Dynamics of genomic innovation in the unicellular ancestry of animals
- Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Spain
- Université Paris-Sud/Paris-Saclay, France
- University of Hawai'i at Mānoa, United States
- Prefectural University of Hiroshima, Japan
- Living Systems Institute, United Kingdom
- University of Exeter, United Kingdom
Abstract
Which genomic innovations underpinned the origin of multicellular animals is still an open debate. Here, we investigate this question by reconstructing the genome architecture and gene family diversity of ancestral premetazoans, aiming to date the emergence of animal-like traits. Our comparative analysis involves genomes from animals and their closest unicellular relatives (the Holozoa), including four new genomes: three Ichthyosporea and Corallochytrium limacisporum. Here we show that the earliest animals were shaped by dynamic changes in genome architecture before the emergence of multicellularity: an early burst of gene diversity in the ancestor of Holozoa, enriched in transcription factors and cell adhesion machinery, was followed by multiple and differently-timed episodes of synteny disruption, intron gain and genome expansions. Thus, the foundations of animal genome architecture were laid before the origin of complex multicellularity – highlighting the necessity of a unicellular perspective to understand early animal evolution.
Data availability
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Transcriptome sequencing data from Abeoforma and ChromosphaeraBioProject accession PRJNA360056.
Article and author information
Author details
Funding
Ministerio de Economía y Competitividad (BFU2014-57779-P)
- Iñaki Ruiz-Trillo
European Commission (ERC-2012-Co -616960)
- Iñaki Ruiz-Trillo
Ministerio de Economía y Competitividad (BFU-2011-23434)
- Iñaki Ruiz-Trillo
Generalitat de Catalunya (2014 SGR 619)
- Iñaki Ruiz-Trillo
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Diethard Tautz, Max-Planck Institute for Evolutionary Biology, Germany
Version history
- Received: February 21, 2017
- Accepted: July 11, 2017
- Accepted Manuscript published: July 20, 2017 (version 1)
- Version of Record published: August 17, 2017 (version 2)
- Version of Record updated: March 1, 2018 (version 3)
Copyright
© 2017, Grau-Bové et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Dynamics of genomic innovation in the unicellular ancestry of animals
eLife 6:e26036.
https://doi.org/10.7554/eLife.26036
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