Cross‐protection interactions in insect pests: Implications for pest management in a changing climate

Abstract Agricultural insect pests display an exceptional ability to adapt quickly to natural and anthropogenic stressors. Emerging evidence suggests that frequent and varied sources of stress play an important role in driving protective physiological responses; therefore, intensively managed agroecosystems combined with climatic shifts might be an ideal crucible for stress adaptation. Cross‐protection, where responses to one stressor offers protection against another type of stressor, has been well documented in many insect species, yet the molecular and epigenetic underpinnings that drive overlapping protective responses in insect pests remain unclear. In this perspective, we discuss cross‐protection mechanisms and provide an argument for its potential role in increasing tolerance to a wide range of natural and anthropogenic stressors in agricultural insect pests. By drawing from existing literature on single and multiple stressor studies, we outline the processes that facilitate cross‐protective interactions, including epigenetic modifications, which are understudied in insect stress responses. Finally, we discuss the implications of cross‐protection for insect pest management, focusing on the consequences of cross‐protection between insecticides and elevated temperatures associated with climate change. Given the multiple ways that insect pests are intensively managed in agroecosystems, we suggest that examining the role of multiple stressors can be important in understanding the wide adaptability of agricultural insect pests. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

[1]  V. Košťál,et al.  Insect cross-tolerance to freezing and drought stress: role of metabolic rearrangement , 2022, Proceedings of the Royal Society B.

[2]  Ross N. Cuthbert,et al.  Transgenerational responses to heat and fasting acclimation in the Angoumois grain moth , 2022, Journal of Stored Products Research.

[3]  N. Desneux,et al.  Transgenerational hormesis effects of nitenpyram on fitness and insecticide tolerance/resistance of Nilaparvata lugens , 2022, Journal of Pest Science.

[4]  G. C. Cutler,et al.  Review of molecular and biochemical responses during stress induced stimulation and hormesis in insects. , 2022, The Science of the total environment.

[5]  G. Benelli,et al.  Hormesis and insects: Effects and interactions in agroecosystems. , 2022, The Science of the total environment.

[6]  B. Moussian,et al.  Xenobiotic responses in insects. , 2022, Archives of insect biochemistry and physiology.

[7]  C. Guerrero-Bosagna,et al.  Insect Epigenetic Mechanisms Facing Anthropogenic-Derived Contamination, an Overview , 2021, Insects.

[8]  Yu-Zhou Du,et al.  Transcriptome analysis reveals gene expression differences in Liriomyza trifolii exposed to combined heat and abamectin exposure , 2021, PeerJ.

[9]  J. Moreau,et al.  Warming increases tolerance of an insect pest to fungicide exposure through temperature-mediated hormesis , 2021, Journal of Pest Science.

[10]  K. Lu,et al.  Olfactory perception of herbicide butachlor by GOBP2 elicits ecdysone biosynthesis and detoxification enzyme responsible for chlorpyrifos tolerance in Spodoptera litura. , 2021, Environmental pollution.

[11]  Kun Xing,et al.  Complex delayed and transgenerational effects driven by the interaction of heat and insecticide in the maternal generation of the wheat aphid, Sitobion avenae. , 2021, Pest management science.

[12]  Yu-Zhou Du,et al.  Temperature affects the tolerance of Liriomyza trifolii to insecticide abamectin. , 2021, Ecotoxicology and environmental safety.

[13]  M. Zovko,et al.  The Impact of Climate Change on Agricultural Insect Pests , 2021, Insects.

[14]  R. Nauen,et al.  Transcriptional regulation of xenobiotic detoxification genes in insects - An overview. , 2021, Pesticide biochemistry and physiology.

[15]  R. Stoks,et al.  Transgenerational exposure to warming reduces the sensitivity to a pesticide under warming. , 2021, Environmental Pollution.

[16]  Dun Jiang,et al.  The susceptibility of Lymantria dispar larvae to Beauveria bassiana under Cd stress: A multi-omics study. , 2021, Environmental pollution.

[17]  D. Renault,et al.  Thermal plasticity and sensitivity to insecticides in populations of an invasive beetle: Cyfluthrin increases vulnerability to extreme temperature. , 2021, Chemosphere.

[18]  Essie M. Rodgers,et al.  Harnessing the potential of cross-protection stressor interactions for conservation: a review. , 2021, Conservation physiology.

[19]  S. McKay,et al.  Insecticide exposure affects intergenerational patterns of DNA methylation in the Colorado potato beetle, Leptinotarsa decemlineata , 2020, Evolutionary applications.

[20]  M. Clark,et al.  Transcriptional frontloading contributes to cross‐tolerance between stressors , 2020, Evolutionary applications.

[21]  K. Lu,et al.  The role of cytochrome P450-mediated detoxification in insect adaptation to xenobiotics. , 2020, Current opinion in insect science.

[22]  Brent J Sinclair,et al.  Help, there are ‘omics’ in my comparative physiology! , 2020, Journal of Experimental Biology.

[23]  A. Córdoba‐Aguilar,et al.  Multigenerational experimental simulation of climate change on an economically important insect pest , 2020, Ecology and evolution.

[24]  R. Stoks,et al.  Reduced stress defence responses contribute to the higher toxicity of a pesticide under warming , 2020, Molecular ecology.

[25]  Cheng Lu,et al.  Comparative genome-wide DNA methylation analysis reveals epigenomic differences in response to heat-humidity stress in Bombyx mori. , 2020, International journal of biological macromolecules.

[26]  R. Hager,et al.  DNA methylation patterns respond to thermal stress in the viviparous cockroach Diploptera punctata , 2020, Epigenetics.

[27]  Y. Gutiérrez,et al.  Multiple mechanisms in which agricultural insects respond to environmental stressors: canalization, plasticity and evolution , 2020, Revista de Ciencias Agrícolas.

[28]  C. Villagra,et al.  Epigenetic Molecular Mechanisms in Insects , 2020, Neotropical Entomology.

[29]  A. Hoffmann,et al.  Validating measurements of acclimation for climate change adaptation. , 2020, Current opinion in insect science.

[30]  R. Stoks,et al.  Mosquito larvae that survive a heat spike are less sensitive to subsequent exposure to the pesticide chlorpyrifos. , 2020, Environmental pollution.

[31]  J. Parrilla-Doblas,et al.  DNA methylation editing by CRISPR-guided excision of 5-methylcytosine. , 2020, Journal of molecular biology.

[32]  G. López-Martínez,et al.  A dose of experimental hormesis: When mild stress protects and improves animal performance. , 2020, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[33]  Ran Wang,et al.  Molecular characterization of DNA methyltransferase 1 and its role in temperature change of armyworm Mythimna separata Walker. , 2020, Archives of insect biochemistry and physiology.

[34]  Zinan Wang,et al.  REVIEW: Climate change and the genetics of insecticide resistance. , 2019, Pest management science.

[35]  K. Lu,et al.  Copper-induced H2O2 accumulation confers larval tolerance to xanthotoxin by modulating CYP6B50 expression in Spodoptera litura. , 2019, Pesticide biochemistry and physiology.

[36]  K. Lu,et al.  Copper exposure enhances Spodoptera litura larval tolerance to β-cypermethrin. , 2019, Pesticide biochemistry and physiology.

[37]  R. Stoks,et al.  Whether warming magnifies the toxicity of a pesticide is strongly dependent on the concentration and the null model. , 2019, Aquatic toxicology.

[38]  N. Zhang,et al.  Molecular characterization of class I histone deacetylases and their expression in response to thermal and oxidative stresses in the red flour beetle, Tribolium castaneum , 2019, Genetica.

[39]  Xiang-Dong Liu,et al.  Multigenerational heat acclimation increases thermal tolerance and expression levels of Hsp70 and Hsp90 in the rice leaf folder larvae. , 2019, Journal of thermal biology.

[40]  R. Zeng,et al.  Exposure to Herbicides Prime P450-Mediated Detoxification of Helicoverpa armigera against Insecticide and Fungal Toxin , 2019, Insects.

[41]  Nathaniel D. Tippens,et al.  methyl-ATAC-seq measures DNA methylation at accessible chromatin , 2018, bioRxiv.

[42]  S. Pillai,et al.  Hypoxic environment protects cowpea bruchid (Callosobruchus maculatus) from electron beam irradiation damage. , 2018, Pest management science.

[43]  Maor Matzrafi.  Climate change exacerbates pest damage through reduced pesticide efficacy. , 2018, Pest management science.

[44]  P. Jha,et al.  Multidimensional relationships of herbicides with insect-crop food webs. , 2018, The Science of the total environment.

[45]  Scott C. Merrill,et al.  Increase in crop losses to insect pests in a warming climate , 2018, Science.

[46]  Toby Bloom,et al.  Whole-genome bisulfite sequencing with improved accuracy and cost , 2018, Genome research.

[47]  A. Roy,et al.  Cap 'n' collar C regulates genes responsible for imidacloprid resistance in the Colorado potato beetle, Leptinotarsa decemlineata. , 2018, Insect biochemistry and molecular biology.

[48]  L. Wijayaratne,et al.  Effects of spinosad on the heat tolerance and cold tolerance of Sitophilus oryzae L. (Coleoptera: Curculionidae) and Rhyzopertha dominica F. (Coleoptera: Bostrichidae) , 2018, Journal of Stored Products Research.

[49]  T. Davies,et al.  An overview of functional genomic tools in deciphering insecticide resistance , 2018, Current opinion in insect science.

[50]  Zewen Liu,et al.  Effects of temperature on fitness costs in chlorpyrifos‐resistant brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae) , 2018, Insect science.

[51]  C. Bradfield,et al.  Transcriptomic analysis reveals similarities in genetic activation of detoxification mechanisms resulting from imidacloprid and chlorothalonil exposure , 2018, bioRxiv.

[52]  B. Salbu,et al.  Deciphering the Combined Effects of Environmental Stressors on Gene Transcription: A Conceptual Approach. , 2018, Environmental science & technology.

[53]  C. Bradfield,et al.  Agricultural fungicides inadvertently influence the fitness of Colorado potato beetles, Leptinotarsa decemlineata, and their susceptibility to insecticides , 2018, bioRxiv.

[54]  C. Short,et al.  Hormetic benefits of prior anoxia exposure in buffering anoxia stress in a soil-pupating insect , 2018, Journal of Experimental Biology.

[55]  F. Wan,et al.  Molecular characterizations of DNA methyltransferase 3 and its roles in temperature tolerance in the whitefly, Bemisia tabaci Mediterranean , 2018, Insect molecular biology.

[56]  S. McKay,et al.  Transgenerational effects of insecticides-implications for rapid pest evolution in agroecosystems. , 2018, Current opinion in insect science.

[57]  J. Terblanche,et al.  Plasticity and cross‐tolerance to heterogeneous environments: divergent stress responses co‐evolved in an African fruit fly , 2018, Journal of evolutionary biology.

[58]  N. Desneux,et al.  Uptake of quercetin reduces larval sensitivity to lambda-cyhalothrin in Helicoverpa armigera , 2018, Journal of Pest Science.

[59]  Yuncai Liu,et al.  Comparative transcriptome analysis of Glyphodes pyloalis Walker (Lepidoptera: Pyralidae) reveals novel insights into heat stress tolerance in insects , 2017, BMC Genomics.

[60]  V. Brahmachari,et al.  Correlation between desiccation stress response and epigenetic modifications of genes in Drosophila melanogaster: An example of environment-epigenome interaction. , 2017, Biochimica et biophysica acta. Gene regulatory mechanisms.

[61]  J. Terblanche,et al.  Effects of nutrient and water restriction on thermal tolerance: A test of mechanisms and hypotheses. , 2017, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[62]  B. Brooke,et al.  The effect of elevated temperatures on the life history and insecticide resistance phenotype of the major malaria vector Anopheles arabiensis (Diptera: Culicidae) , 2017, Malaria Journal.

[63]  R. Arora,et al.  Breeding Insect Resistant Crops for Sustainable Agriculture , 2017, Springer Singapore.

[64]  B. Sinclair,et al.  Can we predict the effects of multiple stressors on insects in a changing climate? , 2016, Current opinion in insect science.

[65]  A. Alyokhin,et al.  Heat‐induced mortality and expression of heat shock proteins in Colorado potato beetles treated with imidacloprid , 2016, Insect science.

[66]  R. Maleszka.  Epigenetic code and insect behavioural plasticity. , 2016, Current opinion in insect science.

[67]  Zewen Liu,et al.  The roles of CYP6AY1 and CYP6ER1 in imidacloprid resistance in the brown planthopper: Expression levels and detoxification efficiency. , 2016, Pesticide biochemistry and physiology.

[68]  J. Chiu,et al.  Seasonal cues induce phenotypic plasticity of Drosophila suzukii to enhance winter survival , 2016, BMC Ecology.

[69]  A. Hoffmann,et al.  What Can Plasticity Contribute to Insect Responses to Climate Change? , 2016, Annual review of entomology.

[70]  M. Horowitz.  Epigenetics and cytoprotection with heat acclimation. , 2016, Journal of applied physiology.

[71]  Y. Wexler,et al.  The negative effect of starvation and the positive effect of mild thermal stress on thermal tolerance of the red flour beetle, Tribolium castaneum , 2016, SCIENCE NATURE.

[72]  J. Stillman,et al.  Multiple Stressors in a Changing World: The Need for an Improved Perspective on Physiological Responses to the Dynamic Marine Environment. , 2016, Annual review of marine science.

[73]  R. R. Rix,et al.  Sublethal concentrations of imidacloprid increase reproduction, alter expression of detoxification genes, and prime Myzus persicae for subsequent stress , 2016, Journal of Pest Science.

[74]  J. Oehlmann,et al.  Epigenetic alterations and decreasing insecticide sensitivity of the Asian tiger mosquito Aedes albopictus. , 2015, Ecotoxicology and environmental safety.

[75]  J. G. Sørensen,et al.  Physiological and molecular mechanisms associated with cross tolerance between hypoxia and low temperature in Thaumatotibia leucotreta. , 2015, Journal of insect physiology.

[76]  B. Sinclair,et al.  The relative importance of number, duration and intensity of cold stress events in determining survival and energetics of an overwintering insect , 2015 .

[77]  T. MacRae,et al.  Insect heat shock proteins during stress and diapause. , 2015, Annual review of entomology.

[78]  D. Renault,et al.  Exposure to desiccating conditions and cross-tolerance with thermal stress in the lesser mealworm Alphitobius diaperinus (Coleoptera : Tenebrionidae) , 2015, Revue de Ecologie-La Terre et la Vie.

[79]  A. Michel,et al.  RNA-Seq reveals a xenobiotic stress response in the soybean aphid, Aphis glycines, when fed aphid-resistant soybean , 2014, BMC Genomics.

[80]  M. Skinner.  Environmental stress and epigenetic transgenerational inheritance , 2014, BMC Medicine.

[81]  Xueyan Shi,et al.  Oral Delivery Mediated RNA Interference of a Carboxylesterase Gene Results in Reduced Resistance to Organophosphorus Insecticides in the Cotton Aphid, Aphis gossypii Glover , 2014, PloS one.

[82]  L. Lindström,et al.  Northward range expansion requires synchronization of both overwintering behaviour and physiology with photoperiod in the invasive Colorado potato beetle (Leptinotarsa decemlineata) , 2014, Oecologia.

[83]  Lukas M. von Ziegler,et al.  Early life epigenetic programming and transmission of stress‐induced traits in mammals , 2014, BioEssays : news and reviews in molecular, cellular and developmental biology.

[84]  E. Calabrese.  Hormesis: a fundamental concept in biology , 2014, Microbial cell.

[85]  Anne-Kathrin Classen,et al.  Sensing cellular states—signaling to chromatin pathways targeting Polycomb and Trithorax group function , 2014, Cell and Tissue Research.

[86]  D. Hahn,et al.  Early Life Hormetic Treatments Decrease Irradiation-Induced Oxidative Damage, Increase Longevity, and Enhance Sexual Performance during Old Age in the Caribbean Fruit Fly , 2014, PloS one.

[87]  Q. Song,et al.  Molecular basis for insecticide‐enhanced thermotolerance in the brown planthopper Nilaparvata lugens Stål (Hemiptera:Delphacidae) , 2013, Molecular ecology.

[88]  Jonathon H Stillman,et al.  Physiological responses to shifts in multiple environmental stressors: relevance in a changing world. , 2013, Integrative and comparative biology.

[89]  B. Sinclair,et al.  Cross-tolerance and cross-talk in the cold: relating low temperatures to desiccation and immune stress in insects. , 2013, Integrative and comparative biology.

[90]  D. Denlinger,et al.  Physiological mechanisms of seasonal and rapid cold‐hardening in insects , 2013 .

[91]  I. Feliciello,et al.  First evidence of DNA methylation in insect Tribolium castaneum , 2013, Epigenetics.

[92]  T. Oliver,et al.  Genomic basis for coral resilience to climate change , 2013, Proceedings of the National Academy of Sciences.

[93]  G. Ma,et al.  Effect of acclimation on heat-escape temperatures of two aphid species: Implications for estimating behavioral response of insects to climate warming. , 2012, Journal of insect physiology.

[94]  M. Goodisman,et al.  DNA methylation in insects: on the brink of the epigenomic era , 2011, Insect molecular biology.

[95]  S. Chown,et al.  Water loss in insects: an environmental change perspective. , 2011, Journal of insect physiology.

[96]  R. Maleszka,et al.  Insects as innovative models for functional studies of DNA methylation. , 2011, Trends in genetics : TIG.

[97]  V. Lushchak.  Adaptive response to oxidative stress: Bacteria, fungi, plants and animals. , 2011, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[98]  Hui Wei,et al.  Interaction between Short-Term Heat Pretreatment and Fipronil on 2nd Instar Larvae of Diamondback Moth, Plutella Xylostella (Linn) , 2010, Dose-response : a publication of International Hormesis Society.

[99]  Rakhee Banerjee,et al.  Polycomb Repressive Complex 2 and Trithorax modulate Drosophila longevity and stress resistance , 2009, Proceedings of the National Academy of Sciences.

[100]  Jian-Kang Zhu,et al.  Epigenetic regulation of stress responses in plants. , 2009, Current opinion in plant biology.

[101]  D. Denlinger,et al.  Dehydration-induced cross tolerance of Belgica antarctica larvae to cold and heat is facilitated by trehalose accumulation. , 2009, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[102]  Toshiharu Tanaka,et al.  RNA interference-mediated knockdown of a cytochrome P450, CYP6BG1, from the diamondback moth, Plutella xylostella, reduces larval resistance to permethrin. , 2009, Insect biochemistry and molecular biology.

[103]  M. Clark,et al.  How insects survive the cold: molecular mechanisms—a review , 2008, Journal of Comparative Physiology B.

[104]  V. Loeschcke,et al.  Mild heat stress at a young age inDrosophila melanogaster leads to increased Hsp70 synthesis after stress exposure later in life , 2003, Journal of Genetics.

[105]  A. Shelton,et al.  Concepts and applications of trap cropping in pest management. , 2006, Annual review of entomology.

[106]  E. Oerke.  Crop losses to pests , 2005, The Journal of Agricultural Science.

[107]  V. Loeschcke,et al.  Environmental stress, adaptation and evolution: an overview , 2005, Journal of evolutionary biology.

[108]  P. Schulte,et al.  Cross‐Tolerance in the Tidepool Sculpin: The Role of Heat Shock Proteins , 2005, Physiological and Biochemical Zoology.

[109]  H. Hirt,et al.  Reactive oxygen species: metabolism, oxidative stress, and signal transduction. , 2004, Annual review of plant biology.

[110]  L. Field,et al.  DNA methylation in insects , 2004, Insect molecular biology.

[111]  V. Loeschcke,et al.  Lifespan extension of Drosophila melanogaster through hormesis by repeated mild heat stress , 2004, Biogerontology.

[112]  Mark Gerber,et al.  Transcriptional Elongation by RNA Polymerase II and Histone Methylation* , 2003, Journal of Biological Chemistry.

[113]  Michael Hampsey,et al.  Tails of Intrigue Phosphorylation of RNA Polymerase II Mediates Histone Methylation , 2003, Cell.

[114]  A. Bird,et al.  Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals , 2003, Nature Genetics.

[115]  A. Bird.  DNA methylation patterns and epigenetic memory. , 2002, Genes & development.

[116]  L. Neven.  Physiological responses of insects to heat , 2000 .

[117]  L. Field.  Methylation and expression of amplified esterase genes in the aphid Myzus persicae (Sulzer). , 2000, The Biochemical journal.

[118]  M B Thomas,et al.  Ecological approaches and the development of "truly integrated" pest management. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[119]  K. Lole,et al.  Adaptive larval thermotolerance and induced cross‐tolerance to propoxur insecticide in mosquitoes Anopheles stephensi and Aedes aegypti , 1996, Medical and veterinary entomology.

[120]  G. Felton,et al.  Antioxidant systems in insects. , 1995, Archives of insect biochemistry and physiology.

[121]  J. H. Porter,et al.  The potential effects of climatic change on agricultural insect pests , 1991 .

[122]  Richard K. Koehn,et al.  Towards a physiological and genetical understanding of the energetics of the stress response , 1989 .

[123]  R. ffrench-Constant,et al.  Changes in DNA methylation are associated with loss of insecticide resistance in the peach‐potato aphid Myzus persicae (Sulz.) , 1989 .