Differential Coding of Fruit, Leaf, and Microbial Odours in the Brains of Drosophila suzukii and Drosophila melanogaster
1
Centre for Mind/Brain Sciences (CIMeC), University of Trento, 38068 Rovereto, Italy
2
Faculty of Agricultural, Environmental and Food Sciences, Free University of Bozen-Bolzano, 39100 Bolzano, Italy
3
Department of Physics, University of Trento, 38123 Trento, Italy
*
Author to whom correspondence should be addressed.
Insects 2025, 16(1), 84; https://doi.org/10.3390/insects16010084
Submission received: 21 November 2024
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Revised: 20 December 2024
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Accepted: 13 January 2025
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Published: 15 January 2025
(This article belongs to the Section Insect Behavior and Pathology)
Simple Summary
Drosophila suzukii is a major pest that damages berries and stone fruits by laying its eggs in ripening fruit still on the plant, in contrast to its sister species Drosophila melanogaster, which lays its eggs on overripe, fermenting fruit on the ground. Both species rely on their sense of smell to find such fruit, but how their brains process these odours and subsequently decide on different hosts is not yet fully understood. In this study, we hypothesised that the differences in behaviour may begin in the antennal lobes, the first brain regions of the olfactory system. Using advanced brain imaging techniques, we investigated how the two species respond to odours of ripe fruit, fermented fruit, leaves, and bacteria. We found structural differences in the antennal lobes and differences in the way the odours are represented in these areas of the brain, while behavioural experiments looking for direct differences in the attractiveness of the tested odours revealed no significant variation between the species. The differences in odour processing could form the basis for alternative species-specific pest control strategies that could reduce dependence on insecticides.
Abstract
Drosophila suzukii severely damages the production of berry and stone fruits in large parts of the world. Unlike D. melanogaster, which reproduces on overripe and fermenting fruits on the ground, D. suzukii prefers to lay its eggs in ripening fruits still on the plants. Flies locate fruit hosts by their odorant volatiles, which are detected and encoded by a highly specialised olfactory system before being translated into behaviour. The exact information-processing pathway is not yet fully understood, especially the evaluation of odour attractiveness. It is also unclear what differentiates the brains of D. suzukii and D. melanogaster to cause the crucial difference in host selection. We hypothesised that the basis for different behaviours is already formed at the level of the antennal lobe of D. suzukii and D. melanogaster by different neuronal responses to volatiles associated with ripe and fermenting fruit. We thus investigated by 3D in vivo two-photon calcium imaging how both species encoded odours from ripe fruits, leaves, fermented fruits, bacteria, and their mixtures in the antennal lobe. We then assessed their behavioural responses to mixtures of ripe and fermenting odours. The neural responses reflect species-dependent shifts in the odour code. In addition to this, morphological differences were also observed. However, this was not directly reflected in different behavioural responses to the odours tested.
