The origin of Metazoa: a unicellular perspective

• Published in: Nature reviews. Genetics Vol. 18; no. 8; pp. 498 - 512
• Main Authors: Sebé-Pedrós, Arnau, Degnan, Bernard M., Ruiz-Trillo, Iñaki
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.08.2017; Nature Publishing Group
• Subjects: 631/181/2474; 631/181/2806; 631/181/757; 631/208/212/2304; 631/208/212/2306; 631/208/212/748; 631/80/79; Agriculture; Analysis; Animal Genetics and Genomics; Animals; Biological Evolution; Biomedicine; Cancer Research; Embryonic development; Eukaryota - classification; Eukaryota - cytology; Eukaryota - genetics; Evolution (Biology); Evolutionary genetics; Gene Function; Genetic aspects; Genomes; Genomics; Human Genetics; Humans; Metazoans; Origin; Phylogeny; review-article
• ISSN: 1471-0056; 1471-0064
• DOI: 10.1038/nrg.2017.21

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. Multicellular organisms rely on a complex interplay between diverse cell types, but how multicellularity evolved from unicellular ancestors has long been a debated research question. In this Review, the authors describe how comparative and functional genomics have provided valuable insights into the transition between unicellularity and multicellularity, including how various molecular networks have been adopted for multicellular life. 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.