Sunday, December 31, 2006

The Three Domain Hypothesis (part 6)

[Part 1][Part 2][Part 3][Part 4][Part 5]

Evolving Biological Organization

Carl Woese discovered archaebacteria and he made them fit into a separate super-kingdom, or “domain.” He is the man behind the claim that archaebacteria are so different from other bacteria that they deserve equal taxonomic status with eukaryotes. Woese is the father of the Three Domain Hypothesis, which not only claims domain-level recognition for archaebacteria, but also claims that eukaryotes descend from a primitive archaebacterium.

Back in 1995, when evidence against the Three Domain Hypothesis was mounting, I made a bet with Steven LaBonne that Woese would recant by January 1997.

I lost that bet, but eight years later Woese has finally come to his senses ... at least partly ....

I’m reviewing articles that appeared in Microbial Phylogeny and Evolution edited by Jan Sapp. Carl Woese’s contribution (“Evolving Biological Organization”) describes his current thoughts about the emergence of defined species from the pool of primitive gene-swapping cells that characterized the early history of life.

Woese’s idea, which has been evolving of a period of ten years, is that primitive life existed as a community of cells that freely exchanged genes. They shared a basic translation system for making proteins, but had little else in common. These cells evolved as a community and not as distinct lineages.

Woese refers to this time as the “progenote era” where the word “progenote” refers to a cell that has not yet established a definite link between a stable genotype and a heritable phenotype. At some point in time, certain cells make the transition from progenote to the founders of a stable lineage. The transition point is known as the “Darwinian threshold.”
The real mystery, however, is how this incredibly simple, unsophisticated, imprecise communal progenote—cells with only ephemeral genealogical traces—evolved to become the complex, precise, integrated, individualized modern cells, which have stable genealogical records. This shift from a primitive genetic free-for-all to modern organisms must by all acounts have been one of the most profound happenings in the whole of evolutionary history. Although we do not yet understand it, the transition needs to be appropriately marked and named. “Darwinian threshold” (or “Darwinian Transition”) seems appropriate: crossing that threshold means entering a new stage, where organismal lineages and genealogies have meaning. where evolutionary descent is largely vertical, and where the evolutionary course can begin to be described by tree representation. (p. 109)
According to Woese, bacteria were the first species to emerge from the pool. From that point onwards, the evolution of bacteria was “Darwinian” and could be represented by a bifurcating tree.

What about archaebacteria and eukaryotes? They emerged later ...
At that point, though, both the archaeal and eukaryotic designs remain in the pre-Darwin progenote, condition: still heavily immersed in the universal HGT field, still in the throes of shaping major features of their representative designs; and so, their evolutions cannot be represented in tree form. In other words, the node in the conventional phylogenetic tree that denotes a common ancestor of the archaea and eukaryotes does not actually exist. The two cell designs are not specifically related; it is just that the tree representation made them “sisters by default.” (p.111)
Woese suggests that the archaebacteria were the next to cross the Darwinian threshold followed by eukaryotes. This explains why archaebacteria have simpler cell components and eukaryotes are more complex. (The precursors of the eukaryote lineage spent more time in the progenote era and accumulated more innovative structures, such as nuclear membranes.)

The progenote community may have spawned other “domains” but these are now extinct, although Woese suggests there are some clues pointing to their previous existence. I assume that the progenote community itself petered out shortly after the emergence of eukaryotes.

This new theory of Woese is not very satisfying. I find the explanation somewhat confusing. Woese is trying to preserve the distinctiveness of the Three Domains while denying that their relationship can be discerned. In other words, he wants to have his cake and eat it too.

In order to defend the monophyletic domains, especially archaebacteria, he has to postulate that each one descends from a single cell, or lineage, that pops out of the progenote community. That’s why each domain has a defined root (i.e. monophyletic). But in order to account for the massive amounts of data that show eukaryotes closer to bacteria than to archaebacteria, he postulates an extended period of evolution where cells exchanged genes in a communal pool. This is not unlike the ideas of many other workers in the field except that for Woese it represents a denial of one of the basic tenets of the original Three Domain Hypothesis.

Woese is very clear about this. He makes the case that the branches at the base of the ribosomal RNA tree are not meaningful. It is wrong to assume that archaebacteria and eukaryotes share a common ancestor. I’ll close this part with an extended quote from Woese to show you just how far he’s willing to go to make the case. (Note how much he has come to agree with people like Ford Doolittle [Part 5] who have been challenging the Three Domain Hypothesis for over a decade.)
Classical biology has also saddled us with the phylogenetic tree, an image the biologist invests with a deep and totally unwarranted significance. The tree is no more than a representational device, but to the biologist it is some God-given truth. Thus, for example, we agonize over how the tree can accommodate horizontal gene transfer events, when it should simply be a matter of when (and to what extent) the evolution course can be usefully represented by a tree diagram. Evolution defines the tree, not the reverse. Tree imagery has locked the biologist into a restricted way of looking at ancestors. It is the tree image, almost certainly, that has caused us to turn Darwin’s conjecture that all organisms might have descended from a simple primordial form into doctrine: the doctrine of common descent. As we shall discuss below, it is also the tree image that has caused biologists (incorrectly) to take the archaea and the eukaryotes to be sister lineages. Much of the current “discussion/debate” about the evolutionary course is couched in the shallow but colorful and cathected rhetoric of “shaking,” “rerooting,” “uprooting,” or “chopping down” the universal phylogenetic tree. (p.102)

Microbobial Phylogeny and Evolution: Concepts and Controversies Jan Sapp, ed., Oxford University Press, Oxford UK (2005)

Jan Sapp The Bacterium’s Place in Nature

Norman Pace The Large-Scale Structure of the Tree of Life.

Woflgang Ludwig and Karl-Heinz Schleifer The Molecular Phylogeny of Bacteria Based on Conserved Genes.

Carl Woese Evolving Biological Organization.

W. Ford Doolittle If the Tree of Life Fell, Would it Make a Sound?.

William Martin Woe Is the Tree of Life.

Radhey Gupta Molecular Sequences and the Early History of Life.

C. G. Kurland Paradigm Lost.

1 comment:

  1. Woese's latest theory doesn't make sense because bacteria still use lateral transfer as a way to acquire new genes. I don't know about archaebacteria but I'd bet the same. I know multicellular eukaryotes swap genes rarely, don't know about protists