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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.

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Model of a regulatory-based parallel mechanism for the emergence of innovations as deduced from the comparison of predicted and observed phenotypes in cnidarians. (A) Innovations in cnidarians, i.e., absent in nonmetazoans or in earlier branching metazoans as porifers, were sorted in four categories of phenotypes: Constrained (dark green) when present in all cnidarians and maintained in bilaterians; labile (light purple) when expressed in some but not all cnidarian species, and largely expressed in bilaterians including vertebrates; latent (light blue) when observed in bilaterians but not in cnidarians; cnidarian-specific (orange) when restricted to cnidarians. Some eumetazoan innovations evolved differently in cnidarians and bilaterians as the sensory motoneurons and the myoepithelial cells that remained multifunctional in cnidarians (light green) but differentiated in more specialized cell types in bilaterians (Arendt 2008). (B) Cnidarian proteomes contain similar numbers of human orthologs (dots), labelled here according to their origin as premetazoan (green), metazoan (blue), eumetazoan (red), or taxon-restricted (yellow). These proteins can participate in genetic modules (GM) that can give rise to constrained phenotypes (gray backgrounds) when regulations between the different proteins are tightly linked, with a limited potential for innovation (upper panel). When forming GM with loose links between preexisting tight GM (middle panel), these protein networks can give rise to labile phenotypes (purple background), prone to innovation through parallel evolution. When not included in predicted GM, the corresponding phenotypes are latent (lowest panel). However, these proteins likely form also taxon-restricted GM that support taxon-specific phenotype (orange background) as anatomical and life cycle differences (Foret et al. 2010; Wenger and Galliot 2013).
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evt142-F8: Model of a regulatory-based parallel mechanism for the emergence of innovations as deduced from the comparison of predicted and observed phenotypes in cnidarians. (A) Innovations in cnidarians, i.e., absent in nonmetazoans or in earlier branching metazoans as porifers, were sorted in four categories of phenotypes: Constrained (dark green) when present in all cnidarians and maintained in bilaterians; labile (light purple) when expressed in some but not all cnidarian species, and largely expressed in bilaterians including vertebrates; latent (light blue) when observed in bilaterians but not in cnidarians; cnidarian-specific (orange) when restricted to cnidarians. Some eumetazoan innovations evolved differently in cnidarians and bilaterians as the sensory motoneurons and the myoepithelial cells that remained multifunctional in cnidarians (light green) but differentiated in more specialized cell types in bilaterians (Arendt 2008). (B) Cnidarian proteomes contain similar numbers of human orthologs (dots), labelled here according to their origin as premetazoan (green), metazoan (blue), eumetazoan (red), or taxon-restricted (yellow). These proteins can participate in genetic modules (GM) that can give rise to constrained phenotypes (gray backgrounds) when regulations between the different proteins are tightly linked, with a limited potential for innovation (upper panel). When forming GM with loose links between preexisting tight GM (middle panel), these protein networks can give rise to labile phenotypes (purple background), prone to innovation through parallel evolution. When not included in predicted GM, the corresponding phenotypes are latent (lowest panel). However, these proteins likely form also taxon-restricted GM that support taxon-specific phenotype (orange background) as anatomical and life cycle differences (Foret et al. 2010; Wenger and Galliot 2013).

Mentions: Next we analyzed whether the predicted eumetazoan innovations deduced from protein-enriched huBPs correspond to actual phenotypes in cnidarians. We found that the predicted innovations correspond to three distinct types of phenotypes: constrained when observed in all cnidarians and maintained in all bilaterians such as neurogenesis or gut development; labile when observed in some but not all cnidarian species, and frequently expressed in bilaterians such as eye development, mesodermal derivatives, and biomineralization; latent when not observed in cnidarians but widely conserved in bilaterians, for example, proteins directing central nervous system, skeletal, or endocrine development (fig. 8). Hence, protein-based predicted innovations in cnidarians are actually expressed with high variability.


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

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

Model of a regulatory-based parallel mechanism for the emergence of innovations as deduced from the comparison of predicted and observed phenotypes in cnidarians. (A) Innovations in cnidarians, i.e., absent in nonmetazoans or in earlier branching metazoans as porifers, were sorted in four categories of phenotypes: Constrained (dark green) when present in all cnidarians and maintained in bilaterians; labile (light purple) when expressed in some but not all cnidarian species, and largely expressed in bilaterians including vertebrates; latent (light blue) when observed in bilaterians but not in cnidarians; cnidarian-specific (orange) when restricted to cnidarians. Some eumetazoan innovations evolved differently in cnidarians and bilaterians as the sensory motoneurons and the myoepithelial cells that remained multifunctional in cnidarians (light green) but differentiated in more specialized cell types in bilaterians (Arendt 2008). (B) Cnidarian proteomes contain similar numbers of human orthologs (dots), labelled here according to their origin as premetazoan (green), metazoan (blue), eumetazoan (red), or taxon-restricted (yellow). These proteins can participate in genetic modules (GM) that can give rise to constrained phenotypes (gray backgrounds) when regulations between the different proteins are tightly linked, with a limited potential for innovation (upper panel). When forming GM with loose links between preexisting tight GM (middle panel), these protein networks can give rise to labile phenotypes (purple background), prone to innovation through parallel evolution. When not included in predicted GM, the corresponding phenotypes are latent (lowest panel). However, these proteins likely form also taxon-restricted GM that support taxon-specific phenotype (orange background) as anatomical and life cycle differences (Foret et al. 2010; Wenger and Galliot 2013).
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Related In: Results  -  Collection

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

evt142-F8: Model of a regulatory-based parallel mechanism for the emergence of innovations as deduced from the comparison of predicted and observed phenotypes in cnidarians. (A) Innovations in cnidarians, i.e., absent in nonmetazoans or in earlier branching metazoans as porifers, were sorted in four categories of phenotypes: Constrained (dark green) when present in all cnidarians and maintained in bilaterians; labile (light purple) when expressed in some but not all cnidarian species, and largely expressed in bilaterians including vertebrates; latent (light blue) when observed in bilaterians but not in cnidarians; cnidarian-specific (orange) when restricted to cnidarians. Some eumetazoan innovations evolved differently in cnidarians and bilaterians as the sensory motoneurons and the myoepithelial cells that remained multifunctional in cnidarians (light green) but differentiated in more specialized cell types in bilaterians (Arendt 2008). (B) Cnidarian proteomes contain similar numbers of human orthologs (dots), labelled here according to their origin as premetazoan (green), metazoan (blue), eumetazoan (red), or taxon-restricted (yellow). These proteins can participate in genetic modules (GM) that can give rise to constrained phenotypes (gray backgrounds) when regulations between the different proteins are tightly linked, with a limited potential for innovation (upper panel). When forming GM with loose links between preexisting tight GM (middle panel), these protein networks can give rise to labile phenotypes (purple background), prone to innovation through parallel evolution. When not included in predicted GM, the corresponding phenotypes are latent (lowest panel). However, these proteins likely form also taxon-restricted GM that support taxon-specific phenotype (orange background) as anatomical and life cycle differences (Foret et al. 2010; Wenger and Galliot 2013).
Mentions: Next we analyzed whether the predicted eumetazoan innovations deduced from protein-enriched huBPs correspond to actual phenotypes in cnidarians. We found that the predicted innovations correspond to three distinct types of phenotypes: constrained when observed in all cnidarians and maintained in all bilaterians such as neurogenesis or gut development; labile when observed in some but not all cnidarian species, and frequently expressed in bilaterians such as eye development, mesodermal derivatives, and biomineralization; latent when not observed in cnidarians but widely conserved in bilaterians, for example, proteins directing central nervous system, skeletal, or endocrine development (fig. 8). Hence, protein-based predicted innovations in cnidarians are actually expressed with high variability.

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