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.
Highlights
The transition from a unicellular organism to the first multicellular animal, more than 600 million years ago (Budd and Jensen, 2017; dos Reis et al, 2015), marks one of the most radical evolutionary innovations within the eukaryotes
Abeoforma and Pirum have larger genome assemblies (101.9 and 84.4 Mb), but these are fragmented (L75 = 25,133 and 25,440 scaffolds) and incomplete (11.9% and 17.0% of BUSCO). These lower contiguities are reflected in their partial gene predictions (Figure 1A, Figure 1—figure supplement 1), which hindered the detection of BUSCO orthologs
The ancestral reconstruction of individual protein domain evolution showed that losses dominate in most nodes, both extant and ancestral – with the exception of animals and their ancestors (Figure 7—figure supplement 1) (Zmasek and Godzik, 2011). In this scenario of pervasive domain rearrangements, we identified a consistent pattern of creation of protein domain architectures in the lineage leading to Metazoa – the line of descent from the opisthokont to the bilaterian last common ancestor (LCA) (Figure 7A–B)
Summary
The transition from a unicellular organism to the first multicellular animal, more than 600 million years ago (Budd and Jensen, 2017; dos Reis et al, 2015), marks one of the most radical evolutionary innovations within the eukaryotes. Key advances in the study of animal origins have been made by comparing the genomes of early branching metazoa, such as cnidarians, ctenophores or sponges (Putnam et al, 2007; Srivastava et al, 2010a; Moroz et al, 2014; Srivastava et al, 2008; Fortunato et al, 2014), with their closest unicellular relatives in the Holozoa clade, such as the choanoflagellates Monosiga brevicollis and Salpingoeca rosetta (King et al, 2008; Fairclough et al, 2013), and the filasterean Capsaspora owczarzaki (Suga et al, 2013) (Figure 1). By focusing on the transition, it is possible to determine which genomic innovations occurred at the origin of metazoa, and whether it required the invention of novel genes or structural features.
Sign-in/Register to view highlights & summary 
Published Version (
Free)
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
