The origin of Metazoa: a unicellular perspective

This article has been updated

Key Points

  • The origin of animal multicellularity is one of the major evolutionary transitions in the history of life.

  • The identification and phylogenetic classification of the closest unicellular relatives of animals initiated the study of this transition from a unicellular perspective.

  • Comparative genomics has revealed that many genes associated with animal multicellularity evolved in a unicellular context and has enabled the rich gene repertoire of the unicellular ancestor of animals to be reconstructed.

  • The presence of highly regulated temporal cell types in animal relatives suggests the existence of cell differentiation in the unicellular ancestor of animals.

  • Initial studies suggest important differences between the genome regulatory mechanisms of animals and those of their closest unicellular relatives.

  • These innovations in genome regulation would have been key to the spatial integration of pre-existing cell types at the onset of Metazoa.

Abstract

The first animals evolved from an unknown single-celled ancestor in the Precambrian period. Recently, the identification and characterization of the genomic and cellular traits of the protists most closely related to animals have shed light on the origin of animals. Comparisons of animals with these unicellular relatives allow us to reconstruct the first evolutionary steps towards animal multicellularity. Here, we review the results of these investigations and discuss their implications for understanding the earliest stages of animal evolution, including the origin of metazoan genes and genome function.

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Figure 1: The multiple origins of multicellularity.
Figure 2: Phylogenetic relationships of animals and unicellular Holozoa.
Figure 3: Comparative genomics of Holozoa.
Figure 4: Unicellular holozoan life cycles.
Figure 5: A model of the origin of multicellularity: a transition from temporal to spatiotemporal cell differentiation.

Change history

  • 10 May 2017

    In Figure 1a of the original version of this article, the Choanoflagellatea branch was missing a yellow-black split circle symbolizing that clonal multicellularity occurs in some Choanoflagellatea species. The symbol inadvertently dropped out prior to publication and has now been reinstated in the corrected article. The editors apologize for this error.

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Acknowledgements

The authors thank X. Grau-Bové and D. Lara-Astiaso for critical comments on the manuscript, and G. Torruella and A. de Mendoza for discussion and ideas. A.S.-P. is supported by a European Molecular Biology Organization Long-Term Fellowship (ALTF 841-2014). Research by B.M.D. is supported by an Australian Research Council grant. Research by I.R.-T. is supported by an Institució Catalana de Recerca i Estudis Avançats (ICREA) contract, a European Research Council Starting Grant (ERC-2007-StG-206883), a European Research Council Consolidator Grant (ERC-2012-Co -616960) grant, and a grant (BFU2014-57779-P) from Ministerio de Economía y Competitividad (MINECO); his latest research is co-funded by the European Regional Development Fund (fondos FEDER). I.R-T. also acknowledges financial support from Secretaria d'Universitats i Recerca del Departament d'Economia i Coneixement de la Generalitat de Catalunya (project 2014 SGR 619).

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Correspondence to Arnau Sebé-Pedrós or Iñaki Ruiz-Trillo.

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Glossary

Protist

An informal name that is given to eukaryotes (usually unicellular eukaryotes) that are not included in the fungal, animal or plant lineages. Protists do not form a monophyletic clade.

Bilaterian animals

A monophyletic group that is defined by bilateral symmetry of the body plan and three germ layers, and that comprises most animal phyla.

Choanocyte

A specialized filter-feeding cell type that is characteristic of sponges. The basic cell structure, with a central flagellum surrounded by a microvilli collar, to some extent resembles that of choanoflagellate cells.

Filopodia

Thin, actin-based cellular projections that are used in environmental sensing and cell motility.

Metabarcoding

Analysis of species or lineage diversity in pooled environmental samples by sequencing of a standardized, common region of DNA, usually the gene encoding the 18S ribosomal RNA.

Coenocyte

A multinucleated cell resulting from successive nuclear divisions (karyokinesis) without associated cytokinesis.

Orthologues

Genes in different species that are descended from a common ancestral gene through a speciation divergence event.

Effector gene

A gene that is related to structural and metabolic cellular functions (for example, enzymes or cytoskeletal proteins), as opposed to a regulatory gene.

Cis-regulatory element

A genomic segment that regulates the transcription of (usually neighbouring) genes on the same chromosome.

Chromatin looping

Physical folding of the chromatin nucleoprotein fibre. It is often associated with regulatory events that involve physical proximity between distal enhancer elements and gene promoters.

Microsyntenic

Describes small genomic regions in which the physical colocalization of loci is conserved between different species.

Chromatin states

Unique combinations of histone post-translational modifications and chromatin-associated proteins that define different biochemical activities of the genome.

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Sebé-Pedrós, A., Degnan, B. & Ruiz-Trillo, I. The origin of Metazoa: a unicellular perspective. Nat Rev Genet 18, 498–512 (2017). https://doi.org/10.1038/nrg.2017.21

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