What you didn't know about evo-devo

The field of evolutionary developmental (evo-devo) biology is populated with scientists from diverse disciplines who are seeking the answers to questions that have been asked for millennia: why do organisms look different,how are these organisms built, are there common themes to how they are built,are there rules governing the evolution of organismal form? The surprise of evo-devo over the last few decades is that a reductionist approach, molecular developmental genetics, has repeatedly determined that the same genes are involved in building divergent organisms. One might decide therefore that morphological evolution is now understood: it is `simply' the evolution of regulation of a conserved `tool box' of genes combined with rare but important events like gene duplication and changes in protein function. It is easy to get caught up in recent progress towards explaining diversity at the molecular level, and to forget, therefore, how much of diversity remains unexplained and how instead of answering many questions about biological diversity we have simply failed to recognize them as problems.

We should therefore welcome attempts to bring our attention to broader themes and overlooked issues. This is just what Alessandro Minelli attempts to do for macro-evolutionary questions in his recent book The Development of Animal Form: Ontogeny, Morphology, and Evolution. Minelli seeks a unification of evolutionary and developmental biology, and believes that this requires a philosophical shift by participants in evo-devo. He encourages workers to view the entire life cycle as development, not just the embryonic patterning phases, and to keep in mind that selection acts upon all these stages, not just upon the final adult form. This is a truism for evolutionary biologists, but perhaps a novel perspective for some developmental biologists. Minelli also questions the prevalence of what he calls `finalism' in developmental biology, or the idea that all of development is directed towards the goal of producing the adult form. He points out that we long ago shed the notion that animals evolve inexorably towards `higher' forms. Why haven`t developmental biologists recognized, therefore, that development is not goal directed? I`m not convinced that this analogy is apt and I`m also not convinced that such finalism is common in developmental biology. Open the pages of any developmental biology journal more or less at random and you will find research delving into the details of developmental mechanisms, often with little concern for the consequences for the adult phenotype. There may,however, be a grain of truth in Minelli's criticism. Evo-devo workers have been quick to infer organ homology from a few embryonic gene expression patterns. It is now clear that such comparisons, even when they involve more than just a few expression patterns, are fraught with difficulty, particularly when they are performed in the absence of phylogenetic information.

Minelli is also concerned that most of the experimental knowledge used to address evo-devo questions is derived from studies of a handful of model systems. There is, however, every indication that investigators will continue to expand the list of animals under study and that tools are being developed for functional assays in `non-model' organisms. So I view Minelli's concern as a short-term issue. Nonetheless, he points out a number of unusual phenomena in little-studied animals and these `exceptions' may provide key insights into the `rules' of evo-devo.

Minelli revisits several subjects he has published on elsewhere, including paramorphism (the idea that limbs are in some way homologous to the main anteroposterior body axis), and various concepts related to segmentation,including the idea that segments are not only made in different ways between taxa but also within a species. I found the chapter on segmentation the most frustrating because I could not get a clear grasp of how Minelli's concepts differed from our current understanding of segmentation in Drosophilaand vertebrates. Minelli introduces the concepts of holomeric segmentation,which produces `true' segments (eosegments), and meromeric segmentation, which produces segmentation within an eosegment. However, Minelli writes `This is not the place for reviewing in detail the mechanisms by which segments are made in annelids, arthropods, and vertebrates' (p. 195). Where is the place,then? What precisely is the relationship between the Drosophilasegmentation cascade, and eosegments and merosegments? This is an extreme example of Minelli's conversational tone. Those who already understand the molecular genetics of segmentation and the terminology associated with segmentation in comparative morphology may find gems in this chapter. The rest of us are left out in the cold. If Minelli wants evo-devo biologists –who traditionally have either a strong background in development or in evolutionary biology – to sit up and take notice, then he needs to make the connections more clearly.FIG1 

This is not a text for undergraduates, and I suspect that many readers,particularly those with poor training in either developmental biology or comparative zoology, will be lost in places. For example, Minelli refuses to explain many of the developmental arguments that require a thorough prior understanding of the contemporary development literature. He writes `There is no need to...explain the concept of the Hox code...or to discuss colinearity'(p. 47). Although most students trained in developmental biology won't need this explanation, most trained in evolutionary biology will. The reverse may be true for the comparative morphology terminology scattered throughout the book, although I fear that most students trained in contemporary evolutionary biology will be more familiar with models of linkage disequilibrium than with the terminology of comparative morphology (I speak from experience). The figures are poorly labeled and will confound those with a limited training in comparative morphology. I found a number of errors of citation for the literature I know, which made me wary of the remaining citations.

My overall impression of the book is that it is like having a conversation with the author. He touches upon many issues that he has clearly thought about deeply and scatters provocative ideas throughout the text. Every time I started getting lost in the ideas, he threw in a fascinating example; every time I lost track of the examples, he threw in a surprising idea. These ideas and examples are not always clearly connected and the arguments are not tightly argued, but the book wraps up with a satisfactory summary that, in my view, should have been the introduction. The book raises far more questions than it answers (I'm not sure it answers any), but that appears to have been Minelli's goal. For the prepared mind, and the mind prepared to focus on essentially macro-evolutionary issues, this is a worthwhile conversation with Minelli.