Selective Sweeps at the Organophosphorus Insecticide Resistance Locus, Rop-1, Have Affected Variation across and beyond the α-Esterase Gene Cluster in the Australian Sheep Blowfly, Lucilia cuprina

A major theoretical consequence of selection at a locus is the genetic hitchhiking of linked sites (selective sweep). The extent of hitchhiking around a gene is related to the strength of selection and the rate of recombination, with its impact diminishing with distance from the selected site. At the Rop-1 locus of the sheep blowfly, Lucilia cuprina, polymorphisms at two different sites within the Lc alpha E7 gene encode forms of the protein that confer organophosphorus insecticide resistance. To assess the impact of selection at these two sites on variation around Lc alpha E7, we sequenced regions within six other genes along chromosome IV across isogenic (IV) strains of L. cuprina. High levels of linkage disequilibrium, characterized by low haplotype number (K) and diversity (H), and significant R-2 values were observed for two genes, Lc alpha E1 and Lc alpha E10, both members of the same alpha-esterase gene cluster as Lc alpha E7. A significant R-2 value was also observed for a gene predicted to be the next closest to Lc alpha E7, AL03, but not for any of the other genes, LcRpL13a, Lcdsx, or LcAce. Skews in the site frequency spectra toward high-frequency variants were significant for Lc alpha E1 (Fay and Wu's H = -2.91), Lc alpha E10 (H = -1.85), and Lcdsx (H = -2.00). Since the selective sweeps, two forms of likely returning variation were observed, including variation in microsatellites in an intron of Lc alpha E10 and a recombination event between Lc alpha E7 and Lc alpha E10. These data suggest that two incomplete soft sweeps have occurred at Lc alpha E7 that have significantly affected variation across, and beyond, the alpha-esterase gene cluster of L. cuprina. The speed and impact of these selective sweeps on surrounding genomic variation and the ability of L. cuprina to respond to future environmental challenges are discussed.