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      High intraspecific variability and previous experience affect polyphenol metabolism in polyphagous Lymantria mathura caterpillars

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          Abstract

          Polyphagous insect herbivores feed on multiple host‐plant species and face a highly variable chemical landscape. Comparative studies of polyphagous herbivore metabolism across a range of plants is an ideal approach for exploring how intra‐ and interspecific chemical variation shapes species interactions. We used polyphagous caterpillars of Lymantria mathura (Erebidae, Lepidoptera) to explore mechanisms that may contribute to its ability to feed on various hosts. We focused on intraspecific variation in polyphenol metabolism, the fates of individual polyphenols, and the role of previous feeding experience on polyphenol metabolism and leaf consumption. We collected the caterpillars from Acer amoenum (Sapindaceae), Carpinus cordata (Betulaceae), and Quercus crispula (Fagaceae). We first fed the larvae with the leaves of their original host and characterized the polyphenol profiles in leaves and frass. We then transferred a subset of larvae to a different host species and quantified how host shifting affected their leaf consumption and polyphenol metabolism. There was high intraspecific variation in frass composition, even among caterpillars fed with one host. While polyphenols had various fates when ingested by the caterpillars, most of them were passively excreted. When we transferred the caterpillars to a new host, their previous experience influenced how they metabolized polyphenols. The one‐host larvae metabolized a larger quantity of ingested polyphenols than two‐host caterpillars. Some of these metabolites could have been sequestered, others were probably activated in the gut. One‐host caterpillars retained more of the ingested leaf biomass than transferred caterpillars. The pronounced intraspecific variation in polyphenol metabolism, an ability to excrete ingested metabolites and potential dietary habituation are factors that may contribute to the ability of L. mathura to feed across multiple hosts. Further comparative studies can help identify if these mechanisms are related to differential host‐choice and response to host‐plant traits in specialist and generalist insect herbivores.

          Abstract

          We studied polyphenol metabolism in polyphagous caterpillars of Lymantria mathura (Erebidae, Lepidoptera) to explore mechanisms that may contribute to its ability to feed on various host‐plants. We detected pronounced intraspecific variation in polyphenol metabolism, an ability to excrete ingested metabolites and potential dietary habituation. Our results provide support for the hypothesis that generalists and specialists may have distinct metabolic strategies for dealing with secondary metabolites.

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          R: a language and environøent for statistical computing

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            Specialist versus generalist insect herbivores and plant defense.

            There has been a long-standing hypothesis that specialist and generalist insects interact with plants in distinct ways. Although many tests exist, they typically compare only one species of each, they sometimes confound specialization and feeding guild, and often do not link chemical or transcriptional measures of the plant to actual resistance. In this review, we synthesize current data on whether specialists and generalists actually differ, with special attention to comparisons of their differential elicitation of plant responses. Although we find few consistencies in plant induction by specialists versus generalists, feeding guilds are predictive of differential plant responses. We outline a novel set of predictions based on current coevolutionary hypotheses and make methodological suggestions for improved comparisons of specialists and generalists. Copyright © 2012 Elsevier Ltd. All rights reserved.
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              The global distribution of diet breadth in insect herbivores.

              Understanding variation in resource specialization is important for progress on issues that include coevolution, community assembly, ecosystem processes, and the latitudinal gradient of species richness. Herbivorous insects are useful models for studying resource specialization, and the interaction between plants and herbivorous insects is one of the most common and consequential ecological associations on the planet. However, uncertainty persists regarding fundamental features of herbivore diet breadth, including its relationship to latitude and plant species richness. Here, we use a global dataset to investigate host range for over 7,500 insect herbivore species covering a wide taxonomic breadth and interacting with more than 2,000 species of plants in 165 families. We ask whether relatively specialized and generalized herbivores represent a dichotomy rather than a continuum from few to many host families and species attacked and whether diet breadth changes with increasing plant species richness toward the tropics. Across geographic regions and taxonomic subsets of the data, we find that the distribution of diet breadth is fit well by a discrete, truncated Pareto power law characterized by the predominance of specialized herbivores and a long, thin tail of more generalized species. Both the taxonomic and phylogenetic distributions of diet breadth shift globally with latitude, consistent with a higher frequency of specialized insects in tropical regions. We also find that more diverse lineages of plants support assemblages of relatively more specialized herbivores and that the global distribution of plant diversity contributes to but does not fully explain the latitudinal gradient in insect herbivore specialization.
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                Author and article information

                Contributors
                volf@entu.cas.cz
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                09 February 2024
                February 2024
                : 14
                : 2 ( doiID: 10.1002/ece3.v14.2 )
                : e10973
                Affiliations
                [ 1 ] Biology Centre Czech Academy of Sciences Ceske Budejovice Czech Republic
                [ 2 ] Faculty of Science University of South Bohemia Ceske Budejovice Czech Republic
                [ 3 ] Department of Chemistry University of Turku Turku Finland
                [ 4 ] Faculty of Science Chiba University Chiba Japan
                [ 5 ] New Guinea Binatang Research Center Madang Papua New Guinea
                [ 6 ] Graduate School of Agricultural and Life Sciences The University of Tokyo Tokyo Japan
                [ 7 ] Agriculture and Environment Department Harper Adams University Newport UK
                Author notes
                [*] [* ] Correspondence

                Martin Volf, Biology Centre, Czech Academy of Sciences, Institute of Entomology, Branisovska 31, 37005 Ceske Budejovice, Czech Republic.

                Email: volf@ 123456entu.cas.cz

                Author information
                https://orcid.org/0000-0003-4126-3897
                https://orcid.org/0000-0002-4707-4918
                https://orcid.org/0000-0003-3608-8780
                https://orcid.org/0000-0002-8818-6991
                https://orcid.org/0000-0003-4374-4045
                https://orcid.org/0000-0001-7918-8023
                https://orcid.org/0000-0002-2912-7094
                https://orcid.org/0000-0001-6621-9409
                Article
                ECE310973 ECE-2023-08-01322.R1
                10.1002/ece3.10973
                10857923
                38343568
                77afd9c5-2eb0-44bf-805d-6b257b8993f4
                © 2024 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 14 December 2023
                : 03 August 2023
                : 21 December 2023
                Page count
                Figures: 6, Tables: 1, Pages: 13, Words: 9177
                Funding
                Funded by: Grantová Agentura České Republiky , doi 10.13039/501100001824;
                Award ID: 19‐28126X
                Funded by: Academy of Finland , doi 10.13039/501100002341;
                Award ID: 341836
                Funded by: European Research Council , doi 10.13039/501100000781;
                Award ID: 669609
                Funded by: Harper Adams University , doi 10.13039/100010011;
                Funded by: Japan Society for the Promotion of Science , doi 10.13039/501100001691;
                Award ID: 26550087
                Categories
                Chemical Ecology
                Research Article
                Research Articles
                Custom metadata
                2.0
                February 2024
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.3.6 mode:remove_FC converted:09.02.2024

                Evolutionary Biology
                chemical defenses,detoxification,flavonoids,frass,habituation,tannins
                Evolutionary Biology
                chemical defenses, detoxification, flavonoids, frass, habituation, tannins

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