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Temperature impacts the environmental suitability for malaria transmission by Anopheles gambiae and Anopheles stephensi

Extrinsic environmental factors influence the spatiotemporal dynamics of many organisms, including insects that transmit the pathogens responsible for vector‐borne diseases (VBDs). Temperature is an especially important constraint on the fitness of a wide variety of ectothermic insects. A mechanisti...

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Autores principales: Villena, Oswaldo C., Ryan, Sadie J., Murdock, Courtney C., Johnson, Leah R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9357211/
https://www.ncbi.nlm.nih.gov/pubmed/35315521
http://dx.doi.org/10.1002/ecy.3685
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author Villena, Oswaldo C.
Ryan, Sadie J.
Murdock, Courtney C.
Johnson, Leah R.
author_facet Villena, Oswaldo C.
Ryan, Sadie J.
Murdock, Courtney C.
Johnson, Leah R.
author_sort Villena, Oswaldo C.
collection PubMed
description Extrinsic environmental factors influence the spatiotemporal dynamics of many organisms, including insects that transmit the pathogens responsible for vector‐borne diseases (VBDs). Temperature is an especially important constraint on the fitness of a wide variety of ectothermic insects. A mechanistic understanding of how temperature impacts traits of ectotherms, and thus the distribution of ectotherms and vector‐borne infections, is key to predicting the consequences of climate change on transmission of VBDs like malaria. However, the response of transmission to temperature and other drivers is complex, as thermal traits of ectotherms are typically nonlinear, and they interact to determine transmission constraints. In this study, we assess and compare the effect of temperature on the transmission of two malaria parasites, Plasmodium falciparum and Plasmodium vivax, by two malaria vector species, Anopheles gambiae and Anopheles stephensi. We model the nonlinear responses of temperature dependent mosquito and parasite traits (mosquito development rate, bite rate, fecundity, proportion of eggs surviving to adulthood, vector competence, mortality rate, and parasite development rate) and incorporate these traits into a suitability metric based on a model for the basic reproductive number across temperatures. Our model predicts that the optimum temperature for transmission suitability is similar for the four mosquito–parasite combinations assessed in this study, but may differ at the thermal limits. More specifically, we found significant differences in the upper thermal limit between parasites spread by the same mosquito (A. stephensi) and between mosquitoes carrying P. falciparum. In contrast, at the lower thermal limit the significant differences were primarily between the mosquito species that both carried the same pathogen (e.g., A. stephensi and A. gambiae both with P. falciparum). Using prevalence data, we show that the transmission suitability metric [Formula: see text] calculated from our mechanistic model is consistent with observed P. falciparum prevalence in Africa and Asia but is equivocal for P. vivax prevalence in Asia, and inconsistent with P. vivax prevalence in Africa. We mapped risk to illustrate the number of months various areas in Africa and Asia predicted to be suitable for malaria transmission based on this suitability metric. This mapping provides spatially explicit predictions for suitability and transmission risk.
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spelling pubmed-93572112022-08-07 Temperature impacts the environmental suitability for malaria transmission by Anopheles gambiae and Anopheles stephensi Villena, Oswaldo C. Ryan, Sadie J. Murdock, Courtney C. Johnson, Leah R. Ecology Articles Extrinsic environmental factors influence the spatiotemporal dynamics of many organisms, including insects that transmit the pathogens responsible for vector‐borne diseases (VBDs). Temperature is an especially important constraint on the fitness of a wide variety of ectothermic insects. A mechanistic understanding of how temperature impacts traits of ectotherms, and thus the distribution of ectotherms and vector‐borne infections, is key to predicting the consequences of climate change on transmission of VBDs like malaria. However, the response of transmission to temperature and other drivers is complex, as thermal traits of ectotherms are typically nonlinear, and they interact to determine transmission constraints. In this study, we assess and compare the effect of temperature on the transmission of two malaria parasites, Plasmodium falciparum and Plasmodium vivax, by two malaria vector species, Anopheles gambiae and Anopheles stephensi. We model the nonlinear responses of temperature dependent mosquito and parasite traits (mosquito development rate, bite rate, fecundity, proportion of eggs surviving to adulthood, vector competence, mortality rate, and parasite development rate) and incorporate these traits into a suitability metric based on a model for the basic reproductive number across temperatures. Our model predicts that the optimum temperature for transmission suitability is similar for the four mosquito–parasite combinations assessed in this study, but may differ at the thermal limits. More specifically, we found significant differences in the upper thermal limit between parasites spread by the same mosquito (A. stephensi) and between mosquitoes carrying P. falciparum. In contrast, at the lower thermal limit the significant differences were primarily between the mosquito species that both carried the same pathogen (e.g., A. stephensi and A. gambiae both with P. falciparum). Using prevalence data, we show that the transmission suitability metric [Formula: see text] calculated from our mechanistic model is consistent with observed P. falciparum prevalence in Africa and Asia but is equivocal for P. vivax prevalence in Asia, and inconsistent with P. vivax prevalence in Africa. We mapped risk to illustrate the number of months various areas in Africa and Asia predicted to be suitable for malaria transmission based on this suitability metric. This mapping provides spatially explicit predictions for suitability and transmission risk. John Wiley & Sons, Inc. 2022-06-14 2022-08 /pmc/articles/PMC9357211/ /pubmed/35315521 http://dx.doi.org/10.1002/ecy.3685 Text en © 2022 The Authors. Ecology published by Wiley Periodicals LLC on behalf of The Ecological Society of America. https://creativecommons.org/licenses/by-nc/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Articles
Villena, Oswaldo C.
Ryan, Sadie J.
Murdock, Courtney C.
Johnson, Leah R.
Temperature impacts the environmental suitability for malaria transmission by Anopheles gambiae and Anopheles stephensi
title Temperature impacts the environmental suitability for malaria transmission by Anopheles gambiae and Anopheles stephensi
title_full Temperature impacts the environmental suitability for malaria transmission by Anopheles gambiae and Anopheles stephensi
title_fullStr Temperature impacts the environmental suitability for malaria transmission by Anopheles gambiae and Anopheles stephensi
title_full_unstemmed Temperature impacts the environmental suitability for malaria transmission by Anopheles gambiae and Anopheles stephensi
title_short Temperature impacts the environmental suitability for malaria transmission by Anopheles gambiae and Anopheles stephensi
title_sort temperature impacts the environmental suitability for malaria transmission by anopheles gambiae and anopheles stephensi
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9357211/
https://www.ncbi.nlm.nih.gov/pubmed/35315521
http://dx.doi.org/10.1002/ecy.3685
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