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Assessing fitness costs of the resistance of Spodoptera frugiperda (Lepidoptera: Noctuidae) to pyramided Cry1 and Cry2 insecticidal proteins on different host plants

Published online by Cambridge University Press:  12 January 2022

Cínthia G. Garlet ,
Dionei S. Muraro ,
Daniela N. Godoy ,
Gisele E. Cossa ,
Manoela R. Hanich ,
Regis F. Stacke  and
Oderlei Bernardi Open the ORCID record for Oderlei Bernardi [Opens in a new window]
Cínthia G. Garlet
Affiliation:
Department of Plant Protection, Federal University of Santa Maria, Roraima avenue 1000, Santa Maria, Rio Grande do Sul 97105-900, Brazil
Dionei S. Muraro
Affiliation:
Department of Entomology and Acarology, University of São Paulo, Padua Dias avenue, 11, Piracicaba, São Paulo 13418-900, Brazil
Daniela N. Godoy
Affiliation:
Department of Plant Protection, Federal University of Santa Maria, Roraima avenue 1000, Santa Maria, Rio Grande do Sul 97105-900, Brazil
Gisele E. Cossa
Affiliation:
Department of Plant Protection, Federal University of Santa Maria, Roraima avenue 1000, Santa Maria, Rio Grande do Sul 97105-900, Brazil
Manoela R. Hanich
Affiliation:
Department of Plant Protection, Federal University of Santa Maria, Roraima avenue 1000, Santa Maria, Rio Grande do Sul 97105-900, Brazil
Regis F. Stacke
Affiliation:
Department of Plant Protection, Federal University of Santa Maria, Roraima avenue 1000, Santa Maria, Rio Grande do Sul 97105-900, Brazil
Oderlei Bernardi*
Affiliation:
Department of Plant Protection, Federal University of Santa Maria, Roraima avenue 1000, Santa Maria, Rio Grande do Sul 97105-900, Brazil
*
Author for correspondence: Oderlei Bernardi, Email: oderlei.bernardi@ufsm.br
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Abstract

Fall armyworm (FAW), Spodoptera frugiperda (Smith), is one of the major pests targeted by transgenic crops expressing insecticidal proteins from Bacillus thuringiensis (Bt) Berliner. However, FAW presents a high capacity to develop resistance to Bt protein-expressing crop lines, as reported in Brazil, Argentina, Puerto Rico and the southeastern U.S. Here, FAW genotypes resistant to pyramided maize events expressing Cry1F/Cry1A.105/Cry2Ab2 (P-R genotype) and Cry1A.105/Cry2Ab2 (Y-R genotype) from Brazil were used to investigate the interactions between non-Bt hosts (non-Bt maize, non-Bt cotton, millet and sorghum) and fitness costs. We also tested a FAW genotype susceptible to Bt maize and F1 hybrids of the resistant and susceptible genotypes (heterozygotes). Recessive fitness costs (i.e., costs affecting the resistant insects) were observed for pupal and neonate to adult survival of the P-R genotype on non-Bt cotton; larval developmental time of the P-R genotype on millet and sorghum; larval and neonate-to-adult developmental time of the Y-R genotype on non-Bt cotton and sorghum; the fecundity of the Y-R genotype on non-Bt cotton; and mean generation time of both resistant genotypes. However, on non-Bt cotton and non-Bt maize, the P-R genotype had a higher fitness (i.e., fitness benefits), displaying greater fecundity and rates of population increases than the Sus genotype. Non-recessive fitness costs (i.e., costs affecting heterozygotes) were found for fecundity and population increases on millet and sorghum. These findings suggest that, regardless of the disadvantages of the resistant genotypes in some hosts, the resistance of FAW to Cry1 and Cry2 Bt proteins is not linked with substantial fitness costs, and may persist in field conditions once present.

Keywords

Bt maizefall armywormpopulation growth parametersresistance management
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 5 , October 2022 , pp. 575 - 583
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Andow, DA and Alstad, DN (1998) F2 screen for rare resistance alleles. Journal of Economic Entomology 91, 572–578.CrossRefGoogle Scholar
Bernardi, D, Salmeron, E, Horikoshi, RJ, Bernardi, O, Dourado, PM, Carvalho, RA, Martinelli, S, Head, GP and Omoto, C (2015) Cross-resistance between Cry1 proteins in fall armyworm (Spodoptera frugiperda) may affect the durability of current pyramided Bt maize hybrids in Brazil. PLoS One 10, e0140130.CrossRefGoogle ScholarPubMed
Bernardi, O, Bernardi, D, Horikoshi, RJ, Okuma, DM, Miraldo, LL, Fatoretto, J, Medeiros, FCL, Burd, T and Omoto, C (2016) Selection and characterization of resistance to the Vip3Aa20 protein from Bacillus thuringiensis in Spodoptera frugiperda. Pest Management Science 72, 1794–1802.CrossRefGoogle Scholar
Blanco, CA, Chiaravalle, C, Dalla-Rizza, M, Farias, JR, García-Degano, MF, Gataminza, G, Mota-Sánchez, D, Murua, MG, Omoto, C, Pieralise, BK, Rodríguez, J, Rodríguez-Maciel, JC, Terán-Santofímioet, H, Terán-Vargas, AP, Valencia, JS and Willink, E (2016) Current situation of pests targeted by Bt crops in Latin America. Current Opinion in Insect Science 15, 131–138.CrossRefGoogle ScholarPubMed
Brookes, G and Barfoot, P (2017) Global income and production impacts of using GM crop technology 1996–2015. GM Crops Food 8, 156–193.CrossRefGoogle ScholarPubMed
Burtet, LM, Bernardi, O, Melo, AA, Pes, MP, Strahl, TT and Guedes, JVC (2017) Managing fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), with Bt maize and insecticides in southern Brazil. Pest Management Science 73, 2569–2577.CrossRefGoogle Scholar
Cao, G and Han, Z (2006) Tebufenozide resistance selected in Plutella xylostella and its cross-resistance and fitness cost. Pest Management Science 62, 746–751.CrossRefGoogle ScholarPubMed
Carpenter, JE (2010) Peer-reviewed surveys indicate positive impact of commercialized GM crops. Nature Biotechnology 28, 319–321.CrossRefGoogle ScholarPubMed
Carrière, Y, Ellers-Kirk, C, Biggs, R, Higginson, DM, Dennehy, TJ and Tabashnik, BE (2004) Effects of gossypol on fitness costs associated with resistance to Bt cotton in pink bollworm. Journal of Economic Entomology 97, 1710–1718.CrossRefGoogle ScholarPubMed
Carrière, Y, Ellers-Kirk, C, Hartfield, K, Larocque, G, Degain, B, Dutilleul, P, Marsh, SE, Crowder, DW, Li, X, Ellsworth, PC, Naranjo, SE, Palumbo, JC, Fournier, A, Antilla, L and Tabashnik, BE (2012) Large-scale, spatially-explicit test of the refuge strategy for delaying insecticide resistance. Proceedings of the National Academy of Sciences of the United States of America 109, 775–780.CrossRefGoogle ScholarPubMed
Cattaneo, MG, Yafuso, C, Schmidt, C, Huang, C, Rahman, M, Olson, C, Ellers-Kirk, C, Orr, BJ, Marsh, SE, Antilla, L, Dutilleul, P and Carrière, Y (2006) Farm-scale evaluation of the impacts of transgenic cotton on biodiversity, pesticide use and yield. Proceedings of the National Academy of Sciences of the United States of America 103, 7571–7576.CrossRefGoogle ScholarPubMed
Chandrasena, DI, Signorini, AM, Abratti, G, Storer, NP, Olaciregui, ML, Alves, AP and Pilcher, CD (2018) Characterization of field-evolved resistance to Bacillus thuringiensis-derived Cry1F δ-endotoxin in Spodoptera frugiperda populations from Argentina. Pest Management Science 74, 746–754.CrossRefGoogle ScholarPubMed
Chen, X, Head, GP, Price, P, Kerns, DL, Rice, ME, Huang, F, Gilreath, RT and Yang, F (2019) Fitness costs of Vip3A resistance in Spodoptera frugiperda on different hosts. Pest Management Science 75, 1074–1080.CrossRefGoogle ScholarPubMed
Dangal, V and Huang, F (2015) Fitness costs of Cry1F resistance in two populations of fall armyworm, Spodoptera frugiperda (J.E. Smith), collected from Puerto Rico and Florida. Journal of Invertebrate Pathology 127, 81–86.CrossRefGoogle Scholar
Farias, JR, Andow, DA, Horikoshi, RJ, Sorgatto, RJ, Fresia, P, Santos, AC and Omoto, C (2014 a) Field-evolved resistance to Cry1F maize by Spodoptera frugiperda (Lepidoptera: Noctuidae) in Brazil. Crop Protection 64, 150–158.CrossRefGoogle Scholar
Farias, JR, Horikoshi, RJ, Santos, AC and Omoto, C (2014 b) Geographical and temporal variability in susceptibility to Cry1F toxin from Bacillus thuringiensis in Spodoptera frugiperda (Lepidoptera: Noctuidae) populations in Brazil. Journal of Economic Entomology 107, 2182–2189.CrossRefGoogle ScholarPubMed
Favetti, BM, Braga-Santos, TL, Massarolli, A, Specht, A and Butnariu, AR (2017) Pearl millet: a green bridge for lepidopteran pests. Journal of Agricultural Science 9, 6.CrossRefGoogle Scholar
Gassmann, AJ, Carrière, Y and Tabashnik, BE (2009) Fitness costs of insect resistance to Bacillus thuringiensis. Annual Review of Entomology 54, 147–163.CrossRefGoogle ScholarPubMed
Gould, F (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology 43, 701–726.CrossRefGoogle ScholarPubMed
Greene, DF, Leppla, NC and Dickerson, WA (1976) Velvetbean caterpillar: a rearing procedure and artificial medium. Journal of Economic Entomology 69, 488–497.CrossRefGoogle Scholar
Hernández-Rodríguez, CS, Hernandez-Martinez, P, Van Rie, J, Escriche, B and Ferré, J (2013) Shared midgut binding sites for Cry1A. 105, Cry1Aa, Cry1Ab, Cry1Ac and Cry1Fa proteins from Bacillus thuringiensis in two important corn pests, Ostrinia nubilalis and Spodoptera frugiperda. PLoS One 8, e68164.CrossRefGoogle ScholarPubMed
Horikoshi, RJ, Bernardi, D, Bernardi, O, Malaquias, JB, Okuma, DM, Miraldo, LL, Amaral, FSDA and Omoto, C (2016 a) Effective dominance of resistance of Spodoptera frugiperda to Bt maize and cotton varieties: implications for resistance management. Scientific Reports 6, 34864.CrossRefGoogle ScholarPubMed
Horikoshi, RJ, Bernardi, O, Bernardi, D, Okuma, DM, Farias, JR, Miraldo, LL, Amaral, FSA and Omoto, C (2016 b) Near-isogenic Cry1F-resistant strain of Spodoptera frugiperda (Lepidoptera: Noctuidae) to investigate fitness cost associated with resistance in Brazil. Journal of Economic Entomology 109, 854–859.CrossRefGoogle ScholarPubMed
Huang, F (2021) Dominance and fitness costs of insect resistance to genetically modified Bacillus thuringiensis crops. GM Crops & Food 12, 192–211.CrossRefGoogle ScholarPubMed
Huang, F, Qureshi, JA, Meagher, RL Jr., Reisig, DD, Head, GP, Andow, DA, Ni, X, Kerns, D, Buntin, GD, Niu, Y, Yang, F and Dangal, V (2014) Cry1F resistance in fall armyworm Spodoptera frugiperda: single gene versus pyramided Bt maize. PLoS One 9, e112958.CrossRefGoogle ScholarPubMed
Jakka, SRK, Knight, VR and Jurat-Fuentes, JL (2014) Fitness costs associated with field-evolved resistance to Bt maize in Spodoptera frugiperda (Lepidoptera: Noctuidae). Journal of Economic Entomology 107, 342–351.CrossRefGoogle Scholar
Janmaat, AF and Myers, JH (2005) The cost of resistance to Bacillus thuringiensis varies with the host plant of Trichoplusia ni. Proceedings of the Royal Society B: Biological Sciences 272, 1031–1038.CrossRefGoogle ScholarPubMed
Lu, YH, Wu, KM, Jiang, YY, Guo, YY and Desneux, N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487, 362–365.CrossRefGoogle ScholarPubMed
Machado, EP, Rodrigues Junior, GLS, Führ, FM, Zago, SL, Marques, LH, Santos, AC, Nowatzki, T, Dahmer, ML, Omoto, C and Bernardi, O (2020) Cross-crop resistance of Spodoptera frugiperda selected on Bt maize to genetically-modified soybean expressing Cry1Ac and Cry1F proteins in Brazil. Scientific Reports 10, 10080.CrossRefGoogle ScholarPubMed
Maia, HNM, Luiz, AJB and Campanhola, C (2000) Statistical inference on associated fertility life table parameters using jackknife technique: computational aspects. Journal of Economic Entomology 93, 511–518.CrossRefGoogle Scholar
Muraro, DS, Garlet, CG, Godoy, DN, Cossa, GE, Rodrigues Junior, GLS, Stacke, RF, Medeiros, SLP, Guedes, JVC and Bernardi, O (2019) Laboratory and field survival of Spodoptera frugiperda (Lepidoptera: Noctuidae) on Bt and non-Bt maize and its susceptibility to insecticides. Pest Management Science 75, 2202–2210.CrossRefGoogle ScholarPubMed
Muraro, DS, Stacke, RF, Cossa, GE, Godoy, DN, Garlet, CG, Vamorbida, I, O'Neal, ME and Bernardi, O (2020) Performance of seed treatments applied on Bt and non-Bt maize against fall armyworm (Lepidoptera: Noctuidae). Environmental Entomology 49, 1137–1144.CrossRefGoogle Scholar
Niu, Y, Yang, F, Dangal, V and Huang, F (2014) Larval survival and plant injury of Cry1F-susceptible, -resistant, and -heterozygous fall armyworm (Lepidoptera: Noctuidae) on non-Bt and Bt corn containing single or pyramided genes. Crop Protection 59, 22–28.CrossRefGoogle Scholar
Niu, Y, Head, GP, Price, PA and Huang, F (2017) Inheritance and fitness costs of Cry1A.105 resistances in two strains of Spodoptera frugiperda (J. E. Smith). Crop Protection 110, 229–235.CrossRefGoogle Scholar
Oliveira, CES, Silva, CS, Zoz, T, Zoz, A, Andrade, AF and Witt, TW (2019) Feeding preference of Spodoptera frugiperda on different sorghum genotypes. Arquivos do Instituto Biológico 86, e0992018.CrossRefGoogle Scholar
Omoto, C, Bernardi, O, Salmeron, E, Sorgatto, JR, Dourado, MP, Crivellari, A, Carvalho, RA, Willse, A, Martinelli, S and Head, GP (2016) Field-evolved resistance to Cry1Ab maize by Spodoptera frugiperda in Brazil. Pest Management Science 72, 1727–1736.CrossRefGoogle ScholarPubMed
Raymond, B, Wright, DJ and Bonsall, MB (2011) Effects of host plant and genetic background on the fitness costs of resistance to Bacillus thuringiensis. Journal of Heredity 131, 533–541.Google Scholar
Santos-Amaya, OF, Rodrigues, JVC, Souza, TC, Tavares, CS, Campos, SO, Guedes, RNC and Pereira, EJG (2015) Resistance to dual-gene Bt maize in Spodoptera frugiperda: selection, inheritance, and cross-resistance to other transgenic events. Scientific Reports 5, 18243.CrossRefGoogle ScholarPubMed
SAS Institute (2002) SAS Statistical Analysis System: Getting Started with the SAS Learning. Cary, NC, USA: SAS Institute.Google Scholar
Storer, NP, Babcock, JM, Schlenz, M, Meade, T, Thompson, GD, Bing, JW and Huckaba, RM (2010) Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. Journal of Economic Entomology 103, 1031–1038. https://doi.org/10.1603/ec10040CrossRefGoogle Scholar
Tabashnik, BE, Van Rensburg, JB and Carrière, Y (2009) Field-evolved insect resistance to Bt crops: definition, theory, and data. Journal of Economic Entomology 102, 2011–2025.CrossRefGoogle ScholarPubMed
Tabashnik, BE, Brévault, T and Carrière, Y (2013) Insect resistance to Bt crops: lessons from the first billion acres. Nature Biotechnology 31, 510–521.CrossRefGoogle ScholarPubMed
Vélez, AM, Spencer, TA, Alves, AP, Crespo, ALB and Siegfried, BD (2014) Fitness costs of Cry1F resistance in fall armyworm, Spodoptera frugiperda. Journal of Applied Entomology 138, 315–325.CrossRefGoogle Scholar
Yang, F, Kerns, DL, Brown, S, Kurtz, R, Dennehy, T, Braxton, B, Head, G and Huang, F (2016) Performance and cross-crop resistance of Cry1F-maize selected Spodoptera frugiperda on transgenic Bt cotton: implications for resistance management. Scientific Reports 6, 28059.CrossRefGoogle ScholarPubMed