Arguing that Selection Pressure Diminishes with Age Even in Immortals

Evolutionary arguments relating to aging are tricky things, typically hinging on details that can be credibly argued either way. You might look at the recent resurrection of group selection in the service of explaining the origins of aging, for example. This is a much debated area of theory, with little in the way of true consensus on exactly why it is that near all species undergo aging. Fortunately, an explanation for aging isn't strictly necessary in order to make inroads into addressing the processes of aging as we observe them today, but evolutionary theories considered in general have in the past proven to be very helpful guides in a variety of medical research. The molecular biochemistry of living beings is vast and enormously complex, and researchers have to start their investigations somewhere.

As old as the evolutionary theory of senescence is its underlying and widespread tenet that senescence evolves because survivorship dwindles with age. Consequently, higher mortality should lead to more senescence. In contrast, several authors have indisputably shown over the last decades that this logic is incorrect. Yet, these results did not suffice to erase the prevailing misconception, which is problematic, because empirical studies keep on testing a theoretical prediction that is, as such, not predicted. What to do, when something repeatedly proven to be wrong is still taken to be right? Here we attempt to advance understanding of the evolutionary theories of aging conditional on survivorship. Clearly, survivorship falls over age, and clearly adding some fixed amount of mortality at every age makes survivorship fall off more steeply. But such a shift in mortality merely reduces fitness; it does not change the selection gradients over the fitness landscape. The selection gradients still decline following the same pattern as in the absence of such mortality; selection does not favor young over old ages more or less strongly than before.

When it comes to understanding why we age, the rarity of survival to old age alone has long served as the explanation for declining selection gradients. This seems curious, because life is driven by birth and death together. Why should one side - survivorship - suffice to explain fundamental patterns of life, such as aging? We have demonstrated that reproduction plays an important role. Births keep on adding new individuals to the population, fueling a population growth factor that reduces the share of old organisms in the population. Even in the absence of death, as we demonstrate, births are enough to achieve declining selection gradients. Mortality is not the all-important driver of selection gradients.

We argue that older organisms have already produced a larger share of their total lifetime reproduction. Therefore a progressively smaller proportion of total production is affected by anything that happens to an organism at higher ages, and the organism will already have passed on its genes. Whether a change at some age affects evolution to a smaller or larger degree hinges not on survivorship per se, but on the relative abundance of individuals and their reproductive values. Provided the population is non-decreasing, the stable age distribution is always dominated by younger individuals over older individuals as a result of reproduction. This is true even in the hypothetical case of zero mortality. Survivorship can be changed by an age independent mortality term without affecting the selection gradients. Similarly, changes in age independent mortality leave optimal strategies unaffected.

The arguments laid out in this paper have theoretical and practical consequences. Empirical research has shown little support for the "central prediction" of the evolutionary theory of senescence, that a higher level of extrinsic mortality (predators, harsh environments, laboratory manipulations) should lead to a higher rate of senescence. A number of authors have called for a more involved theory of senescence, in which mortality is state dependent, and/or in which density effects play a prominent role. The results derived here and elsewhere make clear why there is little support for the central prediction. It is not just that this prediction is not born out in biological reality; life history theory simply makes no such prediction. After decades of theoretical work, we are still challenged to develop theory that provides more than an incidental match with the data. Our results corroborate the need for theory that is more involved; it may include combinations of age- and stage-specific mortality, density effects, and/or interaction mortality. Such a theory should involve mechanisms of senescence, as evolutionary pressures alone are only half the story.



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