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Protein Evolution in the Context of Drosophila Development

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Abstract

The tempo at which a protein evolves depends not only on the rate at which mutations arise but also on the selective effects that those mutations have at the organismal level. It is intuitive that proteins functioning during different stages of development may be predisposed to having mutations of different selective effects. For example, it has been hypothesized that changes to proteins expressed during early development should have larger phenotypic consequences because later stages depend on them. Conversely, changes to proteins expressed much later in development should have smaller consequences at the organismal level. Here we assess whether proteins expressed at different times during Drosophila development vary systematically in their rates of evolution. We find that proteins expressed early in development and particularly during mid–late embryonic development evolve unusually slowly. In addition, proteins expressed in adult males show an elevated evolutionary rate. These two trends are independent of each other and cannot be explained by peculiar rates of mutation or levels of codon bias. Moreover, the observed patterns appear to hold across several functional classes of genes, although the exact developmental time of the slowest protein evolution differs among each class. We discuss our results in connection with data on the evolution of development.

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Acknowledgments

We would like to thank Mark Siegal, Michelle Arbeitman, Bruce Baker, Cristian Castillo-Davis, Asher Cutter, Tobias Meyer, and Nadia Singh for helpful advice and discussions regarding the manuscript and Michael Brudno for technical advice. This work was funded by NSF predoctoral fellowships awarded to J.C.D. and O.B. and the Sloan Research Fellowship awarded to D.A.P.

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Correspondence to Onn Brandman.

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Jerel C. Davis and Onn Brandman contributed equally to this work.

Reviewing Editor: ManYuan Long

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Davis, J.C., Brandman, O. & Petrov, D.A. Protein Evolution in the Context of Drosophila Development. J Mol Evol 60, 774–785 (2005). https://doi.org/10.1007/s00239-004-0241-2

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