4.5 Article

Gene gain and loss across the metazoan tree of life

Journal

NATURE ECOLOGY & EVOLUTION
Volume 4, Issue 4, Pages 524-533

Publisher

NATURE PORTFOLIO
DOI: 10.1038/s41559-019-1069-x

Keywords

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Funding

  1. Juan de la Cierva-Incorporacion Fellowship (Government of Spain)
  2. Marie Sklodowska-Curie Fellowship [747607]
  3. Spanish Ministry of Economy, Industry, and Competitiveness (MEIC) [SEV-2012-0208, BFU2015-67107]
  4. European Regional Development Fund (ERDF)
  5. CERCA Programme/Generalitat de Catalunya
  6. Catalan Research Agency (AGAUR) [SGR857]
  7. European Union's Horizon 2020 research and innovation programme [ERC-2016-724173]
  8. Marie Sklodowska-Curie grant [H2020-MSCA-ITN-2014-642095]
  9. Marie Curie Actions (MSCA) [747607] Funding Source: Marie Curie Actions (MSCA)

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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. Phylogenomic analysis including representatives of all metazoan phyla shows gene duplication followed by differential gene loss throughout the animal tree of life.

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