Role of a gamma‐aminobutryic acid (GABA) receptor mutation in the evolution and spread of Diabrotica virgifera virgifera resistance to cyclodiene insecticides

Abstract

The western corn rootworm, Diabrotica virgifera virgifera, is a damaging pest of cultivated corn that was controlled by applications of cyclodiene insecticides from the late 1940s until resistance evolved ∼10 years later. Range expansion from the western plains into eastern USA coincides with resistance development. An alanine to serine amino acid substitution within the Rdl subunit of the gamma-aminobutyric acid (GABA) receptor confers resistance to cyclodiene insecticides in many species. We found that the non-synonymous single nucleotide polymorphism (SNP) G/T at the GABA receptor cDNA position 838 (G/T(838)) of D. v. virgifera resulted in the alanine to serine change, and the codominant SNP allele T(838) was genetically linked to survival of beetles in aldrin bioassays. A phenotypic gradient of decreasing susceptibility from west to east was correlated with higher frequencies of the resistance-conferring T(838) allele in the eastern-most populations. This pattern exists in opposition to perceived selective pressures since the more eastern and most resistant populations probably experienced reduced exposure. The reasons for the observed distribution are uncertain, but historical records of the range expansion combined with the distribution of susceptible and resistant phenotypes and genotypes provide an opportunity to better understand factors affecting the species' range expansion.

Role of dispersal in resistance evolution and spread

“…Both species were also subsequently introduced into Europe. Resistance to cyclodienes in D. v. virgifera is due to a mutation in the target gamma-amino butyric acid receptor gene, which exhibits a cline of increasing frequency toward the east coast of the United States [31]. This is surprising given that cyclodienes were withdrawn from use over a decade before the species reached the east coast and may represent an example of gene surfing [31].…”

“…Resistance to cyclodienes in D. v. virgifera is due to a mutation in the target gamma-amino butyric acid receptor gene, which exhibits a cline of increasing frequency toward the east coast of the United States [31]. This is surprising given that cyclodienes were withdrawn from use over a decade before the species reached the east coast and may represent an example of gene surfing [31]. Unlike populations in the United States, introduced European populations of D. v. virgifera are uniformly resistant to cyclodienes and susceptible to organophosphates [32].…”

Proliferation and copy number variation of BEL-like long terminal repeat retrotransposons within the Diabrotica virgifera virgifera genome

“…Query of the 4173 D. v. virgifera genomic contigs with previously described BEL/Pao gag-pol protein sequences resulted in "hits" to 99 contigs with amino acid similarities ≥37.6% (contig size 1482 to 9296bp; ORF size 434 to 1866 amino acids; Supplementary File S1). Similarly, queries of previously assembled BAC inserts (Coates et al, 2012;Wang et al, 2013) identified regions of clones 213A05 and 278L20 with ≥38% identity to the T. castaneum BEL12_AG TcBEL LTR transposon (GenBank accession XP_001809963.1; remaining results not shown).…”

“…A BAC library constructed from D. v. virgifera, called DvvBAC1, was previously described by Coates et al (2012). High throughput genomic sequence (HTGS) submissions representing contigs derived from full DvvBAC1 inserts were downloaded from the National Center for Biotechnology Information; JQ581035 to JM581042 (Coates et al, 2012), KC248067 to KC248069 (Wang et al, 2013), and KC962414 to KC962431 (Coates et al, unpublished). BAC inserts were sequenced on a Roche 454 sequencer, and read data were assembled into contigs using the Newbler assembler (Roche Applied Sciences, Penzberg, Germany).…”

“…Recently, resistance to commercial corn hybrids that express a Bacillus thuringiensis (Bt) toxin has been documented in some D. v. virgifera populations (Gassmann et al, 2011). The genetic basis of many resistance traits in D. v. virgifera remains undetermined, but resistance to the organochlorine insecticide, aldrin, has been linked to a point mutation within the gamma-aminobutyric acid (GABA) receptor (Wang et al, 2013). Organophosphate resistance traits were partially linked to increased carboxylesterase activities in adult D. v. virgifera (Miota et al, 1998;Zhou et al, 2003), but the mechanism(s) underlying this adaptation remains unknown.…”