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Habituation to a Deterrent Plant Alkaloid Develops Faster in the Specialist Herbivore Helicoverpa assulta Than in Its Generalist Congener Helicoverpa armigera and Coincides with Taste Neuron Desensitisation

SIMPLE SUMMARY: Habituation to deterrent plant compounds has been found in generalist and specialist insect herbivores. The rate at which plant-feeding insects habituate and at which sensitivity of taste neurons detecting deterrents changes has not been compared among closely related species. The ge...

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Autores principales: Zhou, Dong-Sheng, Wang, Chen-Zhu, van Loon, Joop J. A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8779340/
https://www.ncbi.nlm.nih.gov/pubmed/35055863
http://dx.doi.org/10.3390/insects13010021
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author Zhou, Dong-Sheng
Wang, Chen-Zhu
van Loon, Joop J. A.
author_facet Zhou, Dong-Sheng
Wang, Chen-Zhu
van Loon, Joop J. A.
author_sort Zhou, Dong-Sheng
collection PubMed
description SIMPLE SUMMARY: Habituation to deterrent plant compounds has been found in generalist and specialist insect herbivores. The rate at which plant-feeding insects habituate and at which sensitivity of taste neurons detecting deterrents changes has not been compared among closely related species. The generalist Helicoverpa armigera (Hübner) and the specialist Helicoverpa assulta (Guenée) (Lepidoptera: Noctuidae) differ strongly in degree of host-plant specialism. Both species habituated to the alkaloid strychnine after dietary exposure; however, the specialist H. assulta displayed habituation to strychnine faster (at 48 h) than the generalist H. armigera (at 72 h). Electrophysiological recordings from taste sensilla on mouthparts revealed that a deterrent-sensitive neuron in the medial sensillum styloconicum of both species displayed significantly reduced sensitivity to the deterrent that coincided in time with the onset of habituation. Our findings show that physiological changes in taste neuron sensitivity coincide with habituation to plant compounds that are initially avoided. ABSTRACT: The two closely related moth species, Helicoverpa armigera and H. assulta differ strongly in their degree of host-plant specialism. In dual-choice leaf disk assays, caterpillars of the two species that had been reared on standard artificial diet were strongly deterred by the plant-derived alkaloid strychnine. However, caterpillars of both species reared on artificial diet containing strychnine from neonate to the 5th instar were insensitive to this compound. Fifth instar caterpillars of H. assulta and 4th or 5th instars of H. armigera not exposed to strychnine before were subjected to strychnine-containing diet for 24 h, 36 h, 48 h, or 72 h. Whereas H. assulta displayed habituation to strychnine after 48 h, it took until 72 h for H. armigera to become habituated. Electrophysiological tests revealed that a deterrent-sensitive neuron in the medial sensillum styloconicum of both species displayed significantly reduced sensitivity to strychnine that correlated with the onset of habituation. We conclude that the specialist H. assulta habituated faster to strychnine than the generalist H. armigera and hypothesis that desensitization of deterrent-sensitive neurons contributed to habituation.
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spelling pubmed-87793402022-01-22 Habituation to a Deterrent Plant Alkaloid Develops Faster in the Specialist Herbivore Helicoverpa assulta Than in Its Generalist Congener Helicoverpa armigera and Coincides with Taste Neuron Desensitisation Zhou, Dong-Sheng Wang, Chen-Zhu van Loon, Joop J. A. Insects Article SIMPLE SUMMARY: Habituation to deterrent plant compounds has been found in generalist and specialist insect herbivores. The rate at which plant-feeding insects habituate and at which sensitivity of taste neurons detecting deterrents changes has not been compared among closely related species. The generalist Helicoverpa armigera (Hübner) and the specialist Helicoverpa assulta (Guenée) (Lepidoptera: Noctuidae) differ strongly in degree of host-plant specialism. Both species habituated to the alkaloid strychnine after dietary exposure; however, the specialist H. assulta displayed habituation to strychnine faster (at 48 h) than the generalist H. armigera (at 72 h). Electrophysiological recordings from taste sensilla on mouthparts revealed that a deterrent-sensitive neuron in the medial sensillum styloconicum of both species displayed significantly reduced sensitivity to the deterrent that coincided in time with the onset of habituation. Our findings show that physiological changes in taste neuron sensitivity coincide with habituation to plant compounds that are initially avoided. ABSTRACT: The two closely related moth species, Helicoverpa armigera and H. assulta differ strongly in their degree of host-plant specialism. In dual-choice leaf disk assays, caterpillars of the two species that had been reared on standard artificial diet were strongly deterred by the plant-derived alkaloid strychnine. However, caterpillars of both species reared on artificial diet containing strychnine from neonate to the 5th instar were insensitive to this compound. Fifth instar caterpillars of H. assulta and 4th or 5th instars of H. armigera not exposed to strychnine before were subjected to strychnine-containing diet for 24 h, 36 h, 48 h, or 72 h. Whereas H. assulta displayed habituation to strychnine after 48 h, it took until 72 h for H. armigera to become habituated. Electrophysiological tests revealed that a deterrent-sensitive neuron in the medial sensillum styloconicum of both species displayed significantly reduced sensitivity to strychnine that correlated with the onset of habituation. We conclude that the specialist H. assulta habituated faster to strychnine than the generalist H. armigera and hypothesis that desensitization of deterrent-sensitive neurons contributed to habituation. MDPI 2021-12-23 /pmc/articles/PMC8779340/ /pubmed/35055863 http://dx.doi.org/10.3390/insects13010021 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Zhou, Dong-Sheng
Wang, Chen-Zhu
van Loon, Joop J. A.
Habituation to a Deterrent Plant Alkaloid Develops Faster in the Specialist Herbivore Helicoverpa assulta Than in Its Generalist Congener Helicoverpa armigera and Coincides with Taste Neuron Desensitisation
title Habituation to a Deterrent Plant Alkaloid Develops Faster in the Specialist Herbivore Helicoverpa assulta Than in Its Generalist Congener Helicoverpa armigera and Coincides with Taste Neuron Desensitisation
title_full Habituation to a Deterrent Plant Alkaloid Develops Faster in the Specialist Herbivore Helicoverpa assulta Than in Its Generalist Congener Helicoverpa armigera and Coincides with Taste Neuron Desensitisation
title_fullStr Habituation to a Deterrent Plant Alkaloid Develops Faster in the Specialist Herbivore Helicoverpa assulta Than in Its Generalist Congener Helicoverpa armigera and Coincides with Taste Neuron Desensitisation
title_full_unstemmed Habituation to a Deterrent Plant Alkaloid Develops Faster in the Specialist Herbivore Helicoverpa assulta Than in Its Generalist Congener Helicoverpa armigera and Coincides with Taste Neuron Desensitisation
title_short Habituation to a Deterrent Plant Alkaloid Develops Faster in the Specialist Herbivore Helicoverpa assulta Than in Its Generalist Congener Helicoverpa armigera and Coincides with Taste Neuron Desensitisation
title_sort habituation to a deterrent plant alkaloid develops faster in the specialist herbivore helicoverpa assulta than in its generalist congener helicoverpa armigera and coincides with taste neuron desensitisation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8779340/
https://www.ncbi.nlm.nih.gov/pubmed/35055863
http://dx.doi.org/10.3390/insects13010021
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