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      Thermal biology of mosquito‐borne disease

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          Abstract

          Mosquito‐borne diseases cause a major burden of disease worldwide. The vital rates of these ectothermic vectors and parasites respond strongly and nonlinearly to temperature and therefore to climate change. Here, we review how trait‐based approaches can synthesise and mechanistically predict the temperature dependence of transmission across vectors, pathogens, and environments. We present 11 pathogens transmitted by 15 different mosquito species – including globally important diseases like malaria, dengue, and Zika – synthesised from previously published studies. Transmission varied strongly and unimodally with temperature, peaking at 23–29ºC and declining to zero below 9–23ºC and above 32–38ºC. Different traits restricted transmission at low versus high temperatures, and temperature effects on transmission varied by both mosquito and parasite species. Temperate pathogens exhibit broader thermal ranges and cooler thermal minima and optima than tropical pathogens. Among tropical pathogens, malaria and Ross River virus had lower thermal optima (25–26ºC) while dengue and Zika viruses had the highest (29ºC) thermal optima. We expect warming to increase transmission below thermal optima but decrease transmission above optima. Key directions for future work include linking mechanistic models to field transmission, combining temperature effects with control measures, incorporating trait variation and temperature variation, and investigating climate adaptation and migration.

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          Novel climates, no-analog communities, and ecological surprises

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            Thermal Adaptation

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              Systematic variation in the temperature dependence of physiological and ecological traits.

              To understand the effects of temperature on biological systems, we compile, organize, and analyze a database of 1,072 thermal responses for microbes, plants, and animals. The unprecedented diversity of traits (n = 112), species (n = 309), body sizes (15 orders of magnitude), and habitats (all major biomes) in our database allows us to quantify novel features of the temperature response of biological traits. In particular, analysis of the rising component of within-species (intraspecific) responses reveals that 87% are fit well by the Boltzmann-Arrhenius model. The mean activation energy for these rises is 0.66 ± 0.05 eV, similar to the reported across-species (interspecific) value of 0.65 eV. However, systematic variation in the distribution of rise activation energies is evident, including previously unrecognized right skewness around a median of 0.55 eV. This skewness exists across levels of organization, taxa, trophic groups, and habitats, and it is partially explained by prey having increased trait performance at lower temperatures relative to predators, suggesting a thermal version of the life-dinner principle-stronger selection on running for your life than running for your dinner. For unimodal responses, habitat (marine, freshwater, and terrestrial) largely explains the mean temperature at which trait values are optimal but not variation around the mean. The distribution of activation energies for trait falls has a mean of 1.15 ± 0.39 eV (significantly higher than rises) and is also right-skewed. Our results highlight generalities and deviations in the thermal response of biological traits and help to provide a basis to predict better how biological systems, from cells to communities, respond to temperature change.
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                Author and article information

                Contributors
                emordeca@stanford.edu
                Journal
                Ecol Lett
                Ecol. Lett
                10.1111/(ISSN)1461-0248
                ELE
                Ecology Letters
                John Wiley and Sons Inc. (Hoboken )
                1461-023X
                1461-0248
                08 July 2019
                October 2019
                : 22
                : 10 ( doiID: 10.1111/ele.v22.10 )
                : 1690-1708
                Affiliations
                [ 1 ] Department of Biology Stanford University 371 Serra Mall Stanford CA USA
                [ 2 ] Department of Entomology and Center for Infectious Disease Dynamics Penn State University University Park PA 16802 USA
                [ 3 ] Department of Geography and Emerging Pathogens Institute University of Florida Gainesville FL USA
                [ 4 ] Department of Statistics Virginia Polytechnic and State University 250 Drillfield Drive Blacksburg VA USA
                [ 5 ] Center for Research on Health in Latin America (CISeAL) Pontificia Universidad Católica del Ecuador Quito Ecuador
                [ 6 ] Department of Biological Sciences Eck Institute of Global Health Environmental Change Initiative University of Notre Dame, Notre Dame IN USA
                [ 7 ] School of Life Sciences University of KwaZulu‐Natal Durban South Africa
                [ 8 ] Department of Ecology and Evolutionary Biology and Department of Biomathematics University of California Los Angeles Los Angeles CA 90095 USA
                [ 9 ] Santa Fe Institute 1399 Hyde Park Rd Santa Fe NM 87501 USA
                [ 10 ] Institute for Global Health and Translational Sciences SUNY Upstate Medical University Syracuse NY13210 USA
                Author notes
                [*] [* ] Correspondence: E‐mail: emordeca@ 123456stanford.edu

                Author information
                https://orcid.org/0000-0002-4402-5547
                https://orcid.org/0000-0001-8285-4912
                https://orcid.org/0000-0002-8995-4446
                Article
                ELE13335
                10.1111/ele.13335
                6744319
                31286630
                d73eec4d-f1c0-4a1e-82b3-99ee0db1a2dd
                © 2019 The Authors Ecology Letters published by CNRS and John Wiley & Sons Ltd

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 15 April 2019
                : 22 May 2019
                : 06 June 2019
                Page count
                Figures: 5, Tables: 3, Pages: 19, Words: 16887
                Funding
                Funded by: School of Humanities and Sciences, Stanford University , open-funder-registry 10.13039/100010868;
                Award ID: Terman Fellowship
                Funded by: Division of Environmental Biology , open-funder-registry 10.13039/100000155;
                Award ID: DEB-1518681
                Funded by: Hellman Foundation , open-funder-registry 10.13039/100010336;
                Award ID: Hellman Faculty Fellowship
                Funded by: National Science Foundation , open-funder-registry 10.13039/100000001;
                Award ID: R01AI110793
                Funded by: Stanford Woods Institute for the Environment , open-funder-registry 10.13039/100010869;
                Award ID: Environmental Ventures Program
                Categories
                Review and Synthesis
                Reviews and Syntheses
                Custom metadata
                2.0
                October 2019
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.1 mode:remove_FC converted:13.11.2019

                Ecology
                arbovirus,climate change,dengue virus,malaria,mosquito,ross river virus,temperature,thermal performance curve,west nile virus,zika virus

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