Exposure to ultraviolet-B radiation increases the susceptibility of mosquitoes to infection with dengue virus
By 2100, greenhouse gases are predicted to reduce ozone and cloud cover over the tropics causing increased exposure of organisms to harmful ultraviolet-B radiation (UVBR). UVBR damages DNA and is an important modulator of immune function and disease susceptibility in humans and other vertebrates. Th...
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Veröffentlicht in: | Global change biology 2023-10, Vol.29 (19), p.5540-5551 |
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creator | Alton, Lesley A Novelo, Mario Beaman, Julian E Arnold, Pieter A Bywater, Candice L Kerton, Emily J Lombardi, Emily J Koh, Cassandra McGraw, Elizabeth A |
description | By 2100, greenhouse gases are predicted to reduce ozone and cloud cover over the tropics causing increased exposure of organisms to harmful ultraviolet-B radiation (UVBR). UVBR damages DNA and is an important modulator of immune function and disease susceptibility in humans and other vertebrates. The effect of UVBR on invertebrate immune function is largely unknown, but UVBR together with ultraviolet-A radiation impairs an insect immune response that utilizes melanin, a pigment that also protects against UVBR-induced DNA damage. If UVBR weakens insect immunity, then it may make insect disease vectors more susceptible to infection with pathogens of socioeconomic and public health importance. In the tropics, where UVBR is predicted to increase, the mosquito-borne dengue virus (DENV), is prevalent and a growing threat to humans. We therefore examined the effect of UVBR on the mosquito Aedes aegypti, the primary vector for DENV, to better understand the potential implications of increased tropical UVBR for mosquito-borne disease risk. We found that exposure to a UVBR dose that caused significant larval mortality approximately doubled the probability that surviving females would become infected with DENV, despite this UVBR dose having no effect on the expression of an effector gene involved in antiviral immunity. We also found that females exposed to a lower UVBR dose were more likely to have low fecundity even though this UVBR dose had no effect on larval size or activity, pupal cuticular melanin content, or adult mass, metabolic rate, or flight capacity. We conclude that future increases in tropical UVBR associated with anthropogenic global change may have the benefit of reducing mosquito-borne disease risk for humans by reducing mosquito fitness, but this benefit may be eroded if it also makes mosquitoes more likely to be infected with deadly pathogens. |
doi_str_mv | 10.1111/gcb.16906 |
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UVBR damages DNA and is an important modulator of immune function and disease susceptibility in humans and other vertebrates. The effect of UVBR on invertebrate immune function is largely unknown, but UVBR together with ultraviolet-A radiation impairs an insect immune response that utilizes melanin, a pigment that also protects against UVBR-induced DNA damage. If UVBR weakens insect immunity, then it may make insect disease vectors more susceptible to infection with pathogens of socioeconomic and public health importance. In the tropics, where UVBR is predicted to increase, the mosquito-borne dengue virus (DENV), is prevalent and a growing threat to humans. We therefore examined the effect of UVBR on the mosquito Aedes aegypti, the primary vector for DENV, to better understand the potential implications of increased tropical UVBR for mosquito-borne disease risk. We found that exposure to a UVBR dose that caused significant larval mortality approximately doubled the probability that surviving females would become infected with DENV, despite this UVBR dose having no effect on the expression of an effector gene involved in antiviral immunity. We also found that females exposed to a lower UVBR dose were more likely to have low fecundity even though this UVBR dose had no effect on larval size or activity, pupal cuticular melanin content, or adult mass, metabolic rate, or flight capacity. We conclude that future increases in tropical UVBR associated with anthropogenic global change may have the benefit of reducing mosquito-borne disease risk for humans by reducing mosquito fitness, but this benefit may be eroded if it also makes mosquitoes more likely to be infected with deadly pathogens.</description><identifier>ISSN: 1354-1013</identifier><identifier>EISSN: 1365-2486</identifier><identifier>DOI: 10.1111/gcb.16906</identifier><identifier>PMID: 37560790</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Anthropogenic changes ; Anthropogenic factors ; Antiviral agents ; Aquatic insects ; Cloud cover ; Culicidae ; Defence mechanisms ; Dengue fever ; Deoxyribonucleic acid ; Disease resistance ; DNA ; DNA damage ; Exposure ; Fecundity ; Females ; Gases ; Gene expression ; Greenhouse effect ; Greenhouse gases ; Health risks ; Human diseases ; Immune response ; Immune system ; Immunity ; Insect immunity ; Insects ; Larvae ; Melanin ; Metabolic rate ; Mosquitoes ; Ozone ; Pathogens ; Probability theory ; Public health ; Radiation ; Radiation damage ; Survival ; Tropical environments ; Ultraviolet radiation ; Vector-borne diseases ; Vectors ; Vertebrates ; Viruses</subject><ispartof>Global change biology, 2023-10, Vol.29 (19), p.5540-5551</ispartof><rights>2023 The Authors. Global Change Biology published by John Wiley & Sons Ltd.</rights><rights>2023. This article is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). 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UVBR damages DNA and is an important modulator of immune function and disease susceptibility in humans and other vertebrates. The effect of UVBR on invertebrate immune function is largely unknown, but UVBR together with ultraviolet-A radiation impairs an insect immune response that utilizes melanin, a pigment that also protects against UVBR-induced DNA damage. If UVBR weakens insect immunity, then it may make insect disease vectors more susceptible to infection with pathogens of socioeconomic and public health importance. In the tropics, where UVBR is predicted to increase, the mosquito-borne dengue virus (DENV), is prevalent and a growing threat to humans. We therefore examined the effect of UVBR on the mosquito Aedes aegypti, the primary vector for DENV, to better understand the potential implications of increased tropical UVBR for mosquito-borne disease risk. We found that exposure to a UVBR dose that caused significant larval mortality approximately doubled the probability that surviving females would become infected with DENV, despite this UVBR dose having no effect on the expression of an effector gene involved in antiviral immunity. We also found that females exposed to a lower UVBR dose were more likely to have low fecundity even though this UVBR dose had no effect on larval size or activity, pupal cuticular melanin content, or adult mass, metabolic rate, or flight capacity. We conclude that future increases in tropical UVBR associated with anthropogenic global change may have the benefit of reducing mosquito-borne disease risk for humans by reducing mosquito fitness, but this benefit may be eroded if it also makes mosquitoes more likely to be infected with deadly pathogens.</description><subject>Anthropogenic changes</subject><subject>Anthropogenic factors</subject><subject>Antiviral agents</subject><subject>Aquatic insects</subject><subject>Cloud cover</subject><subject>Culicidae</subject><subject>Defence mechanisms</subject><subject>Dengue fever</subject><subject>Deoxyribonucleic acid</subject><subject>Disease resistance</subject><subject>DNA</subject><subject>DNA damage</subject><subject>Exposure</subject><subject>Fecundity</subject><subject>Females</subject><subject>Gases</subject><subject>Gene expression</subject><subject>Greenhouse effect</subject><subject>Greenhouse gases</subject><subject>Health risks</subject><subject>Human diseases</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunity</subject><subject>Insect immunity</subject><subject>Insects</subject><subject>Larvae</subject><subject>Melanin</subject><subject>Metabolic rate</subject><subject>Mosquitoes</subject><subject>Ozone</subject><subject>Pathogens</subject><subject>Probability theory</subject><subject>Public health</subject><subject>Radiation</subject><subject>Radiation damage</subject><subject>Survival</subject><subject>Tropical environments</subject><subject>Ultraviolet radiation</subject><subject>Vector-borne diseases</subject><subject>Vectors</subject><subject>Vertebrates</subject><subject>Viruses</subject><issn>1354-1013</issn><issn>1365-2486</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNpd0blOxDAQBmALgbgLXgBZooEiMI4TJykBcUlINFBHjj1ZjJJ48cHx9ngPKLALu_hmNJqfkCMG5yydi5nqzploQGyQXcZFmeVFLTYX_7LIGDC-Q_a8fwMAnoPYJju8KgVUDeyS8eZrbn10SIOlcQhOfhg7YMiuqJPayGDsRM2kHEqPnoZXpD56hfNgOjOY8E1tT0fr36MJdgFs0j2qZd2nCa9U4zSLSD-Mi_6AbPVy8Hi4fvfJy-3N8_V99vh093B9-ZgpXtQhUw1q0EyVTAtd1J0EFHWpABR0DdN9lTMOOi9kJ3MEVKwr0200QN-LvlJ8n5yu-s6dfY_oQzuaNPQwyAlt9G1eF3Vd5FDkiZ78o282uilNl5RgUNUcyqTOVko5673Dvp07M0r33TJoFxm0KYN2mUGyx-uOsRtR_8nfpfMfoVyEBg</recordid><startdate>20231001</startdate><enddate>20231001</enddate><creator>Alton, Lesley A</creator><creator>Novelo, Mario</creator><creator>Beaman, Julian E</creator><creator>Arnold, Pieter A</creator><creator>Bywater, Candice L</creator><creator>Kerton, Emily J</creator><creator>Lombardi, Emily J</creator><creator>Koh, Cassandra</creator><creator>McGraw, Elizabeth A</creator><general>Blackwell Publishing Ltd</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7SN</scope><scope>7UA</scope><scope>C1K</scope><scope>F1W</scope><scope>H97</scope><scope>L.G</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-1618-5308</orcidid><orcidid>https://orcid.org/0000-0001-7973-088X</orcidid><orcidid>https://orcid.org/0000-0002-6158-7752</orcidid><orcidid>https://orcid.org/0000-0002-4236-2494</orcidid></search><sort><creationdate>20231001</creationdate><title>Exposure to ultraviolet-B radiation increases the susceptibility of mosquitoes to infection with dengue virus</title><author>Alton, Lesley A ; 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UVBR damages DNA and is an important modulator of immune function and disease susceptibility in humans and other vertebrates. The effect of UVBR on invertebrate immune function is largely unknown, but UVBR together with ultraviolet-A radiation impairs an insect immune response that utilizes melanin, a pigment that also protects against UVBR-induced DNA damage. If UVBR weakens insect immunity, then it may make insect disease vectors more susceptible to infection with pathogens of socioeconomic and public health importance. In the tropics, where UVBR is predicted to increase, the mosquito-borne dengue virus (DENV), is prevalent and a growing threat to humans. We therefore examined the effect of UVBR on the mosquito Aedes aegypti, the primary vector for DENV, to better understand the potential implications of increased tropical UVBR for mosquito-borne disease risk. We found that exposure to a UVBR dose that caused significant larval mortality approximately doubled the probability that surviving females would become infected with DENV, despite this UVBR dose having no effect on the expression of an effector gene involved in antiviral immunity. We also found that females exposed to a lower UVBR dose were more likely to have low fecundity even though this UVBR dose had no effect on larval size or activity, pupal cuticular melanin content, or adult mass, metabolic rate, or flight capacity. We conclude that future increases in tropical UVBR associated with anthropogenic global change may have the benefit of reducing mosquito-borne disease risk for humans by reducing mosquito fitness, but this benefit may be eroded if it also makes mosquitoes more likely to be infected with deadly pathogens.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>37560790</pmid><doi>10.1111/gcb.16906</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-1618-5308</orcidid><orcidid>https://orcid.org/0000-0001-7973-088X</orcidid><orcidid>https://orcid.org/0000-0002-6158-7752</orcidid><orcidid>https://orcid.org/0000-0002-4236-2494</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Anthropogenic changes Anthropogenic factors Antiviral agents Aquatic insects Cloud cover Culicidae Defence mechanisms Dengue fever Deoxyribonucleic acid Disease resistance DNA DNA damage Exposure Fecundity Females Gases Gene expression Greenhouse effect Greenhouse gases Health risks Human diseases Immune response Immune system Immunity Insect immunity Insects Larvae Melanin Metabolic rate Mosquitoes Ozone Pathogens Probability theory Public health Radiation Radiation damage Survival Tropical environments Ultraviolet radiation Vector-borne diseases Vectors Vertebrates Viruses |
title | Exposure to ultraviolet-B radiation increases the susceptibility of mosquitoes to infection with dengue virus |
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