Evidence that a major subpopulation of fall armyworm found in the Western Hemisphere is rare or absent in Africa, which may limit the range of crops at risk of infestation

Abstract

2 1 Abstract 2 The introduction and establishment of fall armyworm (Spodoptera frugiperda) in Africa presents 3 a major threat to agriculture in that continent and potentially to the entire Eastern Hemisphere.4 The species is subdivided into two subpopulations called the R-strain and C-strain that differ in 5 their distribution on different plant hosts. This means that the scope of the economic risk posed 6 by invasive fall armyworm is influenced by whether one or both strains are present. Multiple 7 studies have found mitochondrial markers diagnostic of the two strains throughout Africa but 8 there is substantial disagreement with a nuclear strain marker that makes conclusions about strain 9 composition uncertain. In this study the issue of whether both strains are present in Africa was 10 tested by an assay that can detect strain-biased mating behaviors. Western Hemisphere fall 11 armyworm consistently showed evidence of strain-specific assortative mating in the field that 12 was not found in surveys from multiple locations in Africa. The absence of strain mating biases 13 and the disagreements between the strain diagnostic genetic markers indicates that the R-strain is 14 rare (<1% of the population) or absent in Africa. Instead, it appears that the African fall 15 armyworm populations are dominated by two groups, the C-strain and the descendants of 16 interstrain hybrids. These results suggest that plant hosts associated with the R-strain may not be 17 at high risk of fall armyworm infestation in Africa. 18 Introduction 19Fall armyworm (Spodoptera frugiperda) is an important agricultural pest of the Western 20 Hemisphere that has recently spread into Africa where it has the potential for significant 21 economic impact [1]. The species has a broad host range having been found on greater than 80 22 plant species and cultivars [2]. However, infestations of agricultural importance are limited to a 23 few crops in the Western Hemisphere, indicating that while capable of being broadly 24 polyphagous, fall armyworm tends to be more specific in its host usage. The species can be 25 subdivided into two subpopulations defined by their differential distribution in the field [3]. The 26 C-strain (historically designated the corn-strain) is typically found on corn, sorghum, and cotton, 27 while the R-strain (rice-strain) predominates on rice, alfalfa, pasture grasses, and millet, though 28 subsequent observations indicate that the preference to rice may be variable [4][5][6][7]. There is 29 genetic evidence that both strains are present in Africa suggesting that a variety of crop systems 30 are at risk [8][9][10][11]. However, reports of fall armyworm damage to date have been primarily 31 limited to C-strain preferred hosts, specifically corn and sorghum [12]. There are some anecdotal 32 reports of infestations in R-strain host plants, but whether these occur consistently or incur 33 significant economic damage has yet to be documented. 34The fall armyworm strains were originally defined by the differential distribution o...

Whole genome comparisons reveal panmixia among fall armyworm (Spodoptera frugiperda) from diverse locations

“…Further, we have analyzed individuals that appear to have a C-strain nuclear genome with an R-strain associated mitochondria (maternal lineage). This is consistent with the conflicting host strain assignments using specific genetic markers between R-strain and interstrain hybrids that was previously reported [22]. We still observe host differentiation at the nuclear genome level, though, and may suggest current single locus markers are not sufficient for surveying all S.…”

“…However, host preference is not absolute and discrepancies among haplotype markers have been reported. For example, the Tpi marker agrees with assortative mating and host assessments [22] in describing S. frugiperda samples from corn in the Eastern Hemisphere as Cstrain, yet a predominant COI-R strain marker is obtained in these collections [9]. These conflicting results may reflect interstrain hybridization [22] or be driven by maternally inherited symbionts that skew the distribution and diversity of certain haplotypes [23].…”

Southeastern Asia fall armyworms are closely related to populations in Africa and India, consistent with common origin and recent migration

“…Second, a methodology was developed that could detect suppression of interstrain mating in Western Hemisphere field populations by comparing the frequency of heterozygosity between strain-specific genetic polymorphisms with those that are nonspecific 38 . Application of this method to African fall armyworm found no evidence of similar strain-dependent mating behavior 39 . Third, previous studies in the Western Hemisphere indicate that approximately 20% of fall armyworm larvae collected from corn are of the R-strain based on a variety of molecular markers 17,21,25,40 , including TpiR (Fig.…”

High-depth resequencing reveals hybrid population and insecticide resistance characteristics of fall armyworm (Spodoptera frugiperda) invading China

“…Because of their hybridization, identification based on the maternally-inherited mitochondrial genotype is inaccurate and the insertion of two C-strain mitochondrial fragments in this study further confirms this inaccuracy. Therefore, it is not possible to accurately infer fall armyworm strain status based on the complete mitochondrial genome or the single COI mitochondrial gene, as suggested previously [40][41] . The Tpi gene, located in the nuclear genome, is more suitable for strain identification and 10 SNPs in this gene can distinguish between R-or C-strains fall armyworm in the Americas 37 .…”

“…Recent studies have indicated that the molecular identification of the two strains of fall armyworm is dependent on which markers are used [35][36][37] . The early molecular markers based on mitochondrial Cytochrome Oxidase Subunit I (COI) and Z-chromosome-linked Triosephosphate isomerase (Tpi) genes failed to accurately assign strain identification [38][39][40][41] . The dominant population of fall armyworm invading Africa and Asia were speculated to be hybrid populations of the female R-strain and male C-strain, based on these two molecular markers 42 .…”