The evolutionary process of invasion in the fall armyworm (Spodoptera frugiperda)

Abstract

The fall armyworm (FAW; Spodoptera frugiperda) is one of the major agricultural pest insects. FAW is native to the Americas, and its invasion was first reported in West Africa in 2016. Then it quickly spread through Africa, Asia, and Oceania, becoming one of the main threats to corn production. We analyzed whole genome sequences of 177 FAW individuals from 12 locations on four continents to infer evolutionary processes of invasion. Principal component analysis from the TPI gene and whole genome sequences shows that invasive FAW populations originated from the corn strain. Ancestry coefficient and phylogenetic analyses from the nuclear genome indicate that invasive populations are derived from a single ancestry, distinct from native populations, while the mitochondrial phylogenetic tree supports the hypothesis of multiple introductions. Adaptive evolution specific to invasive populations was observed in detoxification, chemosensory, and digestion genes. We concluded that extant invasive FAW populations originated from the corn strain with potential contributions of adaptive evolution.

Figure 1

Samples used in this study (A) Map indicating the countries from which samples of Spodoptera frugiperda were sequenced. The blue color indicates the native countries of S. frugiperda. The green, red, yellow, and orange colors indicate that the invasion was reported in 2016, 2017, 2018, and 2019 respectively. The map was generated using MapChart. (B) The numbers of sfC and sfR samples according to the host plants using different diagnostic markers (TPI or mitochondrial COX1).

Figure 2

Invasive origins inferred from mitochondrial or nuclear sequences (A) Maximum-likelihood phylogenetic tree was reconstructed from the full-length mitochondrial COX1 gene (1536 bp). The red and blue clades indicate sfR and sfC, respectively. The circles on the branches show bootstrap support values higher than 90%. A branch leading to Spodoptera exigua was deleted while the position was indicated for a visualization purpose. (B) The result of the principal component analysis showed that FAW populations are composed of Rice, Corn, and Corn.Mex groups and that invasive populations belong to the Corn groups. (C) TreeMIX analysis shows that the Corn group was derived from the ancestry of the Corn.Mex and the Corn groups. The arrows indicate the direction of gene flow, which was detected from the Rice group to the Corn group. The color gradient of the arrows indicate the migration weight.

Figure 3

A single origin of invasive populations (A) Ancestry coefficient analysis from SNVs showed homogeneous genomic sequences of invasive populations. (B) A nuclear BIO-NJ phylogenetic tree was reconstructed from whole nuclear genome sequences. The circles on the branches show bootstrap support values higher than 90%. The Corn.Mex group and the Rice group are indicated to the corresponding nodes. The remaining individuals belong to the Corn Group. Invasive individuals were also indicated to the corresponding node. The phylogenetic tree was visualized using iTOL v4.

Figure 4

Loci under adaptive evolution The composite likelihood of being targeted by selective sweeps in invasive populations. The x-axis represents the coordinates of grids in the reference genomes, and the y-axis is the composite likelihood of each grid. The red asterisks indicate potential targets of invasive population-specific selective sweeps.

Figure 5

Models of the invasive process in FAW First, FAWs were introduced from the Corn group between sfC and sfR, possibly multiple times. Second, a stable population was established in a location in the Old World. This population experienced growth in size, and FAW invasion was first reported. Third, range expansion occurred from this population. The first step occurred before 2016, implying the existence of a lag phase. Adaptive evolution contributed to the second and third steps, potentially through insecticide resistance or host plant adaptation.