Multiple recombination events between two cytochrome P450 loci contribute to global pyrethroid resistance in Helicoverpa armigera

Walsh, Tom; Joußen, Nicole; Tian, Kai; McGaughran, Angela; Anderson, C. A.; Qiu, Xinghui; Ahn, Seung‐Joon; Bird, Lisa J.; Pavlidi, Nena; Vontas, John; Ryu, Jaeeun; Rasool, Akhtar; Macedo, Isabella Barony; Tay, Wee Tek; Zhang, Yongjun; Whitehouse, Mary; Silvie, Pierre; Downes, Sharon; Nemec, Lori; Heckel, David G.

doi:10.1371/journal.pone.0197760

Cited by 57 publications

(87 citation statements)

References 57 publications

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“…Another substantial phenotypic difference between H. armigera and H. zea lies in their susceptibility to insecticides widely used for pest control ( Anderson et al. 2018 ; Walsh, Joussen, et al. 2018 ).…”

Section: Introductionmentioning

confidence: 99%

Adaptive Introgression across Semipermeable Species Boundaries between Local Helicoverpa zea and Invasive Helicoverpa armigera Moths

Valencia-Montoya

Elfékih

North

et al. 2020

Molecular Biology and Evolution

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128

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Abstract Hybridization between invasive and native species has raised global concern, given the dramatic increase in species range shifts and pest outbreaks due to anthropogenic dispersal. Nevertheless, secondary contact between sister lineages of local and invasive species provides a natural laboratory to understand the factors that determine introgression and the maintenance or loss of species barriers. Here, we characterize the early evolutionary outcomes following secondary contact between invasive Helicoverpa armigera and native H. zea in Brazil. We carried out whole-genome resequencing of Helicoverpa moths from Brazil in two temporal samples: during the outbreak of H. armigera in 2013 and 2017. There is evidence for a burst of hybridization and widespread introgression from local H. zea into invasive H. armigera coinciding with H. armigera expansion in 2013. However, in H. armigera, the admixture proportion and the length of introgressed blocks were significantly reduced between 2013 and 2017, suggesting selection against admixture. In contrast to the genome-wide pattern, there was striking evidence for adaptive introgression of a single region from the invasive H. armigera into local H. zea, including an insecticide resistance allele that increased in frequency over time. In summary, despite extensive gene flow after secondary contact, the species boundaries are largely maintained except for the single introgressed region containing the insecticide-resistant locus. We document the worst-case scenario for an invasive species, in which there are now two pest species instead of one, and the native species has acquired resistance to pyrethroid insecticides through introgression.

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Section: Introductionmentioning

confidence: 99%

Adaptive Introgression across Semipermeable Species Boundaries between Local Helicoverpa zea and Invasive Helicoverpa armigera Moths

Valencia-Montoya

Elfékih

North

et al. 2020

Molecular Biology and Evolution

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128

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“…Future monitoring of Helicoverpa species at preborder inspection could also consider the method of Nagoshi, Gilligan, and Brambila () that incorporates the z‐linked Triosephosphate isomerase (Tpi) gene with the mtCOI gene for identifying potential H. armigera ‐ H. zea hybrids, although the feasibility of transferring this method to screen for potential H. armigera ‐ H. gelotopoeon , H. assulta ‐ H. gelotopoeon , H. assulta ‐ H. zea , and H. armigera ‐ H. assulta hybrids remained to be tested. Failure to monitor for these interspecific hybrids may lead to invasive genotypes such as enhanced resistance to insecticides being spread unchecked (Walsh et al, ). The identification of naturally occurring hybrids will be difficult and will require significant coordination efforts between governmental departments (e.g., quarantine services, molecular detection, and identification facilities), and the development and adoption of new biosecurity policies.…”

Section: Discussionmentioning

confidence: 99%

Mitochondrial DNA genomes of five majorHelicoverpapest species from the Old and New Worlds (Lepidoptera: Noctuidae)

Walsh

Perera

Anderson

et al. 2019

Ecology and Evolution

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Five species of noctuid moths, Helicoverpa armigera , H. punctigera , H. assulta , H. zea, and H. gelotopoeon, are major agricultural pests inhabiting various and often overlapping global distributions. Visual identification of these species requires a great deal of expertise and misidentification can have repercussions for pest management and agricultural biosecurity. Here, we report on the complete mitochondrial genomes of H. assulta assulta and H. assulta afra , H. gelotopoeon, H. punctigera, H. zea , and H. armigera armigera and H. armigera conferta’ assembled from high‐throughput sequencing data. This study significantly increases the mitogenome resources for these five agricultural pests with sequences assembled from across different continents, including an H. armigera individual collected from an invasive population in Brazil. We infer the phylogenetic relationships of these five Helicoverpa species based on the 13 mitochondrial DNA protein‐coding genes (PCG's) and show that two publicly available mitogenomes of H. assulta ( KP015198 and KR149448 ) have been misidentified or incorrectly assembled. We further consolidate existing PCR‐RFLP methods to cover all five Helicoverpa pest species, providing an updated method that will contribute to species differentiation and to future monitoring efforts of Helicoverpa pest species across different continents. We discuss the value of Helicoverpa mitogenomes to assist with species identification in view of the context of the rapid spread of H. armigera in the New World. With this work, we provide the molecular resources necessary for future studies of the evolutionary history and ecology of these species.

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“…That incursions of H. armigera from the Old World potentially involved multiple pathways will have significant implications to pest and resistance management strategies in the New World. For example, populations of H. armigera around the world have developed resistance to conventional pesticides (e.g., [31,[73][74][75][76][77][78], and the South American populations have also arrived at least with resistance to pyrethroids [77] but also potentially with various enhanced allelochemical detoxification traits. Increasing genetic diversity is a key factor that underpins increasing invasion success [79,80].…”

Section: Discussionmentioning

confidence: 99%

Multiple incursion pathways forHelicoverpa armigerain Brazil show its genetic diversity spreading in a connected world

Arnemann

Roxburgh

Walsh

et al. 2019

Preprint

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The Old World cotton bollworm Helicoverpa armigera was first detected in Brazil with subsequent reports from Paraguay, Argentina, Bolivia, and Uruguay. This pattern suggests that the H. armigera spread across the South American continent following incursions into northern/central Brazil, however, this hypothesis has not been tested. Here we compare northern and central Brazilian H. armigera mtDNA COI haplotypes with those from southern Brazil, Uruguay, Argentina, and Paraguay. We infer spatial genetic and gene flow patterns of this dispersive pest in the agricultural landscape of South America. We show that the spatial distribution of H. armigera mtDNA haplotypes and its inferred gene flow patterns in the southwestern region of South America exhibited signatures inconsistent with a single incursion hypothesis. Simulations on spatial distribution patterns show that the detection of rare and/or the absence of dominant mtDNA haplotypes in southern H. armigera populations are inconsistent with genetic signatures observed in northern and central Brazil. Incursions of H.armigera into the New World are therefore likely to have involved independent events in northern/central Brazil, and southern Brazil/Uruguay-Argentina-Paraguay. This study demonstrates the significant biosecurity challenges facing the South American continent, and highlights alternate pathways for introductions of alien species into the New World.

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Multiple recombination events between two cytochrome P450 loci contribute to global pyrethroid resistance in Helicoverpa armigera

Cited by 57 publications

References 57 publications

Adaptive Introgression across Semipermeable Species Boundaries between Local Helicoverpa zea and Invasive Helicoverpa armigera Moths

Adaptive Introgression across Semipermeable Species Boundaries between Local Helicoverpa zea and Invasive Helicoverpa armigera Moths

Mitochondrial DNA genomes of five majorHelicoverpapest species from the Old and New Worlds (Lepidoptera: Noctuidae)

Multiple incursion pathways forHelicoverpa armigerain Brazil show its genetic diversity spreading in a connected world

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