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On ultra-Darwinian, or even Weismannian principles, the genome you inherit is the one -- granted the shuffling that goes on during sex -- that you pass on to your offspring via your own genes in your gametes (or germ-cells). Materials for change are available only by courtesy of mutation in these genes.

Is this entirely true? Is there any way in which an individual's lifetime experience could affect the genes -- that is, could Lamarckian mechanisms apply to at least some aspect of evolution? This proposition, always attractive to anti-Darwinians, of course runs counter to Crick's Central Dogma, and strictly speaking the answer is surety 'No'. Yet there is mounting experimental evidence that among bacteria there can indeed be adaptive mutations -- that is, mutations in some sense directed by environmental conditions, so that they can occur under circumstances where they might contribute to the survival of the organism much more frequently than might be expected on a purely random basis. 9

The situation is more complex in multicellular eukaryotes, where replication entails not merely sex but, crucially, development. There are aspects of the developmental process which seem to leave some scope for adaptive, rather than chance mutations. Developmental biologists have wrestled with this question for decades. In a sense, the argument goes back to Darwin's resistance to the suggestion that evolution could proceed by leaps -- saltations -- much to the distress of many of his otherwise

enthusiastic followers, such as Francis

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Galton. In the 1930s, the evolutionary geneticist Richard Goldschmidt suggested that significant adaptive changes could occur by a process of pre-adaptation, the creation of what he called 'hopeful monsters' equipped with the mutations necessary for some appropriate substantial change, and awaiting the appropriate environmental circumstances to make the leap.

Goldschmidt's ideas have never won acceptance among evolutionists or geneticists, and an alternative way out of the dilemma was proposed by Conrad (Hal) Waddington, an Edinburgh-based theoretical biologist much influenced by the work of the Cambridge Theoretical Biology Club of the 1930s. He argued that developmental processes in multicellular organisms could help both direct and, as he put it, 'canalize', potentially favourable mutations. Waddington's ideas, focused through the organization of a series of highly influential conferences and published volumes through the 1960s, helped shape a new developmental perspective on evolutionary change. 10 Empirical evidence for such processes is hard to come by, but the Harvard developmental biologist John Tyler Bonner 11 has built on Waddington's ideas by pointing out that Weismann's barrier cannot be as fixed as ultra-Darwinism implies, for two main reasons. The first is rather subtle, and applies only to plants and a relatively limited group of small invertebrate organisms; the second is universal.

To deal with the subtle case first: the Weismannian principle is that, from the earliest stages of development, the gametes (Weismann's germplasm) are sequestered from the rest of the body (the soma), and hence cannot be influenced by factors which affect it. Bonner points out that, while this is generally true for more complex animals (meaning animals with greater numbers of distinct types of body cell), it is not true for plants, or for less complex animals such as the tiny pond-dwelling hydra. Like plant cells, the cells of the hydra retain the capacity either to differentiate into somatic cells, or to become sequestered as gametes, or to remain totipotent. Those cells which remain totipotent retain the prospect of becoming gametes after an indefinite number of cell divisions -- and this means that any genetic variation occurring during those divisions will be heritable ( Figure 8.1 ). Weismann's barrier does not apply.

Figure 8.1 Totipotency: how genetic variation can occur in cells beyond Weissmann's 'germplasm', as proposed by John Tyler Bonner. The original gamete (grey square) gives rise to stem cells (open ellipse) which can differentiate into functional somatic cells (hatched circles) or into gametes (grey circles). A mutation occurring in a stem cell (open lozenge) can thus give rise to a mutant germ line

cell (black circle).

Important as this argument is in breaking the dead grip of Weismannism, until recently it seemed not to apply to more complex animals. This assumption has been made increasingly doubtful by recent

advances in gene technology, however. In 1996 an Edinburghbased team directed by Ian Wilmut succeeded in cloning sheep from embryonic cells, and the following year announced in a paper in Nature 12 which attracted world-wide attention, that they had performed the same operation using DNA extracted from cells obtained from the udder of an adult sheep. The ethical issues and media concern raised by this experiment are not of direct concern to me here; the relevant point from the perspective of the argument in this chapter is that adult sheep DNA and the cells from which it is derived remain totipotent. Weismann's barrier is well and truly breached.

However, there is another, more universal issue to which Bonner points, drawing on earlier insights by the Scottish biologist and

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philosopher Lancelot Law Whyte, 13 who described what he called 'internal factors' in evolution. During development, originally totipotent cells divide, become determined and migrate to appropriate positions within the developing embryo. Migration, as discussed earlier, depends on complex factors including internal features of the cells themselves, the presence of appropriate tissues or surfaces over which they can move, information arriving in the form of secreted chemicals from their neighbours sharing the migratory journey, and 'trophic factors' diffusing out from their target organs and signalling the directions in which the migrant is to move.

This process has the consequence that a type of competitive/selective mechanism operates between cells within the developing organism itself. Many more cells are generated during embryogenesis than

ultimately survive. Those cells that fail to make the migratory journey adequately, or arrive too late, are lost; they will leave no progeny, no daughter cells. What determines success or failure in this migratory journey? Cooperative relations both among the migrating cells and between them and their target organs through their trophic secretions will be part of the mechanism. Contingency -- sheer accident -- may be another. But there may also be variations between the cells, making selection possible in the classical Darwinian sense, as already discussed in the context of Edelman's selection hypothesis. This developmental process, demanding what Bonner calls 'sound rules of construction', 14 must itself be subject to strong selection pressure, but will also constrain the final outcome, the mature,

reproductively competent phenotype. There should be nothing surprising about this. Any large organization has simultaneously to act as a coherent unit in its relations with the outside world, in cooperation and competition with its peers, while at the same time serving as the cockpit for the internal power struggles, the jostling for position, the personal ambitions, of its component members. Once again, this complexity is lost to the onedimensional world of ultra-Darwinism.

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