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.

Global genomic signature reveals the evolution of fall armyworm in the Eastern hemisphere

“…Our f-branch results also indicate gene flow between the two genetic clusters (Figure 4b), which aligns with the field conditions in the Americas (Dumas, 2015). Our phylogenetic results, along with previous studies, suggest that the rice strain may represent an earlier divergent population (Fiteni et al, 2022;Yainna et al, 2022). Previous studies have reported detection of rice-strain Tpi in the Eastern hemisphere based on a single site, TpiE-183 (Jing et al, 2020;Tay et al, 2022).…”

“…Previous studies based on above two markers have indicated that the invasive FAW exhibit hybrid genotypes, with a predominant corn-strain ratio based on the Tpi marker (Nagoshi et al, 2019(Nagoshi et al, , 2022Zhang et al, 2020). Subsequent genome-wide analysis supported the notion that invasive populations were mainly of corn-strain genetic background (Yainna et al, 2022;Zhang et al, 2020). However, a divergent Tpi haplotype has been detected, with 10 unique single nucleotide polymorphisms (SNPs) compared to previously reported corn-or rice-strain genotype in the Americas, suggesting a more complex genetic differentiation of invasive populations (Nagoshi, 2019;Zhang et al, 2020).…”

“…The results based on our covered collections indicate that the invasive population is much closer to the American corn-strain population (W4 cluster). However, it is still possible that the invasive population may originate from a divergent population, considering the presence of more differentiated populations in the native region (Yainna et al, 2022).…”

“…However, the specific origin(s) of the invasion remains unclear, and different hypotheses have been proposed based on various research methods. Studies using CO I and Tpi markers have indicated that the invasive FAW originated from a single source with high similarity to samples from Florida and the Greater Antilles (Nagoshi et al, 2017, 2020), while other studies utilizing mitogenome or whole‐genome analyses have supported multiple introductions of FAW into Africa and suggested South America as a potential source of invasion (Tay et al, 2022; Yainna et al, 2022). There are even phylogenetic analyses that proposed Asian origins and east‐to‐west movements of FAW in the Eastern hemisphere (Rane et al, 2023; Tay et al, 2022).…”

Complex multiple introductions drive fall armyworm invasions into Asia and Australia

“…Genome-wide SNP loci demonstrated that invasive FAW populations from SEA and Australia exhibited admixed genomic signatures similar to that observed in other invasive populations 33,34 . While the current invasive populations in Africa and Asia likely arrived already as hybrids as suggested by Yainna et al 68 , the Malaysia Kedah State population was potentially established by offspring of a non-admixed female. Distinct admixture patterns in Malaysian FAW populations between Kedah and Johor/Penang states therefore suggested that establishment of these populations was likely as separate introduction events.…”