Beyond Darwin – towards an inclusive evolutionary synthesis

What is the main driving force of evolution? What determines the direction of evolutionary change? What causes novelties to arise? During most of the last century, these questions have been addressed by evolutionary biologists and the answer they have come up with is well known, not only to biologists:it's natural selection. In his latest book, Wallace Arthur forces us to re-think. He claims that besides natural selection, there is embryological development as a second major player determining the direction of evolutionary change.

Biased Embryos and Evolution is a short book, which is easy to read and aimed at both biologists and general readers. Although laid out in 17 chapters, it has a straightforward, if provocative, message: `natural selection is not the main orienting agent of evolution, as Darwin claimed. Rather, it is one partner in an interacting duo'. Arthur claims that developmental bias, `the tendency of the developmental system of a creature to produce variant trajectories in some directions more readily than others, is a second major agent of evolution'. He starts his argument by summarizing textbook thinking in developmental biology, evolutionary biology and the history of life. But already in the first part of the book, he sets the stage for his provocative statement by highlighting the limitations of the modern synthesis. Arthur argues that the contributions of Fisher, Haldane, Wright,Dobzhansky, Mayr, Ford and Simpson were all correct and important, but what followed was often an `arrogance about the synthesis that was entirely absent from Darwin's beautiful book'. The importance of mutations that affect the development and, ultimately, the morphology of an organism has been largely ignored in the modern synthesis. Therefore, it is more than logical that one of the central chapters of Arthur's book is entitled `The Return of the Organism'. What follows is an excellent account of how development influences evolution and how developmental biology can influence evolutionary theory.

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Evolutionary change has three major components: mutation, which acts at the level of the gene; natural selection, which acts at the level of the population; and developmental reprogramming, which acts at the level of the organism. Arthur uses `developmental reprogramming' as an umbrella term to describe the many ways in which mutations can affect the timing(heterochrony), the spacing (heterotopy), the quantity (heterometry) or the quality (heterotypy) of developmental processes. It is at this point, at the latest, that it becomes clear that when Arthur talks about the `organism', he mostly means the development of the individual. Molecular changes brought about by mutations affect developmental processes, cause developmental reprogramming, and thereby generate developmental and morphological novelty. Although we are far from having a full account of developmental reprogramming between, and within, any major groups of animals or plants, there are many case studies on their way that will ultimately provide fresh data to support this theoretical assumption. At the same time, the scarce data already available clearly support the importance of incorporating developmental thinking into evolutionary theory.

And here it comes: the book is neither unique nor novel in its attempt to postulate a closer interdependence between evolution and development –this theory is already at the heart of evolutionary developmental biology and several books and even more reviews have been written on this topic. What is novel, and what is only superficially discussed in the last paragraphs of original evo-devo research papers, is the way in which development can influence the direction of evolutionary change. This is what Arthur calls`developmental bias', and what Gould, Lewontin and others have termed`developmental constraints' in former times. Arthur makes a significant contribution to this debate by claiming that one of the reasons for the limited acceptance of the term `developmental constraint' is its negative touch. He argues that `development biases evolutionary directions in both positive (drive) and negative (constraint) ways'. Thus, the internal factors in evolution, the genome and the developmental program on which mutations act,can have a positive or a negative effect. They make some changes more likely than others, and thereby are important components in the evolutionary game. There is no doubt that these considerations and the growing knowledge in the field of evo-devo have to be incorporated in an `inclusive' evolutionary synthesis.

`So what?', the evo-devo folks will ask. We all agree on this, and many of us express it one way or the other in our papers. However, even if this thinking is common, original research papers never provide the space for developing this idea all the way through. Wallace Arthur has taken the time and energy to write a book to precisely drive home that point. In order to do that, he had to criticize `neo-Darwinian' thinking, which he did in a balanced way, while still getting across the important point of the `incompleteness' of the modern synthesis. Even if some people might not like this style, I believe he deserves credit for doing it the way he did. The book is therefore not just another addition to the long list of monographic evo-devo texts. Arthur has a novel and important point. His argument is short and precise. He does his readers, but mostly himself, the favor of driving this point home straight. The style of the book is entertaining and light-hearted, and includes some gossip, which makes it even more rewarding for the non-specialist.

In conclusion, I highly recommend Arthur's book to all fellows of developmental and evolutionary biology. Not that they will learn from it new details in evo-devo, that is not the aim of the book, and Arthur was well-advised in not even trying to persuade the reader with case studies in order to make his argument. Rather, he urges us (in particular the evolutionary biologists) to be open-minded and to accept the concept of`developmental bias' as a major addition to the evolutionary synthesis. The time was ripe for a distinguished fellow – such as Wallace Arthur– to make the claim that embryological development can make a specific contribution to evolutionary theory, and that without it the `modern'synthesis cannot be complete. If the book can persuade evolutionary biologists to embrace its central message as whole-heartedly as the evo-devo crowd surely will, it will have served its purpose. Hopefully they'll read and re-think.