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Trypanosomes Modify the Behavior of Their Insect Hosts: Effects on Locomotion and on the Expression of a Related Gene

BACKGROUND: As a result of evolution, the biology of triatomines must have been significantly adapted to accommodate trypanosome infection in a complex network of vector-vertebrate-parasite interactions. Arthropod-borne parasites have probably developed mechanisms, largely still unknown, to exploit...

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Autores principales: Marliére, Newmar Pinto, Latorre-Estivalis, José Manuel, Lorenzo, Marcelo Gustavo, Carrasco, David, Alves-Silva, Juliana, Rodrigues, Juliana de Oliveira, Ferreira, Luciana de Lima, Lara, Luisa de Melo, Lowenberger, Carl, Guarneri, Alessandra Aparecida
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4546274/
https://www.ncbi.nlm.nih.gov/pubmed/26291723
http://dx.doi.org/10.1371/journal.pntd.0003973
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author Marliére, Newmar Pinto
Latorre-Estivalis, José Manuel
Lorenzo, Marcelo Gustavo
Carrasco, David
Alves-Silva, Juliana
Rodrigues, Juliana de Oliveira
Ferreira, Luciana de Lima
Lara, Luisa de Melo
Lowenberger, Carl
Guarneri, Alessandra Aparecida
author_facet Marliére, Newmar Pinto
Latorre-Estivalis, José Manuel
Lorenzo, Marcelo Gustavo
Carrasco, David
Alves-Silva, Juliana
Rodrigues, Juliana de Oliveira
Ferreira, Luciana de Lima
Lara, Luisa de Melo
Lowenberger, Carl
Guarneri, Alessandra Aparecida
author_sort Marliére, Newmar Pinto
collection PubMed
description BACKGROUND: As a result of evolution, the biology of triatomines must have been significantly adapted to accommodate trypanosome infection in a complex network of vector-vertebrate-parasite interactions. Arthropod-borne parasites have probably developed mechanisms, largely still unknown, to exploit the vector-vertebrate host interactions to ensure their transmission to suitable hosts. Triatomines exhibit a strong negative phototaxis and nocturnal activity, believed to be important for insect survival against its predators. METHODOLOGY/PRINCIPAL FINDINGS: In this study we quantified phototaxis and locomotion in starved fifth instar nymphs of Rhodnius prolixus infected with Trypanosoma cruzi or Trypanosoma rangeli. T. cruzi infection did not alter insect phototaxis, but induced an overall 20% decrease in the number of bug locomotory events. Furthermore, the significant differences induced by this parasite were concentrated at the beginning of the scotophase. Conversely, T. rangeli modified both behaviors, as it significantly decreased bug negative phototaxis, while it induced a 23% increase in the number of locomotory events in infected bugs. In this case, the significant effects were observed during the photophase. We also investigated the expression of Rpfor, the triatomine ortholog of the foraging gene known to modulate locomotion in other insects, and found a 4.8 fold increase for T. rangeli infected insects. CONCLUSIONS/SIGNIFICANCE: We demonstrated for the first time that trypanosome infection modulates the locomotory activity of the invertebrate host. T. rangeli infection seems to be more broadly effective, as besides affecting the intensity of locomotion this parasite also diminished negative phototaxis and the expression of a behavior-associated gene in the triatomine vector.
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spelling pubmed-45462742015-08-26 Trypanosomes Modify the Behavior of Their Insect Hosts: Effects on Locomotion and on the Expression of a Related Gene Marliére, Newmar Pinto Latorre-Estivalis, José Manuel Lorenzo, Marcelo Gustavo Carrasco, David Alves-Silva, Juliana Rodrigues, Juliana de Oliveira Ferreira, Luciana de Lima Lara, Luisa de Melo Lowenberger, Carl Guarneri, Alessandra Aparecida PLoS Negl Trop Dis Research Article BACKGROUND: As a result of evolution, the biology of triatomines must have been significantly adapted to accommodate trypanosome infection in a complex network of vector-vertebrate-parasite interactions. Arthropod-borne parasites have probably developed mechanisms, largely still unknown, to exploit the vector-vertebrate host interactions to ensure their transmission to suitable hosts. Triatomines exhibit a strong negative phototaxis and nocturnal activity, believed to be important for insect survival against its predators. METHODOLOGY/PRINCIPAL FINDINGS: In this study we quantified phototaxis and locomotion in starved fifth instar nymphs of Rhodnius prolixus infected with Trypanosoma cruzi or Trypanosoma rangeli. T. cruzi infection did not alter insect phototaxis, but induced an overall 20% decrease in the number of bug locomotory events. Furthermore, the significant differences induced by this parasite were concentrated at the beginning of the scotophase. Conversely, T. rangeli modified both behaviors, as it significantly decreased bug negative phototaxis, while it induced a 23% increase in the number of locomotory events in infected bugs. In this case, the significant effects were observed during the photophase. We also investigated the expression of Rpfor, the triatomine ortholog of the foraging gene known to modulate locomotion in other insects, and found a 4.8 fold increase for T. rangeli infected insects. CONCLUSIONS/SIGNIFICANCE: We demonstrated for the first time that trypanosome infection modulates the locomotory activity of the invertebrate host. T. rangeli infection seems to be more broadly effective, as besides affecting the intensity of locomotion this parasite also diminished negative phototaxis and the expression of a behavior-associated gene in the triatomine vector. Public Library of Science 2015-08-20 /pmc/articles/PMC4546274/ /pubmed/26291723 http://dx.doi.org/10.1371/journal.pntd.0003973 Text en © 2015 Marliére et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Marliére, Newmar Pinto
Latorre-Estivalis, José Manuel
Lorenzo, Marcelo Gustavo
Carrasco, David
Alves-Silva, Juliana
Rodrigues, Juliana de Oliveira
Ferreira, Luciana de Lima
Lara, Luisa de Melo
Lowenberger, Carl
Guarneri, Alessandra Aparecida
Trypanosomes Modify the Behavior of Their Insect Hosts: Effects on Locomotion and on the Expression of a Related Gene
title Trypanosomes Modify the Behavior of Their Insect Hosts: Effects on Locomotion and on the Expression of a Related Gene
title_full Trypanosomes Modify the Behavior of Their Insect Hosts: Effects on Locomotion and on the Expression of a Related Gene
title_fullStr Trypanosomes Modify the Behavior of Their Insect Hosts: Effects on Locomotion and on the Expression of a Related Gene
title_full_unstemmed Trypanosomes Modify the Behavior of Their Insect Hosts: Effects on Locomotion and on the Expression of a Related Gene
title_short Trypanosomes Modify the Behavior of Their Insect Hosts: Effects on Locomotion and on the Expression of a Related Gene
title_sort trypanosomes modify the behavior of their insect hosts: effects on locomotion and on the expression of a related gene
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4546274/
https://www.ncbi.nlm.nih.gov/pubmed/26291723
http://dx.doi.org/10.1371/journal.pntd.0003973
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