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MBE Advance Access published online on August 19, 2007
Molecular Biology and Evolution, doi:10.1093/molbev/msm165
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© The Author 2007. 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

A Long-Term Evolutionary Pressure on the Amount of Non-Coding DNA

Carole Knibbe1,2, Antoine Coulon2, Olivier Mazet3, Jean-Michel Fayard4 and Guillaume Beslon2

1 Inserm, U571, Paris, F-75015, France
2 Laboratoire d'InfoRmatique en Images et Systèmes d'Information (LIRIS), UMR CNRS 5205, INSA-Lyon / Université, Claude Bernard Lyon 1, F-69621 Villeurbanne Cedex, France
3 Laboratoire de Statistiques et Probabilités (LSP), INSA-Toulouse, F-31077 Toulouse Cedex 4, France
4 Laboratoire de Biologie Fonctionnelle, Insectes et Interactions, UMR INRA/INSA 203 BF2I, INSA-Lyon, F-69621 Villeurbanne Cedex, France

Corresponding author: Guillaume Beslon, LIRIS, INSA-Lyon, Bat. Blaise Pascal, 69621 Villeurbanne cedex, France, Tel. +33 4 72 43 84 87, Fax. +33 4 72 43 83 14, e-mail: guillaume.beslon{at}insa-lyon.fr

Received for publication June 15, 2007. Accepted for publication August 3, 2007.

A significant part of eukaryotic non-coding DNA is viewed as the passive result of mutational processes, such as the proliferation of mobile elements. However, sequences lacking an immediate utility can nonetheless play a major role in the long-term evolvability of a lineage, for instance by promoting genomic rearrangements. They could thus be subject to an indirect selection. Yet such a long-term effect is difficult to isolate either in vivo or in vitro. Here, by performing in silico experimental evolution, we demonstrate that, under low mutation rates, the indirect selection of variability promotes the accumulation of non-coding sequences: Even in the absence of self-replicating elements and mutational bias, non-coding sequences constituted an important fraction of the evolved genome, because the indirectly selected genomes were those that were variable enough to discover beneficial mutations. On the other hand, high mutation rates lead to compact genomes, much like the viral ones, although no selective cost of genome size was applied: The indirectly selected genomes were those that were small enough for the genetic information to be reliably transmitted. Thus the spontaneous evolution of the amount of non-coding DNA strongly depends on the mutation rate. Our results suggest the existence of an additional pressure on the amount of non-coding DNA, namely the indirect selection of an appropriate trade-off between the fidelity of the transmission of the genetic information and the exploration of the mutational neighbourhood. Interestingly, this trade-off resulted robustly in the accumulation of non-coding DNA so that the best individual leaves one offspring without mutation (or only neutral ones) per generation.

Key Words: Adaptive evolution • non-coding DNA • mutation rate • rearrangements • mutational variability • indirect selection


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