Homology (Novartic Foundation Symposium 222).

Gregory R. Bock and Gail Cardew (eds). John Wiley and Sons, Chichester. 1999. Pp. 256. Price £75.00, hardback. ISBN 0 471 98493 0.

We all know that homology is a central concept in biology and we all feel that somewhere out there is an expert who could tell us exactly what it is. The main conclusion of this book is that there is no such person. At school textbook level, the term ‘homology’ has normally been applied to morphological parts of animals and plants. If a structure is similar in two different organisms, it is said to be homologous where it has been retained during evolution from a common ancestor. Conversely, two similar structures are said to be analogous if they have evolved independently in the two lineages.

So far this seems simple enough. But the more we read, the less we believe. The first chapter deals with the history of the concept and it turns out that none of the great zoological luminaries of the past actually did supply a satisfactory definition. Following this, many chapters debate the relationship between the visible structure and the underlying gene network that produced it. Primary sequence analysis has made it relatively straightforward to establish whether genes themselves are homologous. So if the same gene is expressed in two structures in different organisms, does this make the structures homologous? Not necessarily. There is general agreement that the nested expression of the Hox gene cluster does define a homologous anterioposterior axis for all animals. However, we should not be tempted to say that the isthmus of the vertebrate brain is homologous to a Drosophila segment boundary just because both of them express the gene engrailed. This is because most developmental control genes are expressed in several domains and contribute to the development of several structures. An intermediate situation is provided by the eye. The gene pax6 is needed for eye development in creatures as far apart as Drosophila and mouse, and, although the functional information is not available, it is also expressed in the developing eye of planarians and cephalopods. The eyes of these various creatures have long been regarded as analogous because their structure is so totally different, but the new evidence tempts us to call them homologous. However, it is unlikely to be the eye itself but rather a photoreceptive organ-forming territory of the head that is homologous.

An insistence on the importance of the level of homology is a theme running through the book. This is because whole genetic pathways may be preserved as functioning units and used for new purposes. In such a case the pathways are homologous but the structures need not be. For example the hedgehog-patched-decapentaplegic pathway in the Drosophila wing disc is very similar to the sonic hedgehog-patched-BMP2 pathway in the chick wing bud. Here both the genes and their regulationary relationships seem homologous, but the final structures cannot be. At least they cannot be as wings, as we can be quite sure that the Precambrian common ancestor of the chicken and the fruit fly was a marine organism without wings, whatever other appendages it possessed.

Although there is considerable discussion of levels, I feel that more could have been said about cell types and about serial homology. Cell types such as neurons or muscle cells seem clearly homologous in different animals, although the CNS parts or named muscles to which they contribute need not be homologous. Serial homology refers to reiterated structures within an organism. To call these homologous involves an implicit admission that a common mechanism of formation is an essential attribute of homology, something whose necessity between organisms continues to be controversial, and is hotly debated in these pages.

So does all this mean that the concept of homology is actually useless because it cannot be defined, or is its richness precisely that it cannot be defined and so it continues to generate discussion and new research? The book is a stimulating contribution to this debate, and it is regrettable that its high price seems guaranteed to confine its sale to a handful of libraries.