Originally published as Genetics Published Articles Ahead of Print on March 21, 2005.

Genetics, Vol. 170, 433-446, May 2005, Copyright © 2005
doi:10.1534/genetics.104.027607

The Origin of Subfunctions and Modular Gene Regulation

Allan Force*,1, William A. Cresko{dagger},{ddagger}, F. Bryan Pickett§, Steven R. Proulx{ddagger}, Chris Amemiya* and Michael Lynch**

* Benaroya Research Institute at Virginia Mason, Seattle, Washington 98101
{dagger} Institute of Neuroscience, University of Oregon, Eugene, Oregon 97403
§ Department of Biology, Loyola University, Chicago, Illinois 60626
{ddagger} Center for Ecology and Evolutionary Biology, University of Oregon, Eugene, Oregon 97403
** Department of Biology, Indiana University, Bloomington, Indiana 47405

1 Corresponding author: Benaroya Research Institute at Virginia Mason, 1201 Ninth Ave., Seattle, WA 98101.
E-mail: force{at}vmresearch.org

Evolutionary explanations for the origin of modularity in genetic and developmental pathways generally assume that modularity confers a selective advantage. However, our results suggest that even in the absence of any direct selective advantage, genotypic modularity may increase through the formation of new subfunctions under near-neutral processes. Two subfunctions may be formed from a single ancestral subfunction by the process of fission. Subfunction fission occurs when multiple functions under unified genetic control become subdivided into more restricted functions under independent genetic control. Provided that population size is sufficiently small, random genetic drift and mutation can conspire to produce changes in the number of subfunctions in the genome of a species without necessarily altering the phenotype. Extensive genotypic modularity may then accrue in a near-neutral fashion in permissive population-genetic environments, potentially opening novel pathways to morphological evolution. Many aspects of gene complexity in multicellular eukaryotes may have arisen passively as population size reductions accompanied increases in organism size, with the adaptive exploitation of such complexity occurring secondarily.




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