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

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.

Incipient speciation between host-plant strains in the fall armyworm.

BACKGROUND: Recent advancement in speciation biology proposes that genetic differentiation across the whole genome (genomic differentiation, GD) may occur at the beginning of a speciation process and that GD itself may accelerate the rate of speciation. The fall armyworm (FAW, Spodoptera frugiperda) has been used as a model species to study the process of speciation between diverging host-plant strains. We showed in a previous study that GD between the host-plant strains occurred at the beginning of a speciation process based on a population genomics analysis from a population in Mississippi (USA), providing empirical support for the theoretical prediction. In a recent paper, however, panmixia was reported in FAW based on the genomic analysis of 55 individuals collected from Argentina, Brazil, Kenya, Puerto Rico, and the mainland USA. If panmixia is true, the observed differentiation in Mississippi could be at most a phenomenon specific to a geographic population, rather than a status during a speciation process. In this report, we reanalyzed the resequencing data to test the existence of population structure according to host plants using different bioinformatics pipelines. RESULTS: Principal component analysis, FST statistics, and ancestry coefficient analysis supported genetic differentiation between strains regardless of the used bioinformatics pipelines. The strain-specific selective sweep was observed from the Z chromosome, implying the presence of strain-specific divergence selection. Z chromosome has a particularly high level of genetic differentiation between strains, while autosomes have low but significant genetic differentiation. Intriguingly, the re-sequencing dataset demonstrates the spread of Bacillus thuringiensis resistance mutations from Puerto Rico to the US mainland. CONCLUSIONS: These results show that a pair of host-plant strains in FAW experience genomic differentiation at the beginning of a speciation process, including Z chromosome divergent selection and possibly hitchhiking effect on autosomal sequences.

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

Field evolved resistance to insecticides is one of the main challenges in pest control. The fall armyworm (FAW) is a lepidopteran pest species causing severe crop losses, especially corn. While native to the Americas, the presence of FAW was confirmed in West Africa in 2016. Since then, the FAW has been detected in over 70 countries covering sub-Saharan Africa, the Middle East, North Africa, South Asia, Southeast Asia, and Oceania. In this study, we tested whether this invasion was accompanied by the spread of resistance mutations from native to invasive areas. We observed that mutations causing Bt resistance at ABCC2 genes were observed only in native populations where the mutations were initially reported. Invasive populations were found to have higher gene numbers of cytochrome P450 genes than native populations and a higher proportion of multiple resistance mutations at acetylcholinesterase genes, supporting strong selective pressure for resistance against synthetic insecticides. This result explains the susceptibility to Bt insecticides and resistance to various synthetic insecticides in Chinese populations. These results highlight the necessity of regular and standardized monitoring of insecticide resistance in invasive populations using both genomic approaches and bioassay experiments.