High-depth resequencing reveals hybrid population and insecticide resistance characteristics of fall armyworm (Spodoptera frugiperda) invading China

Abstract

The rapid wide-scale spread of fall armyworm (Spodoptera frugiperda) has caused serious crop losses globally. However, differences in the genetic background of subpopulations and the mechanisms of rapid adaptation behind the invasion are still not well understood. Here we report a 393.25-M chromosome-level genome assembly of fall armyworm with scaffold N50 of 13.3 M consisting of 23281 annotated protein-coding genes. Genome-wide resequencing of 105 samples from 16 provinces in China revealed that the fall armyworm population comprises a complex inter-strain hybrid, mainly with the corn-strain genetic background and less of the rice-strain genetic background, which highlights the inaccuracy of strain identification using mitochondrial or Tpi genes. An analysis of genes related to pesticide-and Bt-resistance showed that the risk of fall armyworm developing resistance to conventional pesticides is very high, while remaining currently susceptible to Bt toxins. Laboratory bioassay results showed that insects invading China carry resistance to organophosphate and pyrethroid pesticides, which is consistent with the results of molecular scanning of resistance-related genes, but are sensitive to genetically modified maize expressing Cry1Ab in field experiments. Additionally, we found that two mitochondrial fragments are inserted into the nuclear genome, and the insertion event occurred after the differentiation of the two strains. This study represents a valuable advancement toward the analysis of genetic differences among subpopulations and improving management strategies for fall armyworm.

Genome of the webworm Hyphantria cunea unveils genetic adaptations supporting its rapid invasion and spread

“…Further analyses showed that 94.54 and 92.96% eukaryotic conserved genes were found in the genome of H. cunea by CEGMA and BUSCO, respectively, suggesting that the genome sequence we obtained was largely complete (Tables S3-S6). The genome of H. cunea possesses a comparatively longer contig N50 among all genomes of Lepidoptera species sequenced so far, the top 4 are as follows: Operophtera brumata (6.38 Mb) [40], Spodoptera frugiperda (5.6 Mb) [48], Papilio bianor (5.5 Mb) [49], and H. cunea (3.09 Mb), further confirming the high quality of the genome sequence of H. cunea (Table 1). Homology analysis of the H. cunea genome led to the identification of 2142 pairs of one-to-one single-copy orthologs among twelve species.…”

Monitoring of Target-Site Mutations Conferring Insecticide Resistance in Spodoptera frugiperda

“…More than 30 unique resistance-associated mutations including L1014F or combinations thereof have been described in VGSC in many other different species [53]. Three mutations (T929I, L932F and L1014F) at the VGSC have been recently described in pyrethroid-resistant S. frugiperda from Brazil [29] and one of the mutations, L932F, was detected in FAW populations from China [54]. Our genotyping results revealed the absence of the L1014F mutation in almost all analyzed samples, except for one population from Indonesia (K-I, Table S1), where only two heterozygotes out of 30 individuals were detected.…”

“…Two sympatric host plant strains of S. frugiperda have been previously described: the corn strain and the rice strain, which prefers forage grasses and rice [9][10][11]. Recent studies have reported that S. frugiperda populations present in Asia and Africa are an inter-strain hybrid, with the genetic background mostly from the corn strain [54,66]. Therefore, we were interested in the host-plant strain composition of our samples and analyzed individual larvae of different populations using recently described markers by RFLP and PCR.…”

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

“…Both strains are observed in invasive populations, while the relative proportion of the identified strains depends on their geographic location [25][26][27] In this paper, we aim at testing the potential role of balancing selection in the global invasion of the FAW using population genomics. First, we identified genomic SNV (Single Nucleotide Variants) from 177 samples in both native and invasive populations.…”

“…We identified the strain from a maximum likelihood phylogenetic tree reconstructed from the full sequences of mitochondrial Cytochrome C Oxidase subunit I (COX1) gene, which is the universal barcode gene and also commonly used for FAW strain identification 35 . The COX1 phylogenetic tree shows high bootstrapping confidence scores for both sfC and sfR (bootstrap supporting value > 92%) ( [25][26][27] . We also observed that both native hybrid populations and invasive populations exhibit reproductive barriers between sfC and sfR from genetic differentiation (F ST ) with the statistical significance ( Fig.…”