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MBE Advance Access published online on November 10, 2004
Molecular Biology and Evolution, doi:10.1093/molbev/msi046
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2004; all rights reserved
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Accepted November 2, 2004

Research Article

Identifying Signatures of Selection at the Enhancer of split Neurogenic Gene Complex in Drosophila

Stuart J. Macdonald 1* and Anthony D. Long 1

1 Department of Ecology and Evolutionary Biology, University of California, Irvine, California, 92697-2525

* To whom correspondence should be addressed.
Stuart J. Macdonald, E-mail: sjm{at}uci.edu


  Abstract

The Enhancer of split gene complex [E(spl)-C] is one of the more highly annotated gene regions in Drosophila, and the 12 genes within the complex help determine the spacing and patterning of adult bristles. Any E(spl)-C coding, transcribed, or cis-regulatory regions experiencing non-neutral evolution are strong candidates to harbor polymorphisms contributing to naturally occurring variation in bristle number. We confirm that the E(spl)-C is strongly conserved, and show that 74% of regulatory elements previously identified in D. melanogaster are conserved in D. pseudoobscura. Regulatory elements in enhancer regions show lower nucleotide diversity and more rare polymorphisms compared to adjacent non-regulatory DNA, suggesting they are under purifying selection, and these effects are particularly pronounced when considering only conserved regulatory elements. The ratio of polymorphism to divergence was significantly different between transcription factor binding sites and non-binding sites within enhancer regions, suggesting the action of some form of selection. Too few polymorphisms in regions of the 3' UTR harboring regulatory motifs prevents adequate comparison of diversity and the polymorphism frequency spectrum between 3' UTR motif and non-motif sequence. We identified at least two broad regions of the gene complex showing strong population subdivision among four populations, which is suggestive of local adaptation or background selection. Finally, two regions of the E(spl)-C exhibit low nucleotide diversity, a high level of rare polymorphisms, and an increase in linkage disequilibrium, which together suggest the action of positive selection. Notably, the gene m2 shows a significant deviation from neutrality by the McDonald-Kreitman test, and resides in one of the two regions putatively experiencing a selective sweep. All sites in regions apparently visible to various selective forces are candidates for future work to determine their phenotypic effects.

Keywords: regulatory DNA; enhancer; conservation; selection; population structure.
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