Getting a head

A controversial hypothesis aboutdevelopment is turned on its head and light is shed on one of the world'sstranger creatures.

ONE OF the most striking differences between vertebrates (backboned animals) and other animals is that vertebrates have distinctive heads, each with a well-protected brain, a mouth and a cluster of sense organs.

All developmental biologists agree that many features of the vertebrate head - such as the bones of the face and jaws - owe their beginnings to an embryonic tissue called `neural crest', not found in non- vertebrate animals.

But for some years, Australian researcher Anne Kemp has suggested that there is at least one vertebrate in which the neural crest does not seem to play a part in head formation.

The beast concerned is the Australian lungfish (Neoceratodus forsteri), a weird, primitive fish that just happens to be one of the closest living relatives to land vertebrates (amphibians, reptiles, mammals and birds) and therefore of particular interest to evolutionary biologists.

Kemp's hypothesis - for which she has provided careful experimental support - is extremely controversial. If true, it would put a serious dent in our understanding of the evolution of the vertebrate head. Lennart Olsson of Uppsala University in Sweden and colleagues now show thatthe neural crest does indeed contribute to the development of the head inthe Australian lungfish, much as it does in other vertebrates.

Did Kemp get it wrong, then? The answer, as so often in science, is both yes and no. But first, something about neural crest. Very early in the life of an embryo, a strip of cells running along the back rolls up lengthwise, its edges rising to meet each other, and forms a hollow tube. This, the neural tube, is the basis of the spinal cord and the backbone. As the neural tube closes, a population of cells within the closing edges (the `neural crest' itself) forms a number of distinct migrating streams, spreading downwards and outwards, across the body. One stream travels forward, forming the bones of the face and the jaws. Another travels downwards, forming the bones associated with the tongue and larynx; a third migrates downwards and slightly backwards, forming what in fishes becomes the gill arches.

This pattern is seen in all vertebrates so far examined. Experimental studies in which the neural crest is removed very early in embryogenesis results in the failure to develop distinctive structures in the head - confirming the central role of neural crest cells in head formation. Kemp performed just this kind of study on embryos of the Australian lungfish and found that even when the neural crest was removed prior to the migration of its cells, lungfishes developed quite normally. This suggested to her that there was at least one vertebrate with a perfectly good head on it that did not require neural crest to produce it.

But the time at which neural crest cells start to migrate varies greatly between animals. In frogs and mammals, for example, it gets going before the neural tube has closed. In salamanders and chickens, in contrast, the neural tube is fully closed before migration takes place.

Olsson's team finds, as they explain in the journal Evolution and Development , that the neural crest in the Australian lungfish sleeps late. The neural tube is relatively well- developed before the neural crest cells differentiate, let alone start migrating. So they propose that Kemp may have removed neural crest from lungfish embryos much too soon. This would leave the remaining neural tissue time to generate new neural crest tissue and resume normal service, giving the false impression that the face and jaws of the embryo fish must have come from somewhere else.

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