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Morphological evolution caused by many subtle-effect substitutions in regulatory DNA

Nicolás Frankel, Deniz F. Erezyilmaz, Alistair P. McGregor, Shu Wang, François Payre and David L. Stern ()
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Nicolás Frankel: Princeton University
Deniz F. Erezyilmaz: Princeton University
Alistair P. McGregor: Institut für Populationsgenetik, Veterinärmedizinische Universität Wien
Shu Wang: Princeton University
François Payre: Université de Toulouse and Centre National de la Recherche Scientifique, Centre de Biologie du Développement, UMR5547
David L. Stern: Princeton University

Nature, 2011, vol. 474, issue 7353, 598-603

Abstract: Abstract Morphology evolves often through changes in developmental genes, but the causal mutations, and their effects, remain largely unknown. The evolution of naked cuticle on larvae of Drosophila sechellia resulted from changes in five transcriptional enhancers of shavenbaby (svb), a transcript of the ovo locus that encodes a transcription factor that governs morphogenesis of microtrichiae, hereafter called ‘trichomes’. Here we show that the function of one of these enhancers evolved through multiple single-nucleotide substitutions that altered both the timing and level of svb expression. The consequences of these nucleotide substitutions on larval morphology were quantified with a novel functional assay. We found that each substitution had a relatively small phenotypic effect, and that many nucleotide changes account for this large morphological difference. In addition, we observed that the substitutions had non-additive effects. These data provide unprecedented resolution of the phenotypic effects of substitutions and show how individual nucleotide changes in a transcriptional enhancer have caused morphological evolution.

Date: 2011
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DOI: 10.1038/nature10200

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