AN INDIRECT ROUTE
Some evolutionary biologists like Richard Dawkins have fertile imaginations. Given a starting point, they almost always can spin a story to get to any biological structure you wish. The talent can be valuable, but it is a two-edged sword. Although they might think of possible evolutionary routes other people overlook, they also tend to ignore details and roadblocks that would trip up their scenarios. Science, however, cannot ultimately ignore relevant details, and at the molecular level all the details become critical. If a molecule nut or bolt is missing, then the whole system can crash. Because the cilium is irreducibly complex, no direct, gradual route leads to its production. So an evolutionary story for the cilium must envision a circuitous route, perhaps adapting parts that were originally used for other purposes. Lets try, then, to imagine a plausible indirect route to a cilium using pre-existing parts of the cell.
To begin, microtubules occur in many cells and are usually used as mere structural supports, like girders, to prop up cell shape. Furthermore, motor proteins also are involved in other cell functions, such as transporting cargo from one end of the cell to another. The motor proteins are known to travel along microtubules, using them as little highways to get from one point to another. An indirect evolutionary argument might suggest that at some point several microtubules stuck together, maybe to reinforce some particular cell shape. After that, a motor protein that normally traveled on microtubules might have accidentally acquired the ability to push two neighboring microtubules, causing a slight bending motion that somehow helped the organism to survive. Further small improvements gradually produced the cilium we find in modern cells.
Intriguing as this scenario may sound, though, critical details are overlooked. The question we must ask of this indirect scenario is one for which many evolutionary biologists have little patience: but how exactly?
For example, suppose you wanted to make a mousetrap. In your garage you might have a piece of wood from an old Popsicle stick (for the platform), a spring from an old wind-up clock, a piece of metal (for the hammer) in the form of a crowbar, a darning needle for the holding bar, and a bottle cap that you fancy to use as a catch. But these pieces couldnt form a functioning mousetrap without extensive modification, and while the modification was going on, they would be unable to work as a mousetrap. Their previous functions make them ill-suited for virtually any new role as part of a complex system.
In the case of the cilium, there are analogous problems. The mutated protein that accidentally stuck to microtubules would block their function as highways for transport. A protein that indiscriminately bound microtubules would disrupt the cells shape just as a buildings shape would be disrupted by an erroneously placed cable that accidentally pulled together girders supporting the building. A linker that strengthened microtubule bundles for structural support would tend to make them inflexible, unlike the flexible linker nexin. An unregulated protein, freshly binding to microtubules, would push apart microtubules that should be close together. The incipient cilium would not be at the cell surface. If it were not at the cell surface, then internal beating could disrupt the cell; but even if it were at the cell surface, the number of motor proteins would probably not be enough to move the cilium. And even if the cilium moved, an awkward stroke would not necessarily move the cell. And if the cell did move, it would be an unregulated motion using energy and not corresponding to any need of the cell. A hundred other difficulties would have to be overcome before an incipient cilium would be an improvement to a cell. (Michael J. Behe, Darwins Black Box: The Biochemical Challenge to Evolution, Free Press, 1996, p65-67)
