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Temperature-dependent changes in the host-seeking behaviors of parasitic nematodes

BACKGROUND: Entomopathogenic nematodes (EPNs) are lethal parasites of insects that are of interest as biocontrol agents for insect pests and disease vectors. Although EPNs have been successfully commercialized for pest control, their efficacy in the field is often inconsistent for reasons that remai...

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Autores principales: Lee, Joon Ha, Dillman, Adler R., Hallem, Elissa A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4858831/
https://www.ncbi.nlm.nih.gov/pubmed/27154502
http://dx.doi.org/10.1186/s12915-016-0259-0
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author Lee, Joon Ha
Dillman, Adler R.
Hallem, Elissa A.
author_facet Lee, Joon Ha
Dillman, Adler R.
Hallem, Elissa A.
author_sort Lee, Joon Ha
collection PubMed
description BACKGROUND: Entomopathogenic nematodes (EPNs) are lethal parasites of insects that are of interest as biocontrol agents for insect pests and disease vectors. Although EPNs have been successfully commercialized for pest control, their efficacy in the field is often inconsistent for reasons that remain elusive. EPN infective juveniles (IJs) actively search for hosts to infect using a diverse array of host-emitted odorants. Here we investigate whether their host-seeking behavior is subject to context-dependent modulation. RESULTS: We find that EPN IJs exhibit extreme plasticity of olfactory behavior as a function of cultivation temperature. Many odorants that are attractive for IJs grown at lower temperatures are repulsive for IJs grown at higher temperatures and vice versa. Temperature-induced changes in olfactory preferences occur gradually over the course of days to weeks and are reversible. Similar changes in olfactory behavior occur in some EPNs as a function of IJ age. EPNs also show temperature-dependent changes in their host-seeking strategy: IJs cultured at lower temperatures appear to more actively cruise for hosts than IJs cultured at higher temperatures. Furthermore, we find that the skin-penetrating rat parasite Strongyloides ratti also shows temperature-dependent changes in olfactory behavior, demonstrating that such changes occur in mammalian-parasitic nematodes. CONCLUSIONS: IJs are developmentally arrested and long-lived, often surviving in the environment through multiple seasonal temperature changes. Temperature-dependent modulation of behavior may enable IJs to optimize host seeking in response to changing environmental conditions, and may play a previously unrecognized role in shaping the interactions of both beneficial and harmful parasitic nematodes with their hosts. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-016-0259-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-48588312016-05-07 Temperature-dependent changes in the host-seeking behaviors of parasitic nematodes Lee, Joon Ha Dillman, Adler R. Hallem, Elissa A. BMC Biol Research Article BACKGROUND: Entomopathogenic nematodes (EPNs) are lethal parasites of insects that are of interest as biocontrol agents for insect pests and disease vectors. Although EPNs have been successfully commercialized for pest control, their efficacy in the field is often inconsistent for reasons that remain elusive. EPN infective juveniles (IJs) actively search for hosts to infect using a diverse array of host-emitted odorants. Here we investigate whether their host-seeking behavior is subject to context-dependent modulation. RESULTS: We find that EPN IJs exhibit extreme plasticity of olfactory behavior as a function of cultivation temperature. Many odorants that are attractive for IJs grown at lower temperatures are repulsive for IJs grown at higher temperatures and vice versa. Temperature-induced changes in olfactory preferences occur gradually over the course of days to weeks and are reversible. Similar changes in olfactory behavior occur in some EPNs as a function of IJ age. EPNs also show temperature-dependent changes in their host-seeking strategy: IJs cultured at lower temperatures appear to more actively cruise for hosts than IJs cultured at higher temperatures. Furthermore, we find that the skin-penetrating rat parasite Strongyloides ratti also shows temperature-dependent changes in olfactory behavior, demonstrating that such changes occur in mammalian-parasitic nematodes. CONCLUSIONS: IJs are developmentally arrested and long-lived, often surviving in the environment through multiple seasonal temperature changes. Temperature-dependent modulation of behavior may enable IJs to optimize host seeking in response to changing environmental conditions, and may play a previously unrecognized role in shaping the interactions of both beneficial and harmful parasitic nematodes with their hosts. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-016-0259-0) contains supplementary material, which is available to authorized users. BioMed Central 2016-05-06 /pmc/articles/PMC4858831/ /pubmed/27154502 http://dx.doi.org/10.1186/s12915-016-0259-0 Text en © Lee et al. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Lee, Joon Ha
Dillman, Adler R.
Hallem, Elissa A.
Temperature-dependent changes in the host-seeking behaviors of parasitic nematodes
title Temperature-dependent changes in the host-seeking behaviors of parasitic nematodes
title_full Temperature-dependent changes in the host-seeking behaviors of parasitic nematodes
title_fullStr Temperature-dependent changes in the host-seeking behaviors of parasitic nematodes
title_full_unstemmed Temperature-dependent changes in the host-seeking behaviors of parasitic nematodes
title_short Temperature-dependent changes in the host-seeking behaviors of parasitic nematodes
title_sort temperature-dependent changes in the host-seeking behaviors of parasitic nematodes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4858831/
https://www.ncbi.nlm.nih.gov/pubmed/27154502
http://dx.doi.org/10.1186/s12915-016-0259-0
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