In his generous review of Evolution in Four Dimensions, (1,2) the Editor agrees that the Modern Synthesis version of Darwinism is too narrow, but questions some of our evidence and conclusions about the occurrence of non-random mutations and the evolutionary significance of non-genetic heritable variation. He also questions the wisdom of burdening our arguments with the term ''Lamarckian''. We have recently discussed issues around the history and use of terms like Lamarckism, Neodarwinism, and Darwinism, (3) so we will not repeat this discussion here, but we do wish to make four other points.
The first is that a quotation from the book has been taken out of context. Our assertion (p. 319) that: ''Variation is often targeted, in the sense that it preferentially affects functions or activities that can make organisms better adapted to the environment in which they live'' refers to all sources of heritable variation. Contrary to what is said in the review, it is not a conclusion from our survey of variation in microbial DNA. We discussed the likelihood of directed variations in germline DNA in multicellular organisms (pp. 106 & 107), and came to the conclusion that it is probably very limited. As it happens, in the light of recent discoveries about non-random DNA changes in plants following hybridization (see articles in Biol J Linn Soc 82(4), 2004), we are now less sure about this conclusion.
Our second point concerns the frequency and importance of transgenerationally inherited epigenetic variants. Wilkins suggests that if epimutations are ''responsible for'' only 1/1000 of known morphological changes, and gene mutations are responsible for the rest, then epimutations are relatively unimportant. We think that by focussing on the end-product of evolutionary change, rather than the process, he is oversimplifying the problem. There is now a wealth of evidence, particularly from plants, that heritable epigenetic variants are not rare. ( 4) For example, they seem to be common and repeatable consequences of plant hybridization and polyploidization. We also know from work with transgenes that duplicated sequences are often subject to heritable epigenetic silencing. Even if an epigenetic mark just keeps a duplicate copy silent until it accumulates ''useful'' DNA changes, or it alters the ease with which a copy is turned on or off in certain tissues, its inheritance is probably crucial to the long-term divergence that results in two genes responsible for different structures or functions. One of our main arguments is that all types of heritable variation (genetic, epigenetic, behavioural and symbolic) must be considered when thinking about evolution, because they interact.