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  • Review Article
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A simple plan — cnidarians and the origins of developmental mechanisms

Nature Reviews Genetics volume 5, pages 567–577 (2004)Cite this article

Key Points

  • Cnidarians lack true mesoderm, in the sense of a third germ layer that arises as a direct result of gastrulation. However, at the molecular level, muscle development in the medusa of the hydrozoan Podocoryne carnea seems to mirror its differentiation as a mesodermal lineage in 'higher' animals.

  • Molecular evidence indicates that the Anthozoa are the basal cnidarian group, but they lack both the medusa stage and well-developed muscle. So, there is active debate as to whether the molecular similarities between P. carnea muscle development and that in Bilateria indicate convergent evolution or the loss of the medusa stage in the Anthozoa.

  • Many of the same 'mesodermal marker' genes are expressed during gastrulation in Anthozoa and Bilateria. This might indicate that the primitive function of these genes was in such fundamental processes as cell proliferation, adhesion and motility, and indicates the possibility that as true mesoderm evolved from endomesoderm, these genes became associated with the former.

  • During early coral and anemone development, a second axis is defined by the expression of a gene related to DPP/BMP4 — the key determinant of the dorsal–ventral axis in higher animals — and this asymmetrical expression is maintained in the sea anemone polyp.

  • Molecular analyses establish the bilateral anthozoans, rather than the radial hydrozoans, as the basal cnidarians. Anthozoans have several of the regulatory genes that are responsible for patterning both of the principal axes of higher animals (for example, Emx and dpp/Bmp4), and express them in ways that are inconsistent with the assumption of a single body axis. EST projects on several cnidarians consistently highlight the complexity of the cnidarian gene complement and imply that, at the genetic level, the common ancestor of bilateral animals was more complex than has previously been assumed.

  • The blurring of the triploblast/diploblast divide, the confirmation that basal cnidarians are bilateral and the complexity of their gene set lead us to suggest rethinking the entire notion of cnidarians as 'lower' animals.

  • Several key developmental genes have been independently duplicated in cnidarians, including snail and Hox-related genes, and, even at the genus level, large changes in genome size have occurred. These factors complicate the understanding of the evolution of specific gene families and will need to be considered in selecting representative cnidarians for genomic sequencing.

  • Cnidarians are not a genetically uniform group. Their diversity and genetic complexity indicate that their apparently simple morphology might mask considerable functional complexity, providing great scope for evolutionary studies.

Abstract

Comparisons with cnidarians, long considered to be 'simple' animals, are providing crucial insights into the origins of conserved developmental mechanisms and the nature of the common metazoan ancestor. Traditionally, an extra germ layer and a second axis of body symmetry are the features that distinguish 'higher' Metazoa from lower animals such as cnidarians. Moreover, it was expected that 'lower' animals would have a simple gene set that corresponds to their simple morphology. Now, molecular genetic approaches are blurring the developmental divide between cnidarians and bilateral animals, and cnidarian sequencing projects are showing that the common metazoan ancestor was more genetically complex than was previously assumed.

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Figure 1: Muscle development in the medusa of Podocoryne carnea.
Figure 2: Expression of the mesodermal marker snail during early gastrulation in Acropora millepora and Drosophila melanogaster.

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Acknowledgements

We thank the many cnidarian workers mentioned in the text for their help and cooperation in the production of this paper and apologize to all those whose work has gone unmentioned owing to space limitations; for example, the elegant work of T. Leitz and co-workers on the control of metamorphosis in Hydractinia, which has led to important insights into metamorphosis. We gratefully acknowledge the support of the Australian Research Council (both directly and through the Centre for the Molecular Genetics of Development, Canberra, Australia), and the contributions made both by various external collaborators and by members of our laboratories, past and present. Part of the title is a reference to the excellent eponymous film by Sam Raimi, the plot of which suggested to us some analogies between human behaviour and cnidarian evolution.

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Authors and Affiliations

  1. Centre for the Molecular Genetics of Development and Research School of Biological Sciences, Australian National University, P.O. Box 475, Canberra, ACT 2601, Australia

    Eldon E. Ball, David C. Hayward & Robert Saint

  2. Comparative Genomics Centre, Molecular Sciences Building 21, James Cook University, Townsville, 4811, Queensland, Australia

    David J. Miller

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  1. Eldon E. Ball
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DATABASES

Entrez

Bmp4

Chrd

dorsal

dpp

even skipped

ey

ind

Mef2

Msh (Drop)

Nkx2-1 (Titf1)

PAX6

snail

sog

sparkling (shaven)

T

tinman

twist

vnd

FURTHER INFORMATION

Centre for the Molecular Genetics of Development

Comparative Genomics Centre, James Cook University, Townsville, Australia

Zoologisches Institut der Uni Basel

Glossary

BILATERIA

A monophyletic group of metazoan animals that is characterized by bilateral symmetry. This group comprises all of the Metazoa except for the Radiata (Ctenophores and Cnidaria) and the Parazoa (sponges).

EXPRESSED SEQUENCE TAG

(EST). A nucleic acid sequence that is derived from cDNA, usually from the ends of cDNA clone inserts as part of high-throughput sequencing projects.

HIGHER ANIMALS

(Higher Metazoa). We use these terms as synonyms of Bilateria.

LOWER ANIMALS

(Lower Metazoa). Here used to refer to Cnidaria, Ctenophora and Parazoa. Other authors include the Platyhelminthes (flatworms).

BLASTOPORE

The opening of the archenteron in the gastrula.

MEDUSOZOA

A clade comprising three of the four cnidarian classes, which produce a sexually reproducing medusa (jellyfish) as part of the life cycle.

RADIATA

Animals that are traditionally considered to have radial symmetry. This group includes the ctenophores and cnidarians, and, according to some authors, the sponges.

TRANSVERSE FISSION

A means of asexual reproduction seen in some sea anemones that involves division of the polyp into two or more parts with cleavage occurring in the transverse plane.

BLASTULA

The early stage of animal development in which a single layer of cells surrounds a fluid-filled cavity, forming a hollow ball.

PLANULA

The free-swimming, ciliated larva of a cnidarian.

ZOOID

An individual specialized unit of a colonial cnidarian.

HYPOSTOME

The terminal region of a polyp, on which the mouth is situated.

MESENTERIES

Longitudinal sheets of tissues that extend radially from the body wall into the body cavity.

POLYP

The sessile form of life history in cnidarians; for example, the freshwater Hydra.

ENTOCODON

The mass of cells on the end of a medusa bud that becomes the velum and subumbrella surface.

SUBUMBRELLAR

The oral surface of a medusa.

MESOGLEA

(Also known as mesogloea). The body layer between ectoderm and endoderm in cnidarians, ctenophores and acoelomates, which is traditionally distinguished from mesoderm on the basis of the former being acellular and the latter cellular. However, in reality, enormous variation is seen across the Cnidaria in the extent to which the matrix of the mesoglea is invaded by various cellular and fibrillar components, and only in some hydrozoans does it approach true acellularity.

NEURAL CREST

Cells at the dorsal midline of the vertebrate neural tube, which undergo an epithelial-to-mesenchymal transition and migrate to many locations, contributing to the development of a wide variety of structures, including the peripheral nervous system and craniofacial features, therefore essentially enabling a second wave of development.

SYNAPOMORPHY

A derived state that is shared by several taxa.

PARALOGUE

Two genes are paralogous if they were a result of a duplication event.

SIPHONOPHORE

Any marine colonial hydrozoan of the order Siphonophora, including the Portuguese man-of-war.

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Ball, E., Hayward, D., Saint, R. et al. A simple plan — cnidarians and the origins of developmental mechanisms. Nat Rev Genet 5, 567–577 (2004). https://doi.org/10.1038/nrg1402

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