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Transgenerational hormesis effects of nitenpyram on fitness and insecticide tolerance/resistance of Nilaparvata lugens

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Abstract

Brown planthopper (Nilaparvata lugens) (BPH) is a devastating migratory rice pest in tropical, subtropical, and temperate regions. Insecticide-induced population resurgence is a concern for BPH control. Exposure to low/sublethal concentrations of insecticides has resulted in increased reproduction and fitness as well as insecticide tolerance in many insects. Nitenpyram, a neonicotinoid insecticide, has been frequently used in BPH control. In the present study, the transgenerational hormesis effects in terms of fitness-related traits and insecticide tolerance induced by low concentrations of nitenpyram were reported in both susceptible (S) and field-collected strains (F) of BPH, after exposure to their respective LC20 nitenpyram concentrations for six generations. Our findings stressed that chronic, multigenerational preconditioning of BPHs to LC20 nitenpyram not only increased the biological fitness (in terms of life table parameters and estimated population size), but also primed BPHs to be more tolerate/resistant to insecticides nitenpyram, imidacloprid and cycloxaprid. The upregulation of detoxification (CYP6ER1) and fecundity-related (vitellogenin) genes in both the LC20-preconditioned S and F strains (S-Sub6 and F-Sub6) might contribute to the increased insecticide tolerance and reproduction hormesis. These results support the hypothesis that BPH population outbreaks following multigenerational exposure to low concentrations of nitenpyram in field crops occur through increased reproduction and resistance development. Moreover, based on our results, sulfoxaflor and triflumezopyrim are proposed to be used in rotation with nitenpyram, imidacloprid or cycloxaprid to delay the development of tolerance/resistance in BPHs in paddy fields.

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All data analyzed during this study are included in this published article.

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Acknowledgements

We thank Dr. Jianhong Li of Huazhong Agricultural University for providing the S strain used in this study. We also thank Vicki Stewart (Texas A&M University-Commerce, Texas, 75428, United States) for copyediting the manuscript. This study was supported by a fund from National Natural Science Foundation of China (Grant No: 31801772). Finally, we express deeply gratitude to two reviewers of the manuscript for valuable comments and suggestions.

Funding

This work was funded by the National Natural Science Foundation of China (Grant No: 31801772).

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Correspondence to Youhui Gong or Maolin Hou.

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Communicated by Chris Cutler.

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Corresponding author: Correspondence to Youhui Gong or Maolin Hou.

The original online version of this article was revised: “the corresponding author’s symbol has been added”

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10340_2022_1494_MOESM1_ESM.tiff

Supplementary file 1: Fig. S1. Age-stage survival curve (sxj) of 6-generational LC20 nitenpyram-preconditioned strains (S-Sub6-Control and F-Sub6-Control) and their respective reference strains (SS-Control and FS-Control) (TIFF 3264 kb)

10340_2022_1494_MOESM2_ESM.tiff

Supplementary file 2: Fig. S2. Relative gene expression of CYP6ER1 in FS strain compared to a susceptible strain SS. The statistical data analysis was conducted using an independent-samples T Test (SPSS 20.0, *P < 0.05; **P < 0.01; ***P < 0.001) (TIFF 2892 kb)

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Gong, Y., Cheng, S., Desneux, N. et al. Transgenerational hormesis effects of nitenpyram on fitness and insecticide tolerance/resistance of Nilaparvata lugens. J Pest Sci 96, 161–180 (2023). https://doi.org/10.1007/s10340-022-01494-4

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  • DOI: https://doi.org/10.1007/s10340-022-01494-4

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