Complex multiple introductions drive fall armyworm invasions into Asia and Australia

Abstract

The fall armyworm (FAW) Spodoptera frugiperda is thought to have undergone a rapid ′west-to-east′ spread since 2016 when it was first identified in western Africa. Between 2018 and 2020, it was also recorded from South Asia (SA), Southeast Asia (SEA), East Asia (EA), and Pacific/Australia (PA). Population genomic analyses enables the understanding of pathways, population sources, and gene flow in this notorious agricultural pest species. Using neutral single nucleotide polymorphic (SNP) DNA markers, we detected genome introgression that suggested most populations were overwhelmingly C- and R-strain hybrids. SNP and mitochondrial DNA markers identified multiple introductions that were most parsimoniously explained by anthropogenic-assisted spread, i.e., associated with international trade of live/fresh plants and plant products, and involved ′bridgehead populations′ in countries to enable successful pest establishment in neighbouring countries. Distinct population genomic signatures between Myanmar and China do not support the ′African origin spread′ nor the ′Myanmar source population to China′ hypotheses. Significant genetic differentiation between populations from different Australian states supported multiple pathways involving distinct SEA populations. Our study identified Asia as a biosecurity hotspot and a FAW genetic melting pot, and demonstrated the use of genome analysis to disentangle preventable human-assisted pest introductions from unpreventable natural pest spread

Resistance bioassays and allele characterisation inform analysis ofSpodoptera frugiperda(Lepidoptera: Noctuidae) introduction pathways in Asia and Australia

“…Susceptible and resistant alleles from the three previously reported loci (i.e., F290V, G227A, A201S) from the ACE-1 gene provided evidence to support multiple independent introductions across the invasive S. frugiperda populations, such as in (b) Indonesia (#2; G227A) and South Korea (#4; F290V), and in (c) China (Hubei province (#10-13); G227A) as indicated by the red arrows. In (d) Australia, newly established S. frugiperda populations between Queensland (e.g., #27, #28 (Walkamin), #29 (Strathmore), #32 (Burdekin), and Western Australia (i.e., #2 (Kununurra)/Northern Territory (e.g., #21 (Bluey’s Farm)) suggested this likely involved multiple introductions from diverse populations from neighbouring countries and likely arrived via separate pathways and entry points (see also Rane et al 2022).…”

“…Mapping of partial mtCOI gene was carried out within Geneious v11.1.5 (Biomatters Ltd, Auckland, NZ) using the Geneious Mapper program with assembly parameters specified to ‘Low Sensitivity / Fastest’, with no trimming before mapping, and the ‘Fine Tuning’ option set to ‘Iterate 2 times’ to map reads to the consensus from the previous iteration. Full mitochondrial DNA genomes of all individuals were also assembled following the procedures as outlined in (Otim et al 2018) and have been reported by Rane et al (2022). For all resistance alleles of interest (ABCC2, ACE-1, RyR, VGSC; see Table S1), base-sequence at the genomic location for individuals listed in Table 1 was extracted from the alignment file using BCFTOOLS MPILEUP followed by CALL, since BBMAP does not report ‘non-variant’ sites.…”

“…The moth’s strong flight ability (Rose et al 1975, Sparks 1979, Jones et al 2019), its potential to contaminate certain commodities, and ability to act as a ‘hitchhiker’ in trade (Early et al 2018) contribute to its rapid spread. Whole genome analyses of invasive S. frugiperda populations from various African nations, India, China, Southeast Asia, and Australia also suggested that a high proportion of S. frugiperda individuals were hybrids of the C- and R-strains (Gui et al 2020, Tay et al 2021, 2022a; Zhang et al 2020, Schlum et al 2021, Rane et al 2022).…”

“…Such distinct population genomic structure contradicted the expected gene flow signatures of a single introduction and a west-to-east spread of this pest. Instead, they suggested relatively limited and localised spread of populations while also identified the likely multiple independent introduction pathways of S. frugiperda into the region including in SEA, Asia and Australia (Rane et al 2022).…”

“…In this study, we report on the first bioassay experiments and resistance gene characterisation that aimed to understand how the initial invasive populations of S. frugiperda in Australia responded to selected approved insecticide compounds and Bacillus thuringiensis (Bt) toxins in commercial transgenic plant varieties and available as sprays for the horticultural, grains and cotton industries. Since populations were presumed collected before selection occurred in Australia, these responses served as the first indication of selection against insecticides and Bt toxins used elsewhere (i.e., in the species’ native range and in its recent invasive ranges from Southeast Asia, Asia, and/or Africa (Schlum et al 2021; Tay et al 2022a; Jiang et al 2022; Rane et al 2022)) prior to arrival. While sampling from multiple Australian regions would be ideal (but impossible at the time as our laboratory had only been provided with these two lines during the pandemic travel restriction), comparing the response differences between these two S. frugiperda populations from different northern Australia regions nevertheless could demonstrate the use of bioassay data to distinguish signatures of possible multiple points of entry compared with a single entry and spread event as generally assumed (e.g., Jing et al 2021, Qi et al 2021).…”