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No evidence for long-range male sex pheromones in two malaria mosquitoes

Nature Ecology & Evolution volume 6, pages 1676–1686 (2022)Cite this article

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Abstract

Cues involved in mate seeking and recognition prevent hybridization and can be involved in speciation processes. In malaria mosquitoes, females of the two sibling species Anopheles gambiae s.s. and An. coluzzii mate in monospecific male swarms and hybrids are rare. Long-range sex pheromones driving this behaviour have been debated in literature but so far, no study has proven their existence or their absence. Here, we attempted to bring to light their existence. To put all the odds in our favour, we used different chemical ecology methods such as behavioural and electrophysiological assays as well chemical analyses, and we worked with mosquitoes at their optimal physiological mating state that is with swarming males during their natural swarming windows. Despite all our efforts, our results support the absence of long-range sex pheromones involved in swarm detection and recognition by females. We briefly discuss the implications of this finding in ecology, evolution and for control strategies.

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Fig. 1: Schematic of the olfactometer set-up.
Fig. 2: Mosquito activation rate, expressed as the proportion of females caught in both collecting boxes out of the total number released females for each of the four tested combinations.
Fig. 3: Mosquito choice, expressed as the proportion of females caught in one or the other collecting box out of the total number of ‘activated’ females for each test.
Fig. 4: Quantities of acetoin, sulcatone, octanal, nonanal and decanal collected with SPME fibres.
Fig. 5: Quantities of sulcatone, octanal, nonanal and decanal collected with Twisters, Tenax/Carbotrap or Porapack tubes.
Fig. 6: Mean electrophysiological responses of female An. coluzzii antennae to male swarm solvent extracts, recorded by GC–EAD.

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Data availability

The raw datasets are available online at https://doi.org/10.5281/zenodo.4719568.

Code availability

Script and codes are available online at https://doi.org/10.5281/zenodo.4719568.

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Acknowledgements

We thank D. Sanou for his assistance in the field, S. Somda, S. Somé, B. Scheid, M. Rossignol and C. Ginibre for their help in mosquito rearing and H. Lançon for proofreading the paper. This work was funded by a grant from the Agence Nationale de la Recherche (grant no. ANR-15-CE35-0001-01) awarded to O.R. S.B.P. received financial support through a doctoral fellowship from the IRD.

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Authors and Affiliations

  1. Institut de Recherche en Sciences de la Santé (IRSS), Bobo-Dioulasso, Burkina Faso

    Serge Bèwadéyir Poda, Abdoulaye Diabaté, Roch K. Dabiré & Olivier Roux

  2. Laboratoire d’Entomologie Fondamentale et Appliquée (LEFA), Unité de Formation et de Recherche – Sciences de la Vie et de la Terre (UFR-SVT), University Joseph KI-ZERBO, Ouagadougou, Burkina Faso

    Serge Bèwadéyir Poda & Olivier Gnankiné

  3. MIVEGEC, University of Montpellier, IRD, CNRS, Montpellier, France

    Serge Bèwadéyir Poda & Olivier Roux

  4. CEFE, University of Montpellier, CNRS, EPHE, IRD, University Paul Valery, Montpellier, France

    Bruno Buatois, Benoit Lapeyre & Laurent Dormont

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Contributions

O.R. conceived the study. O.R., S.B.P., B.B., B.L. and L.D. designed the chemical and electrophysiological experiments. O.R. and S.B.P. performed chemical extractions. S.B.P. and B.B. performed the chemical analysis. S.B.P. and B.L. performed the electrophysiological experiments. O.R. and S.B.P. designed olfactometric experiments and S.B.P. performed data collection. S.B.P. and O.R. performed statistical analyses. S.B.P., O.R., B.B. and B.L. drafted the manuscript and L.D., O.G., A.D. and R.K.D critically revised the manuscript. All authors revised the manuscript, gave final approval for publication and are accountable for the work performed therein.

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Correspondence to Olivier Roux.

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Poda, S.B., Buatois, B., Lapeyre, B. et al. No evidence for long-range male sex pheromones in two malaria mosquitoes. Nat Ecol Evol 6, 1676–1686 (2022). https://doi.org/10.1038/s41559-022-01869-x

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