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Associative Learning and Memory in Trichogramma telengai (Hymenoptera, Trichogrammatidae)

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Abstract

Miniaturization presents insects with the task of preserving vital body functions at a significantly reduced body size. We have studied the effects of miniaturization on the functioning of the insect nervous system by the example of the parasitoid wasp Trichogramma telengai. Despite a smaller number and a lower volume of neurons, T. telengai demonstrated the ability for associative learning and memory retention for up to 6 h after training. The training and testing were performed using a setup based on the Morris water maze design and suitable for comparative assessment of associative learning abilities in small animals of different taxa. Our data expand the understanding of the miniaturization effects on the cognitive abilities of animals and may help to determine which structural factors limit the minimum size of the functional insect brain.

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REFERENCES

  1. Bolstad, G.H., Cassara, J.A., Márquez, E., Hansen, T.F., van der Linde, K., Houle, D., and Pélabon, C., Complex constraints on allometry revealed by artificial selection on the wing of Drosophila melanogaster, Proc. Natl. Acad. Sci. U.S.A., 2015, vol. 112, no. 43, p. 13284.

  2. Chittka, L. and Niven, J., Are bigger brains better? Curr. Biol., 2009, vol. 19, no. 21, p. 995.

    Article  Google Scholar 

  3. Farahani, H.K., Ashouri, A., Goldansaz, S.H., Shapiro, M.S., Golshani, A., and Abrun, P., Associative learning and memory duration of Trichogramma brassicae, Progr. Biol. Sci., 2014, vol. 4, no. 1, p. 87.

  4. Farris, S.M. and Schulmeister, S., Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects, Proc. R. Soc. B Biol. Sci., 2011, vol. 278, no. 1707, p. 940.

    Article  Google Scholar 

  5. Fedorova, M.A., Farisenkov, C.E., Timokhov, A.V., and Polilov, A.A., Associative learning and memory in Thrips tabaci (Thysanoptera, Thripidae), Entomol. Rev., 2022, vol. 102, no. 6, p. 769.

  6. Fischer, S., Lu, Z., and Meinertzhagen, I.A., From two to three dimensions: the importance of the third dimension for evaluating the limits to neuronal miniaturization in insects, J. Comp. Neurol., 2018, vol. 526, p. 653.

    Article  CAS  PubMed  Google Scholar 

  7. Fischer, S., Lu, Z., and Meinertzhagen, I.A., Three-dimensional ultrastructural organization of the ommatidium of the minute parasitoid wasp Trichogramma evanescens, Arthropod Struct. Dev., 2019, vol. 48, p. 35.

  8. Hoedjes, K.M., Kruidhof, H.M., Huigens, M.E., Dicke, M., Vet, L.E.M., and Smid, H.M., Natural variation in learning rate and memory dynamics in parasitoid wasps: opportunities for converging ecology and neuroscience, Proc. R. Soc. B Biol. Sci., 2011, vol. 278, p. 889.

    Article  Google Scholar 

  9. Huigens, M.E., Pashalidou, F.G., Qian, M-H., Bukovinszky, T., Smid, H.M., van Loon, J.J.A., Dicke, M., and Fatouros, N.E., Hitch-hiking parasitic wasp learns to exploit butterfly anti­aphrodisiac, Proc. Natl. Acad. Sci. U.S.A., 2009, vol. 106, no. 3, p. 820.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Kaiser, L., Pérez-Maluf, R., Sandoz, J., and Pham-Delècue, M., Dynamics of odour learning in Leptopilina boulardi, a hymeno­pterous parasitoid, Anim. Behav., 2003, vol. 66, no. 6, p. 1077.

  11. Keasar, T., Ney-Nifle, M., and Mangel, M., Evidence for learning of visual host-associated cues in the parasitoid wasp Trichogramma thalense, Isr. J. Zool., 2000, vol. 46, no. 3, p. 243.

  12. Kruidhof, H.M., Pashalidou, F.G., Fatouros, N.E., Figueroa, I.A., Vet, L.E.M., Smid, H.M., and Huigens, M.E., Reward value determines memory consolidation in parasitic wasps, PLoS ONE, 2012, vol. 7, no. 8, p. 1.

    Article  Google Scholar 

  13. Lagasse, F., Moreno, C., Preat, T., and Mery, F., Functional and evolutionary trade-offs co-occur between two consolidated memory phases in Drosophila melanogaster, Proc. R. Soc. B Biol. Sci., 2012, vol. 279, no. 1744, p. 4015.

  14. Makarova, A.A. and Polilov, A.A., Peculiarities of the brain organization and fine structure in small insects related to miniaturization. 4. The smallest Hymenoptera (Mymaridae, Trichogrammatidae), Entomol. Rev., 2013, vol. 93, no. 6, p. 714.

    Article  Google Scholar 

  15. Makarova, A.A., Polilov, A., and Fischer, S., Comparative morphological analysis of compound eye miniaturization in minute Hymenoptera, Arthropod Struct. Dev., 2015, vol. 44, no. 1, p. 21.

    Article  PubMed  Google Scholar 

  16. Makarova, A.A., Veko, E.N., and Polilov, A.A., Metamorphosis of the central nervous system of Trichogramma telengai (Hymenoptera: Trichogrammatidae), Arthropod Struct. Dev., 2021, vol. 60, art. 101005.

  17. Müller, C., Collatz, J., Wieland, R., and Steidle, J.L.M., Associative learning and memory duration in the parasitic wasp Lariophagus distinguendus, Anim. Biol., 2006, vol. 56, no. 2, p. 221.

  18. Murovets, V.O. and Aleksandrov, A.A., Characteristics of memantine influences on learning in the Morris water maze, Pavlov J. Higher Nerv. Act., 2020, vol. 70, no. 1, p. 50. https://doi.org/10.31857/S0044467720010104

    Article  Google Scholar 

  19. Ofstad, T.A., Zuker, C.S., and Reiser, M.B., Visual place learning in Drosophila melanogaster, Nature, 2011, vol. 474, no. 7350, p. 204.

  20. Schurmann, D., Collatz, J., Hagenbucher, S., Ruther, J., and Steidle, J.L.M., Olfactory host finding, intermediate memory and its potential ecological adaptation in Nasonia vitripennis, Naturwissenschaften, 2009, vol. 96, no. 3, p. 383.

  21. Sorokina, A.P., Biological and morphological justification of species distinctness of Trichogramma telengai sp. n. (Hymeno­ptera: Trichogrammatidae), Entomol. Obozr., 1987, vol. 66, no. 1, p. 32.

  22. Telenga, N.A., Taxonomic and ecological characteristics of species of the genus Trichogramma (Hymenoptera: Trichogrammatidae), Nauch. Tr. Ukr. Inst. Zashch. Rast., 1959, vol. 8, p. 124.

  23. Tully, T., Preat, T., Boynton, S.C., and del Vecchio, M., Genetic dissection of consolidated memory in Drosophila, Cell, 1994, vol. 79, no. 1, p. 35.

  24. Van den Berg, M., Duivenvoorde, L., Wang, G., Tribuhl, S., Bukovinszky, T., Vet, L.E.M., Dicke, M., and Smid, H.M., Natural variation in learning and memory dynamics studied by artificial selection on learning rate in parasitic wasps, Anim. Behav., 2011, vol. 81, no. 1, p. 325.

    Article  Google Scholar 

  25. Van der Woude, E., Huigens, M.E., and Smid, H.M., Differential effects of brain size on memory performance in parasitic wasps, Anim. Behav., 2018, vol. 141, p. 57.

    Article  Google Scholar 

  26. Wessnitzer, J., Mangan, M., and Webb, B., Place memory in crickets, Proc. R. Soc. B Biol. Sci., 2008, vol. 275, no. 1637, p. 915.

    Article  Google Scholar 

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ACKNOWLEDGMENTS

We are grateful to S.Ya. Reznik (Zoological Institute of the Russian Academy of Sciences, St. Petersburg, Russia) for providing live insects for experiments.

Funding

This work was supported by the Russian Science Foundation (project 22-74-10008).

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Authors and Affiliations

  1. Department of Entomology, Faculty of Biology, Lomonosov Moscow State University, 119234, Moscow, Russia

    M. A. Fedorova, S. E. Farisenkov, A. V. Timokhov & A. A. Polilov

Authors
  1. M. A. Fedorova
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  2. S. E. Farisenkov
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  3. A. V. Timokhov
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  4. A. A. Polilov
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Correspondence to M. A. Fedorova.

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Conflict of interest. The authors declare that they have no conflict of interest.

Statement on the welfare of animals. All the applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All the procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

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Fedorova, M.A., Farisenkov, S.E., Timokhov, A.V. et al. Associative Learning and Memory in Trichogramma telengai (Hymenoptera, Trichogrammatidae). Entmol. Rev. 103, 7–14 (2023). https://doi.org/10.1134/S0013873823010025

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  • DOI: https://doi.org/10.1134/S0013873823010025

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