Gene gain and loss across the metazoan tree of life

Although recent research has revealed high genomic complexity in the earliest-splitting animals and their ancestors, the macroevolutionary trends orchestrating gene repertoire evolution throughout the animal phyla remain poorly understood. We used a phylogenomic approach to interrogate genome evolution across all animal phyla. Our analysis uncovered a bimodal distribution of recruitment of orthologous genes, with most genes gained very ‘early’ (that is, at deep nodes) or very ‘late’, representing lineage-specific acquisitions. The emergence of animals was characterized by high values of gene birth and duplications. Deuterostomes, ecdysozoans and Xenacoelomorpha were characterized by no gene gain but rampant differential gene loss. Genes considered as animal hallmarks, such as Notch/Delta, were convergently duplicated in all phyla and at different evolutionary depths. Genes duplicated in all nodes from Metazoa to phylum-specific levels were enriched in functions related to the neural system, suggesting that this system has been continuously and independently reshaped throughout evolution across animals. Our results indicate that animal genomes evolved by unparalleled gene duplication followed by differential gene loss, and provide an atlas of gene repertoire evolution throughout the animal tree of life to navigate how, when and how often each gene in each genome was gained, duplicated or lost.

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Main Authors: Fernández, Rosa, Gabaldón, Toni
Other Authors: European Commission
Format: artículo biblioteca
Language:English
Published: Society of Africanist Archaeologists 2020-01-28
Online Access:http://hdl.handle.net/10261/218754
http://dx.doi.org/10.13039/501100002809
http://dx.doi.org/10.13039/501100003030
http://dx.doi.org/10.13039/501100000780
http://dx.doi.org/10.13039/501100000781
http://dx.doi.org/10.13039/501100003329
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spelling dig-ibe-es-10261-2187542021-12-27T16:34:19Z Gene gain and loss across the metazoan tree of life Fernández, Rosa Gabaldón, Toni European Commission Ministerio de Economía y Competitividad (España) Generalitat de Catalunya Agència de Gestió d'Ajuts Universitaris i de Recerca European Research Council Although recent research has revealed high genomic complexity in the earliest-splitting animals and their ancestors, the macroevolutionary trends orchestrating gene repertoire evolution throughout the animal phyla remain poorly understood. We used a phylogenomic approach to interrogate genome evolution across all animal phyla. Our analysis uncovered a bimodal distribution of recruitment of orthologous genes, with most genes gained very ‘early’ (that is, at deep nodes) or very ‘late’, representing lineage-specific acquisitions. The emergence of animals was characterized by high values of gene birth and duplications. Deuterostomes, ecdysozoans and Xenacoelomorpha were characterized by no gene gain but rampant differential gene loss. Genes considered as animal hallmarks, such as Notch/Delta, were convergently duplicated in all phyla and at different evolutionary depths. Genes duplicated in all nodes from Metazoa to phylum-specific levels were enriched in functions related to the neural system, suggesting that this system has been continuously and independently reshaped throughout evolution across animals. Our results indicate that animal genomes evolved by unparalleled gene duplication followed by differential gene loss, and provide an atlas of gene repertoire evolution throughout the animal tree of life to navigate how, when and how often each gene in each genome was gained, duplicated or lost. R.F. was funded by a Juan de la Cierva-Incorporación Fellowship (Government of Spain) and a Marie Skłodowska-Curie Fellowship (747607). T.G. group receives funding from the Spanish Ministry of Economy, Industry, and Competitiveness (MEIC) grants ‘Centro de Excelencia Severo Ochoa 2013-2017’ SEV-2012-0208 and BFU2015-67107 co-funded by the European Regional Development Fund (ERDF); from the CERCA Programme/Generalitat de Catalunya; from the Catalan Research Agency (AGAUR) SGR857, and a grant from the European Union’s Horizon 2020 research and innovation programme under the grant agreement ERC-2016-724173 the Marie Skłodowska-Curie grant agreement no. H2020-MSCA-ITN-2014-642095. Peer reviewed 2020-08-27T11:14:12Z 2020-08-27T11:14:12Z 2020-01-28 artículo http://purl.org/coar/resource_type/c_6501 Nature Ecology & Evolution 4: 524-533 (2020) http://hdl.handle.net/10261/218754 10.1038/s41559-019-1069-x 2397-334X http://dx.doi.org/10.13039/501100002809 http://dx.doi.org/10.13039/501100003030 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100000781 http://dx.doi.org/10.13039/501100003329 31988444 en #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/EC/H2020/747607 info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BFU2015-67107-P info:eu-repo/grantAgreement/EC/H2020/724173 info:eu-repo/grantAgreement/EC/H2020/642095 https://doi.org/10.1038/s41559-019-1069-x Sí none Society of Africanist Archaeologists
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description Although recent research has revealed high genomic complexity in the earliest-splitting animals and their ancestors, the macroevolutionary trends orchestrating gene repertoire evolution throughout the animal phyla remain poorly understood. We used a phylogenomic approach to interrogate genome evolution across all animal phyla. Our analysis uncovered a bimodal distribution of recruitment of orthologous genes, with most genes gained very ‘early’ (that is, at deep nodes) or very ‘late’, representing lineage-specific acquisitions. The emergence of animals was characterized by high values of gene birth and duplications. Deuterostomes, ecdysozoans and Xenacoelomorpha were characterized by no gene gain but rampant differential gene loss. Genes considered as animal hallmarks, such as Notch/Delta, were convergently duplicated in all phyla and at different evolutionary depths. Genes duplicated in all nodes from Metazoa to phylum-specific levels were enriched in functions related to the neural system, suggesting that this system has been continuously and independently reshaped throughout evolution across animals. Our results indicate that animal genomes evolved by unparalleled gene duplication followed by differential gene loss, and provide an atlas of gene repertoire evolution throughout the animal tree of life to navigate how, when and how often each gene in each genome was gained, duplicated or lost.
author2 European Commission
author_facet European Commission
Fernández, Rosa
Gabaldón, Toni
format artículo
author Fernández, Rosa
Gabaldón, Toni
spellingShingle Fernández, Rosa
Gabaldón, Toni
Gene gain and loss across the metazoan tree of life
author_sort Fernández, Rosa
title Gene gain and loss across the metazoan tree of life
title_short Gene gain and loss across the metazoan tree of life
title_full Gene gain and loss across the metazoan tree of life
title_fullStr Gene gain and loss across the metazoan tree of life
title_full_unstemmed Gene gain and loss across the metazoan tree of life
title_sort gene gain and loss across the metazoan tree of life
publisher Society of Africanist Archaeologists
publishDate 2020-01-28
url http://hdl.handle.net/10261/218754
http://dx.doi.org/10.13039/501100002809
http://dx.doi.org/10.13039/501100003030
http://dx.doi.org/10.13039/501100000780
http://dx.doi.org/10.13039/501100000781
http://dx.doi.org/10.13039/501100003329
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