Trailblazing

What a piece of work is a man! For that matter, what an awesomely complex apparatus is any large organism, from a dog to dogwood!

But as we learn more about biology, our awe shifts from the intricate cellular arrangements in mature multicellular life to the ways these structures arise during development from simpler (but not simple) rules. Even if we can accept simple examples of self-organization, like the spontaneous arrangement of wind-blown sand into regular dunes, the self-assembly of living creatures seems to be a different scale of miracle. But researchers have repeatedly found that simple rules, in which cells respond to local cues like chemical concentrations and mechanical stresses, suffice to describe how various aspects of our complex bodies develop.

In The Plausibility of Life, Marc Kirschner and John Gerhart describe this rule-based strategy, which they call "exploratory behavior," as a very effective way for organisms to develop dependably in the face of unpredictable changes in their environment. But they go further, stressing that flexible, adaptive development speeds evolution by letting small genetic changes give rise to vastly different--but still viable--organisms. Exploratory behavior is thus a critical component of their concept of "facilitated variation."

As an illustration of rule-based organization, Kirschner and Gerhart review the foraging of ants. Steven Johnson described this and other examples in his thought-provoking 2002 book, Emergence. Simply by following local rules and responding to the scent trails left behind by their predecessors, individual ants join to form major thoroughfares between a food source and their nest. No master planner guides their motions.

Similarly, in a developing animal, some cells may find themselves far from the nearest blood vessel. In response to the lack of oxygen, they secrete chemicals that encourage the growth of new capillaries nearby. And in the brain, the intricate wiring of nerve cells is guided in part by signals that they receive and transmit during certain periods of development.

It really has to be this way. Although it's true--and amazing--that the 558 cells of the roundworm C. elegans take up pre-ordained positions in the final creature, the cells in much bigger creatures like us simply can't all have designated roles in the final organism. For one thing, there's just not enough information in our 20,000 or so genes to tell every cell where to go on some genetic master plan. Instead, each cell has to have a degree of autonomy in dealing with new situations. For example, if one of your legs is stunted early on, the muscles, nerves, blood vessels, and skin will all adapt to its new size, rather than blindly proceeding with some idealized plan. Even in C. elegans, the fixed cellular arrangement mostly results from such adaptive behavior of individual cells.

If you're still not convinced, think of the offspring of a bulldog and a Great Dane, which will have a facial and body structure unlike either of its parents. But we are not even surprised that the blood vessels and muscles will successfully adapt themselves to this completely novel shape.

It makes perfect sense that creatures that use this adaptive process in their development would be more successful during evolution.

But the reverse is also true: this flexibility makes evolutionary innovations much easier. The repurposing of mammalian digits for a dolphin's flipper, a horse's hoof, or a bat's wing is much faster if only a few genes have to change to determine the new shape, and the others adapt in parallel. In concert with modular organization, development that is built on exploratory principles is critical to letting evolution explore radically new architectures in response to small genetic changes.