American Scientist

THE NEW FOUNDATIONS OF EVOLUTION: On the Tree of Life. Jan Sapp. xx + 425 pp. Oxford University Press, 2009. $99 cloth, $39.95 paper.

Published in the year of the 200th anniversary of Charles Darwin’s birth, The New Foundations of Evolution is concerned with a topic that is decidedly non-Darwinian: the evolution of microorganisms and the structure of the universal tree of life. This is not really surprising, given that the author is Jan Sapp, an eminent historian of science at York University in Toronto whose previous books have challenged the accepted paradigms of biology. His first, published in 1987, was titled Beyond the Gene: Cytoplasmic Inheritance and the Struggle for Authority in Genetics, and he has written several others on such topics as the history of symbiosis and the evolution of evolutionary thought. Like these others before it, Sapp’s latest book is both penetrating and paradigm-shifting.

In the first half of the book, Sapp presents a thorough history of microbiology and microbial evolutionary biology from the 1600s to the middle of the 20th century. This sets the scene for the second half of the book, in which he recounts the compelling story of the efforts of Carl Woese, a microbiologist at the University of Illinois at Urbana-Champaign, to construct a universal tree of life using ribosomal RNA sequences. Woese, by constructing his tree, which divided life into three primary lineages or domains—archaea, bacteria and eukarya—rather than the traditional five kingdoms (plants, animals, fungi, protists and monera), and by abolishing the venerable prokaryote-eukaryote dichotomy (to Woese the term prokaryote was inappropriate and misleading), shook the very foundations of evolutionary thought. Sapp’s account here is often riveting as he tells how Woese gathered evidence to support the tree, forged a successful collaboration with Otto Kandler of Germany, and encountered resistance from prominent scientists and scientific journals.

But, wait, you might say; what about that earlier statement that microbial evolution is non-Darwinian? Didn’t Darwin discover the natural process by which all life evolves, in which natural selection acts on heritable variation within populations? How could any form of evolution, microbial or otherwise, be an exception to this rule? How could anything lie outside Darwin’s overarching evolutionary mechanism?

In the preface to The New Foundations of Evolution, Sapp writes that “to come to grips with microbial evolution is to reconsider much of classical biology’s understanding of the processes of evolution, its imagery, methods, and doctrines.” That’s because Darwinism and the Modern Synthesis traditionally have focused on the origins of species of animals and plants, Sapp explains, whereas microbial evolutionary biology probes the earliest origins of life itself. It is largely concerned with “the evolution that occurred before organisms as we know them appeared.” It looks at such problems as how the cell and its parts evolved, and how the genetic code might have arisen. Furthermore, he writes, “transfers of genes, of gene clusters, and of whole genomes between distantly related taxonomic groups [through horizontal gene transfer and symbiosis] are fundamental processes in microbial evolution.” And they are processes that lie outside the Darwinian scheme, which assumes gradual, incremental change.

As Sapp reveals, microbes have always been problematic for evolutionary biologists. From the very beginning, microbes were not considered appropriate for evolutionary study. Discovered by Antony van Leeuwenhoek (1632–1723), microorganisms (including protists) were initially all lumped together in a group called the “infusoria.” Darwin himself, interested primarily in the origin of species, ignored these inhabitants of the invisible world because it was not clear to him (just as it is not clear to us now) whether bacteria even existed as distinct species. When the Modern Synthesis was forged in the 1930s and 1940s, bacteria again were left out. They were thought to dwell in a murky, Lamarckian world outside the Darwinian realm. Now, in our age of comparative genomics, we know that bacteria and archaea can swap genes through horizontal gene transfer, and they apparently have done so extensively in the past. Thus the pesky microbes may once again be causing trouble, this time threatening to turn Woese’s nicely branching tree into a web of interconnecting lines.

But the saving grace—the redeeming feature—of the tree that Woese built is this: It is based on the analysis of not just any nucleic acid, but of 16S ribosomal RNA (rRNA). And 16S rRNA is a component of one of the subunits of the ribosome, a highly complex structure involved in the translation of messenger RNA into protein. It lies at the core of the cell’s information-processing system, where it has direct and indirect interactions with myriad other proteins and RNAs. Its gene is thus a highly unlikely candidate for a horizontal transfer event.

As Sapp explains, in the early 1970s Woese very deliberately chose to use ribosomal RNA in his comparative analysis. This was a brilliant (and extremely lucky) decision on his part. We now know that there are only about 50 genes that lie at the universal informational core of organisms and thus would be appropriate for constructing a tree. Because Woese chose to base his tree on rRNA, it has, at least in terms of its major branches, withstood the test of time.

In the 1990s, University of Colorado biologist Norman Pace dramatically expanded the tree by including 16S rRNA sequences obtained directly from microorganisms in environmental samples. He did this by developing a method that circumvented the need to establish cultures. The universal phylogenetic tree that Pace published in 1997 is reproduced at right.

There are still difficulties in rooting the tree, and in pinpointing when the last universal common ancestor lived and what it looked like, but many scientists who once expressed doubts about the tree now by and large accept its broad outlines. This comes through clearly in a 2005 book edited by Sapp—Microbial Phylogeny and Evolution: Concepts and Controversies, which contains chapters written by some of the earlier skeptics. Whereas The New Foundations of Evolution gives a history of microbiology and tells the story of the discovery of the universal tree, Microbial Phylogeny and Evolution answers the question, How do things stand now regarding the universal tree of life? What one sees is broad acceptance by many, with some debate over the details.

It is nonetheless true that many biologists still believe in a dichotomous prokaryote-eukaryote division of life in which there are prokaryotes on one hand (bacteria and archaea, both of which lack a distinct nucleus) and eukaryotes on the other. Moreover, for many, the gut bacterium Escherichia coli still serves as the prototype for all prokaryotes. Sapp discusses this whole debate, describing the twists and turns it has taken over the years.

Ernst Mayr (1904–2005), an icon of evolutionary biology, was one of a number of scientists who vigorously opposed Woese’s (and Norman Pace’s) suggestion that the catch-all term “prokaryote” be banned from biology. Woese and Pace had made this suggestion based on 16S rRNA analysis and the fact that a number of other cellular features also differentiate archaea from bacteria: their cell-wall structure and transfer RNA structure, the fact that archaean RNA polymerases resemble those of eukaryotes more than those of bacteria, the presence of unique lipids in their cell membranes, and the presence of introns in their genes. But to Mayr, evolution was “an affair of phenotypes,” and the purpose of taxonomy was to serve as “an information storage and retrieval system.” For Mayr, a taxonomic system (a tree, if you will) that was based on molecular phylogenetics and thus ignored the huge morphological differences between prokaryotes and eukaryotes was nonsensical. But Woese argued that the primary aim of taxonomy from the time of Darwin has been to “encapsulate descent,” and that doing so—in this case by constructing a 16S rRNA tree—would automatically take care of information storage and retrieval. This disagreement between Mayr and Woese was a battle between titans over the very foundation of evolutionary biology.

Sapp expertly describes this debate and others, and thereby brings alive the dynamism at the heart of one of the most significant revolutions in the history of biology.

W. Malcolm Byrnes is associate professor of biochemistry and molecular biology at Howard University College of Medicine. His research is concerned with the structure and function of archaeal and bacterial metabolic enzymes. He currently is working on a book applying concepts from evolutionary and developmental biology and ecology to issues in bioethics and Christian theology.