Senescence as an Adaptive Trait

SENESCENCE AS AN ADAPTIVE TRAIT R. D. GUTHRIE* There is a growing consensus among gerontologists that senescence, the degenerative phenomenon accompanying aging, is not a direct product of natural selection [i]. They contend either that senescence occurs at a point in the ontogeny when the reproductive value is so low that selection would be inoperative [2, 3] or that senescence is subject to natural selection only indirectly, when it is bound genetically with other characters [4, 5]. The popularity ofthese "non-adaptive" theories is not difficult to understand . Most ofthe evolutionary theories about senescence, which directly invoke natural selection, have been rather unsatisfying. Although there may be exceptions to the efficacy of natural selection [6], the process is so general that a character which is seemingly outside its realm necessarily attracts attention. Ifin such situations we are able to find a plausible alternative model utilizing natural selection, it generally proves to be the more attractive explanation. It was this challenge that drew me to the question of the evolution of senescence. Many authors have referred to senescence as having evolved, and have pointed out several ofits advantages [e.g., 7, 8, 9]. Wynne-Edwards [10], as well as suggesting an advantageous feature ofsenescence, has also postulated a selection mechanism. According to him, its cardinal advantage is to regulate density, thus keeping the population as near as possible to its optimal rate ofdispersion. He has further stated that any specific senescence behavior, since it is only adaptive to the group, must have evolved by "intergroup selection." Williams [11] and Lack [12] have criticized intergroup selection as a general mode ofevolutionary change, and there * Department of Biological Sciences, University of Alaska, College, Alaska. Part of this work was done under National Science Foundation grant GB-335S. I am grateful to Drs. Leigh Van Valen, David Klein, Robert S. Bader, and Vemon Harms for their advice and constructive criticisms of the theory. 313 seems to be a firm basis for their criticism, particularly in this instance. The idea of intergroup selection and its relation to senescence are discussed in more detail later. Unlike Wynne-Edwards, most gerontologists who think senescence is adaptive have only outlined the advantages to the organism or group of organisms. However, merely postulating thepossible benefits derivedfrom a character, without discussing the selection mechanics involved in its evolution, does not constitute a complete evolutionary explanation. This latter step has presented the key part ofthe problem. Ifwe suppose that senescence can be explained by selection acting between individuals rather than between groups, it is the apparent absence ofpressures which select for senescence, that is, shorten potential longevity, that present the most difficulty. Possible selection pressures which extend potential longevity, that is, postpone senescence, can easily be found. All other things being equal, the longer one lives the more offspring, theoretically, one should be able to contribute to future generations, thereby selecting for the genetic variants which contribute to longevity. In the ensuing discussion I have proposed a theory outlining one ofthe possible means whereby senescence can be controlled by selection within a population. The model accounts for the selection pressures acting both to decrease and to increase the expression ofsenescence. There are situations where members ofa species can contribute more of their genotype to future generations by living a short life and other situations where a long life makes the greater contribution. These opposing selection forces act as balanced stabilizing pressures which maintain a characteristic mode of senescence for each species. The evolution of senescence occurs when a disequilibrium of these pressures results in directional selection and, eventually, a change in the balance fulcrum. The equilibrium point and the strength ofthe stabilizing pressures are determined by the species' particular ecological situation. Selection Balance within the Population It is unexpected, in view ofthe recent emphasis on the important role of stabilizing selection in population genetics, that no evolutionists have applied it to senescence. One can visualize a conceptual model, based on a balance of selection pressures acting within a given population, that could be responsible for the regulation ofsenescence. For an introduction 314 J?. D. Guthrie · Senescence as an Adaptive Trait Perspectives in Biology and Medicine · Winter 1969 to the idea we...