Fitness cost of resistance

Fitness costs of stored-product insect resistance have been studied by: 1) selection experiments, 2) measuring fitness components while controlling for genetic background (same strain before and after selection for resistance), and 3) measuring fitness components without controlling for genetic background. The fitness cost investigated included life histories (developmental time, fecundity, fertility and population growth), metabolism (respiration, fat body morphology and body weight) and behavior (walking, flying, mating and feeding). Studies have been done with 12 species of stored-product insect and more than 14 pesticides and pathogens. The majority of research (30 out of 39) has been done in Australia, Brazil, England and the US and since 1990 (32 out of 39).

Fitness costs were detected less frequently when studies controlled for genetic background. Jagadeesan et al. (2012) with Tribolium castaneum, Nguyen (2016) with Sitophilus oryzae and White and Bell (1990) with Cryptolestes ferrugineus concluded that fitness costs are either too minor to resolve or are not consistent enough for strategies, such as temporal rotation of chemicals or the use of refuges, to be effective in reducing resistance. Two studies (Lloyd and Parkin 1963, Tewari and Pandey 1978) concluded that resistant strains are more tolerant than susceptible strains to stresses such as starvation, heat, cold and desiccation. Research on the fitness costs of resistance for other species are reviewed by Coustau et al. (2011), Gassmann et al. (2009) and Kliot and Ghanim (2012).

For several insecticide classes, the role of fitness cost in reversing insecticide resistance has been studied for crop, urban and medically important disease vector insect pests (Freeman et al. 2020). Fitness cost reversed organophosphate resistance in 35 of 47 studies, pyrethoid resistance in 10 of 30 studies, organochlorine resistance in 2 of 12 studies, Bacillus thuringiensis resistance in 7 out of 10 studies, neonicotinoid resistance in 17 of 17 studies, and resistance other insecticide classes (Diflubenzuron, Pyriproxyfen, Fipronil, Spinosad, Spirotetramat, Emamectin benzoate, Spinetoram) in 10 of 11 studies. Only a few studies have examined the effects of environmental stress on reversion rate. Only 4 field studies examined reversion, all for organophosphate resistance. Fitness cost may be able to extend the life of a class of insecticide but modifier genes will eventually reduce fitness cost and make resistant insects more competitive with susceptible.

A few studies have been published on reversing insecticide resistance for 5 species of stored product insects (Oryzaephilus surinamensis by Mason 1998, Tribolium castaneum by Ahuja 1990, Beeman and Nanis 1986, Bhatia 1968, Trogoderma granarium by Amjad et al. 2022). Wool et al. (1992) found that repeated introductions of susceptible male Cadra cautella decreased larval survival after malathion treatment and the reversion rate to susceptibility increased with number of susceptible males released. For Tribolium castaneum, a few generation of combined release of insecticide susceptible males and insecticide treatment resulted in an increase in mortality from nearly zero to 40-80% depending on the release rate (Wool and Manheim 1980, Wool and Noiman 1983, Wool 1986). Kaduskar et al. (2022) reversed insecticide resistance using allelic-drive to insert dichlorodiphenyltrichloroethane (DDT) susceptible gene into Drosophila melanogaster population in the laboratory.

Fitness Cost Resistance References (Reversing Resistance References separate list at end)

Armitage, S. A. O., J. J. W. Thompson, J. Rolff, and M. T. Siva-Jothy. 2003. Examining costs of induced and constitutive immune investment in Tenebrio molitor. Journal of evolutionary biology 16(5): 1038-1044.

Arnaud, L., Y. Brostaux, L. K. Assié, C. Gaspar, and E. Haubruge. 2002a. Increased fecundity of malathion-specific resistant beetles in absence of insecticide pressure. Heredity 89: 425-429.

Arnaud, Ludovic, and Eric Haubruge. 2002b. Insecticide resistance enhances male reproductive success in a beetle. Evolution 56(12): 2435-2444.

Arnaud, Ludovic, Eric Haubruge, and M. J. G. Gage. 2005. The malathion-specific resistance gene confers a sperm competition advantage in Tribolium castaneum. Functional Ecology 19(6): 1032-1039.

Andreev, D., Kreitman, M., Phillips T.W., Beeman, R.W. and ffrench-Constant, R.H. 1999. Multiple origins of cyclodiene insecticide resistance in Tribolium castaneum (Coleoptera: Tenebrionidae). J. Mol. Evol. 48: 615-624.

Bajracharya, N. S., G. P. Opit, J. Talley, S. G. Gautam and M. E. Payton. 2016. Assessment of fitness effects associated with phosphine resistance in Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae) and Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). African Entomology 24(1): 39-49.

Bajracharya, N. S. 2013. Phosphine Resistance in Stored-Product Insect Pests: Management and Fitness Cost. Doctoral dissertation, Oklahoma State University.

Baker, J. E., R. W. Beeman, J. E. Throne and J. Perez-Mendoza. 1997. Fitness of an insecticide-resistant parasitic wasp Anisopteromalus calandrae. Resistant Pest Management 9: 12-14.

Baker, J., J. Perez-Mendoza, R. Beeman and J. Throne. 1998. Fitness of a malathion-resistant strain of the parasitoid Anisopteromalus calandrae (Hymenoptera : Pteromalidae). J. Econ. Entomol. 91: 50-55.

Beeman, R. W. and S. M. Nanis. 1986. Malathion resistance alleles and their fitness in the red flour beetle (Coleoptera: Tenebrionidae). J. Econ. Entomol. 79: 580-587.

Boots, M. and M. Begon, 1993. Trade-offs with resistance to a granulosis virus in the Indian meal moth, examined by a laboratory evolution experiment. Functional Ecology 7: 528–534.

Cordeiro, Erick Mauricio G., Alberto S. Corrêa, Conrado A. Rosi‐Denadai, Hudson Vaner V. Tomé and Raul Narciso C. Guedes. 2016. Insecticide resistance and size assortative mating in females of the maize weevil (Sitophilus zeamais). Pest Management Science DOI: 10.1002/ps.4437.

Correa, A. S., E. J. G. Pereira, E. M. G. Cordeiro, L. S. Braga and R. N. C. Guedes. 2011. Insecticide resistance, mixture potentiation and fitness in populations of the maize weevil (Sitophilus zeamais). Crop Protection 30: 1655-1666.

Correa, A. S., J. Tolledo, E. J. G. Pereira and R. N. C. Guedes. 2011. Bidirectional selection for body mass and correlated response of pyrethroid resistance and fitness in Sitophilus zeamais. J. Appl. Entomol. 135: 285-292.

Coustau, Christine, Christine Chevillon and Richard ffrench-Constant. 2000. Resistance to xenobiotics and parasites: can we count the cost? Trends in Ecology and Evolution 15: 378-383.

Daglish, G. J., M. K. Nayak and H. Pavic. 2014. Phosphine resistance in Sitophilus oryzae (L.) from eastern Australia: Inheritance, fitness and prevalence. J. Stored Prod. Res. 59: 237-244.

Daglish, Gregory J., Manoj K. Nayak, Hervoika Pavic and Lawrence W. Smith. 2015. Prevalence and potential fitness cost of weak phosphine resistance in Tribolium castaneum (Herbst) in eastern Australia. Journal of Stored Products Research 61: 54-58.

Demkovich, M., J. P. Siegel, B. S. Higbee and M. R. Berenbaum. 2015. Mechanism of Resistance Acquisition and Potential Associated Fitness Costs in Amyelois transitella (Lepidoptera: Pyralidae) Exposed to Pyrethroid Insecticides. Environ. Entomol. 44: 855-863.

Fragoso, D. B., R.N.C. Guedes and L. A. Peternelli. 2005. Developmental rates and population growth of insecticide-resistant and susceptible populations of Sitophilus zeamais. J. Stored Prod. Res. 41: 271-281.

Gassmann, Aaron J., Yves Carrière and Bruce E. Tabashnik. 2009. Fitness costs of insect resistance to Bacillus thuringiensis. Annual review of entomology 54: 147-163.

Guedes, R.N.C., E. E. Oliveira, N.M.P. Guedes, B. Ribeiro and J. E. Serrão. 2006. Cost and mitigation of insecticide resistance in the maize weevil, Sitrophilus zeamais. Physiol. Entomol. 31: 30-38.

Guedes, N.M.P., R.N.C. Guedes1, G.H. Ferreira and L.B. Silva 2009. Flight take-off and walking behavior of insecticide-susceptible and -resistant strains of Sitophilus zeamais exposed to deltamethrin. Bulletin of Entomological Research 99: 393–400.

Guedes, N. M. P., R. N. C. Guedes, L. B. Silva and E. M. G. Cordeiro. 2009. Deltamethrin-induced feeding plasticity in pyrethroid-susceptible and -resistant strains of the maize weevil, Sitophilus zeamais. Journal of Applied Entomology 133(7): 524-532.

Halliday, W. Ross. 1990. Comparative Fitness of Malathion-Resistant and Susceptible Indianmeal moth (Lepidoptera: Pyralidae). Journal of Entomological Science 25(2): 239-245.

Haubruge, E. and A. Arnaud. 2001. Fitness consequences malathion-specific resistance in red flour beetle (Coleoptera: Tenebrionidae) and selection for resistance in the absence of malathion. J. Econ. Entomol. 94: 552-557.

Heather, N. W. 1982. Comparison of population growth rates of malathion resistant and susceptible populations of the rice weevil, Sitophilus oryzae (Linnaeus) (Coleoptera: Curculionidae). Queensl. J. Agric. Anim. Sci. 39: 61-68.

Jagadeesan, R., P. J. Collins, G. J. Daglish, P. R. Ebert and D. I. Schlipalius. 2012. Phosphine Resistance in the Rust Red Flour Beetle, Tribolium castaneum (Coleoptera: Tenebrionidae): Inheritance, Gene Interactions and Fitness Costs. Plos One 7:e31582-e31582.

Kaur, R., Ebert, P.E., Walter, G.H., Swain and A.J., Schlipalius, D.I., 2013. Do phosphine resistance genes influence movement and dispersal under starvation? J. Econ. Entomol. 106: 2259-2266.

Kliot, Adi and Murad Ghanim. 2012. Fitness costs associated with insecticide resistance. Pest Manag. Sci. 68: 1431–1437

Lloyd, C.J. and E.A. Parkin. 1963. Further Studies on a Pyrethrum-Resistant Strain of Granary Weevil, Sitophilus Granarius (L). J. Sci. Food Agric. 14: 655-663.

Longstaff, B. 1991. An Experimental-Study of the Fitness of Susceptible and Resistant Strains of Sitophilus oryzae (L) (Coleoptera, Curculionidae) Exposed to Insecticide. J. Stored Prod. Res. 27:75-82.

Malekpour, R., M. A. Rafter, G. J. Daglish and G. H. Walter. 2016. Influence of phosphine resistance genes on flight propensity and resource location in Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae): the landscape for selection. Biological Journal of the Linnean Society 119: 348-358.

Mason, P.L. 1998. Selection for and against resistance to insecticides in the absence of insecticide: a case study of malathion resistance in the saw-toothed grain beetle, Oryzaephilus surinamensis (Coleoptera: Silvanidae). Bull. Entomol. Res. 88: 177-188.

McGaughey, W.H. and Beeman, R.W. 1988. Resistance to Bacillus thuringiensis in colonies of Indianmeal moth and almond moth (Lepidoptera: Pyralidae). J. Econ. Entomol. 81: 28–33

Memon, N. and Gilbert, F., 2013. Costs of resistance to insecticides in the maize weevil, Sitophilus zeamais (Coleoptera: Curculionidae). Pakistan J. Zool., 45: 874-878

Muggleton, J. 1982. A model for the elimination of insecticide resistance using heterozygous disadvantage. Heredity 49: 247–251.

Muggleton, J. 1983. Relative fitness of malathion-resistant phenotypes of Oryzaephilus surinamensis L (Coleoptera, Silvanidae). J. Appl. Ecol. 20:245-254.

Muggleton, J. 1986. Selection for malathion resistance in Oryzaephilus surinamensis (L.) (Coleoptera: Sylvanidae): fitness values of resistant and susceptible phenotypes and their inclusion in a general model describing the spread of resistance. Bulletin of Entomological Research 76: 469-480.

Nguyen, Tam Thi. 2016. Genetics of phosphine resistance in the rice weevil Sitophilus oryzae (L.) (Coleoptera: Curculionidae).PhD diss. The University of Queensland.

Oliveira, E. E., R.N.C. Guedes,M.R. Totola and P.DeMarco, Jr. 2007. Competition between insecticide-susceptible and-resistant populations of the maize weevil, Sitophilus zeamais. Chemosphere 69: 17-24.

Oppert, B., R.Hammel, J. E. Throne and K. J. Kramer. 2000 Fitness costs of resistance to Bacillus thuringiensis in the Indian meal moth, Plodia interpunctella. Entomol. Exp. Appl. 96: 281–287.

Pimentel, M.A.G., L. R. D’A. Faroni, R.N.C. Guedes, A. P. Neto and F. M. Garcia. 2006. Phosphine resistance, respiration rate and fitness consequences in Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae), pp. 345-351. In I. Lorini, B. Bacaltchuk, H. Beckel, D. Deckers, E. Sundfeld, J. P. dos Santos, J. D. Biagi, J. C. Celaro, L. R. D‟A. Faroni, L de O. F. Bortolini, M. R. Sartori, M. C. Elias, R.N.C. Guedes, R. G. da Fonseca, and V. M. Scussel (eds.). Proceedings of the 9th International Working Conference on Stored Product Protection. Brazilian Post-harvest Association – ABRAPOS, Campinas, Brazil. Brazilian Post-harvest Association – Associação Brasileira de Pós-Colheita (ABRAPOS), Campinas, São Paulo, Brazil.

Pimentel, M. A. G., L. R. D. Faroni, M. R. Totola and R. N. C. Guedes. 2007. Phosphine resistance, respiration rate and fitness consequences in stored-product insects. Pest Manag. Sci. 63: 876-881.

Sousa, A. H., L.R.D’A. Faroni, M.A.G. Pimentel and R.N.C. Guedes. 2009. Developmental and population growth rates of phosphine-resistant and –susceptible populations of stored-product insect pests. J. Stored Prod. Res. 45: 241-246.

Tewari, G. C. and N. D. Pandey. 1978. Effect of insecticide-resistance on the tolerance to various environmental stresses in rice weevil, Sitophilus oryzae Linnaeus. Bulletin of Grain Technology 16: 25-28.

Wang Jinjun, Zhao Zhimo and Li Longshu 1998. Ecological fitness of CA resistant and susceptible strains of Liposcelis bostrychophila B. (Psocoptera:Liposcelididae) p. 702-705. In: Jin Z, Liang Q, Liang Y, Tan X, Guan L, eds. Proceedings of the Seventh International Working Conference on Stored Prodcut Protection; China Sichuan Publishing House of Science and Technology, Chengdu.

White, N. and R. Bell. 1990. Relative fitness of a malathion-resistant strain of Cryptolestes ferrugineus (Coleoptera, Cucujidae) when development and oviposition occur in malathion-treated and untreated wheat kernels. J. Stored Prod. Res. 26: 23-37.

Yang, C., Dianxuan, W. and Collins P.J. 1998. Stored Product Protection: Fitness difference between phosphine-resistant and susceptible strains of Tribolium castaneum. In: Jin Z, Liang Q, Liang Y, Tan X, Guan L, eds. Proceedings of the Seventh International Working Conference on Stored Prodcut Protection; China Sichuan Publishing House of Science and Technology, Chengdu. pp 617–621.

Zhong, D., A. Pai, and G. Yan. 2005. Costly resistance to parasitism: Evidence from simultaneous quantitative trait loci mapping for resistance and fitness in Tribolium castaneum. Genetics 169: 2127-2135.

Reversing Resistance References 

Ahuja, DB. 1990. Reversion of Insecticide Resistance in Tribolium – Fate of p,p’DDT, Lindane, Malathion and Phosphine Resistance during Selection for Pirimiphos-Methyl Resistance in Tribolium castaneum (Herbst). Entomon 15(1–2): 79–81.

Amjad, Faizan, Farooq Ahmad, and Shahbaz Talib Sahi. 2022. Pyrethroid resistance and selection against Trogoderma granarium (Everts) in Punjab, Pakistan. International Journal of Tropical Insect Science 42(1): 191-202.

Beeman, R. W. and S. M. Nanis 1986. Malathion resistance alleles and their fitness in the red flour beetle (Coleoptera: Tenebrionidae). J. Econ. Entomol. 79: 580–587

Bhatia, S. Pradhan 1968. Studies on resistance to insecticides in Tribolium castaneum Herbst 1. Selection of a strain resistant to p,p’ DDT and its biological characteristics, Indian J. Entomol. 30: 13-32.

Freeman, Jamie C., Letícia B. Smith, Juan J. Silva, Yinjun Fan, Haina Sun, and Jeffrey G. Scott 2021. Fitness studies of insecticide resistant strains: lessons learned and future directions. Pest Management Science 77(9): 3847-3856.

Kaduskar, Bhagyashree, Raja Babu Singh Kushwah, Ankush Auradkar, Annabel Guichard, Menglin Li, Jared B. Bennett, Alison Henrique Ferreira Julio, John M. Marshall, Craig Montell, and Ethan Bier. 2022. Reversing insecticide resistance with allelic-drive in Drosophila melanogaster. Nature Communications 13(1), 291

Mason, P. L. 1998. Selection for and against resistance to insecticides in the absence of insecticide: a case study of malathion resistance in the saw-toothed grain beetle, Oryzaephilus surinamensis (Coleoptera: Silvanidae). Bulletin of Entomological Research 88(2): 177-188.

Wool, David 1986. Immigrant males as tools for reducing or preventing insecticide resistance. Environmental Quality and Ecosystem Stability 3: 77-85.

Wool, David, John H. Brower, and Nurit Kamin-Belsky 1992. Reduction of malathion resistance in caged almond moth, Cadra cautella (Walker)(Lepidoptera: Pyralidae), populations by the introduction of susceptible males. Journal of stored products research 28(1): 59-65.

Wool, David, and Ora Manheim. 1980. Genetically‐induced susceptibility to malathion in Tribolium castaneum despite selection for resistance. Entomologia Experimentalis et Applicata 28(2): 183-190.

Wool, D., and Sylvia Noiman. 1983. Integrated control of insecticide resistance by combined genetic and chemical treatments: a warehouse model with flour beetles (Tribolium; Tenebrionidae, Coleoptera). Zeitschrift für Angewandte Entomologie 95(1‐5): 22-30.