Drosophila suzukii and Drosophila melanogaster prefer distinct microbial and plant aroma compounds in a complex fermented matrix

Maria C Dzialo; Somasundar Arumugam; Supinya Piampongsant; Lloyd Cool; Christophe Vanderaa; Beatriz Herrera-Malaver; Tomas Opsomer; Wim Dehaen; Tom Wenseleers; Miguel Roncoroni; Amani Alawamleh; Felix Wäckers; Bart Lievens; Bill S Hansson; Karin Voordeckers; Silke Sachse; Kevin J Verstrepen

doi:10.1016/j.isci.2024.111141

Drosophila suzukii and Drosophila melanogaster prefer distinct microbial and plant aroma compounds in a complex fermented matrix

iScience. 2024 Oct 10;27(11):111141. doi: 10.1016/j.isci.2024.111141. eCollection 2024 Nov 15.

Authors

Maria C Dzialo^{1

2}, Somasundar Arumugam^{3

4}, Supinya Piampongsant^{1

2}, Lloyd Cool^{1

2

5}, Christophe Vanderaa⁵, Beatriz Herrera-Malaver^{1

2}, Tomas Opsomer⁶, Wim Dehaen⁶, Tom Wenseleers⁵, Miguel Roncoroni^{1

2}, Amani Alawamleh^{7

8}, Felix Wäckers^{7

9}, Bart Lievens¹⁰, Bill S Hansson^{4

11}, Karin Voordeckers^{1

2}, Silke Sachse^{3

4}, Kevin J Verstrepen^{1

2}

Affiliations

¹ VIB - KU Leuven Center for Microbiology, Gaston Geenslaan 1, 3001 Leuven, Belgium.
² CMPG Laboratory of Genetics and Genomics, Department M2S, KU Leuven, Gaston Geenslaan 1, 3001 Leuven, Belgium.
³ Research Group Olfactory Coding, Max Planck Institute for Chemical Ecology, Hans-Knoell-Str, 8, 07745 Jena, Germany.
⁴ Max Planck Center Next Generation Insect Chemical Ecology (nGICE), Hans-Knoell-Str, 8, 07745 Jena, Germany.
⁵ Laboratory of Socioecology and Social Evolution, Department of Biology, KU Leuven, Naamsestraat 59, 3000 Leuven, Belgium.
⁶ Sustainable Chemistry for Metals and Molecules, Department of Chemistry, KU Leuven, Celestijnenlaan 200F, 3001 Leuven, Belgium.
⁷ Biobest NV, Ilse Velden 18, 2260 Westerlo, Belgium.
⁸ University of Molise, Department of Agricultural, Environmental and Food Sciences, Via De Sanctis 1, 86100 Campobasso, Italy.
⁹ Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK.
¹⁰ CMPG Laboratory for Process Microbial Ecology and Bioinspirational Management (PME&BIM), Department M2S, KU Leuven, Willem De Croylaan 46, 3001 Leuven, Belgium.
¹¹ Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Hans-Knoell-Str, 8, 07745 Jena, Germany.

Abstract

Volatile aroma compounds are important chemical cues for insects. Behavioral responses to specific odors differ strongly between insect species, and the exact causative molecules are often unknown. Beer is frequently used in insect traps because it combines hundreds of plant and microbial aromas that attract many insects. Here, we analyzed responses of the pest fruit fly Drosophila suzukii and benign Drosophila melanogaster to beers with different chemical compositions. Using extensive chemical and behavioral assays, we identified ecologically relevant chemicals that influence drosophilid behavior and that induce different odor-evoked activity patterns in the antennal lobe of the two species obtained by functional imaging. Specific mixes of compounds increased the species-specificity and sex-specificity of lures in both laboratory and greenhouse settings. Together, our study shows how examining insect responses to highly complex natural mixtures of aroma compounds provides insight into insect-specific behavioral responses and also opens avenues for improved pest control.

Keywords: Ethology; Microbiology; Sensory neuroscience.