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

Abstract

Imidacloprid, the world's most utilised insecticide 1 , has raised considerable controversy due to its harmful effects on non-pest species 2-6 and there is increasing evidence showing that insecticides have become the primary selective force in many insect species [7][8][9][10][11][12][13][14] . The genetic response to insecticides is heterogeneous across population and environment [15][16][17] , 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, demonstrated a polygenic basis to resistance and a major trade-off with thermotolerance. Reduced genetic differentiation at resistance-associated loci indicate enhanced gene flow at these loci. Resistance alleles showed stronger evidence of positive selection in temperate populations compared to tropical populations. Polygenic architecture and ecological factors should be considered when developing sustainable management strategies for both pest and beneficial insects. 1

Climate change and the genetics of insecticide resistance

“…The tradeoffs between alleles that confer thermotolerance and alleles that confer insecticide resistance may therefore restrict the frequency of insecticide resistance alleles in warmer areas. Taken together, these data suggest that temperature increase from climate change may restrict the spread of imidacloprid resistance in natural populations of D. melanogaster due to tradeoffs with thermotolerance . One of the important messages of this study is that tradeoffs between insecticide resistance and thermotolerance might not occur in a single gene or locus but could result from tradeoffs between different alleles of linked genes.…”

“…In other cases, these tradeoffs or facilitations may not be the consequences of changes in a single locus. The comprehensive study of D. melanogaster from four different locations showed that reduced recombination due to chromosomal inversions may lead to linked genes or alleles which are inherited together . Such chromosomal blocks may contain alleles of genes that have opposite effects with regard to thermotolerance and insecticide resistance, leading to tradeoffs under the dual selection pressures of temperature and insecticide.…”

“…A recent study undertook a comprehensive population and quantitative genomics study of multiple field populations of D. melanogaster to investigate the complex genetic architecture of the tradeoff between insecticide resistance and temperature. Using D. melanogaster collected from four climatic extremes from Australia and North America, the authors performed a genome‐wide association study focusing on Single nucleotide polymorphisms (SNPs) and transposable elements with resistance to imidacloprid, a widely used insecticide . Two major loci were identified: the Nicotinic‐Acetylcholine Receptor Alpha 3 ( nAChRα3 ) gene, which is predicted to be involved in target‐site resistance to neonicotinoids such as imidacloprid, and the Paramyosin ( Prm ) gene, which is predicted to encode an invertebrate muscle protein.…”

“…The fitness of allelic deletions of both genes was tested in the presence of imidacloprid at two different temperatures, 20 and 30 °C. The deletion of nAChRα3 increased susceptibility to imidacloprid at both temperatures while the deletion of Prm only increased susceptibility at 20 °C, suggesting that resistance conferred by this gene may be temperature dependent …”

“…Genes which are involved in thermotolerance and genes which are involved in insecticide resistance are ‘locked’ in genomic areas of reduced recombination, resulting from chromosomal inversions (Fig. (b)) . This study focused on a single insecticide, imidacloprid, and the model organism D. melanogaster , which is a non‐target insect for insecticides .…”