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Chemical Deception and Structural Adaptation in Microdon (Diptera, Syrphidae, Microdontinae), a Genus of Hoverflies Parasitic on Social Insects

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Abstract

Various organisms, especially arthropods, are able to live as parasites in ant nests and to prey upon ant broods without eliciting any aggressive behaviour in the hosts. Understanding how these intruders are able to break the ants’ communication codes in their favour represents a challenging and intriguing evolutionary question. We studied the chemical strategies of three European hoverfly species, Microdon mutabilis (parasitic on Formica cunicularia), M. analis (parasitic on Lasius emarginatus) and M. devius (parasitic on L. distinguendus). The peculiar slug-like larvae of these three species live inside ant nests feeding upon their broods. Gas chromatography-mass spectrometry analyses show that: 1) these parasites mimic the host brood rather than the ant workers, although each differs distinctly in the extent of chemical mimicry; 2) isolation experiments indicate that after 14 days the responsible cuticular hydrocarbons (CHCs) are not passively acquired but synthesized by the fly larvae. Additionally, Microdon larvae show an array of protective structural features, such as a thick and multi-layered cuticle, retractable head, dome-shaped tergum and a flat and strongly adhesive “foot” (sternum). This combination of protective chemical and structural features represents a successful key innovation by Microdon species, and one that may facilitate host switching. The results of a preliminary adoption analysis confirm that Microdon larvae of at least some species can readily be accepted by different species of ants.

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Acknowledgments

We are indebted to our friend Robert Wolton (UK) for the English revision of the text and for his precious comments and suggestions that widely improved the manuscript. We are very grateful to our colleagues Marco Molfini, Luigi Cao Pinna and Francesco Simone Mensa for their help during the field sampling and Chloé Leroy for her support during gas chromatography-mass spectrometry analysis. Electron microscopy analyses were done at L.I.M.E. (Laboratorio Interdipartimentale Microscopia Elettronica) of University of Roma Tre and funded by Department of Science Research Grants (CAL Di Giulio 2017) and the Grant of Excellence Departments, MIUR-Italy (ARTICOLO 1, COMMI 314 – 337 LEGGE 232/2016). P. d’Ettorre was funded by the French National Research Agency (ANR-14-CE18-0003, PHEROMOD). We are grateful to two anonymous referees for their useful suggestions.

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Authors and Affiliations

  1. Department of Science, University Roma Tre, Viale G. Marconi 446, 00146, Rome, Italy

    G. Scarparo & A. Di Giulio

  2. Laboratorio Interdipartimentale di Microscopia Elettronica (LIME), University Roma Tre, Rome, Italy

    G. Scarparo & A. Di Giulio

  3. Laboratoire d′Ethologie Expérimentale et Comparée, Université Paris 13 Sorbonne Paris Cité, 93430, Villetaneuse, France

    P. d’Ettorre

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  1. G. Scarparo
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Correspondence to A. Di Giulio.

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Scarparo, G., d’Ettorre, P. & Di Giulio, A. Chemical Deception and Structural Adaptation in Microdon (Diptera, Syrphidae, Microdontinae), a Genus of Hoverflies Parasitic on Social Insects. J Chem Ecol 45, 959–971 (2019). https://doi.org/10.1007/s10886-019-01121-0

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