Reduced neuronal sensitivity and susceptibility of the fall armyworm, Spodoptera frugiperda, to pyrethroids in the absence of known knockdown mutations
Graphical abstract
Introduction
The fall armyworm (FAW), Spodoptera frugiperda (Lepidoptera: Noctuiidae), is a polyphagous herbivore that is known to be a major insect pest of multiple economically important row crops, such as corn, cotton, sorghum, and rice (Koffi et al., 2020; Montezano et al., 2018). The ability of FAW to feed on a wide range of host plants, the occurrence of multiple generations in a single growing season, and their ability to migrate make FAW one of the most significant economic pests of the Western Hemisphere. If left uncontrolled, FAW has been documented to cause up to 100% crop yield loss and global economic losses have been estimated to be upwards of $6 billion USD annually (Blanco et al., 2016; C. C. F. A. A. B. International, 2017). In addition to the economic damage, FAW is a serious threat to the food security of millions of people as FAW populations have recently become established across Africa, India, and China (Koffi et al., 2020; Goergen et al., 2016; Sharanabasappa et al., 2018; Wu et al., 2019), which rely heavily on maize and rice as staple food crops. To mitigate these global economic and food security concerns, synthetic insecticides remain a significant component of FAW control programs (Blanco et al., 2016; Brookes and Barfoot, 2016; Gutierrez-Moreno et al., 2019) despite the use of Bacillus thuringiensis technologies. Unfortunately, insecticide use rates have been documented to be extreme as is evidenced by Mexican maize farmers using an estimated 3000 tons of synthetic insecticides per year to control FAW (Blanco et al., 2014) and African countries using copious amounts of synthetic insecticides as an emergency response to slow immigration into new regions of the continent (Fotso Kuate et al., 2019).
As with other insect pests, the evolution of insecticide resistance is likely to be amplified in FAW by the high use rates and limited availability of registered mechanisms of action. Thus, current resistance management practices suggest alternating between five foliar insecticide mechanism of actions based on pre-planting, planting, vegetative, and reproductive stages of the plant as well as incorporating seed treatments and transgenic technologies (I. I. R. A. Committee, 2016). However, despite the implementation of resistance management practices, field-evolved resistance to multiple classes of synthetic insecticides has occurred in many populations across the world (Gutierrez-Moreno et al., 2019), which threatens the efficacy of current FAW control paradigms. Furthermore, although multiple insecticidal classes are available and suggested for use in FAW control programs, pyrethroids and organophosphates remain the most commonly used chemical insecticide classes (B. M. O. Agriculture, 2013).
Pyrethroid resistance in lepidopteran pests is multifactorial and considered to be due to reduced penetration, increased metabolism, and altered target-site sensitivity (Carvalho et al., 2013; Ottea et al., 1995; Nicholson and Miller, 1985; Yu et al., 2003). Furthermore, lambda (λ)-cyhalothrin resistance in FAW was shown to be driven by multiple recessive genes and additional studies have identified three different kdr- and super kdr-type mutations (Carvalho et al., 2013; Rios-Diez and Saldamando-Benjumea, 2011) that are analogous to known house fly gene regions causing insensitivity to pyrethroid insecticides (Miyazaki et al., 1996; Soderlun and Lee, 2001). Although metabolic and non-metabolic mechanisms are known to contribute to reduced pyrethroid susceptibility, the majority of efforts to determine mechanisms of resistance have focused on genetic analyses that identify target-site mutations analogous to kdr mutations established in model arthropod pests. Although this is a general predictor of insecticide sensitivity within that arthropod population, the presence or absence of target-site mutations does not necessarily predict the neuronal sensitivity or resistance ratios (RR) to the insecticide within the population of interest. Therefore, this study aimed to develop an electrophysiological assay to measure the spontaneous activity of the FAW central nervous system and provide a proof-of-concept method for the rapid quantification of reduced potency within a field-collected population of FAW at the level of the nerve.
Section snippets
Compounds and compound synthesis
Permethrin, λ-cyhalothrin, and dichlorvos were all purchased from Sigma-Aldrich Chemical Co. (St. Louis, MO, USA). The organophosphates chlorpyrifos and chlorpyrifos-oxon were purchased through ChemService Inc. (West Chester, PA, USA). All compounds were > 95% purity. Karate Z was generously donated by Dr. Sebe Brown (Assistant Professor, Louisiana State University). The solvents dimethyl sulfoxide (DMSO) and absolute ethanol were purchased from Sigma-Aldrich Chemical Co. A molecular sieve OP
Spontaneous firing rate of thoracic and abdominal ganglia of 3rd-instar FAW
To determine the ideal ganglia to use for determinations of potency for insecticides, we compared the spontaneous discharge frequency of abdominal and thoracic ganglia over a 60-min period. For thoracic ganglia, the mean firing rate was found to be 25 ± 6 Hz at 0–10 min and increased to an average firing rate of 31 ± 5 Hz, 31 ± 4 Hz, 29 ± 3 Hz for 10–20 min, 20–30 min, and 30–40 min, respectively, which were not significantly different from each other (Fig. 1C). A significant (p < .05)
Discussion
Previous studies have investigated the biochemical, molecular, and genomic characteristics of pyrethroid and organophosphate resistance in FAW with data indicating multiple mechanisms for insecticide resistance (Carvalho et al., 2013; Yu et al., 2003). Multiple mechanisms of pyrethroid resistance of other lepidopteran pests, such as H. virescens, has also been documented and it was suggested that expression of enhanced metabolism in the absence of reduced target-site sensitivity is inadequate
Declaration of Competing Interest
The authors declare no conflicts of interest.
Acknowledgements
We thank Dr. Sebe Brown (LSU, Entomology) from Macon Ridge Research Station in Winnsboro, Louisiana for providing farm plots of late corn to collect S. frugiperda and for providing Karate Z. We also thank Dr. Mike Stout (LSU, Entomology) for assistance with rearing S. frugiperda. Funding provided by USDA Hatch grant number CT-0273 (project # 94313), Louisiana Board of Regents (LEQSF(2016–2019)-RD-A-26; PI Swale).
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