The Transcriptomic Response of the Boll Weevil, Anthonomus grandis grandis Boheman (Coleoptera: Curculionidae), following Exposure to the Organophosphate Insecticide Malathion

SIMPLE SUMMARY: The boll weevil, Anthonomus grandis grandis Boheman (Coleoptera: Curculionidae), is a pest of commercial cotton in the Americas. Eradication programs in the United States (USA) have been very successful and have reduced boll weevil occurrence to a small region in South Texas. The programs have relied almost exclusively on the chemical insecticide malathion for over forty years to treat boll weevils in the field. Despite this heavy selection pressure, the boll weevil remains susceptible to field application rates of this insecticide. Here, we present findings from an RNA-seq experiment documenting gene expression post-exposure to field-relevant concentrations of malathion, which was used to glean information about the boll weevil’s continued susceptibility to this insecticide. Additionally, we incorporated whole genome sequence data from nearly 200 pest individuals obtained from three distinct geographical areas (Texas, Mexico, and Argentina) to determine SNP frequency in the malathion target site: acetylcholine esterase. No evidence was found from gene expression or single nucleotide polymorphism (SNP) data consistent with a mechanism of enhanced tolerance or resistance adaptation in the boll weevil, corroborating long-term field observations. ABSTRACT: Insecticide tolerance and resistance have evolved countless times in insect systems. Molecular 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 USA 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 allele frequency of the malathion target site, as a proxy for directional selection in response to malathion exposure. 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.