Gaian takes on Darwin

The puffs on the back cover are extraordinary. E. O. Wilson calls Lynn Margulis "one of the most successful synthetic thinkers in modern biology". James Lovelock says the book has the "flavour of real science". And David Suzuki says we need "more of this kind of stimulation". Having read the book, I am totally perplexed at both their comments and its value.

Margulis has several biological obsessions. She is obsessed with symbiosis, Gaia, and hates neo-Darwinian ideas about evolution. She also has a passion for unicellular organisms, particularly bacteria. Most of the essays are by Margulis herself, often with a co-author, her son the philosopher Dorian Sagan, and some together with others, including Lovelock. A few of the essays are by Sagan alone, but Margulis's is the major voice. She wholeheartedly embraces Kirkegaard's assertion that the less support an idea has, the more fervently it must be believed. It makes the book rather repetitive.

An early essay is on Robert Oppenheimer and the atom bomb, related to a term paper she wrote in 1955. She asks: "Could I ever lose myself like he did? I love science, could I ever hurt and then be haunted by its application forgetting about the knowledge in and for itself?" And she reports a brief interview with him. She does not lack confidence and describes her own life story as one of enthusiasm and enlightenment by a girl who turned down dates and never watched TV.

Gaia is an idea developed by James Lovelock, who is among a very small group of scientists on whom she heaps praise. It is the "Earth's physiology: the sum of the energy -and material - exchanging activities of the living network of our planet's surface." It views Earth as being a living system, a single self-regulating entity. The conditions essential for life, such as the average temperature and the chemical composition of the atmosphere, are maintained by living matter itself using energy from the sun.

Gaia is linked to symbiosis which is the physical connection between organisms of different species, even though they may be only distantly related. A remarkable example of symbiosis is the leiognathid fish which can see in the dark because of the light produced by luminescent bacteria in its gut. In general all living things are essentially in contact with one another through water, atmosphere and soil. Gaia is thus global symbiosis. It is suggested that the greatest psychological block to the scholarly acceptance of Gaia is that it throws in doubt the uniqueness of humanity in nature because of "its intricate planning by subvisible entities". But what planning? This is not explained.

Bacteria are relatively simple cells compared to the cells that make up the bodies of animals and plants. Our cells - which are eukaryotes - have a nucleus which is bounded by a membrane and contains the chromosomes with all their thousands of genes. Our cells also have mitochondria, sausage-like structures which produce energy and which have a small number of genes which code for some of the mitochondria's proteins. Bacteria have neither a nucleus nor mitochondria. Bacteria are primitive and so how then did eukaryotes evolve? Margulis has contributed significantly to the now-accepted idea that mitochondria have their origin in free living bacteria that became symbiotically incorporated into another cell. She claims that the original suggestion was dismissed and disparaged by the biological community but provides no evidence. It would be interesting to have this hostility documented. Were her papers rejected? Were they criticised in the literature? Were her grants turned down?

This idea of symbiotic incorporation in the evolution of the eukaryotic cell is central to her thinking. She rightly points out that chloroplasts in plants have a similar origin, but her attempts to extend the idea further are pursued almost completely without evidence. She wants to believe that cilia, whip-like beating structures on the outside of many eukaryotic cells, have a similar origin and is very excited at a report that there is evidence for genes associated with these structures, as there is for mitochondria. Again and again she quotes the original report but only once points out that the authors have now withdrawn part of their original claim. I regard it as grossly misleading the reader not to draw attention to this each time she uses it to support her claim. The fact that the essays may have been written at a time when the retraction had not yet been made is no excuse: a footnote should have been inserted.

She is right to emphasise the enormous variety of bacteria and other single-cell organisms. Also her claim that there were major changes in the evolution of eukaryotes from bacteria is justified, and the changes are probably more fundamental than anything that occurred later when multicellular organisms evolved. I have myself argued that the eukaryotic cells are the true "miracle" of evolution and that virtually nothing new had to be invented for the evolution and development of multicellular organisms. The eukaryotic cells had already acquired all the necessary machinery and multicellular evolution was, by comparison, much simpler.

Her comment on Darwinian ideas of evolution is more insult than reasoned arguments. There is "Darwinian smarm"; "The popular neo-Darwinian view, in which all evolutionary innovation is assumed to be generated by chance accumulation of mutations, I claim, is mechanical, parochial and repressive." She wishes to replace it with what is known as the autopoietic concept. I find it impenetrable. It apparently refers to the living nature of material systems which are self-making and self-repairing, which produce and maintain their own boundaries. Phrases in autopoietic terms that "Cell metabolism constructs plasma membrane" are essentially meaningless.

A key feature is the effect of the system on the environment which, falsely, she says Darwinians neglect. Gaia is the largest example, the smallest, bacteria. She denies that life is determined by a physical universe run by mechanical laws. No evidence is offered. It is related to an idea that there is nothing so special about life, as claimed by the Russian scientist Vladimir Vernadsky. According to Dorion Sagan, animals are in a "deep sense also a 'group' of organisms, namely cells with their proposed histories and origins". The fact that cells in animals share the same genes and that genes, and genes alone, are what changes in the evolution of multicellular organisms, is nowhere discussed. Mathematical models, apart from Lovelock's "Daisy World", are an anathema and are claimed merely to soothe with their certainty. Thus the seminal ideas of W. D. Hamilton on inclusive fitness and of John Maynard Smith on evolutionary stable strategies, as well as Robert May's studies in ecology, are dismissed in a sentence.

Gaia, not Darwinism, is the grand unified theory of biology and Margulis thinks it is hated by Darwinians. But why? I cannot see anything in Gaia that would have any significance for most evolutionary theory, which is concerned with relationship and origin of species and the origin of structures like limbs and eyes. The suggestion that evolutionary theory cannot, in principle, explain the latter is simply false. She also rejects out of hand most current evolutionary theories about sex and relates it to bacterial DNA repair.

No lay reader should try to learn cell biology from these essays. The discussion on cell death - a major current field of research - is primitive, to say the least, and out of date (again, the age of the paper could have been qualified with a footnote). Her terminology makes no concession to clarity: an undulipodia is used for cells having cilia or flagella. And the neurobiology is wildly eccentric. "My basic speculation is that mind-brain processes are the nutrition, physiology, sexuality, reproduction and microbial community ecology of the microbes that compose us." But our neurons are not microbes and no attempt is made to show how this explains anything about the mind.

However, I cannot but admire her description of her first husband, the young Carl Sagan. "Carl, less sophomoric than I, enjoyed an exaggerated sense of his own importance. He had only superficially understood Copernicus' lessons. Galileo's ideas had been taken in logically but not emotionally ... my aspiring astronomer functioned as if the earth (... in particular his home), was the dead centre of the universe. His mother, incessantly orbiting around her son."

Lewis Wolpert is professor of biology as applied to medicine, University College London.