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Early central nervous system evolution: an era of skin brains?

Nature Reviews Neuroscience volume 4, pages 617–627 (2003)Cite this article

Key Points

  • In the late nineteenth century, there were numerous attempts to show how the central nervous system (CNS) evolved. However, no consensus was reached and the subject went out of style until around 20 years ago, when rapid progress in molecular biology began to impact ideas about animal evolution.

  • The nervous system is difficult to consider in a phylogenetic context, because many of its properties are emergent novelties. A CNS is defined as a place where neurons are more concentrated than elsewhere in the body, but this definition blurs the distinction between the CNS and the peripheral nervous system of basal invertebrates.

  • It is not known whether the common ancestor of the protostomes and deuterostomes — the two main groups of bilaterally symmetrical animals — had a biphasic life history, in which a swimming larva undergoes metamorphosis to become a benthic adult. However, when proposing homologies for CNS regions, it is better to consider adult rather than larval characters.

  • Most current phylogenetic analyses place the cnidarians, which comprise organisms like hydras and jellyfish, just basal to the bilateral animals. Cnidarian polyps have several relatively independent nerve nets. These nets tend to be especially condensed near the oral opening, where they are usually termed nerve rings.

  • There are half a dozen hypothetical evolutionary schemes for transforming an anthozoan-like creature (with a solid or hollowed-out endoderm) into a bilateral animal with a through gut. Most begin with an individual non-colonial ancestor, although one — the colonial scenario — proposes that an ancestral colony of polyps individuated into a single, bilaterally symmetrical animal.

  • Until recently, it was assumed that the ancestral nerve net became localized as all or part of the CNS in the basal groups of bilaterally symmetrical animals. However, in the enteropneust hemichordate Saccoglossus, expression of homologues of vertebrate CNS anteroposterior patterning genes is not limited to the nerve tracts, but extends widely throughout the ectoderm, implying that the CNS of this animal includes the entire basiepidermal nerve net.

Abstract

The central nervous system (CNS) in different animals develops under the control of genes that are often conserved both structurally and functionally. The question of whether such conservation means that the common ancestor of all bilateral animals had an anatomically complex CNS is controversial. Recently, a hemichordate was found to express homologues of many of these genes in a rostrocaudal order resembling that in Drosophila and vertebrates. Surprisingly, however, the hemichordate genes are expressed not in a localized CNS, but in widespread epidermal domains pervaded by a basiepidermal nerve net. Here, I discuss the implications of this discovery for CNS evolution.

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Figure 1: Current ideas about central nervous system (CNS) evolution from a cnidarian-like ancestor.
Figure 2: Nervous systems in adult and developing enteropneust hemichordates, vertebrates and Drosophila.
Figure 3: Two alternative scenarios for central nervous system (CNS) evolution.

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Acknowledgements

I am deeply indebted to C. Lowe, J. Gerhart and D. Erwin for their constructive criticisms. Work in my laboratory is supported by grants from the US National Science Foundation.

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    Nicholas D. Holland

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FURTHER INFORMATION

Encyclopedia of Life Sciences

brain evolution and comparative neuroanatomy

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Glossary

PROTOSTOMES

One of the two main groups of bilaterally symmetrical animals. The name derives from 'proto' (first) 'stome' (mouth), because the first opening (blastopore) of the embryo becomes the definitive mouth. Awkwardly, there are many exceptions to this rule within the group.

DEUTEROSTOMES

The second of the two main groups of bilaterally symmetrical animals. The name derives from 'deutero' (second) 'stome' (mouth), referring to the origin of the definitive mouth as an opening independent from the blastopore of the embryo.

HEMICHORDATES

A phylum of marine worms comprising the enteropneusts and pterobranchs.

PANARTHROPODS

A large monophyletic group including not only arthropods in the strict sense, but also two more basal phyla — the tardigrades (water bears) and the onycophorans (velvet worms).

CYCLOSTOMES

The most basal group of living vertebrates.

BENTHIC

Living on the bottom of a sea or lake.

PLANULA/PLANULOID

A planula is the swimming, slipper-shaped larva of cnidarians. Its ciliated epidermis covers either a solid or a hollowed-out mass of endoderm cells. The planuloid is a hypothetical ancestral animal with roughly the same morphology as a planula larva, but it is sexually mature.

LOPHOTROCHOZOANS

One of the two groups of protostomes, which includes molluscs and various worm-like phyla, none of which moult when they grow.

CLADE

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

POU FAMILY

A family of transcription factors, each of which contains two DNA binding domains — the POU homeodomain, which is homologous to domains that are found in other types of transcription factor, and the POU-specific domain, which is specific to the POU factors.

AMPHISTOME

A developmental term that is applied to the first embryonic opening in instances when it gives rise to both the mouth and the anus.

COELOM

The body cavity of an animal, such as a vertebrate or insect, which is completely lined with mesodermal cells.

DEFAULT MODEL OF NEURAL INDUCTION

A model in which it is proposed that in the absence of cell–cell signalling, ectodermal cells will adopt a neural fate.

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Holland, N. Early central nervous system evolution: an era of skin brains?. Nat Rev Neurosci 4, 617–627 (2003). https://doi.org/10.1038/nrn1175

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  • DOI: https://doi.org/10.1038/nrn1175

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