Universal pacemaker of genome evolution

Abstract

Molecular clock (MC) is a central concept of molecular evolution according to which each gene evolves at a characteristic, near constant rate. Numerous evolutionary studies have demonstrated the validity of MC but also have shown that MC is substantially overdispersed, i.e. lineage-specific deviations of the evolutionary rate of the given gene from the clock greatly exceed the expectation from the sampling error. A fundamental observation of comparative genomics that appears to complement the MC is that the distribution of evolution rates across orthologous genes in pairs of related genomes remains virtually unchanged throughout the evolution of life, from bacteria to mammals. The conservation of this distribution implies that the relative evolution rates of all genes remain nearly constant, or in other words, that evolutionary rates of different genes are strongly correlated within each evolving genome. We hypothesized that this correlation is not a simple consequence of MC but could be better explained by a model we dubbed Universal PaceMaker (UPM) of genome evolution. The UPM model posits that the rate of evolution changes synchronously across genome-wide sets of genes in all evolving lineages. We sought to differentiate between the MC and UPM models by fitting thousands of phylogenetic trees for bacterial and archaeal genes to supertrees that reflect the dominant trend of vertical descent in the evolution of archaea and bacteria and that were constrained according to the two models. The goodness of fit for the UPM model was better than the fit for the MC model, with overwhelming statistical significance. These results reveal a universal pacemaker of genome evolution that could have been in operation throughout the history of life.