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  • Review Article
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The evolution of signalling pathways in animal development

Key Points

  • Surprisingly, only a few classes of signalling pathways are sufficient to pattern the development of individuals, and they are used repeatedly throughout the evolution of animals.

  • Signalling pathways are robust and flexible, resulting in the reproducibility of developmental decisions and the generation of evolutionary novelty.

  • Whereas most signalling systems are found in all multicellular animals, only a few signalling molecules have been identified in unicellular eukaryotes, such as Plasmodium falciparum or Monosiga brevicollis.

  • The evolution of signalling pathways might therefore have been a prerequisite for the occurrence of animal multicellularity.

  • Whole-genome comparisons offer unique opportunities to study the evolution of signalling systems by combining an in silico approach with comparative functional studies in selected organisms.

  • Signalling pathways have been co-opted during animal evolution and are important for the emergence of morphological novelties.

  • Selected case studies in non-model organisms that are amenable to genetic analysis can reveal how individual components are added to signalling systems, thereby indicating how the signalling pathways themselves evolve.

Abstract

Despite the bewildering number of cell types and patterns found in the animal kingdom, only a few signalling pathways are required to generate them. Most cell–cell interactions during embryonic development involve the Hedgehog, Wnt, transforming growth factor-β, receptor tyrosine kinase, Notch, JAK/STAT and nuclear hormone pathways. Looking at how these pathways evolved might provide insights into how a few signalling pathways can generate so much cellular and morphological diversity during the development of individual organisms and the evolution of animal body plans.

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Figure 1: Mechanisms of signalling specificity.
Figure 2: Gene duplication events do not correlate with the origin of the principal animal groups.
Figure 3: Co-option of the Hedgehog signalling pathway for the induction of butterfly eyespots in the wing.
Figure 4: Somatic sex determination in Caenorhabditis elegans.

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Acknowledgements

We apologize to those scientists whose work has not been cited due to space restrictions. We thank D. Rudel and J. Srinivasan for critically reading the manuscript.

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Correspondence to Ralf J. Sommer.

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DATABASES

LocusLink

axin

dsx

engrailed

eve

Fz

Fz2

Gli/Ci

hairy

Hh

JAK

Mad

Patched

Pnt

STAT

Su(H)

Tcf/Lef

TGF-β

Ubx

Wg

Wnt

WormBase

β-catenin

egl-1

fem-2

GSK-3

HER-1

JNK

LET-23

LIN-31

mab-3

pry-1

sdc-1

sdc-2

sdc-3

TRA-1

TRA-2

ZFIN

masterblind

FURTHER INFORMATION

Ralf J. Sommer's lab

Glossary

K M

The substrate concentration at which the reaction rate of an enzyme is half maximal, also known as the Michaelis–Menten constant.

BILATERIANS

Multicellular animals that have a real body cavity (coelom) and a primary bilateral symmetry. They include all multicellular organisms except for the sponges, cnidarians and ctenophorans.

PROTOSTOMES

Animals whose development is characterized by the formation of a single opening. The protostomial phyla are subdivided into the ecdysozoans and the lophotrochozoans.

ECDYSOZOA

A bilaterian clade that is characterized by external cuticles that are shed during stages of development. It includes the insects and nematodes.

LOPHOTROCHOZOA

A bilaterian clade that is characterized by a lophophore (a specific morphological structure) or a trochophore larval stage. Well-known members include the molluscs and the annelids.

DEUTEROSTOMES

A bilaterian clade that is characterized by the formation of distinct mouth and anal openings.

ASCERTAINMENT BIAS

An error that is introduced with a biased sampling scheme.

PARALOGUES

Homologous genes that have originated by gene duplication.

DIPLOBLASTS

A group of ancestral animals, such as the cnidarians and the porifera, that do not develop mesoderm.

PROTISTS

Unicellular heterotrophic eukaryotes.

CNIDARIANS

A simple and ancient phylum of multicellular animals, such as jellyfish or corals, found mainly in marine environments.

PORIFERA

A phylum of multicellular animals with only two cell layers, the ectoderm and the endoderm, that are separated by an acellular mesogloea.

CHOANOFLAGELLATES

A group of protists that contain one flagellum at some stage of their life history.

PARAZOANS

An animal subkingdom that includes the porifera and the placozoa, the latter of which contains only one species (Trichoplax).

EUMETAZOANS

An animal subkingdom that includes the cnidarians, the ctenophorans and the bilaterians.

CYCLOSTOMES

A group of ancestral jawless fishes, including the lampreys.

GNATHOSTOMES

The group of higher fishes, all of which are characterized by the presence of jaws.

PSEUDOCOELOMATES

Animals, such as the nematode, that do not have a body cavity that is fully lined with mesodermal cells.

CLADE

A taxon or other group of organisms that share a closer common ancestor with one another than with members of any other clade.

HETEROTOPY

The displacement of the development of an organ in space.

DOSAGE COMPENSATION

A mechanism that regulates the expression of sex-linked genes that differ in dose between females and males.

NEOMORPHIC

A qualitatively new feature of a phenotype that is produced by a mutant allele.

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Pires-daSilva, A., Sommer, R. The evolution of signalling pathways in animal development. Nat Rev Genet 4, 39–49 (2003). https://doi.org/10.1038/nrg977

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