Adaptation by copy number variation increases insecticide resistance in fall armyworms

Abstract

Insecticide resistance is a major main challenge in pest control, and understanding its genetic basis is a key topic in agricultural ecology. Detoxification genes are well-known genetic elements that play a key role in adaptation to xenobiotics. The adaptive evolution of detoxification genes by copy number variations has been interpreted as a cause of insecticide resistance. However, the same pattern can be generated by the adaptation to host-plant defense toxins as well. In this study, we tested in fall armyworms (Lepidoptera Spodoptera frugiperda) if adaptation by copy number variation is the cause of the increased level of insecticide resistance from two geographic populations with different levels of resistance and two strains with different host plants. Following the generation of an assembly with chromosome-sized scaffolds (N50 = 13.2Mb), we observed that these two populations show a significant allelic differentiation of copy number variations, which is not observed between strains. In particular, a locus with almost complete allelic differentiation (Fst > 0.8) includes a cluster of P450 genes, which are well-known key players in detoxification. Detoxification genes are overrepresented in the genes with copy number variations, and the observed copy number variation appears to have beneficial effects in general. From this result, we concluded that copy number variation of detoxification genes in fall armyworms plays a key role in the insecticide resistance but not in the adaptation to host-plants, suggesting that the evolution of insecticide resistance may occur independently from host-plant adaptation.

Genomic and transcriptomic analysis unveils population evolution and development of pesticide resistance in fall armyworm Spodoptera frugiperda

“…Genomes size assembled in this study fell within the scope of 246 Mb to 809 Mb of the Lepidopteran species (Triant et al, 2018). However, the size of the genome reported in the current study is larger than that of the previously assembled FAW genomes (Kakumani et al, 2014;Gouin et al, 2017;Nam et al, 2018Nam et al, , 2019Nandakumar et al, 2017;Zhang et al, 2019Zhang et al, , 2020Xiao et al, 2020) (Table 1). The extra regions of c h r 2 7 c h r 2 8 c h r2 9 ch r3 0 chr3 1 Figure 1.…”

“…Taking the advantages of stLFR and Hi-C technologies with long fragment reads, super high coverage and reads quality, we de novo assembled a high-quality FAW genome, which is so far the largest FAW genome assembly with a size of 542.42 Mb (Nandakumar et al, 2017;Zhang et al, 2019Zhang et al, , 2020Xiao et al, 2020). The genome of FAW was greatly different (Kakumani et al, 2014;Gouin et al, 2017;Nam et al, 2018Nam et al, , 2019Nandakumar et al, 2017;Zhang et al, 2019Zhang et al, , 2020Xiao et al, 2020) (Table 1), which led to the different genome size and unmapped reads among different individuals. However, the FAW genome assembled in the current study is a high-quality genome in most of the key parameters, including the BUSCO evaluation, WGS mapping rate and RNA mapping rate.…”

“…However, the FAW genomes from its cell lines or strains are fragmented without anchoring on chromosomes before the year 2019 (Gouin et al, 2017;Kakumani et al, 2014;Nam et al, 2018Nam et al, , 2019Nandakumar et al, 2017). With the advancement in genome sequencing and assembly technology, three chromosome-level genome assemblies of FAW have been published or pre-printed (Nam et al, 2019;Zhang et al, 2019Zhang et al, , 2020Xiao et al, 2020). Nevertheless, only two of them are available to the public (Xiao et al, 2020;Zhang et al, 2020).…”

Genomic balancing selection is key to the invasive success of the fall armyworm

“…Mbp, respectively. L90 is 26, which is close to the chromosome number in FAW (31), implying nearly chromosome-sized scaffolds in this assembly. BUSCO analysis 30 demonstrates that this assembly has the highest correctness among all published FAW genome assemblies (Table S1).…”

Genomic balancing selection is key to the invasive success of the fall armyworm

“…with ~20X coverage was used to perform whole genome resequencing with 150bp paired-end and 300bp insert length. Then, we combined the resequencing data from Puerto Rico and Mississippi, which were generated for our previous studies (Hiseq 2500, Hiseq 4000, and Novaseq 6000) 31,32 , as well as the resequencing data of Brazil, Malawi, and Uganda from CSIRO (Novaseq 6000, 150bp paired-end sequencing) 28 . Lastly, resequencing data from China 33 was also combined with the dataset.…”