Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-05T05:02:01.590Z Has data issue: false hasContentIssue false
  • English
  • Français

Inheritance and activity of some esterases associated with organophosphate resistance in mosquitoes of the complex of Culex pipiens L. (Diptera: Cnlicidae)

Published online by Cambridge University Press:  10 July 2009

F. Villani ,
G. B. White ,
C. F. Curtis  and
S. J. Miles
F. Villani
Affiliation:
London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK.
G. B. White
Affiliation:
London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK.
C. F. Curtis
Affiliation:
London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK.
S. J. Miles
Affiliation:
London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK.
Get access Rights & Permissions [Opens in a new window]

Abstract

Eighteen strains of the complex of Culex pipiens L. from Africa, Asia and Europe were bioassayed for resistance to chlorpyrifos and electro-phoresed and stained for esterases. Susceptible strains showed only low activity esterase bands. The resistant strains of C. quinquefasciatus Say from hot countries (Liberia, Nigeria, Sri Lanka, Tanzania, Thailand) all showed the same two high intensity esterase bands (Rm 0·60 + 0·82). Different patterns of high esterase were found in resistant C. pipiens strains from cooler localities in Nairobi, Kenya (Rm 100), and Mont-pellier, France (Rm 0–50). Selection experiments on strains originally polymorphic for resistance and esterase pattern showed, without exception, that high esterase remained associated with resistance, and it is concluded that the association is almost certainly causal and not merely due to genetic linkage. The high intensity esterase bands were probably due to alleles of the loci Est-l, Est-2 and Est-3, separated by crossover distances of approximately 2·4 and 5·5 units, respectively. Strains monomorphic for what appeared to be the same high esterase pattern varied markedly in resistance level. Enzyme assays showed a direct relationship between levels of enzyme activity and resistance. Bioassays with fenthion and chlorpyrifos revealed differences in the relative resistance of C. quinquefasciatus from Colombo (Sri Lanka) and Dar-es-Salaam (Tanzania). Despite these differential degrees of cross-effectiveness, it is concluded that high intensity esterases are reliable indicators of organophosphate resistance in mosquitoes of the C. pipiens complex, although the possibility of other resistance mechanisms means that the lack of abnormally active esterases does not necessarily indicate the absence of resistance.

Type
Original Articles
Information
Bulletin of Entomological Research , Volume 73 , Issue 1 , March 1983 , pp. 153 - 170
Copyright
Copyright © Cambridge University Press 1983

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

Baker, J. P.. (1977). Assessment of the potential for and development of organophosphorus resistance in field populations of Myzus persicae. —Ann. appl. Biol. 86, 1–9.CrossRefGoogle Scholar
Baker, J. P.. (1978). Electrophoretic studies on populations of Myzus persicae in Scotland from March to July, 1976. —Ann. appl. Biol. 88, 1–11.CrossRefGoogle Scholar
Barr, A. R.. (1962). Resistance of mosquitoes to insecticides in California: a review. —Proc. Pap. Annual Conf. Calif. Mosquito Control Ass. 30, 88–103.Google Scholar
Barr, A. R.. (1975). Culex. — pp. 347–375in King, R. C.. (Ed.). Handbook of genetics 3. —874 pp. New York, Plenum.Google ScholarPubMed
Barr, A. R.. (1981). The Culex pipiens complex. —pp. 123–136 in Pal, RKitzmiller, J. B.Kanda, T.(Eds.). Cytogenetics and genetics of vectors. —263 pp. Tokyo, Kodansha.Google Scholar
Beranek, A. P.. (1974). Esterase variation and organophosphate resistance in populations of Aphis fabae and Myzus persicae. —Entomologia exp. appl. 17, 129–142.CrossRefGoogle Scholar
Beranek, A. P.Oppenoorth, F. J.. (1977). Evidence that the elevated carboxylesterase(esterase 2) in organophosphorus-resistant Myzus persicae (Sulz.) is identical with the organophosphate-hydrolyzing enzyme. —Pesticide Biochem. & Physiol. 7, 16–20.CrossRefGoogle Scholar
Berl, D.. (1981). Étude des estérases de deux souches d'Anopheles stephensi Liston, une sensible aux organochlorés et l'autre resistante. —Cah. Orstom, Ser. Entomol. mid.Parasitol. 19, 23–32.Google Scholar
Bhalla, S. C., Cajaiba, A. C. I.Carvalho, W. W. M.Santos, J. M.. (1974). Transloca-tions, inversions and correlation of linkage groups to chromosomes in the mosquito Culex pipiens fatigans. —Can. J. Genet. Cytol. 16, 837–850.CrossRefGoogle ScholarPubMed
Blackman, R. L.Devonshire, A. L.Sawicki, R. M.. (1977). Co-inheritance of increased carboxylesterase activity and resistance to organophosphorus insecticides in Myzus persicae (Sulzer). —Pestic. Sci. 8, 163–166.CrossRefGoogle Scholar
Brown, A. W. A.Pal, R.. (1971). Insecticide resistance in arthropods. —2nd edn, 491 pp. Geneva, Wld Hlth Org.Google ScholarPubMed
Bull, D. L.Whitten, C. J.. (1972). Factors influencing organophosphorus insecticide resistance in tobacco budworms. —agric. Fd Chem. 20, 561–564.Google Scholar
Bunting, S.VanEmden, H. F.. (1980). Rapid response to selection for increased esterasea ctivity on small populations of an apomictic clone of Myzus persicae. —Nature, Lond. 285, 502–503.Google Scholar
Curtis, C. F.Ellis, D. S.Doyle, P. E.Hill, N.Ramji, B. D.Irungu, L. W.Townson, H.. (in press). Susceptibility of aposymbiotic Culex quinquefasciatus to Wuchereria bancrofti. —J. Invertebr. Pathol. 41.Google Scholar
Curtis, C. F.Feachem, R. G.. (1981). Sanitation and Culex pipiens mosquitoes: a brief review. —J. trop. Med. Hyg. 84, 17–25.Google Scholar
Curtis, C. F.Pasteur, N.. (1981). Organophosphate resistance in vector populations of the complex of Culex pipiens L. (Diptera: Culicidae). Bull. ent. Res. 71, 153–161.CrossRefGoogle Scholar
DennhÖfer, L.. (1972). Die Zuordnung der Koppelungsgruppen zu den Chromosomen bei der Stechmiicke Culex pipiens L. —Chromosoma 37, 43–52.CrossRefGoogle ScholarPubMed
DeStordeur, E.. (1976). Esterases in the mosquito Culex pipiens pipiens L.: formal genetics and polymorphism of adult esterases. —Biochem. Genet. 14, 481–493.Google Scholar
Devonshire, A. L.. (1977). The properties of a carboxylesterase from the peach-potato aphid, Myzus persicae (Sulz.), and its role in conferring insecticide resistance. —Biochem. J. 167, 675–683.CrossRefGoogle ScholarPubMed
Devonshire, A. L.Sawicki, R. M.. (1979). Insecticide-resistant Myzus persicae as an example of evolution by gene duplication. —Nature, Lond. 280, 140–141.CrossRefGoogle Scholar
Dorval, C.Brown, A. W. A.. (1970). Inheritance of resistance to fenthion in Culex pipiens fatigans Wied. —Bull. Wld Hlth Org. 43, 727–734.Google Scholar
Dover, G. A.Flavell, R. B.. (Eds.) (1982). Genome evolution. —382 pp. London, Academic Press (Systematics Association Special Volume no. 20).Google Scholar
Dyte, C. E.Ellis, V. J.Lloyd, C. J.. (1966). Studies on the contrasting susceptibilities of the larvae of two hide beetles (Dermestes spp. Coleoptera, Dermestidae) to malathion. —J. stored Prod. Res. 1, 223–234.CrossRefGoogle Scholar
Dyte, C. E.Rowlands, D. G.. (1968). The metabolism and synergism of malathion in resistant and susceptible strains of Tribolium castaneum (Herbst) (Coleoptera, Tenebrionidae). —J. stored Prod. Res. 4, 157–173.Google Scholar
Freyvogel, T. A., Hunter, R. L.Smith, E. M.. (1968). Non-specific esterases in mosquitoes. —J. Histochem. Cytochem. 16, 765–789.CrossRefGoogle Scholar
Gargan, T. P.Barr, A. R.. (1977). Inheritance of an esterase locus in Culex pipiens. —Ann. ent. Soc. Am. 70, 402–408.CrossRefGoogle Scholar
Garnett, P.French, W. L.. (1971). A genetic study of an esterase in Culex pipiens quinquefasciatus. —Mosquito News 31, 379–386.Google Scholar
Georghiou, G. P.Ariaratnam, V.Pasternak, M. E.Lin, C. S.. (1975). Organophosphorus multiresistance in Culex pipiens quinquefasciatus in California. —J. econ. Ent. 68, 461–467.CrossRefGoogle ScholarPubMed
Georghiou, G. P.Pasteur, N.. (1978). Electrophoretic esterase patterns in insecticide-resistant and susceptible mosquitoes. —J. econ. Ent. 71, 201–205.CrossRefGoogle ScholarPubMed
Georghiou, G. P.Pasteur, N.. (1980). Organophosphate resistance and esterase pattern in a natural population of the southern house mosquito from California. —J. econ. Ent. 73, 489–492.Google Scholar
Georghiou, G. P.Pasteur, N.Hawley, M. K.. (1980). Linkage relationships between organophosphate resistance and a highly active esterase-B in Culex quinquefasciatus from California. —J. econ. Ent. 73, 301–305.Google Scholar
Georghiou, G. P.Saito, T.. (Eds.) (1983). Pest resistance to pesticides: challenges and prospects. —800pp. New York, Plenum.Google Scholar
Gratz, N. G.. (1973). Mosquito-borne disease problems in the urbanization of tropical countries. — CRC Crit. Rev. Environ. Contr. (Chem. Rubb. Co.) 3, 455–495.CrossRefGoogle Scholar
Guillet, P.Escaffre, H.Ouedraogo, M.QuillÉvÉrÉ, D.. (1980). Mise en évidence d'une résistance au téméphos dans le complexe Simulium damnosum (S. sanctipauli et S. soubrense) en Cöte d'lvoire (zone du programme de lutte contre l'onchocercose dans la rtgion du Bassin de la Volta).—Cah. ORSTOM, Ser. Entomol. med. Parasitol. 18, 291–299.Google Scholar
Guptavanij, P.Barr, A. R.. (1979). Plum-eye, a marker for the third linkage group in Culex pipiens (Diptera: Culicidae). —J. med. Entomol. 16, 219–222.CrossRefGoogle Scholar
Hamon, J.Burnett, G. F.Adam, J. P.Rickenbach, A.Grjebine, A.. (1967). Culex pipiens fatigans Wiedemann, Wuchereria bancrofti Cobbold, et le développement économique de l'Afrique tropicale. —Bull. WldHlth Org. 37, 217–237.Google Scholar
Hamon, J.Mouchet, J.. (1967). La résistance aux insecticides chez Culex pipiens fatigans Wiedemann. —Bull. Wld Hlth Org. 37, 277–286.Google Scholar
Ish-Horowicz, D.. (1982) Somatic gene amplification during Drosophila oogenesis. —Nature, Lond. 296, 806–807.Google Scholar
Kimura, T.Brown, A. W. A.. (1964). DDT-dehydrochlorinase in Aedes aegypti. —J. econ. Ent. 57, 710–716.CrossRefGoogle Scholar
Kimura, T.Youshi, A.Tipton, V. J.. (1971). Disc-electrophoretic analysis of some members of the Culex pipiens complex. —J. med. Entomol. 8, 1–16.CrossRefGoogle ScholarPubMed
Kuwahara, M.Miyata, T.Saito, T.Eto, M.. (1981). Relationship between high esterase activity and in vitro degradation of 14C–malathion by organophosphate.Google Scholar
Laird, M.. (Ed.) (1981). Blackflies. The future for biological methods in integrated control. —399 pp. London, Academic Press.Google Scholar
Loukas, M.Krimbas, C. B.. (1975). The genetics of Drosophila subobscura populations. V. A study of linkage disequilibrium in natural populations between genes and inversions of the E chromosome. —Genetics 80, 331–347.CrossRefGoogle Scholar
Matsumura, F.. (1975). Toxicology of insecticides. mdash;503 pp. New York & London, Plenum Press.CrossRefGoogle Scholar
Matsumura, F.Brown, A. W. A.. (1961). Biochemistry of malathion resistance in Culex tarsalis. —J econ. Ent. 54, 1176–1185.CrossRefGoogle Scholar
Meredith, S. E. O.. (1982). The improvement and refinement of electrophoretic techniques for the study of esterases and organophosphate resistance in the S. damnosum complex. —12 pp. Unpublished report to the Onchocerciasis Control Programme, World Health Organization.Google Scholar
Miles, S. J.. (1974). Biochemical polymorphisms and evolutionary relationships in the Culex pipiens complex (Diptera: Culicidae). —155 pp. Ph.D. dissertation, Univ. Western Australia, Perth.Google Scholar
MILES, S. J.PATERSON, H. E.. (1979). Protein variation and systematics in the Culex pipiens group of species.—Mosq. Syst. 11, 187–202.Google Scholar
Miyata, T.Honda, H.Saito, T.Ozaki, K.Sasaki, Y.. (1976). In vitro degradation of 14C-methyl malathion by organophosphate susceptible and resistant smaller brown planthopper, Laodelphax striatellus Fallén. —Botyu-Kagaku 41, 10–15.Google Scholar
Miyata, T.Saito, T.. (1976). Mechanism of malathion resistance in the green rice leaf-hopper, Nephotettix cincticeps Uhler (Hemiptera: Deltocephalidae). —J. Pestic. Sci. 1, 23–29.CrossRefGoogle Scholar
Narang, S.Seawright, J. A.Baker, R. H.. (1982 a). Linkage relationships and genetic mapping in Culex and Anopheles. —in Steiner, W. W. M.Tabachnik, W. J.Rai, K. S.Narang, S.. (Eds.). Recent developments in the genetics of insect disease vectors. Champaign, Illinois, Stipesm.Google Scholar
Narang, S.Seawright, J. A.Benedict, M. Q.. (1982 b). Linkage studies on bald antenna, a sex-limited mutant of Anopheles albimanus (Diptera: Culicidae). —J. med. Entomol. 19, 195–197.CrossRefGoogle Scholar
Needham, P. H.Sawicki, R. M.. (1971). Diagnosis of resistance to organophosphorus insecticides in Myzus persicae (Sulz.). —Nature, Lond. 230, 125–126.CrossRefGoogle Scholar
Ozaki, K.. (1969). The resistance to organophosphorus insecticides of the green rice leaf-hopper, Nephotettix cincticeps Uhler, and the small brown planthopper, Laodelphax striatellus Fallen. —Rev. Plant Prot. Res. 2, 1–15.Google Scholar
Ozaki, K.Kassai, T.. (1970). Biochemical genetics of malathion resistance in the smaller brown planthopper, Laodelphax striatellus. —Entomologia exp.appl. 13, 162–172.CrossRefGoogle Scholar
Ozaki, K.Koike, H.. (1965). Naphthyl acetate esterase in the green rice leafhopper, Nephotettix cincticeps Uhler, with special reference to the resistant colony of the organophosphorus insecticide. —Jap. J. appl. Ent. Zool. 9, 53–59.CrossRefGoogle Scholar
Pasteur, N.. (1977). Recherches de génétique chez Culex pipiens pipiens L. Polymorphisme enzymatique, autogenese et resistance aux insecticides organophosphorés. —162 pp. These de Doctorat d'Etat, University de Montpellier II, France.Google Scholar
Pasteur, N.Georghiou, G. P.. (1980). Analysis of esterases as a means of determining organophosphate resistance in field populations of Culex pipiens mosquitoes. —Proc. Pap. Annual Conf. Calif. Mosquito Vector Control Ass. 48, 74–77.Google Scholar
Pasteur, N.Georghiou, G. P.. (1981). Filter paper test for rapid determination of pheno-types with high esterase activity in organophosphate resistant mosquitoes. —Mosquito News 41, 181–183.Google Scholar
Pasteur, N.Georghiou, G. P.Ranasinghe, L. E.. (1980). Variations in the degree of homozygous resistance to organophosphorus insecticides in Culex quinquefasciatus Say. —Proc. Pap. Annual Conf. Calif. Mosquito Vector Control Ass. 48, 69–73.Google Scholar
Pasteur, N.Iseki, A.Georghiou, G. P.. (1981 a). Genetic and biochemical studies of the highly active esterases A' and B associated with organophosphate resistance in mosquitoes of the Culex pipiens complex. —Biochem. Genet. 19, 909–919.CrossRefGoogle Scholar
Pasteur, N.Sinegre, G.. (1975). Esterase polymorphism and sensitivity to Dursban organophosphorus insecticide in Culex pipiens populations. —Biochem. Genet. 13, 789–803.Google Scholar
Pasteur, N.Sinégre, G. (1978). Chlorpyrifos (Dursban) resistance in Culex pipiens L. from southern France: inheritance and linkage. —Experientia 34, 709–711.Google Scholar
Pasteur, N.SinÉgre, G.Gabinaud, A.. (1981 b). Est-2 and Est-3 polymorphisms in Culex pipiens L. from southern France in relation to organophosphate resistance. —Biochem. Genet. 19, 499–508.CrossRefGoogle Scholar
Pennington, N.E. (1968). Resistance of Culex tritaeniorhynchus Giles and Culex quinquefasciatus Say to malathion on Okinawa with notes on susceptibility to other insecticides. —Mosquito News 28, 193–198.Google Scholar
Peters, J.Nash, H. R.. (1977). Polymorphism of esterase 11 in Mus musculus, a further esterase locus on chromosome 8. —Biochem. Genet. 15, 217–226.CrossRefGoogle ScholarPubMed
Plapp, F. W.. (1976). Biochemical genetics of insecticide resistance. —A. Rev. Ent. 21, 179–197.Google Scholar
Poulik, M. D.. (1957). Starch gel electrophoresis in a discontinuous system of buffers. —Nature, Lond. 180, 1477–1479.CrossRefGoogle Scholar
Reiter, P.. (1982). Migration and the "dilution" of resistance genes. —Trans. R. Soc. trop. Med. Hyg. 76, 282–283.CrossRefGoogle ScholarPubMed
Sasa, M.Shirasaka, A.Wada, Y.Kanda, T.. (1967). Comparative studies on some morphological and physiological characters of the Culex pipiens complex of Japan and southern Asia. —Jap. J. exp. Med. 37, 475–504.Google ScholarPubMed
Sawicki, R. M.. (1973). Recent advances in the study of the genetics of resistance in the housefly, Musca domestica. —Pestic. Sci. 4, 501–512.CrossRefGoogle Scholar
Schimke, R. T.. (Ed.) (1982). Gene amplification. —340 pp. New York, Cold Spring Harbor Laboratory.Google ScholarPubMed
Schimke, R. T.Kaufman, R. J.Alt, F. W.Kellems, R. F.. (1978). Gene amplification and drug resistance in cultured murine cells. —Science, N.Y. 202, 1051–1055.Google Scholar
Shaw, C. R.Prasad, R.. (1970). Starch gel electrophoresis of enzymes. A compilation of recipes. —Biochem. Genet. 4, 297–320.CrossRefGoogle ScholarPubMed
Simon, J. P.. (1969). Esterase isozymes in the mosquito Culex pipiens fatigans. Developmental and genetic variation. —Ann. ent. Soc. Am 62, 1307–1311.CrossRefGoogle ScholarPubMed
Stone, B. F.Brown, A. W. A.. (1969). Mechanisms of resistance to fenthion in Culex pipiens fatigans Wied. —Bull. Wld Hlth Org. 40, 401–408.Google ScholarPubMed
Sudderuddin, K. I.. (1973 a). An electrophoretic study of some hydrolases from an OP-sus-ceptible and an OP-resistant strain of the green peach aphid, Myzus persicae (Sulz.). —Comp. Biochem. Physiol. (B) 44, 923–929.Google Scholar
Sudderuddin, K. I.. (1973 b). An in vitro study of esterases hydrolysing specific substrates of an OP-susceptible and an OP-resistant strain of the green peach aphid Myzus persicae Sulz. —Comp. & gen. Pharmacol. 4, 219–223.CrossRefGoogle Scholar
Tadano, T.. (1969 a). Genetical linkage of malathion-resistance in Culex pipiens L. —Jap. J. exp. Med. 39, 13–16.Google Scholar
Tadano, T.. (1969 b). Genetical relationships between malathion-resistance and fenthion-resistance in larvae of Culex pipiens pollens Coquillett. —Jap. J. sanit. Zool. 20, 158–160.CrossRefGoogle Scholar
Tadano, T.. (1970 a). Genetics of cross–resistance to organophosphates, Abate, fenitrothion and malathion in larvae of Culex pipiens pollens Coquillett. —Jap. J. exp. Med. 40, 59–66.Google Scholar
Tadano, T.. (1970 b). Recombination values between the white eye and factors for resistance to dieldrin, Abate, fenthion and fenitrothion in larvae of Culex pipiens pollens Coquillett. —Jap. J. sanit. Zool. 21, 156–160.CrossRefGoogle Scholar
Tadano, T.Sato, H.. (1970). Parathion-resistance in larvae of Culex pipiens pollens Coquillett. —Jap. J. sanit. Zool. 21, 186–188.CrossRefGoogle Scholar
Thomas, V.. (1970). Fenthion-resistance in Culex pipiens fatigans Wiedemann in Kuala Lumpur, West Malaysia. —Southeast Asian J. trop. Med. & Public Health 1, 93–98.Google Scholar
Van Asperen, K.. (1962). A study of housefly esterases by means of a sensitive colorimetric method. —J. Insect Physiol. 8, 401–416.CrossRefGoogle Scholar
Wagner, R. P.Selander, R. K.. (1974). Isozymes in insects and their significance. —A. Rev. Ent. 19, 117–138.CrossRefGoogle Scholar
White, G. B.. (1971). The present importance of domestic mosquitoes (Culex pipiens fatigans Wiedemann) in East Africa and recent steps towards their control. —E. Afr. med. J. 48, 266–274.Google ScholarPubMed
White, G. B.. (1979). The identification of mosquitoes as vectors of malaria and filariasis. —Symp. Br. Soc. Parasit. 17, 103–143 (see pp. 132–133).Google Scholar
Whitten, C. J.Bull, D. L.. (1970). Resistance to organophosphorus insecticides in tobacco budworms. —J. econ. Ent. 63, 1492–1495.Google Scholar
WHO (World Health Organization) (1970). Insecticide resistance and vector control. —Tech. Rep. Ser. Wld Hlth Org. no. 443, 279 pp. (see pp. 73–79).Google Scholar
WHO (World Health Organization) (1980). Resistance of vectors of disease to pesticides. —Tech. Rep. Ser. Wld Hlth Org. no. 655, 82 pp.Google Scholar
Wilkinson, C. F.. (Ed.) (1976). Insecticide biochemistry and physiology. — 768 pp. London, Heyden&New York, Plenum.CrossRefGoogle Scholar
Wood, R. J.. (1981). Insecticide resistance: genes and mechanisms. —pp. 53–96 in Bishop, J. A.Cook, L. M.. (Eds.). Genetic consequences of man made change. —409 pp. London, Academic Press.Google Scholar
Yasutomi, K.. (1970). Studies on organophosphate-resistance and esterase activity in the mosquitoes of the Culex pipiens group. I. —Jap. J. sanit. Zool. 21, 41–45.Google Scholar
Yasutomi, K.. (1971) Studies on diazinon-resistance and esterase activity in Culex tritaenio-rhynchus. I. —Jan. J. sanit. Zool. 22, 8–13.CrossRefGoogle Scholar
Yasutomi, K.. (1983). Role of detoxication esterases in insecticide resistance. —pp. 249–264 in Georghiou, G. P.Saito, T.. (Eds.). Pest resistance to pesticides: challenges andprospects. —800 pp. New York, Plenum.Google Scholar