Leonid A. Gavrilov* and Natalia S. Gavrilova (Excerpts)
Center on Aging, NORC/University of Chicago, 1155 East 60th Street, Chicago, IL 60637
Abstract
The purpose of this article is to provide students and researchers entering the field of aging studies with an introduction to the evolutionary theories of aging, as well as to orient them in the abundant modern scientific literature on evolutionary gerontology. The following three major evolutionary theories of aging are discussed: 1) the theory of programmed death suggested by August Weismann, 2) the mutation accumulation theory of aging suggested by Peter Medawar, and 3) the antagonistic pleiotropy theory of aging suggested by George Williams. We also discuss a special case of the antagonistic pleiotropy theory, the disposable soma theory developed by Tom Kirkwood and Robin Holliday. The theories are compared with each other as well as with recent experimental findings. At present the most viable evolutionary theories are the mutation accumulation theory and the antagonistic pleiotropy theory; these theories are not mutually exclusive, and they both may become a part of a future unifying theory of aging.
Evolutionary theories of aging are useful because they open new opportunities for further research by suggesting testable predictions, but they have also been harmful in the past when they were used to impose limitations on aging studies. At this time, the evolutionary theories of aging are not ultimate completed theories, but rather a set of ideas that themselves require further elaboration and validation. This theoretical review article is written for a wide readership.
TABLE OF CONTENTS
Introduction
Why Did It Take So Long?
Evolutionary Theory of Aging vs. Life History Theory
Evolutionary Fundamentalism in Gerontology
Historical Evolution of Scientific Ideas on the Evolution of Aging
The Theory of Programmed Death
Weismann’s Evolutionary Theory and the Cell Division Limit
Evolution of Weismann’s Views on the Evolution of Aging
Testing the Theory of Programmed Death
Mutation Accumulation Theory of Aging
“Pay Later” Theory: Antagonistic Pleiotropy Theory of Aging
Implications for Aging Research
Acknowledgments
INTRODUCTION
There is a growing interest in the topic of aging and in the search for a general theory that can explain what aging is and why and how it happens. There is also a need for a general theoretical framework that may allow researchers to handle an enormous amount of diverse observations related to aging phenomena. Empirical observations on aging have become so numerous and abundant that a special encyclopedia, The Macmillan Encyclopedia of Aging, is now required for even a partial coverage of the accumulated facts[1]. To transform these numerous and diverse observations into a comprehensive body of knowledge, a general theory of species aging and longevity is required.
A general theory of aging may come in the future from a synthesis between systems theory (reliability theory) and specific biological knowledge. Reliability theory is a general theory about systems failure, which allows researchers to predict age-related failure kinetics for a system of given architecture (reliability structure) and given reliability of its components. As for specific biological knowledge, many researchers believe that it could be provided by evolutionary theories of aging based on the Darwinian theory of biological evolution by natural selection.
The purpose of this article is to provide a balanced scientific discussion of the evolutionary theories of aging, which evolutionary biologists suggest as “the intellectual core of gerontology”. Such a discussion of the evolutionary theories of aging is needed, and it may be particularly useful for students and researchers entering the field of aging studies. This article will also provide them with an orientation to the abundant scientific literature on the evolution of aging, which requires knowledge of the historical background, i.e., how these evolutionary ideas evolved themselves over time. While working on this article, we found that the scientific literature on evolutionary gerontology should be handled with great care because the significance of some publications could only be understood in the context of related studies made by other researchers.
Evolutionary theories of aging and longevity are those theories that try to explain the remarkable differences in observed aging rates and longevity records across different biological species (compare, for example, mice and humans) through interplay between the processes of mutation and selection. The appeal for understanding the biological evolution of aging and lifespan comes also from puzzling observations of the life cycles of some biological species. For example, a bamboo plant reproduces vegetatively (asexually) for about 100 years, forming a dense stand of plants. Then in one season all of the plants flower simultaneously, reproduce sexually, and die. About 100 years later (depending on the exact bamboo species) the process is repeated. This intriguing observation, as well as other similar observations of “suicidal” life cycles of species like pacific salmon, has promoted the idea that sexual reproduction may come with a cost for species longevity. Thus, in addition to mutation and selection, the reproductive cost, or, more generally, the trade-offs between different traits of organisms may also contribute to the evolution of species aging and longevity. The evolutionary theories of aging are closely related to the genetics of aging because biological evolution is possible only for heritable manifestations of aging.
