Compartments

The development of a single cell into a complex creature such as you or me is almost miraculous. Early scientists were so baffled by this process that some supposed that the fertilized egg might contain a complete specification of the final organism.

This is just silly.

Still, it has only been in the last few decades that researchers have worked out how a smooth starting pattern in the concentrations of a few molecules develops into a complex, highly structured pattern. These molecules act as transcription factors that modify the activity of genes making dozens of other transcription factors, which spontaneously form patterns that serve as the invisible framework driving all subsequent development. The essence of this understanding is described in the charming 2006 book Coming to Life: How Genes Drive Development by Christiane Nüsslein-Volhard, who shared a Nobel Prize for her germinal work on the development of the fruit fly, Drosophila melanogaster.

A central part of this view is that different regions of the developing embryo are uniquely identified by the particular combination of transcription factor concentrations they contain. Each combination (influenced in part by its neighbors) stimulates the cells in that local region, or "compartment," to develop toward a particular final structure, such as the hindmost edge of a wing. Mutated animals that are missing the genes for particular factors develop characteristic problems, like extra wings or legs sprouting where their antennae should be. Researchers have also learned how to label the molecules with fluorescent dies that directly reveals the invisible patterns of factors that drive later development.

In their book The Plausibility of Life, Marc Kirschner and John Gerhart include developmental compartments as one of the key elements, along with weakly-linked modules and exploratory behavior, of "facilitated variation": the ability of organisms to respond to small genetic changes with large but viable changes in their structure.

Compartmentalization is in some ways similar to exploratory behavior, in which developing body structures such as blood vessels respond to local stimuli such as chemicals emitted by oxygen-starved cells. In both cases, individual cells respond to nearby cues, without needing to refer to some master plan. In the case of compartmentalization, however, both the cues and responses are more general chemical changes, in contrast to the more apparent structural changes seen in exploratory development.

What the two processes have in common is that they allow development that is flexible enough to succeed in diverse situations, for example when nutrients are scarce or the embryo is damaged. This sort of robustness presents a clear evolutionary advantage, since it makes it more likely that a complex organism will grow up and survive to reproduce.

But in addition, robust development lets organisms deal with genetic changes. Although many mutations are fatal, some cause dramatic changes in body organization or other features, while the flexible development process adapts to the new situation. As a result of this facilitated variation, evolution is able to explore a wider variety of strategies and move quickly to new solutions.

For Kirschner and Gerhart, this flexibility is key to understanding the nature and rapidity of evolution. A population can explore the potential advantage of a longer hindlimb, for example, without the need to separately coordinate changes in bone, muscle, blood vessels, nerves, and so forth. Adaptive development takes care of all that.

In fact, the pattern of compartmentalization appears to have been much more stable over the course of evolution than the details of body structure have been. The appearance of compartmentalization and the other features that allow facilitated variation look like the crucial revolutionary events that made rapid evolutionary change possible.