Ongoing insecticide resistance evolution in beet armyworm via changes in the utilization of pre-existing and new...

Little has been known until now about the population genomic processes underpinning pest insect species' rapid and ongoing adaptation to chemical insecticides. This paper elucidates these processes for six mutations encoding resistances to four insecticide classes in Chinese Spodoptera exigua: F116V in CYP9A186 against avermectins, T929I and L1014F in VGSC against pyrethroids, V1848I in VGSC against indoxacarb and I4790M and I4790K in RyR against diamides. Whole genome sequencing of 139 individuals from 20 populations across China revealed little genetic differentiation among the populations and soft selective sweeps for all six mutations. Ancestral Recombination Graphs (ARGs) showed at least five of them each had a single origin, with CYP9A186-F116V, VGSC-L1014F and RyR-I4790M and likely also RyR-I4790K arising before use of the corresponding insecticides. VGSC-T929I and VGSC-V1848I arose subsequently in VGSC-L1014F backgrounds. Bioassays of near-isogenic lines showed the double mutant VGSCs enhanced pyrethroid resistance and created pyrethroid/indoxacarb cross-resistance, respectively. While the ARGs predicted the younger RyR-I4790K mutation had overtaken RyR-I4790M in frequency by the time diamides were introduced, the latter has since surged again, to a frequency of ca. 95 %. Thus, S. exigua has evolved resistances to several major insecticides through soft selective sweeps of pre-existing mutations in a panmictic population, supplemented by new mutations that enhance or broaden resistance. The findings demonstrate the power of modern population genomics, including ARG, to reconstruct resistance evolution and, in so doing, improving preparedness for, and pro-active management of, resistance.