Abstract
Neonicotinoid insecticides (e.g., imidacloprid) are some of the most prevalent tools used to control hemipterans that attack soybean crops worldwide. However, the emergence of neonicotinoid-resistant strains of phytosuccivorous soybean pests, such as the Neotropical brown stink bug Euschistus heros, has posed a challenge to the sustainable use of these compounds. Here, we laboratory-selected two E. heros strains for imidacloprid resistance and evaluated the activity of detoxification enzymes (e.g., cytochrome P450, esterases and glutathione-S-transferases) as well as potential adaptive costs associated with resistance (e.g., in survival, fecundity and fertility) in both strains, while laboratory selection for 13 generations in a known imidacloprid-susceptible E. heros strain (ImiSusc) resulted in an imidacloprid-resistant strain (ImiLabSel) with a resistance ratio (RR) of 11.6; similar resistance levels (i.e., RR = 13.5) were also achieved in another imidacloprid-resistant strain, which was field-collected (ImiGoias) and laboratory-selected for only six generations (ImiRes). Regarding enzymatic activity, both resistant strains differed from the imidacloprid-susceptible strain only in the activity of cytochrome P450, where the ImiLabSel and ImiRes strains exhibited higher activity by 72.3% and 40.5%, respectively. Furthermore, severe fitness costs (reductions of 86% for ImiLabSel and 68.0% for ImiRes) were recorded in both imidacloprid-resistant strains. Collectively, our results showed that E. heros rapidly responded to laboratory selection for neonicotinoid resistance, with enhanced cytochrome P450 activity as the likely underlying mechanism, and that they exhibit associated fitness costs, which have direct implications for the management of this insect pest.
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References
Abbas N, Khan H, Shad SA (2015) Cross-resistance, stability, and fitness cost of resistance to imidacloprid in Musca domestica L., (Diptera: Muscidae). Parasitol Res 114:247–255. https://doi.org/10.1007/s00436-014-4186-0
Bacca T, Haddi K, Pineda M et al (2017) Pyrethroid resistance is associated with a kdr-type mutation (L1014F) in the potato tuber moth Tecia solanivora. Pest Manag Sci 73:397–403. https://doi.org/10.1002/ps.4414
Bass C, Carvalho RA, Oliphant L et al (2011a) Overexpression of a cytochrome P450 monooxygenase, CYP6ER1, is associated with resistance to imidacloprid in the brown planthopper, Nilaparvata lugens. Insect Mol Biol 20:763–773. https://doi.org/10.1111/j.1365-2583.2011.01105.x
Bass C, Puinean AM, Andrews M et al (2011b) Mutation of a nicotinic acetylcholine receptor β subunit is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. BMC Neurosci 12:51. https://doi.org/10.1186/1471-2202-12-51
Bass C, Denholm I, Williamson MS, Nauen R (2015) The global status of insect resistance to neonicotinoid insecticides. Pestic Biochem Physiol 121:78–87
Berticat C, Boquien G, Raymond M, Chevillon C (2002) Insecticide resistance genes induce a mating competition cost in Culex pipiens mosquitoes. Genet Res 79:41–47. https://doi.org/10.1017/s001667230100547x
Borges M, Laumann RA, Silva CCA, et al (2006) Metodologias de criação e manejo de colônias de percevejos da soja (Hemiptera-pentatomidae) para estudos de comportamento e ecologia química. Embrapa Recur Genéticos e Biotecnol Doc
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Brogdon WG, McAllister JC, Vulule J (1997) Heme peroxidase activity measured in single mosquitoes identifies individuals expressing an elevated oxidase for insecticide resistance. J Am Mosq Control Assoc 13:233–237
Clements J, Schoville S, Peterson N et al (2016a) Characterizing molecular mechanisms of imidacloprid resistance in select populations of Leptinotarsa decemlineata in the Central sands region of Wisconsin. PLoS ONE 11:e0147844. https://doi.org/10.1371/journal.pone.0147844
Clements J, Schoville S, Peterson N, et al (2016b) RNA interference of three up-regulated transcripts associated with insecticide resistance in an imidacloprid resistant population of Leptinotarsa decemlineata. Pestic Biochem Physiol. https://doi.org/10.1016/j.pestbp.2016.07.001
Corrêa AS, Pereira EJG, Cordeiro EMG et al (2011) Insecticide resistance, mixture potentiation and fitness in populations of the maize weevil (Sitophilus zeamais). Crop Prot 30:1655–1666. https://doi.org/10.1016/j.cropro.2011.08.022
Daborn P, Boundy S, Yen J et al (2001) DDT resistance in correlates with over-expression and confers cross-resistance to the neonicotinoid imidacloprid. Mol Genet Genomics 266:556–563. https://doi.org/10.1007/s004380100531
De Souza PV, Machado BR, Cristina Da Silva D et al (2014) Effect of resistance and trichome inducers on attraction of Euschistus heros (Hemiptera: Pentatomidae) to soybeans. Afr J Agric Res 9:889–894. https://doi.org/10.5897/ajar2013.8030
Ding Z, Wen Y, Yang B et al (2013) Biochemical mechanisms of imidacloprid resistance in Nilaparvata lugens: over-expression of cytochrome P450 CYP6AY1. Insect Biochem Mol Biol 43:1021–1027. https://doi.org/10.1016/j.ibmb.2013.08.005
Foster SP, Denholm I, Thompson R (2003a) Variation in response to neonicotinoid insecticides in peach-potato aphids, Myzus persicae (Hemiptera: Aphididae). Pest Manag Sci 59:166–173. https://doi.org/10.1002/ps.570
Foster SP, Young S, Williamson MS et al (2003b) Analogous pleiotropic effects of insecticide resistance genotypes in peach-potato aphids and houseflies. Heredity (Edinb) 91:98–106. https://doi.org/10.1038/sj.hdy.6800285
Foster SP, Tomiczek M, Thompson R et al (2007) Behavioural side-effects of insecticide resistance in aphids increase their vulnerability to parasitoid attack. Anim Behav 74:621–632. https://doi.org/10.1016/j.anbehav.2006.12.018
Gonzales Correa YDC, Faroni LRA, Haddi K et al (2015) Locomotory and physiological responses induced by clove and cinnamon essential oils in the maize weevil Sitophilus zeamais. Pestic Biochem Physiol 125:31–37. https://doi.org/10.1016/j.pestbp.2015.06.005
Guedes RNC (2017) Insecticide resistance, control failure likelihood and the first law of geography. Pest Manag Sci 73:479–484. https://doi.org/10.1002/ps.4452
Guedes RNC, Oliveira EE, Guedes NMP et al (2006) Cost and mitigation of insecticide resistance in the maize weevil, Sitophilus zeamais. Physiol Entomol 31:30–38. https://doi.org/10.1111/j.1365-3032.2005.00479.x
Guedes RNC, Smagghe G, Stark JD, Desneux N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu Rev Entomol 61:43–62. https://doi.org/10.1146/annurev-ento-010715-023646
Guedes RNC, Walse SS, Throne JE (2017) Sublethal exposure, insecticide resistance, and community stress. Curr Opin Insect Sci 21:47–53
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139
Haddi K, Mendonca LP, Dos Santos MF et al (2015) Metabolic and behavioral mechanisms of indoxacarb resistance in Sitophilus zeamais (Coleoptera: Curculionidae). J Econ Entomol 108:362–369. https://doi.org/10.1093/jee/tou049
Haddi K, Mendes MV, Barcellos MS et al (2016) Sexual success after stress? Imidacloprid-induced hormesis in males of the Neotropical stink bug Euschistus heros. PLoS ONE 11:e0156616. https://doi.org/10.1371/journal.pone.0156616
Hardstone MC, Lazzaro BP, Scott JG (2009) The effect of three environmental conditions on the fitness of cytochrome P450 monooxygenase-mediated permethrin resistance in Culex pipiens quinquefasciatus. BMC Evol Biol 9:42. https://doi.org/10.1186/1471-2148-9-42
Hegeto LA, Ronqui L, Lapenta AS, Albuquerque FA (2015) Identification and functional characterization of esterases in Euschistus heros (Hemiptera, pentatomidae) and their relationship with thiamethoxam and lambda-cyhalothrin. Genet Mol Res 14:11079–11088. https://doi.org/10.4238/2015.september.22.1
Hemingway J (1998) Techniques to detect insecticide resistance mechanisms (field and laboratory manual). WHO/CDC/CPC/MAL/98.6, World Health Organization, Geneva
Højland DH, Vagn Jensen K-M, Kristensen M (2014) A comparative study of P450 gene expression in field and laboratory Musca domstica L. strains. Pest Manag Sci 70:1237–1242. https://doi.org/10.1002/ps.3681
Jeschke P, Nauen R (2008) Neonicotinoids-from zero to hero in insecticide chemistry. Pest Manag Sci 64:1084–1098. https://doi.org/10.1002/ps.1631
Karatolos N, Pauchet Y, Wilkinson P et al (2011) Pyrosequencing the transcriptome of the greenhouse whitefly, Trialeurodes vaporariorum reveals multiple transcripts encoding insecticide targets and detoxifying enzymes. BMC Genom 12:56. https://doi.org/10.1186/1471-2164-12-56
Karunker I, Morou E, Nikou D et al (2009) Structural model and functional characterization of the Bemisia tabaci CYP6CM1vQ, a cytochrome P450 associated with high levels of imidacloprid resistance. Insect Biochem Mol Biol 39:697–706. https://doi.org/10.1016/j.ibmb.2009.08.006
Khan HAA, Akram W, Iqbal J, Naeem-Ullah U (2015) Thiamethoxam resistance in the house fly, Musca domestica L.: current status, resistance selection, cross-resistance potential and possible biochemical mechanisms. PLoS One 10:e0125850. https://doi.org/10.1371/journal.pone.0125850
Kliot A, Ghanim M (2012) Fitness costs associated with insecticide resistance. Pest Manag Sci 68:1431–1437. https://doi.org/10.1002/ps.3395
Lind RJ, Clough MS, Reynolds SE, Earley FGP (1998) [3H]Imidacloprid labels high- and low-affinity nicotinic acetylcholine receptor-like binding sites in the aphid Myzus persicae (Hemiptera: Aphididae). Pestic Biochem Physiol 62:3–14. https://doi.org/10.1006/pest.1998.2364
Liu Z, Han Z (2006) Fitness costs of laboratory-selected imidacloprid resistance in the brown planthopper, Nilaparvata lugens Stål. Pest Manag Sci 62:279–282. https://doi.org/10.1002/ps.1169
Liu Z, Williamson MS, Lansdell SJ et al (2005) A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (brown planthopper). Proc Natl Acad Sci U S A 102:8420–8425. https://doi.org/10.1073/pnas.0502901102
Macfadyen S, Hardie DC, Fagan L et al (2014) Reducing insecticide use in broad-acre grains production: an Australian study. PLoS ONE 9:e89119. https://doi.org/10.1371/journal.pone.0089119
Nauen R, Denholm I (2005) Resistance of insect pests to neonicotinoid insecticides: current status and future prospects. Arch Insect Biochem Physiol 58:200–215. https://doi.org/10.1002/arch.20043
Naveen NC, Chaubey R, Kumar D et al (2017) Insecticide resistance status in the whitefly, Bemisia tabaci genetic groups Asia-I, Asia-II-1 and Asia-II-7 on the Indian subcontinent. Sci Rep 7:40634. https://doi.org/10.1038/srep40634
Oliveira EE, Pippow A, Salgado VL et al (2010) Cholinergic currents in leg motoneurons of Carausius morosus. J Neurophysiol 103:2770–2782
Oliveira EE, Schleicher S, Büschges A et al (2011) Desensitization of nicotinic acetylcholine receptors in central nervous system neurons of the stick insect (Carausius morosus) by imidacloprid and sulfoximine insecticides. Insect Biochem Mol Biol 41:872–880
Panizzi AR, Vivan LM (1997) Seasonal abundance of the neotropical brown stink bug, Euschistus heros, in overwintering sites, and the breaking of dormancy. Entomol Exp Appl 82:213–217. https://doi.org/10.1046/j.1570-7458.1997.00132.x
Panizzi AR, Bueno AF, Silva FAC (2012) Insetos que atacam vagens e grãos. Hoffman-Campo, CB; al Soja manejo Integr pragas e outros Artrópodes-pragas Brasília EMBRAPA 335–420
Pereira CJ, Pereira EJG, Cordeiro EMG et al (2009) Organophosphate resistance in the maize weevil Sitophilus zeamais: magnitude and behavior. Crop Prot 28:168–173. https://doi.org/10.1016/j.cropro.2008.10.001
Puinean AM, Foster SP, Oliphant L et al (2010) Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. PLoS Genet 6:1–11. https://doi.org/10.1371/journal.pgen.1000999
Rinkevich FD, Leichter CA, Lazo TA et al (2013) Variable fitness costs for pyrethroid resistance alleles in the house fly, Musca domestica, in the absence of insecticide pressure. Pestic Biochem Physiol 105:161–168. https://doi.org/10.1016/j.pestbp.2013.01.006
Robertson JL, Savin NE, Russell RM, Preisler HK (2007) Bioassays with arthropods, second edition, 2nd edn. Taylor & Francis Group, Boca Raton
Roush RT, McKenzie JA (1987) Ecological genetics of insecticide and acaricide resistance. Annu Rev Entomol 32:361–380. https://doi.org/10.1146/annurev.en.32.010187.002045
Salgado VL (2016) Antagonist pharmacology of desensitizing and non-desensitizing nicotinic acetylcholine receptors in cockroach neurons. Neurotoxicology 56:188–195. https://doi.org/10.1016/j.neuro.2016.08.003
Salgado VL, Saar R (2004) Desensitizing and non-desensitizing subtypes of alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors in cockroach neurons. J Insect Physiol 50:867–879. https://doi.org/10.1016/j.jinsphys.2004.07.007
Santos MF, Santos RL, Tomé HVV et al (2015) Imidacloprid-mediated effects on survival and fertility of the Neotropical brown stink bug Euschistus heros. J Pest Sci 89:1–10. https://doi.org/10.1007/s10340-015-0666-y
Santos MF, Campos MR, Bravim JN et al (2016) Non-targeted insecticidal stress on the Neotropical brown stink bug Euschistus heros. Crop Prot 82:10–16. https://doi.org/10.1016/j.cropro.2015.12.023
Seraydar KR, Kaufman PE (2015) Does behaviour play a role in house fly resistance to imidacloprid-containing baits? Med Vet Entomol 29:60–67. https://doi.org/10.1111/mve.12095
Snodgrass GL, Adamczyk JJ, Gore J (2005) Toxicity of insecticides in a glass-vial bioassay to adult brown, green, and southern green stink bugs (Heteroptera: Pentatomidae). J Econ Entomol 98:177–181
Sosa-Gómez DR, Omoto C (2012) Resistência a inseticidas e outros agentes de controle em artrópodes associados à cultura da soja. Hoffmann-Campo, CB, Corrêa-Ferreira, BS, Moscardi, F Soja manejo Integr insetos e outros artrópodes-praga Embrapa
Sosa-Gómez DR, Silva JJ (2010) Neotropical brown stink bug (Euschistus heros) resistance to methamidophos in Paraná, Brazil. Pesqui Agropecuária Bras 45:767–769
Sosa-Gomez DR, Corso IC, Morales L (2001) Insecticide resistance to endosulfan, monocrotophos and metamidophos in the neotropical brown stink bug, Euschistus heros (F.). Neotrop Entomol 30:317–320
Sosa-Gomez DR, Delpin KE, Almeida AMR, Hirose E (2004) Genetic differentiation among Brazilian populations of Euschistus heros (Fabricius) (Heteroptera: Pentatomidae) based on RAPD analysis. Neotrop Entomol 33:179–187. 26 ref. doi: http://dx.doi.org/10.1590/S1519-566X2004000200009
Tomizawa M, Casida JE (2005) Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol 45:247–268
Tuelher ES, Silva ÉH, Hirose E et al (2016) Competition between the phytophagous stink bugs Euschistus heros and Piezodorus guildinii in soybeans. Pest Manag Sci 72:1837–1843. https://doi.org/10.1002/ps.4306
Tuelher ES, da Silva ÉH, Freitas HL et al (2017) Chlorantraniliprole-mediated toxicity and changes in sexual fitness of the Neotropical brown stink bug Euschistus heros. J Pest Sci 90:397–405. https://doi.org/10.1007/s10340-016-0777-0
Tuelher ES, da Silva ÉH, Rodrigues HS et al (2018) Area-wide spatial survey of the likelihood of insecticide control failure in the neotropical brown stink bug Euschistus heros. J Pest Sci 91:849–859. https://doi.org/10.1007/s10340-017-0949-6
van Asperen K (1962) A study of housefly esterases by means of a sensitive colorimetric method. J Insect Physiol 8:401–416. https://doi.org/10.1016/0022-1910(62)90074-4
Wang YH, Wu SG, Zhu YC et al (2009) Dynamics of imidacloprid resistance and cross-resistance in the brown planthopper, Nilaparvata lugens. Entomol Exp Appl 131:20–29. https://doi.org/10.1111/j.1570-7458.2009.00827.x
Willrich MM, Leonard BR, Cook DR (2003) Laboratory and field evaluations of insecticide toxicity to stink bugs (Heteroptera: Pentatomidae). J Cotton Sci
Yang N, Xie W, Jones CM et al (2013a) Transcriptome profiling of the whitefly Bemisia tabaci reveals stage-specific gene expression signatures for thiamethoxam resistance. Insect Mol Biol 22:485–496. https://doi.org/10.1111/imb.12038
Yang N, Xie W, Yang X et al (2013b) Transcriptomic and proteomic responses of sweetpotato whitefly, Bemisia tabaci, to thiamethoxam. PLoS ONE 8:e61820. https://doi.org/10.1371/journal.pone.0061820
Yang X, Xie W, Wang SL et al (2013c) Two cytochrome P450 genes are involved in imidacloprid resistance in field populations of the whitefly, Bemisia tabaci, in China. Pestic Biochem Physiol 107:343–350. https://doi.org/10.1016/j.pestbp.2013.10.002
Yang Y, Huang L, Wang Y et al (2016) No cross-resistance between imidacloprid and pymetrozine in the brown planthopper: status and mechanisms. Pestic Biochem Physiol 130:79–83. https://doi.org/10.1016/j.pestbp.2015.11.007
Yang Z, Zhang Y, Liu X, Wang X (2017) Two novel cytochrome P450 genes CYP6CS1 and CYP6CW1 from Nilaparvata lugens (Hemiptera: Delphacidae): cDNA cloning and induction by host resistant rice. https://doi.org/10.1017/s0007485310000192
Zhang Y, Wang X, Yang B et al (2015) Reduction in mRNA and protein expression of a nicotinic acetylcholine receptor α8 subunit is associated with resistance to imidacloprid in the brown planthopper, Nilaparvata lugens. J Neurochem 135:686–694. https://doi.org/10.1111/jnc.13281
Zhang J, Zhang Y, Wang Y et al (2016a) Expression induction of P450 genes by imidacloprid in Nilaparvata lugens: a genome-scale analysis. Pestic Biochem Physiol 132:59–64. https://doi.org/10.1016/j.pestbp.2015.10.016
Zhang Y, Yang Y, Sun H, Liu Z (2016b) Metabolic imidacloprid resistance in the brown planthopper, Nilaparvata lugens, relies on multiple P450 enzymes. Insect Biochem Mol Biol 79:50–56. https://doi.org/10.1016/j.ibmb.2016.10.009
Zhu YC, Luttrell R (2015) Altered gene regulation and potential association with metabolic resistance development to imidacloprid in the tarnished plant bug, Lygus lineolaris. Pest Manag Sci 71:40–57. https://doi.org/10.1002/ps.3761
Acknowledgements
The provision of stock colonies of E. heros by Dr. R. Laumann (EMBRAPA Genetic Resources and Biotechnology, Brasília, DF, Brazil) was greatly appreciated. This work was supported by grants from the CAPES Foundation, the National Council of Scientific and Technological Development (CNPq), the Goiás State Research Foundation (FAPEG), the Minas Gerais State Foundation for Research Aid (FAPEMIG) and the Special Research Fund (BOF) of Ghent University (Belgium).
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Castellanos, N.L., Haddi, K., Carvalho, G.A. et al. Imidacloprid resistance in the Neotropical brown stink bug Euschistus heros: selection and fitness costs. J Pest Sci 92, 847–860 (2019). https://doi.org/10.1007/s10340-018-1048-z
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DOI: https://doi.org/10.1007/s10340-018-1048-z