Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-24T00:49:15.624Z Has data issue: false hasContentIssue false
  • English
  • Français

Enhanced activity of carbohydrate- and lipid-metabolizing enzymes in insecticide-resistant populations of the maize weevil, Sitophilus zeamais

Published online by Cambridge University Press:  18 February 2008

R.A. Araújo ,
R.N.C. Guedes ,
M.G.A. Oliveira  and
G.H. Ferreira
R.A. Araújo
Affiliation:
Departamento de Biologia Animal, Universidade Federal de Viçosa, Viçosa, MG 36571-000, Brazil: School of Biology, University of Nottingham, University Park, Nottingham, NG7 2RD, UK:
R.N.C. Guedes*
Affiliation:
Departamento de Biologia Animal, Universidade Federal de Viçosa, Viçosa, MG 36571-000, Brazil: Biological Research Unit, USDA Grain Marketing and Production Research Center, 1515 College Avenue, Manhattan, KS 66502, USA:
M.G.A. Oliveira
Affiliation:
Departamento de Bioquímica e Biologia Molecular, Instituto de Biotecnologia Aplicada à Agropecuária (BIOAGRO), Universidade Federal de Viçosa, Viçosa, MG 36571-000, Brazil
G.H. Ferreira
Affiliation:
Departamento de Biologia Animal, Universidade Federal de Viçosa, Viçosa, MG 36571-000, Brazil:
*
*Author for correspondence Fax: (+55) 31 3899-4012 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Insecticide resistance is frequently associated with fitness disadvantages in the absence of insecticides. However, intense past selection with insecticides may allow the evolution of fitness modifier alleles that mitigate the cost of insecticide resistance and their consequent fitness disadvantages. Populations of Sitophilus zeamais with different levels of susceptibility to insecticides show differences in the accumulation and mobilization of energy reserves. These differences may allow S. zeamais to better withstand toxic compounds without reducing the beetles' reproductive fitness. Enzymatic assays with carbohydrate- and lipid-metabolizing enzymes were, therefore, carried out to test this hypothesis. Activity levels of trehalase, glycogen phosphorylase, lipase, glycosidase and amylase were determined in two insecticide-resistant populations showing (resistant cost) or not showing (resistant no-cost) associated fitness cost, and in an insecticide-susceptible population. Respirometry bioassays were also carried out with these weevil populations. The resistant no-cost population showed significantly higher body mass and respiration rate than the other two populations, which were similar. No significant differences in glycogen phosphorylase and glycosidase were observed among the populations. Among the enzymes studied, trehalase and lipase showed higher activity in the resistant cost population. The results obtained in the assays with amylase also indicate significant differences in activity among the populations, but with higher activity in the resistant no-cost population. The inverse activity trends of lipases and amylases in both resistant populations, one showing fitness disadvantage without insecticide exposure and the other not showing it, may underlay the mitigation of insecticide resistance physiological costs observed in the resistant no-cost population. The higher amylase activity observed in the resistant no-cost population may favor energy storage, preventing potential trade-offs between insecticide resistance mechanisms and basic physiological processes in this population, unlike what seems to take place in the resistant cost population.

Keywords

insecticide resistanceamylaselipasetrehalasefitness costcost mitigation
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 98 , Issue 4 , August 2008 , pp. 417 - 424
Copyright
Copyright © 2008 Cambridge University Press

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

Arrese, E.L., Canavoso, L.E., Jouni, Z.E., Pennington, J.E., Tsuchida, K. & Wells, M.A. (2001) Lipid storage and mobilization in insects: current status and future directions. Insect Biochemistry and Molecular Biology 31, 7–17.CrossRefGoogle ScholarPubMed
Arrese, E.L., Patel, R.T. & Soulages, J.L. (2006) The main triglyceride-lipase from the insect fat body is an active phospholipase A1: identification and characterization. Journal of Lipid Research 47, 2656–2667.CrossRefGoogle ScholarPubMed
Baker, J.E. (1986) Amylase/proteinase ratios in larval midguts of ten stored-product insects. Entomologia Experimentalis et Applicata 40, 41–46.CrossRefGoogle Scholar
Baker, J.E. (1987) Electrophoretic analysis of amylase isozymes in geographical strains of Sitophilus oryzae (L.), S. zeamais Motsch., and S. granarius (L.). Journal of Stored Products Research 23, 125–131.CrossRefGoogle Scholar
Baker, J.E. (1988) Dietary modulation of α-amylase activity in eight geographical strains of Sitophilus oryzae and Sitophilus zeamais. Entomologia Experimentalis et Applicata 46, 47–54.Google Scholar
Baker, J.E. (1991) Properties of glycosidases from the maize weevil, Sitophilus zeamais. Insect Biochemistry 21, 615–621.Google Scholar
Baker, J.E. & Woo, S.M. (1992) Digestion of starch granules by α-amylases from the rice weevil, Sitophilus oryzae: effect of starch type, fat extraction, granule size, mechanical damage, and detergent treatment. Insect Biochemistry and Molecular Biology 22, 529–537.Google Scholar
Candy, D.J., Becker, A. & Wegener, G. (1997) Coordination and integration of metabolism in insect flight. Comparative Biochemistry and Physiology 117, 497–512.Google Scholar
Caraway, W.T. (1959) A stable starch substrate for the determination of amylase in serum and other body fluids. American Journal of Clinical Pathology 32, 97–99.Google ScholarPubMed
Cherry, I.S. & Crandall, L.A. (1932) The specificity of pancreatic lipase: its appearance in the blood after pancreatic injury. American Journal of Physiology 100, 266–270.Google Scholar
Chown, S.L. & Nicolson, S.W. (2004) Insect Physiological Ecology: Mechanisms and Patterns. 243 pp. Oxford, Oxford University.CrossRefGoogle Scholar
Clarke, A. (1993) Seasonal acclimatization and latitudinal compensation in metabolism: do they exist? Functional Ecology 7, 139–149.Google Scholar
Coustau, C., Chevillon, C. & ffrench-Constant, R. (2000) Resistance to xenobiotics and parasites: can we count the cost? Trends in Ecology and Evolution 15, 378–383.CrossRefGoogle ScholarPubMed
Dahlqvist, A. (1968) Assay of intestinal disaccharides. Analytical Biochemistry 22, 99–107.CrossRefGoogle Scholar
Fiske, C.H. & Subbarow, Y. (1925) The colorimetric determination of phosphorus. Journal of Biological Chemistry 66, 375.CrossRefGoogle Scholar
Foster, S.P., Denholm, I. & Devonshire, A.L. (2000) The ups and downs of insecticide resistance in peach-potato aphids (Myzus persicae) in the U.K. Crop Protection 19, 873–879.CrossRefGoogle Scholar
Fragoso, D.B., Guedes, R.N.C. & Rezende, S.T. (2003) Glutathione S-transferase detoxification as a potential pyrethroid resistance mechanism in the maize weevil, Sitophilus zeamais. Entomologia Experimentalis et Applicata 109, 21–29.CrossRefGoogle Scholar
Fragoso, D.B., Guedes, R.N.C. & Peternelli, L.A. (2005) Developmental rates and population growth of insecticide-resistant and susceptible populations of Sitophilus zeamais. Journal of Stored Products Research 41, 271–281.CrossRefGoogle Scholar
Fragoso, D.B., Guedes, R.N.C. & Oliveira, M.G.A. (2007) Partial characterization of glutathione S-transferases in pyrethroid-resistant and -susceptible populations of the maize weevil, Sitophilus zeamais. Journal of Stored Products Research 43, 167–170.Google Scholar
Friedman, S. (1985) Carbohydrate metabolism. pp. 43–76in Kerkut, G.A. & Gilbert, L.I. (Eds). Comprehensiv Iinsect Physiology, Biochemistry and Pharmacology, vol. 10. Oxford, Pergamon.Google Scholar
Georghiou, G.P. & Taylor, C.E. (1977) Operational influences in evolution of insecticide resistance. Journal of Economic Entomology 70, 653–658.Google ScholarPubMed
Guedes, R.N.C., Lima, J.O.G., Santos, J.P. & Cruz, C.D. (1994) Inheritance of deltamethrin resistance in a Brazilian strain of maize weevil (Sitophilus zeamais Mots.). International Journal of Pest Management 40, 103–106.Google Scholar
Guedes, R.N.C., Lima, J.O.G., Santos, J.P. & Cruz, C.D. (1995) Resistance to DDT and pyrethroids in Brazilian populations of Sitophilus zeamais Motsch. (Coleoptera: Curculionidae). Journal of Stored Products Research 31, 145–150.CrossRefGoogle Scholar
Guedes, R.N.C., Oliveira, E.E., Guedes, N.M.P., Ribeiro, B. & Serrão, J.E. (2006) Cost and mitigation of insecticide resistance in the maize weevil, Sitophilus zeamais. Physiological Entomology 31, 30–38.CrossRefGoogle Scholar
Hill, S.R. & Orchard, I. (2005) In vitro analysis of the digestive enzymes amylase and α-glucosidase in the midgets of Locusta migratoria L. in response to the myosupressin, SchistoFLRFamide. Journal of Insect Physiology 51, 1–9.Google Scholar
Kunieda, T., Fujiyuki, T., Kucharski, R., Foret, S., Ament, S.A., Toth, A.L., Ohashi, K., Takeuchi, H., Kamikouchi, A., Kage, E., Morioka, M., Beye, M., Kubo, T., Robinson, G.E. & Maleszka, R. (2006) Carbohydrate metabolism genes and pathways in insects: insights from the honey bee genome. Insect Molecular Biology 15, 563–576.CrossRefGoogle ScholarPubMed
Marais, E. & Chown, S.L. (2003) Repeatability of standard metabolic rate and gas exchange characteristics in a highly variable cockroach, Perisphaeria sp. Journal of Experimental Biology 206, 4565–4574.CrossRefGoogle Scholar
McKenzie, J.A. (1996) Ecological and Evolutionary Aspects of Insecticide Resistance. 185 pp. Austin, TX, Academic Press.Google Scholar
Miller, G.L. (1959) Use of dinitrosalicylic acid reagent for the determination of reducing sugars. Analytical Chemistry 31, 426–428.Google Scholar
Oliveira, E.E., Guedes, R.N.C., Corrêa, A.S., Damasceno, B.L. & Santos, C.T. (2005) Resistência vs susceptibilidade a piretróides em Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae): há vencedor? Neotropical Entomology 34, 981–990.Google Scholar
Oliveira, E.E., Guedes, R.N.C., Tótola, M.R. & De Marco, P. Jr. (2007) Competition between insecticide-susceptible and -resistant populations of the maize weevil, Sitophilus zeamais. Chemosphere 67, 17–24.Google Scholar
Perez-Mendoza, J. (1999) Survey of insecticide resistance in Mexican populations of maize weevil, Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae). Journal of Stored Products Research 35, 107–115.Google Scholar
Rees, D.P. (1996) Coleoptera. pp. 1–39in Subramanyam, Bh. & Hagstrum, D.W. (Eds) Integrated Management of Insects in Stored Products. New York, Marcel Dekker.Google Scholar
Ribeiro, B.M., Guedes, R.N.C., Oliveira, E.E. & Santos, J.P. (2003) Insecticide resistance and synergism in Brazilian populations of Sitophilus zeamais (Coleoptera: Curculionidae). Journal of Stored Products Research 39, 21–31.CrossRefGoogle Scholar
Ribeiro, B., Guedes, R.N.C., Corrêa, A.S. & Santos, C.T. (2007) Fluctuating asymmetry in insecticide-resistant and insecticide-susceptible strains of the maize weevil, Sitophilus zeamais (Coleoptera: Curculionidae). Archives of Environmental Contamination and Toxicology 53, 77–83.Google ScholarPubMed
Roush, R.T. & McKenzie, J.A. (1987) Ecological genetics of insecticide and acaricide resistance. Annual Review of Entomology 32, 361–380.CrossRefGoogle ScholarPubMed
SAS Institute (2002) SAS/STAT user's guide, vol. 8., 3809 pp. Cary, NC, SAS.Google Scholar
SPSS (2000) SigmaPlot 2000 user's guide, revised edn, 35 pp. Chicago, SPSS.Google Scholar
Steele, J.E. (1982) Glycogen phosphorylase in insects. Insect Biochemistry 12, 131–147.CrossRefGoogle Scholar
Suarez, R.K., Darveau, C.-A., Welch, K.C. Jr., O'Brien, D.M., Roubik, D.W. & Hochachka, P.W. (2005) Energy metabolism in orchid bee flight muscles: carbohydrate fuels all. Journal of Experimental Biology 208, 3573–3579.Google Scholar
Subramanyam, Bh. & Hagstrum, D.W. (1996) Resistance measurement and management. pp. 331–397in Subramanyam, Bh. & Hagstrum, D.W. (Eds) Integrated Management of Insects in Stored Products. New York, Marcel Dekker.Google Scholar
Thompson, S.N., Borchardt, D.B. & Wang, L.-W. (2003) Dietary nutrient levels regulate protein and carbohydrate intake, gluconeogenic/glycolytic flux and blood trehalose level in the insect Manduca sexta L. Journal of Comparative Physiology 173B, 149–163.CrossRefGoogle Scholar
Tolman, J.H. & Steele, J.E. (1980) The control of glycogen metabolism in the cockroach hindgut: the effect of the corpora cardiaca-corpora allata system. Comparative Biochemistry and Physiology 66B, 59–65.Google Scholar
USDA (1980) Stored-Grain Insects. 43 pp. Washington, DC, ARS-USDA.Google Scholar
Warburg, O. & Christian, W. (1941) Isohierung und kristallisation des garungsferments enolase. Biochemische Zeitschrift 310, 384–421.Google Scholar
White, N.D.G. & Leesch, J.G. (1996) Chemical control. pp. 287–330in Subramanyam, Bh. & Hagstrum, D.W. (Eds) Integrated Management of Insects in Stored Products. New York, Marcel Dekker.Google Scholar