{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T16:41:47Z","timestamp":1787330507360,"version":"build-2736575974"},"reference-count":44,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T00:00:00Z","timestamp":1787270400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Major Special Projects for Green Pest Control of CNTC","award":["110202401012(LS-02)"],"award-info":[{"award-number":["110202401012(LS-02)"]}]},{"name":"Major Special Projects for Green Pest Control of CNTC","award":["110202401017(LS-07)"],"award-info":[{"award-number":["110202401017(LS-07)"]}]},{"name":"Agricultural Science and Technology Innovation Program of CAAS","award":["ASTIP-TRIC04"],"award-info":[{"award-number":["ASTIP-TRIC04"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Insects"],"abstract":"<jats:p>The cotton bollworm Helicoverpa armigera (H\u00fcbner, 1808) (Lepidoptera: Noctuidae) is a globally distributed polyphagous pest that damages various crops. Pesticides remain a primary and effective strategy for controlling cotton bollworm populations. This study evaluated the effects of broflanilide on H. armigera by integrating life-table analysis, detoxification enzyme activity assays, and gut microbiome characterization. Broflanilide showed high toxicity against third-instar larvae. Parental LC50 exposure prolonged larval development and reduced larval survival in the F1 generation. In addition, parental exposure to both LC30 and LC50 reduced adult emergence, fecundity and major population growth parameters, especially the intrinsic rate of increase (r) and net reproductive rate (R0), demonstrating a significant transgenerational inhibitory effect. Enzyme assays showed that carboxylesterase (CarE) activity was induced after broflanilide exposure, glutathione S-transferase (GST) activity showed a time-dependent response with the strongest induction generally observed under LC10 treatment, whereas cytochrome P450 monooxygenase (P450) activity was generally inhibited. Gut microbiota analysis showed that LC50 exposure significantly reduced the relative abundance of Enterococcus. Functional prediction further indicated enrichment trends in pathways related to xenobiotic degradation and metabolism. Overall, broflanilide not only exhibited strong lethal activity against H. armigera, but also produced sustained effects on population fitness, detoxification metabolism and gut microbial ecology. These findings provide a theoretical basis for the rational use of broflanilide and improve our understanding of its sublethal physiological and microbial effects on H. armigera.<\/jats:p>","DOI":"10.3390\/insects17080878","type":"journal-article","created":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T15:51:05Z","timestamp":1787327465000},"page":"878","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Parental Broflanilide Exposure Impairs Offspring Fitness and Alters Detoxification Enzymes and Gut Microbiota in Helicoverpa armigera"],"prefix":"10.3390","volume":"17","author":[{"given":"Xue","family":"Gao","sequence":"first","affiliation":[{"name":"Key Laboratory of Tobacco Pest Monitoring Controlling & Integrated Management, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qihui","family":"Li","sequence":"additional","affiliation":[{"name":"Key Laboratory of Tobacco Pest Monitoring Controlling & Integrated Management, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fangfang","family":"Yan","sequence":"additional","affiliation":[{"name":"Panzhihua Branch of Sichuan Tobacco Company, Panzhihua 617026, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chenyu","family":"Su","sequence":"additional","affiliation":[{"name":"Key Laboratory of Tobacco Pest Monitoring Controlling & Integrated Management, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiufang","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Tobacco Pest Monitoring Controlling & Integrated Management, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2020-1435","authenticated-orcid":false,"given":"Pengjun","family":"Xu","sequence":"additional","affiliation":[{"name":"Key Laboratory of Tobacco Pest Monitoring Controlling & Integrated Management, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0009-5361-0623","authenticated-orcid":false,"given":"Guangwei","family":"Ren","sequence":"additional","affiliation":[{"name":"Key Laboratory of Tobacco Pest Monitoring Controlling & Integrated Management, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Min","family":"Mao","sequence":"additional","affiliation":[{"name":"Panzhihua Branch of Sichuan Tobacco Company, Panzhihua 617026, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,8,21]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1146\/annurev-ento-011118-111959","article-title":"Movement ecology of pest Helicoverpa: Implications for ongoing spread","volume":"64","author":"Jones","year":"2019","journal-title":"Annu. Rev. Entomol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1111\/jen.12880","article-title":"A review on biological interactions and management of the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae)","volume":"145","author":"Riaz","year":"2021","journal-title":"J. Appl. Entomol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"859","DOI":"10.1093\/jee\/toy409","article-title":"Resistance and synergism of novel insecticides in field populations of cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae) in Pakistan","volume":"112","author":"Ahmad","year":"2019","journal-title":"J. Econ. Entomol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1146\/annurev-ento-080421-071655","article-title":"Determinants of insecticide resistance evolution: Comparative analysis among Heliothines","volume":"67","author":"Walsh","year":"2022","journal-title":"Annu. Rev. Entomol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"5086","DOI":"10.1002\/ps.6548","article-title":"Field-evolved resistance to 11 insecticides and the mechanisms involved in Helicoverpa armigera (Lepidoptera: Noctuidae)","volume":"77","author":"Wang","year":"2021","journal-title":"Pest Manag. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"900","DOI":"10.1002\/ps.1960","article-title":"Multiple P450 genes overexpressed in deltamethrin-resistant strains of Helicoverpa armigera","volume":"66","author":"Hema","year":"2010","journal-title":"Pest Manag. Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"105542","DOI":"10.1016\/j.pestbp.2023.105542","article-title":"Absence of known knockdown resistance mutations but fixation of CYP337b3 was detected in field populations of Helicoverpa armigera across China","volume":"195","author":"Ni","year":"2023","journal-title":"Pest. Biochem. Physiol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Walsh, T.K., Joussen, N., Tian, K., McGaughran, A., Anderson, C.J., Qiu, X., Ahn, S.J., Bird, L., Pavlidi, N., and Vontas, J. (2018). Multiple recombination events between two cytochrome P450 loci contribute to global pyrethroid resistance in Helicoverpa armigera. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0197760"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1199","DOI":"10.1007\/s10340-023-01593-w","article-title":"Expanding risk predictions of pesticide resistance evolution in arthropod pests with a proxy for selection pressure","volume":"96","author":"Thia","year":"2023","journal-title":"J. Pest Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1016\/j.bmc.2015.08.008","article-title":"Broflanilide: A meta-diamide insecticide with a novel mode of action","volume":"24","author":"Nakao","year":"2016","journal-title":"Bioorg. Med. Chem."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.1002\/ps.6719","article-title":"Novel meta-diamide insecticide, broflanilide, suppresses the population of common cutworm Spodoptera litura through its lethal and sublethal effects","volume":"78","author":"Shen","year":"2022","journal-title":"Pest Manag. Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1118","DOI":"10.1111\/1744-7917.13142","article-title":"Baseline susceptibility of Helicoverpa armigera, Plutella xylostella, and Spodoptera frugiperda to the meta-diamide insecticide broflanilide","volume":"30","author":"Wang","year":"2023","journal-title":"Insect Sci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.cotox.2022.02.001","article-title":"Pesticide-induced hormesis in arthropods: Towards biological systems","volume":"29","author":"Guedes","year":"2022","journal-title":"Curr. Opin. Toxicol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"154085","DOI":"10.1016\/j.scitotenv.2022.154085","article-title":"Review of molecular and biochemical responses during stress induced stimulation and hormesis in insects","volume":"827","author":"Rix","year":"2022","journal-title":"Sci. Total Environ."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1146\/annurev.ento.52.110405.091440","article-title":"The sublethal effects of pesticides on beneficial arthropods","volume":"52","author":"Desneux","year":"2007","journal-title":"Annu. Rev. Entomol."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Ye, M., Nayak, B., Xiong, L., Xie, C., Dong, Y., You, M., Yuchi, Z., and You, S. (2022). The role of insect cytochrome P450s in mediating insecticide resistance. Agriculture, 12.","DOI":"10.3390\/agriculture12010053"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1146\/annurev-ento-070621-061328","article-title":"The role of cytochrome P450s in insect toxicology and resistance","volume":"67","author":"Nauen","year":"2022","journal-title":"Annu. Rev. Entomol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1186\/s40168-020-00823-y","article-title":"Most dominant roles of insect gut bacteria: Digestion, detoxification, or essential nutrient provision?","volume":"8","author":"Jing","year":"2020","journal-title":"Microbiome"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1111\/1574-6976.12025","article-title":"The gut microbiota of insects-diversity in structure and function","volume":"37","author":"Engel","year":"2013","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"6432","DOI":"10.1038\/s41467-021-26649-2","article-title":"Insecticide resistance by a host-symbiont reciprocal detoxification","volume":"12","author":"Sato","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1016\/j.chom.2020.01.009","article-title":"Changes in microbiome confer multigenerational host resistance after sub-toxic pesticide exposure","volume":"27","author":"Wang","year":"2020","journal-title":"Cell Host Microbe"},{"key":"ref_22","unstructured":"Chen, W. (2025). Effects of Lambda-Cyhalothrin on CYP302a1 in Helicoverpa armigera and Construction of a dsRNA Nano-Delivery System. [Master\u2019s Thesis, Chinese Academy of Agricultural Sciences]."},{"key":"ref_23","first-page":"772","article-title":"Control efficacy of broflanilide against Helicoverpa armigera in tobacco fields and its impact on related enzyme","volume":"64","author":"Li","year":"2025","journal-title":"Agrochemicals"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1038\/nmeth.3869","article-title":"DADA2: High-resolution sample inference from illumina amplicon data","volume":"13","author":"Callahan","year":"2016","journal-title":"Nat. Methods"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1127\/entomologia\/2020\/0936","article-title":"Age-stage, two-sex life table: An introduction to theory, data analysis, and application","volume":"40","author":"Chi","year":"2020","journal-title":"Entomol. Gen."},{"key":"ref_26","first-page":"27663","article-title":"Analysis of composition of microbiomes: A novel method for studying microbial composition","volume":"26","author":"Mandal","year":"2015","journal-title":"Microb. Ecol. Health Dis."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"685","DOI":"10.1038\/s41587-020-0548-6","article-title":"PICRUSt2 for prediction of metagenome functions","volume":"38","author":"Douglas","year":"2020","journal-title":"Nat. Biotechnol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"852","DOI":"10.1038\/s41587-019-0209-9","article-title":"Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2","volume":"37","author":"Bolyen","year":"2019","journal-title":"Nat. Biotechnol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.cois.2017.12.007","article-title":"Transgenerational effects of insecticides-implications for rapid pest evolution in agroecosystems","volume":"26","author":"Brevik","year":"2018","journal-title":"Curr. Opin. Insect Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"106421","DOI":"10.1016\/j.cropro.2023.106421","article-title":"Sublethal and transgenerational effects of broflanilide on Myzus persicae (Sulzer) (Hemiptera: Aphididae)","volume":"174","author":"Zhang","year":"2023","journal-title":"Crop Prot."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1146\/annurev-ento-010715-023646","article-title":"Pesticide-induced stress in arthropod pests for optimized integrated pest management programs","volume":"61","author":"Guedes","year":"2016","journal-title":"Annu. Rev. Entomol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"106953","DOI":"10.1016\/j.cropro.2024.106953","article-title":"Sublethal and transgenerational effects of tetraniliprole on the tomato pinworm Phthorimaea (=Tuta) absoluta (Lepidoptera: Gelechiidae)","volume":"187","author":"Yao","year":"2025","journal-title":"Crop Prot."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1211","DOI":"10.1038\/s41598-025-30907-4","article-title":"Neonicotinoid-induced signature dysbiosis identified via metagenomic sequencing of the honey bee gut microbiome","volume":"16","author":"Tran","year":"2025","journal-title":"Sci. Rep."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.pestbp.2019.03.009","article-title":"Identification and biochemical characterization of carboxylesterase 001G associated with insecticide detoxification in Helicoverpa armigera","volume":"157","author":"Bai","year":"2019","journal-title":"Pest. Biochem. Physiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"5713","DOI":"10.7150\/ijbs.77141","article-title":"Functional and structural diversity of insect glutathione s-transferases in xenobiotic adaptation","volume":"18","author":"Koirala","year":"2022","journal-title":"Int. J. Biol. Sci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1146\/annurev-ento-010814-020828","article-title":"Insecticide resistance in mosquitoes: Impact, mechanisms, and research directions","volume":"60","author":"Liu","year":"2015","journal-title":"Annu. Rev. Entomol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"3390","DOI":"10.1021\/acs.jafc.9b06690","article-title":"Functional characterization of two carboxylesterase genes involved in pyrethroid detoxification in Helicoverpa armigera","volume":"68","author":"Li","year":"2020","journal-title":"J. Agric. Food. Chem."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Zhang, Y., Huang, Q., Sheng, C., Liu, G., Zhang, K., Jia, Z., Tang, T., Mao, X., Jones, A.K., and Han, Z. (2023). G3\u2019M TMD3 in the insect GABA receptor subunit, RDL, confers resistance to broflanilide and fluralaner. PLoS Genet., 19.","DOI":"10.1371\/journal.pgen.1010814"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1007\/s10482-024-01970-0","article-title":"The role of insect gut microbiota in host fitness, detoxification and nutrient supplementation","volume":"117","author":"Shamjana","year":"2024","journal-title":"Antonie Van Leeuwenhoek"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Siddiqui, J.A., Khan, M.M., Bamisile, B.S., Hafeez, M., Qasim, M., Rasheed, M.T., Rasheed, M.A., Ahmad, S., Shahid, M.I., and Xu, Y. (2022). Role of insect gut microbiota in pesticide degradation: A review. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.870462"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Jaffar, S., Ahmad, S., and Lu, Y. (2022). Contribution of insect gut microbiota and their associated enzymes in insect physiology and biodegradation of pesticides. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.979383"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Xia, X., Gurr, G.M., Vasseur, L., Zheng, D., Zhong, H., Qin, B., Lin, J., Wang, Y., Song, F., and Li, Y. (2017). Metagenomic sequencing of diamondback moth gut microbiome unveils key holobiont adaptations for herbivory. Front. Microbiol., 8.","DOI":"10.3389\/fmicb.2017.00663"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"8618","DOI":"10.1073\/pnas.1200231109","article-title":"Symbiont-mediated insecticide resistance","volume":"109","author":"Kikuchi","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1039\/C7NP00051K","article-title":"Detoxifying symbiosis: Microbe-mediated detoxification of phytotoxins and pesticides in insects","volume":"35","author":"Itoh","year":"2018","journal-title":"Nat. Prod. Rep."}],"container-title":["Insects"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4450\/17\/8\/878\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T16:09:54Z","timestamp":1787328594000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4450\/17\/8\/878"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,21]]},"references-count":44,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2026,8]]}},"alternative-id":["insects17080878"],"URL":"https:\/\/doi.org\/10.3390\/insects17080878","relation":{},"ISSN":["2075-4450"],"issn-type":[{"value":"2075-4450","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,21]]}}}