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MBE Advance Access published online on August 28, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn189
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© The Author 2008. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Article

Developmental Stage and Level of Codon Usage Bias in Drosophila

Saverio Vicario1,3, Christopher E. Mason2, Kevin P. White2 and Jeffrey R. Powell1

1 Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT USA 06520-8105
2 Department of Genetics (School of Medicine), Yale University, New Haven, CT USA 06520-8105

3 Corresponding author and current address: Saverio Vicario, CNR- ITB, Via Amendola 122D, Bari 70126. Telephone: 39-338-7407518 (Vicario) or 1-203-432-3887 (Powell). Email: saverio.vicario{at}yale.edu or jeffrey.powell{at}yale.edu

Received for publication February 29, 2008. Revision received June 29, 2008. Accepted for publication July 4, 2008.

Codon usage bias (CUB) is a ubiquitous observation in molecular evolution. As a model, Drosophila has been particularly well-studied and indications are that selection at least partially controls codon usage probably through selection for translational efficiency. While many aspect of Drosophila CUB have been studied, this is the first study relating codon usage to development in this holometabolous insect with very different life stages. Here we ask the question: What developmental stage of Drosophila melanogaster has the greatest CUB? Genes with maximum expression in the larval stage have the greatest overall CUB compared to embryos, pupae, and adults. (The same pattern was observed in D. pseudoobscura, Supplementary Material.) We hypothesize this is related to the very rapid growth of larvae, placing increased selective pressure to produce large amounts of protein: a 300-fold increase requiring an approximate doubling of protein content every 10 hours. Genes with highest expression in adult males and early embryos, stages with the least de novo protein synthesis, display the least CUB. These results are consistent with the hypothesis that codon usage bias is caused (at least in part) by selection for efficient protein production. This seems to hold on the individual gene level (highly expressed genes are more biased than lowly expressed genes) as well as on a more global scale where genes with maximum expression during times of very rapid growth and protein stynthesis are more biased than genes with maximum expression during times of low growth.

Key Words: codon usage bias • protein synthesis • Drosophila • development • melanogaster • pseudoobscura • larval stage


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