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PMID: 21720363 Published · epublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

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

Nature ·Vol. 474 ·No. 7353 ·2011-06-29 ·Pages 598-603

Frankel N, Erezyilmaz DF, McGregor AP, Wang S, Payre F, Stern DL

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.

MeSH Terms
Animals Base Sequence Biological Evolution DNA-Binding Proteins/genetics,metabolism Drosophila/anatomy & histology,embryology,genetics Drosophila Proteins/genetics,metabolism Drosophila melanogaster/anatomy & histology,embryology,genetics Embryo, Nonmammalian Enhancer Elements, Genetic/genetics Female Gene Expression Regulation, Developmental Larva Male Phenotype Sequence Alignment Sequence Homology, Nucleic Acid Transcription Factors/genetics,metabolism
Chemicals
DNA-Binding Proteins Drosophila Proteins Transcription Factors ovo protein, Drosophila
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Frankel Nicolás
Howard Hughes Medical Institute and Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey 08544, USA.
Erezyilmaz Deniz F
McGregor Alistair P
Wang Shu
Payre François
Stern David L
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Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
DOI
10.1038/nature10200
Published
2011-06-29
Epub
2011-00-29
Pages
598-603
Language
English
Region
England
NLM ID
0410462
PMCID
PMC3170772
Subset
IM
Grants
NIGMS NIH HHS · GM063622-06A1 · United States
NIGMS NIH HHS · F32 GM 83546-02 · United States
Howard Hughes Medical Institute · United States
NIGMS NIH HHS · F32 GM083546 · United States
NIGMS NIH HHS · R01 GM063622-09 · United States
NIGMS NIH HHS · R01 GM063622 · United States
External Links
PubMed source DOI: 10.1038/nature10200 PMC Full Text View journal details
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