilla bear a striking similarity, in structure and mode of action, to those of the ant Myrmecia gulosa (Fabricius), suggesting either retention of ancestral toxins, or convergence driven by similar life histories and defensive selection pressures. Finally, we propose that other highly expressed Dasymutilla venom peptides may play a role in parasitisation, possible in delay or arrest of host development. This study represents the first detailed account of the composition and function of the venoms of the Mutillidae.

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Precursor sequences of venom peptides have been deposited with GenBank under accessions MW323130–MW323158 (D. klugii), MW323159–MW323187 (D. bioculata), MW323188–MW323215 (D. gloriosa), MW323216–MW323243 (D. occidentalis), and MW323244–MW323300 (D. sicheliana). Raw sequencing data have been deposited in the NCBI sequence read archive under accessions SRR13038346 (D. klugii), SRR13038345 (D. gloriosa), SRR13038344 (D. bioculata), SRR13038343 (D. sicheliana), and SRR13038342 (D. occidentalis).

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Acknowledgements

This work was funded by the Australian Research Council (Discovery Project DP190103787 to G.F.K., S.D.R, I.V.) and a National Geographic Society early career grant (EC-58468R-19 to S.D.R.). GFK is supported by Principal Research Fellowship APP1136889 from the Australian National Health & Medical Research Council. Henrik Y. O’Brien assisted with specimen collection. Apis mellifera were provided by Peter Ryan.

Funding

This work was funded by the Australian Research Council (Discovery Project DP190103787 to G.F.K., S.D.R, I.V.) and a National Geographic Society early career grant (EC-58468R-19 to S.D.R.). GFK is supported by Principal Research Fellowship APP1136889 from the Australian National Health & Medical Research Council.

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Conceptualisation, JOS, SDR; methodology, IV, JOS and SDR; investigation, TJ, AA, SHN, AHJ, JRD, JOS and SDR; writing—original draft, TJ, SDR; writing—review and editing, all authors; funding acquisition, IV, GFK and SDR; resources, IV, GFK, JOS and SDR; supervision, IV, GFK and SDR.

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Correspondence to Samuel D. Robinson.

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Experiments involving animals or animal tissue were approved by The University of Queensland animal ethics committee (UQ AEC).

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Jensen, T., Walker, A.A., Nguyen, S.H. et al. Venom chemistry underlying the painful stings of velvet ants (Hymenoptera: Mutillidae). Cell. Mol. Life Sci. 78, 5163–5177 (2021). https://doi.org/10.1007/s00018-021-03847-1

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