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  • Review Article
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The evolution of cell types in animals: emerging principles from molecular studies

Nature Reviews Genetics volume 9, pages 868–882 (2008)Cite this article

Key Points

  • Cell types in animals evolved by step-wise diversification into sister cell types, which is analogous to the evolution of species or genes. We can identify homologous cell types between species by comparing molecular fingerprints, which represent the unique aspects of the gene expression profile of a specific cell type.

  • Molecular fingerprint comparisons recently allowed the identification of homologous cell types in distantly related phyla, for example: motor neurons that are conserved across insects, vertebrates, nematodes and annelids; photoreceptors that are conserved across the animal kingdom; and blood cells in various bilaterian animals.

  • Ancient cell types are multifunctional, for example: the light-sensitive and locomotor steering rudder cell of sponges and cnidarians; the epithelial muscle cells in cnidarians; and the photosensitive–neurosecretory 'protoneuron'.

  • During cell type evolution, the multiple functions of ancient cell types are distributed in a complementary manner to descendant sister cell types. This major principle of cell type evolution is referred to here as functional segregation.

  • Cell type functional segregation explains the evolutionary emergence of axonal circuits in nervous-system evolution. For example, the wiring of the vertebrate retina and of the nose–hypothalamus–pituitary axis may have arisen by the functional segregation of sister cell types.

  • Functional divergence is a second important principle of cell type evolution. Here, cellular functions are retained in both descendant cell types but modified in different directions. Cell type functional divergence often involves gene duplication.

  • The acquisition of new functions can occur via the co-option of differentiation genes that were previously used by other cell types or by the de novo emergence of genes that are added to existing gene batteries.

  • In many cases, the development of cell types recapitulates the evolution of cell types. However, highly divergent developmental paths frequently generate homologous cell types that are shared between species, which indicate that cell type development is more plastic than cell type identity.

Abstract

Cell types are fundamental units of multicellular life but their evolution is obscure. How did the first cell types emerge and become distinct in animal evolution? What were the sets of cell types that existed at important evolutionary nodes that represent eumetazoan or bilaterian ancestors? How did these ancient cell types diversify further during the evolution of organ systems in the descending evolutionary lines? The recent advent of cell type molecular fingerprinting has yielded initial insights into the evolutionary interrelationships of cell types between remote animal phyla and has allowed us to define some first principles of cell type diversification in animal evolution.

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Figure 1: Cell typogenesis: homologous cell types and sister cell types.
Figure 2: Homologous cell types identified by molecular fingerprints.
Figure 3: Ancient multifunctional cell types.
Figure 4: Modes of cell type diversification.
Figure 5: The evolution of neuronal circuits by functional segregation.

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Acknowledgements

I would like to thank G. Jekely, D. Nilsson, F. Spitz and the three unknown referees for helpful comments on earlier versions of the manuscript, and the members of the Arendt laboratory for various valuable discussions.

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    Detlev Arendt

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Glossary

Opsins

A family of G-protein-coupled receptors that function as light-sensitive photopigments.

Urbilaterian

The last common ancestor of all bilaterians.

Nematocyte

A venomous cell that evolved for catching prey and for predator defence by releasing the nematocyst, which is a miniature cellular weapon, in one of the fastest movements in the animal kingdom.

Cnidarian

Radially symmetrical animal that has a sac-like body with only one opening. The group includes jellyfish, corals, hydra and anemones

Amphioxus

The common name for the cephalochordate Branchiostoma lanceolatus, the most basal living invertebrate that is related to vertebrates.

Ascidian

A group of sessile animals with swimming larvae that are the closest living invertebrate relatives of the vertebrates.

Eumetazoa

All animals (metazoa) except sponges.

Ostracod

The ostracoda are a group of crustaceans known as seed shrimps.

Subfunctionalization

The process whereby a pair of duplicated genes becomes permanently preserved because the two gene copies have reciprocally lost essential subfunctions by acquiring complementary degenerative mutations.

Horizontal gene transfer

The transfer of genetic material between the genomes of two organisms that does not occur through parent–progeny transmission.

Notochord

A rod-shaped structure that runs along the dorsal axis of the embryo, separating the muscle blocks. The notochord is one of the defining features of the phylum Chordata, which vertebrates belong to.

Neural crest

A migratory cell population that arises at the lateral extremities of the embryonic neural plate, and which differentiates into various cell types, depending on the location. These cells include endothelial cells, smooth and skeletal muscle cells, bone, adrenal medulla, and cells of the sensory and autonomic nervous systems.

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Arendt, D. The evolution of cell types in animals: emerging principles from molecular studies. Nat Rev Genet 9, 868–882 (2008). https://doi.org/10.1038/nrg2416

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