DDT resistance in flies carries no cost

Mutations that confer pesticide resistance are predicted to carry a cost in the absence of pesticide and consequently not to spread to fixation [1,2]. However, DDT resistance in Drosophila melanogaster (DDT-R) is approaching fixation globally, long after withdrawl of DDT [3]. There are two possible explanations for this. First, other insecticides, to which DDT-R confers cross-resistance [4], may be continuing selection. Second, DDT-R may not carry the expected fitness cost. Here we look at the fitness of DDT-R in the absence of insecticide. Surprisingly, when inherited via the female, the DDT-R locus actually increases both adult fecundity and the viability of eggs and larvae, as well as speeding both larval and pupal development. Despite the ability to select for several different cytochrome P450 genes conferring resistance to DDT in the laboratory [5-8], resistance in all current field strains is associated with overexpression of a single allele of a single gene, Cyp6g1, carrying an Accord transposon in its 5′ end [3,9]. This single allele was found in all resistant strains from a global survey of ~600 current field strains, and global frequencies of DDT-R, in nonAfrican D. melanogaster populations, are approaching fixation [3]. In an outstanding example of parallel evolution, insertion of a different transposable element in the 5′ end of the Cyp6g1 homolog in D. simulans was also shown to be associated with insecticide resistance [10]. DDT-R is therefore a widespread and representative mechanism of insecticide resistance. To look for costs associated with DDT-R we chose the historically important strain Hikone-R [11], which contains exactly the same allele as that present in all current resistant field strains [9]. We backcrossed the Hikone-R resistant strain five times to a standard susceptible strain Canton-S, to reduce the effect of differing genetic backgrounds. We also cured both strains of Wolbachia (see the supplemental data available with this article online), to eliminate any potential alteration of fecundity by this intracellular bacterium [12,13]. We then compared egg, larval and pupal viability, as well as the total number of eggs laid by adults, at two different temperatures, in a full life history analysis of the backcrossed resistant strain versus the original susceptible strain. We also compared heterozygous flies where resistance was inherited from the female (RS) with flies where resistance was inherited from the male (SR). Surprisingly, RS flies significantly outperform their SR counterparts in counts of egg and larval viability at both 20°C and 25°C (Figure 1A,B); however, this advantage disappears during the pupal stage (Figure1C). This disappearance of the RS advantage in the pupal stage is similar to phenotypes conferred by other genes showing a maternal contribution in flies [14]. Further at 20°C, RS genotypes again developed faster than their