Clarifying biotic homogenization.

nouns – ‘hierarchy’, ‘connec- tivity’, ‘evolvability’, ‘complexity’ to name four – are becoming increasingly popular as evolutionary developmental biology tries to find its theoretical feet. With Gerhard Schlosser, an amphibian developmental biologist, Gunter Wagner has brought together a stellar team of contributors to discuss the abstract noun du jour, ‘modularity.’ In Modularity in Development and Evolution, we can read contributions from 42 authors, many of them distinguished, about topics as diverse as basic helix– loop–helix transcription factors, data-mining genome- wide expression data, vertebrate limbs, nematode vulvas and Wolbachia symbionts. Unsurprisingly, all authors agree that modularity is very important to development. The question is: what do they mean? The answer is: many different things. The editors make a brave attempt to keep matters under control by defining modules as structures or processes composed of tightly integrated parts, whilst being relatively autonomous from their surroundings. For developmental geneticists, modules are thereforegroups ofproteins that worktogether tospecify cells [e.g. the Notch–Delta–Su(H), pathway]. For a quan- titative geneticist, modules can be seen in the distribution of the pleiotropic effects of quantitative trait loci, which control various morphological traits. Developmental neurobiolo- gists point to embryologically and functionally distinct units of the central nervous system, whereas a nematode geneticist points to cells. Bioinformaticists see modules in ‘synexpression groups’ – clusters of co-ordinately regulated genes visible from expression profiling studies; dynamic systems modelers see them as networks of genes necessary and sufficient for carrying out a particular function; a complexity theorist sees them in basins of attraction in random boolean networks. And this is only a partial list. The sheer ubiquity of modular things, whatever those happen to be, suggests that modules matter to development. Having said that, one has the feeling that many contributors are cherry-picking the data. They are looking for, and finding, modules whilst ignoring non-modules. The problem seems to be that the modularity of things is, as the editors point out, a matter of degree. However, there is no formal theory of modularity and, in the absence of that, no consensus about how to measure it. The result is that we are invariably given the history of a case rather than a sense of its distribution. This is a natural history of modules. What about their evolution? As with more mundane attributes that organisms might have, say, parental care or wings, evolutionary biologists want to know several things about them. Why do modules exist? Are they the result of natural selection? Or can mutation and drift explain their presence? If selection, what kind of selection? We also want know how they evolve. If a module is found in Caenor- habditis elegans, is it also found in another nematode species? A fruit-fly? Humans? Are modules more con- served than non-modules? Has modularity – like complex- ity – increased over the course of evolution? These are important but difficult questions, and the contributors give a diversity of answers. Taking the last set of questions first, (how do modules evolve), it seems that sophisticated comparative studies of the evolution of modules are some way off. This is not a criticism: such studies need lots of data, which hardly exist outside of a few model organisms – but they will surely come. Why do modules exist? Some contributors seem to view modularity asanemergentpropertyofgeneticnetworks.Otherssuggest that developmental modularity evolves for its variational properties – it enables organisms to be more resistant to environmentalormutationalperturbations.Thesplithereis analogous to the Wright–Fisher dispute over dominance. Others again, suggest that modules permit evolvability (i.e. the production of heritable, selectable, phenotypic variation). This is a clade-selection argument – with all the weaknesses of such arguments. Many contributors hedge their bets by citing some or all of the above without considering the matter too deeply. But more careful discussions can be found in at least two papers. Force, Cresko and Pickett argue that ‘genotypic modularity’ – the use of genes in particular places and times independently of other genes – can increase simply as a consequence of Corresponding author: Armand M. Leroi (a.leroi@ic.ac.uk). Update TRENDS in Ecology and Evolution Vol.19 No.6 June 2004 284 www.sciencedirect.com