Multiplexed amplicon sequencing reveals the heterogeneous spatial distribution of pyrethroid resistance mutations in Aedes albopictus mosquito populations in southern France
Abstract Background The risk of mosquito-borne disease transmission is increasing in temperate climates with the colonization and proliferation of the Asian tiger mosquito vector Aedes albopictus and the rapid mass transport of passengers returning from tropical regions where viruses are endemic. Th...
Saved in:
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2024-12-01
|
| Series: | Parasites & Vectors |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13071-024-06632-8 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1846101413352964096 |
|---|---|
| author | Albin Fontaine Antoine Mignotte Guillaume Lacour Agnès Nguyen Nicolas Gomez Lionel Chanaud Grégory L’Ambert Sébastien Briolant |
| author_facet | Albin Fontaine Antoine Mignotte Guillaume Lacour Agnès Nguyen Nicolas Gomez Lionel Chanaud Grégory L’Ambert Sébastien Briolant |
| author_sort | Albin Fontaine |
| collection | DOAJ |
| description | Abstract Background The risk of mosquito-borne disease transmission is increasing in temperate climates with the colonization and proliferation of the Asian tiger mosquito vector Aedes albopictus and the rapid mass transport of passengers returning from tropical regions where viruses are endemic. The prevention of major Aedes-borne viruses heavily relies on the use of insecticides for vector control, mainly pyrethroids. In Europe, only deltamethrin is authorized. Methods High-throughput molecular assays can provide a cost-effective surrogate to phenotypic insecticide resistance assays when mutations have been previously linked to a resistance phenotype. Here, we screened for the spatial distribution of knockdown resistance (kdr) mutations at a large scale using a two-step approach based on multiplexed amplicon sequencing and an unprecedented collection of field-derived mosquitoes from 95 sites in 61 municipalities, alongside a west-to-east transect in the south of France, from June to September 2021. Results We identified the presence of the V1016G allele in 14 sites. The V1016G allele was predominantly found in southeast France close to the Italian border, with two additional isolated sites close to Bordeaux and Marmande. All mosquitoes were heterozygous for this mutation and should not be phenotypically resistant to pyrethroid insecticide. Four other mutations were identified in our targeted genomic sequence: I1532T, M1006L, M1586L, M995L. Sequencing a section of maternally inherited mitochondrial genome confirmed that the spread of Ae. albopictus in France originated from founders within haplogroup A1. Conclusions These findings contribute to the broader understanding of resistance dynamics in Europe and can inform targeted approaches to mitigate the impact of resistance on vector control. |
| format | Article |
| id | doaj-art-73b1e2e20805462a9b1e8148d36ea30d |
| institution | Kabale University |
| issn | 1756-3305 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | BMC |
| record_format | Article |
| series | Parasites & Vectors |
| spelling | doaj-art-73b1e2e20805462a9b1e8148d36ea30d2024-12-29T12:11:55ZengBMCParasites & Vectors1756-33052024-12-0117111010.1186/s13071-024-06632-8Multiplexed amplicon sequencing reveals the heterogeneous spatial distribution of pyrethroid resistance mutations in Aedes albopictus mosquito populations in southern FranceAlbin Fontaine0Antoine Mignotte1Guillaume Lacour2Agnès Nguyen3Nicolas Gomez4Lionel Chanaud5Grégory L’Ambert6Sébastien Briolant7Unité des Virus Émergents (UVE: Aix-Marseille Univ, Università di Corsica, IRD 190, Inserm 1207, IRBA)AltopictusAltopictusMicrosynth FranceInstitut de Recherche Biomédicale des Armées (IRBA), Unité de Parasitologie et EntomologieEntente Interdépartementale pour la Démoustication du Littoral Méditerranéen (EID Méditerranée)Entente Interdépartementale pour la Démoustication du Littoral Méditerranéen (EID Méditerranée)Institut de Recherche Biomédicale des Armées (IRBA), Unité de Parasitologie et EntomologieAbstract Background The risk of mosquito-borne disease transmission is increasing in temperate climates with the colonization and proliferation of the Asian tiger mosquito vector Aedes albopictus and the rapid mass transport of passengers returning from tropical regions where viruses are endemic. The prevention of major Aedes-borne viruses heavily relies on the use of insecticides for vector control, mainly pyrethroids. In Europe, only deltamethrin is authorized. Methods High-throughput molecular assays can provide a cost-effective surrogate to phenotypic insecticide resistance assays when mutations have been previously linked to a resistance phenotype. Here, we screened for the spatial distribution of knockdown resistance (kdr) mutations at a large scale using a two-step approach based on multiplexed amplicon sequencing and an unprecedented collection of field-derived mosquitoes from 95 sites in 61 municipalities, alongside a west-to-east transect in the south of France, from June to September 2021. Results We identified the presence of the V1016G allele in 14 sites. The V1016G allele was predominantly found in southeast France close to the Italian border, with two additional isolated sites close to Bordeaux and Marmande. All mosquitoes were heterozygous for this mutation and should not be phenotypically resistant to pyrethroid insecticide. Four other mutations were identified in our targeted genomic sequence: I1532T, M1006L, M1586L, M995L. Sequencing a section of maternally inherited mitochondrial genome confirmed that the spread of Ae. albopictus in France originated from founders within haplogroup A1. Conclusions These findings contribute to the broader understanding of resistance dynamics in Europe and can inform targeted approaches to mitigate the impact of resistance on vector control.https://doi.org/10.1186/s13071-024-06632-8Knock-down resistancePyrethroid resistanceMolecular surveillanceAmplicon sequencingPool DNA-sequencingAedes albopictus |
| spellingShingle | Albin Fontaine Antoine Mignotte Guillaume Lacour Agnès Nguyen Nicolas Gomez Lionel Chanaud Grégory L’Ambert Sébastien Briolant Multiplexed amplicon sequencing reveals the heterogeneous spatial distribution of pyrethroid resistance mutations in Aedes albopictus mosquito populations in southern France Parasites & Vectors Knock-down resistance Pyrethroid resistance Molecular surveillance Amplicon sequencing Pool DNA-sequencing Aedes albopictus |
| title | Multiplexed amplicon sequencing reveals the heterogeneous spatial distribution of pyrethroid resistance mutations in Aedes albopictus mosquito populations in southern France |
| title_full | Multiplexed amplicon sequencing reveals the heterogeneous spatial distribution of pyrethroid resistance mutations in Aedes albopictus mosquito populations in southern France |
| title_fullStr | Multiplexed amplicon sequencing reveals the heterogeneous spatial distribution of pyrethroid resistance mutations in Aedes albopictus mosquito populations in southern France |
| title_full_unstemmed | Multiplexed amplicon sequencing reveals the heterogeneous spatial distribution of pyrethroid resistance mutations in Aedes albopictus mosquito populations in southern France |
| title_short | Multiplexed amplicon sequencing reveals the heterogeneous spatial distribution of pyrethroid resistance mutations in Aedes albopictus mosquito populations in southern France |
| title_sort | multiplexed amplicon sequencing reveals the heterogeneous spatial distribution of pyrethroid resistance mutations in aedes albopictus mosquito populations in southern france |
| topic | Knock-down resistance Pyrethroid resistance Molecular surveillance Amplicon sequencing Pool DNA-sequencing Aedes albopictus |
| url | https://doi.org/10.1186/s13071-024-06632-8 |
| work_keys_str_mv | AT albinfontaine multiplexedampliconsequencingrevealstheheterogeneousspatialdistributionofpyrethroidresistancemutationsinaedesalbopictusmosquitopopulationsinsouthernfrance AT antoinemignotte multiplexedampliconsequencingrevealstheheterogeneousspatialdistributionofpyrethroidresistancemutationsinaedesalbopictusmosquitopopulationsinsouthernfrance AT guillaumelacour multiplexedampliconsequencingrevealstheheterogeneousspatialdistributionofpyrethroidresistancemutationsinaedesalbopictusmosquitopopulationsinsouthernfrance AT agnesnguyen multiplexedampliconsequencingrevealstheheterogeneousspatialdistributionofpyrethroidresistancemutationsinaedesalbopictusmosquitopopulationsinsouthernfrance AT nicolasgomez multiplexedampliconsequencingrevealstheheterogeneousspatialdistributionofpyrethroidresistancemutationsinaedesalbopictusmosquitopopulationsinsouthernfrance AT lionelchanaud multiplexedampliconsequencingrevealstheheterogeneousspatialdistributionofpyrethroidresistancemutationsinaedesalbopictusmosquitopopulationsinsouthernfrance AT gregorylambert multiplexedampliconsequencingrevealstheheterogeneousspatialdistributionofpyrethroidresistancemutationsinaedesalbopictusmosquitopopulationsinsouthernfrance AT sebastienbriolant multiplexedampliconsequencingrevealstheheterogeneousspatialdistributionofpyrethroidresistancemutationsinaedesalbopictusmosquitopopulationsinsouthernfrance |