Microbiota-mediated competition between Drosophila species

Abstract Background The influence of microbiota in ecological interactions, and in particular competition, is poorly known. We studied competition between two insect species, the invasive pest Drosophila suzukii and the model Drosophila melanogaster, whose larval ecological niches overlap in ripe, b...

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Main Authors: Antoine Rombaut, Romain Gallet, Kenza Qitout, Mukherjy Samy, Robin Guilhot, Pauline Ghirardini, Brian P. Lazzaro, Paul G. Becher, Anne Xuéreb, Patricia Gibert, Simon Fellous
Format: Article
Language:English
Published: BMC 2023-09-01
Series:Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s40168-023-01617-8
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author Antoine Rombaut
Romain Gallet
Kenza Qitout
Mukherjy Samy
Robin Guilhot
Pauline Ghirardini
Brian P. Lazzaro
Paul G. Becher
Anne Xuéreb
Patricia Gibert
Simon Fellous
author_facet Antoine Rombaut
Romain Gallet
Kenza Qitout
Mukherjy Samy
Robin Guilhot
Pauline Ghirardini
Brian P. Lazzaro
Paul G. Becher
Anne Xuéreb
Patricia Gibert
Simon Fellous
author_sort Antoine Rombaut
collection DOAJ
description Abstract Background The influence of microbiota in ecological interactions, and in particular competition, is poorly known. We studied competition between two insect species, the invasive pest Drosophila suzukii and the model Drosophila melanogaster, whose larval ecological niches overlap in ripe, but not rotten, fruit. Results We discovered D. suzukii females prevent costly interspecific larval competition by avoiding oviposition on substrates previously visited by D. melanogaster. More precisely, D. melanogaster association with gut bacteria of the genus Lactobacillus triggered D. suzukii avoidance. However, D. suzukii avoidance behavior is condition-dependent, and D. suzukii females that themselves carry D. melanogaster bacteria stop avoiding sites visited by D. melanogaster. The adaptive significance of avoiding cues from the competitor’s microbiota was revealed by experimentally reproducing in-fruit larval competition: reduced survival of D. suzukii larvae only occurred if the competitor had its normal microbiota. Conclusions This study establishes microbiotas as potent mediators of interspecific competition and reveals a central role for context-dependent behaviors under bacterial influence. Video Abstract
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spelling doaj.art-8ade6928bea747e29154b5e03fe89abb2023-11-20T10:19:45ZengBMCMicrobiome2049-26182023-09-0111111210.1186/s40168-023-01617-8Microbiota-mediated competition between Drosophila speciesAntoine Rombaut0Romain Gallet1Kenza Qitout2Mukherjy Samy3Robin Guilhot4Pauline Ghirardini5Brian P. Lazzaro6Paul G. Becher7Anne Xuéreb8Patricia Gibert9Simon Fellous10CBGP, INRAE, CIRAD, IRD, Montpellier SupAgro, Univ MontpellierCBGP, INRAE, CIRAD, IRD, Montpellier SupAgro, Univ MontpellierCBGP, INRAE, CIRAD, IRD, Montpellier SupAgro, Univ MontpellierCBGP, INRAE, CIRAD, IRD, Montpellier SupAgro, Univ MontpellierCBGP, INRAE, CIRAD, IRD, Montpellier SupAgro, Univ MontpellierCBGP, INRAE, CIRAD, IRD, Montpellier SupAgro, Univ MontpellierDepartment of Entomology, Cornell Institute of Host-Microbe Interactions and Disease, Cornell UniversityDept Plant Protection Biology - Chemical Ecology Horticulture, Swedish University of Agricultural SciencesCBGP, INRAE, CIRAD, IRD, Montpellier SupAgro, Univ MontpellierLaboratoire de Biométrie Et Biologie Evolutive, UMR 5558, CNRS, Université Lyon 1, Université de LyonCBGP, INRAE, CIRAD, IRD, Montpellier SupAgro, Univ MontpellierAbstract Background The influence of microbiota in ecological interactions, and in particular competition, is poorly known. We studied competition between two insect species, the invasive pest Drosophila suzukii and the model Drosophila melanogaster, whose larval ecological niches overlap in ripe, but not rotten, fruit. Results We discovered D. suzukii females prevent costly interspecific larval competition by avoiding oviposition on substrates previously visited by D. melanogaster. More precisely, D. melanogaster association with gut bacteria of the genus Lactobacillus triggered D. suzukii avoidance. However, D. suzukii avoidance behavior is condition-dependent, and D. suzukii females that themselves carry D. melanogaster bacteria stop avoiding sites visited by D. melanogaster. The adaptive significance of avoiding cues from the competitor’s microbiota was revealed by experimentally reproducing in-fruit larval competition: reduced survival of D. suzukii larvae only occurred if the competitor had its normal microbiota. Conclusions This study establishes microbiotas as potent mediators of interspecific competition and reveals a central role for context-dependent behaviors under bacterial influence. Video Abstracthttps://doi.org/10.1186/s40168-023-01617-8MicrobiotaSymbiosisCompetitionAgroecology
spellingShingle Antoine Rombaut
Romain Gallet
Kenza Qitout
Mukherjy Samy
Robin Guilhot
Pauline Ghirardini
Brian P. Lazzaro
Paul G. Becher
Anne Xuéreb
Patricia Gibert
Simon Fellous
Microbiota-mediated competition between Drosophila species
Microbiome
Microbiota
Symbiosis
Competition
Agroecology
title Microbiota-mediated competition between Drosophila species
title_full Microbiota-mediated competition between Drosophila species
title_fullStr Microbiota-mediated competition between Drosophila species
title_full_unstemmed Microbiota-mediated competition between Drosophila species
title_short Microbiota-mediated competition between Drosophila species
title_sort microbiota mediated competition between drosophila species
topic Microbiota
Symbiosis
Competition
Agroecology
url https://doi.org/10.1186/s40168-023-01617-8
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