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  • Review Article
  • Published:

The evolution of metazoan axial properties

Nature Reviews Genetics volume 6, pages 917–927 (2005)Cite this article

Key Points

  • Insights into the origin of bilaterian characteristics will be obtained by investigating the four basal bilaterian taxa: Cnidaria, Ctenophora, sponges and the placozoan Trichoplax adhaerens. Understanding the correct phylogenetic relationship of these organisms is necessary to understand the direction of evolutionary change.

  • Molecular expression studies argue that cnidarians, which have been considered to be radially symmetrical on morphological grounds, are actually bilaterally symmetrical and have an anterior–posterior (A–P) and a dorso-ventral (D–V) axis.

  • Ctenophores have definitive muscle cells, and the gastrodermis of cnidarians is both functionally and molecularly a bifunctional endomesoderm.

  • Although total genome sequencing for all four taxa is not yet complete, A–P patterning seems to have arisen before Hox genes evolved.

  • Cnidarians clearly possess gene family members that have been lost in bilaterian taxa such as flies and nematodes.

  • Changing patterns of gastrulation must have had a role in body-plan evolution. Gastrulation, and the genes that control it, originated at the animal pole, but have migrated to the vegetal pole in deuterostomes, and to intermediate locations in other taxa.

  • Some, but not all, genes that are expressed at the site of gastrulation in cnidarians are expressed at the site of gastrulation in other metazoans, indicating that these gene networks can and have been dissociated with one another.

Abstract

Renewed interest in the developmental basis of organismal complexity, and the emergence of new molecular tools, is improving our ability to study the evolution of metazoan body plans. The most substantial changes in body-plan organization occurred early in metazoan evolution; new model systems for studying basal metazoans are now being developed, and total-genome-sequencing initiatives are underway for at least three of the four most important taxa. The elucidation of how the gene networks that are involved in axial organization, germ-layer formation and cell differentiation are used differently during development is generating a more detailed understanding of the events that have led to the current diversity of multicellular life.

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Figure 1: How did the metazoan body plan evolve?
Figure 2: The phylogenetic relationships of basal metazoans.
Figure 3: Body plans of four basal metazoan taxa.

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Acknowledgements

I would like to thank the memory of S. Beroe, and also members of the Kewalo Marine Laboratory for spirited discussions about the views expressed in this article.

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  1. Kewalo Marine Laboratory, PBRC/University of Hawaii, 41 Ahui Street, Honolulu, 96813, Hawaii, USA

    Mark Q. Martindale

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Glossary

METAZOAN

A multicellular animal.

RADIAL SYMMETRY

The presence of multiple planes of mirror symmetry running through the longitudinal axis.

GASTRULATION

The process during which cells move from the outer regions of the embryo to the inside, to give rise to the endodermal (gut) and mesodermal (for example, muscle and blood) germ-layer derivatives; the cells that remain on the external surface of the embryo give rise to the ectodermal derivatives (skin and nervous system).

INGRESSION OR DELAMINATION

Two forms of cell movement at gastrulation. Ingression involves individual cells actively migrating into the blastocoel, whereas delamination occurs when a cell divides perpendicularly to the surface of the embryo, to generate one internal and one peripheral daughter cell.

ORGANIZER

A small dorsal region of the blastopore of a vertebrate gastrula-stage embryo that has the remarkable capacity to organize a complete embryonic body plan.

AMNIOTE

An animal, such as a reptile, bird or mammal, whose eggs contain an amnion — an extra-embryonic membrane that surrounds the embryo and helps retain fluids and store waste products.

BASAL METAZOAN

A term given to animal phyla that diverged from more derived groups early in animal evolution.

DERIVED

Evolved to a state that is distinct from the primitive condition.

CLADE

A lineage of organisms or alleles that comprises an ancestor and all its descendants.

OUTGROUP TAXON

A closely related taxon that is used for comparison; for example, to infer the ancestral versus the derived state of character evolution.

ACOELOMATE

An animal that does not possess a mesodermally lined body cavity in which the internal organs (gut and derivatives) are suspended. The coelom is a design character that is often used in evolutionary arguments about the origin of body-plan complexity.

TRIPLOBLAST

An animal that has derivatives of all three germ layers (ectoderm, mesoderm and endoderm). A diploblast has derivatives of two germ layers (ectoderm and endoderm (also known as endomesoderm)).

PLACOZOA

A 'group' (currently defined by one species, Trichoplax adhaerens) that has been proposed to be an intermediate between protozoans (single-celled animals) and metazoans (multicellular animals).

MESENCHYMAL

Describes an individual migratory cell or populations of cells that are not part of an epithelial sheet.

ARCHENTERON

The primitive gut that forms during embryogenesis at gastrulation.

BLASTULA

The stage of animal development that follows the early cleavage programme but precedes gastrulation.

GASTRULA

The stage of animal development during which the formation of distinct germ layers occurs; that is, gastrulation.

PLANKTON

Small plants and animals that live and drift in the open ocean without associating with the ocean floor for at least part of their life cycle.

BENTHOS

The bottom of the ocean or body of water. The sea floor.

DIRECT DEVELOPMENT

A developmental strategy in which embryogenesis generates a juvenile adult without the formation of an intervening larval form.

HYDROSTATIC SKELETON

A means of maintaining body integrity by internal hydrostatic pressure, rather than by using a hard external exoskeleton (arthropods) or an internal endoskeleton (chordates).

PARENCHYMAL

Describes the loose tissue that fills the space between other tissues or organs.

LIFE HISTORY

The reproductive strategy of an organism.

DEMOSPONGE

The largest class of sponge (poriferans) that has siliceous (not calcareous) spicules and comprises roughly 95% of all sponge species.

ORAL–ABORAL AXIS

The body axis that runs from the oral side to the side that is opposite the oral (the 'ab' prefix means opposite). The term is used in animals that do not have an obvious anterior–posterior axis.

SHALLOW EST SCREENS

The sequencing of relatively small numbers (typically thousands) of random cDNA molecules from a given tissue to gain insight into the nature of gene expression, but is not intended to catalogue all rare transcripts.

PARAHOX GENES

Developmentally regulated transcription factors that are the evolutionary sister group to Hox genes and show collinear patterns of expression in chordate embryos.

MESOGLEA

The extracellular space between the outer ectoderm and inner endoderm of diploblastic animals that is composed primarily of extracellular matrix molecules and can house loose populations of cells.

COMB PLATES

'Paddles' that are composed of arrays of thousands of cilia and that are found only in the locomotory organs of ctenophores.

ANIMAL POLE

The position on the oocyte and embryo in which the meiotic reduction divisions occur, and that will give rise to the anterior region of the adult body plan. It is the side opposite to the vegetal pole, which generally gives rise to the gut.

DEUTEROSTOME

A bilaterian animal in which the mouth forms as a secondary opening, separate from the blastopore. Deuterostomes include chordates, hemichordates and echinoderms. By contrast, the mouth of protostomes develops before the anus during embryogenesis. Protostomes include arthropods, molluscs and worms.

CHAETOGNATHS

An enigmatic phylum of marine animals that have features of both protostomes and deuterostomes and therefore defy phylogenetic placement.

MEIOFAUNAL

A class of small but highly diverse interstitial animals that live between grains of sand.

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Martindale, M. The evolution of metazoan axial properties. Nat Rev Genet 6, 917–927 (2005). https://doi.org/10.1038/nrg1725

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