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The spread of resistance to imidacloprid is restricted by thermotolerance in natural populations of Drosophila melanogaster

Abstract

Imidacloprid, the world’s most used insecticide, has caused considerable controversy due to harmful effects on non-pest species and increasing evidence showing that insecticides have become the primary selective force in many insect species. The genetic response to insecticides is heterogeneous across populations and environments, leading to more complex patterns of genetic variation than previously thought. This motivated the investigation of imidacloprid resistance at different temperatures in natural populations of Drosophila melanogaster originating from four climate extremes replicated across two continents. Population and quantitative genomic analysis, supported by functional tests, have revealed a mixed genetic architecture to resistance involving major genes (Paramyosin and Nicotinic-Acetylcholine Receptor Alpha 3) and polygenes with a major trade-off with thermotolerance. Reduced genetic differentiation at resistance-associated loci indicated enhanced gene flow at these loci. Resistance alleles showed stronger evidence of positive selection in temperate populations compared to tropical populations in which chromosomal inversions In(2L)t, In(3R)Mo and In(3R)Payne harbour susceptibility alleles. Polygenic architecture and ecological factors should be considered when developing sustainable management strategies for both pest and beneficial insects.

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Fig. 1: Sampling locations and effects of imidacloprid resistance and thermotolerance on longevity.
Fig. 2: Genome-wide association for imidacloprid resistance.
Fig. 3: Functional tests for the effect of Prm and nAChRα3.
Fig. 4: Genomic location of candidate genes and genome-wide pattern of diversity and selection.

Data availability

Aligned sequence data generated in this study are deposited on NCBI under the BioProject ID PRJNA515537 (https://www.ncbi.nlm.nih.gov/bioproject/515537). All custom codes are deposited on GitHub (https://github.com/aflevel/IMIresist_vs_TEMPtol) and the derived data are deposited on figshare (https://doi.org/10.26188/5b592f305226b).

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Acknowledgements

We thank D. Begun, S. Myles and C. Hart for sharing their laboratory facilities, P. Griffin for fly collection, and K. Charles at Foursights Wines, D. Herbert at Herbert Vineyard, P. Dixon at the Henty Estate, J. Leahy at Becker’s Vineyard, J. Seago at Ponchartrain Vineyard and Landry Vineyards for providing access to their estates. This work was supported by the Human Frontier in Sciences Long-Term fellowship no. LT000907/2012-L awarded to A.F.L.

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A.F.-L. and C.R. designed the study and wrote the manuscript with contributions from T.P. and A.A.H. A.F.-L., R.T.G. and S.W. performed the experiments. A.F.-L. analysed the data with contributions from A.A.H., R.V.R. and P. Battlay. A.A.H., P. Battlay and T.P. revised the manuscript. A.A.H., M.S., P. Batterham, T.P. and W.C. provided new genetic material.

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Correspondence to Alexandre Fournier-Level or Charles Robin.

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Supplementary Information

Supplementary Figures 1–5, Supplementary Tables 1–5 and 7–9

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Supplementary Table 6

List of candidate genes for imidacloprid resistance. Candidate genes were identified on the basis of the excess of significantly associated polymorphism within 2.5 kbp of a gene coding sequence in at least two GWAS or present in 300-bp segments with significant copy-number association.

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Fournier-Level, A., Good, R.T., Wilcox, S.A. et al. The spread of resistance to imidacloprid is restricted by thermotolerance in natural populations of Drosophila melanogaster. Nat Ecol Evol 3, 647–656 (2019). https://doi.org/10.1038/s41559-019-0837-y

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