Is Behe's experiment (evolving the bacterial flagellum) plausible in the lab?

Question

[Warning: this question is motivated by a prominent proponent of "intelligent design": Prof. Michael Behe. I'm not interested in debating creationism.]

According to Wikipedia^[1]:

In Darwin’s Black Box (Behe 1996) I claimed that the bacterial flagellum was irreducibly complex and so required deliberate intelligent design. The flip side of this claim is that the flagellum can’t be produced by natural selection acting on random mutation, or any other unintelligent process. To falsify such a claim, a scientist could go into the laboratory, place a bacterial species lacking a flagellum under some selective pressure (for mobility, say), grow it for ten thousand generations, and see if a flagellum--or any equally complex system--was produced. If that happened, my claims would be neatly disproven.

[emphasis mine.]

As far as I can tell, nobody has actually performed this experiment (although, my literature search was not comprehensive, so it is possible I simply haven't found the appropriate publications). [However, there are arguments that the flagellum could have (or likely has) evolved from the type III secretory system, which shows similarity^[2].] This state of affairs strikes me as peculiar -- Behe's proposal sounds like an interesting experiment to perform (even disregarding any external debate).

Question: Is the experiment proposed by Behe (or another experiment in the same spirit) plausible to implement in a laboratory experiment?

Experiments reproducing steps in evolution seem to turn out much easier than I would have expected a priori, e.g. reproductive isolation of fruit flies^[3], experimental evolution of multicellularity^[4], so perhaps Behe's experiment would also be surprisingly easy to implement.

References:

1. Wikipedia: Michael Behe

2. Blocker A, Komoriya K, Aizawa S-I. 2003. Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proceedings of the National Academy of Sciences of the United States of America 100: 3027–30.

3. Dodd DMB. 1989. Reproductive Isolation as a Consequence of Adaptive Divergence in Drosophila pseudoobscura. Evolution 43: 1308.

4. Ratcliff WC, Denison RF, Borrello M, Travisano M. 2012. Experimental evolution of multicellularity. Proceedings of the National Academy of Sciences of the United States of America 109: 1595–600.

Answer 1

The experiment itself is technically feasible - but whether there is any point (as opposed to using the resources to perform a different experiment) is highly questionable. The problem is this: Behe's claim is that the mechanism is irreducibly complex, and that it could not have arisen by natural selection. This is theoretically falsifiable, but the experiment he proposed does not provide a good dichotomy - there is a very large chance that he is wrong but over the experimental term of 10,000 or 10,000,000 generations, the flagellum might not arise.

The absence of the flagellum in the experiment is the most likely scenario, and doesn't either support or falsify his claim. It took evolutionary time, something on the order of 10¹⁰⁺ generations, to arise the first time (according to the consensus claim); we could not expect similar complexity to arise for the same purpose under conditions of directed evolution. That's a terrible experimental design: huge resource input, huge likelihood of no result.

To be clear: it is technically feasible, but not a good experiment. He proposed it because he knew that nobody would do it (because it's a bad idea).

Answer 2

You may be interested in this paper and a video that summarizes it. It seems to be made quite clear that 1) effectively all of the parts of the flagellum are not original to it, and 2) there is a reasonable evolutionary path (one involving only increment/refine steps) that could have been responsible for it.

The video mentions but doesn't describe experiments that were in support of the proposed model. I assume they might involve refinement or statistical issues of the environment, not the whole-thing-at-once as Behe outlines. Obviously, if you can show that each step is independently adaptive, then the whole chain is shown to be possible evolutionarily, without trying to set up an experiment where you win the lottery n times simultaneously.

Personally I think the fact that the most awesome thing about the flagellum -- the rotation -- already exists in ATP synthase steals a lot of the flagellum's thunder. :)

Edit (Douglas S. Stones): Following the above references led me to this paper:

M.J. Pallen, N.J. Matzke "From The Origin of Species to the origin of bacterial flagella" Nature Reviews Microbiology 4 (2006), 784-790. (pdf)

In this article the authors discuss the possibility of designing a lab experiment to reproduce (steps of) the evolution of the flagellum.

Scott Minnich speculated in his testimony that studies on flagellar evolution need not be restricted to sequence analysis or theoretical models, but that instead this topic could become the subject of laboratory-based experimental studies. But obviously, one cannot model millions of years of evolution in a few weeks or months.

So how might such studies be conducted? One option might be to look back in time. It is feasible to use phylogenetic analyses to reconstruct plausible ancestral sequences of modern-day proteins, and then synthesize and investigate these ancestral proteins. Proof of principle for this approach has already been demonstrated on several NF proteins[69–75]. Similar studies could recreate plausible ancestors for various flagellar components (for example, the common ancestor of flagellins and HAP3 proteins). These proteins could then be reproduced in the laboratory in order to examine their properties (for example, how well they self-assemble into filaments and what those filaments look like).

An alternative, more radical, option would be to model flagellar evolution prospectively, for example, by creating random or minimally constrained libraries and then iteratively selecting proteins that assemble into ever more sophisticated artificial analogues of the flagellar filament.

Another experimental option might be to investigate the environmental conditions that favour or disfavour bacterial motility. The fundamental physics involved (diffusion due to Brownian motion) is mathematically tractable, and has already been used to predict, for example, that powered motility is useless in very small bacteria[76,77].

[For readability, I've added some line breaks to the above. There's too many cited references to list them all.]

Answer 3

[I'm answering my own question, but this seems too important not to include as an answer.]

A long-term E. coli evolution experiment (Wikipedia) was begun in February 1988 by Richard Lenski. He took 12 initially identical populations of Escherichia coli, and let them grow, having now completed over 50,000 generations.

One striking observation made through this research, is that one sample of E. coli evolved the ability to metabolise citrate, which took over 30,000 generations (see Blount, Borland, Lenski, "Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli" PNAS (2008)). This evolutionary step was achieved in a glucose-limited medium, thereby adding evolutionary pressure. Moreover, their results suggest that a necessary "potentiating change" occurred at around 20,000 generations.

These results demonstrate that significant evolutionary change is possible to observe in the laboratory, and gives a feel for how long it might take for something as complicated as the flagellum.