Metabolic consequences of various fruit-based diets in a generalist insect species

Most phytophagous insect species exhibit a limited diet breadth and specialize on a few or a single host plant. In contrast, some species display a remarkably large diet breadth, with host plants spanning several families and many species. It is unclear, however, whether this phylogenetic generalism...

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Main Authors: Laure Olazcuaga, Raymonde Baltenweck, Nicolas Leménager, Alessandra Maia-Grondard, Patricia Claudel, Philippe Hugueney, Julien Foucaud
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-06-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/84370
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author Laure Olazcuaga
Raymonde Baltenweck
Nicolas Leménager
Alessandra Maia-Grondard
Patricia Claudel
Philippe Hugueney
Julien Foucaud
author_facet Laure Olazcuaga
Raymonde Baltenweck
Nicolas Leménager
Alessandra Maia-Grondard
Patricia Claudel
Philippe Hugueney
Julien Foucaud
author_sort Laure Olazcuaga
collection DOAJ
description Most phytophagous insect species exhibit a limited diet breadth and specialize on a few or a single host plant. In contrast, some species display a remarkably large diet breadth, with host plants spanning several families and many species. It is unclear, however, whether this phylogenetic generalism is supported by a generic metabolic use of common host chemical compounds (‘metabolic generalism’) or alternatively by distinct uses of diet-specific compounds (‘multi-host metabolic specialism’)? Here, we simultaneously investigated the metabolomes of fruit diets and of individuals of a generalist phytophagous species, Drosophila suzukii, that developed on them. The direct comparison of metabolomes of diets and consumers enabled us to disentangle the metabolic fate of common and rarer dietary compounds. We showed that the consumption of biochemically dissimilar diets resulted in a canalized, generic response from generalist individuals, consistent with the metabolic generalism hypothesis. We also showed that many diet-specific metabolites, such as those related to the particular color, odor, or taste of diets, were not metabolized, and rather accumulated in consumer individuals, even when probably detrimental to fitness. As a result, while individuals were mostly similar across diets, the detection of their particular diet was straightforward. Our study thus supports the view that dietary generalism may emerge from a passive, opportunistic use of various resources, contrary to more widespread views of an active role of adaptation in this process. Such a passive stance towards dietary chemicals, probably costly in the short term, might favor the later evolution of new diet specializations.
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spelling doaj.art-eb2adafd68364a27ad581e8bc9fcf99b2023-06-06T06:31:01ZengeLife Sciences Publications LtdeLife2050-084X2023-06-011210.7554/eLife.84370Metabolic consequences of various fruit-based diets in a generalist insect speciesLaure Olazcuaga0https://orcid.org/0000-0001-9100-1305Raymonde Baltenweck1https://orcid.org/0000-0002-8228-1517Nicolas Leménager2Alessandra Maia-Grondard3Patricia Claudel4Philippe Hugueney5Julien Foucaud6https://orcid.org/0000-0003-2272-3149UMR CBGP (INRAE-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, Montferrier, France; Department of Agricultural Biology, Colorado State University, Fort Collins, United StatesUniversité de Strasbourg, INRAE, Colmar, FranceUMR CBGP (INRAE-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, Montferrier, FranceUniversité de Strasbourg, INRAE, Colmar, FranceUniversité de Strasbourg, INRAE, Colmar, FranceUniversité de Strasbourg, INRAE, Colmar, FranceUMR CBGP (INRAE-IRD-CIRAD, Montpellier SupAgro), Campus International de Baillarguet, Montferrier, FranceMost phytophagous insect species exhibit a limited diet breadth and specialize on a few or a single host plant. In contrast, some species display a remarkably large diet breadth, with host plants spanning several families and many species. It is unclear, however, whether this phylogenetic generalism is supported by a generic metabolic use of common host chemical compounds (‘metabolic generalism’) or alternatively by distinct uses of diet-specific compounds (‘multi-host metabolic specialism’)? Here, we simultaneously investigated the metabolomes of fruit diets and of individuals of a generalist phytophagous species, Drosophila suzukii, that developed on them. The direct comparison of metabolomes of diets and consumers enabled us to disentangle the metabolic fate of common and rarer dietary compounds. We showed that the consumption of biochemically dissimilar diets resulted in a canalized, generic response from generalist individuals, consistent with the metabolic generalism hypothesis. We also showed that many diet-specific metabolites, such as those related to the particular color, odor, or taste of diets, were not metabolized, and rather accumulated in consumer individuals, even when probably detrimental to fitness. As a result, while individuals were mostly similar across diets, the detection of their particular diet was straightforward. Our study thus supports the view that dietary generalism may emerge from a passive, opportunistic use of various resources, contrary to more widespread views of an active role of adaptation in this process. Such a passive stance towards dietary chemicals, probably costly in the short term, might favor the later evolution of new diet specializations.https://elifesciences.org/articles/84370niche breadthecological specializationmetabolomicsgeneralismdietDrosophila suzukii
spellingShingle Laure Olazcuaga
Raymonde Baltenweck
Nicolas Leménager
Alessandra Maia-Grondard
Patricia Claudel
Philippe Hugueney
Julien Foucaud
Metabolic consequences of various fruit-based diets in a generalist insect species
eLife
niche breadth
ecological specialization
metabolomics
generalism
diet
Drosophila suzukii
title Metabolic consequences of various fruit-based diets in a generalist insect species
title_full Metabolic consequences of various fruit-based diets in a generalist insect species
title_fullStr Metabolic consequences of various fruit-based diets in a generalist insect species
title_full_unstemmed Metabolic consequences of various fruit-based diets in a generalist insect species
title_short Metabolic consequences of various fruit-based diets in a generalist insect species
title_sort metabolic consequences of various fruit based diets in a generalist insect species
topic niche breadth
ecological specialization
metabolomics
generalism
diet
Drosophila suzukii
url https://elifesciences.org/articles/84370
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