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PREFACE

The Cooperative Gene
How Mendel's Demon Explains the Evolution of Complex Beings
By MARK RIDLEY
The Free Press

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When the extraterrestrial visitors land on Earth in their space-saucer, they will be excited to see that ours is one of those rare planets where complex life has evolved. They will have found microbes, like our viruses and bacteria, on every life-bearing planet. Naked biological molecules and simple single cells will be so familiar that they will need only some box-ticking on the extraterrestrials' report: 'they are carbon-based; they use DNA; they are fuelled by electromagnetic radiation and chemical resources; they copy themselves.' But only a few planets will have complex life — creatures like us, with our supercomputing brains; or like swans, with their great wings beating out on either side; or like roses, with their symmetric flowers, delicate petals and seductive perfumes. Complex life forms are built from many cells, and each individual grows up from a single cell to an adult that has an organic form and may be capable of intelligent behaviour.

The extraterrestrials will have some experience of complex life, and they will know that the real fun begins when trying to understand complex, rather than simple, life forms. There is no finer cosmic spectacle than the sight of a complex life form struggling to reproduce itself. The first question they will ask is how many copying mistakes Earthly life makes when it reproduces its hereditary molecules. They can then start on the more interesting part of their report. 'The whole lot use DNA, with about fifty catalysts. They make copying mistakes once every thousand million letters or so — which looks about right.' From this, certain consequences obviously follow. 'The big creatures have a thousand million or more letters of DNA code and a hundred or so cell generations in a body. They use sex, of course...' Other apparent consequences less obviously follow: '...but it's a crazy sort of sex. They pick their partners from only half their kind. The other half are just ruled out...this is nothing to do with choosing among potential mates, it's some kind of pre-choice inhibition. Anyhow, we'll bring some of the larger ones for the circus. They can go after those music-freaks from the planet near Nemesis, the ones who take in code, one-tenth at a time, from ten different partners, after ten distinct mating dances. The trouble they had keeping the other nine-tenths of their partners' code out is nursery stuff compared with what these Earthlings get up to in egg manufacture.'


Complex life is the masterpiece of nature, and I want to understand it. Life itself poses less of a problem than complex life. The fossil record tells us that life was probably easy to evolve, but complex life was hard to evolve and might not have evolved at all. Simple life appears to have evolved almost instantaneously, as soon as it was possible. But complex life evolved only after a long delay, as if it had been held up by some inherent difficulty. In this book I follow up the idea that the main difficulty was for a complex life form to copy all its genes accurately enough. More DNA is needed to code for a complex life form than for a simple life form. The DNA in a human being is 6600 million letters long and codes for about thirty thousand genes. In contrast, the DNA of a bacterium is two or three million letters long and codes for two or three thousand genes. Copying mistakes will have become more numerous as the DNA grew longer, for much the same reason as they happen when we are copying written text. A scribe can hope to copy an advertising slogan without making a mistake, and mistakes do not matter much in any case because it is easy to throw the bad copy away and make a new one. But a scribe can hardly hope to copy out the Bible — a job that took a mediaeval scribe about a year and a half — without making some mistakes.

The evolution of complex life required mechanisms to deal with copying mistakes in the DNA. The first mechanisms improved the accuracy of the copying itself. The earliest life forms probably made about one copying mistake in 100 letters, but bacteria had reduced the rate to less than one mistake in 1,000,000,000 letters. This huge improvement is due to the use of DNA for the master-copy — it is an impressively error-proof molecule — and a molecular machinery for proofreading and repairing mistakes. But the possibilities for improving the accuracy of copying seem to have been exhausted by the bacterial stage. The basic DNA copying machinery has remained much the same since then, and we make copying mistakes at a similar rate per letter of DNA as bacteria do. Our total error rate is much higher, however, because we use so many more letters of DNA code. Between bacteria and us the length of the DNA molecule has increased 1000-fold and the DNA has come to be copied 100 times per generation, against the once per generation of a bacterial cell. Our total error rate has gone up 100,000 times, and whereas a bacteria makes a mistake once in every 1000 offspring, we make over 100 mistakes in every offspring. It is something of a paradox how we can persist, while making so many copying mistakes in our DNA. The solution is uncertain, but is probably — sex. Sex can act to concentrate the copying errors in some of a parent's offspring, leaving other offspring relatively error-free. Sexual life forms could evolve to be more complex than clonal life forms.

Sex, however, created a new problem even while it was solving the problem of excess copying mistakes. In a clonal life form, every gene in the parent is put into its offspring: genes are passed on with a probability of 100 per cent. In us, and all complex sexually reproducing life forms, a gene has only a 50 per cent chance of being passed on from a parent to an offspring. The reduction from 100 per cent to 50 per cent in the chance that a gene is passed on was probably a difficult evolutionary step. When each gene had its chance of being passed on cut in half, natural selection would have favoured 'selfish' genes, in one sense of Richard Dawkins' famous expression: genes that could disrupt the system and increase their chances of being passed on to more than 50 per cent. The evolution of complex life was impossible until these selfish genes had been tamed.

The two, related, big themes of this book are both about error. The first kind of error is passive copying error — mutational mistakes in the copying of the DNA. The second kind is active — selfish genes that harm the body by uncooperative and subversive acts. Both kinds of error threaten the existence of complex life. They are also related in their solution. The main solution to the problem of copying error, in complex life, is sexual reproduction. But complex life on Earth uses a particular kind of sex — Mendelian sex: the genes are inherited in the manner first described by Gregor Mendel, in his garden peas at the monastery of St Thomas in Brünn (now Brno, in the Czech Republic) almost 150 years ago. Mendelian inheritance, it turns out, is designed to prevent selfish genes from acts of subversion.

The genes only tolerate, in an evolutionary sense, the reduced chance of being passed on because the lucky genes are picked at random, as if by lot. It is a basic property of Mendelian inheritance that you cannot predict whether or not a particular gene will be passed on. If it could be predicted which genes were to live on in future generations, and which were to die, natural selection could never have brought complex life forms into existence. The genes destined to die would have rebelled and the whole system would have collapsed. God may or may not play dice in the laws of physics and of chemistry. God did not need to play dice in the simple stages of biology, while life reproduced itself clonally. But the evolution of complex life required a mechanism of inheritance with an inherently random component. Somewhere between the bacteria and us — perhaps at about the stage of simple worms — God did have to start to play dice. Life started to use a randomizing system of inheritance, and all subsequent complex life forms have necessarily been built using the randomizing, Mendelian procedure to pass genes from parents to offspring.

Mendelian inheritance controls how genes are inherited in complex life. It combines sex, reproduction, and the probabilistic rather than certain inheritance of genes. Mendel himself was an Augustinian friar, and I like to imagine the chance mechanism as a rather monkish figure — Mendel's demon — who stands over each gene in a parent and decides whether it will be inherited in the next generation, and which other genes it will be passed on with. Mendel was a near-contemporary of the physicist James Clerk Maxwell, after whom the famous (or fairly famous) 'Maxwell's demon' is named. Mendel published his ideas in 1866; Maxwell described his demon five years later. Maxwell's demon is a hypothetical demon. It stands by a hole between two parts of a vessel and, by allowing only the fast-moving molecules through in one direction, can make (without expenditure of work) one part of the vessel hot and the other part cold. Maxwell's demon is an anti-randomizing demon, who opposes the random movement of molecules and produces a more ordered state of the vessel — that is, it comes to have a hot half and a cold half rather than a uniform temperature throughout. Mendel's demon, by contrast, is a more realistic demon. It is a randomizing demon, who creates an ordered state (that is, complex life) by opposing the disruptive force of natural selection.

Complex life depends on Mendel's demon, and complex life probably did not evolve until the demon was assembled one or two thousand million years ago. Maxwell's demon was a lawless kind of demon, which could violate one of the laws of physics. Mendel's demon is more of a law-enforcing kind of demon. It redirects the laws of biology to a more creative, rather than destructive, direction. There is nothing diabolical about Mendel's demon. People who are familiar with the UNIX computer operating system may see an analogy in the unseen 'daemons' or 'dæmons' that work behind the scenes to perform useful computing tasks. Moral philosophers can think of eudemonism, in which actions are judged by whether they promote happiness. Classicists may think of eudaimonia, meaning happiness or good fortune. Pagans may think of the goddess Fortune. Mendel's demon is the executive of gene justice, and we all depend on it for our existence.

The book aims to explain several deep, general features of life. Some of these features, such as sex, are well-known existential puzzles. Others, such as the reproductive cell division called meiosis that determines how genes are passed on, pose puzzles that are just as deep but less well-known. Meiosis is the fateful cell division in which each gene has only a 50 per cent chance of surviving to the end. Meiosis reduces the number of genes by half. So why does it begin not by reducing the number of genes but by doubling them? And why does the demon act only at the first of the two stages during which the gene numbers are reduced? It turns out that the smoke-and-mirrors of meiosis are a trick to baffle the selfish genes. We can therefore understand sex, and the procedures of inheritance, as design features that enabled the evolution of complex life.

It is intellectually satisfying to understand deep, general features of life. It also allows us to predict which features of complex life on Earth will be found in other complex life forms — including future life here, and independently evolved life elsewhere in the Universe. We can predict that all complex life forms will use something like sex and the randomizing procedures of Mendelian inheritance. But other features of Earthly complex life may be more of an accident. Gender is a universal feature of complex life, and intimately related to sex and Mendelian genetics; but its existence may be an accident.

The cells of complex life forms, including ours, contain two independent sets of genes in two different parts of the cell. Mendel's demon keeps one set well behaved, but not the other. The reason why we have these two sets of genes per cell is that complex life on Earth happened to originate in an accidental merger event, roughly two thousand million years ago. Two cells merged into one, bringing two gene sets into one cell. A cell with two gene sets is likely to suffer the same fate as a merged business that fails to unify its management structures. One of the management teams usually resigns after a business merger, and gender works in much the same way in us. Males eject one of the gene sets from their sperm, but females retain it in their eggs. The long-term consequences have been huge. The sperm have shrivelled in size, as all the potentially troublesome entities have been sucked out; eggs have stayed large, or even grown larger. Sperm, being small, are more abundant than eggs, and this fact underlies the supply-and-demand economics of the mating market. All modern male-female differences (in so far as they are due to evolution) can therefore be traced to an accidental merger event deep in the past. If complex life had not evolved via a merger, it would not have gender. Gender will be the most puzzling feature of complex life on Earth for our extraterrestrial visitors. They will not be able to understand it until they have read our DNA and reconstructed the merger event that is implicit in its codes.

The two big themes of copying error and uncooperative genes make up the core of the book. Chapters 1 and 2 explain the paradox of complex life, the history of complex life on Earth, and the gene number criterion of complexity. Chapters 3 to 5 are about how life has evolved to deal with passive copying error, and Chapters 6 to 8 are about how life has evolved to deal with actively selfish genes. I use the theory of Chapters 3 to 8 to look at human evolution in the present and recent past (Chapter 9) and the possible future evolution of more complex life (Chapter 10). Some of the emerging new reproductive and genetic technologies, such as gene therapy and the preservation of youthful gametes for use later in life, take on a new significance in the grand historical sweep of complex life. They could be the first new error-reduction devices since the evolution of the bacteria 3500 million years ago. Certain kinds of complex life are ruled out at present, because error rates are too high. A reduction in the error rates might allow the evolution of forms with superhuman complexity, in intellect or social organization. Alternatively, it might allow the evolution of flexible life forms, that contain the DNA codes for several species but use the code for only one of those species each generation. A flexible life form might contain the code for a fish, a tree, a bird and a human. An individual would, early in life, select which was the best form to grow up as, and switch off the codes for all the other forms. I look at these ideas at the end of the book.

I have added a glossary and end-notes. I have tried to avoid technical terms as much as possible, and defined them when they do appear; but the glossary may help with recurrent technical terms that I have not defined every time I use them. I have also avoided references in the text; they are in the end-notes, together with some provisos and complications that I thought most readers could do without, but some readers might be interested in.

I have been working on the book for an alarmingly long time, and I am grateful to the many people who have helped me, in conversation, in lecture-audience feedback and by e-mail, by telling me about facts, explaining theories, and directing me to references. Alan Grafen and Alex Kondrashov have helped with a particularly large number of my queries. They are high-powered thinkers, and I should say that their help is no kind of imprimatur for what follows. The deleterious mutations are my own. Alan Grafen read two chapters of a much earlier draft, and a residue from them remains in the current Chapter 5. Thanks also to Mark Pagel, who read an early draft of Chapter 3. Big thanks to John Bohannon, Jo Ridley, and my editor at Weidenfeld & Nicolson, Peter Tallack, who read the whole book in its penultimate draft, and helped with comments on style and exposition, as well as the science. I am also grateful to Paul Harvey and Marian Stamp Dawkins, for facilities in the Department of Zoology, Oxford.

(C) 2001 Mark Ridley All rights reserved. ISBN: 0-7432-0161-2




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