Searching for the Devil

This is a beautifully written philosophical book on the nature of the developmental process, and on both past and current thinking about its relationship with evolution. I would urge all developmental and evolutionary biologists to read it. You will probably find, as I did, that there are some things you agree with and some that you don't. But of course,'twas ever thus.

I'll start with the things that I liked. Jason Scott Robert is enthusiastic about the new `evo-devo' approach, and he emphasizes its philosophical significance, rather than its minutiae. In particular, he notes the possibility that development may `bias' (p. 32) or `drive' (pp. 101-102) evolution in particular directions – something that I have long felt to be important(Arthur, 2004). However, he also draws attention to `developmental systems theory' (DST), the existence of which had entirely escaped me, as it seems to have been a story told largely in the philosophical, rather than the biological, literature (not that this is any excuse for my having missed it). In particular, Robert focuses on the work of Oyama [(Oyama, 1985) and subsequent publications]. The main difference between DST and evo-devo,according to Robert, is that the former adopts a holistic stance in which genes are simply some of the players in a very multifactorial process, whereas much evo-devo is centred on comparisons of gene expression patterns between different taxa, and so tends to emphasize the roles of genes above those of the other players in the developmental game. I'm sure there's some truth in this contrast, although my own view of evo-devo is that it is also a holistic endeavour. But in any event, I entirely agree with one of Robert's closing comments – that `evolutionary developmental biologists and developmental systems theorists would do well to interact with each other in establishing a genuinely synthetic biology' (p. 130).

And so to the location of the Devil. Robert's final chapter is entitled`The Devil is in the Gestalt'. By this, he means that it is in the flavour of the whole, and not in the detail, where the Devil is proverbially to be found. The particular devil to which Robert is alluding is that of actual, or apparent, disagreement between different camps on the nature of the relationship between development and evolution. And I believe that he's right in his identification of its location. Few if any evo-devo folk would deny the importance of population processes, such as changing gene frequencies, in evolution (though of course they do rebel against the excesses of some neo-Darwinians, such as those who define evolution as changes in gene frequency). Equally, few, if any, of the more enlightened wing of neo-Darwinism (such as quantitative geneticists) would now deny the possibility that development may indeed often `drive' or `bias' evolution in certain directions. But the emphases of the two endeavours are still much more different than they should be. I think this is a case of the need to discard historical baggage, and I believe that Robert's book will help to achieve this.

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Finally (in terms of my likes), the book is not only well written but also well structured, with `summaries of the argument so far' available at sensible places, just when you feel the need for them. It also has a certain humility of style that is endearing. At one point (p. 90), Robert goes so far as to contemplate the possibility that his book might be considered to be `verbal gymnastics' that are `utterly useless to practicing biologists'. Of course, he doesn't really believe this is true, and neither do I. It is entirely sensible, even perhaps necessary, for practising biologists to stand back from the individual trees from time to time, and to reconsider the nature of the wood.

Now for the things I didn't like. There are just two of these, but they're both important, one from a scientific and one from a historical perspective. I'll discuss them in that order.

In his favouring of a holistic stance, Robert sometimes goes too far. In trying to correct what he sees as an overplaying of the role of genes, he sometimes comes across as not being balanced but rather as being equally unbalanced – in the opposite direction – as the folk he criticizes as being too pro-gene. So, he sometimes seems almost anti-gene, and,associated with this, anti-genetic programme For example, he states that `we don't need genetic programmes or instructions, or even specifically genetic information, in order to understand and explain the developmental effects or evolutionary significance of genes' (p. 31).

Now this is one of the craziest statements in a generally sane book, and I suspect it is one that the author himself, in retrospect, might feel slightly uneasy about. But his dislike for genetic programmes re-surfaces all over the place, usually in less extreme forms. For example, in the context of a reference to the work of Keller [(Keller,2001) and others], he states (p. 86) that `the genome does not itself contain or comprise a programme for development'. I have mixed feelings about this. If he simply means that epigenetic and environmental factors also influence the course of development, then I (and probably everyone) would agree. However, I have tended to think of development as an interplay between a genetic programme and an epigenetic programme, with that interplay itself being potentially altered by many environmental variables(Arthur, 2004). So in my view,the idea of a genetic programme, if used broadly, is entirely compatible,rather than at odds, with a holistic view of development. This train of thought leads inexorably to a crucial question: exactly what is meant by a`programme'? I was hoping that Robert would devote a substantial block of text to this issue (in the same way that he does for the meaning of modularity on pp. 122-124), but I was disappointed to find that he did not.

Now to my historical gripe, which concerns our current interpretation of the work of Haeckel. Robert re-iterates the view of some other recent authors that `according to Haeckel, the ancestral stages of adults could be identified in the embryos of descendants' (p. 94). He refers to Hall(Hall, 1999) here rather than to any of Haeckel's works. Personally, I don't buy this argument. Although Haeckel may have thought that `higher' vertebrate embryos pass through, for example, a `molluscan' stage, did he really think that they resemble adult molluscs? If so, which ones? Perhaps a garden snail or an octopus? Surely not. It is clear from some of Haeckel's later work that he did not think in this way at that stage of his life. I will only be persuaded that he thought in this way at an earlier stage if someone can come up with a specific quotation to that effect. Meanwhile, anyone interested in this issue should consult Sander (Sander, 2002).

In conclusion, I liked more than I disliked Robert's book. And I think its main virtue is to force readers to reflect on where theoretical biology in general, and evo-devo in particular, are going, both philosophically and scientifically. Such reflection is all the more necessary in these pressured times, when many biologists feel forced to concentrate on the latest-emerging details in their own particular neck of the woods, in order to keep sufficiently up to date to get that next grant. Of course, without research funds, few of the details that ultimately accumulate to give us something substantial enough on which to reflect would be discovered. So, like much in life, it is all a question of balance. Despite some ups and downs along the way, on reaching the final page I felt that I had become better balanced than I had been before beginning this interesting book.