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      Altered capsaicin levels in domesticated chili pepper varieties affect the interaction between a generalist herbivore and its ectoparasitoid

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          Abstract

          Plant domestication has commonly reduced levels of secondary metabolites known to confer resistance against insects. Chili pepper is a special case because the fruits of different varieties have been selected for lower and higher levels of capsaicin, the main compound associated with defence. This may have important consequences for insect herbivores and their natural enemies. Despite the widespread consumption of chili peppers worldwide, the effects of capsaicin on insects are poorly understood. Here, we investigated the effect of capsaicin on a generalist herbivore, Spodoptera latifascia (Lepidoptera: Noctuidae) and its ectoparasitoid, Euplectrus platyhypenae (Hymenoptera: Eulophidae). Using chili varieties with three pungency levels: non-pungent (Padron), mild (Cayenne) and highly pungent (Habanero), as well as artificial diets spiked with three different levels of synthetic capsaicin, we determined whether higher capsaicin levels negatively affect the performance of these insects. Overall, capsaicin had a negative effect on both herbivore and parasitoid performance , particularly at high concentrations. Caterpillars reared on highly pungent fruits and high-capsaicin diet had longer development time, reduced pupation success, lower adult emergence, but also lower parasitism rates than caterpillars reared on mild or non-capsaicin treatments. In addition, we found that the caterpillars were capable of sequestering capsaicinoids in their haemolymph when fed on the high pungent variety with consequences for parasitoids’ performance and oviposition decisions. These results increase our understanding of the role of capsaicin as a chemical defence against insects and its potential implications for pest management.

          Supplementary Information

          The online version contains supplementary material available at 10.1007/s10340-021-01399-8.

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          Most cited references75

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          Ecology of Infochemical Use by Natural Enemies in a Tritrophic Context

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            Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops.

            Domesticated food crops are derived from a phylogenetically diverse assemblage of wild ancestors through artificial selection for different traits. Our understanding of domestication, however, is based upon a subset of well-studied 'model' crops, many of them from the Poaceae family. Here, we investigate domestication traits and theories using a broader range of crops. We reviewed domestication information (e.g. center of domestication, plant traits, wild ancestors, domestication dates, domestication traits, early and current uses) for 203 major and minor food crops. Compiled data were used to test classic and contemporary theories in crop domestication. Many typical features of domestication associated with model crops, including changes in ploidy level, loss of shattering, multiple origins, and domestication outside the native range, are less common within this broader dataset. In addition, there are strong spatial and temporal trends in our dataset. The overall time required to domesticate a species has decreased since the earliest domestication events. The frequencies of some domestication syndrome traits (e.g. nonshattering) have decreased over time, while others (e.g. changes to secondary metabolites) have increased. We discuss the influences of the ecological, evolutionary, cultural and technological factors that make domestication a dynamic and ongoing process. © 2012 The Authors. New Phytologist © 2012 New Phytologist Trust.
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              Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species.

              Hot pepper (Capsicum annuum), one of the oldest domesticated crops in the Americas, is the most widely grown spice crop in the world. We report whole-genome sequencing and assembly of the hot pepper (Mexican landrace of Capsicum annuum cv. CM334) at 186.6× coverage. We also report resequencing of two cultivated peppers and de novo sequencing of the wild species Capsicum chinense. The genome size of the hot pepper was approximately fourfold larger than that of its close relative tomato, and the genome showed an accumulation of Gypsy and Caulimoviridae family elements. Integrative genomic and transcriptomic analyses suggested that change in gene expression and neofunctionalization of capsaicin synthase have shaped capsaicinoid biosynthesis. We found differential molecular patterns of ripening regulators and ethylene synthesis in hot pepper and tomato. The reference genome will serve as a platform for improving the nutritional and medicinal values of Capsicum species.
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                Author and article information

                Contributors
                betty.benrey@unine.ch
                Journal
                J Pest Sci (2004)
                J Pest Sci (2004)
                Journal of Pest Science
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                1612-4758
                1612-4766
                25 June 2021
                25 June 2021
                2022
                : 95
                : 2
                : 735-747
                Affiliations
                [1 ]GRID grid.10711.36, ISNI 0000 0001 2297 7718, Laboratory of Evolutionary Entomology, Institute of Biology, , University of Neuchâtel, ; Rue Emile-Argand 11, 2000 Neuchâtel, Switzerland
                [2 ]GRID grid.10711.36, ISNI 0000 0001 2297 7718, Fundamental and Applied Research in Chemical Ecology, Institute of Biology, , University of Neuchâtel, ; Rue Emile-Argand 11, 2000 Neuchâtel, Switzerland
                [3 ]GRID grid.10711.36, ISNI 0000 0001 2297 7718, Neuchâtel Platform of Analytical Chemistry, Institute of Chemistry, , University of Neuchâtel, ; Rue Emile-Argand 11, 2000 Neuchâtel, Switzerland
                Author notes

                Communicated by Antonio Biondi.

                Author information
                http://orcid.org/0000-0002-3230-4450
                Article
                1399
                10.1007/s10340-021-01399-8
                8860780
                619f4a9f-7ba6-4bb0-95b9-0bd90ac8deec
                © The Author(s) 2021

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 23 February 2021
                : 31 May 2021
                : 8 June 2021
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001711, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung;
                Award ID: 31003A-162860
                Award Recipient :
                Funded by: Université de Neuchâtel
                Categories
                Original Paper
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2022

                Pests, Diseases & Weeds
                chili pepper,domestication,capsaicinoids,plant-mediated,sequestration,tritrophic interactions

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