Elevated rates of positive selection drive the evolution of pestiferousness in the Colorado potato beetle (Leptinotarsa decemlineata, Say).

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.

Transposable elements differ between geographic populations of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae).

Agricultural insect herbivores show a remarkable ability to adapt to modern agroecosystems, making them ideal for the study of the mechanisms underlying rapid evolution. The mobilization of transposable elements is one mechanism that may help explain this ability. The Colorado potato beetle, Leptinotarsa decemlineata, is a highly adaptable species, as shown by its wide host range, broad geographic distribution, and tolerance to insecticides. However, beetle populations vary in insecticide tolerance, with Eastern US beetle populations being more adaptable than Western US ones. Here, we use a community ecology approach to examine how the abundance and diversity of transposable elements differs in 88 resequenced genomes of L. decemlineata collected throughout North America. We tested if assemblages and mobilization of transposable elements differed between populations of L. decemlineata based on the beetle's geography, host plant, and neonicotinoid insecticide resistance. Among populations of North American L. decemlineata, individuals collected in Mexico host more transposable elements than individuals collected in the United States. Transposable element insertion locations differ among geographic populations, reflecting the evolutionary history of this species. Total transposable element diversity between L. decemlineata individuals is enough to distinguish between populations, with more TEs found in beetles collected in Mexico than in the United States. Transposable element diversity does not appear to differ between beetles found on different host plants, or relate to different levels of insecticide resistance.

Insecticide exposure affects intergenerational patterns of DNA methylation in the Colorado potato beetle, Leptinotarsa decemlineata.

Insecticide use is pervasive as a selective force in modern agroecosystems. Insect herbivores exposed to these insecticides have been able to rapidly evolve resistance to them, but how they are able to do so is poorly understood. One possible but largely unexplored explanation is that exposure to sublethal doses of insecticides may alter epigenetic patterns that are heritable. For instance, epigenetic mechanisms, such as DNA methylation that modifies gene expression without changing the underlying genetic code, may facilitate the emergence of resistant phenotypes in complex ways. We assessed the effects of sublethal insecticide exposure, with the neonicotinoid imidacloprid, on DNA methylation in the Colorado potato beetle, Leptinotarsa decemlineata, examining both global changes in DNA methylation and specific changes found within genes and transposable elements. We found that exposure to insecticide led to decreases in global DNA methylation for parent and F2 generations and that many of the sites of changes in methylation are found within genes associated with insecticide resistance, such as cytochrome P450s, or within transposable elements. Exposure to sublethal doses of insecticide caused heritable changes in DNA methylation in an agricultural insect herbivore. Therefore, epigenetics may play a role in insecticide resistance, highlighting a fundamental mechanism of evolution while informing how we might better coexist with insect species in agroecosystems.

Pesticide durability and the evolution of resistance: A novel application of survival analysis.

BACKGROUND: Arthropod pests are widely perceived to evolve resistance to insecticides at different rates. Although widespread "successful" species are assumed to evolve quickly and minor pests slowly, few studies have utilized published data on resistance events to test for differences among species. Using 532 records from the Arthropod Pesticide Resistance Database covering 20 species, we applied a survival analysis to model the number of generations from insecticide introduction to the first report of arthropod resistance, providing one of the most comprehensive analyses of this question to date. Our approach tested: 1) whether successful pests evolve resistance faster than close relatives, 2) whether species differ significantly in the time to demonstrate resistance, and 3) whether different insecticide classes differ in durability (length of time an insecticide is used before resistance arises). RESULTS: We found that species differed significantly in the amount of time it took for resistance to be reported. Overall, the median duration between the introduction of an insecticide and the first report of resistance was 66 generations (95% c.i. 60-78 generations), and highly-resistant arthropods did not evolve resistance faster than their relatives. Insecticide durability did not differ by the mode of action or year of introduction. CONCLUSION: Arthropod species significantly varied in how rapidly they evolve resistance to new insecticides, regardless of their chemistry. Visualization of the history of insecticide resistance provides information to be used for understanding how pesticide resistance evolved and how it can best be managed. © 2018 Society of Chemical Industry.

Transgenerational effects of insecticides-implications for rapid pest evolution in agroecosystems.

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.

A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae).

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.