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LUIGI CORNARO (1464–1566). TINTORETTO.

Huntington disease has several strange features. One is the way in which its symptoms become more severe from one generation to the next. This phenomenon, called ‘anticipation’, arises from a peculiarity of the Huntington gene itself and the mutations that cause the disease. The gene contains a region in which three nucleotides, CAG, are repeated over and over again. Most people have between eight and thirty-six of these repeats. Huntington disease mutations increase the number of repeats, so disordering the structure of the protein. Several mutations of this sort cripple the protein ever further over successive generations, increasing the severity of the disease.

Another oddity of Huntington is its frequency. It afflicts about 1 in 10,000 Europeans. This is very high – most dominant mutations that kill have frequencies of about one in a million. But Huntington disease can persist in a family for generations. In 1872, George Huntington, a New York physician, described the disorder from families in Long Island, New York. Among their ancestors was one Jeffrey Ferris who emigrated from Leicester, England, in 1634. He almost certainly had the disease, as do many of his descendants today. In South Africa, about two hundred Huntington’s patients are descended from Elsje Cloetens, the daughter of a Dutchman who arrived with Jan van Riebeeck to found the Cape Colony in 1652. A large group of Huntington’s patients who live near Lake Maracaibo, Venezula, are the decendants of a German sailor who landed there in 1860.

How can so lethal a disorder transcend the span of so many generations? In 1941 the brilliant and eccentric British geneticist J.B.S. Haldane proposed an answer. He pointed out that, unlike most genetic disorders, the symptoms of Huntington disease usually appear in middle age. By this time most people with the defective gene have had their children – each of whom will have had a 50 per cent chance of inheriting the defective gene. Unlike most lethal dominant mutations that kill in childhood and so are never transmitted to the following generation, the Huntington mutation hardly impairs the reproductive success of those who bear it. Middle age is almost invisible to natural selection.

Few other disorders caused by a single mutation have such devastating effects so late in life. Yet the strangeness of Huntington disease is deceptive, for Haldane’s explanation of why it is so common also explains, with a little generalisation, why we, and most other animals, age. In this chapter I will argue that ageing is a genetic disorder, or rather, it is many genetic disorders, some of which afflict us all, others of which afflict only some of us. This point of view goes against the grain of most definitions of disease. Medical tradition distinguishes between ‘normal’ ageing, about which nothing much is done, and ‘age-related diseases’, such as arteriosclerosis, cancer and osteoporosis, that consume vast amounts of national health budgets. But this distinction is an illusion, a necessary medical fiction that allows physicians to ignore a disease that affects us all but which they are impotent to cure or even ameliorate. Properly understood, ageing is precisely what it seems: a grim and universal affliction.

IMPOTENT SELECTION

Ageing is the intrinsic decline of our bodies. Its most obvious manifestation is the increased rate at which we die as we grow older. An eight-year-old child in a developed country has about a 1 in 5000 chance of not seeing her next birthday; for an eighty-year-old it is about 1 in 20. Of course, it is possible to be killed by causes quite unrelated to ageing – violence, contagious disease, accidents – but their collective toll is quite small. Were it not for ageing’s pervasive effects, 95 per cent of us would celebrate our centenaries; half of us would better the biblical Patriarchs by centuries and live for more than a thousand years. We could see in the fourth millennium AD.

The evolutionary explanation for why we, and most other creatures, age rests upon two ideas, both implicit in Haldane’s explanation for the frequency of Huntington disease. The first is that the ill-effects of some mutations are felt only late in life. Most obviously a mutation might cause a slow-progressing disease. The Huntington mutation is just such a time-bomb. So is the SOST mutation that causes sclerosteosis in Afrikaaners; children are relatively unaffected but the excess bone growth kills in middle age. So are mutations in BRCA1, the familial breast-cancer gene whose ill-effects are usually felt only by women in their thirties and forties. And so is a variant of the APOE gene called ?-4 that predisposes elderly people to heart attacks and Alzheimer’s.

Such examples could be multiplied, yet it must be conceded that not a great deal is known about the time-bombs with the longest fuses, those that detonate past middle age and that cause senescence. For the moment, let us simply suppose that they exist. To do so, however, is not sufficient to explain ageing. It is also necessary to understand how it is that time-bomb mutations have come to be such an inescapable part of human life. Haldane alluded to the explanation for this when he argued that the Huntington mutation is not seen by natural selection. The same logic can be applied more generally. Imagine a dominant mutation that renders a twenty-year-old man impotent for the rest of his life. In twenty-first-century Britain at least, relatively few men have fathered children by the age of twenty, and after age twenty, the victim of such a mutation will never do so. Whatever he may accomplish in the course of the rest of his life, as far as genetic posterity is concerned he may as well never have been born. The same mutation may occur many times in many men but it will, adolescent fathers aside, never be transmitted to future generations and so will always remain rare. Imagine now another dominant mutation, one that also renders its carrier impotent, but does so only at the age of ninety. For such a man, the odds are excellent that he will be quite oblivious to his loss for the simple reason that he will be dead, having been previously claimed by cancer, a cardiac infarction, influenza, or a failure to notice the approach of the Clapham omnibus. Six feet under, the cost of Viagra is not an issue. Alive and virile he will, however, have sired any number of children, some of whom will bear the mutation, as will some of their children, and so on. Indeed, it is quite possible that the mutation will, simply by chance, spread throughout the population so that, after many generations, all men will be impotent at age ninety – essentially the case today.

This argument is just a restatement of Haldane’s: that the force of natural selection against deleterious mutations declines over the course of life. But it was another British scientist, Sir Peter Medawar, who first generalised this to explain the diversity of ways in which our bodies break down while ageing. Late in life, some mutations impair our cardiovascular fitness, others our resistance to cancers or pathogens, others virility, yet others our wits. Such long-fuse mutations have afflicted us forever and, unimpeded by natural selection, they have spread and become universal.

Medawar’s explanation of the ultimate causes of ageing surely has a great deal of truth to it, but it has one weakness, and that is its appeal to chance. It is easy to see why mutations that cause some grievous error in old age are not selected against, but is that absence of impediment enough to account for their spread throughout humanity? Perhaps. There are probably thousands of different mutations that have ill-effects late in life, and each of these must have occurred incalculably many times in human history. It is certainly plausible that some spread by chance, particularly at times when population sizes were small.