The role of structural variants in pest adaptation and genome evolution of the Colorado potato beetle, <i>Leptinotarsa decemlineata</i> (Say)

Structural variation has been associated with genetic diversity and adaptation. Despite these observations, it is not clear what their relative importance is for evolution, especially in rapidly adapting species. Here, we examine the significance of structural polymorphisms in pesticide resistance evolution of the agricultural super-pest, the Colorado potato beetle, Leptinotarsa decemlineata. By employing a parent offspring trio sequencing procedure, we develop highly contiguous reference genomes to characterize structural variation. These updated assemblies represent >100-fold improvement of contiguity and include derived pest and ancestral nonpest individuals. We identify >200,000 structural variations, which appear to be nonrandomly distributed across the genome as they co-occur with transposable elements and genes. Structural variations intersect with exons in a large proportion of gene annotations (~20%) that are associated with insecticide resistance (including cytochrome P450s), development, and transcription. To understand the role structural variations play in adaptation, we measure their allele frequencies among an additional 57 individuals using whole genome resequencing data, which represents pest and nonpest populations of North America. Incorporating multiple independent tests to detect the signature of natural selection using SNP data, we identify 14 genes that are probably under positive selection, include structural variations, and SNPs of elevated frequency within the pest lineages. Among these, three are associated with insecticide resistance based on previous research. One of these genes, CYP4g15, is coinduced during insecticide exposure with glycosyltransferase-13, which is a duplicated gene enclosed within a structural variant adjacent to the CYP4g15 genic region. These results demonstrate the significance of structural variations as a genomic feature to describe species history, genetic diversity, and adaptation.