1932

Abstract

It is increasingly clear that pest species vary widely in their propensities to develop insecticide resistance. This review uses a comparative approach to analyze the key pest management practices and ecological and biochemical or genetic characteristics of the target that contribute to this variation. We focus on six heliothine species, three of which, , , and , have developed resistances to many pesticide classes. The three others, , , and , also significant pests, have developed resistance to very few pesticide classes. We find that host range and movement between alternate hosts are key ecological traits that influence effective selection intensities for resistance. Operational issues are also critical; area-wide, cross-pesticide management practices that account for these ecological factors are key to reducing selection intensity. Without such management, treatment using broad-spectrum chemicals serves to multiply the effects of host plant preference, preadaptive detoxification ability, and high genetic diversity to create a pesticide treadmill for the three high-propensity species.Without rigorous ongoing management, such a treadmill could still develop for newer, more selective chemistries and insecticidal transgenic crops.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-080421-071655
2022-01-07
2024-06-25
Loading full text...

Full text loading...

/deliver/fulltext/ento/67/1/annurev-ento-080421-071655.html?itemId=/content/journals/10.1146/annurev-ento-080421-071655&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abdelghafar SF, Knowles CO, Wall ML. 1993. Pyrethroid resistance in two field strains of Helicoverpa zea (Lepidoptera: Noctuidae). J. Econ. Entomol. 86:1651–55
    [Google Scholar]
  2. 2. 
    Adkisson PL. 1967. Development of resistance by tobacco budworm to mixtures of toxaphene or strobane plus DDT. J. Econ. Entomol. 60:788–91
    [Google Scholar]
  3. 3. 
    Aggarwal N, Brar D, Basedow T. 2006. Insecticide resistance management of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) and its effect on pests and yield of cotton in North India. J. Plant Dis. Prot. 113:120–27
    [Google Scholar]
  4. 4. 
    Ahmad M, Rasool B, Russell D 2019. Resistance and synergism of novel insecticides in field populations of cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae) in Pakistan. J. Econ. Entomol. 112:859–71
    [Google Scholar]
  5. 5. 
    Anderson C, Oakeshott J, Tay W, Gordon K, Zwick A, Walsh T 2018. Hybridization and gene flow in the mega-pest lineage of moth, Helicoverpa. PNAS 115:5034–39
    [Google Scholar]
  6. 6. 
    Anderson CJ, Tay WT, McGaughran A, Gordon K, Walsh TK 2016. Population structure and gene flow in the global pest, Helicoverpa armigera. Mol. Ecol. 25:5296–311
    [Google Scholar]
  7. 7. 
    Armes N, Jadhav D, DeSouza K 1996. A survey of insecticide resistance in Helicoverpa armigera in the Indian subcontinent. Bull. Entomol. Res. 86:499–514
    [Google Scholar]
  8. 8. 
    Avalos S, Mazzuferi V, Fichetti P, Berta DC, Carreras J 2010. Entomofauna asociada a garbanzo en el noroeste de Córdoba (Argentina). Hortic. Argent. 29:5–12
    [Google Scholar]
  9. 9. 
    Baek S, Cho K, Song YH, Lee J-H. 2009. Sampling plans for estimating pepper fruit damage levels by oriental tobacco budworm, Helicoverpa assulta (Guenée), in hot pepper fields. J. Asia-Pac. Entomol. 12:175–78
    [Google Scholar]
  10. 10. 
    Baker GH, Leven T, May T, Tann CR 2016. Planting window requirements for Bt cotton in Australia: Do they limit the exposure of Helicoverpa spp. (Lepidoptera: Noctuidae) to Bt toxins?. Aust. Entomol. 55:32–42
    [Google Scholar]
  11. 11. 
    Baker GH, Tann CR. 2014. Refuge crop performance as part of the Bt resistance management strategy for Helicoverpa spp. (Lepidoptera: Noctuidae) in Australian cotton production systems. Aust. Entomol. 53:240–47
    [Google Scholar]
  12. 12. 
    Bilbo TR, Reay-Jones FPF, Reisig DD, Greene JK. 2019. Susceptibility of corn earworm (Lepidoptera: Noctuidae) to Cry1A.105 and Cry2Ab2 in North and South Carolina. J. Econ. Entomol. 112:1845–57
    [Google Scholar]
  13. 13. 
    Bird L. 2018. Pyrethroid and carbamate resistance in Australian Helicoverpa armigera (Lepidoptera: Noctuidae) from 2008 to 2015: What has changed since the introduction of Bt cotton?. Bull. Entomol. Res. 108:781–91
    [Google Scholar]
  14. 14. 
    Bird L, Walker P. 2019. Baseline susceptibility of Helicoverpa punctigera (Lepidoptera: Noctuidae) to indoxacarb, emamectin benzoate, and chlorantraniliprole. J. Econ. Entomol. 112:818–26
    [Google Scholar]
  15. 15. 
    Bird LJ. 2015. Baseline susceptibility of Helicoverpa armigera (Lepidoptera: Noctuidae) to indoxacarb, emamectin benzoate, and chlorantraniliprole in Australia. J. Econ. Entomol. 108:294–300
    [Google Scholar]
  16. 16. 
    Bird LJ. 2016. Susceptibility of Helicoverpa armigera (Lepidoptera: Noctuidae) to cyantraniliprole determined from topical and ingestion bioassays. J. Econ. Entomol. 109:1350–56
    [Google Scholar]
  17. 17. 
    Bird LJ. 2017. Genetics, cross-resistance and synergism of indoxacarb resistance in Helicoverpa armigera (Lepidoptera: Noctuidae). Pest Manag. Sci. 73:575–81
    [Google Scholar]
  18. 18. 
    Bird LJ, Akhurst RJ. 2007. Variation in susceptibility of Helicoverpa armigera (Hübner) and Helicoverpa punctigera (Wallengren) (Lepidoptera: Noctuidae) in Australia to two Bacillus thuringiensis toxins. J. Invertebrate Pathol. 94:84–94
    [Google Scholar]
  19. 19. 
    Bol. Fitosanit 2017. Dinamica del complejo de Helicoverpa spp. en garbanzo. Campana 2017. Situation: del 28 de junio al 24 de octobre Rep., Estac. Exp. Agroind. Obispo Colombres, Tucumán, Argent.
    [Google Scholar]
  20. 20. 
    Boza Barducci T 1972. Ecological consequences of pesticides used for the control of cotton insects in Cañete Valley, Peru. The Careless Technology: Ecology and International Development MT Farvar, JP Milton 423–38 Garden City, NY: Nat. Hist. Press
    [Google Scholar]
  21. 21. 
    Brazzel JR. 1963. Resistance to DDT in Heliothis virescens. J. Econ. Entomol. 56:571–74
    [Google Scholar]
  22. 22. 
    Brazzel JR. 1964. DDT resistance in Heliothis zea. J. Econ. Entomol. 57:455–57
    [Google Scholar]
  23. 23. 
    Brown TM, Bryson PK. 1992. Selective inhibitors of methyl parathion-resistant acetylcholinesterase from Heliothis virescens. Pestic. . Biochem. Physiol. 44:155–64
    [Google Scholar]
  24. 24. 
    Brown TM, Bryson PK. 1996. Synergism by propynyl aryl ethers in permethrin-resistant tobacco budworm larvae, Heliothis virescens. Pestic. Sci. 46:323–31
    [Google Scholar]
  25. 25. 
    Brown TM, Bryson PK, Brickle DS, Pimprale S, Arnette F et al. 1998. Pyrethroid-resistant Helicoverpa zea and transgenic cotton in South Carolina. Crop Prot 17:441–45
    [Google Scholar]
  26. 26. 
    Campanhola C, McCutchen BF, Baehrecke EH, Plapp FW Jr. 1991. Biological constraints associated with resistance to pyrethroids in the tobacco bud worm (Lepidoptera: Noctuidae). J. Econ. Entomol. 84:1404–11
    [Google Scholar]
  27. 27. 
    Carrière Y, Brown Z, Downes S, Gujar G, Epstein G et al. 2020. Governing evolution: a socioecological comparison of resistance management for insecticidal transgenic Bt crops among four countries. Ambio 49:1–16
    [Google Scholar]
  28. 28. 
    Castaeda G, Miranda D. 1982. Evaluación de la resistencia de Heliothis virescens Fabricius a metil parathion y fenovarelato: Spodoptera frugiperda (J.E. Smith) y Spodoptera Sunia (Guenée) a metil parathion y toxafeno en la zona algodonera de El Espinal (Tolima) Rep., Univ. Nac. Colomb Bogotá:
    [Google Scholar]
  29. 29. 
    Cordeiro EMG, Pantoja-Gomez LM, de Paiva JB, Nascimento ARB, Omoto C et al. 2020. Hybridization and introgression between Helicoverpa armigera and H. zea: an adaptational bridge. BMC Evol. Biol. 20:61
    [Google Scholar]
  30. 30. 
    Cork A, Lobos E. 2003. Female sex pheromone components of Helicoverpa gelotopoeon: first heliothine pheromone without (Z)-11-hexadecenal. Entomol. Exp. Appl. 107:201–6
    [Google Scholar]
  31. 31. 
    Czepak C, Albernaz KC, Vivan LM, Guimarães HO, Carvalhais T. 2013. First reported occurrence of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in Brazil. Pesqui. Agropecu. Trop. 43:110–13
    [Google Scholar]
  32. 32. 
    Dalazen G, Curioletti LE, Cagliari D, Stacke RF, Guedes JVC. 2016. Hairy fleabane as a source of major insect pests of soybean. Planta Daninha 34:403–9
    [Google Scholar]
  33. 33. 
    Dhurua S, Gujar GT. 2011. Field-evolved resistance to Bt toxin Cry1Ac in the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), from India. Pest Manag. Sci. 67:898–903
    [Google Scholar]
  34. 34. 
    Downes S, Kriticos D, Parry H, Paull C, Schellhorn N, Zalucki MP. 2017. A perspective on management of Helicoverpa armigera: transgenic Bt cotton, IPM, and landscapes. Pest Manag. Sci. 73:485–92
    [Google Scholar]
  35. 35. 
    Downes S, Mahon R. 2012. Evolution, ecology and management of resistance in Helicoverpa spp. to Bt cotton in Australia. J. Invertebr. Pathol. 110:281–86
    [Google Scholar]
  36. 36. 
    Downes S, Parker TL, Mahon RJ. 2009. Frequency of alleles conferring resistance to the Bacillus thuringiensis toxins Cry1Ac and Cry2Ab in Australian populations of Helicoverpa punctigera (Lepidoptera: Noctuidae) from 2002 to 2006. J. Econ. Entomol. 102:733–42
    [Google Scholar]
  37. 37. 
    Downes S, Walsh T, Tay WT 2016. Bt resistance in Australian insect pest species. Curr. Opin. Insect Sci. 15:78–83
    [Google Scholar]
  38. 38. 
    ffrench-Constant RH, Bass C. 2017. Does resistance really carry a fitness cost?. Curr. Opin. Insect Sci. 21:39–46
    [Google Scholar]
  39. 39. 
    Fitt G, Dillon M, Hamilton J 1995. Spatial dynamics of Helicoverpa populations in Australia—simulation modelling and empirical studies of adult movement. Comput. Electron. Agric. 13:177–92
    [Google Scholar]
  40. 40. 
    Fitt GP. 1989. The ecology of Heliothis species in relation to agroecosystems. Annu. Rev. Entomol. 34:17–52
    [Google Scholar]
  41. 41. 
    Folsom JW. 1936. Notes on little known cotton insects. J. Econ. Entomol. 29:282–85
    [Google Scholar]
  42. 42. 
    Forrester NW, Cahill M, Bird LJ, Layland JK. 1993. Management of pyrethroid and endosulfan resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) in Australia. Bull. Entomol. Res.Suppl. 1R1–132
    [Google Scholar]
  43. 43. 
    Fritz M, DeYonke A, Papanicolaou A, Micinski S, Westbrook J, Gould F 2018. Contemporary evolution of a Lepidopteran species, Heliothis virescens, in response to modern agricultural practices. Mol. Ecol. 27:167–81
    [Google Scholar]
  44. 44. 
    Georghiou GP, Taylor CE. 1977. Operational influences in the evolution of insecticide resistance. J. Econ. Entomol. 70:653–58
    [Google Scholar]
  45. 45. 
    Goodyer GJ, Wilson AGL, Attia FI, Clift AD. 1975. Insecticide resistance in Heliothis armigera (Hübner) (Lepidoptera: Noctuidae) in the Namoi valley of New South Wales, Australia. Aust. J. Entomol. 14:171–73
    [Google Scholar]
  46. 46. 
    Gould F, Martinez-Ramirez A, Anderson A, Ferré J, Silva FJ, Moar WJ. 1992. Broad-spectrum resistance to Bacillus thuringiensis toxins in Heliothis virescens. PNAS 89:7986–90
    [Google Scholar]
  47. 47. 
    Gregg PC, Daly JC. 1989. The Australian species of Heliothis—identification, genetic variation and migration. Acta Phytopathol. Entomol. Hung. 24:85–91
    [Google Scholar]
  48. 48. 
    Gregg PC, Del Socorro AP, Hawes AJ, Binns MR 2016. Developing bisexual attract-and-kill for polyphagous insects: ecological rationale versus pragmatics. J. Chem. Ecol. 42:666–75
    [Google Scholar]
  49. 49. 
    Gregg PC, Henderson GS, Del Socorro AP, Le Mottee K, Birchall C 2016. Polyphagy in an uncertain environment: Helicoverpa punctigera in inland Australia. Aust. Ecol. 41:819–28
    [Google Scholar]
  50. 50. 
    Gregg PC, McDonald G, Bryceson KP. 1989. The occurrence of Heliothis punctigera Wallengren and Heliothis armigera (Hübner) in inland Australia. J. Aust. Entomol. Soc. 28:135–40
    [Google Scholar]
  51. 51. 
    Groot AT, Classen A, Inglis O, Blanco CA, López J et al. 2011. Genetic differentiation across North America in the generalist moth Heliothis virescens and the specialist H. subflexa. Mol. Ecol. 20:2676–92
    [Google Scholar]
  52. 52. 
    Grubor V, Heckel D. 2007. Evaluation of the role of CYP6B cytochrome P450s in pyrethroid resistant Australian Helicoverpa armigera. Insect Mol. Biol. 16:15–23
    [Google Scholar]
  53. 53. 
    Guan F, Hou BF, Dai XG, Liu ST, Liu JJ et al. 2021. Multiple origins of a single point mutation in the cotton bollworm tetraspanin gene confers dominant resistance to Bt cotton. Pest Manag. Sci. 77:1169–77
    [Google Scholar]
  54. 54. 
    Gunning R, Moores G, Devonshire A. 1997. Esterases and fenvalerate resistance in a field population of Helicoverpa punctigera (Lepidoptera: Noctuidae) in Australia. Pestic. Biochem. Physiol. 58:155–62
    [Google Scholar]
  55. 55. 
    Gunning R, Moores G, Devonshire A. 1999. Esterase inhibitors synergise the toxicity of pyrethroids in Australian Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Pestic. . Biochem. Physiol. 63:50–62
    [Google Scholar]
  56. 56. 
    Gunning RV, Easton CS, Greenup LR, Edge VE. 1984. Pyrethroid resistance in Heliothis armiger (Hübner) (Lepidoptera: Noctuidae) in Australia. J. Econ. Entomol. 77:1283–87
    [Google Scholar]
  57. 57. 
    Gunning FV, Forrester NW, Easton CS, Greenup LR 1990. Relationship between DDT and pyrethroid resistance in Heliothis armigera (Hubner) (Lepidoptera: Noctuidae) in Australia. Trop. Pest Manag. 36:293–95
    [Google Scholar]
  58. 58. 
    Gunning RV, Moores GD, Devonshire AL. 1998. Insensitive acetylcholinesterase and resistance to organophosphates in Australian Helicoverpa armigera. Pestic. Biochem. Physiol. 62:147–51
    [Google Scholar]
  59. 59. 
    Hambleton EJ. 1944. Heliothis virescens as a pest of cotton, with notes on host plants in Peru. J. Econ. Entomol. 37:660–66
    [Google Scholar]
  60. 60. 
    Harris FA. 1972. Resistance to methyl parathion and toxaphene-DDT in bollworm and tobacco budworm from cotton in Mississippi. J. Econ. Entomol. 65:1193–94
    [Google Scholar]
  61. 61. 
    Hawkins NJ, Bass C, Dixon A, Neve P. 2018. The evolutionary origins of pesticide resistance. Biol. Rev. 94:135–55
    [Google Scholar]
  62. 62. 
    Head DJ, McCaffery AR, Callaghan A. 1998. Novel mutations in the para-homologous sodium channel gene associated with phenotypic expression of nerve insensitivity resistance to pyrethroids in Heliothine lepidoptera. Insect Mol. Biol. 7:191–96
    [Google Scholar]
  63. 63. 
    Heckel DG, Bryson PK, Brown TM. 1998. Linkage analysis of insecticide-resistant acetylcholinesterase in Heliothis virescens. J. Hered. 89:71–78
    [Google Scholar]
  64. 64. 
    Huang HZ, Ottea JA. 2004. Development of pyrethroid substrates for esterases associated with pyrethroid resistance in the tobacco budworm, Heliothis virescens (F.). J. Agric. Food Chem. 52:6539–45
    [Google Scholar]
  65. 65. 
    Common IFB 1953. The Australian species of Heliothis (Lepidoptera: Noctuidae) and their pest status. Aust. J. Zool. 1:319–44
    [Google Scholar]
  66. 66. 
    Ivy EE, Scales AL. 1954. Are cotton insects becoming resistant to insecticides?. J. Econ. Entomol. 47:981–84
    [Google Scholar]
  67. 67. 
    Jadhav DR, Armes NJ. 1996. Comparative status of insecticide resistance in the Helicoverpa and Heliothis species (Lepidoptera: Noctuidae) of south India. Bull. Entomol. Res. 86:525–31
    [Google Scholar]
  68. 68. 
    Jin L, Wang J, Guan F, Zhang J, Yu S et al. 2018. Dominant point mutation in a tetraspanin gene associated with field-evolved resistance of cotton bollworm to transgenic Bt cotton. PNAS 115:11760–65
    [Google Scholar]
  69. 69. 
    Jin L, Zhang HN, Lu YH, Yang YH, Wu KM et al. 2015. Large-scale test of the natural refuge strategy for delaying insect resistance to transgenic Bt crops. Nat. Biotechnol. 33:169–74
    [Google Scholar]
  70. 70. 
    Jones CM, Papanicolaou A, Mironidis GK, Vontas J, Yang Y et al. 2015. Genomewide transcriptional signatures of migratory flight activity in a globally invasive insect pest. Mol. Ecol. 24:4901–11
    [Google Scholar]
  71. 71. 
    Jones CM, Parry H, Tay WT, Reynolds DR, Chapman JW 2019. Movement ecology of pest Helicoverpa: implications for ongoing spread. Annu. Rev. Entomol. 64:277–95
    [Google Scholar]
  72. 72. 
    Joussen N, Agnolet S, Lorenz S, Schone SE, Ellinger R et al. 2012. Resistance of Australian Helicoverpa armigera to fenvalerate is due to the chimeric P450 enzyme CYP337B3. PNAS 109:15206–11
    [Google Scholar]
  73. 73. 
    Jurat-Fuentes JL, Heckel DG, Ferré J 2021. Mechanisms of resistance to insecticidal proteins from Bacillus thuringiensis. Annu. Rev. Entomol. 66:121–40
    [Google Scholar]
  74. 74. 
    Kranthi KR, Stone GD. 2020. Long-term impacts of Bt cotton in India. Nat. Plants 6:188–96
    [Google Scholar]
  75. 75. 
    Kukanur V, Singh T, Kranthi K, Andow D 2018. Cry1Ac resistance allele frequency in field populations of Helicoverpa armigera (Hübner) collected in Telangana and Andhra Pradesh, India. Crop Prot 107:34–40
    [Google Scholar]
  76. 76. 
    Lee K, Boo KS 1985. Studies on biology and control program of the oriental tobacco budworm, Heliothis assulta, with insect growth regulators and sex pheromone. II. Effects of an insect growth regulator, diflubenzuron, on embryonic and postembryonic development. Agric. Res. Seoul Nat. Univ. 10:27–34
    [Google Scholar]
  77. 77. 
    Little N, Catchot A, Allen K, Gore J, Musser F et al. 2017. Supplemental control with diamides for Heliothines in Bt cotton. Southwest. Entomol. 42:15–26
    [Google Scholar]
  78. 78. 
    Luttrell RG, Roush RT, Ali A, Mink JS, Reid MR, Snodgrass GL 1987. Pyrethroid resistance in field populations of Heliothis virescens (Lepidoptera: Noctuidae) in Mississippi in 1986. J. Econ. Entomol. 80:985–89
    [Google Scholar]
  79. 79. 
    Mahon R, Olsen K, Downes S, Addison S. 2007. Frequency of alleles conferring resistance to the Bt toxins Cry1Ac and Cry2Ab in Australian populations of Helicoverpa armigera (Lepidoptera: Noctuidae). J. Econ. Entomol. 100:1844–53
    [Google Scholar]
  80. 80. 
    Mahon R, Olsen K, Garsia K, Young S 2007. Resistance to Bacillus thuringiensis toxin Cry2Ab in a strain of Helicoverpa armigera (Lepidoptera: Noctuidae) in Australia. J. Econ. Entomol. 100:894–902
    [Google Scholar]
  81. 81. 
    Mahon RJ, Downes SJ, James B. 2012. Vip3A resistance alleles exist at high levels in Australian targets before release of cotton expressing this toxin. PLOS ONE 7:e39192
    [Google Scholar]
  82. 82. 
    Matthews M. 1999. Heliothine Moths of Australia: A Guide to Pest Bollworms and Related Noctuid Groups Collingwood, Victoria, Aust: CSIRO Publ.
    [Google Scholar]
  83. 83. 
    Mazza SM, Sosa MA, Avanza MA. 2007. Spatial distribution pattern of lepidopteron cotton pests in Argentine Paper presented at the World Cotton Research Conference 4 Sept 10–14 Lubbock, TX:
    [Google Scholar]
  84. 84. 
    McCaffery AR. 1998. Resistance to insecticides in heliothine Lepidoptera: a global view. Philos. Trans. R. Soc. Lond. B 353:1735–50
    [Google Scholar]
  85. 85. 
    Mota-Sanchez D, Wise JC. 2021. The Arthropod Pesticide Resistance Database Database, Mich. State Univ., East Lansing http://www.pesticideresistance.org
    [Google Scholar]
  86. 86. 
    Murúa MG, Cazado LE, Casmuz A, Herrero MI, Villagrán ME et al. 2016. Species from the Heliothinae complex (Lepidoptera: Noctuidae) in Tucumán, Argentina, an update of geographical distribution of Helicoverpa armigera. J. Insect Sci. 16:61
    [Google Scholar]
  87. 87. 
    Murúa MG, Nagoshi RN, Dos Santos DA, Hay-Roe MM, Meagher RL, Vilardi JC 2015. Demonstration using field collections that Argentina fall armyworm populations exhibit strain-specific host plant preferences. J. Econ. Entomol. 108:2305–15
    [Google Scholar]
  88. 88. 
    Niu Y, Oyediran I, Yu WB, Lin SC, Dimase M et al. 2021. Populations of Helicoverpa zea (Boddie) in the southeastern United States are commonly resistant to Cry1Ab, but still susceptible to Vip3Aa20 expressed in MIR 162 corn. Toxins 13:63
    [Google Scholar]
  89. 89. 
    Park S, Brown TM 2002. Linkage of genes for sodium channel and cytochrome P450 (CYP6B10) in Heliothis virescens. Pest Manag. Sci. 58:209–12
    [Google Scholar]
  90. 90. 
    Pastrana JA. 2004. Los Lepidopteros Argentinos: Sus Plantas Hospedadoras y Otros Sustratos Alimenticious Buenos Aires: Soc. Entomol. Argent.
    [Google Scholar]
  91. 91. 
    Pearce SL, Clarke DF, East PD, Elfekih S, Gordon KHJ et al. 2017. Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species. BMC Biol 15:63
    [Google Scholar]
  92. 92. 
    Pereira RM, Abbade Neto D, Amado D, Durigan MR, Franciscatti RA et al. 2020. Baseline susceptibility and frequency of resistance to diamide insecticides in Helicoverpa armigera (Lepidoptera: Noctuidae) populations in Brazil. Crop Prot 137:105266
    [Google Scholar]
  93. 93. 
    Pietrantonio P, Junek T, Parker R, Mott D, Siders K et al. 2007. Detection and evolution of resistance to the pyrethroid cypermethrin in Helicoverpa zea (Lepidoptera: Noctuidae) populations in Texas. Environ. Entomol. 36:1174–88
    [Google Scholar]
  94. 94. 
    Plapp FW, Campanhola C. 1986. Synergism of pyrethroids by chlordimeform against susceptible and resistant Heliothis. Proceedings of the 1986 Beltwide Cotton Production and Research Conference, Jan. 4–9, Las Vegas, NV167–69 Washington, DC: Nat. Cotton Counc. Am.
    [Google Scholar]
  95. 95. 
    Plapp FW Jr, Jackman JA, Campanhola C, Frisbie RE, Graves JB et al. 1990. Monitoring and management of pyrethroid resistance in the tobacco budworm (Lepidoptera: Noctuidae) in Texas, Mississippi, Louisiana, Arkansas, and Oklahoma. J. Econ. Entomol. 83:335–41
    [Google Scholar]
  96. 96. 
    Pogue MG. 2013. Revised status of Chloridea Duncan and (Westwood), 1841, for the Heliothis virescens species group (Lepidoptera: Noctuidae: Heliothinae) based on morphology and three genes. Syst. Entomol. 38:523–42
    [Google Scholar]
  97. 97. 
    Pyke BA, Fitt GP 1998. Field performance of INGARD cotton—the first two years. Pest Management: Future Challenges MP Zalucki, RAI Drew, GG White 230–37 Brisbane, Aust: Univ. Queensland Press
    [Google Scholar]
  98. 98. 
    Rane RV, Ghodke AB, Hoffmann AA, Edwards OR, Walsh TK, Oakeshott JG. 2019. Detoxifying enzyme complements and host use phenotypes in 160 insect species. Curr. Opin. Insect Sci. 31:131–38
    [Google Scholar]
  99. 99. 
    Rane RV, Walsh TK, Pearce SL, Jermiin LS, Gordon KHJ et al. 2016. Are feeding preferences and insecticide resistance associated with the size of detoxifying enzyme families in insect herbivores?. Curr. Opin. Insect Sci. 13:70–76
    [Google Scholar]
  100. 100. 
    Reisig D, Huseth A, Bacheler J, Aghaee M, Braswell L et al. 2018. Long-term empirical and observational evidence of practical Helicoverpa zea resistance to cotton with pyramided Bt toxins. J. Econ. Entomol. 111:1824–33
    [Google Scholar]
  101. 101. 
    Richards KT. 1964. Insect pests of cotton in the Ord River irrigation area. J. Dept. Agric. West. Aust. 5:4
    [Google Scholar]
  102. 102. 
    Russell RJ, Claudianos C, Campbell PM, Horne I, Sutherland TD, Oakeshott JG 2004. Two major classes of target site insensitivity mutations confer resistance to organophosphate and carbamate insecticides. Pestic. Biochem. Physiol. 79:84–93
    [Google Scholar]
  103. 103. 
    Sayyed AH, Ahmad M, Crickmore N 2008. Fitness costs limit the development of resistance to indoxacarb and deltamethrin in Heliothis virescens (Lepidoptera: Noctuidae). J. Econ. Entomol. 101:1927–33
    [Google Scholar]
  104. 104. 
    Scalora F, Casmuz A, Cazado L, Socias G, Tolosa G et al. 2012. Evaluacion de diferentes insecticidas el control de la oruga bolillera Helicoverpa gelotopoeon Dyar (Lepidoptera: Noctuidae). El Cultivo de la Soja en el Noroeste Argentine MR Devani, F Ledesma, JR Sanchez 147–51 Tucumán, Argent: Estac. Exp. Agroindust. Obispo Colombres
    [Google Scholar]
  105. 105. 
    Seymour M, Perera OP, Fescemyer HW, RE Jackson, Fleischer SJ, Abel CA. 2016. Peripheral genetic structure of Helicoverpa zea indicates asymmetrical panmixia. Ecol. Evol. 6:3198–207
    [Google Scholar]
  106. 106. 
    Sorenson CE, Schreiber A, Townsend HG, Abd-Elghafar SF, Fairchild ML, Knowles CO. 1998. Monitoring pyrethroid resistance in bollworm (Lepidoptera: Noctuidae) moths in Missouri, 1988 to 1994. J. Entomol. Sci. 33:300–12
    [Google Scholar]
  107. 107. 
    Sosa-Gómez DR, Specht A, Paula-Moraes SV, Lopes-Lima A, Yano SAC et al. 2016. Timeline and geographical distribution of Helicoverpa armigera (Hübner) (Lepidoptera, Noctuidae: Heliothinae) in Brazil. Rev. Bras. Entomol. 60:101–4
    [Google Scholar]
  108. 108. 
    Sparks TC. 1981. Development of insecticide resistance in Heliothis zea and Heliothis virescens in North America. Bull. Entomol. Soc. Am. 27:186–92
    [Google Scholar]
  109. 109. 
    Specht A, Sosa-Gómez D, de Paula-Moraes S, Yano S. 2013. Morphological and molecular identification of Helicoverpa armigera (Lepidoptera: Noctuidae) and expansion of its occurrence record in Brazil. Pesqui. Agropecu. Bras. 48:689–92
    [Google Scholar]
  110. 110. 
    Steinbach D, Gutbrod O, Lummen P, Matthiesen S, Schorn C, Nauen R. 2015. Geographic spread, genetics and functional characteristics of ryanodine receptor based target-site resistance to diamide insecticides in diamondback moth, Plutella xylostella. Insect Biochem. Mol. Biol. 63:14–22
    [Google Scholar]
  111. 111. 
    Sudbrink D, Grant J. 1995. Wild host plants of Helicoverpa zea and Heliothis virescens (Lepidoptera: Noctuidae) in Eastern Tennessee. Environ. Entomol. 24:1080–85
    [Google Scholar]
  112. 112. 
    Tabashnik B, Carrière Y. 2017. Surge in insect resistance to transgenic crops and prospects for sustainability. Nat. Biotechnol. 35:926–35
    [Google Scholar]
  113. 113. 
    Tabashnik BE, Brevault T, Carrière Y. 2013. Insect resistance to Bt crops: lessons from the first billion acres. Nat. Biotechnol. 31:510–21
    [Google Scholar]
  114. 114. 
    Tabashnik BE, Carrière Y 2015. Successes and failures of transgenic Bt crops: global patterns of field-evolved resistance. Bt Resistance: Characterization and Strategies for GM Crops Producing Bacillus Thuringiensis Toxins M Soberón, A Gao, A Bravo 1–14 Wallingford, UK: CABI
    [Google Scholar]
  115. 115. 
    Tay WT, Mahon RJ, Heckel DG, Walsh TK, Downes S et al. 2015. Insect resistance to Bacillus thuringiensis toxin Cry2Ab is conferred by mutations in an ABC transporter subfamily A protein. PLOS Genet 11:e1005534
    [Google Scholar]
  116. 116. 
    Tay WT, Soria M, Walsh T, Thomazoni D, Silvie P et al. 2013. A brave new world for an Old World pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. PLOS ONE 8:e80134
    [Google Scholar]
  117. 117. 
    Tay WT, Walsh TK, Downes S, Anderson C, Jermiin LS et al. 2017. Mitochondrial DNA and trade data support multiple origins of Helicoverpa armigera (Lepidoptera, Noctuidae) in Brazil. Sci. Rep 7:45302
    [Google Scholar]
  118. 118. 
    Taylor MFJ, Heckel DG, Brown TM, Kreitman ME, Black B. 1993. Linkage of pyrethroid insecticide resistance to a sodium channel locus in the tobacco budworm. Insect Biochem. Mol. Biol. 23:763–75
    [Google Scholar]
  119. 119. 
    Teese M, Farnsworth C, Li Y, Coppin C, Devonshire A et al. 2013. Heterologous expression and biochemical characterisation of fourteen esterases from Helicoverpa armigera. PLOS ONE 8:e65951
    [Google Scholar]
  120. 120. 
    Thia JA, Hoffmann AA, Umina PA. 2020. Empowering Australian insecticide resistance research with genetic information: the road ahead. Aust. Entomol 60:147–62
    [Google Scholar]
  121. 121. 
    Urena E, Guillem-Amat A, Couso-Ferrer F, Beroiz B, Perera N et al. 2019. Multiple mutations in the nicotinic acetylcholine receptor Ccα6 gene associated with resistance to spinosad in medfly. Sci. Rep. 9:2961
    [Google Scholar]
  122. 122. 
    Valencia-Montoya WA, Elfekih S, North HL, Meier JI, Warren IA et al. 2020. Adaptive introgression across semipermeable species boundaries between local Helicoverpa zea and invasive Helicoverpa armigera moths. Mol. Biol. Evol. 37:2568–83
    [Google Scholar]
  123. 123. 
    Van den Bosch R. 1978. The Pesticide Conspiracy Garden City, NY: Doubleday
    [Google Scholar]
  124. 124. 
    Vinson SB, Brazzel JR. 1966. Penetration and metabolism of C14-labeled DDT in resistant and susceptible tobacco budworm larvae Heliothis virescens (F). J. Econ. Entomol. 59:600–4
    [Google Scholar]
  125. 125. 
    Walsh T, James B, Chakroun M, Ferré J, Downes S 2018. Isolating, characterising and identifying a Cry1Ac resistance mutation in field populations of Helicoverpa punctigera. Sci. Rep. 8:2626
    [Google Scholar]
  126. 126. 
    Walsh T, Joussen N, Tian K, McGaughran A, Anderson C et al. 2018. Multiple recombination events between two cytochrome P450 loci contribute to global pyrethroid resistance in Helicoverpa armigera. PLOS ONE 13:e0197760
    [Google Scholar]
  127. 127. 
    Walsh TK, Perera O, Anderson C, Gordon K, Czepak C et al. 2019. Mitochondrial DNA genomes of five major Helicoverpa pest species from the Old and New Worlds (Lepidoptera: Noctuidae). Ecol. Evol. 9:2933–44
    [Google Scholar]
  128. 128. 
    Wang C, Dong J, Tang D, Zhang J, Li W, Qin J 2004. Host selection of Helicoverpa armigera and H. assulta and its inheritance. Prog. Nat. Sci. 14:880–84
    [Google Scholar]
  129. 129. 
    Wang H, Shi Y, Wang L, Liu S, Wu S et al. 2018. CYP6AE gene cluster knockout in Helicoverpa armigera reveals role in detoxification of phytochemicals and insecticides. Nat. Commun. 9:4820
    [Google Scholar]
  130. 130. 
    Wang P, Ma J, Head G, Xia D, Li J et al. 2019. Susceptibility of Helicoverpa armigera to two Bt toxins, Cry1Ac and Cry2Ab, in northwestern China: toward developing an IRM strategy. J. Pest Sci. 92:923–31
    [Google Scholar]
  131. 131. 
    Wang X, Wang R, Yang Y, Wu S, O'Reilly AO, Wu Y. 2016. A point mutation in the glutamate-gated chloride channel of Plutella xylostella is associated with resistance to abamectin. Insect Mol. Biol. 25:116–25
    [Google Scholar]
  132. 132. 
    Wang X-L, Su W, Zhang J-H, Yang Y-H, Dong K, Wu Y-D 2016. Two novel sodium channel mutations associated with resistance to indoxacarb and metaflumizone in the diamondback moth, Plutella xylostella. Insect Sci 23:50–58
    [Google Scholar]
  133. 133. 
    Wilson AGL. 1974. Resistance of Heliothis armigera to insecticides in Ord irrigation area, north-western Australia. J. Econ. Entomol. 67:256–58
    [Google Scholar]
  134. 134. 
    Wilson L, Whitehouse M, Herron G, Berenbaum M. 2018. The management of insect pests in Australian cotton: an evolving story. Annu. Rev. Entomol. 63:215–37
    [Google Scholar]
  135. 135. 
    Wilson LJ, Bauer LR, Lally DA. 1998. Effect of early season insecticide use on predators and outbreaks of spider mites (Acari: Tetranychidae) in cotton. Bull. Entomol. Res. 88:477–88
    [Google Scholar]
  136. 136. 
    Wilson LJ, Herron GA, Bauer LR, Lally DA. 1999. Acaricidal and stimulatory effects of insecticides on Tetranychus urticae Koch (Acari: Tetranychidae) in cotton. Aust. J. Entomol. 38:30–33
    [Google Scholar]
  137. 137. 
    Wolfenbarger DA, Lukefahr MJ, Graham HM. 1973. LD50 values of methyl parathion and endrin to tobacco budworms and bollworms collected in the Americas and hypothesis on the spread of resistance in these Lepidopterans to these insecticides. J. Econ. Entomol. 66:211–16
    [Google Scholar]
  138. 138. 
    Wu K, Guo Y, Gao S. 2002. Evaluation of the natural refuge function for Helicoverpa armigera (Lepidoptera: Noctuidae) within Bacillus thuringiensis transgenic cotton growing areas in north China. J. Econ. Entomol. 95:832–37
    [Google Scholar]
  139. 139. 
    Wu K, Mu W, Liang G, Guo Y. 2005. Regional reversion of insecticide resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) is associated with the use of Bt cotton in northern China. Pest Manag. Sci. 61:491–98
    [Google Scholar]
  140. 140. 
    Wu KM, Lu YH, Feng HQ, Jiang YY, Zhao JZ. 2008. Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-containing cotton. Science 321:1676–78
    [Google Scholar]
  141. 141. 
    Xia X, Wang K, Wang H 2009. Resistance of Helicoverpa assulta (Guenée) (Lepidoptera: Noctuidae) to fenvalerate, phoxim and methomyl in China. Crop Prot 28:162–67
    [Google Scholar]
  142. 142. 
    Yang C, Jeon H, Cho M-R, Kim D, Yiem M 2004. Seasonal occurrence of oriental tobacco budworm (Lepidoptera: Noctuidae) male and chemical control at red pepper fields. Korean J. Appl. Entomol. 43:49–54
    [Google Scholar]
  143. 143. 
    Yang Y, Chen H, Wu S, Yang Y, Xu X, Wu Y 2006. Identification and molecular detection of a deletion mutation responsible for a truncated cadherin of Helicoverpa armigera. Insect Biochem. Mol. Biol. 36:735–40
    [Google Scholar]
  144. 144. 
    Yang Y, Li Y, Wu Y 2013. Current status of insecticide resistance in Helicoverpa armigera after 15 years of Bt cotton planting in China. J. Econ. Entomol. 106:375–81
    [Google Scholar]
  145. 145. 
    Yang Y, Wu Y, Chen S, Devine G, Denholm I et al. 2004. The involvement of microsomal oxidases in pyrethroid resistance in Helicoverpa armigera from Asia. Insect Biochem. Mol. Biol. 34:763–73
    [Google Scholar]
  146. 146. 
    Young HP, Bailey WD, Roe RM. 2003. Spinosad selection of a laboratory strain of the tobacco budworm, Heliothis virescens (Lepidoptera: Noctuidae), and characterization of resistance. Crop Prot 22:265–73
    [Google Scholar]
  147. 147. 
    Zalucki M, Murray D, Gregg P, Fitt G, Twine P, Jones C. 1994. Ecology of Helicoverpa armigera (Hübner) and Heliothis punctigera (Wallengren) in the inland of Australia: larval sampling and host-plant relationships during winter and spring. Aust. J. Zool. 42:329–46
    [Google Scholar]
  148. 148. 
    Zalucki MP, Daglish G, Firempong S, Twine P 1986. The biology and ecology of Heliothis armigera (Hübner) and Heliothis punctigera Wallengren (Lepidoptera, Noctuidae) in Australia: What do we know?. Aust. J. Zool. 34:779–814
    [Google Scholar]
  149. 149. 
    Zhang HN, Wu SW, Yang YH, Tabashnik BE, Wu YD. 2012. Non-recessive Bt toxin resistance conferred by an intracellular cadherin mutation in field-selected populations of cotton bollworm. PLOS ONE 7:e53418
    [Google Scholar]
  150. 150. 
    Zhao J, Jin L, Yang Y, Wu Y 2010. Diverse cadherin mutations conferring resistance to Bacillus thuringiensis toxin Cry1Ac in Helicoverpa armigera. Insect Biochem. Mol. Biol. 40:113–18
    [Google Scholar]
  151. 151. 
    Zhao Y, Park Y, Adams ME 2000. Functional and evolutionary consequences of pyrethroid resistance mutations in S6 transmembrane segments of a voltage-gated sodium channel. Biochem. Biophys. Res. Commun. 278:516–21
    [Google Scholar]
/content/journals/10.1146/annurev-ento-080421-071655
Loading
/content/journals/10.1146/annurev-ento-080421-071655
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error