Population genomics reveal multiple independent origins of pesticide resistance in the polyphagous pest, Tetranychus urticae

The rapid evolution of pesticide resistance imposes great pressure on food production. However, how resistance alleles arise and spread across field populations remains largely understood. Here, we study the evolutionary trajectories of resistance alleles in Tetranychus urticae, a rapidly evolving pest. We sequence the genomes of 258 T. urticae females collected from China. Combined with global reference genomic data, we examine the evolutionary origin(s) of 18 mutations across 10 target-site genes and analyze the global population genetic structure using genome-wide SNPs. Our findings reveal a striking prevalence of multiple independent origins of resistance mutations, with only two of 18 mutations showing an apparent single origin. Population structure and haplotype analyses point to an important role of gene flow in the spread of resistance alleles. Selection analyses reveal pesticide-driven sweeps affecting genetic diversity. These findings advance our understanding of the rapid adaptation of arthropod herbivores to extreme selective pressure.