Evolution of Aging

Genetic program for death. August Weismann, the great German theorist of the nineteenth century, was one of the first biologists to use evolutionary arguments to explain aging. His initial idea was that a specific death-mechanism exists, designed by natural selection to eliminate the old, and therefore worn-out, members of a population. The purpose of this programmed death of the old, Weisman thought, was to make space and resources available for younger generations. He probably came to this idea while reading the notes of Alfred Russel Wallace (one of Darwin's contemporaries and a co-discoverer of natural selection), which he later cited in his essay "The Duration of Life" (1889): "Wallace wrote that when one or more individuals have provided a sufficient number of successors, they themselves, as consumers of nourishment in a constantly increasing degree, are an injury to those successors. Natural selection therefore weeds them out, and in many cases favors such races as die almost immediately after they have left successors." Weismann enthusiastically accepted and developed further this idea, which also corresponded well with the hiring practices of German universities of that time, whereby a new candidate had to wait for the death of an old professor to obtain a position.

Suggesting the theory of programmed death, Weismann had to think about the exact biological mechanisms executing this death program, and he came to the idea that there is a specific limitation on the number of divisions that somatic cells can undergo. Specifically, he suggested "that life span is connected with the number of somatic cell generations which follow after each other in the course of an individual life, and that this number, like the life span of individual generations of cells, is already determined in the embryonic cell" (Weismann, 1892). Weismann tried to explain "the different life span of animals by making it dependent on the number of cell generations which was the norm for each different species" (1892). Remarkably, his purely theoretical speculation on the existence of a cell division limit was experimentally confirmed many decades later by H. Earle Swim (1959); and this scientific discovery was then successfully developed and publicized by Leonard Hayflick (Gavrilov and Gavrilova, 1991).

Weismann eventually stopped writing about the "injuriousness" of the old and changed his evolutionary views, considering old organisms not to be harmful, but simply neutral for the biological species: "In regulating duration of life, the advantage to the species, and not to the individual, is alone of any importance. This must be obvious to any one who has once thoroughly thought out the process of natural selection. It is of no importance to the species whether the individual lives longer or shorter, but it is of importance that the individual should be enabled to do its work towards the maintenance of the species. . . . The unlimited existence of individuals would be a luxury without any corresponding advantage" (Weismann, 1889).

Subsequent studies confirmed that Weismann's decision to abandon the initial idea of programmed death was a wise one. Many scientific tests of the programmed death hypothesis have been made, and some of them are summarized here.

One way of testing the programmed death hypothesis is based on a comparison of life-span data for individuals of a single species in natural (wild) and protected (laboratory, domestic, civilized) environments. If the hypothesis is correct, there should not be very large differences in the life spans of adult individuals across compared environments. Indeed, for a self-destruction program to arise, take hold, and be maintained in the course of evolution, it must at least have some opportunity, however small, of expression in natural (wild) conditions. Consequently, the age at which such a program is "switched on" cannot be too high, otherwise (because of the high mortality in the wild from predators, hunger, infections, and harsh natural conditions) no one would live to the fateful age, and the self-destruction mechanism would not be able to be expressed. It follows from this that life spans, in even the most favorable conditions, cannot significantly exceed the ages reached by the most robust individuals in the wild—if, of course, the concept is correct.

The analysis of the actual data reveals, however, a picture completely opposite to what would be expected from the programmed death theory: the life spans of organisms in protected environments greatly exceed the life spans observed in natural (wild) conditions. For example, the chaffinch (Fringilla coelebs) can live for twenty-nine years in captivity. However, in the wild this is practically impossible, since about a half of all of these birds perish during their first year from hunger, cold, diseases, and attacks by predators, and the mean life span is only about 1.4 to 1.5 years. As a result of this high mortality, only 0.1 percent of the initial number of chaffinches survives to age eleven in the wild. Similar observations were made for field voles (Microtus arvalis Pall). In protected laboratory conditions, the average life span of voles is about seven or eight months, while individual specimens survive to twenty-five months. In the wild, however, the average life span of voles is only 1.2 months, and only 0.1 percent survive to ten months. Observations like these are common for many biological species. Thus, if one attempts to estimate the age of programmed death on the basis of life spans in laboratory conditions, it becomes clear that no death program could arise or be maintained in evolution, if only because it would not be able to come into operation in natural conditions, where practically no individual lives to the required age.

The same conclusion is reached from an analysis of data on the human life span. At present, the mean life expectancy in developed countries is between seventy and eighty years, while the documented record for longevity is 122 years. If we take these figures as an estimate for the age range in which the death program is switched on, we are forced to admit that such a program could not have arisen in human evolution, since, according to paleodemographic data, virtually nobody survived to such an age. For example, only half of those born in the Late Paleolithic era (30,000–10,000 B.C.E.) reached eight or nine years, and only a half of those born in the Neolithic era (6,000–2,000 B.C.E.) reached twenty-six years. Even in the Middle Ages, life expectancy at birth was no greater than twenty-nine years. Investigations of the skeletons of American Indians have shown that just two centuries ago only 4 percent of the population survived to age fifty. Note for comparison, that the probability of surviving to this age in developed countries today is 94 to 96 percent. If these facts are compared, it is difficult to refrain from posing the following question: can the guaranteed destruction of a few old people, who are chance survivors and doomed in the wild, be a sufficient evolutionary basis for the formation and preservation of a special self-destruction program in the human genome? Viewed in this light, the inconsistency of the programmed death hypothesis becomes obvious.

In addition, if the question of whether death is programmed is approached from the evolutionary point of view, it becomes obvious that special mechanisms for the termination of life could hardly help an individual to fight successfully for his survival and the survival of his progeny. On the contrary, those individuals in whom the action of such a program had been impaired by some spontaneous mutation would quickly displace all the remaining individuals, since in their longer life span they would produce more offspring, or at least could increase the survival of their offspring by providing longer parental support.

In 1957, George Williams, the author of another evolutionary theory of aging summarized the critical arguments against the programmed death theory (called Weismann's theory for historical reasons). Here is a partial list of his most forceful critical arguments:

1. The extreme rarity, in natural populations, of individuals that would be old enough to die of the postulated death-mechanism
2. The failure of several decades (now over a century) of gerontological research to uncover any death mechanism (the discovery of apoptosis, or programmed cell death, is irrelevant to this discussion, which is focused on the whole organism rather than some of the organisms somatic cells)
3. the difficulties involved in visualizing how such a feature could be produced by natural selection

There is, however, one good reason why this dead theory of programmed death should not be ignored as outdated and should not be forgotten—the ghosts of the theory can still be found in many publications, including the Encyclopaedia Britannica which states: "Locked within the code of the genetic material are instructions that specify the age beyond which a species cannot live given even the most favorable conditions," (Encyclopaedia Britannica, 15th ed., 1998, p. 424.)

As for August Weismann, he should be credited with at least four significant contributions to aging studies:

1. Suggesting the first evolutionary theory of aging that attracted the attention of other researchers
2. Abandoning his own theory when he understood that it was incorrect—this honest decision allowed new evolutionary theories of aging to develop
3. Correctly predicting the existence of a cell-division limit—without having any data at all
4. Discriminating between germ cells and the somatic cells ("soma"), with a prophetic understanding of "the perishable and vulnerable nature of the soma." (Weismann, 1889); this idea is related to the more recent disposable soma theory of aging