Heterogeneous genetic invasions of three insecticide resistance mutations in Indo‐Pacific populations of Aedes aegypti (L.)
Nations throughout the Indo‐Pacific region use pyrethroid insecticides to control Aedes aegypti, the mosquito vector of dengue, often without knowledge of pyrethroid resistance status of the pest or origin of resistance. Two mutations (V1016G + F1534C) in the sodium channel gene (Vssc) of Ae. aegypt...
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Veröffentlicht in: | Molecular ecology 2020-05, Vol.29 (9), p.1628-1641 |
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description | Nations throughout the Indo‐Pacific region use pyrethroid insecticides to control Aedes aegypti, the mosquito vector of dengue, often without knowledge of pyrethroid resistance status of the pest or origin of resistance. Two mutations (V1016G + F1534C) in the sodium channel gene (Vssc) of Ae. aegypti modify ion channel function and cause target‐site resistance to pyrethroid insecticides, with a third mutation (S989P) having a potential additive effect. Of 27 possible genotypes involving these mutations, some allelic combinations are never seen whereas others predominate. Here, five allelic combinations common in Ae. aegypti from the Indo‐Pacific region are described and their geographical distributions investigated using genome‐wide SNP markers. We tested the hypothesis that resistance allele combinations evolved de novo in populations versus the alternative that dispersal of Ae. aegypti between populations facilitated genetic invasions of allele combinations. We used latent factor mixed‐models to detect SNPs throughout the genome that showed structuring in line with resistance allele combinations and compared variation at SNPs within the Vssc gene with genome‐wide variation. Mixed‐models detected an array of SNPs linked to resistance allele combinations, all located within or in close proximity to the Vssc gene. Variation at SNPs within the Vssc gene was structured by resistance profile, whereas genome‐wide SNPs were structured by population. These results demonstrate that alleles near to resistance mutations have been transferred between populations via linked selection. This indicates that genetic invasions have contributed to the widespread occurrence of Vssc allele combinations in Ae. aegypti in the Indo‐Pacific region, pointing to undocumented mosquito invasions between countries. |
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Two mutations (V1016G + F1534C) in the sodium channel gene (Vssc) of Ae. aegypti modify ion channel function and cause target‐site resistance to pyrethroid insecticides, with a third mutation (S989P) having a potential additive effect. Of 27 possible genotypes involving these mutations, some allelic combinations are never seen whereas others predominate. Here, five allelic combinations common in Ae. aegypti from the Indo‐Pacific region are described and their geographical distributions investigated using genome‐wide SNP markers. We tested the hypothesis that resistance allele combinations evolved de novo in populations versus the alternative that dispersal of Ae. aegypti between populations facilitated genetic invasions of allele combinations. We used latent factor mixed‐models to detect SNPs throughout the genome that showed structuring in line with resistance allele combinations and compared variation at SNPs within the Vssc gene with genome‐wide variation. Mixed‐models detected an array of SNPs linked to resistance allele combinations, all located within or in close proximity to the Vssc gene. Variation at SNPs within the Vssc gene was structured by resistance profile, whereas genome‐wide SNPs were structured by population. These results demonstrate that alleles near to resistance mutations have been transferred between populations via linked selection. This indicates that genetic invasions have contributed to the widespread occurrence of Vssc allele combinations in Ae. aegypti in the Indo‐Pacific region, pointing to undocumented mosquito invasions between countries.</description><identifier>ISSN: 0962-1083</identifier><identifier>ISSN: 1365-294X</identifier><identifier>EISSN: 1365-294X</identifier><identifier>DOI: 10.1111/mec.15430</identifier><identifier>PMID: 32246542</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Aedes - genetics ; Aedes aegypti ; Alleles ; Animals ; Aquatic insects ; Biological invasions ; Dengue fever ; Dispersal ; genetic invasion ; Genomes ; Genotypes ; Geographical distribution ; Insecticide resistance ; Insecticide Resistance - genetics ; Insecticides ; Insecticides - pharmacology ; Ion channels ; linked selection ; Mosquito Vectors - genetics ; Mosquitoes ; Mutation ; Pesticide resistance ; Polymorphism, Single Nucleotide ; Population genetics ; Populations ; Pyrethrins ; Pyrethroids ; Single-nucleotide polymorphism ; Sodium channels ; Sodium Channels - genetics ; Vector-borne diseases ; voltage sensitive sodium channel</subject><ispartof>Molecular ecology, 2020-05, Vol.29 (9), p.1628-1641</ispartof><rights>2020 John Wiley & Sons Ltd</rights><rights>2020 John Wiley & Sons Ltd.</rights><rights>Copyright © 2020 John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4540-3fb5b97e028e90b76768e118ab621071432a9a144530f0dbd31319cd0fb729db3</citedby><cites>FETCH-LOGICAL-c4540-3fb5b97e028e90b76768e118ab621071432a9a144530f0dbd31319cd0fb729db3</cites><orcidid>0000-0002-9834-4068 ; 0000-0002-0627-0955 ; 0000-0003-4695-075X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fmec.15430$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmec.15430$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27903,27904,45553,45554</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32246542$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Endersby‐Harshman, Nancy M.</creatorcontrib><creatorcontrib>Schmidt, Thomas L.</creatorcontrib><creatorcontrib>Chung, Jessica</creatorcontrib><creatorcontrib>Rooyen, Anthony</creatorcontrib><creatorcontrib>Weeks, Andrew R.</creatorcontrib><creatorcontrib>Hoffmann, Ary A.</creatorcontrib><title>Heterogeneous genetic invasions of three insecticide resistance mutations in Indo‐Pacific populations of Aedes aegypti (L.)</title><title>Molecular ecology</title><addtitle>Mol Ecol</addtitle><description>Nations throughout the Indo‐Pacific region use pyrethroid insecticides to control Aedes aegypti, the mosquito vector of dengue, often without knowledge of pyrethroid resistance status of the pest or origin of resistance. Two mutations (V1016G + F1534C) in the sodium channel gene (Vssc) of Ae. aegypti modify ion channel function and cause target‐site resistance to pyrethroid insecticides, with a third mutation (S989P) having a potential additive effect. Of 27 possible genotypes involving these mutations, some allelic combinations are never seen whereas others predominate. Here, five allelic combinations common in Ae. aegypti from the Indo‐Pacific region are described and their geographical distributions investigated using genome‐wide SNP markers. We tested the hypothesis that resistance allele combinations evolved de novo in populations versus the alternative that dispersal of Ae. aegypti between populations facilitated genetic invasions of allele combinations. We used latent factor mixed‐models to detect SNPs throughout the genome that showed structuring in line with resistance allele combinations and compared variation at SNPs within the Vssc gene with genome‐wide variation. Mixed‐models detected an array of SNPs linked to resistance allele combinations, all located within or in close proximity to the Vssc gene. Variation at SNPs within the Vssc gene was structured by resistance profile, whereas genome‐wide SNPs were structured by population. These results demonstrate that alleles near to resistance mutations have been transferred between populations via linked selection. This indicates that genetic invasions have contributed to the widespread occurrence of Vssc allele combinations in Ae. aegypti in the Indo‐Pacific region, pointing to undocumented mosquito invasions between countries.</description><subject>Aedes - genetics</subject><subject>Aedes aegypti</subject><subject>Alleles</subject><subject>Animals</subject><subject>Aquatic insects</subject><subject>Biological invasions</subject><subject>Dengue fever</subject><subject>Dispersal</subject><subject>genetic invasion</subject><subject>Genomes</subject><subject>Genotypes</subject><subject>Geographical distribution</subject><subject>Insecticide resistance</subject><subject>Insecticide Resistance - genetics</subject><subject>Insecticides</subject><subject>Insecticides - pharmacology</subject><subject>Ion channels</subject><subject>linked selection</subject><subject>Mosquito Vectors - genetics</subject><subject>Mosquitoes</subject><subject>Mutation</subject><subject>Pesticide resistance</subject><subject>Polymorphism, Single Nucleotide</subject><subject>Population genetics</subject><subject>Populations</subject><subject>Pyrethrins</subject><subject>Pyrethroids</subject><subject>Single-nucleotide polymorphism</subject><subject>Sodium channels</subject><subject>Sodium Channels - genetics</subject><subject>Vector-borne diseases</subject><subject>voltage sensitive sodium channel</subject><issn>0962-1083</issn><issn>1365-294X</issn><issn>1365-294X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kc9q3DAQh0VpabZpD3mBIOglOXij_7aOYUmbwJb20EJvQpbHiYJtOZKdsIdAH6HP2CepsrvNIdC5DMx8fMzwQ-iIkiXNddaDW1IpOHmFFpQrWTAtfr5GC6IVKyip-AF6l9ItIZQzKd-iA86YUFKwBXq8hAliuIYBwpzwU5-8w364t8mHIeHQ4ukmAuRRApd3vgEcIfk02cEB7ufJTlvSD_hqaMKfX7-_WefbbBnDOHf7bfacQwMJW7jejJPHJ-vl6Xv0prVdgg_7foh-fLr4vros1l8_X63O14UTUpCCt7WsdQmEVaBJXapSVUBpZWvFKCmp4MxqS4WQnLSkqRtOOdWuIW1dMt3U_BCd7LxjDHczpMn0PjnoOrt92zBeKVYJpWVGP75Ab8Mch3ydYYJorThhZaZOd5SLIaUIrRmj723cGErMUyYmZ2K2mWT2eG-c6x6aZ_JfCBk42wEPvoPN_03my8Vqp_wLFoqWjg</recordid><startdate>202005</startdate><enddate>202005</enddate><creator>Endersby‐Harshman, Nancy M.</creator><creator>Schmidt, Thomas L.</creator><creator>Chung, Jessica</creator><creator>Rooyen, Anthony</creator><creator>Weeks, Andrew R.</creator><creator>Hoffmann, Ary A.</creator><general>Blackwell Publishing Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-9834-4068</orcidid><orcidid>https://orcid.org/0000-0002-0627-0955</orcidid><orcidid>https://orcid.org/0000-0003-4695-075X</orcidid></search><sort><creationdate>202005</creationdate><title>Heterogeneous genetic invasions of three insecticide resistance mutations in Indo‐Pacific populations of Aedes aegypti (L.)</title><author>Endersby‐Harshman, Nancy M. ; Schmidt, Thomas L. ; Chung, Jessica ; Rooyen, Anthony ; Weeks, Andrew R. ; Hoffmann, Ary A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4540-3fb5b97e028e90b76768e118ab621071432a9a144530f0dbd31319cd0fb729db3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Aedes - genetics</topic><topic>Aedes aegypti</topic><topic>Alleles</topic><topic>Animals</topic><topic>Aquatic insects</topic><topic>Biological invasions</topic><topic>Dengue fever</topic><topic>Dispersal</topic><topic>genetic invasion</topic><topic>Genomes</topic><topic>Genotypes</topic><topic>Geographical distribution</topic><topic>Insecticide resistance</topic><topic>Insecticide Resistance - genetics</topic><topic>Insecticides</topic><topic>Insecticides - pharmacology</topic><topic>Ion channels</topic><topic>linked selection</topic><topic>Mosquito Vectors - genetics</topic><topic>Mosquitoes</topic><topic>Mutation</topic><topic>Pesticide resistance</topic><topic>Polymorphism, Single Nucleotide</topic><topic>Population genetics</topic><topic>Populations</topic><topic>Pyrethrins</topic><topic>Pyrethroids</topic><topic>Single-nucleotide polymorphism</topic><topic>Sodium channels</topic><topic>Sodium Channels - genetics</topic><topic>Vector-borne diseases</topic><topic>voltage sensitive sodium channel</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Endersby‐Harshman, Nancy M.</creatorcontrib><creatorcontrib>Schmidt, Thomas L.</creatorcontrib><creatorcontrib>Chung, Jessica</creatorcontrib><creatorcontrib>Rooyen, Anthony</creatorcontrib><creatorcontrib>Weeks, Andrew R.</creatorcontrib><creatorcontrib>Hoffmann, Ary A.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Endersby‐Harshman, Nancy M.</au><au>Schmidt, Thomas L.</au><au>Chung, Jessica</au><au>Rooyen, Anthony</au><au>Weeks, Andrew R.</au><au>Hoffmann, Ary A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Heterogeneous genetic invasions of three insecticide resistance mutations in Indo‐Pacific populations of Aedes aegypti (L.)</atitle><jtitle>Molecular ecology</jtitle><addtitle>Mol Ecol</addtitle><date>2020-05</date><risdate>2020</risdate><volume>29</volume><issue>9</issue><spage>1628</spage><epage>1641</epage><pages>1628-1641</pages><issn>0962-1083</issn><issn>1365-294X</issn><eissn>1365-294X</eissn><abstract>Nations throughout the Indo‐Pacific region use pyrethroid insecticides to control Aedes aegypti, the mosquito vector of dengue, often without knowledge of pyrethroid resistance status of the pest or origin of resistance. Two mutations (V1016G + F1534C) in the sodium channel gene (Vssc) of Ae. aegypti modify ion channel function and cause target‐site resistance to pyrethroid insecticides, with a third mutation (S989P) having a potential additive effect. Of 27 possible genotypes involving these mutations, some allelic combinations are never seen whereas others predominate. Here, five allelic combinations common in Ae. aegypti from the Indo‐Pacific region are described and their geographical distributions investigated using genome‐wide SNP markers. We tested the hypothesis that resistance allele combinations evolved de novo in populations versus the alternative that dispersal of Ae. aegypti between populations facilitated genetic invasions of allele combinations. We used latent factor mixed‐models to detect SNPs throughout the genome that showed structuring in line with resistance allele combinations and compared variation at SNPs within the Vssc gene with genome‐wide variation. Mixed‐models detected an array of SNPs linked to resistance allele combinations, all located within or in close proximity to the Vssc gene. Variation at SNPs within the Vssc gene was structured by resistance profile, whereas genome‐wide SNPs were structured by population. These results demonstrate that alleles near to resistance mutations have been transferred between populations via linked selection. This indicates that genetic invasions have contributed to the widespread occurrence of Vssc allele combinations in Ae. aegypti in the Indo‐Pacific region, pointing to undocumented mosquito invasions between countries.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>32246542</pmid><doi>10.1111/mec.15430</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-9834-4068</orcidid><orcidid>https://orcid.org/0000-0002-0627-0955</orcidid><orcidid>https://orcid.org/0000-0003-4695-075X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Aedes - genetics Aedes aegypti Alleles Animals Aquatic insects Biological invasions Dengue fever Dispersal genetic invasion Genomes Genotypes Geographical distribution Insecticide resistance Insecticide Resistance - genetics Insecticides Insecticides - pharmacology Ion channels linked selection Mosquito Vectors - genetics Mosquitoes Mutation Pesticide resistance Polymorphism, Single Nucleotide Population genetics Populations Pyrethrins Pyrethroids Single-nucleotide polymorphism Sodium channels Sodium Channels - genetics Vector-borne diseases voltage sensitive sodium channel |
title | Heterogeneous genetic invasions of three insecticide resistance mutations in Indo‐Pacific populations of Aedes aegypti (L.) |
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