Global population genomic signature of Spodoptera frugiperda (fall armyworm) supports complex introduction events across the Old World

Abstract

Native to the Americas, the invasive Spodoptera frugiperda (fall armyworm; FAW) was reported in West Africa in 2016, followed by its chronological detection across the Old World and the hypothesis of an eastward Asia expansion. We explored population genomic signatures of American and Old World FAW and identified 12 maternal mitochondrial DNA genome lineages across the invasive range. 870 high-quality nuclear single nucleotide polymorphic DNA markers identified five distinct New World population clusters, broadly reflecting FAW native geographical ranges and the absence of host-plant preferences. We identified unique admixed Old World populations, and admixed and non-admixed Asian FAW individuals, all of which suggested multiple introductions underpinning the pest’s global spread. Directional gene flow from the East into eastern Africa was also detected, in contrast to the west-to-east spread hypothesis. Our study demonstrated the potential of population genomic approaches via international partnership to address global emerging pest threats and biosecurity challenges.

Complex multiple introductions drive fall armyworm invasions into Asia and Australia

“…We did not detect significant overall differences between the various invasive populations, and for the SE Asian and Australian populations the nucleotide diversity estimates were generally between 0.258-0.291. All invasive populations from Africa (Benin, Malawi, Uganda), SA/EA (India, China (CY, XP, XJ), South Korea), SEA (PNG, Malaysia (Johor, Kedah, Penang), Laos, Vietnam, Myanmar, Philippines), and Australia (WA (Kununurra), NT, QLD (Strathmore, Walkamin, Burdekin), NSW (Wee Waa)) showed higher average observed heterozygosity (Het obs ) than the average expected heterozygosity (Het exp ), with the highest Het obs seen in the Malawian population as also reported previously (Tay et al 2022d). Within the Australian populations, highest average observed heterozygosity was seen in the Strathmore population, while in populations in SEA (i.e., Myanmar, Philippines) and the EA (i.e., South Korea) all showed similar average Het obs .…”

“…Nucleotide diversity (π) varied across a narrow range with the lowest (0.237) being from the Malaysian Kedah State population (i.e., reflected its lab-colony background), and the highest from the Malawian population (0.324), similar to that reported (Tay et al 2022d; π = 0.279 – 0.329) in native and invasive populations based on the same set of 870 SNP loci. The high nucleotide diversity estimates from the SEA, Australia and South Korean populations likely reflected effects of limited (i.e., 870) highly polymorphic SNPs from non-coding genomic regions being used, and are comparable to the findings from Tay et al (2022d) that used the same sets of SNP loci. We did not detect significant overall differences between the various invasive populations, and for the SE Asian and Australian populations the nucleotide diversity estimates were generally between 0.258-0.291.…”

“…However, even in the native range, particularly in the tropics, this distinction seems to break down. Several studies have shown that, at the genetic level, the invasive populations are hybrids (e.g., Zhang et al 2020; Tay et al 2021b, 2022d).…”

“…Studies based on nuclear DNA markers involving African (e.g., Schlum et al 2021, Tay et al 2022d) and Asian (e.g., Jiang et al 2022) invasive populations identified gene flow patterns and signatures that suggested the FAW’s recent spread was due to multiple introductions, with invasive populations likely to have moved from the east (i.e., EA/SEA) to Africa (e.g., Tay et al 2022d). Genomic analyses of Chinese and African FAW populations by Gui et al (2020) also detected signatures that were best explained by independent introduction events in EA, and a likely east-to-west movement of the FAW.…”

The phylogeny of host choice in a global agricultural pest undergoing sympatric speciation.

“…Recent whole genome attempts to identify genomic differentiation between the strains have been mixed, with one study nding strain speci c nuclear SNPs 17 while others did not 18,19 . The lack of consistent evidence of nuclear differentiation between the strains led one group to conclude that the host strains do not exist and therefore that further efforts to identify strains are not only ineffectual but potentially a hindrance to mitigation efforts 19 . Related to this possibility are studies describing reproductive isolation mechanisms for the strains that appear to be independent of host and habitat selection.…”