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

Authors: Nufer, Marissa; COATES, BRAD - US Department Of Agriculture (USDA); ABEL, CRAIG - US Department Of Agriculture (USDA); O'NEILL, PATRICK - Soil Health Services; MCKRACKEN, MEGAN - Olathe Spray Services, Inc; JAIN, DEVENDRA - Maharana Pratap University Of Agriculture And Technology; Pierce, Calvin; Glover, James; TOWELS, TYLER - Mississippi State Extension Service; Reddy, Gadi V.P.; Perera, Omaththage

Submitted to: Journal of Insect Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/3/2024
Publication Date: 9/30/2024
Citation: Nufer, M., Coates, B.S., Abel, C.A., O'Neill, P., Mckracken, M., Jain, D., Pierce Iii, C.A., Glover, J.P., Towels, T., Reddy, G.V., Perera, O.P. 2024. Anatomy of a pest control failure: Introgression of cytochrome P450 337B3 alleles from invasive Helicoverpa armigera into native corn earworm (Lepidoptera: Noctuidae). Journal of Insect Science. 24:04(1-10). https://doi.org/10.1093/jisesa/ieae094.
DOI: https://doi.org/10.1093/jisesa/ieae094

Interpretive Summary: The establishment of invasive species populations can threaten the ecological balance in natural habitats and cause great economic impact on agricultural production. In some instances, invasive species can mate with native species where their progeny can have a larger negative impact. In 2023, in Olathe, CO, samples of native corn earworm (CEW: Helicoverpa zea) were collected from sweetcorn fields with documented pyrethroid insecticide control failure. These samples were screened for two genes specific for invasive old-world bollworms (OWBW: Helicoverpa armigera). Analysis of 1618 CEW DNA samples identified one sample carrying a DNA marker called ribosomal RNA internal transcribed spacer 1 (ITS1) with a signature of the invasive OWBW. Screening of 850 DNA samples for the presence of OWBW- specific cytochrome P450 337B3 (CYP337B3) gene, which confers resistance to pyrethroid insecticides, was detected in 243 insects (28.6%) carrying two different alleles of the CYP337B3. The results of this study indicate that the hybridization of CEW with OWBW has led to the transfer of OWBW-specific genes into native CEW populations in the United States. One allele (CYP337B3v2), reported initially from Pakistan, had previously been reported in Brazil in 2021 where invasive OWBW was detected. The second allele, CYP337B3v6, was initially reported in Uganda in West Africa but has not been reported in North or South American populations. Selection pressure from frequent field applications of pyrethroid insecticide has likely increased the allele frequency of the CYP337B3 gene in American CEW populations. The CYP337B3 gene is only an indicator of the extent of gene transfer between these two species. We expect other genes with a selective advantage in the agroecosystem might be present in hybrid CEW populations. The impacts of genes derived from invasive OWBW on grower production practices remain uncertain, but continued selection for pest adaptions to practices that rely on insecticidal agents may be predicted to drive introgression of other associated resistance alleles into CEW.

Technical Abstract: The establishment of invasive species populations can threaten the ecological balance in naïve habitats and impact agricultural production practices. The lepidopteran species Helicoverpa armigera and H. zea were distributed across “Old-“ and “New-world” regions, respectively, prior to the 2013 report of H. armigera invasion into South America. Detection of hybrid genotypes inferred permeability of species boundaries with introgression of the H. armigera-specific cytochrome P450 337B3 (CYP337B3) gene locus that confers resistance to pyrethroid insecticides. Introgression of H. armigera CYP337B3 alleles into H. zea was repeatedly detected across South America and the Caribbean, and two hybrids were documented among samples collected in Texas during 2019. A potential breeding population of H. armigera was also detected near Chicago, Illinois, from 2019 to 2022. A documented failure of pyrethroids to control Helicoverpa damage to conventional sweetcorn occurred near Olathe, Colorado, USA in 2023. In this study, screening of 850 samples from this location detected 243 (28.6%) with the H. armigera-specific CYP337B3 marker. Subsequent sequencing of CYP337B3 from 141 individuals identified 103 and 38 and homozygotes 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 the restricted distribution of the v6 allele to Ghana in West Africa, and possible South American or Caribbean origin of the v2 allele. In contrast, one of 1618 individuals carried a ribosomal RNA internal transcribed spacer 1 (ITS1) derived from H. armigera. 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 H. armigera may continue to impact management tactics for H. zea.