Functional characterization and fitness cost of spinosad-resistant alleles in Ceratitis capitata

Abstract

<jats:title>Abstract</jats:title><jats:p>The sustainability of control programs for the Mediterranean fruit fly, <jats:italic>Ceratitis capitata,</jats:italic> for citrus crops in Spain has been threatened by the development of resistance to malathion and lambda-cyhalothrin in recent years. Spinosad is widely used without apparent loss of efficacy. However, a highly resistant strain, JW-100s, has been obtained after laboratory selection. Spinosad resistance in JW-100s has been associated with different mutant alleles of the α6 subunit of the nicotinic acetylcholine receptor (<jats:italic>Ccα6</jats:italic>) including an isoform-specific truncation allele, <jats:italic>Ccα6</jats:italic><jats:sup><jats:italic>3aQ68*</jats:italic></jats:sup>. Using the GAL4 &gt; UAS system in <jats:italic>Drosophila melanogaster</jats:italic> to demonstrate expression of this truncated α6 subunit, in a <jats:italic>dα6</jats:italic> loss-of-function genetic background, does not rescue susceptibility to spinosad, while the expression of <jats:italic>Ccα6</jats:italic> wild-type isoforms does. We have also generated <jats:italic>C. capitata</jats:italic> isolines from JW-100s homozygous for: (1) the <jats:italic>Ccα6</jats:italic><jats:sup><jats:italic>3aQ68*Δ3b</jats:italic>-<jats:italic>4</jats:italic></jats:sup> allele, which contains the mutation 3aQ68*, and (2) the <jats:italic>Ccα6</jats:italic><jats:sup><jats:italic>3aQ68*</jats:italic>–<jats:italic>K352*</jats:italic></jats:sup> allele, which contains the mutations 3aQ68* and K352*. Neither of these produce complete <jats:italic>Ccα6</jats:italic> transcripts. The frequency of resistant alleles declined when in competition with individuals carrying the wild-type allele. Through extensive testing of both biological and behavioral fitness traits, we identified a reduced ability of <jats:italic>Ccα6</jats:italic><jats:sup><jats:italic>3aQ68*Δ3b</jats:italic>-<jats:italic>4</jats:italic></jats:sup> males to detect the parapheromone and to mate with females carrying the <jats:italic>Ccα6</jats:italic><jats:sup><jats:italic>3aQ68*</jats:italic>–<jats:italic>K352*</jats:italic></jats:sup> allele in competition experiments. Thus, not only the potential for spontaneous resistant mutations to arise in <jats:italic>Ccα6</jats:italic> but also their fitness costs must be considered when planning resistance management strategies for <jats:italic>C. capitata</jats:italic>.</jats:p>