Population Genetic Structure of the Cotton Bollworm Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in India as Inferred from EPIC-PCR DNA Markers

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Behere, Gajanan Tryambak ^a,d   Tay, Wee Tek ^b   Russell, Derek Alan ^c   Kranthi, Keshav Raj ^e   Batterham, Philip ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b CSIRO   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d ICAR RESEARCH COMPLEX FOR NEH REGION   (India)

^e CENTRAL INSTITUTE FOR COTTON RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; COTTON; CROP; DNA MARKER; EXON PRIMED INTRON CROSSING; GENE CLUSTER; GENE FREQUENCY; GENETIC PROCEDURES; GENETIC VARIABILITY; HELICOVERPA ARMIGERA; HETEROZYGOTE; INBREEDING; INDIA; NONHUMAN; NUCLEOTIDE SEQUENCE; NULL ALLELE; POLYMERASE CHAIN REACTION; POPULATION GENETIC STRUCTURE;

ALLELES; ANIMALS; EXONS; GENE FREQUENCY; GENETIC MARKERS; GENETIC VARIATION; GENETICS, POPULATION; GEOGRAPHY; GOSSYPIUM; INDIA; INTRONS; MOTHS; POLYMERASE CHAIN REACTION; SPECIMEN HANDLING;

GOSSYPIUM HIRSUTUM; HELICOVERPA ARMIGERA; LEPIDOPTERA; NOCTUIDAE;

EID: 84872236157     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053448     Document Type: Article

References (73)

1. Fitt GP, (1989) The ecology of Heliothis species in relation to agroecosystems. Ann Rev Entomol 34: 17-52.
2. Manjunath TM, Bhatnagar VS, Pawar CS, Sithanantham S (1989) Economic importance of Heliothis spp. in India and an assessment of their natural enemies and host plants; 11-15 November, 1989; New Delhi, India. pp. 197-228.
3. Singh J, Bains SS, (1986) Role of plants in population build up of Heliothis armigera (Hübner) in Punjab. Indian J Ecol 13: 113-119.
4. Bhatnagar VS (1980) A report on research on the Heliothis complex at ICRISAT (India) 1974-79; 24-26 April, 1980; Udaipur, India.
5. Jayaraj S (1982) Biological and Ecological studies of Heliothis. In: Reed W, editor, 15-20 November 1981; ICRISAT Center, Patancheru, A.P., India. pp. 17-28.
6. Kranthi KR, Jadav DR, Wanjari RR, Shaki-Ali S, Russell DA, (2001) Carbamate and organophosphate resistance in cotton pests in India, 1995-1999. Bull Entomol Res 91: 37-46.
7. Sachan JN (1987) Status of gram pod borer H. armigera (Hb.) in India and its management. In: Mathour YK, editor. Recent Advances in Entomology. Parade, Kanpur: Gopal Parkashan. pp. 91-110.
8. Singh J, Sandhu SS, Singla ML, (1990) Ecology of Heliothis armigera (Hub.) on chickpea in Punjab. J Insect Sci 3: 47-52.
9. Singh J, Sidhu AS (1992) Present status of Helicoverpa armigera in cotton and strategies for its management in Punjab, Haryana and Rajasthan. In: Sachan JN, editor. Directorate of Pulse Research, Kanpur. pp. 92-98.
10. Durairaj C, Subbaratnam GV, Singh TVK, Shannower TG (2005) Helicoverpa in India: Spatial and temporal dynamics and management options. In: Sharma H, editor. Heliothis/Helicoverpa management - Emerging trends and strategies for future research Oxford&IBH Publishing Co, New Delhi. pp. 91-117.
11. Verma AK, Sankhyan S, (1993) Pheromone monitoring of Heliothis armigera (Hubner) and relationship of moth activity with larval infestation on important cash crops in mid-hills of Himachal Pradesh. Pest Manag Eco Zool 1: 43-49.
12. Pedgley DE, Tucker MR, Pawar CS, (1987) Windborne migration of Heliothis armigera (Hübner) (Lepidoptera: Noctuidae) in India. Int J Trop Insect Sci 8: 599-604.
13. Bhattacherjee NS, (1972) Heliothis armigera (Hübner) a polytypic species. Ent Newsl 2: 3-4.
14. Reed W, Pawar CS (1982) Heliothis: A global problem. In: Reed W, editor. 15-20 November 1981; ICRISAT Center, Patancheru, A.P., India. pp. 9-14.
15. Jallow MFA, Cunningham JP, Zalucki MP, (2004) Intra-specific variation for host plant use in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae): implications for management. Crop Prot 23: 955-964.
16. Kranthi KR, Armes NJ, Rao NGV, Sheo R, Sundarmurthy VT, (1997) Seasonal dynamics of metabolic mechanisms mediating pyrethroid resistance in Helicoverpa armigera in central India. Pestic Sci 50: 91-98.
17. Armes NJ, Jadhav DR, DeSouza KR, (1996) A survey of insecticide resistance in Helicoverpa armigera in the Indian subcontinent. Bull Entomol Res 86: 499-514.
18. Madden AD, Holt J, Armes NJ, (1995) The role of uncultivated hosts in the spread of pyrethroid resistance in Helicoverpa armigera populations in Andhra Pradesh, India: a simulation approach. Ecol Model 82: 61-74.
19. Armes NJ, Jadhav DR, Bond GS, King ABS, (1992) Insecticide resistance in Helicoverpa armigera in South India. Pestic Sci 43: 355-364.
20. De Souza K, Holt J, Colvin J, (1995) Diapause, migration and pyrethroid-resistance dynamics in the cotton bollworm, HeIicoverpa armigera (Lepidoptera: Noctuidae). Ecol Entomol 20: 333-342.
21. Tamhankar AJ, Rajendran TP, Hariprasad Rao N, Lavekar RC, Jeyakumar P, et al. (2003) Variability in response of Helicoverpa armigera males from different locations in India to varying blends of female sex pheromone suggests male sex pheromone response polymorphism. Curr Sci 84: 448-450.
22. Zalucki MP, Cunningham JP, Downes S, Ward P, Lange C, et al. (2012) No evidence for change in oviposition behaviour of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) after widespread adoption of transgenic insecticidal cotton. Bull Entomol Res 102: 468-476.
23. Chowda-Reddy RV, Kirankumar M, Seal SE, Muniyappa V, Valand GB, et al. (2012) Bemisia tabaci phylogenetic groups in India and the relative transmission efficacy of Tomato leaf curl Bangalore virus by an indigenous and an exotic population. J Integrative Agric 11 (2):: 235-248.
24. Zhou X, Faktor O, Applebaum SW, Coll M, (2000) Population structure of the pestiferous moth Helicoverpa armigera in the eastern Mediterranean using RAPD analysis. Heredity 85: 251-256.
25. Nibouche S, Buès R, Toubon J-F, Poitout S, (1998) Allozyme polymorphism in the cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae): comparison of African and European populations. Heredity 80: 438-445.
26. Behere GT, Tay WT, Russell DA, Heckel DG, Appleton BR, et al. (2007) Mitochondrial DNA analysis of field populations of Helicoverpa armigera (Lepidoptera: Noctuidae) and of its relationship to H. zea. BMC evolutionary biology 7: 117.
27. Vassal JM, Brevault T, Achaleke J, Menozzi P, (2008) Genetic structure of the polyphagous pest Helicoverpa armigera (Lepidoptera: Noctuidae) across the Sub-Saharan cotton belt. Commun Agric Appl Biol Sci 73: 433-437.
28. Endersby NM, Hoffmann AA, McKechnie SW, Weeks AR, (2007) Is there genetic structure in populations of Helicoverpa armigera from Australia? Entomol Exp Appl 122: 253-263.
29. Daly JC, Gregg P, (1985) Genetic variation in Heliothis in Australia: species identification and gene flow in the two pest species H. armigera (Hübner) and H. punctigera Wallengren (Lepidoptera: Noctuidae). Bull Entomol Res 75: 169-184.
30. McKechnie SW, Spackman ME, Naughton NE, Kovacs IV, Ghosn M, et al. (1993) Assessing budworm population structure in Australia using the A-T rich region of mitochondrial DNA; New Orleans. Proceedings of Beltwide Cotton Conference. pp. 838-840.
31. Stokes NH, McKechnie SW, Forrester NW, (1997) Multiple allelic variation in sodium channel gene from populations of Australian Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) detected via temperature gel electrophoresis. Aust J Entomol 36: 191-196.
32. Scott KD, Lawrence N, Lange CL, Scott LJ, Wilkinson KS, et al. (2005) Assessing moth migration and population structuring in Helicoverpa armigera (Lepidoptera: Noctuidae) at the regional scale: example from the Darling Downs, Australia. J Econ Entomol 98: 2210-2219.
33. Scott KD, Wilkinson KS, Lawrence N, Lange CL, Scott LJ, et al. (2005) Gene-flow between populations of cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae) is highly variable between years. Bull Entomol Res 95: 381-392.
34. Scott KD, Wilkinson KS, Merritt MA, Scott LJ, Lange CL, et al. (2003) Genetic shifts in Helicoverpa armigera Hübner (Lepidoptera: Noctuidae) over a year in the Dawson/Callide Valleys. Aust J Agr Res 54: 739-744.
35. Scott LJ, Lawrence N, Lange CL, Graham GC, Hardwick S, et al. (2006) Population dynamics and gene flow of Helicoverpa armigera (Lepidoptera: Noctuidae) on cotton and grain crops in the Murrumbidgee Valley, Australia. J Econ Entomol 99: 155-163.
36. Scott KD, Lange CL, Scott LJ, Gahan LJ, (2004) Isolation and characterization of microsatellite loci from Helicoverpa armigera Hübner (Lepidoptera: Noctuidae). Mol Ecol Notes 4: 204-205.
37. Ji Y-J, Zhang D-X, Hewitt GM, Kang L, Li D-M, (2003) Polymorphic microsatellite loci for the cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae) and some remarks on their isolation. Mol Ecol Notes 3: 102-104.
38. Weeks A, Endersby NM, Lange CL, Low A, Zalucki MP, et al. (2010) Genetic variation among Helicoverpa armigera populations as assessed by microsatellites: a cautionary tale about accurate allele scoring. Bull Entomol Res 100: 445-450.
39. Tay WT, Behere GT, Batterham P, Heckel DG, (2010) Generation of microsatellite repeat families by RTE retrotransposons in lepidopteran genomes. BMC Evol Biol 10: 144.
40. Lessa EP, (1992) Rapid survey of DNA sequence variation in natural populations. Mol Biol Evol 9: 323-330.
41. Palumbi SR, Baker CS, (1994) Contrasting population structure from nuclear intron sequences and mtDNA of Humpback whales. Mol Biol Evol 11: 426-435.
42. Tay WT, Behere GT, Heckel DG, Lee SF, Batterham P, (2008) Exon-Primed Intron-Crossing (EPIC) PCR markers of Helicoverpa armigera (Lepidoptera: Noctuidae). Bull Entomol Res 98: 509-518.
43. Zraket CA, Barth JL, Heckel DG, Abbott AG (1989) Genetic linkage mapping with restriction fragment length polymorphisms in the tobacco budworm, Heliothis virescens. In: Hagedorn HH, Hildebrand JG, Kidwell MG, Law JH, editors, 22-27 October 1989; Tucson, Arizona. Plenum Press. pp. 13-20.
44. Behere GT, Tay WT, Russell DA, Batterham P, (2008) Molecular markers to discriminate among four pest species of Helicoverpa (Lepidoptera: Noctuidae). Bull Entomol Res 98: 599-603.
45. Weir BS, Cockerham CC, (1984) Estimating F-statistics for the analysis of population structure. Evol 38: 1358-1370.
46. Goudet J, (1995) FSTAT (version 1.2): A computer program to calculate F-statistics. J Hered 86: 485-486.
47. Raymond M, Rousset F, (1995) GENEPOP (version 1.2): Population genetics software for exact tests and ecumenicism. J Hered 86: 248-249.
48. Rice WR, (1989) Analyzing tables of statistical tests. Evol 43: 223-225.
49. Kranthi KR, Jadhav DR, Kranthi S, Wanjari RR, Ali SS, et al. (2002) Insecticide resistance in five major insect pests of cotton in India. Crop Protec 21: 449-460.
50. Kranthi S, Dhawad CS, Naidu S, Bharose A, Chaudhary A, et al. (2009) Susceptibility of the cotton bollworm, Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) to the Bacillus thuringiensis toxinCry2Ab before and after the introduction of Bollgard-II. Crop Protec 28: 371-375.
51. Excoffier L, Smouse PE, Quattro JM, (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genet 131: 479-491.
52. Schneider S, Roessli D, Excoffier L (2000) Arlequin: A Software for Population Genetics Data Analysis, Version 2.000. 2.000 ed. Geneva: Genetics and Biometry Laboratory, Dept. of Anthropology, University of Geneva, Switzerland.
53. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genet 155: 945-959.
54. Evanno G, Regnaut S, Goudet J, (2005) Detecting the number of clusters of individuals using the software Structure: a simulation study. Mol Ecol 14: 2611-2620.
55. Chapuis M-P, Estoup A, (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24: 621-631.
56. Carlsson J, (2008) Effects of microsatellite null alleles on assignment testing. J Hered 99: 616-623.
57. Gordon K, Tay WT, Collinge D, Williams A, Batterham P (2009) Genetics and molecular biology of the major crop pest genus Helicoverpa. In: Goldsmith MR, Marec F, editors. Molecular Biology and Genetics of the Lepidoptera: CRC Press. pp. 219-238.
58. Johnson MS, Black R, (1984) The Wahlund effect and the geographical scale of variation in the intertidal limpet Siphonaria sp. Marine Biol 79: 295-302.
59. De Barro PJ, (2005) Genetic structure of the whitefly Bemisia tabaci in the Asia-Pacific region revealed using microsatellite markers. Mol Ecol 14: 3695-3718.
60. Brown JE, McBride CS, Johnson P, Ritchie S, Paupy C, et al. (2011) Worldwide patterns of genetic differentiation imply multiple 'domestications' of Aedes aegypti, a major vector of human diseases. Proc Biol Sci 278: 2446-2454.
61. Nielsen EE, Hansen MM, Ruzzante DE, Meldrup D, Gronkjaer P, (2003) Evidence of a hybrid-zone in Atlantic cod (Gadus morhua) in the Baltic and the Danish Belt Sea revealed by individual admixture analysis. Mol Ecol 12: 1497-1508.
62. Stipanovic RD, Lopez JD Jr, Dowd MK, Puckhaber LS, Duke SE, (2006) Effect of racemic and (+)- and (-)-gossypol on the survival and development of Helicoverpa zea larvae. J Chem Ecol 32: 959-968.
63. Kranthi KR, Kranthi NR, (2004) Modelling adaptability of cotton bollworm, Helicoverpa armigera (Hübner) to Bt-cotton in India. Curr Sci 87: 1096-1107.
64. Manjunath TH, Phalak VR, Subramanian S, (1970) First records of egg parasites of Heliothis armigera (Hubner) (Lepidoptera: Noctuidae) in India. Comm Inst Biol Contr Tech Bull 13: 111-115.
65. Zalucki MP, Furlong MJ, (2005) Forecasting Helicoverpa populations in Australia: A comparison of regression based models and a bio-climatic based modeling approach. Insect Sci 12: 45-56.
66. Fakrudin B, Prakash SH, Krishnareddy KB, Vijaykumar, Badari Prasad PR, et al. (2004) Genetic variation of cotton bollworm, Helicoverpa armigera (Hübner) of South Indian cotton ecosystem using RAPD markers. Curr Sci 87: 1654-1657.
67. Khadi BM, Kulkarni VN, Katageri IS, Vamadevaiah HM, Maralappanavar M (2003) Strengths, weaknesses, opportunities and threats (SWOT) analysis of Bt cotton in India. In: Swanepoel A, editor. 9-13 March 2003; Cape Town, South Africa. Agricultural Research Council- Institute for Industrial Crops. pp. 393-406.
68. Ravi KC, Mohan KS, Manjunath TM, Head G, Patil BV, et al. (2005) Relative abundance of Helicoverpa armigera (Lepidoptera: Noctuidae) on different host crops in India and the role of these crops as natural refuge for Bacillus thuringiensis cotton. Env Entomol 34: 59-69.
69. Directorate of Economics and Statistics, State Wise Land Use Statistics, Department of Agriculture and Cooperation, Ministry of Agriculture, Government of India (2007) Section 9. Area under crops (pulses, food grains & sugarcane) 1996-97 & 2005-06; Section 14. Area under crops (fibers) 1996-97 & 2005-06. Available: http://eands.dacnet.nic.in/state.htm.
70. Firempong S, Zalucki MP, (1990) Host plant preferences of populations of Helicoverpa-Armigera (Hubner) (Lepidoptera, Noctuidae) from different geographic locations. Aust J Zool 37: 665-673.
71. Jallow MFA, Zalucki MP, (1996) Within- and between-population variation in host-plant preference and specificity in Australian Helicoverpa Armigera (Hubner) (Lepidoptera: Noctuidae). Aust J Zool 44: 503-519.
72. Endersby NM, McKechnie SW, Ridland PM, Weeks AR, (2006) Microsatellites reveal a lack of structure in Australian populations of the diamondback moth, Plutella xylostella (L.). Mol Ecol 15: 107-118.
73. Franck P, Reyes M, Olivares J, Sauphanor B, (2007) Genetic architecture in codling moth populations: comparison between microsatellite and insecticide resistance markers. Mol Ecol 16: 3554-3564.