Evolution of the genomic universe

Abstract

The rapid growth of the collection of genome sequences from diverse bacteria, archaea, eukaryotes and viruses representing all known major taxa allows us to start charting the “genomic universe”, that is the entirety of distinct genes that comprise the genomes. The key feature of the genomic universe is the striking evolutionary stability of genes some of which have maintained their identity throughout almost the entire 4 billion years since the origin of life on earth. Genes are organized into clusters of orthologs which are descendants of the same ancestral gene from different life forms in some of which they expand to form families of paralogs. In contrast to the evolutionary stability of genes is the fluidity of genomes that on the evolutionary scale are dynamic, transient ensembles of genes. The existence of this distinctive organization in the genomic universe makes it conducive to quantitative analysis in search of “genomic laws”. Such analyses have led to the discovery of several universal relationships between variables that characterize evolution and function of genomes, genes and their products. The most important of such universals include the log-normal distribution of the evolutionary rates of orthologous genes; the distinct, U-shaped distribution of gene frequencies in genomes; the power law-like distribution of paralogous family size; and the differential scaling of functional classes of genes with genome size. These universal patterns can be explained by straightforward mathematical models of evolution that consist only of simple fundamental processes, such as gene gain, loss and duplication, but require selection to fully account for the shapes of the observed distributions. The existence of universals that can be accounted for through simple generative models implies that at coarse grain, the genomic universe can be represented as a “gas” of weakly interacting genes although such a description certainly is insufficient to explain organismal biology. Phylogenomic analysis reveals a highly dynamic picture of the evolution of the genomic universe that is dominated by horizontal gene transfer. Nevertheless, a “statistical Tree of Life” can be recovered as a strong signal of vertical evolution.