Books et al.Microbiology

The Trouble with Trees

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Science  05 Feb 2010:
Vol. 327, Issue 5966, pp. 645-646
DOI: 10.1126/science.1185784

It has been said before, but it bears repeating: evolutionary biology has been developed, almost without exception “by sexually reproducing eukaryotes, for sexually reproducing eukaryotes” (1). Given that the vast majority of living things on this planet, both in numbers and biomass, are not sexually reproducing eukaryotes, this might be considered an oversight. Jan Sapp certainly thinks so. In The New Foundations of Evolution: On the Tree of Life, he gives us a history of microbiology, from Leeuwenhoek to modern-day disputes, taking an evolutionary perspective.

Sapp (an evolutionary biologist and historian of science at York University, Toronto) recounts how microbiological thinking developed in almost total isolation from evolution until the 1970s. That is when the comparison of 16S rRNA sequences became possible, allowing the phylogeny of species to be readily estimated. More closely related species have more similar 16S sequences, because there has been less time for them to diverge. When the new methods were applied to bacteria, the results completely upset previous taxonomy, which had been based on relatively crude metabolic tests and morphology. It also revealed the previously unimagined diversity of single-celled life.

The heroes of Sapp's book (because it is that kind of history) are Carl Woese and his colleagues, who first pressed the 16S sequence into service. Their most remarkable discovery concerned an obscure group of bacteria typically isolated from environments characterized by, for example, very high temperature or salt concentrations. (I say obscure because they were far from the driving concerns of medicine and industry.) Together with the methanogens, they were the first examples of what came to be known as the Archaea. Although they superficially resembled bacteria (being single-celled and lacking a nucleus), these organisms had a distinctively different metabolism, cell wall, and transcription machinery. In time, they came to be recognized as a whole new domain of life alongside eukaryotes and eubacteria (“true” bacteria). It is now thought that the Archaea are more closely related to us humans than they are to bacteria. This finding shook taxonomy to its foundations.

It is always easier to convince your fellow scientists of something they think they know already. Woese's work was emphatically not in this category, and much of Sapp's story describes the rocky road to its acceptance. Few obstacles were greater than the opposition of Ernst Mayr, which Sapp describes in some detail. Although Mayr recognized that finding the Archaea was “like discovering a new continent” (2), the great biologist argued that when it came to classification, phylogeny was irrelevant in the face of such a stark difference as the presence or absence of a membrane-bound nucleus that contained chromosomes. If a cell had such a nucleus, it was a eukaryote, and if not, it was a prokaryote. This was all that was required for “an information storage and retrieval system” (2), which was to Mayr the purpose of classification. From the viewpoint of the present day, Mayr comes across as small-minded, with a classical biologist's ignorance of microbiology. But his position offers a fine illustration of the tension between theoretical consistency and pragmatism, which runs throughout the book and continues to plague bacterial classification.

Two views of life.

A five-kingdom system based on three levels of organization [after R. H. Whittaker (3)] and a three-domain phylogenetic tree [after Norman Pace (4)].

CREDIT: (LEFT) AFTER (3); (RIGHT) AFTER (4)

A more fundamental problem is horizontal gene transfer. Bacteria (and archaea too) are notoriously promiscuous and can take up DNA with scant regard for the boundaries of named species. Horizontal transfer raises severe questions about any analysis that is based on phylogeny because different genes in a single organism can have different histories. Although the book raises in passing the notion that the tree of life should be replaced by something like a worldwide web of life, neither the evidence for this web nor its implications are considered in any depth—despite that fact that it strikes at the very heart of the phylogenetic approach to classification championed by Woese. It is churlish to complain too much, because the debate about horizontal gene transfer and the tree of life is far from settled. But the topic deserves a more thorough treatment than Sapp affords it, if only because it is so fundamental to evolutionary microbiology.

My other concern is that in several places the author describes prokaryotic evolution (with its high rate of horizontal gene transfer and the uncoupling of sex from reproduction) as “non-Darwinian”—this stretches to the publisher's claim on its Web site that the book “puts forth a new theory on evolution,” which it emphatically does not. Given that evolution even among archaea and bacteria is still based on the generation of variation, which is winnowed by selection and then inherited, I would argue Darwin was substantially right. Or more right than one could reasonably expect given that he had no conception of the gene and little knowledge of bacteria.

That Sapp makes his story so sparkling is an achievement all the more impressive when one remembers he must include a fair amount of taxonomy, both antiquated and modern. The debates and disputes that animate his account remain current today. Most microbiologists still do not know very much about evolutionary biology, and vice versa. Nevertheless, the tide of microbial genomes is changing this state of affairs. In order to know where we are going, it is helpful to reflect on how we came to be where we are. We all carry with us intellectual baggage and preconceptions from not only our own experiences but also those of our friends, colleagues, and mentors. Perhaps the highest compliment I can pay The New Foundations of Evolution is that having read it, I feel that I better understand the minds of my fellow microbiologists—and even my own.

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