Comparative analysis of complete genomes reveals gene loss, acquisition and acceleration of evolutionary rates in Metazoa, suggests a prevalence of evolution via gene acquisition and indicates that the evolutionary rates in animals tend to be conserved

Abstract

In this study we systematically examined the differences between the proteomes of Metazoa and other eukaryotes. Metazoans (Homo sapiens, Ceanorhabditis elegans and Drosophila melanogaster) were compared with a plant (Arabidopsis thaliana), fungi (Saccharomyces cerevisiae and Schizosaccaromyces pombe) and Encephalitozoan cuniculi. We identified 159 gene families that were probably lost in the Metazoan branch and 1263 orthologous families that were specific to Metazoa and were likely to have originated in their last common ancestor (LCA). We analyzed the evolutionary rates of pan-eukaryotic protein families and identified those with higher rates in animals. The acceleration was shown to occur in: (i) the LCA of Metazoa or (ii) independently in the Metazoan phyla. A high proportion of the accelerated Metazoan protein families was found to participate in translation and ribosome biogenesis, particularly mitochondrial. By functional analysis we show that no metabolic pathway in animals evolved faster than in other organisms. We conclude that evolution in the LCA of Metazoa was extensive and proceeded largely by gene duplication and/or invention rather than by modification of extant proteins. Finally, we show that the rate of evolution of a gene family in animals has a clear, but not absolute, tendency to be conserved.

Figure 1

Functional categories of genes lost in Metazoa. Gene loss specific to Metazoa is analyzed for distribution among functional categories. The fraction of lost genes belonging to each category (red bars) is compared with the fraction of genes among all studied gene families belonging to the same functional category (blue bars). Categories for which there is a statistically significant (P < 0.05) difference within a functional category are shown. The significance value (P-value) is shown above the bars.

Figure 2

(A) Functional categories of Metazoa-specific genes. The fraction of Metazoa-specific genes belonging to each category (red bars) is compared with the fraction of genes among all studied gene families belonging to the same functional category (blue bars). Categories for which there is a statistically significant difference within a functional category are shown. The functional categories are abbreviated as follows, the significance value (P-value) is in parenthesis: T, Signal transduction mechanisms (1.64 × 10⁻²¹); N, Cell motility (0.0293); K,Transcription (0.0160); Y, Nuclear structure (0.0266); E, Amino acid transport and metabolism (0.0026); V, Defense mechanisms (0.0454); Z, Cytoskeleton (0.0097); C, Energy production and conversion (0.0009); L, Replication, recombination and repair (2.47 × 10⁻⁹); A, RNA processing and modification (8.27 × 10⁻⁷); O, Posttranslational modification, protein turnover, chaperones (8.02 × 10⁻⁷); J, Translation, ribosomal structure and biogenesis (2.08 × 10⁻¹¹); W, Extracellular structures (0.000002); P, Inorganic ion transport and metabolism (0.0420); B, Chromatin structure and dynamics (0.0020); H, Coenzyme transport and metabolism (0.00009); D, Cell cycle control, cell division, chromosome partitioning (0.0075); G, Carbohydrate transport and metabolism (0.0037); U, Intracellular trafficking, secretion and vesicular transport (0.0217). (B) The origin of Metazoa-specific proteins. Metazoa-specific proteins without direct orthologs in other taxa are analyzed for detectable homologues in the following groups: META, only in Metazoa; MET-BAC, in Metazoa and bacteria; META-BAC-ARCH, in Metazoa, bacteria and Archaea; EUK-ARCH, in different eukaryotes and Archaea; EUK, in different eukaryotes only; EUK-BAC, in different eukaryotes and bacteria; EUK-BAC-ARCH, in different eukaryotes, bacteria and Archaea; EUK-ARCH, in different eukaryotes and Archaea.

Figure 3

(A) Evolutionary rates in the LCAs of Metazoa and fungi. The protein substitution rates in the LCAs are reflected by the length of branches preceding the split into individual clades. (B) Function of genes with rapid evolutionary rates in the LCA of Metazoa. The fraction of Metazoa-specific genes belonging to each category (red bars) is compared with the fraction of genes among all studied gene families belonging to the same functional category (blue bars). Functional categories are abbreviated as follows: F, Nucleotide transport and metabolism; S, Function unknown; T, Signal transduction mechanisms; N, Cell motility; K, Transcription; Y, Nuclear structure; E, Amino acid transport and metabolism; V, Defense mechanisms; Z, Cytoskeleton; Q, Secondary metabolites biosynthesis, transport and catabolism; M, Cell wall/membrane/envelope biogenesis; C, Energy production and conversion; L, Replication, recombination and repair; A, RNA processing and modification; O, Posttranslational modification, protein turnover, chaperones; J, Translation, ribosomal structure and biogenesis; W, Extracellular structures; P, Inorganic ion transport and metabolism; B, Chromatin structure and dynamics; H, Coenzyme transport and metabolism; D, Cell cycle control, cell division, chromosome partitioning; I, Lipid transport and metabolism; R, General function prediction only; G, Carbohydrate transport and metabolism; U, Intracellular trafficking, secretion and vesicular transport.

Figure 4

(A) Evolutionary rates in the separate lineages of Metazoa, fungi and plants. The protein substitution rates in the lineages are reflected by the length of branches after the split into individual clades. (B) Function of genes with rapid evolutionary rates in separate Metazoan phyla. Categories for which there is a statistically significant difference within a functional category are shown. The functional categories are abbreviated as follows, the significance value (P-value) is listed here in parenthesis: E, Amino acid transport and metabolism (0.033); Z, Cytoskeleton (0.023); L, Replication, recombination and repair (0.0037); O, Posttranslational modification, protein turnover, chaperones (0.0154); J, Translation, ribosomal structure and biogenesis (0.0000015); U, Intracellular trafficking, secretion and vesicular transport (0.0266).