Absence of known knockdown resistance mutations but fixation of CYP337B3 was detected in field populations of Helicoverpa armigera across China

Ni, Ruoyao; Wang, Yawei; QiuZan, Zhong; Li, Mei; Zhang, Dandan; Wu, Kongming; Qiu, Xinghui

doi:10.1016/j.pestbp.2023.105542

Cited by 9 publications

(21 citation statements)

References 45 publications

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“…However, bootstrap support values were low within the H. armigera clade; there was no resolution to distinguish source populations. This result is consistent with low population structure within H. armigera and directional selection at this locus across the species’ native and invasive range (Ni et al 2023; Jin et al 2023).…”

Section: Resultssupporting

confidence: 81%

“…Our results show that the admixed samples carried alleles that, due to their semidominant phenotypic effect, enable resistance to fenvalerate, deltamethrin and possibly cypermethrin (Rasool et al 2014; Ni et al 2023; Joußen et al 2012). Thus, an otherwise absent resistance phenotype was introduced to the North American H. zea population via interspecific introgression.…”

Section: Discussionmentioning

confidence: 79%

“…A (0-9Mbp), which shows no signs of admixture, and B (>9Mbp) in which H. armigera haplotypes have introgressed. We next sought to determine whether the admixed samples carried the H. armigera CYP337B3 (Ni et al 2023;Jin et al 2023). Together, these results suggest that two of 237 individuals sampled are admixed, that introgression in these two samples is concentrated around the CYP337B3 locus, and that both samples carry at least one H. armigera CYP337B3 allele.…”

Section: Resultsmentioning

confidence: 99%

“…Thus, an otherwise absent resistance phenotype was introduced to the North American H. zea population via interspecific introgression. The introgression of this gene is an indirect result of adaptation to pyrethroid exposure both in the native range of H. armigera (Rasool et al 2014; Ni et al 2023; Joußen et al 2012) and subsequently in South American H. zea (Valencia-Montoya et al 2020; Durigan et al 2017). As anthropogenic activity increasingly brings pest species into secondary contact, introgression could become an important mechanism of rapid adaptation.…”

Section: Discussionmentioning

confidence: 99%

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Rapid evolution of pesticide resistance via adaptation and interspecific introgression in a major North American crop pest

North,

Fu,

Metz

et al. 2023

Preprint

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Insect crop pests threaten global food security. This threat is amplified through the spread of non-native species and the evolution of pesticide resistance, which can be introduced to a population thoughde novomutation or gene flow. We investigate these processes in an economically important noctuid crop pest,Helicoverpa zea, which has rapidly evolved resistance to several pesticides. Its sister speciesHelicoverpa armigera, first detected as an invasive species in Brazil in 2013, introduced the pyrethroid resistance geneCYP337B3to South AmericanH. zeavia introgression. To understand whether this contributes to pesticide resistance in North America, we sequenced 237H. zeagenomes across 10 sample sites in the US. First, we reportH. armigeraintrogression into the North AmericanH. zeapopulation. Two individuals sampled in Texas in 2019 carryH. armigerahaplotypes in a 4Mbp region containingCYP337B3. Second, we show that the remarkable dispersal ability ofH. zearesults in a panmictic North American population. Third, we detect signatures of selection in non-admixedH. zea, identifying a selective sweep at a second pesticide resistance locus with a similar name:CYP333B3. We estimate that its derived allele conferred a ∼4.9% fitness advantage and show that this estimate explains independently observed rare nonsynonymousCYP333B3mutations approaching fixation over a ∼20-year period. We also detect putative signatures of selection at a kinesin gene associated with Bt resistance. Our results show that pesticide resistance inH. zeaevolved rapidly and recently via two independent mechanisms: interspecific introgression and rapid intraspecific adaptation.

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Section: Resultssupporting

confidence: 81%

Section: Discussionmentioning

confidence: 79%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 2 more Smart Citations

Rapid evolution of pesticide resistance via adaptation and interspecific introgression in a major North American crop pest

North,

Fu,

Metz

et al. 2023

Preprint

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“…The pest surveillance program of USDA Animal and Plant Health Inspection Service (USDA APHIS) later detected several H. armigera adults near the Chicago O'Hare International Airport between 2019 and 2022, however no individuals were detected in surrounding agricultural areas (APHIS, 2024). Introgression between these two species was shown by the detection of the invasive H. armigera-specific CYP337B3 allele in two H. zea collected from a Texas population in 2019 (North et al, 2023). Our current study focuses on a collection of Helicoverpa moths from Olathe, Colorado, where a failure to control damage to conventional sweetcorn was reported following repeated pyrethroid insecticide applications in 2023.…”

Section: Introductionmentioning

confidence: 99%

Anatomy of a pest control failure: Introgression of cytochrome P450 337B3 alleles from invasive old-world bollworm into native corn earworm (Lepidoptera: Noctuidae)

Nufer,

Coates,

Abel

et al. 2024

Preprint

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The establishment of invasive species populations can threaten the ecological balance in naive habitats and impact agricultural production practices. The old-world bollworm (OWBW),Helicoverpa armigera, and the corn earworm (CEW),H. zea, were geographically separated prior to the 2013 report of OWBW invasion into South America. Introgression of OWBW-specific cytochrome P450 337B3 (CYP337B3) gene into CEW was repeatedly detected across South America and the Caribbean. Two hybrids were documented among samples collected in Texas during 2019. In this study, screening insects collected in Olathe, Colorado, USA where a failure of pyrethroids to control CEW damage to conventional sweetcorn in 2023, detected 28.59% insects with the OWBW-specific CYP337B3 marker. Nucleotide sequencing of CYP337B3 gene identified 73.05 and 26.95% insects homozygous for CYP337B3v2 and CYP337B3v6 alleles, respectively. Based on prior data for distinct phylogeographic origins of CYP337B3v2 and v6 alleles, our results indicate Olathe samples were derived from two different introductions. Specifically, a novel origin based on restricted distribution of v6 allele to Ghana in West Arica, and possible South American or Caribbean origin of the v2 allele. One of the 1618 individuals screened also carried a ribosomal RNA internal transcribed spacer 1 (ITS1) derived from OWBW. Local selection pressures at the Olathe location imposed by repeated pyrethroid exposures are likely attributed to the prevalence of CYP337B3, where control practices hasten the accumulation of phenotypic resistance by adaptive introgression. Pyrethroid and other resistance factors carried by invasive OWBW may continue to impact CEW management tactics for across the Americas.

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Genome-wide exploration of metabolic-based pyrethroid resistance mechanism in Helicoverpa armigera

Kim,

Rahman,

Han

et al. 2024

J Pest Sci

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Absence of known knockdown resistance mutations but fixation of CYP337B3 was detected in field populations of Helicoverpa armigera across China

Cited by 9 publications

References 45 publications

Rapid evolution of pesticide resistance via adaptation and interspecific introgression in a major North American crop pest

Rapid evolution of pesticide resistance via adaptation and interspecific introgression in a major North American crop pest

Anatomy of a pest control failure: Introgression of cytochrome P450 337B3 alleles from invasive old-world bollworm into native corn earworm (Lepidoptera: Noctuidae)

Genome-wide exploration of metabolic-based pyrethroid resistance mechanism in Helicoverpa armigera

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