Insecticide resistance and genetic structure of Aedes aegypti populations from Rio de Janeiro State, Brazil

Author summary Monitoring of insecticide resistance (IR) is mandatory for the effectiveness of vector control programs. We investigate six populations of Aedes aegypti regarding their IR status towards insecticides previously or currently in use, their frequency of IR alleles and resistance ratio, their genetic ancestry and structure, and the gene flow. We observed that Ae. aegypti populations from RJ are becoming susceptible to the larvicide organophosphate temephos. The resistance ratios of temephos are lower among populations where gene flow might be occurring. All RJ populations are highly resistant to deltamethrin, partially explained by the high frequency of kdr alleles. Besides, all populations are susceptible to pyriproxyfen's insect growth regulator and the organophosphate malathion. Population genomic analyses using more than 15,000 SNPs identified three potential genetic clusters within RJ populations, with higher gene flow to and out of the touristic region called Regiao dos Lagos. IR data, together with knowledge of the genetic structure and gene flow among different mosquito populations, can help with vector control program decisions. Vector control largely relies on neurotoxic chemicals, and insecticide resistance (IR) directly threatens their effectiveness. In some cases, specific alleles cause IR, and knowledge of the genetic diversity and gene flow among mosquito populations is crucial to track their arrival, rise, and spread. Here we evaluated Aedes aegypti populations' susceptibility status, collected in 2016 from six different municipalities of Rio de Janeiro state (RJ), to temephos, pyriproxyfen, malathion, and deltamethrin. We collected eggs of Ae. aegypti in Campos dos Goytacazes (Cgy), Itaperuna (Ipn), Iguaba Grande (Igg), Itaborai (Ibr), Mangaratiba (Mgr), and Vassouras (Vsr). We followed the World Health Organization (WHO) guidelines and investigated the degree of susceptibility/resistance of mosquitoes to these insecticides. We used the Rockefeller strain as a susceptible positive control. We genotyped the V1016I and F1534C knockdown resistance (kdr) alleles using qPCR TaqMan SNP genotyping assay. Besides, with the use of Ae. aegypti SNP-chip, we performed genomic population analyses by genotyping more than 15,000 biallelic SNPs in mosquitoes from each population. We added previous data from populations from other countries to evaluate the ancestry of RJ populations. All RJ Ae. aegypti populations were susceptible to pyriproxyfen and malathion and highly resistant to deltamethrin. The resistance ratios for temephos was below 3,0 in Cgy, Ibr, and Igg populations, representing the lowest rates since IR monitoring started in this Brazilian region. We found the kdr alleles in high frequencies in all populations, partially justifying the observed resistance to pyrethroid. Population genetics analysis showed that Ae. aegypti revealed potential higher migration among some RJ localities and low genetic structure for most of them. Future population genetic studies, together with IR data in Ae aegypti on a broader scale, can help us predict the gene flow within and among the Brazilian States, allowing us to track the dynamics of arrival and changes in the frequency of IR alleles, providing critical information to improving vector control program.

Automated summary

Research found that Aedes aegypti populations in RJ are becoming more susceptible to larvicide temephos, with lower resistance ratios in populations where gene flow might be occurring. Additionally, populations were susceptible to pyriproxyfen and malathion, highly resistant to deltamethrin, and partially explained by high frequencies of kdr alleles. Population genetic analysis identified potential genetic clusters within RJ populations and higher gene flow in a touristic region. The study highlights the importance of monitoring insecticide resistance and genetic diversity for effective vector control programs.