Adaptation by copy number variation increases insecticide resistance in the fall armyworm

Abstract

Understanding the genetic basis of insecticide resistance is a key topic in agricultural ecology. The adaptive evolution of multi-copy detoxification genes has been interpreted as a cause of insecticide resistance, yet the same pattern can also be generated by the adaptation to host-plant defense toxins. In this study, we tested in the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), if adaptation by copy number variation caused insecticide resistance in two geographically distinct populations with different levels of resistance and the two host-plant strains. We observed a significant allelic differentiation of genomic copy number variations between the two geographic populations, but not between host-plant strains. A locus with positively selected copy number variation included a CYP gene cluster. Toxicological tests supported a central role for CYP enzymes in deltamethrin resistance. Our results indicate that copy number variation of detoxification genes might be responsible for insecticide resistance in fall armyworm and that evolutionary forces causing insecticide resistance could be independent of host-plant adaptation.

Geographic Monitoring of Insecticide Resistance Mutations in Native and Invasive Populations of the Fall Armyworm

“…P450 genes increase the level of synthetic insecticide resistance in FAW, and P450 gene duplication has been suggested as a possible cause underpinning resistance [ 23 ]. In total, 99 P450 genes were identified from the reference genome ( Table S2 ).…”

“…Bioassay experiments demonstrated that Chinese populations have resistance to pyrethroid insecticides [ 32 , 45 ]. As P450 genes are known to cause resistance against deltamethrin [ 23 ], a type of pyrethroid in FAWs, the increased P450 gene numbers might be responsible for this resistance. Chinese populations also have resistance against organophosphate [ 32 , 45 ] as well as oxadiazine and diamide [ 32 ].…”

“…For example, a population in Puerto Rico was reported to have resistance against a wide range of synthetic insecticides including flubendiamide, chlorantraniliprole, methomyl, thiodicarb, permethrin, chlorpyriphos, zeta-cypermethrin, deltamethrin, triflumuron, and spinetoram [ 22 ]. We observed that P450 genes cause resistance against deltamethrin [ 23 ]. Boaventura et al reported that I4734M and G4946E substitutions at the ryanodine receptor (RyR) cause resistance against diamides [ 24 ].…”

Circadian regulation of night feeding and daytime detoxification in a formidable Asian pest Spodoptera litura

“…Detoxification of abundant plant secondary compounds, much of which takes place in the fat body, is a vital process for survival on host plants. Detoxification of xenobiotics is also crucial for ecological adaptation to different host plants in highly polyphagous pests 7 , 39 , 40 . In S. litura and S. frugiperda , expansion of detoxification genes, such as cytochrome P450 (P450), carboxylesterase (COE), and glutathione S -transferase (GST), is reported to have enhanced the insects’ detoxification ability 7 , 40 .…”

“…Detoxification of xenobiotics is also crucial for ecological adaptation to different host plants in highly polyphagous pests 7 , 39 , 40 . In S. litura and S. frugiperda , expansion of detoxification genes, such as cytochrome P450 (P450), carboxylesterase (COE), and glutathione S -transferase (GST), is reported to have enhanced the insects’ detoxification ability 7 , 40 . Using RNA-seq, we performed a transcriptome analysis of 313 previously annotated detoxification genes in the midgut and fat body of S. litura 6th-instar larvae every 3 h during 24 h. These consisted of 138 SlituP450s , 47 SlituGSTs , 110 SlituCOEs , and 18 S. litura Aminopeptidase N ( SlituAPNs) based on the published S. litura genome 7 .…”