Abstract

Cockroaches are important global urban pests from aesthetic and health perspectives. Insecticides represent the most cost-effective way to control cockroaches and limit their impacts on human health. However, cockroaches readily develop insecticide resistance, which can quickly limit efficacy of even the newest and most effective insecticide products. The goal of this research was to understand whole-body physiological responses in German cockroaches, at the metatranscriptome level, to defined insecticide selection pressures. We used the insecticide indoxacarb as the selecting insecticide, which is an important bait active ingredient for cockroach control. Six generations of selection with indoxacarb bait produced a strain with substantial (>20×) resistance relative to inbred control lines originating from the same parental stock. Metatranscriptome sequencing revealed 1,123 significantly differentially expressed (DE) genes in ≥two of three statistical models (81 upregulated and 1,042 downregulated; FDR P < 0.001; log2FC of ±1). Upregulated DE genes represented many detoxification enzyme families including cytochrome-P450 oxidative enzymes, hydrolases and glutathione-S-transferases. Interestingly, the majority of downregulated DE genes were from microbial and viral origins, indicating that selection for resistance is also associated with elimination of commensal, pathogenic and/or parasitic microbes. These microbial impacts could result from: (i) direct effects of indoxacarb, (ii) indirect effects of antimicrobial preservatives included in the selecting bait matrix, or (iii) selection for general stress response mechanisms that confer both xenobiotic resistance and immunity. These results provide novel physiological insights into insecticide resistance evolution and mechanisms, as well as novel insights into parallel fitness benefits associated with selection for insecticide resistance.

Highlights

  • The German cockroach, Blattella germanica L. is an international urban pest that affects millions of residences on a global scale (Vargo, 2021)

  • The resulting overlapping sequences were assembled into 207,672 contiguous sequences, hereafter referred to as “contigs.” Sequence reads are deposited in the NCBI GEO archive under accession number GSE188950

  • Further investigation of candidate gene expression in the highly resistant Oviedo-R strain suggests common phenomena that underlie resistance evolution. These findings support the idea that high-level resistance evolution results from a dual process whereby the host tolerates the selecting insecticide through a number of potential mechanisms, and in parallel, host fitness is further increased as the body is cleared of parasites and pathogens. At present it remains unclear if the microbial impacts result from (i) direct effects of indoxacarb, (ii) indirect effects of antimicrobial preservatives included in the selecting bait matrix, or (iii) selection for general stress response mechanisms that confer both xenobiotic resistance and microbial immunity

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Summary

Introduction

The German cockroach, Blattella germanica L. is an international urban pest that affects millions of residences on a global scale (Vargo, 2021). Insecticide resistance has been a formidable recurring barrier to effective cockroach control for decades (Scharf and Gondhalekar, 2021). Because cockroaches live in relatively closed populations (Crissman et al, 2010; Vargo et al, 2014; Vargo, 2021), resistance can build quickly, even with moderate insecticide selection pressure (Scharf et al, 1997a,b; Gondhalekar et al, 2013; Fardisi et al, 2019). Cockroach baits are widely used in management programs and have been an effective tool for controlling cockroaches and reducing pesticide loads in urban housing (e.g., Miller and Smith, 2020); resistance can readily develop even to bait insecticides (Gondhalekar et al, 2011, 2013, 2016; Gondhalekar and Scharf, 2012, 2013; Ko et al, 2016; Fardisi et al, 2019)

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