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, non-mutually 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 non-pest 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.
Contextualizing evolutionary history and identifying genomic features of an insect that might contribute to its pest status is important in developing early detection and control tactics. In order to understand the evolution of pestiferousness, which we define as the accumulation of traits that contribute to an insect population's success in an agroecosystem, we tested the importance of known genomic properties associated with rapid adaptation in the Colorado potato beetle (CPB), Leptinotarsa decemlineata Say. Within the leaf beetle genus Leptinotarsa, only CPB, and a few populations therein, has risen to pest status on cultivated nightshades, Solanum. Using whole genomes from ten closely related Leptinotarsa species native to the United States, we reconstructed a high-quality species tree and used this phylogenetic framework to assess evolutionary patterns in four genomic features of rapid adaptation: standing genetic variation, gene family expansion and contraction, transposable element abundance and location, and positive selection at protein-coding genes. Throughout approximately 20 million years of history, Leptinotarsa species show little evidence of gene family turnover and transposable element variation. However, there is a clear pattern of CPB experiencing higher rates of positive selection on protein-coding genes. We determine that these rates are associated with greater standing genetic variation due to larger effective population size, which supports the theory that the demographic history contributes to rates of protein evolution. Furthermore, we identify a suite of coding genes under positive selection that are putatively associated with pestiferousness in the Colorado potato beetle lineage. They are involved in the biological processes of xenobiotic detoxification, chemosensation and hormone function.
19Insect pests are characterized by expansion, preference and performance on agricultural 20 crops, high fecundity and rapid adaptation to control methods, which we collectively refer to as 21 pestiferousness. Which organismal traits and evolutionary processes facilitate certain taxa 22 becoming pests remains an outstanding question for evolutionary biologists. In order to 23 understand these features, we set out to test the relative importance of genomic properties that 24 underlie the rapid evolution of pestiferousness in the emerging pest model: the Colorado potato 25 beetle (CPB), Leptinotarsa decemlineata Say. Within the Leptinotarsa genus, only CPB has 26 risen to pest status on cultivated Solanum. Using whole genomes from ten closely related 27 Leptinotarsa species, we reconstructed a high-quality species tree of this genus. Within this 28 phylogenetic framework, we tested the relative importance of four drivers of rapid adaptation: 29 standing genetic variation, gene family expansion and contraction, transposable element 30 variation, and protein evolution. Throughout approximately 20 million years of divergence, 31 Leptinotarsa show little evidence of gene family turnover or transposable element variation 32 contributing to pest evolution. However, there is a clear pattern of pest lineages experiencing 33 greater rates of positive selection on protein coding genes, as well as retaining higher levels of 34 standing genetic variation. We also identify a suite of positively selected genes unique to the 35 Colorado potato beetle that are directly associated with pestiferousness. These genes are 36 involved in xenobiotic detoxification, chemosensation, and hormones linked with pest behavior 37 and physiology.38 39
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.
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