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Neo-Darwinism has never claimed to be a theory of everything

Bad weather, a defeat of Manchester United and Mondays are all blamed on the government of the day. Brian Goodwin seems to have elected what he calls "Neo-Darwinism" to government status in the biological sciences. Many of the points he makes are ones I happen to agree with, although they seem to have little to do with one another or with Neo-Darwinism. Other claims are more problematic.

Neo-Darwinism is hard to recognise disguised as Goodwin's straw man. Neo-Darwinism has never claimed to be a theory of everything; it sets out to solve a specific set of problems. Blaming it for failing to explain how organisms develop is no more sensible than excoriating medical practitioners for failing to predict earthquakes.

So what exactly is Neo-Darwinism? It emerged in the 1930s, when Darwin's idea of evolution by natural selection was recast in the light of all that had been discovered since, particularly about genetics. Darwin was inevitably rather hazy about genetics. The general confusion was subsequently made worse by the apparent contradiction between Mendel's discovery of the particulate nature of inheritance in peas, implying large effects of single genes, and the discovery that much genetic variation causes continuous differences, in traits like body size. That paradox was resolved by the realisation that such characteristics are affected by genetic variants that cause only small differences, and that the environment often also plays a role in causing differences between individuals. A lot of progress has been made in identifying the genes associated with this kind of continuous variation, partly because they are important in genetic improvement of livestock and crops.

The big contribution of Neo-Darwinism was to produce a theory for the behaviour of genes in populations, and to identify the forces that can change the genetic composition of populations, in other words cause evolution. One of these forces is mutation, the production of random mutations in the genes of every new generation and hence the origin of all new genetic variation. Another is natural selection, the action of the environment on each individual, causing some to die, others to survive, passing their mutations on to their offspring.

So this is what Neo-Darwinism is about; the forces that change the genetic composition of populations. It does not pretend, and never has done, to be a complete and self-sufficient theory of why organisms are as they are, still less a solution to the ontological question of why they exist at all. The core of Goodwin's unfortunate misunderstanding about Neo-Darwinism is that he demands too much of it, and like anyone who makes too many demands in a relationship, he fails to find satisfaction.

A simple example will serve. Neo-Darwinists might, indeed do, try to explain how natural selection acts on the eye-spot colour patterns found on the wings of many butterflies. Eye spots may scare predators and allow the butterfly to escape, or they may deflect attack to less vulnerable parts of the body and leave the predator with a mouthful of scales. What Neo-Darwinists are not trying to explain is how the eye-spots are produced during the development of the wing, although they would be unwise indeed if they did not regard this information as relevant, because it could explain how readily and in what ways new mutations might alter the colour pattern.

The work of developmental biologists has told us a lot about how eye-spots are produced. For instance, the central bit of tissue that instructs its neighbours to make eye-spot rings can be transplanted between strains, and then an eye-spot of the size characteristic of the donor strain is made, showing that it is mainly the signal and not the responding tissue that determines how big the eye-spot will be. So developmentalists and Neo-Darwinists are often interested in similar traits, but they approach them in rather different ways, and with different questions in mind.

Few would quarrel with Goodwin's assertion that we need to know about more than genes to understand the development of organisms, indeed many others have said the same. But his description of the state of knowledge is remote from what is happening in the laboratory. His complaint is reminiscent of one made repeatedly in the late 19th century and early 20th centuries by supporters of "entelechy'' and "elan vitale'' and all the other substitutes for scientific explanation that preceded the golden age of experimental embryology, and the even more recent age of molecular genetics. If Goodwin wishes to enlighten the general reader, why does he not describe in detail what is now known about the development of the tiny worm Caenorhabditis, every cell of which can now be tracked precisely through development? Why does he not describe the fascinating and entirely unexpected phenomenon of apoptosis, or cell death, which seems to be a key to development of complex structures such as the nervous system? These are mere enumerations of progress, to be sure, but it is difficult to know how to respond, other than by producing concrete facts, when confronted with the bland, and entirely undocumented, assertion that the development of organisms is a total mystery beyond the ken of the biologist.

The specific problem of three-dimensional form is crucial, and Goodwin is in good company in pointing this out. The adult products of development have to have the right things in the right places. From the start of development, spatial information comes from sources other than genes, like the spatial arrangement of gene products in the egg, sometimes the point of sperm entry into the egg and, most importantly, the state of the developing embryo. But these ideas are not contentious, nor are they shrouded in mystery. The molecular gradients and interactions that produce the three-dimensional order in the developing body are being identified, as are the important physical inputs, like light from the outside world in the development of binocular vision. Of course when we understand development we still shall not understand everything. We are taken no further forward in understanding how a fly sees by discovering a "master" gene for eye development. To understand seeing we need to know about optics and a great deal more besides.

So when Goodwin says that to understand the development of organisms we have to understand the physical forces acting on them, and the interactions inside them, I agree entirely. And if this were the only point he wished to make, one would regard his attempted demolition of Neo-Darwinism as only the latest in a long historical succession of misunderstandings of its purpose. Unhappily, he has further complaints, and here he falls into factual error. The main one of these misreporting errors has to do with "directed mutation". A central tenet of Neo-Darwinism, and the one its critics find most unpalatable, is that gene mutations are random events. Goodwin claims recent discoveries in molecular biology have revealed a process of "directed mutation". The sense in which mutations are random is that they occur without regard to current needs. So a mouse in a cold climate is no more likely to produce a mutation for a thick coat than is one sweltering in a heat wave. The claim is not that all mutations are equally likely - they are not. Some, like the change producing red-green colour blindness are common, while those producing green hair are rare. And some kinds of genetic change, like movement of bits of genetic material around the genome, are more common than others, like a reversal of gene order.

So for the Neo-Darwinist necessity is not the mother of mutation. This orthodoxy was challenged recently by the claim that bacteria starving to death in the presence of an unusable potential food source were more likely to produce the mutations that would let them eat it than were bacteria that were happily growing. But there were a number of problems with this. For example, it was not shown that the mutations were specific - dying bacteria may simply produce more mutations generally, not just those enabling them to eat what is locally available. Also, the logic behind the experiments rested on the idea that the new mutation did not affect the ability of the bacteria to survive and reproduce in normal conditions, which may well be wrong.

"Directed mutation", then, fails to support the weight Goodwin wishes to place upon it. The same can be said of the dual claims that Neo-Darwinists can only address the problem of adaptation with naive and risible hand-waving, and that they cannot accommodate the effects of history; they can deal with both, using the comparative method. Darwin's theory was one of descent with modification - the descent corresponds to Goodwin's constraints, the modification corresponds to evolutionary change.

If a Neo-Darwinist wants to know, for instance, why some monkeys and apes have relatively large testes, and suspects that it may have something to do with the mating behaviour of females, she will first make a phylogeny - a family tree - of the species involved, probably using molecular methods. She will then record on the tree which species have females that mate with more than one male, and which species do not. By looking outside the species group to its nearest relatives, she will then deduce the ancestral state of the mating system when the group first evolved. She will then go through the tree, working out the most likely locations on the branches for the transitions, she will record whether testis size increased or decreased afterwards, and hence whether the mating system was a probable cause of the changes. This procedure acknowledges that testes size can depend both on history and on current circumstances.

Goodwin ends with a plea against social and economic misuse of genetic information. All of us, biologists and non-biologists alike, would vote against the fruits of the human genome product being denied to medical practice, and against the release of dangerous genetically modified organisms into nature. Neo-Darwinists are no exception.

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