Evolutionary Approaches A Theories of Senescence

Both physiological and evolutionary senescence show genetic control, yet the details of our understanding of senescence at these two levels is very different (Bleecker, 1998). Physiological studies have demonstrated that within an individual plant, there is a genetic program which results in an orderly degenerative process leading either to the reabsorption of nutrients and the abscission of plant parts, or in the case of semelparous species, to the death of the whole organism (Nooden, 1988). Physiological senescence of plant parts is an active process that requires energy and protein synthesis and often involves the redistribution of nutrients and photosynthates. It is a beneficial process which increases an individual's chance for survival, for example by preparing a plant for harsh environmental conditions (e.g., winter), or by allowing a plant to shed unnecessary and inefficient structures.

Genetic control of evolutionary senescence is clear from the fact that there are species-specific differences in maximum life span and from the inheritance of longevity traits within populations. An evolutionary approach to the study of senescence seeks to understand the ultimate reasons why senescence occurs, and how we can explain variation in the rates of senescence between species. Given that there is genetic control of evolutionary senescence, it is interesting to ask why there has not been selection for increased longevity and perhaps even infinite life span. Instead, this phenomenon of senescence, which increases the probability of dying with increasing age, persists in populations and because of this, it is often considered to reflect a failure of natural selection to act against a deleterious trait.

The paradox of senescence from an evolutionary point of view is that, at the level of the individual, there is no scenario in which an increased rate of dying with age can be considered an adaptive trait, in other words a trait directly favored by natural selection. Historically, the one direct "adaptive" theory of senescence in the animal literature suggested that senescence was a mechanism to eliminate older, weaker, individuals from a population in order to conserve resources for younger more vigorous individuals (Weismann, 1889). Within the plant literature, it has been suggested that mortality will be selectively advantageous for an individual if it would result in a better chance for the immediate colonization of its offspring (Wilson, 1997). These hypotheses rely on the principles of group selection, and they can be shown to be theoretically improbable given that selection acts primarily at the level of the individual (Charlesworth, 1980).

Evolutionary theorists have alternatively suggested that senescence may be a non-adaptive trait which has evolved indirectly as a consequence of a selective premium on genes with favorable effects on survival or fecundity early in the life history. The key element to allow the evolution of senescence is the fact that the force of natural selection on survival and fertility necessarily decreases with age because organisms have a nonzero chance of dying from external causes such as predation and accidents. Medawar (1952) provided the foundation for the major theoretical progress on the evolution of senescence. He suggested that, even in the hypothetical complete absence of senescence, if constant fertility is assumed, the reproductive output of each age class declines with age, because survivorship from birth is a decreasing function of age. As a result, the relative importance of traits expressed at late ages, to the lifetime fitness of an individual, is less than the importance of traits expressed at earlier ages. This implies that the intensity of selection will be stronger on age-specific genes acting early in life, than it will on genes that affect traits later in life. Some genes, which have their effect at very late ages, after an organism is usually dead, can completely escape the influences of selection. The first direct experimental test of Medawar's hypothesis is presented later in this chapter (Section IIB).

With this major assumption, that natural selection is weaker at later ages, two major evolutionary theories, mutation accumulation and pleiotropy, have been proposed to explain the evolution and persistence of senescence in populations. The evolutionary theory of mutation accumulation suggests that due to the decline in the strength of selection on age-specific characters, mutations with a deleterious effect at the end of the life cycle will accumulate, resulting in a decrease in age-specific mortality and fecundity with increasing age (Medawar, 1952). In other words, because they will be effectively neutral, genes with deleterious effects will spread in the population because they affect only late-life traits. This type of mutation accumulation is distinct from the somatic mutations that may accumulate during the life of an individual. It refers instead to the large number of deleterious genes that are expressed at late ages and which persist in the population as a result of a change in the mutation-selection balance. The accumulation of mutations is thus due either to increasingly ineffective selection against recurrent deleterious mutations, or from genetic drift.

The second major evolutionary theory, antagonistic pleiotropy, suggests that genes affecting traits negatively late in life may get established in a population if those genes also have positive effects at an earlier age (Williams, 1957; Williams, 1957; for plant example see Roach, 1986). This theory is based on an optimality approach in which late-life performance is sacrificed for early survival or reproduction (Partridge and Barton, 1993). A closely related theory, the disposable soma theory, is a variation of the pleiotropy theory and incorporates a trade-off between reproduction, on the one hand, and maintenance and repair, on the other (Kirkwood and Holliday, 1979). This theory suggests that if there are a limited amount of resources available to the organism, then the allocation of energy to early reproduction will be favored at the expense of somatic maintenance and repair. Repair will consequently occur at a sub-optimal level leading to senescence. The lack of repair leads to an accumulation of damage to somatic cells and an increased probability of death at later ages. One of the primary assumptions of the disposable soma theory is that there is an early separation of germ line from the soma. This separation does not occur until just prior to reproduction in plants, yet as will be discussed later in this chapter, a violation of this assumption does not appear to be an important factor in the evolution of senescence.

The evolutionary theories of senescence suggest that the decline with age in reproduction and survival is the result of the failure of natural selection to act against genes with late age-specific effects (Charlesworth, 1980). The common thread of the evolutionary theories is that senescence is a consequence of a selective premium on genes with favorable effects on survival and fecundity early in the life history. The theories suggest that senescence is a trait that has evolved because of the absence of selection against degenerative changes in old age, or because of positive selection for mutations that increase early success even when they have later deleterious effects. There are several lines of evidence that can be used to evaluate the theories. First, the assumptions and predictions of the theories can be directly tested through experimental manipulation. Secondly, evidence needs to be obtained from demographic studies to determine whether there is, in fact, evidence for a change in mortality with increasing age, and to determine how species differ with respect to their mortality patterns. Both of these approaches will be used in the remainder of this chapter.

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