Evidence that strong positive selection drives neofunctionalization in the tandemly duplicated polyhomeotic genes in Drosophila

Abstract

The polyhomeotic (ph) locus in Drosophila melanogaster consists of the two tandemly duplicated genes ph-d (distal) and ph-p (proximal). They code for transcriptional repressors belonging to the Polycomb group proteins, which regulate homeotic genes and hundreds of other loci. Although the duplication of ph occurred at least 25 million to 30 million years ago, both copies are very similar to each other at both the DNA and the protein levels, probably because of the action of frequent gene conversion. Despite this homogenizing force, differential regulation of both transcriptional units suggests that the functions of the duplicates have begun to diverge. Here, we provide evidence that this functional divergence is driven by positive selection. Based on resequencing of an approximately 30-kb region around the ph locus in an African sample of D. melanogaster X chromosomes, we identified a selective sweep, estimated its age and the strength of selection, and mapped the target of selection to a narrow interval of the ph-p gene. This noncoding region contains a large intron with several regulatory elements that are absent in the ph-d duplicate. Our results suggest that neofunctionalization has been achieved in the Drosophila ph genes through the action of strong positive selection and the inactivation of gene conversion in part of the gene.