Invasive fall armyworms are corn strain

Abstract

The fall armyworm (Spodoptera frugiperda) is one of the major pest insects in diverse crop plants, including maize, rice, and cotton. While the fall armyworm is native to North and South America, its invasion was first reported in West Africa in 2016. Since then, this species has rapidly spread across Sub-Saharan Africa, Asia, and Oceania, as well as Egypt and Cyprus. The fall armyworm is composed of two sympatric strains, the corn and rice strains, designated to their preferred host plants, in native areas. It remains surprisingly unclear whether invasive fall armyworms belong to the corn strain, rice strain, or hybrids of the two, despite a large number of population genetics studies. In this study, we performed population genomics analyses using globally collected 116 samples to identify the strains of invasive fall armyworms. We observed that invasive fall armyworms are genomically most similar to the corn strain. The reconstructed phylogenetic tree supports the hypothesis that invasive fall armyworms originated from the corn strain. All genomic loci of invasive populations exhibit higher genetic similarity to the corn strains compared to the rice strains. Furthermore, we found no evidence of gene flow from rice strains to invasive populations at any genomic locus. These results demonstrate that invasive fall armyworms belong to the corn strain. These results suggest that invasive fall armyworms likely have very limited potential to infest rice. Therefore, the management plan should primarily focus on crops preferred by the corn strain.

Keywords: Spodoptera frugiperda; Corn strain; Fall armyworm; Invasion; Pest genomics.

Figure 1

The phylogeny of FAW populations. (A) Principal component analysis revealed clear groupings of FAW individuals into three groups: sfC, sfR, and invasive populations. This figure was regenerated with the modification of Yainna et al. to visualize the population structure of FAW. A clear grouping among sfC, sfR, and invasive populations is shown. Along the first principal component, sfC appeared closer to invasive populations than sfR. (B) The TreeMIX analysis indicated that ancestral FAWs split into sfR and sfC + invasive FAWs, suggesting that invasive FAWs originated from sfC. (C) Gene flow from sfR to invasive populations was not detected with a range of edge numbers.

Figure 2

Invasive populations are genetically closer to sfC than sfR across the whole genome. (A) The log-transformed ratio of F_ST between sfC and invasive populations (Fst_sfC-inv) to F_ST between sfR and the invasive population (Fst_sfR-inv) is represented. If Fst_sfC-inv < Fst_sfR-inv, the log-transformed ratio will be below zero, indicated by the horizontal red dotted bar. Five 500 kb windows with Fst_sfC-inv > Fst_sfR-inv are marked with red asterisks. (B) The vertical blue bar represents the average difference between Fst_sfC-inv and Fst_sfR-inv across the five windows. The histogram illustrates the difference of F_ST calculated from two randomly generated native groups. The proportion of random groups with higher values than Fst_sfC-inv − Fst_sfR-inv corresponds to the p-values.

Figure 3

Testing gene flow from sfR to invasive populations. (A) If a mutation that changes from A to B originated from the common ancestor between sfC and invasive populations (indicated by the red stars), the genotype combination among sfC, invasive populations, sfR, and the outgroup will be BBAA. In the presence of incomplete lineage sorting, the gene tree may differ from the FAW strain tree in Fig. 1B. In such cases, when the frequency of ABBA and BABA will be the same. Then, D statistics, normalized differences between the frequency of ABBA and BABA will be zero. In the presence of gene flow from sfR to invasive populations, the invasive populations will acquire mutations generated in the sfR genealogy. As a result, the frequency of ABBA will be higher than that of BABA. Consequently, the D statistic will be higher than zero. (B) The majority of D statistics calculated across the genome are below zero, indicating a lack of gene flow. However, there are three loci with slightly higher D statistics than zero, as denoted by the red asterisks.