6/14/11 10:32 AMThe Biology of What Is Not There » American ScientistPage 1 of 2http://www.americanscientist.org/issues/id.11375,y.0,no.,content.true,page.1,css.print/issue.aspx
The Biology of What Is Not There
Is it only natural selection that guides the shapes seen in nature?
Robert L. Dorit
Understanding the living world seems challenge enough for biologists. Technological advances have produced a cascade of data—from detailed genomesequences to the sophisticated satellite imagery that documents the planet’s ecosystems—but our ability to make sense of these data still lags far behindtheir acquisition. With such a backlog, the idea that we might want to think about objects that are not real seems, frankly, capricious.Yet without thinking about life-forms that never were, we cannot fully understand the life forms that do exist. Questions about absence lie at the very coreof evolutionary biology: Is the living world we behold the only possible outcome of the evolutionary forces that produced it? Or can we imagine, instead,different unfoldings, of which this is but one? The one actual unfurling of the tree of life, of course, places restrictions on our capacity to address thisquestion. I would argue that there are nonetheless ways of posing such queries that may prove productive.
The most accessible example of how to examine the shapes of the possible comes from work on shell forms carried out inthe 1960s by American paleontologist David Raup and his collaborators
(see the first figure).
Shell shapes are beautiful; theyare also geometrically well behaved and can be described relatively easily in mathematical terms. The mathematical modelof shell shape, at its most basic, includes the rate at which a shell grows around its central axis, the rate at which itdescends down that same axis and the rate at which the shell opening expands as its architect grows. With these threeparameters we can depict a three-dimensional shape space: Any point in that space defines a single shell shape that may ormay not occur in the living world. Real shell-bearing organisms are varied, abundant both in the current biosphere and in thefossil record, and their shapes can be plotted onto the shape space we have defined. When we do so, the pattern is striking.Certain regions of the cube, shown in color, are densely occupied, but most of the cube is uninhabited.The challenge of understanding the distribution of biological objects in shape space thus consists of two separate, butinterrelated, problems. The first of these problems involves the definition of the space of possibilities. For snail shells, we arefortunate, because the shape is mathematically tractable (a logarithmic spiral is a reasonable first approximation). The shapealso involves a limited number of variables (in this case, three, which allows us to depict the space as a three-dimensionalcube). For other biological shapes at other scales, defining the shape space may be considerably more challenging. How, forinstance, do we define the space of all possible protein or RNA shapes? What mathematical expression will capture all of thepossible architectures of tree shape? Not only are these spaces likely to be of a higher dimensionality, making them harder to depict, but the underlyingmathematical function that can generate the shapes is likely to be far more complex.The second problem with understanding shape distributions involves mapping the real objects of the world onto the shape space that we have constructed—and then accounting for the distribution of these realized forms. And it is here that we find an astonishingly consistent result. In every case studied, thedistribution of realized shapes is nonisotropic: Some parts of the cube are densely populated with realized shapes, whereas others are virtually, if notentirely, empty. Such patterns in biology demand an explanation. What is this strange occupancy of shape space at all scales telling us about the forcesthat give form to the living world?
The temptation to attribute the occupancy of shape space to the action of natural selection is almost irresistible. In this optimalist light, the occupancyproblem 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 madeshort work of them. The nautilus shell is a stunning example of how propulsion and buoyancy can be elegantly balanced, and biologists and navalengineers alike justly admire its shape. The barnacle shell has indeed evolved a shape that enables its tenant to survive the pounding of the waves, andthe 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 donot see has been tested by natural selection and found wanting. What that formulation assumes is that every corner of shape space is accessible, thatevery 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 shapesliving 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, theoccupancy of shape space derives (at least in part) from the consequences of how biological forms are constructed. Organisms have ontogenies, and theway 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, itis 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 toget bigger as they mature. Even though it is possible to model a logarithmic spiral whose leading edge grows and then shrinks, that excursion in shapespace appears to be inaccessible to real organisms. Importantly, this inaccessibility is not due to the fact that such a shape would not function and thuswould be eliminated by natural selection. Instead, we do not see it as a realized shape because, given the rules that govern shell construction, it occupiesforbidden 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, arenotoriously scarce in proteins, for reasons that flow both from the chemical character of the amino-acid components of proteins and from the mechanismsthat govern protein folding. (In the interest of full disclosure, I should note that until fairly recently we thought knots to be a virtually impossible geometryfor real proteins to adopt. We were wrong. They are rare, but not impossible.)
Following the Rules