The transcriptomic response of the boll weevil, Anthonomus grandis grandis Boheman (Coleoptera: Curculionidae), following exposure to the organophosphate insecticide malathion

Authors: Perkin, Lindsey; Cohen, Zachary; CARLSON, JASON - Animal And Plant Health Inspection Service (APHIS); Suh, Charles

Submitted to: Insects
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/11/2023
Publication Date: 2/16/2023
Citation: Perkin, L.C., Cohen, Z.P., Carlson, J.W., Suh, C.P. 2023. The transcriptomic response of the boll weevil, Anthonomus grandis grandis Boheman (Coleoptera: Curculionidae), following exposure to the organophosphate insecticide malathion. Insects. 14(2). Article 197. https://doi.org/10.3390/insects14020197.
DOI: https://doi.org/10.3390/insects14020197

Interpretive Summary: Boll weevil eradication programs in the U.S. have relied exclusively on the insecticide malathion for the past 40 years to suppress weevil populations in cotton. Although the boll weevil quickly developed resistance to several insecticides during the early stages of eradication, the boll weevil has not developed resistance to malathion despite its extensive and long-term use. However, the development of malathion resistance in the boll weevil remains a major concern to programs because alternative insecticides that are relatively safe, and both economical and effective do not exist. We exposed boll weevils to malathion and identified genes that changed in expression over a 24-hour period to gain insight into the boll weevil's ability to develop resistance to malathion and to better understand why the boll weevil remains susceptible to this insecticide. We found the boll weevil possesses the same types of genes that are known to play a critical role in insecticide resistance in other insects but unlike in insecticide-resistant insects, these types of genes in the boll weevil do not increase in expression following exposure to malathion. Our findings indicate that the boll weevil possesses the foundational genes to develop resistance to malathion but these genes fail to increase in expression following malathion exposure. The reason these genes fail to increase in expression is unknown but this finding explains why the boll weevil remains susceptible to malathion.

Technical Abstract: Insecticide tolerance and resistance have evolved countless times in insect systems. Drivers of resistance include mutations in the insecticide target site and/or gene duplication, and increased gene expression of detoxification enzymes. The boll weevil, Anthonomus grandis grandis Boheman (Coleoptera: Curculionidae), is a pest of commercial cotton and has developed resistance in the field to several insecticides; however, the current organophosphate insecticide, malathion, used by US eradication programs remains effective despite its long-term use. Here, we present findings from an RNA-seq experiment documenting gene expression post-exposure to field-relevant concentrations of malathion, which was used to provide insight on the boll weevil’s continued susceptibility to this insecticide. Additionally, we incorporated a large collection of boll weevil whole-genome resequencing data from nearly 200 individuals collected from three geographically distinct areas to determine SNP frequency in the malathion target site, as a proxy for directional selection in response to malathion treatment. No evidence was found in the gene expression data or SNP data consistent with a mechanism of enhanced tolerance or resistance adaptation to malathion in the boll weevil. Although this suggests continued effectiveness of malathion in the field, we identified important temporal and qualitative differences in gene expression between weevils exposed to two different concentrations of malathion. We also identified several tandem isoforms of the detoxifying esterase B1 and glutathione S-transferases, which are putatively associated with organophosphate resistance.