Crop domestication is the process of artificially selecting plants to increase their suitability to human requirements: taste, yield, storage, and cultivation practices. There is increasing evidence that crop domestication can profoundly alter interactions among plants, herbivores, and their natural enemies. Overall, little is known about how these interactions are affected by domestication in the geographical ranges where these crops originate, where they are sympatric with the ancestral plant and share the associated arthropod community. In general, domestication consistently has reduced chemical resistance against herbivorous insects, improving herbivore and natural enemy performance on crop plants. More studies are needed to understand how changes in morphology and resistance-related traits arising from domestication may interact with environmental variation to affect species interactions across multiple scales in agroecosystems and natural ecosystems.

The Colorado potato beetle is one of the most challenging agricultural pests to manage. It has shown a spectacular ability to adapt to a variety of solanaceaeous plants and variable climates during its global invasion, and, notably, to rapidly evolve insecticide resistance. To examine evidence of rapid evolutionary change, and to understand the genetic basis of herbivory and insecticide resistance, we tested for structural and functional genomic changes relative to other arthropod species using genome sequencing, transcriptomics, and community annotation. Two factors that might facilitate rapid evolutionary change include transposable elements, which comprise at least 17% of the genome and are rapidly evolving compared to other Coleoptera, and high levels of nucleotide diversity in rapidly growing pest populations. Adaptations to plant feeding are evident in gene expansions and differential expression of digestive enzymes in gut tissues, as well as expansions of gustatory receptors for bitter tasting. Surprisingly, the suite of genes involved in insecticide resistance is similar to other beetles. Finally, duplications in the RNAi pathway might explain why Leptinotarsa decemlineata has high sensitivity to dsRNA. The L. decemlineata genome provides opportunities to investigate a broad range of phenotypes and to develop sustainable methods to control this widely successful pest.

Background:Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods. Results:Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality and chemoperception. Conclusions:These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.

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Background: Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods. Results: Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception. Conclusions: These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.

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.

Although pesticides are a major selective force in driving the evolution of insect pests, the evolutionary processes that give rise to insecticide resistance remain poorly understood. Insecticide resistance has been widely observed to increase with frequent and intense insecticide exposure, but can be lost following the relaxation of insecticide use. One possible but rarely explored explanation is that insecticide resistance may be associated with epigenetic modifications, which influence the patterning of gene expression without changing underlying DNA sequence. Epigenetic modifications such as DNA methylation, histone modifications, and small RNAs have been observed to be heritable in arthropods, but their role in the context of rapid evolution of insecticide resistance remain poorly understood. Here, we discuss evidence supporting how: firstly, insecticide-induced effects can be transgenerationally inherited; secondly, epigenetic modifications are heritable; and thirdly, epigenetic modifications are responsive to pesticide and xenobiotic stress. Therefore, pesticides may drive the evolution of resistance via epigenetic processes. Moreover, insect pests primed by pesticides may be more tolerant of other stress, further enhancing their success in adapting to agroecosystems. Resolving the role of epigenetic modifications in the rapid evolution of insect pests has the potential to lead to new approaches for integrated pest management as well as improve our understanding of how anthropogenic stress may drive the evolution of insect pests.

The ability of insect pests to rapidly and repeatedly adapt to insecticides has long challenged entomologists and evolutionary biologists. Since Crow's seminal paper on insecticide resistance in 1957, new data and insights continue to emerge that are relevant to the old questions about how insecticide resistance evolves: such as whether it is predominantly mono- or polygenic, and evolving from standing vs. de novo genetic variation. Many studies support the monogenic hypothesis, and current management recommendations assume single- or two-locus models. But inferences could be improved by integrating data from a broader sample of pest populations and genomes. Here, we generate evidence relevant to these questions by applying a landscape genomics framework to the study of insecticide resistance in a major agricultural pest, Colorado potato beetle, Leptinotarsa decemlineata (Say). Genome-environment association tests using genomic variation from 16 populations spanning gradients of landscape variables associated with insecticide exposure over time revealed 42 strong candidate insecticide resistance genes, with potentially overlapping roles in multiple resistance mechanisms. Measurements of resistance to a widely used insecticide, imidacloprid, among 47 L. decemlineata populations revealed heterogeneity at a small (2 km) scale and no spatial signature of origin or spread throughout the landscape. Analysis of nucleotide diversity suggested candidate resistance loci have undergone varying degrees of selective sweeps, often maintaining similar levels of nucleotide diversity to neutral loci. This study suggests that many genes are involved in insecticide resistance in L. decemlineata and that resistance likely evolves from both de novo and standing genetic variation.