Effect of octopamine on the frequency tuning of the auditory system in Culex pipiens pipiens mosquito (Diptera, Culicidae)

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Abstract

We aimed at demonstrating the direct physiological effects of octopamine on the auditory responses of the Johnston’s organ sensory neurons in Culex pipiens pipiens mosquitoes. Responses to acoustic stimulation were measured as the frequency-threshold curves and as an instantly recorded autoexcitation frequency before and after the injection of octopamine (or chlordimeform, an agonist of octopamine receptors). The autoexcitation frequency was assessed by including the auditory neurons into a positive feedback loop, when the amplified neuronal response was used to drive the stimulating loudspeaker. Our results indicate that: octopamine affects the properties of the auditory system both in male and female mosquitoes; in female mosquitoes, octopamine significantly reduces the sensitivity of auditory neurons below 90 Hz and produces little effect in the high-frequency range (100 Hz and above); in male mosquitoes, octopamine significantly raises the tuning frequency of the auditory system (ratio of tuning frequencies before and after the injection 1.32–1.55). There is a strong sexual dimorphism in the octopaminergic modulation of the mosquito auditory system. The observed physiological effects of octopamine, both in male and female mosquitoes, cannot be fully explained by the modulation of mechanical stiffness of the antenna and must include the changes in frequency tuning of the auditory neurons.

About the authors

D. D. Vorontsov

Koltzov Institute of Developmental Biology Russian Academy of Sciences

Author for correspondence.
Email: d.vorontsov@idbras.ru
Russia, 119334, Moscow, Vavilova, 26

D. N. Lapshin

Institute for Information Transmission Problems of the Russian Academy of Sciences (Kharkevich Institute)

Author for correspondence.
Email: lapshin@iitp.ru
Russia, 127994, Moscow, Bolshoy Karetny per., 19

References

  1. Apasov S.R., Zhantiev R.D., Tamarina N.A., Federova M.V. Akusticheskaja orientacija samcov Aedes diantaeus pri sparivanii [Acoustic orientation of Aedes diantaeus males during pairing]. Parazitologiya [Parasitology]. 1986. V. 20. № 5. P. 351–355.
  2. Lapshin D.N. Sluhovaja sistema samok krovososushhih komarov (Diptera, Culicidae): akusticheskoe vosprijatie v uslovijah imitacii poljota. [Auditory system of blood-sucking mosquito females (Diptera, Culicidae): acoustic perception during the flight simulation]. Jentomologicheskoe obozrenie [Entomological review]. 2012. V. 91. № 3. P. 465–484.
  3. Lapshin D.N. Prostranstvennaja i chastotnaja izbiratel’nost' sluhovyh receptorov komarov-zvoncov (Diptera, Chironomidae) [Directional and frequency characteristics of auditory receptors in midges (Diptera, Chironomidae)]. Jentomologicheskoe obozrenie [Entomological review]. 2015. V. 94. № 4. P. 761–776.
  4. Sitnik V.V. Vlijanie massiva rastitel’nosti na rasprostranenie akusticheskih vozmushhenij [A forestry influence on an acoustic perturbance propagation]. Matematicheskoye modelirovaniye [Math modeling]. 2007. V. 19. № 8. P. 90–96 (in Russian).
  5. Aldersley A., Cator L.J. Female resistance and harmonic convergence influence male mating success in Aedes aegypti. Scientific Reports. 2019. V. 9 (2145). https://doi.org/10.1038/s41598-019-38599-3
  6. Andrés M., Seifert M., Spalthoff C., Warren B., Weiss L., Giraldo D., Winkler M., Pauls S., Go M., Göpfert M.C. Auditory efferent system modulates mosquito hearing. Current Biology. 2016. V. 26. P. 1–9. https://doi.org/10.1016/j.cub.2016.05.077
  7. Andrés M., Su M.P., Albert J., Cator L.J. Buzzkill: targeting the mosquito auditory system. Current Opinion in Insect Science. 2020. V. 40. P. 11–7. https://doi.org/10.1016/j.cois.2020.04.003
  8. Bartlett-Healy K., Crans W., Gaugler R. Phonotaxis to amphibian vocalizations in Culex territans (Diptera: Culicidae). Annals of the Entomological Society of America. 2008. V. 101 P. 95–103. https://doi.org/10.1603/0013-8746(2008)101[95:PTAVIC]2.0.CO;2
  9. Boo K.S., Richards A.G. Fine structure of the scolopidia in the johnston’s organ of male Aedes aegypti (L.) (Diptera: Culicidae). Int. J. Insect Morphol. Embryol. 1975. V. 4. P. 549–566. https://doi.org/10.1016/0020-7322(75)90031-8
  10. Boo K.S., Richards A.G. Fine structure of scolopidia in Johnston’s organ of female Aedes aegypti compared with that of the male. J. Insect Physiology. 1975 V. 21. P. 1129–1139. https://doi.org/10.1016/0022-1910(75)90126-2
  11. Feugère L., Simões P.M.V., Russell I.J., Gibson G. The role of hearing in mosquito behaviour. Chapter 26. In: Ignell R., Lazzari C.R., Lorenzo M.G., Hill S.R. (eds.) Sensory ecology of disease vectors. Wageningen Academic Publishers, Wageningen, the Netherlands. 2022. P. 683–708. https://doi.org/10.3920/978-90-8686-932-9_26
  12. Finetti L., Paluzzi J.P., Orchard I., Lange A.B. Octopamine and tyramine signalling in Aedes aegypti: Molecular characterization and insight into potential physiological roles. PloS one. 2023. V. 18. № 2. e0281917. https://doi.org/10.1371/journal.pone.0281917
  13. Fyodorova M.V., Azovsky A.I. Interactions between swarming Chironomus annularius (Diptera: Chironomidae) males: Role of acoustic behavior. J. Insect Behav. 2003. V. 16. № 2. P. 295–306. https://doi.org/10.1023/A:1023976120723
  14. Georgiades M., Alampounti C.A., Somers J., Su M., Ellis D., Bagi J., Ntabaliba W., Moore S., Albert J.T., Andrés M. A novel beta-adrenergic like octopamine receptor modulates the audition of malaria mosquitoes and serves as insecticide. URL: https://www.biorxiv.org/content/10.1101/ 2022.08.02.502538v1 (accessed 08.02.2022) (preprint). https://doi.org/10.1101/2022.08.02.502538
  15. Gibson G., Russell I.J. Flying in tune: sexual recognition in mosquitoes. Current Biology. 2006. V. 16. № 13. P. 1311–1316. https://doi.org/10.1016/j.cub.2006.05.053
  16. Gibson G., Warren B., Russell I. Humming in tune: sex and species recognition by mosquitoes on the wing. J. Association for Research in Otolaryngology. 2010. V. 11. P. 527–540. https://doi.org/10.1007/s10162-010-0243-2
  17. Göpfert M.C., Briegel H., Robert D. Mosquito hearing: sound-induced antennal vibrations in male and female Aedes aegypti. J. Experimental Biology. 1999. V. 202. P. 2727–2738. https://doi.org/10.1242/jeb.202.20.2727
  18. Göpfert M.C., Humphris A.D., Albert J.T., Robert D., Hendrich O. Power gain exhibited by motile mechanosensory neurons in Drosophila ears. Proc. Natl. Acad. Sci. USA. 2005. V. 102. № 2. P. 325–330. https://doi.org/10.1073/pnas.0405741102
  19. Hammer O., Harper D.A., Ryan P.D. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia electronica. 2001. V. 4. № 1. P. 9.
  20. Hart M., Belton P., Kuhn R. The Risler manuscript. European mosquito. European Mosquito Bulletin. 2011. V. 29. P. 103–113.
  21. Lapshin D.N. Auditory system of blood-sucking mosquito females (Diptera, Culicidae): acoustic perception during the flight simulation. Entomological Review. 2013. V. 93. № 2. P. 135–149. https://doi.org/10.1134/S0013873813020012
  22. Lapshin D.N. Directional and frequency characteristics of auditory receptors in midges (Diptera, Chironomidae). Entomological Review. 2015. 95, 1155–1165. https://doi.org/10.1134/S001387381509002X
  23. Lapshin D.N., Vorontsov D.D. Frequency tuning of individual auditory receptors in female mosquitoes (Diptera, Culicidae). J. Insect Physiology. 2013. V. 59. P. 828–839. https://doi.org/10.1016/j.jinsphys.2013.05.010
  24. Lapshin D.N., Vorontsov D.D. Frequency organization of the Johnston’s organ in male mosquitoes (Diptera, Culicidae). J. Experimental Biology. 2017. V. 220. P. 3927–3938. https://doi.org/10.1242/jeb.152017
  25. Lapshin D.N., Vorontsov D.D. Mapping the auditory space of Culex pipiens female mosquito in 3D. URL: https://www.biorxiv.org/content/10.1101/2023.01.09. 523250v1 (accessed 09.01.2023) (preprint). https://doi.org/10.1101/2023.01.09.523250
  26. Legett H.D., Aihara I., Bernal X.E. Within host acoustic signal preference of frog-biting mosquitoes (Diptera: Culicidae) and midges (Diptera: Corethrellidae) on Iriomote Island, Japan. Entomological Science. 2021. V. 24. № 2. P. 116–122. https://doi.org/10.1111/ens.12455
  27. Loh Y.M., Su M.P., Ellis D.A. and Andrés M. The auditory efferent system in Mosquitoes. Frontiers in Cell and Developmental Biology. 2023. V. 11–1123738.11. P. 1–15. https://doi.org/10.3389/fcell.2023.1123738
  28. Mukundarajan H., Hol F.J.H., Castillo E.A., Newby C., Prakash M. Using mobile phones as acoustic sensors for high-throughput mosquito surveillance. Ecology Epidemiology and Global Health. 2017. V. 6–e27854. https://doi.org/10.7554/eLife.27854
  29. Ogawa K., Sato H. Relationship between male acoustic response and female wingbeat frequency in a chironomid midge, Chironomus yoshimatsui (Diptera: Chironomidae). Jpn. J. Sanit. Zool. 1993. V. 44. № 4. P. 355–360. https://doi.org/10.7601/mez.44.355
  30. Pantoja-Sánchez H., Vargas J.F., Ruiz-López F., Rúa-Uribe G., Vélez V., Kline D.V., Bernal X.E. A new approach to improve acoustic trapping effectiveness for Aedes aegypti (Diptera: Culicidae). Journal of Vector Ecology. 2019. V. 44. № 2. P. 216–222. https://doi.org/10.1111/jvec.12352
  31. Simões P.M., Gibson G., Russell I.J. Pre-copula acoustic behaviour of males in the malarial mosquitoes Anopheles coluzzii and Anopheles gambiae s.s. does not contribute to reproductive isolation. J. Experimental Biology. 2017. V. 220. № 3. P. 379–385. https://doi.org/10.1242/jeb.149757.
  32. Su M.P., Andrés M., Boyd-Gibbins N., Somers J., Albert J.T. Sex and species specific hearing mechanisms in mosquito flagellar ears. Nature Communications. 2018. V. 9. № 1. P. 3911.
  33. Toma T., Takara T., Miyagi I., Futami K., Higa Y. Mosquitoes and frog-biting midges (Diptera: Culicidae and Corethrellidae) attracted to traps with natural frog calls and synthesized sounds at Iriomote Island, Ryukyu Archipelago, Japan. Medical Entomology and Zoology. 2019. V.70. № 4. P. 221–234. https://doi.org/0.7601/mez.70.221
  34. Warren B., Gibson G., Russell I.J. Sex recognition through midflight mating duets in Culex mosquitoes is mediated by acoustic distortion. Current Biology. 2009. V. 9. P. 485–491. https://doi.org/10.1016/j.cub.2009.01.059
  35. Warren B., Lukashkin A.N., Russell I.J. The dynein–tubulin motor powers active oscillations and amplification in the hearing organ of the mosquito. Proceedings of the Royal Society B. 2010. V. 277. P. 1761–1769. https://doi.org/10.1098/rspb.2009.2355

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