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MARGINALIA

The Biology of What Is Not There

Is it only natural selection that guides the shapes seen in nature?

Robert L. Dorit

Invoking Selection

The temptation to attribute the occupancy of shape space to the action of natural selection is almost irresistible. In this optimalist light, the occupancy problem is easily dismissed: What is there is what works; what is not, doesn’t. Yet this easy solution may be based on a set of problematic assumptions. To be sure, the objects of the real world—shell shapes in our example—do function effectively in their environment, or natural selection would have made short work of them. The nautilus shell is a stunning example of how propulsion and buoyancy can be elegantly balanced, and biologists and naval engineers alike justly admire its shape. The barnacle shell has indeed evolved a shape that enables its tenant to survive the pounding of the waves, and the rising and falling of the tides. But the fact that natural selection acts incessantly to shape the natural world does not mean that anything that we do not see has been tested by natural selection and found wanting. What that formulation assumes is that every corner of shape space is accessible, that every conceivable shape in our cube has in fact been tried—which is to assume too much.

Evolutionary theory, especially in its Anglo-American formulation, has traditionally favored the idea of natural selection as the driving force that shapes living form. Natural selection is indeed a powerful chisel, but a complete theory of evolution also needs to take into account the material being chiseled. The occupancy riddle will not be solved until we think about how organisms are actually built, and until we give history its proper due as an architect of form.

Constructionist explanations for the occupancy of shape space acknowledge that not all corners of shape space are equally accessible. Under this rubric, the occupancy of shape space derives (at least in part) from the consequences of how biological forms are constructed. Organisms have ontogenies, and the way they develop from a fertilized single cell into a final adult form has implications for the resulting shape. Thus, to stay with our shell-shape example, it is unlikely, if not impossible, for the opening of the shell (where new material is deposited) to decrease in size as the animal matures. Organisms tend to get bigger as they mature. Even though it is possible to model a logarithmic spiral whose leading edge grows and then shrinks, that excursion in shape space appears to be inaccessible to real organisms. Importantly, this inaccessibility is not due to the fact that such a shape would not function and thus would be eliminated by natural selection. Instead, we do not see it as a realized shape because, given the rules that govern shell construction, it occupies forbidden territory. Given how shapes are made, certain among them cannot even show up to participate in the struggle for existence.

Proteins too have ontogenies, dictated by folding rules. And similar forbidden zones in shape space exist at the molecular level. Knots, for example, are notoriously scarce in proteins, for reasons that flow both from the chemical character of the amino-acid components of proteins and from the mechanisms that govern protein folding. (In the interest of full disclosure, I should note that until fairly recently we thought knots to be a virtually impossible geometry for real proteins to adopt. We were wrong. They are rare, but not impossible.)




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