References for Evolution of flagella

Note 1: Behe referenced this paper in Darwin's Black Box.
Note 2: Behe cites this on p. 279 as a 1986 paper. The volume was published in 1987 and is so listed in databases, but the meeting was in 1986, which is probably what Behe was thinking of.
Note 3: It is worth pointing out that this 1992 exchange between Cavalier-Smith and Margulis, described by Behe thusly: "Margulis and Cavalier-Smith have clashed in print in recent years6 [cites the 1992 papers]. Each points out the enormous problems with the other's model, and each is correct." (DBB, p. 69) -- had essentially nothing to do with the origin of the cilium. Cavalier-Smith's 15-page article was essentially entirely about protozoan taxonomy and how often well-accepted symbioses, like those of mitochondria and chloroplasts, had occurred (and he did criticize Margulis, and others, along these lines). Cavalier-Smith devotes only two sentences to commenting on Margulis' spirochete hypothesis, and these are merely to say that he won't be discussing it because he regards it an "implausible speculation". Margulis' brief reply (one and a half pages) is also mostly about taxonomy and symbiotic questions. She takes a few sentences to cite some of the evidence she thought supported the spirochete hypothesis (it was disconfirmed in the literature in following years), but she spends no time criticizing Cavalier-Smith's scenario. Critiques (in my opinion marginal) of Cavalier-Smith's earlier (1978 and 1982) papers can be found in Szathmary (1987) and Bermudes et al. (1987), but that same year Cavalier-Smith (1987b) revised his earlier model and integrated it with his larger work on the origin of eukaryotes. I have not found any critiques of Cavalier-Smith's (1987b) model, but in his 1992 (b) paper "Origin of the Cytoskeleton" Cavalier-Smith refers to his earlier work as the "classical" autogenous hypothesis. This (1992b) paper, not cited by Behe, is where one will find the actual detailed criticisms of Margulis' and Szathmary's models by Cavalier-Smith, which are in my opinion devastating, although documenting all of this will require quite a long review article.
Note 4: This book discusses the origin and evolution of numerous key systems in biology, from the origin of life, to eukaryote mitosis, meiosis, and sex, to multicellularity and sociality. It also includes a good discussion of the centriole and the possibilities for its replication and origin (which is closely tied to the same questions for the cilium), but the authors (early spirochete-hypothesis supporters, both) do little discussion and no defense of the spirochete hypothesis, and although they do cite Szathmary (1987), one gets the impression that they do not remain strong supporters. More importantly for Behe, the book even discusses the challenge of irreducible complexity on the very first page (p. 3, now displayed online at amazon.com), although the actual term is not used. This is yet another book that Behe should have found, especially since he mentions other work by both authors in DBB, and the book was preceded by numerous scientific articles by the authors, and particularly since Behe makes extragant, confident claims to the public about what books and articles do and do not exist.

Some references to the work of Cavalier-Smith and others on the origin of the cilium, cytoskeleton, and components thereof (and a few on related aspects of Cavalier-Smith's work on the origin of the cell)

Note 1: Behe referenced this paper in Darwin's Black Box.
Note 2: This 1987(c) article, "The simultaneous symbiotic origin of mitochondria, chloroplasts, and microbodies," is mentioned by Behe in footnote 4 of chapter 5 (DBB, p. 155, footnote on p. 281). Chapter 5 of DBB is on vesicular transport and protein translocation, and Behe says he found this article along with several others after failing to find anything via computer search: "Slogging through the literature the old-fashioned way turns up a few scattered papers that speculate on how gated transport between compartments of a eukaryotic cell might have developed [footnote 4 is here]." (Behe 1996, 114-115) Regarding vesicular transport, I have little knowledge of the subject so will refrain from judgement (but see note 3, below).
But returning to the cilium, the interesting point is that Behe -- if he looked up this Cavalier-Smith paper from pages 55-71 of volume 503 of Annals of the New York Academy of Sciences -- cannot have failed to notice Cavalier-Smith's other paper ("The origin of eukaryotic and archaebacterial cells", 1987b) in the same volume, on pages 17-54. And this paper updates Cavalier-Smith's 1978 and 1982 work on the evolutionary origin of the cilium, by placing the origin of the cilium in the context of the origin of eukaryote mitosis, explicitly deriving the cilium from the primitive mitotic spindle, which provides a base and nucleation center for the microtubules. This answers the "how did the microtubules get pointed perpendicular to the cell membrane" question Behe raises, as well as helps to explain the peculiar connections found in modern eukaryotes between the cilium, the centriole, and mitosis. Anyway, as I said this topic requires it's own large FAQ, but the point for now is that Behe should have mentioned Cavalier-Smith's work on the origin of the cilium after his 1978 paper.
Here is Cavalier-Smith's (1997) opinion on Behe's treatment of the cilium subject:

[W]hen criticizing existing evolutionary explanations, Behe uses intellectually dishonest double standards. He dismisses my first treatment of the origin of cilia2 [footnote 2: the 1978 paper] as non-quantitative and therefore 'utterly useless', and ignores my later work on the topic3,4 [these are the 1982 and 1987b papers, respectively]. But it does not worry him that his empty, religious notion of 'intelligent design' is equally non-quantitative; worse still, lacking in even qualitative detail of what did the designing, and how the hypothetical design was executed, it explains nothing. He states that 'if a theory claims to be able to explain some phenomenon but does not even generate an attempt at an explanation is should be banished' and 'without details, discussion is doomed to be unscientific and fruitless'. If he had applied these strictures to his panacea of 'intelligent design' we would have been spared this worthless book.

Note 3: This volume of the Cold Spring Harbor Symposia on Quantitative Biology is mentioned by Behe in DBB (p. 179). Of the articles in it, Behe says that about "two-thirds...are simply overviews of what was going on in the author's lab at the time, with little or no attempt to tie it into the theme of the book." Having looked at the volume, this alone is a highly debatable statement. But Behe continues: "Of the remaining papers, most are sequence analyses, and some are concerned with prebiotic chemistry or simple catalysts (not the complex machinery of known organisms)."
But strangely Behe failed to mention the 20-page article by Cavalier-Smith (1987a) on the origin of cells. The article addresses (among other things) the origin of protein translocation. Here is Cavalier-Smith's (1997) take on this situation (Ref 3 is Cavalier-Smith 1987b; Ref 7 is Cavalier-Smith 1987a, Ref 6 is Blobel 1980):

Behe, ignorant of much of the literature, claims that no scientist has ever discussed the origin of vesicle targeting (actually discussed in Ref. 3 [Cavalier-Smith, 1987b], not cited by Behe, though the most detailed one on the origin of eukaryotic biochemical properties) or protein translocation (see Refs 6 [Blobel, 1980, PNAS, v.77, 1496-1500] and 7 [Cavalier-Smith, 1987a]), the most detailed discussion of the origin of the most basic complex cellular biochemical properties, which he deceitfully ignored despite citing the volume containing it as 'evidence' that no paper has ever been published on the subject!). Maybe he did not want his readers to find the papers (Refs 3 and 7) that most clearly show how one can explain (in outline at least -- obviously they are not the final answer) the origins of complex biochemical and cellular structures in logical steps using mutation, selection and detailed phylogenetic arguments. His ignorant assumption that the origin of a protoSRP would have killed the cell is refuted by the absence of the translation arrest domain in the eubacterial signal recognition partical (SRP) RNA8 [Poritz, 1989, Cell, 4-6], which provides a simpler ancestor to the more complex archaebacterial/eukaryotic particle. The problem he raises [p. 112] for the origin of secreted eukaryotic glycoproteins is spurious, because the sugar must have been added to the protein on the non-cytosolic side of the membrane in the common ancestor of eukaryotes and archaebacteria, even before the ER (endoplasmic reticulum) evolved, since it is added thus at the archaebacterial cell surface, as any good biochemist should have known, even without reading my discussion of the origin of the ER (Ref. 3).

Notably, Behe also failed to mention two other papers in the very same volume as the Cavalier-Smith (1987a) paper in Cold Spring Harbor Symposia on Quantitative Biology. One is even by Russell Doolittle, on the evolution of vertebrate blood coagulation.
...all of which goes to show that Cavalier-Smith was not engaging in ad hominem when he wrote of Behe: "What is sad about this book is that the author thinks that he has something new to say and is contributing to science."

Not to pile things on, but upon discovering the foregoing I was inspired to double-check Behe's claims about how often the cilium papers Cavalier-Smith (1978) and Szathmary (1987) were cited in other papers. On page 69, Behe says "The scientific community at large has ignored both contributions; neither paper has been cited by other scientists more than a handful of times in the years since publication.7" Note 7 on page 280 reads, "A search of Science Citation Index shows that each paper receives an average of less than one citation per year."

Well, I don't know if Behe made a mistake or if the Science Citation Index was in 1995 just not adequate on these papers for some reason, but my search of the Science Citation Index Expanded (SCI-EXPANDED)--1945-present on the Web of Science, while it lists only six citations of Szathmary (1987), lists 53 citations of Cavalier-Smith (1978). Seven citations are from 1996-present (four of those being in other papers by Cavalier-Smith). For 1995 and before, this leaves 47 citations. Ten of these are in other papers Cavalier-Smith authored or co-authored, leaving 37 citations of Cavalier-Smith (1978) by papers not written by Cavalier-Smith. For those who are counting, that is 2.056 citations per year for the years 1978-1995 inclusive (and including 1978 is being generous to Behe), and while not an overwhelming number, (a) it is higher than "less than one citation per year" and (b) 37 citations (40 to present, and not counting several references in books that I know of) is frankly significantly more attention than the average scientific paper receives.

Out of curiosity, I performed the same search on Cavalier-Smith (1982) and got a result of zero citations. This is clearly a mistake, as not only does Cavalier-Smith reference his 1982 paper in several other papers, but a cursory manual search on Web of Science of the reference lists of other papers reveals that it is cited in (at least) Bermudes et al. (1994), Rizzotti (1995), and Thornhill and Ussery (2000). Obviously there is an error in the Science Citation Index record for the 1982 paper, a good demonstration of the potential risks of relying completely on computer searches.

Cavalier-Smith's 1975, 1987(a), 1987(b), and 1987(c) papers are listed as having 98, 41, 94, and 133 citations respectively, although it appears that self-citation occurs in proportions similar to the 1978 case (self-citation is common in scientific papers).

Finally, Cavalier-Smith recently (November 2001) published in the Journal of Molecular Evolution a long (40 pages, huge for a journal) comprehensive article on the origin of the first cells, a major update of his 1987(a) paper:

I attempt to sketch a unified picture of the origin of living organisms in their genetic, bioenergetic, and structural aspects. Only selection at a higher level than for individual selfish genes could power the cooperative macromolecular coevolution required for evolving the genetic code. The protein synthesis machinery is too complex to have evolved before membranes. Therefore a symbiosis of membranes, replicators, and catalysts probably mediated the origin of the code and the transition from a nucleic acid world of independent molecular replicators to a nucleic acid/protein/lipid world of reproducing organisms. Membranes initially functioned as supramolecular structures to which different replicators attached and were selected as a higher-level reproductive unit: the proto-organism. I discuss the roles of stereochemistry, gene divergence, codon capture, and selection in the code's origin. I argue that proteins were primarily structural not enzymatic and that the first biological membranes consisted of amphipathic peptidyl-tRNAs and prebiotic mixed lipids. The peptidyl-tRNAs functioned as genetically-specified lipid analogues with hydrophobic tails (ancestral signal peptides) and hydrophilic polynucleotide heads. Protoribosomes arose from two cooperating RNAs: peptidyl transferase (large subunit) and mRNA-binder (small subunit). Early proteins had a second key role: coupling energy flow to the phosphorylation of gene and peptide precursors, probably by lithophosphorylation by membrane-anchored kinases scavenging geothermal polyphosphate stocks. These key evolutionary steps probably occurred on the outer surface of an 'inside out-cell' or obcell, which evolved an unambiguous hydrophobic code with four prebiotic amino acids and proline, and initiation by isoleucine anticodon CAU; early proteins and nucleozymes were all membrane-attached. To improve replication, translation, and lithophosphorylation, hydrophilic substrate-binding and catalytic domains were later added to signal peptides, yielding a ten-acid doublet code. A primitive proto-ecology of molecular scavenging, parasitism, and predation evolved among obcells. I propose a new theory for the origin of the first cell: fusion of two cup-shaped obcells, or hemicells, to make a protocell with double envelope, internal genome and ribosomes, protocytosol, and periplasm. Only then did water-soluble enzymes, amino acid biosynthesis, and intermediary metabolism evolve in a concentrated autocatalytic internal cytosolic soup, causing 12 new amino acid assignments, termination, and rapid freezing of the 22-acid code. Anticodons were recruited sequentially: GNN, CNN, INN, and *UNN. CO2 fixation, photoreduction, and lipid synthesis probably evolved in the protocell before photophosphorylation. Signal recognition particles, chaperones, compartmented proteases, and peptidoglycan arose prior to the last common ancestor of life, a complex autotrophic, anaerobic green bacterium.

In this paper he repeatedly cites two additional recent papers:

...both of which came out in the International Journal of Systematic and Evolutionary Microbiology. Together these three papers constitute some 150 pages, and they serve as only the barest introduction to the topic of the origin of the three domains and their various biochemical systems. For more articles by Cavalier-Smith, click over to PubMed and search on "Cavalier-Smith". Be sure to click on "related articles" for topics you are interested in.

If you are looking for a single scientist to serve as the "Darwin of microbiology" as a counter to Mike "the Paley of microbiology" Behe, it would be Thomas Cavalier-Smith.

Some references on the high variability in the construction of the cilium ("the cilium" isn't IC, just a subset of its components), and on the evolution of the cilium in reference to Behe's arguments

Some web references on FtsZ-tubulin homology

Structure of the bacterial tubulin homolog FtsZ by Lowe and Amos

Tubulin-like protofilaments in Ca-induced FtsZ sheets by Lowe and Amos

Structure & function of homologous proteins tubulin and FtsZ -- some strong medical applications of this evolutionary deduction

Egelman EH (1998). "Tubulin family: kinship of key proteins across phylogenetic domains". Current Biology. 8 (8): R288–90. doi:10.1016/S0960-9822(98)70175-7. PMID 9550697. ((cite journal)): Unknown parameter |month= ignored (help)

Faguy DM, Doolittle WF (1998). "Cytoskeletal proteins: the evolution of cell division". Current Biology. 8 (10): R338–41. doi:10.1016/S0960-9822(98)70216-7. PMID 9601632. ((cite journal)): Unknown parameter |month= ignored (help)

Check out this phylogenetic tree of FtsZs.

(Cornelis and Gijsegem, 2000). So if the IDer did after all design the (eu)bacterial flagellum, we also have the IDer to thank for "front-loading" in the potential for some of the nastiest bacterial virulence systems, including those of Salmonella and Yersinia, the latter being better known as the Bubonic Plague or Black Death. Comparing the explanations given for the virulence of Yersinia between the medievals of the 14th century and the ID theorists of the 21st may be a worthwhile research project.

Two pages in the UCSD transport system database note that the flagellar motor proteins (MotA and MotB) are distant homologs of other bacterial membrane proteins (ExbB-ExbD).

For a few months, the Mot-Exb connection was an isolated mention on a webpage. But in October 2001, an article by Kojima and Blair in Biochemistry made it official. The abstract is here. In their conclusion, the authors write (see the article for a comparative graphic),

The occurrence of significant conformational change in the stator has implications not only for the present-day mechanism but also for the evolution of the flagellar motor. A membrane complex that undergoes proton-driven conformational changes could perform useful work in contexts other than (and simpler than) the flagellar motor, and ancestral forms of the MotA/MotB complex might have arisen independently of any part of the rotor. We queried the sequence database using the sequence of the best-conserved part of MotA (the segment containing membrane segments 3 and 4) from Aquifex aeolicus, a species whose lineage is deeply branched from other bacteria. In addition to the expected MotA homologues, the search returned a protein sequence from the archaeal species Methanobacterium thermoautotrophicum (protein MTH1022) that shows significant sequence similarity not only to MotA but also to the protein ExbB (Figure 9). ExbB is a cytoplasmic-membrane protein that functions in conjunction with ExbD, TonB, and outer-membrane receptors to drive active transport of certain essential nutrients across the outer membrane of Gram-negative bacteria. The energy for this transport comes from the proton gradient across the inner membrane. Thus, MotA and ExbB are both components of systems that tap the proton gradient to do work some distance away (at either the rotor-stator interface or the outer membrane; Figure 9).

Other features also point to a connection between the Mot and Exb systems. MotA functions in a complex with MotB, which as noted contains the critical residue Asp32 near the cytoplasmic end of its single membrane segment. ExbB functions in a complex with ExbD, which likewise has a single membrane segment with a critical Asp residue near its cytoplasmic end (Asp25 in ExbD of E. coli; ref 59). Although ExbB has only three membrane segments in contrast to the four in MotA, the membrane segments that show sequence similarity have the same topology. The protein TonB is also present in the complex with ExbB and ExbD (59, 60) and would provide an additional membrane segment to round out the topological correspondence (Figure 9). ExbB contains a well-conserved Pro residue (Pro141 in E. coli ExbB) that is the counterpart of Pro173 of MotA. Although MotB and ExbD do not share close sequence similarity apart from the critical Asp residue, in certain positions in the membrane segment the residues most common in MotB proteins are also common in ExbD proteins. Finally, like the MotA/MotB complex the ExbB/ExbD complex contains multiple copies of each protein (61). Together, these facts make a reasonable case for an evolutionary connection between the Mot proteins of the flagellar motor and the Exb proteins of outer-membrane transport (and by extension the TolQ/TolR proteins, which are related to ExbB/ExbD but whose functions are less understood).

...which appears to improve significantly on the situation as stated in Ian Musgrave's draft flagellum FAQ, "There is no apparent homolog of the motor (MotAB) in type III secretory systems."

For additional information on homologies see:

The UCSD page on The Type III (Virulence-related) Secretory Pathway (IIISP) Family

In addition, the ATPase involved in flagellar construction is thought to be homologous to this family. Rizzotti, in his (2000) book Early Evolution has cited this in his scenario for the origin of the bacterial flagellum from an F1F0 ATPase. In light of the other homologies mentioned here, this is very unlikely, although there may be a connection between the F1F0 ATPase and transport systems at some very remote level.

Discovery Institute fellow Scott Minnich recently (November 2000) spoke at the DI's "Science and Evidence for Design in the Universe" conference. The talk, "Flagella: Tails of Molecular Cooption", is available in audio format online, and includes the muddled reaction from the audience. Minnich raised the issue of Type III virulence systems, speaking of "malevolent design", and suggested "If we're going to use this [flagellum] as a designed system, we're going to have to use this [Type III virulence system] as well", and "In the original design, they [virulence factors] weren't involved. You can almost look at this type III system as a perversion." Compare to Kathryn Brown's introduction to a Yersinia article in Science, "Why, the people wondered? Was the Plague the work of an angry God? A medieval curse? As it happens, the real culprit was a tiny bacterium: Yersinia pestis." And of course its syringe-like, IC, "designed-looking" virulence system. According to ID, apparently the "angry God" and "bacterium" theory for The Plague aren't as mutually exclusive as one might think.

Some online articles on Type III transport virulence systems and flagella

Type III Protein Secretion Systems in Bacterial Pathogens of Animals and Plants by Christoph J. Hueck

Interactions of Salmonella with host cells: Encounters of the closest kind by Jorge Galan

Assembly and Function of Type III Secretory Systems by Cornelis and Gijsegem

Molecular Mechanisms of Bacterial Virulence: Type III Secretion and Pathogenicity Islands by Mecsas and Strauss. On the Center for Disease Control webpage.

Unlocking the Secrets of the Grim Reaper, by Kathryn Brown, introducing an article on Yersinia in Science.

For references and more info on the archaeal flagellum, see almost anything that Ken Jarrell has written, e.g. the articles linked from The Jarrell Laboratory hompage.

Also see this online version of "A twisted tale: the origin and evolution of motility and chemotaxis in prokaryotes", by Faguy and Jarrell

"Recent excitement about the Archaea", by Jarrell, in Bioscience

Finally, in a 1998 article by Bayley and Jarrell, they write,

We feel that the discoveries of archaeal flagella-related putative gene products with similarity to type IV pilus accessory proteins indicate that the archaeal flagella also share this common origin and have evolved it to function as the primary motility apparatus. Although the function of the common origin can only be speculated, this system must predate the last common ancestor of extant life. ("Further Evidence to Suggest That Archaeal Flagella Are Related to Bacterial Type IV Pili", Journal of Molecular Evolution, 46: 370-373, 1998)

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