Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Barcelona, Catalonia, Spain; Departament de Genètica, Microbiologia i Estadística, Universitat de Barelona, Barcelona, Catalonia, Spain
Unité d'Ecologie, Systématique et Evolution, Université Paris-Sud/Paris-Saclay, AgroParisTech, Orsay, France
Stuart Donachie
Department of Microbiology, University of Hawai'i at Mānoa, Honolulu, United States; Advanced Studies in Genomics, Proteomics and Bioinformatics, University of Hawai'i at Mānoa, Honolulu, United States
Hiroshi Suga
Faculty of Life and Environmental Sciences, Prefectural University of Hiroshima, Hiroshima, Japan
Guy Leonard
Department of Biosciences, University of Exeter, Exeter, United Kingdom
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.
