Genome resequencing reveals rapid, repeated evolution in the Colorado potato beetle,Leptinotarsa decemlineata

Background Insecticide resistance and rapid pest evolution threatens food security and the development of sustainable agricultural practices. An improved understanding of the evolutionary mechanisms that allow pests to rapidly adapt to novel control tactics will help prevent economically damaging outbreaks. The Colorado potato beetle (CPB), Leptinotarsa decemlineata, is a global super-pest that 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, non-mutually exclusive models of rapid evolution: pervasive selection on novel mutations, rapid regulatory evolution, and repeated selection on standing genetic variation. Results Population genomic analysis demonstrates that CPB is geographically structured, even among recently established pest populations. Pest populations exhibit only modest reductions in nucleotide diversity, relative to non-pest ancestral populations, and show evidence of recent demographic expansion. Genome scans of selection provide clear signatures of repeated adaptation across different CPB populations, with especially strong evidence that insecticide resistance involves selection of different genes in different populations. Similarly, analyses of gene expression show that constitutive upregulation of candidate insecticide resistance genes drives distinctive population patterns. Conclusion CPB evolves insecticide resistance repeatedly across agricultural regions, and oftentimes at the same loci, supporting a prominent role of polygenic evolution 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. An important future goal will be to understand how polygenic resistance phenotypes spread among local pest populations, in order to refine integrated pest management practices to maintain the efficacy and sustainability of novel control techniques.