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1 February 2003 Microbial Actors in the Evolutionary Drama
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Liaisons of Life: From Hornworts to Hippos, How the Unassuming Microbe Has Driven Evolution. Tom Wakeford. Wiley, New York, 2001. 212 pp. $24.95 (ISBN 0471399728 cloth).

Wakeford hiked the fens and watched insects on the waters amongst the woodlands and dairy farms of northern England before his migration, at the age of 16, to Cambridge University in search of a formal education in evolutionary biology. From the beginning, “the orthodox story of life evolving via chance mutations and competitive struggles” (p. 18) never sat well with the naturalist–writer. Indeed, our author found himself “at the bottom of a huge reading list on mathematical modeling” that seemed to ignore all microbiologically informed work. Even the definitive experiments of someone as important as Sir Vincent Wigglesworth were overlooked. Before Wakeford was born, Wigglesworth, in 1952, had shown how sterilized fly eggs died if their food (onions) was deprived of its normal bacilli associates. A teaspoonful of soil contains 10,000 genetically different types of bacteria. Bacteria swim, photosynthesize, and respire not only oxygen but also sulfate and nitrate. They alone convert refractory nitrogen of the air into delectable and useful food components. Why, Wakeford puzzled, did none of the metabolic virtuosities of bacteria and other microbes (e.g., protists and yeast) ever appear in any of his assigned readings in evolutionary biology? Why was the physiological need of flies for their live bacilli not mentioned?

The perspective that helped to develop the ideas of this book was greatly enhanced by a year's course of study in the philosophy and history of science. Now a professional prize-winning writer and biologist at the University of Sussex in England, Wakeford, on completion of his undergraduate degree, took a doctorate at the University of York, where he worked directly with microbial symbioses in the field and the laboratory. This experience, along with an insatiable reading habit, lively conversations, and study at the Marine Biological Laboratory at Woods Hole, Massachusetts, and at the National Centre for Biological Sciences in Bangalore, India, led Wakeford to the thesis of his narrative. The basic idea of Liaisons of Life is that microbes are “fundamental to the origin, evolution and current function of every creature we encounter.”

These small but complete organisms are best visualized through microscopic analysis in their physical associations with one another and with larger forms of life. From the hornwort, a moss-like plant, to the algae-infested corals of the tropical oceans and fungi-intertwined roots of forest trees, and from the languid hippo to all other mammals, subvisible microbial associations abound. The microbes have silently changed the course of evolutionary history.

One of Wakeford's admirably achieved goals is to explain why, from the 19th-century works of Charles Darwin and Louis Pasteur until now, the microbial world has been ignored in nearly all evolutionary writings. He relates the scientific discoveries to the times and places in which they were made. He shows especially clearly the profound influence of Pasteur's imagery of the “loathsome bacterial mob” and his incessant “war on germs.” To this day Pasteur's legacy colors our cultural view of microbiology. Wakeford notes how the study of symbioses “fell afoul of global politics: world wars, nationalism, and anticommunism, to name a few” (p. 17). Symbiosis, as Wakeford claims, was fatally bracketed in the minds of its enemies with dangerous political movements.

Nor did it help that the pioneers in this field were largely from non-English-speaking countries such as France, Germany and prerevolutionary Russia. In the wake of the carnage of World War I and the new threat from the Soviet Union, symbiosis was condemned by mainstream science as a political subversion that could provide explanations neither for humanity's apparent lust for conflict nor for the evolutionary patterns of life. Symbiosis became an international pariah subject, the victim of tacit textbook censorship and McCarthy-like witch-hunts among professional scientists. (p. 17)

I suspect that Wakeford is too impassioned here. He attributes too much to willful maligning of symbiosis research and too little to ordinary belief–system inertia and ignorance. The tide is turning. Protein and nucleic acid sequence studies, cytoplasm transmission genetics, and electron microscopy have all contributed to rising waves of understanding. We now realize that symbiosis is a major source of evolutionary innovation and that microbes are active and incessant agents of evolutionary change. Better that Wakeford were more accurate in his details and less preachy. Nevertheless, it is indisputable that here he has done teachers, students, and the public the fine service of interpretation of facts from disparate sources. By teasing out a fascinating narrative from a jargon-filled, stilted, and obscurantist literature, Wakeford presents the reader, in accessible language, compelling and well-supported evidence for the role of the microbe in the 4000-million-year history of life on Earth.

Scientific papers that concurred with and extended observations of Simon Schwendener (ca. 1870) garnered much evidence that lichens were not plants. The superb naturalist and artist Beatrix Potter had, in the late 1890s, prepared detailed studies, including beautiful watercolor plates, of many British lichens. Indeed, no lichen was a plant—the more she observed, the surer she became that lichens were “dual organisms”: a green partner in intimate contact with a fungal associate in each case examined. Though Potter is famous today as the author of the popular and charming Peter Rabbit series of children's books, few know the story Wakeford tells of her thwarted career as a scientific investigator. Not only was her work ridiculed and rejected by the botanists of the day (e.g., Reverend Leighton in his classic book The Lichen-Flora of Great Britain, Ireland and the Channel Islands [1871] wrote, “I have purposely omitted any mention of the Schwendenerian Theory of Lichens, as I cannot but regard it as purely imaginary, the baseless fabric of a vision,” and well-known naturalist Reverend James Crombie mused, “A useful and invigorating parasitism—who ever before heard of such a thing?”). As a woman, Potter was even refused entry to the open sessions of the Linnean Society, Burlington House, London, where these issues were routinely discussed. In the end, in 1897, her influential and favorite uncle, the chemist Sir Henry Roscoe, was permitted to read her paper for her. The manuscript itself was lost and not until a century later, in 1997, did Potter receive an official—of course, posthumous— apology from that venerable society for its treatment of her undoubtedly correct Schwendenerist analyses of lichens. The term Schwendenerist was one of serious abuse: It mocked not only those who claimed that lichens were not plants but any who took seriously the importance of symbiosis in physiology, taxonomy, and evolution. Botanist M. C. Cooke wrote in 1879 that “even if endorsed by the nineteenth century,” such ludicrous symbiotic ideals “will certainly be forgotten in the twentieth.”

Of course, the main point of Wakeford's well-written book is how wrong Cooke has been shown to be. All 20th- and 21st-century lichenologists are today Schwendenerists, since all of the 14,000 documented species of lichens are at least “dual.” None are plants. Schwendenerism, the 19th-century term that labeled and dismissed the concept of the central importance of symbiosis, especially microbial symbiosis, in the evolutionary history of life, has been replaced in the 21st century by symbiogenesis. Symbiosis, à la Anton de Bary, the distinguished botanist, is an ecological idea, the protracted physical contact between organisms of different species, whereas symbiogenesis, the origin of new organisms, organs, tissues, or behavior traits as a consequence of long-term symbiosis, is an evolutionary term. What Wakeford's book shows is the ascendancy of ideas, facts, natural history observations, and molecular biological proofs of the importance of symbiosis as an impetus to evolutionary innovation relative to the sterile anthro- pocentric rhetoric of neodarwinism.


Distinguished University Professor, Department of Geosciences, University of Massachusetts, Amherst, MA 01003-9297

LYNN MARGULIS "Microbial Actors in the Evolutionary Drama," BioScience 53(2), 179-180, (1 February 2003).[0179:MAITED]2.0.CO;2
Published: 1 February 2003

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