Global, asynchronous partial sweeps at multiple insecticide resistance genes in Aedes mosquitoes

• Published in: Nature communications Vol. 15; no. 1; pp. 6251 - 19
• Main Authors: Schmidt, Thomas L, Endersby-Harshman, Nancy M, van Rooyen, Anthony R J, Katusele, Michelle, Vinit, Rebecca, Robinson, Leanne J, Laman, Moses, Karl, Stephan, Hoffmann, Ary A
• Format: Journal Article
• Language: English
• Published: England Nature Publishing Group 24.07.2024; Nature Publishing Group UK; Nature Portfolio
• Subjects: Aedes - drug effects; Aedes - genetics; Aedes aegypti; Aedes albopictus; Animals; Aquatic insects; Chromosome 2; Chromosome 3; Chromosomes; Copy number; Culicidae; DNA Copy Number Variations; Evolution; Evolutionary genetics; Genes; Genetic diversity; Geographical distribution; Glutathione; Glutathione transferase; Glutathione Transferase - genetics; Glutathione Transferase - metabolism; Insect Proteins - genetics; Insect Proteins - metabolism; Insecticide resistance; Insecticide Resistance - genetics; Insecticides; Insecticides - pharmacology; Invasive species; Mosquito Vectors - drug effects; Mosquito Vectors - genetics; Mosquitoes; Nucleotides; Pesticide resistance; Pests; Phenotypes; Population genetics; Population studies; Populations; Sodium channels (voltage-gated); Vector-borne diseases; Voltage-Gated Sodium Channels - genetics; Yellow fever
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-49792-y

Aedes aegypti (yellow fever mosquito) and Ae. albopictus (Asian tiger mosquito) are globally invasive pests that confer the world's dengue burden. Insecticide-based management has led to the evolution of insecticide resistance in both species, though the genetic architecture and geographical spread of resistance remains incompletely understood. This study investigates partial selective sweeps at resistance genes on two chromosomes and characterises their spread across populations. Sweeps at the voltage-sensitive sodium channel (VSSC) gene on chromosome 3 correspond to one resistance-associated nucleotide substitution in Ae. albopictus and three in Ae. aegypti, including two substitutions at the same nucleotide position (F1534C) that have evolved and spread independently. In Ae. aegypti, we also identify partial sweeps at a second locus on chromosome 2. This locus contains 15 glutathione S-transferase (GST) epsilon class genes with significant copy number variation among populations and where three distinct genetic backgrounds have spread across the Indo-Pacific region, the Americas, and Australia. Local geographical patterns and linkage networks indicate VSSC and GST backgrounds probably spread at different times and interact locally with different genes to produce resistance phenotypes. These findings highlight the rapid global spread of resistance and are evidence for the critical importance of GST genes in resistance evolution.