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

Abstract

Background The fall armyworm (Spodoptera frugiperda (J.E. Smith)) is a highly polyphagous agricultural pest with long-distance migratory behavior threatening food security worldwide. This pest has a host range of > 80 plant species, but two host strains are recognized based on their association with corn (C-strain) or rice and smaller grasses (R-strain). The population genomics of the United States (USA) fall armyworm remains poorly characterized to date despite its agricultural threat. Results In this study, the population structure and genetic diversity in 55 S. frugiperda samples from Argentina, Brazil, Kenya, Puerto Rico and USA were surveyed to further our understanding of whole genome nuclear diversity. Comparisons at the genomic level suggest a panmictic S. frugiperda population, with only a minor reduction in gene flow between the two overwintering populations in the continental USA, also corresponding to distinct host strains at the mitochondrial level. Two maternal lines were detected from analysis of mitochondrial genomes. We found members from the Eastern Hemisphere interspersed within both continental USA overwintering subpopulations, suggesting multiple individuals were likely introduced to Africa. Conclusions Our research is the largest diverse collection of United States S. frugiperda whole genome sequences characterized to date, covering eight continental states and a USA territory (Puerto Rico). The genomic resources presented provide foundational information to understand gene flow at the whole genome level among S. frugiperda populations. Based on the genomic similarities found between host strains and laboratory vs. field samples, our findings validate the experimental use of laboratory strains and the host strain differentiation based on mitochondria and sex-linked genetic markers extends to minor genome wide differences with some exceptions showing mixture between host strains is likely occurring in field populations.

Genetic Screening to Identify Candidate Resistance Alleles to Cry1F Corn in Fall Armyworm Using Targeted Sequencing

“…In agreement with this observation, previous genotyping efforts did not detect SfABCC2mut among Brazilian S. frugiperda populations [ 9 ]. However, whole-genome comparisons suggest panmixia among S. frugiperda populations [ 42 ]. We did find two heterozygote individuals from Lajas (PRL_168 and PRL_164) carrying a GY deletion (DGY784D in our model, allele frequency 0.0571) previously described in Cry1F-resistant and field-collected S. frugiperda from Brazil [ 10 ].…”

“…In addition, Taqman assays are limited to known alleles and cannot provide detection of novel candidate resistance alleles. Targeted sequencing provided preliminary evidence of a common mutation associated with Cry1F resistance in S. frugiperda from Brazil and Puerto Rico, which may suggest genetic flow between these populations as supported by whole genome-level comparisons [ 42 ]. Targeted sequencing such as Hi-Plex is adaptable to other pest-toxin resistance gene models, as long as known or suspected resistance loci are available, and the method can be expanded to sequence multiple genes within a single sample.…”

The fall armyworm strain associated with most rice, millet, and pasture infestations in the Western Hemisphere is rare or absent in Ghana and Togo

“…Since their original designation as strains [12,15], the characterizations of the groups have ranged from "host forms" where the divergence is relatively small [13], to "sibling species" associated with evidence of significant reproductive isolation [16]. Genomic studies have been similarly inconclusive with reports for both the presence [17] and absence [18] of significant nuclear genomic differences between strains. Molecular markers remain the best definer of strain identity, as empirically demonstrated by strong correlations between genetic polymorphisms and host plant in fall armyworm surveyed from multiple locations in the Western Hemisphere [14,19,20].…”

Novel real-time PCR based assays for differentiating fall armyworm strains using four single nucleotide polymorphisms

“…This species is highly polyphagous, feeding on more than 357 different host plants (Montezano et al, 2018), but it causes most economic damage to gramineous crops such as corn, sorghum, and pasture grasses (Johnson, 1987;Luginbill, 1928;Pashley, 1988). Although S. frugiperda is considered discordance could be the result of occasional hybridization, a phenomenon that has been observed in the lab (Dumas et al, 2015;Kost et al, 2016;Pashley & Martin, 1987;Whitford et al, 1988) and in field samples (Schlum et al, 2021). However, the fact that these genetic markers have not become homogenous over time suggests the two strains remain genetically distinct despite occasional gene flow (Schlum et al, 2021).…”

“…Although S. frugiperda is considered discordance could be the result of occasional hybridization, a phenomenon that has been observed in the lab (Dumas et al, 2015;Kost et al, 2016;Pashley & Martin, 1987;Whitford et al, 1988) and in field samples (Schlum et al, 2021). However, the fact that these genetic markers have not become homogenous over time suggests the two strains remain genetically distinct despite occasional gene flow (Schlum et al, 2021).…”