Cargando…

The effect of multiple blood-feeding on the longevity and insecticide resistant phenotype in the major malaria vector Anopheles arabiensis (Diptera: Culicidae)

BACKGROUND: Anopheles arabiensis is a major malaria vector in Africa. Adult females are likely to imbibe multiple blood meals during their lifetime. This results in regular exposure to potential toxins and blood-meal induced oxidative stress. Defence responses to these stressors may affect other fac...

Descripción completa

Detalles Bibliográficos
Autores principales: Oliver, Shüné V, Brooke, Basil D
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4161849/
https://www.ncbi.nlm.nih.gov/pubmed/25150975
http://dx.doi.org/10.1186/1756-3305-7-390
_version_ 1782334605736542208
author Oliver, Shüné V
Brooke, Basil D
author_facet Oliver, Shüné V
Brooke, Basil D
author_sort Oliver, Shüné V
collection PubMed
description BACKGROUND: Anopheles arabiensis is a major malaria vector in Africa. Adult females are likely to imbibe multiple blood meals during their lifetime. This results in regular exposure to potential toxins and blood-meal induced oxidative stress. Defence responses to these stressors may affect other factors of epidemiological significance, such as insecticide resistance and longevity. The aims of this study were to examine the effect of multiple blood-feeding on insecticide tolerance/resistance with increasing age, to assess the underlying biochemical mechanisms for the responses recorded, and to assess the effect of multiple blood-feeding on the life histories of adult females drawn from insecticide resistant and susceptible laboratory reared An. arabiensis. METHODS: Laboratory reared An. arabiensis females from an insecticide resistant and an insecticide susceptible colony were offered either a single blood meal or multiple blood meals at 3-day intervals. Their tolerance or resistance to insecticide was then monitored by WHO bioassay four hours post blood-feeding. The biochemical basis of the phenotypic response was assessed by examining the effect of blood on detoxification enzyme activity and the effect of blood-meals on detoxification enzyme activity in ageing mosquitoes. RESULTS: Control cohorts that were not offered any blood meals showed steadily decreasing levels of insecticide tolerance/resistance with age, whereas a single blood meal significantly increased tolerance/resistance primarily at the age of three days. The expression of resistance/tolerance in those cohorts fed multiple blood meals generally showed the least variation with age. These results were consistent following exposure to DDT and pyrethroids but not to malathion. Multiple blood-meals also maintained the DDT and permethrin resistant phenotype, even after treatment females had stopped taking blood-meals. Biochemical analysis suggests that this phenotypic effect in resistant females may be mediated by the maintenance of increased glutathione s-transferase activity as a consequence of multiple blood-feeding. Multiple blood-feeding increased the longevity of insecticide resistant females regardless of their mating status, but only increased the longevity of unmated susceptible females. CONCLUSION: These data suggest that multiple blood-feeding confers a competitive advantage to insecticide resistant females by increased longevity and maintenance of the expression of resistance with age.
format Online
Article
Text
id pubmed-4161849
institution National Center for Biotechnology Information
language English
publishDate 2014
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-41618492014-09-13 The effect of multiple blood-feeding on the longevity and insecticide resistant phenotype in the major malaria vector Anopheles arabiensis (Diptera: Culicidae) Oliver, Shüné V Brooke, Basil D Parasit Vectors Research BACKGROUND: Anopheles arabiensis is a major malaria vector in Africa. Adult females are likely to imbibe multiple blood meals during their lifetime. This results in regular exposure to potential toxins and blood-meal induced oxidative stress. Defence responses to these stressors may affect other factors of epidemiological significance, such as insecticide resistance and longevity. The aims of this study were to examine the effect of multiple blood-feeding on insecticide tolerance/resistance with increasing age, to assess the underlying biochemical mechanisms for the responses recorded, and to assess the effect of multiple blood-feeding on the life histories of adult females drawn from insecticide resistant and susceptible laboratory reared An. arabiensis. METHODS: Laboratory reared An. arabiensis females from an insecticide resistant and an insecticide susceptible colony were offered either a single blood meal or multiple blood meals at 3-day intervals. Their tolerance or resistance to insecticide was then monitored by WHO bioassay four hours post blood-feeding. The biochemical basis of the phenotypic response was assessed by examining the effect of blood on detoxification enzyme activity and the effect of blood-meals on detoxification enzyme activity in ageing mosquitoes. RESULTS: Control cohorts that were not offered any blood meals showed steadily decreasing levels of insecticide tolerance/resistance with age, whereas a single blood meal significantly increased tolerance/resistance primarily at the age of three days. The expression of resistance/tolerance in those cohorts fed multiple blood meals generally showed the least variation with age. These results were consistent following exposure to DDT and pyrethroids but not to malathion. Multiple blood-meals also maintained the DDT and permethrin resistant phenotype, even after treatment females had stopped taking blood-meals. Biochemical analysis suggests that this phenotypic effect in resistant females may be mediated by the maintenance of increased glutathione s-transferase activity as a consequence of multiple blood-feeding. Multiple blood-feeding increased the longevity of insecticide resistant females regardless of their mating status, but only increased the longevity of unmated susceptible females. CONCLUSION: These data suggest that multiple blood-feeding confers a competitive advantage to insecticide resistant females by increased longevity and maintenance of the expression of resistance with age. BioMed Central 2014-08-23 /pmc/articles/PMC4161849/ /pubmed/25150975 http://dx.doi.org/10.1186/1756-3305-7-390 Text en © Oliver and Brooke; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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
Oliver, Shüné V
Brooke, Basil D
The effect of multiple blood-feeding on the longevity and insecticide resistant phenotype in the major malaria vector Anopheles arabiensis (Diptera: Culicidae)
title The effect of multiple blood-feeding on the longevity and insecticide resistant phenotype in the major malaria vector Anopheles arabiensis (Diptera: Culicidae)
title_full The effect of multiple blood-feeding on the longevity and insecticide resistant phenotype in the major malaria vector Anopheles arabiensis (Diptera: Culicidae)
title_fullStr The effect of multiple blood-feeding on the longevity and insecticide resistant phenotype in the major malaria vector Anopheles arabiensis (Diptera: Culicidae)
title_full_unstemmed The effect of multiple blood-feeding on the longevity and insecticide resistant phenotype in the major malaria vector Anopheles arabiensis (Diptera: Culicidae)
title_short The effect of multiple blood-feeding on the longevity and insecticide resistant phenotype in the major malaria vector Anopheles arabiensis (Diptera: Culicidae)
title_sort effect of multiple blood-feeding on the longevity and insecticide resistant phenotype in the major malaria vector anopheles arabiensis (diptera: culicidae)
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4161849/
https://www.ncbi.nlm.nih.gov/pubmed/25150975
http://dx.doi.org/10.1186/1756-3305-7-390
work_keys_str_mv AT olivershunev theeffectofmultiplebloodfeedingonthelongevityandinsecticideresistantphenotypeinthemajormalariavectoranophelesarabiensisdipteraculicidae
AT brookebasild theeffectofmultiplebloodfeedingonthelongevityandinsecticideresistantphenotypeinthemajormalariavectoranophelesarabiensisdipteraculicidae
AT olivershunev effectofmultiplebloodfeedingonthelongevityandinsecticideresistantphenotypeinthemajormalariavectoranophelesarabiensisdipteraculicidae
AT brookebasild effectofmultiplebloodfeedingonthelongevityandinsecticideresistantphenotypeinthemajormalariavectoranophelesarabiensisdipteraculicidae