Deltamethrin Resistance Mechanisms in Aedes aegypti Populations from Three French Overseas Territories Worldwide

Abstract

Background

Aedes aegypti is a cosmopolite mosquito, vector of arboviruses. The worldwide studies of its insecticide resistance have demonstrated a strong loss of susceptibility to pyrethroids, the major class of insecticide used for vector control. French overseas territories such as French Guiana (South America), Guadeloupe islands (Lesser Antilles) as well as New Caledonia (Pacific Ocean), have encountered such resistance.

Methodology/Principal Findings

We initiated a research program on the pyrethroid resistance in French Guiana, Guadeloupe and New Caledonia. Aedes aegypti populations were tested for their deltamethrin resistance level then screened by an improved microarray developed to specifically study metabolic resistance mechanisms. Cytochrome P450 genes were implicated in conferring resistance. CYP6BB2, CYP6M11, CYP6N12, CYP9J9, CYP9J10 and CCE3 genes were upregulated in the resistant populations and were common to other populations at a regional scale. The implication of these genes in resistance phenomenon is therefore strongly suggested. Other genes from detoxification pathways were also differentially regulated. Screening for target site mutations on the voltage-gated sodium channel gene demonstrated the presence of I1016 and C1534.

Conclusion /significance

This study highlighted the presence of a common set of differentially up-regulated detoxifying genes, mainly cytochrome P450 genes in all three populations. GUA and GUY populations shared a higher number of those genes compared to CAL. Two kdr mutations well known to be associated to pyrethroid resistance were also detected in those two populations but not in CAL. Different selective pressures and genetic backgrounds can explain such differences. These results are also compared with those obtained from other parts of the world and are discussed in the context of integrative research on vector competence.

Author Summary

Aedes aegypti is vector of Dengue, Chikungunya and Zika viruses, all causing emerging or re-emerging diseases worldwide. Fighting these diseases relies on the control of the vector. Therefore, insecticides have been extensively used worldwide, resulting in the development of insecticide resistance. In the French overseas territories, resistance to pyrethroids has been monitored for many years with high levels in the South American French territories. We then investigated the mechanisms underlying this resistance in populations from French Guiana, Guadeloupe and New Caledonia. Transcription levels of detoxification genes were measured and alongside screening for target site mutations. Upregulation of cytochrome P450 genes and carboxylesterases were observed in all three populations. Mutations related to pyrethroid resistance in position 1016 and 1534 of the voltage-gated sodium channel gene were also observed. French Guiana and Guadeloupe populations presented a closer profile of resistance mechanisms whereas the New Caledonia population had a more restricted profile. Such differences can be explained by different vector control practices, regional insecticide uses and genetic backgrounds. These results are also compared with others obtained from other parts of the world and are discussed with the perspective of integrative research on vector competence.