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 recorded from South Asia (SA), Southeast Asia (SEA), East Asia (EA), and Pacific/Australia (PA). Population genomic analyses enabled 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 in this study were overwhelmingly C- and R-strain hybrids (n = 252/262). 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.

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

“…Moreover, we do not recommend utilizing COI genes or mitochondrial genomes for strain identification, population structure an Asian origin or a secondary invasion of invasive FAW (Nagoshi et al, 2022;Rane et al, 2023). However, our data strongly support a homogeneous genetic structure among field-collected samples in invasive areas, indicating that African and Asian samples share similar genomic features, which is consistent with the monitoring results of a short-term expansion from Africa into Asia (Feldmann et al, 2019;Ganiger et al, 2018;Goergen et al, 2016;Sun et al, 2021).…”

“…This implies that even a small number of invasive individuals can lead to an exaggerated population structure following colonization and reproduction. Recently published studies, based on mitochondrial data or a limited number of nuclear genomic SNPs, support either an Asian origin or a secondary invasion of invasive FAW (Nagoshi et al, 2022; Rane et al, 2023). However, our data strongly support a homogeneous genetic structure among field‐collected samples in invasive areas, indicating that African and Asian samples share similar genomic features, which is consistent with the monitoring results of a short‐term expansion from Africa into Asia (Feldmann et al, 2019; Ganiger et al, 2018; Goergen et al, 2016; Sun et al, 2021).…”

“…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). There is a need for more data to clarify the potential origin of the invasive FAW.…”

“…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). There is a need for more data to clarify the potential origin of the invasive FAW.…”

Farmer perception of impacts of fall armyworm (Spodoptera frugiperda J.E. Smith) and transferability of its management practices in Uganda

“…Native to the North, Central, and South Americas, the FAW was reported in western Africa in (Goergen et al 2016 and by 2018, it was reported also in at least 44 African countries that included almost all of the sub-Saharan African nations (Rwomushana et al 2018;Uzayisenga et al 2018) and from Egypt in northern Africa (e.g., IPPC 2019), the Middle East and the Indian sub-continent, and China (Tay and Gordon 2019). The FAW has also been reported in the Near East and Asian/Southeast Asian countries including India (Ganiger et al 2018;Sharanabassappa et al 2018;EPPO 2019), Taiwan (IPPC 2019a; Shrikanth 2019), Japan, Myanmar, Vietnam (Vu 2008;Hang et al 2019;IPPC 2019b;Rane et al 2023), Indonesia (Bauventura et al 2020), Papua New Guinea (Tay et al 2023a), Philippines (Navasero et al 2019), before being detected in Australia by February 2020 (IPPC 2020;Rane et al 2023).…”