Genome Resequencing Reveals Rapid, Repeated Evolution in the Colorado Potato Beetle.

ABSTRACT

Insecticide resistance and rapid pest evolution threatens food security and the development of sustainable agricultural practices, yet the evolutionary mechanisms that allow pests to rapidly adapt to control tactics remains unclear. Here, we examine how a global super-pest, the Colorado potato beetle (CPB), Leptinotarsa decemlineata, rapidly evolves resistance to insecticides. Using whole-genome resequencing and transcriptomic data focused on its ancestral and pest range in North America, we assess evidence for three, nonmutually exclusive models of rapid evolution pervasive selection on novel mutations, rapid regulatory evolution, and repeated selection on standing genetic variation. Population genomic analysis demonstrates that CPB is geographically structured, even among recently established pest populations. Pest populations exhibit similar levels of nucleotide diversity, relative to nonpest populations, and show evidence of recent expansion. Genome scans provide clear signatures of repeated adaptation across CPB populations, with especially strong evidence of selection on insecticide resistance genes in different populations. Analyses of gene expression show that constitutive upregulation of candidate insecticide resistance genes drives distinctive population patterns. CPB evolves insecticide resistance repeatedly across agricultural regions, leveraging similar genetic pathways but different genes, demonstrating a polygenic trait architecture for insecticide resistance that can evolve from standing genetic variation. Despite expectations, we do not find support for strong selection on novel mutations, or rapid evolution from selection on regulatory genes. These results suggest that integrated pest management practices must mitigate the evolution of polygenic resistance phenotypes among local pest populations, in order to maintain the efficacy and sustainability of novel control techniques.