Global FAW population genomic signature supports complex introduction events across the Old World

Abstract

Accurate genomic knowledge can elucidate the global spread patterns of invasive pests. The highprofile invasive agricultural pest Spodoptera frugiperda (fall armyworm; FAW) is a case in point. Native to the Americas, the FAW was first reported in West Africa in 2016 and has rapidly spread to over 64 countries across the Old World, resulting in significant economic losses. The chronological order of reported detections has led to the hypothesis that the FAW moved eastwards across Africa and then Asia, however genomic evidence remains lacking to test this hypothesis and to identify the potential origin of invasive populations. Using a whole genome sequencing approach, we explored the population genomic signatures of FAW populations from the Americas and the Old World. Analyses of complete mitochondrial DNA genomes identified 12 maternal lineages across the invasive range, while genomic signatures from 870 high-quality nuclear genome-wide single nucleotide polymorphic (SNP) DNA markers identified five distinct New World populations that broadly reflected their native geographical ranges and absence of host-plant preference status. Unique FAW populations in the Old World were also identified that suggested multiple introductions underpinned their rapid global spread. We identified in Asian FAW individuals, genomes lacking evidence of admixture; while analysis of identified complex substructure revealed significant directional geneflow from Asia into East Africa, in contrast to a simple east-towest spread. Our study highlights the need for population genomics approaches in analysing complex pest invasions, and the importance of international partnership to address global biosecurity challenges presented by emerging high priority insect pests. Correspondence

Comparative Genetic Analysis of Invasive Fall Armyworm Populations Provides Evidence for Population Expansion in India

“…One would be the uncharacteristic similarity between the ancestral population for all the invaded regions, which is indicative of a recent and a common source. Secondly, most of the earlier studies on FAW sequences in India have reported low levels of genetic variation, similar to the one found in Africa and East Asia [7,18,[21][22]. Thirdly, the distribution of the novel haplotypes in Indian populations is unimodal, typical of founder effect with recent population expansion.…”

“…In fact, India, Africa and other regions of Asia shared common ancestral haplotypes and similar polymorphisms with each other, signifying a common source for all these populations. However, a recent study involving whole genome sequencing of FAW populations from New World and invaded regions has proposed multiple origins for FAW in the invaded countries [22]. On that basis, we think it would be prudent to analyse the diversity in Indian populations with multiple gene loci to conclusively trace the geographic origins or monitor the out ows from India.…”

“…Spodoptera frugiperda provides an excellent model system in this regard since it is believed to have expanded its distribution range very recently and has been well documented and characterised for its diversity in its native as well as the extended range. Most of the studies involving diversity of Indian FAW populations were performed around two years ago from few locations where it was rst detected in India [7,18,[21][22]. Thus we thought it was imperative to understand the diversity of Indian FAW population over the course of last two years after the expansive migration of FAW across India.…”

“…In addition, detection of a unique African Tpi 'rice' haplotype in the populations from India and South East Asia further strengthened the hypothesis that the invasive populations shared a recent and a common origin [18][19]. Though the notion was challenged by whole mitochondrial sequencing analysis, but there was consensus on highly reduced genetic diversity in invasive populations indicative of small number of founders [22].…”

“…Most of the studies analysing the genetic diversity of FAW in India were primarily undertaken in 2018, when FAW was rst detected in India and had spread to limited regions within the country [21][22]. The Indian population exhibited high homogeneity with East and South African populations with the majority showing mitochondrial rice strain COI and nuclear corn strain Tpi marker [18].…”