Darwinian evolution in the light of genomics

Abstract

Comparative genomics and systems biology offer unprecedented opportunities for testing central tenets of evolutionary biology formulated by Darwin in the Origin of Species in 1859 and expanded in the Modern Synthesis 100 years later. Evolutionary-genomic studies show that natural selection is only one of the forces that shape genome evolution and is not quantitatively dominant, whereas non-adaptive processes are much more prominent than previously suspected. Major contributions of horizontal gene transfer and diverse selfish genetic elements to genome evolution undermine the Tree of Life concept. An adequate depiction of evolution requires the more complex concept of a network or 'forest' of life. There is no consistent tendency of evolution towards increased genomic complexity, and when complexity increases, this appears to be a non-adaptive consequence of evolution under weak purifying selection rather than an adaptation. Several universals of genome evolution were discovered including the invariant distributions of evolutionary rates among orthologous genes from diverse genomes and of paralogous gene family sizes, and the negative correlation between gene expression level and sequence evolution rate. Simple, non-adaptive models of evolution explain some of these universals, suggesting that a new synthesis of evolutionary biology might become feasible in a not so remote future.

Figure 1.

Two views of life history to replace the Tree of Life. (A) The ‘TOL as a central trend’ model. The history of life is represented as a tree, with connecting lines between branches depicting HGT and shaded trapezoids depicting phases of compressed cladogenesis (276). The origin of eukaryotes is depicted according to the archezoan hypothesis whereby the host of the mitochondrial endosymbiont was a proto-eukaryotes (archezoan). A cellular Last Universal Common Ancestor (LUCA) is envisaged. (B) The ‘Big Bang’ model. The history of life is represented as a succession of tree-like phases accompanied by HGT and non-tree-like, Big Bang phases. Connecting lines between tree branches depict HGT and colored trapezoids depict Big Bang phases (151). The origin of eukaryotes is depicted according to the symbiogenesis model whereby the host of the mitochondrial endosymbiont was an archaeon. A pre-cellular Last Universal Common Ancestral State (LUCAS) is envisaged. Ar, archaeon (host of the mitochondrion in b), AZ, archezoan (host of the mitochondrion in a), BB, Big Bang, C, chloroplast, CC, compressed cladogenesis, M, mitochondrion.

Figure 2.

Dependence between genome size and gene density for large viruses and diverse cellular life forms. The plot is semi-logarithmic. Points corresponding to selected organisms are marked: Af, Archaeoglobus fulgidus (archaeon), Cp, Cryptosporidium parvum (unicellular eukaryote, alveolate), Hs, Homo sapiens, Os, Oryza sativa (rice), Mg, Mycoplasma genitalium (obligate parasitic bacterium), Mv, mimivirus, Tv, Trichomonas vaginalis (unicellular eukaryote, excavate).

Figure 3.

Evolutionary genomics and systems biology. (A) Evolutionary and phenomic variables. The phenomic variables are viewed as mutually dependent and affecting evolutionary variables (left). Positive correlations are shown by red arrows and negative correlations are shown by blue arrows. (B) The concept of gene status. The red points schematically denote data scatter.

Figure 4.

Universals of evolution. (A) Distributions of evolutionary rates between orthologs in pairs of closely related genomes of bacteria, archaea and eukaryotes. The evolutionary distances between aligned nucleotide sequences of orthologous genes were calculated using the Jukes–Cantor correction and standardized so that the mean of each distribution equaled to 0, and the standard deviation equaled to 1. The plot is semi-logarithmic. Metma—Methanococcus maripaludis C5 versus M. maripaludis C7 (Euryarchaeota); Bursp—Burkholderia cenocepacia MC0-3 versus B. vietnamiensis G4 (Proteobacteria); Salsp—Salinispora arenicola CNS-205 versus S. tropica CNB-440 (Actinobacteria). All sequences were from the NCBI RefSeq database. The probability density curves were obtained by Gaussian-kernel smoothing of the individual data points. (B) Fit of empirical paralogous gene family size distributions to the balanced birth-and-death model. The results are shown for yeast Saccharomyces cerevisiae (Sc, left) and humans (Hs, right). Upper panels, binned distributions of paralogous family sizes; middle panels, paralogous family size distributions in double logarithmic coordinates; bottom panels, cumulative distribution function of paralogous family sizes. The lines show the predictions the balanced birth-and-death model. The figure is from (204).