Genomic patterns of pleiotropy and the evolution of complexity

Pleiotropy refers to the phenomenon of a single mutation or gene affecting multiple distinct phenotypic traits and has broad implications in many areas of biology. Due to its central importance, pleiotropy has also been extensively modeled, albeit with virtually no empirical basis. Analyzing phenoty...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 107; no. 42; pp. 18034 - 18039
Main Authors Wang, Zhi, Liao, Ben-Yang, Zhang, Jianzhi, Wagner, Günter P.
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 19.10.2010
National Acad Sciences
SeriesFrom the Cover
Subjects
Adaptations
Biological Evolution
Biological Sciences
Datasets
Evolution
Evolutionary genetics
Gene deletion
Genes
Genetic mutation
Genetic research
Genomics
Modularity
Mutation
Nematoda
Phenotypic traits
Pleiotropy
Quantitative traits
Scaling
Yeasts
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Summary:Pleiotropy refers to the phenomenon of a single mutation or gene affecting multiple distinct phenotypic traits and has broad implications in many areas of biology. Due to its central importance, pleiotropy has also been extensively modeled, albeit with virtually no empirical basis. Analyzing phenotypes of large numbers of yeast, nematode, and mouse mutants, we here describe the genomic patterns of pleiotropy. We show that the fraction of traits altered appreciably by the deletion of a gene is minute for most genes and the gene–trait relationship is highly modular. The standardized size of the phenotypic effect of a gene on a trait is approximately normally distributed with variable SDs for different genes, which gives rise to the surprising observation of a larger per-trait effect for genes affecting more traits. This scaling property counteracts the pleiotropy-associated reduction in adaptation rate (i.e., the “cost of complexity”) in a nonlinear fashion, resulting in the highest adaptation rate for organisms of intermediate complexity rather than low complexity. Intriguingly, the observed scaling exponent falls in a narrow range that maximizes the optimal complexity. Together, the genome-wide observations of overall low pleiotropy, high modularity, and larger per-trait effects from genes of higher pleiotropy necessitate major revisions of theoretical models of pleiotropy and suggest that pleiotropy has not only allowed but also promoted the evolution of complexity.
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Author contributions: Z.W. and J.Z. designed research; Z.W. and B.-Y.L. performed research; Z.W. and J.Z. analyzed data; and Z.W. and J.Z. wrote the paper.
Edited by Günter P. Wagner, Yale University, New Haven, CT, and accepted by the Editorial Board August 31, 2010 (received for review April 6, 2010)
1Present address: Sage Bionetworks, Seattle, WA 98109.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1004666107