Hostname: page-component-848d4c4894-wg55d Total loading time: 0 Render date: 2024-05-22T14:17:30.378Z Has data issue: false hasContentIssue false

Autosomal inheritance of alphamethrin, a synthetic pyrethroid, resistance in Anopheles stephensi – Liston, a malaria mosquito

Published online by Cambridge University Press:  22 March 2013

T.P.N. Hari Prasad*
Affiliation:
Centre for Applied Genetics, Jnana Bharathi, Bangalore University, Bangalore 560 056, India
N.J. Shetty
Affiliation:
Centre for Applied Genetics, Jnana Bharathi, Bangalore University, Bangalore 560 056, India Janardhana Foundation, Nagadevanahalli, Jnana Bharathi Post, Bangalore 560 056, India
*
*Author for correspondence Phone: +91 80 22961301 Fax: +91 80 23212318 E-mail: hariprasad.tpn@gmail.com

Abstract

Anopheles stephensi – Liston (Culicidae: Diptera) is an important urban malarial vector in the Indian sub-continent, accounting for about 15% of the total annual malaria incidence. Chemical control represents a key strategy in the management of this insect vector. However, owing to erratic and continuous application of insecticides, resistance has become a common phenomenon among them and their control has become an uphill task. The genetics of alphamethrin, a synthetic pyrethroid resistance was studied to determine its mode of inheritance. The late third instar larvae were selectively inbred for 27 and ten generations to synthesize homozygous resistant (R) and susceptible (S) stocks, respectively, to the diagnostic dose of 0.12 mg l−1. The log-dosage probit mortality relationships and degree of dominance (D) were calculated. Resistance was observed in both sexes, the dosage-mortality (d-m) line of F1 was towards the resistant parent and the ‘D’ value was found to be 0.8 indicating alphamethrin resistant (amr) gene to be autosomal and incompletely dominant. The d-m lines of F2/backcross exhibited a clear plateau of mortality across a range of doses indicating monogenic resistance. The null hypothesis for monogenic resistance was tested from mortality data of backcross progeny compared with theoretical expectations using the χ2 test and was found to be non-significant. Understanding genetics of insecticide resistance is significant in prediction and management of resistant insects. The amr genes can be used as genetic marker in A. stephensi, which can be used in several applications in conducting basic and applied genetic research.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abbott, W.S. (1925) A method of computing the effectiveness of an insecticide. Journal of Economic Entomology 18, 265267.Google Scholar
Andreev, D., Kreitman, M., Phillips, T.W., Beeman, R.W. & Ffrench-Constant, R.H. (1999) Multiple origins of cyclodiene insecticide resistance in Tribolium castaneum (Coleoptera: Tenebrionidae). Journal of Molecular Evolution 48, 615624.Google Scholar
Bailey, N.T.J. (1959) Statistical Methods in Biology. pp. 1200. London, English Universities Press.Google Scholar
Bloomquist, J.R. (1988) Neurophysiological assays for the characterization and monitoring of pyrethroid resistance. pp. 543551in Lunt, G.G. (Ed.) The Molecular Basis of Drug and Pesticide Action. Amsterdam, Elsevier.Google Scholar
Bloomquist, J.R. (1993) Neuroreceptor mechanisms in pyrethroid mode of action and resistance. pp. 181226in Roe, M. & Kuhr, R.J. (Eds) Reviews in Pesticide Toxicology. Raleigh, NC, Toxicology Communications.Google Scholar
Bouvier, J.C., Bues, R., Boudinhon, L., Beslay, D. & Sauphanor, B. (2001) Deltamethrin resistance in codling moth: inheritance and number of genes involved. Heredity 87, 456462.CrossRefGoogle ScholarPubMed
Brogdon, W.G. & Barber, A.M. (1990) Fenitrothion-deltamethrin cross-resistance conferred by esterases in Guatemalan Anopheles albimanus. Pesticide Biochemistry and Physiology 37, 130139.CrossRefGoogle Scholar
Brogdon, W.G. & McAllister, J.C. (1998) Insecticide resistance and vector control. Emerging Infectious Diseases 4, 605613.Google Scholar
Chandrakala, B.N. & Shetty, N.J. (2006) Genetics studies of cyfluthrin resistance in Anopheles stephensi Liston – a malaria mosquito. pp. 4858in Sobti, R.C. et al. , (Ed.) Proceedings of Prof. G.P. Sharma Felicitation – New trends in Life Sciences. Chandigarh, Punjab University.Google Scholar
Cuamba, N., Morgan, J.C., Irving, H., Steven, A. & Wondji, C.S. (2010) High level of pyrethroid resistance in an Anopheles funestus population of the Chokwe district in Mozambique. PLoS ONE Jun 8; 5(6):e11010. doi: 10.1371/journal.pone.0011010.Google Scholar
Curtis, C.F., Akiyama, J. & Davidson, G. (1976) A genetic sexing system in Anopheles gambiae species A. Mosquito News 36, 492498.Google Scholar
Davies, T.G.E. & Williamson, M.S. (2009) Interactions of pyrethroids with the voltage-gated sodium channel. Bayer Crop Science Journal 62, 159178.Google Scholar
Denholm, I., Devine, G.J. & Williamson, M.S. (2002) Insecticide resistance on the move. Science 297, 22222223.Google Scholar
Dhingra, N., Jha, P., Sharma, V.P., Cohen, A.A., Jotkar, R.M., Rodriguez, P.S., Bassani, D.G., Suraweera, W., Laxminarayan, R. & Peto, R. (2010) Adult and child malaria mortality in India: a nationally representative mortality survey. Lancet 376, 17681774.Google Scholar
Elissa, N., Mouchet, J., Riviere, F., Meunier, J.Y. & Yao, K. (1993) Resistance of Anopheles gambiae s.s. to pyrethroids in Cote d'Ivoire. Annales de la Societe belge de medecine tropicale 73, 291294.Google Scholar
Enayati, A.A., Vatandoost, H., Ladonni, H., Townson, H. & Hemingway, J. (2003) Molecular evidence for a kdr-like pyrethroid resistance mechanism in the malaria vector mosquito Anopheles stephensi. Medical and Veterinary Entomology 17, 138144.Google Scholar
Ferrari, J.A. (1996) Insecticide resistance. pp. 512516in Beaty, B.J. & Marquardt, W.C. (Eds) The Biology of Disease Vectors. Niwol, CO, University Press of Colorado.Google Scholar
Ffrench-Constant, R.H., Daborn, P.J. & Goff, G.L. (2004) The genetics and genomics of insecticide resistance. Trends in Genetics 20, 163170.Google Scholar
Finney, D.J. (1971) Probit Analysis. pp. 25235. Cambridge, Cambridge University Press.Google Scholar
Georghiou, G.P. (1969) Genetics of resistance to insecticides in house flies and mosquitoes. Experimental Parasitology 26, 224255.CrossRefGoogle Scholar
Georghiou, G.P. & Garber, M.J. (1965) Studies on the inheritance of carbamate-resistance in the housefly (Musca domestica L.). Bulletin of the World Health Organization 32, 181196.Google Scholar
Georghiou, G.P. & Taylor, C.E. (1986) Factors influencing the evolution of resistance. pp. 157169in Pesticide Resistance: Strategies and Tactics for Management. Washington, DC, National Academy Press.Google Scholar
Ghosh, C. & Shetty, N.J. (2004) Tests for association of fenitrothion resistance with inversion polymorphism in the malaria vector, Anopheles stephensi. Nucleus 47, 164168.Google Scholar
Krogstad, D.J. (1996) Malaria as a reemerging disease. Epidemiologic Reviews 18, 7789.Google Scholar
Li, X., Schuler, M.A. & Berenbaum, M.R. (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Reviews of Entomology 52, 231253.Google Scholar
Liu, N., Xu, Q., Zhu, F. & Zhang, L. (2006) Pyrethroid resistance in mosquitoes. Insect Science 13, 159166.Google Scholar
Magesa, S.M., Aina, O. & Curtis, C.F. (1994) Detection of pyrethroid resistance in Anopheles mosquitos. Bulletin of the World Health Organization 72, 737740.Google Scholar
Malcolm, C.A. (1988) Current status of pyrethroid resistance in Anophelines. Parasitology Today 4, S13S15.Google Scholar
Mazzari, M.B. & Georghiou, G.P. (1995) Characterization of resistance to organophosphate, carbamate and pyrethroid insecticide in the field populations of Aedes aegypti from Venezeula. Journal of American Mosquito Control Association 11, 315332.Google Scholar
McCarroll, L. & Hemingway, J. (2002) Can insecticide resistance status affect parasite transmission in mosquitoes? Insect Biochemistry and Molecular Biology 32, 13451351.Google Scholar
Meinke, L.J., Siegfried, B.D., Wright, R.J. & Chandler, L.D. (1998) Adult susceptibility of Nebraska western corn rootworm (Coleoptera: Chrysomelidae) populations to selected insecticides. Journal of Economic Entomology 91, 594600.Google Scholar
Muller, P., Warr, E., Stevenson, B.J., Pignatelli, P.M., Morgan, J.C., Steven, A., Yawson, A.E., Mitchell, S.N., Ranson, H., Hemingway, J., Paine, M.J.I. & Donnelly, M.J. (2008) Field-caught permethrin-resistant Anopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids. PLoS Genetics Nov; 4(11):e1000286. doi: 10.1371/journal.pgen.1000286.CrossRefGoogle ScholarPubMed
Najera, J.A. & Zaim, M. (2001) Malaria vector control: insecticides for indoor residual spraying. WHO/CDS/WHOPES/2001.3.Google Scholar
Omer, S.M., Georghiou, G.P. & Irving, S.N. (1980) DDT/pyrethroid resistance inter-relationships in Anopheles stephensi. Mosquito News 40, 200209.Google Scholar
Perry, T., Batterham, P. & Daborn, P.J. (2011) The biology of insecticidal activity and resistance. Insect Biochemistry and Molecular Biology 41, 411422.Google Scholar
Priester, T.M. & Georghiou, G.P. (1980) Penetration of permethrin and knockdown in larvae of pyrethroid resistant and susceptible strains of the Southern House mosquito. Journal of Medical Entomology 73, 165167.Google Scholar
Rajashree, B.H. & Shetty, N.J. (1998 a) Genetic study of deltamethrin resistance in the malaria mosquito Anopheles stephensi Liston. Journal of Cytology and Genetics 22, 140143.Google Scholar
Rajashree, B.H. & Shetty, N.J. (1998 b) Biochemical studies on proteins and enzymes in deltamethrin resistance strains of Anopheles stephensi Liston, a malaria mosquito. pp. 9293 in 67th Annual Meeting of Society of Biological Chemists, New Delhi, December 19–21.Google Scholar
Raymond, M., Pasteur, N. & Georghiou, G.P. (1987) Inheritance of chlorpyrifos resistance in Culex pipiens L. (diptera: culicidae) and estimation of the number of genes involved. Heredity 58, 351356.Google Scholar
Robinson, A.S. (1986) Genetic sexing strain of Anopheles stephensi using dieldrin resistance. Journal of American Mosquito Control Association 2, 9395.Google Scholar
Roush, R.T. & Daly, J.C. (1990) The role of population genetics in resistance research and management. pp. 97152in Roush, R.T. & Tabashnik, B.E. (Eds) Pesticide Resistance in Arthropods. London, Chapman and Hall.CrossRefGoogle Scholar
Roush, R.T. & McKenzie, J.A. (1987) Ecological genetics of insecticide and acaricide resistance. Annual Review of Entomology 32, 361380.Google Scholar
Santolamazza, F., Calzetta, M., Etang, J., Barrese, E., Dia, I., Caccone, A., Donnelly, M.J., Petrarca, V., Simard, F., Pinto, J. & della Torre, A. (2008) Distribution of knock-down resistance mutations in Anopheles gambiae molecular forms in west and west-central Africa. Malaria Journal 7, 74. doi:10.1186/1475-2875-7-74.Google Scholar
Singh, O.P., Dykes, C.L., Das, M.K., Pradhan, S., Bhatt, R.M., Agrawal, O.P. & Adak, T. (2010) Presence of two alternative kdr-like mutations, L1014F and L1014S, and a novel mutation, V1010L, in the voltage gated Na+ channel of Anopheles culicifacies from Orissa, India. Malaria Journal 9, 146. doi:10.1186/1475-2875-9-146.Google Scholar
Singh, O.P., Dykes, C.L., Lather, M., Agrawal, O.P. & Adak, T. (2011) Knockdown resistance (kdr)-like mutations in the voltage-gated sodium channel of a malaria vector Anopheles stephensi and PCR assays for their detection. Malaria Journal 10, 59. doi:10.1186/1475-2875-10-59.Google Scholar
Shetty, N.J. (1983) Chromosomal translocations and inherited semisterility in the malaria vector, Anopheles fluviatilis-James. Indian Journal of Malariology 20, 4547.Google Scholar
Shetty, N.J. (1987) Genetic sexing system for the preferential elimination of females in Culex quinquefasciatus. Journal of American Mosquito Control Association 3, 8486.Google Scholar
Shetty, N.J. (2002) The genetic control of Anopheles stephensi – a malaria mosquito. pp. 4479in Raghunath, D. & Nayak, R. (Eds) Trends in Malaria and Vaccine Research: The Current Indian Scenario. New Delhi, Tata Mcgraw-Hill.Google Scholar
Stone, B.F. (1968) A formula for determining degree of dominance in case of monofactorial inheritance of resistance to chemicals. Bulletin of the World Health Organization 38, 325326.Google Scholar
Tabashnik, B.E. (1986) Computer stimulation as a tool for pesticide resistance management. pp. 195203 in Pesticide Resistance: Strategies and Tactics for Management. Washington, DC, National Academy Press.Google Scholar
Tiwari, S., Ghosh, S.K., Ojha, V.P., Dash, A.P. & Raghavendra, K. (2010) Reduced susceptibility to selected synthetic pyrethroids in urban malaria vector Anopheles stephensi: a case study in Mangalore city, South India. Malaria Journal 9, 179. doi:10.1186/1475-2875-9-179.Google Scholar
Verma, K.V.S. & Rahman, S.J. (1986) Development of knockdown resistance against fenvalerate in a DDT resistance stain of Anopheles stephensi. Current Science 55, 914916.Google Scholar
Williamson, M.S., Martinez-Torrez, D., Hick, C.A. & Devonshire, A.L. (1996) Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Molecular and General Genetics 252, 5160.Google Scholar
World Health Organization (WHO). (1964) Genetics of vectors and insecticide resistance. World Health Organization Technical Report Series 268.Google Scholar
World Health Organization (WHO). (1992) Vector resistance to insecticides: 15th report of the WHO expert committee on vector biology and control. Technical Report Series 818, 162.Google Scholar
World Health Organization (WHO). (2005) Guidelines for laboratory and field testing of mosquito larvicides. WHO/CDS/WHOPES/GCDPP/2005.13.Google Scholar
World Health Organization (WHO). (2006) Mosquito adulticides for indoor residual spraying and treatment of mosquito nets. Guidelines for testing. WHO/CDS/NTD/WHOPES/GCDPP/2006.3.Google Scholar
World Health Organization (WHO). (2011) World Malaria Report. Available online at http://www.who.int/malaria/world_malaria_report_2011/9789241564403_eng.pdfGoogle Scholar
Zaim, M., Aitio, A. & Nakashima, N. (2000) Safety of pyrethroid-treated mosquito nets. Medical and Veterinary Entomology 14, 15.Google Scholar