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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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Autores principales: Olazcuaga, Laure, Baltenweck, Raymonde, Leménager, Nicolas, Maia-Grondard, Alessandra, Claudel, Patricia, Hugueney, Philippe, Foucaud, Julien
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10259468/
https://www.ncbi.nlm.nih.gov/pubmed/37278030
http://dx.doi.org/10.7554/eLife.84370
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author Olazcuaga, Laure
Baltenweck, Raymonde
Leménager, Nicolas
Maia-Grondard, Alessandra
Claudel, Patricia
Hugueney, Philippe
Foucaud, Julien
author_facet Olazcuaga, Laure
Baltenweck, Raymonde
Leménager, Nicolas
Maia-Grondard, Alessandra
Claudel, Patricia
Hugueney, Philippe
Foucaud, Julien
author_sort Olazcuaga, Laure
collection PubMed
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 pubmed-102594682023-06-13 Metabolic consequences of various fruit-based diets in a generalist insect species Olazcuaga, Laure Baltenweck, Raymonde Leménager, Nicolas Maia-Grondard, Alessandra Claudel, Patricia Hugueney, Philippe Foucaud, Julien eLife Ecology 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. eLife Sciences Publications, Ltd 2023-06-06 /pmc/articles/PMC10259468/ /pubmed/37278030 http://dx.doi.org/10.7554/eLife.84370 Text en © 2023, Olazcuaga, Baltenweck et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Ecology
Olazcuaga, Laure
Baltenweck, Raymonde
Leménager, Nicolas
Maia-Grondard, Alessandra
Claudel, Patricia
Hugueney, Philippe
Foucaud, Julien
Metabolic consequences of various fruit-based diets in a generalist insect species
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 Ecology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10259468/
https://www.ncbi.nlm.nih.gov/pubmed/37278030
http://dx.doi.org/10.7554/eLife.84370
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