Abstract
The increased transcription of the Cyp6g1 gene of Drosophila melanogaster, and consequent resistance to insecticides such as DDT, is a widely cited example of adaptation mediated by cis-regulatory change. A fragment of an Accord transposable element inserted upstream of the Cyp6g1 gene is causally associated with resistance and has spread to high frequencies in populations around the world since the 1940s. Here we report the existence of a natural allelic series at this locus of D. melanogaster, involving copy number variation of Cyp6g1, and two additional transposable element insertions (a P and an HMS-Beagle). We provide evidence that this genetic variation underpins phenotypic variation, as the more derived the allele, the greater the level of DDT resistance. Tracking the spatial and temporal patterns of allele frequency changes indicates that the multiple steps of the allelic series are adaptive. Further, a DDT association study shows that the most resistant allele, Cyp6g1-[BP], is greatly enriched in the top 5% of the phenotypic distribution and accounts for ∼16% of the underlying phenotypic variation in resistance to DDT. In contrast, copy number variation for another candidate resistance gene, Cyp12d1, is not associated with resistance. Thus the Cyp6g1 locus is a major contributor to DDT resistance in field populations, and evolution at this locus features multiple adaptive steps occurring in rapid succession.
Highlights
The genetic basis of adaptation remains one of the central unresolved issues within evolutionary biology
Cyp6g1 resistance alleles are selected, in parallel, in sibling species, we show that they have been repeatedly selected, in series, in D. melanogaster
These results are pertinent to a long-standing evolutionary debate concerning the number of steps that have to occur to move a species to a new adaptive optimum [6,55]
Summary
The genetic basis of adaptation remains one of the central unresolved issues within evolutionary biology. Recent studies of Drosophila and bacteria suggest that a large proportion of nucleotide fixations in these genomes are adaptive, their individual effects on fitness are typically small [1,2,3,4,5]. The predominant examples come from Quantitative Trait Loci (QTL) studies, which suffer from biases, notably that genes of small effect will generally not be identified. Another bias is that a single Quantitative Trait Locus may result from multiple allelic substitutions and QTL studies by themselves could underestimate the number of changes in a bout of adaptive evolution. It offers an opportunity to view an adaptive response to a change in a single environmental component and it occurs on a timescale that allows multiple genetic changes to be observed
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