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Open Access Research article

Natural selection governs local, but not global, evolutionary gene coexpression networks in Caenorhabditis elegans

I King Jordan1*, Lee S Katz1, Dee R Denver2 and J Todd Streelman3

Author Affiliations

1 School of Biology, Georgia Institute of Technology, Atlanta, GA, USA

2 Department of Zoology & Center for Genome Research and Biocomputing, Oregon State University, Corvallis, OR, USA

3 School of Biology & Institute of Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, USA

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BMC Systems Biology 2008, 2:96  doi:10.1186/1752-0509-2-96

Published: 13 November 2008

Abstract

Background

Large-scale evaluation of gene expression variation among Caenorhabditis elegans lines that have diverged from a common ancestor allows for the analysis of a novel class of biological networks – evolutionary gene coexpression networks. Comparative analysis of these evolutionary networks has the potential to uncover the effects of natural selection in shaping coexpression network topologies since C. elegans mutation accumulation (MA) lines evolve essentially free from the effects of natural selection, whereas natural isolate (NI) populations are subject to selective constraints.

Results

We compared evolutionary gene coexpression networks for C. elegans MA lines versus NI populations to evaluate the role that natural selection plays in shaping the evolution of network topologies. MA and NI evolutionary gene coexpression networks were found to have very similar global topological properties as measured by a number of network topological parameters. Observed MA and NI networks show node degree distributions and average values for node degree, clustering coefficient, path length, eccentricity and betweeness that are statistically indistinguishable from one another yet highly distinct from randomly simulated networks. On the other hand, at the local level the MA and NI coexpression networks are highly divergent; pairs of genes coexpressed in the MA versus NI lines are almost entirely different as are the connectivity and clustering properties of individual genes.

Conclusion

It appears that selective forces shape how local patterns of coexpression change over time but do not control the global topology of C. elegans evolutionary gene coexpression networks. These results have implications for the evolutionary significance of global network topologies, which are known to be conserved across disparate complex systems.