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MBE Advance Access published online on June 25, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn143
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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

Frequent and Widespread Parallel Evolution of Protein Sequences

Antonis Rokas1 and Sean B. Carroll2,*

1 . Vanderbilt University, Department of Biological Sciences, VU Station B 351634, Nashville, TN 37235, USA. Email: antonis.rokas{at}vanderbilt.edu

2 . Howard Hughes Medical Institute and University of Wisconsin-Madison, R. M. Bock Laboratories, 1525 Linden Drive, Madison, WI 53706, USA. Email: sbcarrol@wisc.edu

* Author for correspondence: Sean B. Carroll (Email: sbcarrol{at}wisc.edu, tel: 608-262-6191, fax: 608-262-9343)

Received for publication May 13, 2008. Revision received June 17, 2008. Accepted for publication June 19, 2008.

Understanding the patterns and causes of protein sequence evolution is a major challenge in evolutionary biology. One of the critical unresolved issues is the relative contribution of selection and genetic drift to the fixation of amino acid sequence differences between species. Molecular homoplasy, the independent evolution of the same amino acids at orthologous sites in different taxa, is one potential signature of selection, however, relatively little is known about its prevalence in eukaryotic proteomes. To quantify the extent and type of homoplasy among evolving proteins, we used phylogenetic methodology to analyze eight genome-scale data matrices from clades of different evolutionary depths that span the eukaryotic tree of life. We found that the frequency of homoplastic amino acid substitutions in eukaryotic proteins was more than 2-fold higher than expected under neutral models of protein evolution. The overwhelming majority of homoplastic substitutions were parallelisms that involved the most frequently exchanged amino acids with similar physicochemical properties and that could be reached by a single mutational step. We conclude that the role of homoplasy in shaping the protein record is much larger than generally assumed, and we suggest that its high frequency can be explained by both weak positive selection for certain substitutions and purifying selection that constrains substitutions to a small number of functionally equivalent amino acids.

Key Words: homoplasy • positive selection • selective constraint • protein • independent evolution


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