The mechanisms of metabolic resistance to pyrethroids and neonicotinoids fade away without selection pressure in the tarnished plant bug Lygus lineolaris

BACKGROUNDHeavy selection pressure prompted the development of resistance in a serious cotton pest tarnished plant bug (TPB), Lygus Lineolaris in the mid-southern United States. Conversely, a laboratory resistant TPB strain lost its resistance to five pyrethroids and two neonicotinoids after 36 generations without exposure to any insecticide. It is worthwhile to examine why the resistance diminished in this population and determine whether the resistance fade away has practical value for insecticide resistance management in TPB populations. RESULTSA field-collected resistant TPB population in July (Field-R1) exhibited 3.90-14.37-fold resistance to five pyrethroids and two neonicotinoids, while another field-collected TPB population in April (Field-R2) showed much lower levels of resistance (0.84-3.78-fold) due to the absence of selection pressure. Interestingly, after 36 generations without exposure to insecticide, the resistance levels in the same population [laboratory resistant strain (Lab-R)] significantly decreased to 0.80-2.09-fold. The use of detoxification enzyme inhibitors had synergistic effects on permethrin, bifenthrin and imidacloprid in resistant populations of Lygus lineolaris. The synergism was more pronounced in Field-R2 than laboratory susceptible (Lab-S) and Lab-R TPB population. Moreover, esterase, glutathione S-transferase (GST), and cytochrome P450-monooxygenases (P450) enzyme activities increased significantly by approximately 1.92-, 1.43-, and 1.44-fold in Field-R1, respectively, and 1.38-fold increased P450 enzyme activities in Field-R2 TPB population, compared to the Lab-S TPB. In contrast, the three enzyme activities in the Lab-R strain were not significantly elevated anymore relative to the Lab-S population. Additionally, Field-R1 TPB showed elevated expression levels of certain esterase, GST and P450 genes, respectively, while Field-R2 TPB overexpressed only P450 genes. The elevation of these gene expression levels in Lab-R expectedly diminished to levels close to those of the Lab-S TPB populations. CONCLUSIONOur results indicated that the major mechanism of resistance in TPB populations was metabolic detoxification, and the resistance development was likely conferred by increased gene expressions of esterase, GST, and P450 genes, the fadeaway of the resistance may be caused by reversing the overexpression of esterase, GST and P450. Without pesticide selection, resistant gene (esterase, GST, P450s) frequencies declined, and detoxification enzyme activities returned to Lab-S level, which resulted in the recovery of the susceptibility in the resistant TPB populations. Therefore, pest's self-purging of insecticide resistance becomes strategically desirable for managing resistance in pest populations. Published 2023. This article is a U.S. Government work and is in the public domain in the USA.