Characterization of Indoxacarb Resistance in the Fall Armyworm: Selection, Inheritance, Cross-Resistance, Possible Biochemical Mechanisms, and Fitness Costs

Abstract

The fall armyworm, Spodoptera frugiperda (J.E. Smith), is a voracious insect pest that is difficult to control due to resistance to insecticides and Bt proteins. We assessed cross-resistance, resistance mechanism, and fitness costs based on the life history traits of S. frugiperda. We established an S. frugiperda strain selected for resistance to indoxacarb (Ind-SEL) from a field-collected population and an unselected strain, Ind-UNSEL. Results indicated that after 24 generations of selection, the resistance to indoxacarb was increased by 472.67-fold as compared to the Ind-UNSEL. There was high cross-resistance to deltamethrin (31.23-fold) with very low or negligible cross-resistance to chlorantraniliprole, emamectin benzoate, and/or methoxyfenozide in the Ind-SEL population. Butoxide synergist increased susceptibility to indoxacarb, indicating that P450 enzymes may be involved in indoxacarb resistance. Significantly longer developmental time of larvae extended pupal duration, shorter adult longevity, and lower fecundity were observed in Ind-SEL as compared with the Ind-UNSEL population. The Net reproductive rate (R0) was the only growth parameter that differs between crosses of Ind-SEL♂ × Ind-UNSEL♀ (176 ± 46) and Ind-SEL♀ × Ind-UNSEL♂ (328 ± 57). On the other hand, all population growth parameters differ between Ind-SEL and Ind-UNSEL strains. Our work contributes to the growing body of research that demonstrates the importance of strain genetics in fitness cost experiments and helps resistance management programs make decisions.

Risk Assessment of Fluxametamide Resistance and Fitness Costs in Fall Armyworm (Spodoptera frugiperda)

“…It could be attributed to the fact that the potential cross-resistance between fluxametamide and emamectin benzoate in the fluxametamide-selected strain of FAW was a possible resultant effect of a similar detoxification mechanism concerning elevated GST activities. The involvement of P450 in the indoxacarb resistance [65] and GST in the resistance to synthetic pyrethroid insecticides [71] in FAW have been reported by previous workers. In this study, the activities of detoxification enzymes were mild in fluxametamide-selected generations of FAW; we speculate that the limited resistance development rate is correlated with the slow metabolic detoxification process.…”

“…It might be attributed to the fact that fluxametamide has shown an asymmetric nature of cross-resistance with emamectin benzoate, which is an example of a sudden unpredictable phenomenon [61,62]. Several cases of cross-resistance between Cry1 proteins [63], spinosad and spinetoram [64], indoxacarb, and deltamethrin [65] in FAW have already been reported previously. Roy et al [32] investigated a similar type of cross-resistance pattern between fluxametamide and emamectin benzoate in P. xylostella, another invasive lepidopteran insect pest.…”

“…When a single molecule chooses an isoenzyme that can interact with other compounds, cross-resistance to insecticides with independent modes of action may be conceivable [67]. Detoxification enzymes, including cytochrome P450s, GST, and esterase genes, have been demonstrated to promote the capacity of FAW to metabolically detoxify a wide range of chemical insecticides [24,65,68]. In the present study, a gradual increase in the activities of P450 and GST was observed after the continuous exposure of fluxametamide to FAW, and was found to be significantly different at Flux-SEL (F10) generation.…”

Frequency and diversity of indoxacarb resistance in Australian Helicoverpa armigera (Lepidoptera: Noctuidae)

“…Evaluation of fitness and stability in selected populations has a high level of practical importance for determining resistance risk associated with the use of insecticides and can be useful for formulating insecticide resistance management strategies (Carrière and Tabashnik 2001, 2023). Recent studies of indoxacarb resistant noctuid populations showed significantly slower growth and development, and lower fecundity in S. frugiperda (Hafeez et al 2022b) and H. armigera (Cui et al 2018) suggesting the presence of indoxacarb resistance genes in these populations was deleterious. In the present study a lack of stability in a heterogeneous population of the UN1U3-10 strain resulted in a decline in resistance ratio from 313-fold to 53-fold after the strain had been reared for 6 generations in the absence of selection, indicating that a fitness cost may be associated with the allele(s) that confer resistance in the UN1U3-10 strain, the effects of which cumulate over multiple generations causing an overall decline in the number of resistant individuals in the population.…”

Synthesis and Biological Activity of Sulfamate–Adamantane Derivatives as Glucosinolate Sulfatase Inhibitors

“…In addition, cytochrome P450 (CYP450), glutathione S -transferases (GSTs), and carboxylesterases (CAREs) of insects are known to be central to pesticide metabolism and resistance. − Inhibitors of the above detoxifying enzymes, such as triphenyl phosphate (TPP), diethyl maleate (DEM), and piperonyl butoxide (PBO), could be used to attenuate the pesticide resistance in insects. , P. xylostella GSSs were identified as a specific protective strategy to cope with host plant defense compounds, while the function of GSSs in the metabolism of conventional pesticides has not been reported, as far as we know.…”