Insecticide exposure affects intergenerational patterns of DNA methylation in the Colorado potato beetle, <i>Leptinotarsa decemlineata</i>

Brevik, Kristian; Bueno, Erika; McKay, Stephanie; Schoville, Sean D.; Chen, Yolanda H.

doi:10.1111/eva.13153

Cited by 31 publications

(20 citation statements)

References 115 publications

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“…From our results, evolution of multiple resistance loci from standing variation appears to best explain this pattern, although we note that some alternative mechanisms were not investigated and could contribute to rapid evolutionary change. Notably, recent work in CPB has shown that changes in DNA methylation patterns might drive transgenerational epigenetic mechanisms of regulatory evolution that lead to pesticide resistance ( Brevik et al 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Genome Resequencing Reveals Rapid, Repeated Evolution in the Colorado Potato Beetle

Pélissié

Chen

Cohen

et al. 2022

Molecular Biology and Evolution

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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.

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Section: Discussionmentioning

confidence: 99%

Genome Resequencing Reveals Rapid, Repeated Evolution in the Colorado Potato Beetle

Pélissié

Chen

Cohen

et al. 2022

Molecular Biology and Evolution

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“…The study of anthropogenically derived influences as epigenetic stimuli, such as pollution and climate change, are among the fast-growing areas of interest within insect EMMs [ 79 , 80 , 81 ]. The goal of these studies is to assess how stressors may affect different ecological levels [ 82 ], considering exposure to pesticides [ 41 , 44 , 83 ], endocrine disruptors [ 11 , 84 , 85 ], heavy metals [ 84 , 86 , 87 ], or temperature changes [ 88 ] as triggers of epigenetic changes.…”

Section: Epigenetic Molecular Mechanismsmentioning

confidence: 99%

“…For instance, in the parasitic wasps key for biological control in agricultural management such as Nasonia vitripennis (Walker, 1836) (Hymenoptera: Pteromalidae), the neonicotinoid imidacloprid disrupts sex allocation cues, reducing their reproductive success [ 212 ]. Sub-lethal IMI exposure in the Colorado potato beetle, pest Leptinotarsa decemlineata Say, 1824 (Coleoptera: Chrysomelidae) has been linked to alterations in specific genes, C5-cytosine methylation, and transposable elements that have been postulated as linked to the development of insecticide resistance [ 81 ].…”

Section: Neonicotinoid Insecticidesmentioning

confidence: 99%

Insect Epigenetic Mechanisms Facing Anthropogenic-Derived Contamination, an Overview

Olivares-Castro

Cáceres-Jensen

Guerrero-Bosagna

et al. 2021

Insects

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Currently, the human species has been recognized as the primary species responsible for Earth’s biodiversity decline. Contamination by different chemical compounds, such as pesticides, is among the main causes of population decreases and species extinction. Insects are key for ecosystem maintenance; unfortunately, their populations are being drastically affected by human-derived disturbances. Pesticides, applied in agricultural and urban environments, are capable of polluting soil and water sources, reaching non-target organisms (native and introduced). Pesticides alter insect’s development, physiology, and inheritance. Recently, a link between pesticide effects on insects and their epigenetic molecular mechanisms (EMMs) has been demonstrated. EMMs are capable of regulating gene expression without modifying genetic sequences, resulting in the expression of different stress responses as well as compensatory mechanisms. In this work, we review the main anthropogenic contaminants capable of affecting insect biology and of triggering EMMs. EMMs are involved in the development of several diseases in native insects affected by pesticides (e.g., anomalous teratogenic reactions). Additionally, EMMs also may allow for the survival of some species (mainly pests) under contamination-derived habitats; this may lead to biodiversity decline and further biotic homogenization. We illustrate these patterns by reviewing the effect of neonicotinoid insecticides, insect EMMs, and their ecological consequences.

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“…It has also been suggested that sublethal exposure to pesticides may pro-duce immune suppression in pollinators [148], increasing their susceptibility to pathogens. Recent evidence regarding epigenetic inheritance has demonstrated that pesticides drive pathological alterations in insect pollinators [149], while in target organisms it has been reported the development of IA promotes epigenetic transgenerational resistance against pesticides [150]. Thus, while pesticide detrimental impact may last several generations on non-target organisms, their efficacy on pest species may be reduced as they became immune to their effects [151].…”

Section: Pesticidesmentioning

confidence: 99%

Agroecological Strategies to Safeguard Insect Pollinators in Biodiversity Hotspots: Chile as a Case Study

et al. 2021

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Industrial agriculture (IA) has been recognized among the main drivers of biodiversity loss, climate change, and native pollinator decline. Here we summarize the known negative effects of IA on pollinator biodiversity and illustrate these problems by considering the case of Chile, a “world biodiversity hotspot” (WBH) where food exports account for a considerable share of the economy in this country. Most of Chile’s WBH area is currently being replaced by IA at a fast pace, threatening local biodiversity. We present an agroecological strategy for sustainable food production and pollinator conservation in food-producing WBHs. In this we recognize native pollinators as internal inputs that cannot be replaced by IA technological packages and support the development of agroecological and biodiversity restorative practices to protect biodiversity. We suggest four fundamental pillars for food production change based on: (1) sharing the land, restoring and protecting; (2) ecological intensification; (3) localized knowledge, research, and technological development; and (4) territorial planning and implementation of socio-agroecological policies. This approach does not need modification of native pollination services that sustain the world with food and basic subsistence goods, but a paradigm changes where the interdependency of nature and human wellbeing must be recognized for ensuring the world’s food security and sovereignty.

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

Cited by 31 publications

References 115 publications

Genome Resequencing Reveals Rapid, Repeated Evolution in the Colorado Potato Beetle

Genome Resequencing Reveals Rapid, Repeated Evolution in the Colorado Potato Beetle

Insect Epigenetic Mechanisms Facing Anthropogenic-Derived Contamination, an Overview

Agroecological Strategies to Safeguard Insect Pollinators in Biodiversity Hotspots: Chile as a Case Study

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