Cast an eye on growth factors

Paul Harvey switches on to the mix of genes and development.

One thing that almost all evolutionary biologists agree on is that development has returned to their fold. The story of its demise and resurrection is the subject of this book.

The demise started after Darwin, who recognised the importance of comparative embryology's support for his argument that constituted On the Origin of Species . As the decades progressed, however, particularly with our increased understanding of genetics, development became marginalised. The generally held view from evolutionary genetics was epitomised by Ernst Mayr, who argued that similar adaptations in different taxa were almost invariably the result of different genetic causes. This had the implication, as the molecular biologist Gunther Stent argued 20 years ago, that differences in development that lead to differences in phenotype involve "a near infinitude of particulars, which have to be sorted out case by case".

Everything changed in the 1980s and 1990s, when it became apparent that many of the genes that controlled the expression of other genes had nucleotide sequences that were very highly conserved across virtually the whole of the animal kingdom. Mayr turned out to be right about many things, but his claim that "the search for homologous genes is futile except in very close relatives" was wrong. What is more, the same control genes have often been used by evolution to perform very similar functions on different occasions.

A good example involves the eyeless gene of the fruit fly Drosophila and the small eye gene in mice. If wild-type eyeless genes are turned on in unexpected places on the body of a developing fruit fly, then eye tissue develops there. And if wild-type small-eye genes from mice are expressed in fruit flies during development, then fruit-fly eye tissue develops. This is extraordinary because fruit flies have compound eyes, evolutionarily very different from mammalian eyes, yet it seems that homologous genes that have been largely conserved in sequence over evolutionary time induce the development of eyes in insects and mammals.

Sean Carroll takes his reader through the earliest evidence in which we might be able to discern common patterns in the evolution of development.

Animals frequently consist of repeated modules, some of which become specialised for new functions while others are lost through time, so there may be common control genes involved. Then there were examples of "organisers" and "zones of polarising activity" that could be transplanted from one early developing embryo into another, causing the development in the host of what was to have appeared in the donor - this meant that an effectively irreversible developmental cascade had been initiated. Finally, there were "homeotic mutants" - individuals in which one body part was inexplicably replaced by another. For example, fruit-fly antennae may very occasionally develop as legs.

The finding that would eventually illuminate the path was the understanding of how genes are induced to be switched on and off. Francois Jacob and Jacques Monod (with Andre Lwoff) received the Nobel prize in 1965 for their work with bacteria that showed how repressors could bind to the end of a gene to prevent its expression. But those repressors may be removed by the presence of particular agents, so that the gene is activated to produce its product. For example, there is no evolutionary benefit to be had in producing the enzyme that breaks down lactose if there is no lactose to break down, so in bacteria a repressor stops production of the enzyme. But that repressor is inactivated by the presence of lactose. This is the world of genetic switches on which the new field of "evo-devo" was to be constructed.

We learn about Hox genes that have controlled development of different body regions and retained their function since pre-Cambrian times. It was the discovery of Hox genes - and the fact that they are aligned on the chromosome in the same sequence as the body parts they influence are aligned along the body's axis - that really wakened the evolutionary biologist to the potential to understand more about development. From here, Carroll introduces the concept of a "genetic toolkit" of genes producing proteins that control development.

Getting this far takes a third of the book. The rest explains what we know about how this relatively small genetic toolkit can control the development of the huge variety of species inhabiting our world. It is a story of genes switching on and off in response to knowing where they are spatially and temporally in the process of development and of the same genes being reused during evolution.

The second part of the book is rather patchy in its coverage but illustrative nonetheless. There are some fascinating model systems for investigating the evolution of developmental diversity that are relatively well understood - for example, patterning of butterfly wings. But there are other areas, such as the evolution of the human brain and mind, about which this field currently has little to say.

This book is the only account available in this field for scientifically literate laypeople, scientists outside the field and undergraduates. But it is difficult to use. Carroll's style is very personal - the text is littered with irrelevant anecdotes about his and his family's lives. There are lots of stomach-churning asides - when describing the fact that female flies choose males with blotches on their wings, we are told: "Hey, different strokes for different folks." And whenever a popular song can be quoted, Carroll will do it.

Carroll's perspective can also be suspect. He suggests that evo-devo was the next big thing to happen in our understanding of evolution since the modern synthesis, which incorporated genetics. Surely the discovery of DNA as a genetic material, the genetic code and the whole replication process has been overlooked. A generation of undergraduates could come out inspired by the new science of evo-devo but misguided about quite where it fits.

Paul Harvey is head of the department of zoology, Oxford University.