Evidence for a gut microbial community conferring adaptability to diet quality and temperature stressors in phytophagous insects: the melon fruit fly Zeugodacus cucurbitae (Diptera: Tephritidae) as a case study

Abstract Background The high invasiveness of phytophagous insects is related to their adaptability to various environments, that can be influenced by their associated microbial community. Microbial symbionts are known to play a key role in the biology, ecology, and evolution of phytophagous insects,...

Full description

Saved in:
Bibliographic Details
Main Authors: Abir Hafsi, Laura Moquet, Wouter Hendrycks, Marc De Meyer, Massimiliano Virgilio, Hélène Delatte
Format: Article
Language:English
Published: BMC 2024-12-01
Series:BMC Microbiology
Subjects:
Online Access:https://doi.org/10.1186/s12866-024-03673-y
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850136754935300096
author Abir Hafsi
Laura Moquet
Wouter Hendrycks
Marc De Meyer
Massimiliano Virgilio
Hélène Delatte
author_facet Abir Hafsi
Laura Moquet
Wouter Hendrycks
Marc De Meyer
Massimiliano Virgilio
Hélène Delatte
author_sort Abir Hafsi
collection DOAJ
description Abstract Background The high invasiveness of phytophagous insects is related to their adaptability to various environments, that can be influenced by their associated microbial community. Microbial symbionts are known to play a key role in the biology, ecology, and evolution of phytophagous insects, but their abundance and diversity are suggested to be influenced by environmental stressors. In this work, using 16 S rRNA metabarcoding we aim to verify (1) if laboratory rearing affects microbial symbiont communities of Zeugodacus cucurbitae females, a cosmopolitan pest of cucurbitaceous crops (2) if temperature, diet quality, and antibiotic treatments affect microbial symbiont communities of both laboratory and wild populations, and (3) if changes in microbial symbiont communities due to temperature, diet and antibiotic affect longevity and fecundity of Z. cucurbitae. Results The results showed that microbial diversity, particularly the β-diversity was significantly affected by insect origin, temperature, diet quality, and antibiotic treatment. The alteration of gut microbial symbionts, specifically Enterobacteriaceae, was associated with low fecundity and longevity of Z. cucurbitae females feeding on optimal diet only. Fecundity reduction in antibiotic treated females was more pronounced when flies were fed on a poor diet without protein. Conclusions our study proves the relationship between gut microbiome and host fitness under thermal and diet fluctuation highlighting the importance of microbial community in the adaptation of Z. cucurbitae to environmental stress. Clinical trial number Not applicable.
format Article
id doaj-art-9929edfbe35b412b85724c122e4cce8d
institution OA Journals
issn 1471-2180
language English
publishDate 2024-12-01
publisher BMC
record_format Article
series BMC Microbiology
spelling doaj-art-9929edfbe35b412b85724c122e4cce8d2025-08-20T02:31:02ZengBMCBMC Microbiology1471-21802024-12-0124111510.1186/s12866-024-03673-yEvidence for a gut microbial community conferring adaptability to diet quality and temperature stressors in phytophagous insects: the melon fruit fly Zeugodacus cucurbitae (Diptera: Tephritidae) as a case studyAbir Hafsi0Laura Moquet1Wouter Hendrycks2Marc De Meyer3Massimiliano Virgilio4Hélène Delatte5CIRAD, UMR PVBMTCIRAD, UMR PVBMTRoyal Museum for Central AfricaRoyal Museum for Central AfricaRoyal Museum for Central AfricaCIRAD, UMR PVBMTAbstract Background The high invasiveness of phytophagous insects is related to their adaptability to various environments, that can be influenced by their associated microbial community. Microbial symbionts are known to play a key role in the biology, ecology, and evolution of phytophagous insects, but their abundance and diversity are suggested to be influenced by environmental stressors. In this work, using 16 S rRNA metabarcoding we aim to verify (1) if laboratory rearing affects microbial symbiont communities of Zeugodacus cucurbitae females, a cosmopolitan pest of cucurbitaceous crops (2) if temperature, diet quality, and antibiotic treatments affect microbial symbiont communities of both laboratory and wild populations, and (3) if changes in microbial symbiont communities due to temperature, diet and antibiotic affect longevity and fecundity of Z. cucurbitae. Results The results showed that microbial diversity, particularly the β-diversity was significantly affected by insect origin, temperature, diet quality, and antibiotic treatment. The alteration of gut microbial symbionts, specifically Enterobacteriaceae, was associated with low fecundity and longevity of Z. cucurbitae females feeding on optimal diet only. Fecundity reduction in antibiotic treated females was more pronounced when flies were fed on a poor diet without protein. Conclusions our study proves the relationship between gut microbiome and host fitness under thermal and diet fluctuation highlighting the importance of microbial community in the adaptation of Z. cucurbitae to environmental stress. Clinical trial number Not applicable.https://doi.org/10.1186/s12866-024-03673-yInsect adaptationLongevityFecundityMicrobial symbiontMetabarcoding
spellingShingle Abir Hafsi
Laura Moquet
Wouter Hendrycks
Marc De Meyer
Massimiliano Virgilio
Hélène Delatte
Evidence for a gut microbial community conferring adaptability to diet quality and temperature stressors in phytophagous insects: the melon fruit fly Zeugodacus cucurbitae (Diptera: Tephritidae) as a case study
BMC Microbiology
Insect adaptation
Longevity
Fecundity
Microbial symbiont
Metabarcoding
title Evidence for a gut microbial community conferring adaptability to diet quality and temperature stressors in phytophagous insects: the melon fruit fly Zeugodacus cucurbitae (Diptera: Tephritidae) as a case study
title_full Evidence for a gut microbial community conferring adaptability to diet quality and temperature stressors in phytophagous insects: the melon fruit fly Zeugodacus cucurbitae (Diptera: Tephritidae) as a case study
title_fullStr Evidence for a gut microbial community conferring adaptability to diet quality and temperature stressors in phytophagous insects: the melon fruit fly Zeugodacus cucurbitae (Diptera: Tephritidae) as a case study
title_full_unstemmed Evidence for a gut microbial community conferring adaptability to diet quality and temperature stressors in phytophagous insects: the melon fruit fly Zeugodacus cucurbitae (Diptera: Tephritidae) as a case study
title_short Evidence for a gut microbial community conferring adaptability to diet quality and temperature stressors in phytophagous insects: the melon fruit fly Zeugodacus cucurbitae (Diptera: Tephritidae) as a case study
title_sort evidence for a gut microbial community conferring adaptability to diet quality and temperature stressors in phytophagous insects the melon fruit fly zeugodacus cucurbitae diptera tephritidae as a case study
topic Insect adaptation
Longevity
Fecundity
Microbial symbiont
Metabarcoding
url https://doi.org/10.1186/s12866-024-03673-y
work_keys_str_mv AT abirhafsi evidenceforagutmicrobialcommunityconferringadaptabilitytodietqualityandtemperaturestressorsinphytophagousinsectsthemelonfruitflyzeugodacuscucurbitaedipteratephritidaeasacasestudy
AT lauramoquet evidenceforagutmicrobialcommunityconferringadaptabilitytodietqualityandtemperaturestressorsinphytophagousinsectsthemelonfruitflyzeugodacuscucurbitaedipteratephritidaeasacasestudy
AT wouterhendrycks evidenceforagutmicrobialcommunityconferringadaptabilitytodietqualityandtemperaturestressorsinphytophagousinsectsthemelonfruitflyzeugodacuscucurbitaedipteratephritidaeasacasestudy
AT marcdemeyer evidenceforagutmicrobialcommunityconferringadaptabilitytodietqualityandtemperaturestressorsinphytophagousinsectsthemelonfruitflyzeugodacuscucurbitaedipteratephritidaeasacasestudy
AT massimilianovirgilio evidenceforagutmicrobialcommunityconferringadaptabilitytodietqualityandtemperaturestressorsinphytophagousinsectsthemelonfruitflyzeugodacuscucurbitaedipteratephritidaeasacasestudy
AT helenedelatte evidenceforagutmicrobialcommunityconferringadaptabilitytodietqualityandtemperaturestressorsinphytophagousinsectsthemelonfruitflyzeugodacuscucurbitaedipteratephritidaeasacasestudy