Genetic analyses and detection of point mutations in the acetylcholinesterase-1 gene associated with organophosphate insecticide resistance in fall armyworm (Spodoptera frugiperda) populations from Uganda

Abstract

Background The fall armyworm (FAW), Spodoptera frugiperda; J.E. Smith (Lepidoptera: Noctuidae), is now an economically important pest that causes huge losses to maize productivity in sub-Saharan Africa. Variations in sub-population genetics and the processes of rapid adaptation underpinning the invasion remain unclear. For this, the genetic identity and diversity of FAW populations in Uganda were revealed by sequencing 87 samples (collected across the country). Based on the partial mitochondrial cytochrome oxidase I (COI) gene polymorphisms, we further examined the mitochondrial haplotype configuration and compared the FAW in Uganda with sequences from other parts of the world. The molecular target for organophosphate and carbamate resistance, acetylcholinesterase, was also investigated. Results Analysis of the partial COI gene sequences showed the presence of both rice (predominant) and corn strain haplotypes, with a haplotype diversity of 0.382. Based on the COI marker, pairwise difference distribution analyses, and neutrality tests, showed that the FAW populations in Uganda and the rest of Africa are evolving neutrally, but those in America and Asia are undergoing expansion. Our findings support observations that invasive FAW populations throughout the rest of Africa and Asia share a common origin. Sequencing of the S. frugiperda ace-1 gene revealed four amino acid substitutions, two of which (A201S and F290V) were previously shown to confer organophosphate resistance in both S. frugiperda and several other insect species. The other two previously reported new variations in positions g-396 and g-768, are presumed to be related to the development of insecticide resistance. Conclusions This research has increased our knowledge of the genetics of FAW in Uganda, which is critical for pest surveillance and the detection of resistance. However, due to the low gene polymorphism of COI, more evolutionary studies incorporating the Spodoptera frugiperda whole-genome sequence are required to precisely understand the FAW population dynamics, introduction paths, origin, and subsequent spread.

Genetic Diversity of the Fall Armyworm Spodoptera frugiperda (J.E. Smith) in the Democratic Republic of the Congo

“…Most (84%) of the samples were COI-R, whereas COI-C occurred in 16%. These findings were consistent with those of a recent study conducted in Uganda, a neighboring country [32], and a previous report from 11 sub-Saharan African countries, including two provinces of the DRC [19]. Based on the COI marker, both corn and rice strains were detected in FAW specimens collected from corn fields, despite the known association of strains to their host plant [35,36].…”

“…Based on the COI marker, both corn and rice strains were detected in FAW specimens collected from corn fields, despite the known association of strains to their host plant [35,36]. Similar findings have been reported in several African and Asian countries [19,22,32]. These findings suggested that the discordance between the COI marker and host plants may be due to FAW's plasticity in plant choice or the inability of the marker to reliably discriminate between the corn and rice strains of FAW.…”

“…The median joining network method was used to infer haplotype relationships. To generate the evolutionary relationship between the DRC FAW haplotypes, a phylogenetic tree for the COI gene was constructed using the maximum likelihood method implemented in MEGA 6.0 [30], with other Spodoptera species and FAW corn and rice strains retrieved from NCBI [31,32]. For each phylogeny, 1000 bootstrap replicates were used to assess robustness using the Hasegawa-Kishino-Yano (HKY850) model and gamma distribution rate of variation between sites [33].…”

Old and new association of Cotesia icipe (Hymenoptera: Braconidae) with alien invasive and native Spodoptera species and key stemborer species: implication for their management

“…An overreliance on chemical insecticides often leads to the development of resistance by the target pest(s). Indeed, insecticide resistance in S. frugiperda populations has been reported widely in its native range 12 and more recently in its invasion regions in Africa, Asia and Australia 13–17 . The resistance to variety of insecticide classes (e.g.…”

“…Indeed, insecticide resistance in S. frugiperda populations has been reported widely in its native range 12 and more recently in its invasion regions in Africa, Asia and Australia. [13][14][15][16][17] The resistance to variety of insecticide classes (e.g. organophosphates, spinosyn and carbamates, among others) by the pest, results from its genetic plasticity and high fecundity, as well as intense selection pressure.…”