Limits...
Punctuated emergences of genetic and phenotypic innovations in eumetazoan, bilaterian, euteleostome, and hominidae ancestors.

Wenger Y, Galliot B - Genome Biol Evol (2013)

Bottom Line: Interestingly, groups of proteins that act together in their modern human functions often originated concomitantly, although the corresponding human phenotypes frequently emerged later.For example, the three cnidarians Acropora, Nematostella, and Hydra express a highly similar protein inventory, and their protein innovations can be affiliated either to traits shared by all eumetazoans (gut differentiation, neurogenesis); or to bilaterian traits present in only some cnidarians (eyes, striated muscle); or to traits not identified yet in this phylum (mesodermal layer, endocrine glands).The variable correspondence between phenotypes predicted from protein enrichments and observed phenotypes suggests that a parallel mechanism repeatedly produce similar phenotypes, thanks to novel regulatory events that independently tie preexisting conserved genetic modules.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetics and Evolution, Institute of Genetics and Genomics in Geneva (iGE3), University of Geneva, Geneva, Switzerland.

ABSTRACT
Phenotypic traits derive from the selective recruitment of genetic materials over macroevolutionary times, and protein-coding genes constitute an essential component of these materials. We took advantage of the recent production of genomic scale data from sponges and cnidarians, sister groups from eumetazoans and bilaterians, respectively, to date the emergence of human proteins and to infer the timing of acquisition of novel traits through metazoan evolution. Comparing the proteomes of 23 eukaryotes, we find that 33% human proteins have an ortholog in nonmetazoan species. This premetazoan proteome associates with 43% of all annotated human biological processes. Subsequently, four major waves of innovations can be inferred in the last common ancestors of eumetazoans, bilaterians, euteleostomi (bony vertebrates), and hominidae, largely specific to each epoch, whereas early branching deuterostome and chordate phyla show very few innovations. Interestingly, groups of proteins that act together in their modern human functions often originated concomitantly, although the corresponding human phenotypes frequently emerged later. For example, the three cnidarians Acropora, Nematostella, and Hydra express a highly similar protein inventory, and their protein innovations can be affiliated either to traits shared by all eumetazoans (gut differentiation, neurogenesis); or to bilaterian traits present in only some cnidarians (eyes, striated muscle); or to traits not identified yet in this phylum (mesodermal layer, endocrine glands). The variable correspondence between phenotypes predicted from protein enrichments and observed phenotypes suggests that a parallel mechanism repeatedly produce similar phenotypes, thanks to novel regulatory events that independently tie preexisting conserved genetic modules.

Show MeSH

Related in: MedlinePlus

Timing of emergences of human orthologs and related Biological Processes (huBPs) in metazoan evolution. (A) Parallel bursts in human orthologs’ gains (green bars) and emergence of huBPs (gray bars, corrected P value ≤10−3). (B) Gains (green bars) and losses (blue bars) in human orthologs obtained by testing the complete human proteome against the proteomes of species belonging to phyla branching at various steps of metazoan evolution. (C) Rates of emergence of human orthologs across metazoan evolution expressed as numbers of novel ortholog proteins (y axis) detected by million year (Myr). Rates were deduced from the protein gains shown in A and B over the time periods separating the LCAs of two clades as indicated by inverted arrows at the bottom. References for each time period are given in the legend of figure 2.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3814200&req=5

evt142-F4: Timing of emergences of human orthologs and related Biological Processes (huBPs) in metazoan evolution. (A) Parallel bursts in human orthologs’ gains (green bars) and emergence of huBPs (gray bars, corrected P value ≤10−3). (B) Gains (green bars) and losses (blue bars) in human orthologs obtained by testing the complete human proteome against the proteomes of species belonging to phyla branching at various steps of metazoan evolution. (C) Rates of emergence of human orthologs across metazoan evolution expressed as numbers of novel ortholog proteins (y axis) detected by million year (Myr). Rates were deduced from the protein gains shown in A and B over the time periods separating the LCAs of two clades as indicated by inverted arrows at the bottom. References for each time period are given in the legend of figure 2.

Mentions: Next, we focused our interest on the innovations that took place in metazoan, eumetazoan, deuterostome, chordate, vertebrate, and primate LCAs. To characterize gains and losses of proteins over each evolutionary period, we mapped the 20,231 human proteins to the proteomes of 21 holozoan species, as shown in figure 2, and inferred that protein gain had taken place in the LCA of a given clade when i) species derived from this LCA possess a human ortholog and ii) no occurrence is observed in species branching from more ancient ancestors (figs. 4A and 4B). As S. cerevisiae underwent severe genome reduction, a complementary analysis was performed on 25 holozoan species that include four additional fungal species. This analysis yields highly similar results (supplementary fig. S3B, Supplementary Material online). We also inferred protein loss within a given clade when orthologs to human proteins were not found in species of this clade but were present in sister groups or in phyla having diverged earlier (fig. 4B). In this study, losses that affect branches or ancestors with human descendants cannot be traced.Fig. 4.—


Punctuated emergences of genetic and phenotypic innovations in eumetazoan, bilaterian, euteleostome, and hominidae ancestors.

Wenger Y, Galliot B - Genome Biol Evol (2013)

Timing of emergences of human orthologs and related Biological Processes (huBPs) in metazoan evolution. (A) Parallel bursts in human orthologs’ gains (green bars) and emergence of huBPs (gray bars, corrected P value ≤10−3). (B) Gains (green bars) and losses (blue bars) in human orthologs obtained by testing the complete human proteome against the proteomes of species belonging to phyla branching at various steps of metazoan evolution. (C) Rates of emergence of human orthologs across metazoan evolution expressed as numbers of novel ortholog proteins (y axis) detected by million year (Myr). Rates were deduced from the protein gains shown in A and B over the time periods separating the LCAs of two clades as indicated by inverted arrows at the bottom. References for each time period are given in the legend of figure 2.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3814200&req=5

evt142-F4: Timing of emergences of human orthologs and related Biological Processes (huBPs) in metazoan evolution. (A) Parallel bursts in human orthologs’ gains (green bars) and emergence of huBPs (gray bars, corrected P value ≤10−3). (B) Gains (green bars) and losses (blue bars) in human orthologs obtained by testing the complete human proteome against the proteomes of species belonging to phyla branching at various steps of metazoan evolution. (C) Rates of emergence of human orthologs across metazoan evolution expressed as numbers of novel ortholog proteins (y axis) detected by million year (Myr). Rates were deduced from the protein gains shown in A and B over the time periods separating the LCAs of two clades as indicated by inverted arrows at the bottom. References for each time period are given in the legend of figure 2.
Mentions: Next, we focused our interest on the innovations that took place in metazoan, eumetazoan, deuterostome, chordate, vertebrate, and primate LCAs. To characterize gains and losses of proteins over each evolutionary period, we mapped the 20,231 human proteins to the proteomes of 21 holozoan species, as shown in figure 2, and inferred that protein gain had taken place in the LCA of a given clade when i) species derived from this LCA possess a human ortholog and ii) no occurrence is observed in species branching from more ancient ancestors (figs. 4A and 4B). As S. cerevisiae underwent severe genome reduction, a complementary analysis was performed on 25 holozoan species that include four additional fungal species. This analysis yields highly similar results (supplementary fig. S3B, Supplementary Material online). We also inferred protein loss within a given clade when orthologs to human proteins were not found in species of this clade but were present in sister groups or in phyla having diverged earlier (fig. 4B). In this study, losses that affect branches or ancestors with human descendants cannot be traced.Fig. 4.—

Bottom Line: Interestingly, groups of proteins that act together in their modern human functions often originated concomitantly, although the corresponding human phenotypes frequently emerged later.For example, the three cnidarians Acropora, Nematostella, and Hydra express a highly similar protein inventory, and their protein innovations can be affiliated either to traits shared by all eumetazoans (gut differentiation, neurogenesis); or to bilaterian traits present in only some cnidarians (eyes, striated muscle); or to traits not identified yet in this phylum (mesodermal layer, endocrine glands).The variable correspondence between phenotypes predicted from protein enrichments and observed phenotypes suggests that a parallel mechanism repeatedly produce similar phenotypes, thanks to novel regulatory events that independently tie preexisting conserved genetic modules.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetics and Evolution, Institute of Genetics and Genomics in Geneva (iGE3), University of Geneva, Geneva, Switzerland.

ABSTRACT
Phenotypic traits derive from the selective recruitment of genetic materials over macroevolutionary times, and protein-coding genes constitute an essential component of these materials. We took advantage of the recent production of genomic scale data from sponges and cnidarians, sister groups from eumetazoans and bilaterians, respectively, to date the emergence of human proteins and to infer the timing of acquisition of novel traits through metazoan evolution. Comparing the proteomes of 23 eukaryotes, we find that 33% human proteins have an ortholog in nonmetazoan species. This premetazoan proteome associates with 43% of all annotated human biological processes. Subsequently, four major waves of innovations can be inferred in the last common ancestors of eumetazoans, bilaterians, euteleostomi (bony vertebrates), and hominidae, largely specific to each epoch, whereas early branching deuterostome and chordate phyla show very few innovations. Interestingly, groups of proteins that act together in their modern human functions often originated concomitantly, although the corresponding human phenotypes frequently emerged later. For example, the three cnidarians Acropora, Nematostella, and Hydra express a highly similar protein inventory, and their protein innovations can be affiliated either to traits shared by all eumetazoans (gut differentiation, neurogenesis); or to bilaterian traits present in only some cnidarians (eyes, striated muscle); or to traits not identified yet in this phylum (mesodermal layer, endocrine glands). The variable correspondence between phenotypes predicted from protein enrichments and observed phenotypes suggests that a parallel mechanism repeatedly produce similar phenotypes, thanks to novel regulatory events that independently tie preexisting conserved genetic modules.

Show MeSH
Related in: MedlinePlus