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Cattel, J.

Publications and source records attributed to Cattel, J..

4 recordsLinked to original sources

Development of the Incompatible Insect Technique targeting Aedes albopictus: introgression of a wild nuclear background restores the performance of males artificially infected with Wolbachia

The bacterium Wolbachia pipientis is increasingly studied for its potential use in controlling insect vectors or pests due to its ability to induce Cytoplasmic Incompatibility (CI). CI can be exploited by establishing an opportunistic Wolbachia infection in a targeted insect species through trans-infection and then releasing the infected males into the environment as sterilizing agents. Several host life history traits (LHT) have been reported to be negatively affected by artificial Wolbachia infection. Wolbachia is often considered as the causative agent of these detrimental effects, and the importance of the hosts genetic origins in the outcome of trans-infection is generally overlooked. In this study, we investigated the impact of host genetic background using an Aedes albopictus line recently trans-infected with wPip from Culex pipiens mosquito, which exhibited some fitness costs. We measured several LHTs including fecundity, egg hatch rate and male mating competitiveness in the incompatible line after four rounds of introgression aiming at restoring genetic diversity in the nuclear genome. Our results show that introgression with a wild genetic background restored most fitness traits and conferred mating competitiveness comparable to that of wild males. Finally, we show that introgression leads to faster and stronger population suppression under laboratory conditions. Overall, our data support that host genome plays a decisive role in determining the fitness of Wolbachia infected incompatible males. ImportanceThe bacterium Wolbachia pipientis is increasingly used to control insect vectors and pests through the Incompatible Insect Technique (IIT) inducing a form of conditional sterility when a Wolbachia-infected male mates with an uninfected or differently infected female. Wolbachia artificial trans-infection has been repeatedly reported to affect mosquitoes LHTs, which may in turn compromise the efficiency of IIT. Using a tiger mosquito (Aedes albopictus) line recently trans-infected with a Wolbachia strain from Culex pipiens and displaying reduced fitness, we show that restoring genetic diversity through introgression significantly mitigated the fitness costs associated with Wolbachia trans-infection. This was further demonstrated through experimental population suppression, showing that introgression is required to achieve mosquito population suppression under laboratory conditions. These findings are significant for the implementation of IIT programs, as an increase in female fecundity and male performance improves mass rearing productivity as well as the sterilizing capacity of released males.

bioengineering↗

A genomic duplication spanning multiple P450s contributes to insecticide resistance in the dengue mosquito Aedes aegypti

Resistance of mosquitoes to insecticides is one example of rapid adaptation to anthropogenic selection pressures having a strong impact on human health and activities. Target-site modification and increased insecticide detoxification are the two main mechanisms underlying insecticide resistance in mosquitoes. While target-sites mutations are well characterised and often used to track resistance in the field, the genomic events associated with insecticide detoxification remain partially characterised. Recent studies evidenced the key role of gene duplications in the over-expression of detoxification enzymes and their potential use to track metabolic resistance alleles in the field. However, such genomic events remain difficult to characterise due to their complex genomic architecture and their co-occurrence with other resistance alleles. In this concern, the present work investigated the role of a large genomic duplication affecting a cluster of detoxification enzymes in conferring resistance to the pyrethroid insecticide deltamethrin in the mosquito Aedes aegypti. Two isofemale lines originating from French Guiana and being deprived from major target-site mutations showed distinct insecticide resistance levels. Combining RNA-seq and whole genome pool-seq identified a 220 Kb genomic duplication enhancing the expression of multiple contiguous cytochrome P450s in the resistant line. The genomic architecture of the duplicated loci was elucidated through long read sequencing, evidencing its transposon-mediated evolutionary origin. The involvement of this P450 duplication in deltamethrin survival was supported by a significant phenotypic response to the P450 inhibitor piperonyl butoxide together with genotype-phenotype association and RNA interference. Experimental evolution suggested that this P450 duplication is associated with a significant fitness cost, potentially affecting its adaptive value in presence of other resistance alleles. Overall, this study supports the importance of genomic duplications affecting detoxification enzymes in the rapid adaptation of mosquitoes to insecticides. Deciphering their genomic architecture provides new insights into the evolutionary processes underlying such rapid adaptation. Such findings provide new tools for the surveillance and management of resistance in the field.

evolutionary biology↗

A novel assay for tracking carboxylesterase gene amplifications conferring organophosphate resistance in the mosquito Aedes aegypti: from experimental evolution to field application

By altering gene expression and creating paralogs, genomic amplifications represent a key component of short-term adaptive processes. In insects, the use of insecticides can select gene amplifications causing an increased expression of detoxification enzymes, supporting the usefulness of these DNA markers for monitoring the dynamics of resistance alleles in the field. In this context, the present study aims to characterise a genomic amplification event associated with resistance to organophosphate insecticides in the mosquito Aedes aegypti and to develop a molecular assay to monitor the associated resistance alleles in the field. An experimental evolution experiment using a composite population from Laos supported the association between the over-transcription of multiple contiguous carboxylesterase genes on chromosome 2 and resistance to multiple organophosphate insecticides. Combining whole genome sequencing and qPCR on specific genes confirmed the presence of a ~100 Kb amplification spanning at least five carboxylesterase genes at this locus with the co-existence of multiple structural duplication haplotypes. Field data confirmed their circulation in South-East Asia and revealed high copy number polymorphism among and within populations suggesting a trade-off between this resistance mechanism and associated fitness costs. A dual-colour multiplex TaqMan assay allowing the rapid detection and copy number quantification of this amplification event in Ae. aegypti was developed and validated on field populations. The routine use of this novel assay will improve the tracking of resistance alleles in this major arbovirus vector.

evolutionary biology↗

Combining genetic crosses and pool targeted DNA-seq for untangling genomic variations associated with resistance to multiple insecticides in the dengue vector Aedes aegypti

In addition to combating vector-borne diseases, studying the adaptation of mosquitoes to insecticides provides a remarkable example of evolution-in-action driving the selection of complex phenotypes. Indeed, most resistant mosquito populations show multi-resistance phenotypes as a consequence of the variety of insecticides employed and of the complexity of selected resistance mechanisms. Such complexity makes challenging the identification of alleles conferring resistance to specific insecticides and prevents the development of molecular assays to track them in the field. Here we showed that combining simple genetic crosses with pool targeted DNA-seq can enhance the specificity of resistance alleles detection while maintaining experimental work and sequencing effort at reasonable levels. A multi-resistant population of the mosquito Aedes aegypti was exposed to three distinct insecticides (deltamethrin, bendiocarb and fenitrothion) and survivors to each insecticide were crossed with a susceptible strain to generate 3 distinct lines. F2 individuals from each line were then segregated with 2 insecticide doses. Bioassays supported the improved segregation of resistance alleles between lines. Hundreds of genes covering all detoxifying enzymes and insecticide targets together with more than 7,000 intergenic regions equally spread over mosquito genome were sequenced from pools of F0 and F2 individuals unexposed or surviving insecticide. Differential coverage analysis identified 39 detoxification enzymes showing an increased gene copy number in association with resistance. Combining an allele frequency filtering approach with a Bayesian FST-based genome scan identified multiple genomic regions showing strong selection signatures together with 50 non-synonymous variations associated with resistance. This study provides a simple and cost-effective approach to improve the segregation of resistant alleles in multi-resistant populations while reducing false positives frequently arising when comparing populations showing divergent genetic backgrounds. The identification of these insecticide resistance markers paves the way for the design of novel DNA-based resistance tracking assays.\n\nAuthor summaryIn addition to combating vector-borne diseases, understanding how mosquitoes adapt to insecticides provides a remarkable example of evolution-in-action. However, the variety of insecticides used and the complexity of adaptive mechanisms make it difficult to identify the genetic changes conferring resistance to each insecticide. Here we combined simple controlled crosses with mass DNA sequencing for enhancing the specificity of resistance gene detection. A multi-resistant mosquito population was exposed to three distinct insecticides and survivors were crossed with a susceptible strain to generate 3 distinct mosquito lines. Individuals from the second generation of each line were then segregated based on their resistance to each insecticide. Bioassays supported the improved segregation of genetic resistance markers between lines. Hundreds of genes potentially involved in resistance together with thousands non-genic regions equally spread over mosquito genome were sequenced from individuals from each line. Genomic analyses identified detoxification enzymes showing an increased gene copy number in association with resistance and multiple genomic regions showing strong selection signatures and carrying point mutations associated with resistance. Such approach improves the specificity of resistance gene detection in field mosquito populations resisting to multiple insecticides and paves the way for the design of novel DNA-based resistance tracking tools.

genomics↗