Cargando…

Carry-over effects of urban larval environments on the transmission potential of dengue-2 virus

BACKGROUND: Mosquitoes are strongly influenced by environmental temperatures, both directly and indirectly via carry-over effects, a phenomenon by which adult phenotypes are shaped indirectly by the environmental conditions experienced in previous life stages. In landscapes with spatially varying mi...

Descripción completa

Detalles Bibliográficos
Autores principales: Evans, Michelle V., Shiau, Justine C., Solano, Nicole, Brindley, Melinda A., Drake, John M., Murdock, Courtney C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6050736/
https://www.ncbi.nlm.nih.gov/pubmed/30016993
http://dx.doi.org/10.1186/s13071-018-3013-3
_version_ 1783340399773876224
author Evans, Michelle V.
Shiau, Justine C.
Solano, Nicole
Brindley, Melinda A.
Drake, John M.
Murdock, Courtney C.
author_facet Evans, Michelle V.
Shiau, Justine C.
Solano, Nicole
Brindley, Melinda A.
Drake, John M.
Murdock, Courtney C.
author_sort Evans, Michelle V.
collection PubMed
description BACKGROUND: Mosquitoes are strongly influenced by environmental temperatures, both directly and indirectly via carry-over effects, a phenomenon by which adult phenotypes are shaped indirectly by the environmental conditions experienced in previous life stages. In landscapes with spatially varying microclimates, such as a city, the effects of environmental temperature can therefore lead to spatial patterns in disease dynamics. To explore the contribution of carry-over effects on the transmission of dengue-2 virus (DENV-2), we conducted a semi-field experiment comparing the demographic and transmission rates of Aedes albopictus reared on different urban land classes in the summer and autumn season. We parameterized a model of vectorial capacity using field- and literature-derived measurements to estimate the bias introduced into predictions of vectorial capacity not accounting for carry-over effects. RESULTS: The larval environment of different land classes and seasons significantly impacted mosquito life history traits. Larval development and survival rates were higher in the summer than the autumn, with no difference across land class. The effect of land class on adult body size differed across season, with suburban mosquitoes having the smallest wing length in the summer and the largest wing length in the autumn, when compared to other land classes. Infection and dissemination rates were higher in the autumn and on suburban and rural land classes compared to urban. Infectiousness did not differ across land class or season. We estimate that not accounting for carry-over effects can underestimate disease transmission potential in suburban and urban sites in the summer by up to 25%. CONCLUSIONS: Our findings demonstrate the potential of the larval environment to differentially impact stages of DENV-2 infection in Ae. albopictus mosquitoes via carry-over effects. Failure to account for carry-over effects of the larval environment in mechanistic models can lead to biased estimates of disease transmission potential at fine-scales in urban environments. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13071-018-3013-3) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-6050736
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-60507362018-07-19 Carry-over effects of urban larval environments on the transmission potential of dengue-2 virus Evans, Michelle V. Shiau, Justine C. Solano, Nicole Brindley, Melinda A. Drake, John M. Murdock, Courtney C. Parasit Vectors Research BACKGROUND: Mosquitoes are strongly influenced by environmental temperatures, both directly and indirectly via carry-over effects, a phenomenon by which adult phenotypes are shaped indirectly by the environmental conditions experienced in previous life stages. In landscapes with spatially varying microclimates, such as a city, the effects of environmental temperature can therefore lead to spatial patterns in disease dynamics. To explore the contribution of carry-over effects on the transmission of dengue-2 virus (DENV-2), we conducted a semi-field experiment comparing the demographic and transmission rates of Aedes albopictus reared on different urban land classes in the summer and autumn season. We parameterized a model of vectorial capacity using field- and literature-derived measurements to estimate the bias introduced into predictions of vectorial capacity not accounting for carry-over effects. RESULTS: The larval environment of different land classes and seasons significantly impacted mosquito life history traits. Larval development and survival rates were higher in the summer than the autumn, with no difference across land class. The effect of land class on adult body size differed across season, with suburban mosquitoes having the smallest wing length in the summer and the largest wing length in the autumn, when compared to other land classes. Infection and dissemination rates were higher in the autumn and on suburban and rural land classes compared to urban. Infectiousness did not differ across land class or season. We estimate that not accounting for carry-over effects can underestimate disease transmission potential in suburban and urban sites in the summer by up to 25%. CONCLUSIONS: Our findings demonstrate the potential of the larval environment to differentially impact stages of DENV-2 infection in Ae. albopictus mosquitoes via carry-over effects. Failure to account for carry-over effects of the larval environment in mechanistic models can lead to biased estimates of disease transmission potential at fine-scales in urban environments. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13071-018-3013-3) contains supplementary material, which is available to authorized users. BioMed Central 2018-07-17 /pmc/articles/PMC6050736/ /pubmed/30016993 http://dx.doi.org/10.1186/s13071-018-3013-3 Text en © The Author(s). 2018 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
Evans, Michelle V.
Shiau, Justine C.
Solano, Nicole
Brindley, Melinda A.
Drake, John M.
Murdock, Courtney C.
Carry-over effects of urban larval environments on the transmission potential of dengue-2 virus
title Carry-over effects of urban larval environments on the transmission potential of dengue-2 virus
title_full Carry-over effects of urban larval environments on the transmission potential of dengue-2 virus
title_fullStr Carry-over effects of urban larval environments on the transmission potential of dengue-2 virus
title_full_unstemmed Carry-over effects of urban larval environments on the transmission potential of dengue-2 virus
title_short Carry-over effects of urban larval environments on the transmission potential of dengue-2 virus
title_sort carry-over effects of urban larval environments on the transmission potential of dengue-2 virus
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6050736/
https://www.ncbi.nlm.nih.gov/pubmed/30016993
http://dx.doi.org/10.1186/s13071-018-3013-3
work_keys_str_mv AT evansmichellev carryovereffectsofurbanlarvalenvironmentsonthetransmissionpotentialofdengue2virus
AT shiaujustinec carryovereffectsofurbanlarvalenvironmentsonthetransmissionpotentialofdengue2virus
AT solanonicole carryovereffectsofurbanlarvalenvironmentsonthetransmissionpotentialofdengue2virus
AT brindleymelindaa carryovereffectsofurbanlarvalenvironmentsonthetransmissionpotentialofdengue2virus
AT drakejohnm carryovereffectsofurbanlarvalenvironmentsonthetransmissionpotentialofdengue2virus
AT murdockcourtneyc carryovereffectsofurbanlarvalenvironmentsonthetransmissionpotentialofdengue2virus