Abstract
Aging is an elusive property of life, and many important questions about aging depend on its definition. This article proposes to draw a definition from the scientific literature on aging. First, a broad review reveals five features commonly used to define aging: structural damage, functional decline, depletion, typical phenotypic changes or their cause, and increasing probability of death. Anything that can be called ‘aging’ must present one of these features. Then, although many conditions are not consensual instances of aging, aging is consensually described as a process of loss characterized by a rate and resulting from the counteraction of protective mechanisms against mechanisms that limit lifespan. Beyond such an abstract definition, no one has yet succeeded in defining aging by a specific mechanism of aging because of an explanatory gap between such a mechanism and lifespan, a consensual explanandum of a theory of aging. By contrast, a sound theoretical definition can be obtained by revisiting the evolutionary theory of aging. Based on this theory, aging evolves thanks to the impossibility that natural selection eliminates late traits that are neutral mainly due to decreasing selective pressure. Yet, the results of physiological research suggest that this theory should be revised to also account for the small number of different aging pathways and for the existence of mechanisms counteracting these pathways, that must, on the contrary, have been selected. A synthetic, but temporary definition of aging can finally be proposed.
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Notes
This paper will thus rely heavily on the scientific literature. It follows Carnap’s views on explication (or rational reconstruction) as a preliminary work useful for science (Wagner 2012). It is not only descriptive, but also constructive whenever useful, and reflects important uncertainties instead of trying to solve them.
Most of the references cited in this article are among the most cited in their field (according to Web of Science). This does not necessarily make them the most interesting, but they are arguably the most representative.
In humans and many mammals. Depending on how it is defined, sarcopenia is not necessarily a universal trait. An interesting discussion of the aging phenotype of C. elegans can be found in (Garigan et al. 2002).
The choice of a defining feature has empirical consequences. For example, sarcopenia can be interpreted in terms of structural decay and measured as a loss of muscular mass, but also in functional terms, as a loss of strength, or even in terms of the muscle mass/strength ratio (Doherty 2003). It can be used as a sign predictive of disability (Guralnik et al. 1995) or even death.
Thanks to an anonymous referee for suggesting the analogy.
Concepts, such as lifespan and longevity, should nevertheless be clarified as well.
Typically, Rose (1995) starts with a definition based on common sense then provides one based on his theory (see below).
An alternative is the reliability theory of aging (Gavrilov and Gavrilova 2001, 2003). Reliability is the probability that a physiological system (organism, organ, etc.) fulfils its role at a given point in its lifetime. This forms the basis of the definition of a mathematical function that represents the accumulation of causes of potential failures of the system. The shape of the resulting curve lies between two extremes: exponential increasing (Gompertz’s law of mortality) and exponentially decreasing/increasing (Weibull’s law) functions, respectively corresponding to systems with many redundant but less reliable components and to systems with few, non-redundant but extremely reliable components. A simple definition would be: aging is the progressive disappearance of the parts of a system that make it reliable, according to a pattern lying between Gompertz’s law and Weibull’s law. In this view, the diversity of the pathways of aging is lost, but the main feature is probably conserved.
I contrast an age-structured population with an age-structured model of a population. In the former, traits do differ importantly depending on age and not all populations are age-structured, while in the latter, any population can in principle be age-structured, although differing traits are not necessarily important. Hamilton (1966) has described and formalized these effects on a population, but he did not clearly stated that age structure is a condition of the evolution of aging. See also (Charlesworth 1994).
Different definitions of ‘extrinsic cause of death’ have been used. I consider this one to be the most consistent with the theory of the evolution of aging.
Thanks to an anonymous reviewer for pointing this to me. The reviewer also objected, rightly I think, that if fecundity increases with age, the force of natural selection should not decrease as much (or at all) with age. In this case, this should be added as a condition to the evolution of aging.
Slightly different formalized versions of the evolutionary theory of aging can be found in Rose (1995, Martin et al. (1996), Bengtson et al. (2008). I emphasize logical independence rather than chronological sequence. I also choose to present the main result of the disposable soma theory as an additional, independent condition for aging to evolve. Some think that it is just a case of antagonistic pleiotropy. Kirkwood himself sees them as complementary: while the antagonistic pleiotropy theory explains that variations limiting longevity are selected because they enhance early maintenance, the disposable soma theory explains that variations that limit early maintenance and longevity are selected because they enhance early reproduction (Kirkwood and Rose 1991). In this account, I consider the condition of limited maintenance to be Kirkwood’s truly original contribution. An additional question is whether the contribution of biodemography is original (Carey and Vaupel 2006).
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Thanks to the Conceptual Biology and Medicine Group in Bordeaux, and most particularly to Jean-François Moreau, for reading and commenting on earlier versions of the paper. The final version has improved thanks to the objections of one anonymous referee.
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