The malathion-specific resistance gene confers a sperm competition advantage in Tribolium castaneum

1. Genes for insecticide resistance are usually traded against other fitness traits. However, in Tribolium castaneum, the opposite effect occurs under malathion-specific resistance: susceptible individuals show reduced reproductive success compared with resistant lines. 2. To determine the mechanisms within this unusual relationship, we explored male fertilization success after sperm competition between homozygotes of two isogenic lines that were only either resistant or susceptible to malathion. We also measured key male reproductive traits known to influence sperm competition and reproductive success. 3. Malathion-resistant males were superior sperm competitors than susceptible ones, which explains the rapid proliferation of the resistant genotype. This reproductive advantage was associated with increased ejaculate sperm number and sperm length for males carrying the resistance gene. Conversely, susceptible males have absolutely and relatively larger testis size. 4. Resistance to malathion is conferred by an increase in activity of a qualitatively variant detoxifying carboxylesterase enzyme compared to the 'original' enzyme composition in susceptible populations. Carboxylesterases also play important and conserved roles in sperm development, maturation and possibly fertilization in different taxa. 5. Our findings reveal a potential pleiotropic link between a single gene that codes for both insecticide resistance and influences key male reproductive traits through the regulation of carboxylesterase production.