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Gene gain and loss across the metazoan tree of life

Abstract

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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Fig. 1: Gene gain, loss and duplication ratios show a similar pattern across animal phyla.
Fig. 2: Gene gain and duplication ratios are high at deeper nodes, and gene loss at shallower ones.
Fig. 3: Genes related to the neural system are among the most highly duplicated.
Fig. 4: The core gene repertoire of metazoans includes genes from a plethora of KEGG pathways that have undergone different degrees of duplication.
Fig. 5: Pairwise gene loss is pervasive across phyla.

Data availability

All data, code and supplementary information are available in the manuscript. The supplementary materials are deposited in the Harvard dataverse repository https://doi.org/10.7910/DVN/ZKDAE2. The accession numbers for all taxa included in each analysis are indicated in Supplementary Mat. 1. All phylomes can be accessed at PhylomeDB 4.0 under the phylome numbers 431, 462, 747, 778, 782, 812, 819, 824, 875, 888, 937, 950 and 953 (that is, for example, http://www.phylomedb.org/phylome_431 for direct access).

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Acknowledgements

We are grateful to M. Marcet-Houben and I. Julca for multiple discussions that contributed to greatly improve this study. 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.

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R.F. and T.G. developed the overall conceptual approach and analysis. R.F. compiled and analysed the data. R.F. and T.G. wrote the manuscript. T.G. supervised the study.

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Correspondence to Toni Gabaldón.

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Fernández, R., Gabaldón, T. Gene gain and loss across the metazoan tree of life. Nat Ecol Evol 4, 524–533 (2020). https://doi.org/10.1038/s41559-019-1069-x

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