A novel classification system for evolutionary aging theories

Abstract

Theories of lifespan evolution are a source of confusion amongst aging researchers. After a century of aging research the dispute over whether the aging process is active or passive persists and a comprehensive and universally accepted theoretical model remains elusive. Evolutionary aging theories primarily dispute whether the aging process is exclusively adapted to favor the kin or exclusively non-adapted to favor the individual. Interestingly, contradictory data and theories supporting both exclusively programmed and exclusively non-programmed theories continue to grow. However, this is a false dichotomy; natural selection favors traits resulting in efficient reproduction whether they benefit the individual or the kin. Thus, to understand the evolution of aging, first we must understand the environment-dependent balance between the advantages and disadvantages of extended lifespan in the process of spreading genes. As described by distinct theories, different niches and environmental conditions confer on extended lifespan a range of fitness values varying from highly beneficial to highly detrimental. Here, we considered the range of fitness values for extended lifespan and develop a fitness-based framework for categorizing existing theories. We show that all theories can be classified into four basic types: secondary (beneficial), maladaptive (neutral), assisted death (detrimental), and senemorphic aging (varying between beneficial to detrimental). We anticipate that this classification system will assist with understanding and interpreting aging/death by providing a way of considering theories as members of one of these classes rather than consideration of their individual details.

Keywords: altruism; caloric restriction; evolution; longevity; senemorphism; senescence.

FIGURE 1

Aging and death theories can be classified into two groups: (1) causality theories which address questions of how aging and death occur and can be subdivided into entropy-based processes and “sudden death.” (2) Evolutionary theories which try to explain why species age and die in the way they do. They consist of programmed aging, non-programmed aging and senemorphic aging which is a special case where parallel evolution of “senemorphisms” (independent aging phenotypes encoded by the genome) are related to both a genetic profile to accelerate aging and a genetic profile to maximize lifespan.

FIGURE 2

Maladaptive aging theories. Illustration of “Mutation Accumulation Theory.” Here the probability of an individual being dead (P(dead), red) increases over time solely due to harsh extrinsic mortality. Consequently the likelihood of successful reproduction (P(reproduction)) at any given time decreases over time (blue). The increasing probability of being dead acts as the main force restricting the selection for longer lifespan. It is reasonable to assume that there is no selective pressure for longevity after a certain threshold at which the likelihood of reproducing is very low. In this case the fitness associated with extended lifespan is neutral. Here death is supposed to occur before senescence has an effect, thus senescence is not necessary to affect the probability of death. M, maturity.

FIGURE 3

Secondary aging theories. This class of evolutionary aging theory assumes that a continuous trade-off restricts selection for longer lifespan. (A) Example representing “Antagonistic Pleiotropy” where selection for longevity is assumed to be restricted due to the pressure for faster reproduction. Here a fitter individual (F) is able to produce two offspring with generation time, t. After 2t, individual F has four descendents. In this case, fast reproduction is supposed to cause a side effect on body homeostasis (shown by jagged edges and non-green color) and to minimize regeneration (curly arrow with red cross). A more slowly reproducing individual (S), although more able to regenerate and limit deterioration, is unable to compete under these conditions, as it produces only two descendents in 2t. (B) Example representing “Disposable Soma” where selection for longevity is assumed to be restricted due to optimized, efficient utilization of energy (e) for reproduction. Here the fitter individual (F) uses more of the energy consumed to produce offspring rather than regenerate its own body. As a result it deteriorates faster but produces more offspring than an individual (S) which uses more energy for regeneration.