Evolution of Varied Life Spans without Antagonistic Pleiotropy

A successful evolutionary theory of aging must explain how a mix of species with shorter and longer life spans can emerge from a common ancestor with a longer life span. Putting theories of programmed aging to one side for a moment, as in that case one only has to argue that a shorter life span is more optimal for the ecological niche in question, antagonistic pleiotropy is the most readily available explanation for shorter lifespans to arise from natural selection. The theory here is that evolution selects for mechanisms and systems that both (a) ensure reproductive success in early life and (b) damage health in later life. There are all too many examples of biological systems that work well in childhood and youth, but inevitably fail because they are not capable of comprehensive repair and therefore accumulate damage, or because they are otherwise limited in some important capacity, and that limit will eventually be reached.

Can the evolution of shorter life spans appear in models without employing the assumption of antagonistic pleiotropy, and without invoking programmed aging, however? The authors of this paper argue that it can, and arises as an inevitable consequence of the dispersion of a population over the landscape. Interestingly, the details of the explanation touch on some of the same group dynamics - such as resistance to population collapse due to resource contention - that at least one programmed aging theorist employs to argue that aging must be selected. This is far from the only line of thought to approach group selection, which is still very much out of favor, while not being group selection.

With only a few exceptions, organisms deteriorate as they age and consequently die, but large variation in longevity still exists among species. A comparative study of 107 bird species found that fatty acid characteristics of cellular membranes have a prominent causative role in the aging process: species with longer maximum lifespans have higher proportions of long and monounsaturated fatty acids in their membranes. The question then arises as to why high proportions of long and monounsaturated fatty acids have not evolved in all species, given that this would maximize their lifespan and should therefore be promoted by natural selection, as aging is clearly detrimental for the fitness of individual organisms. In other words, why has a variability of lifespans evolved among species?

Evolutionary theory is still based on the antagonistic pleiotropy hypothesis: high mortality rates promote rapid reproduction, and direct selection for rapid reproduction leads to indirect selection for shorter lifespan. While this hypothesis has sometimes been supported by data from wild populations of animals, other empirical studies have frequently called into question the claimed role of extrinsic mortality in promoting senescence and the evolution of short lifespan.

Maybe as a response to this incapacity of the antagonistic pleiotropy hypothesis to provide a general explanation for the evolution of lifespan variability, some theoretical models have appeared in the last years based on the idea of programmed aging, stating that organisms have a genetically fixed senescence rate that is favored by natural selection because senescence may be adaptive in certain circumstances. These models have the important limitation of dealing with group selection, as they assume that senescence benefits lineages by avoiding overpopulation and associated problems such as resource depletion and epidemics, and thus lack an evolutionary logic. In fact, no genes exist that promote aging.

Here we propose that the evolution of lifespan is based on the ecological process of dispersal and does not depend on extrinsic mortality nor assume any adaptive benefit of aging, thus avoiding the above-mentioned limitations of group selection. Dispersal has previously been proposed in a theoretical model as a determinant of aging assuming that shorter dispersal distances create more competition for resources and shorter lifespans are then favored under such conditions because it would be beneficial for the lineages, therefore carrying the problems of group selection and programmed aging. Here we first provide theoretical arguments by which a similar dependence of lifespan evolution on dispersal distance can be achieved with basic concepts of population dynamics without the need of assuming adaptive group benefits or a genetic aging clock.

Our model considers that limited dispersal can generate, through reduced gene flow, spatial segregation of individual organisms according to lifespan. Individuals from subpopulations with shorter lifespan could thus resist collapse in a growing population better than individuals from subpopulations with longer lifespan, hence reducing lifespan variability within species. As species that disperse less may form more homogeneous subpopulations regarding lifespan, this may lead to a greater capacity to maximize lifespan that generates viable subpopulations, therefore creating negative associations between dispersal capacity and lifespan across species.

Link: https://doi.org/10.1002/ece3.4073


Clearly no species evolves in isolation; all are part of an intricate web of relationships with predator and prey populations. It seems intuitively obvious to me that a prey species whose individuals evolved a long lifespan would be more at risk from an aggressive and adaptive predator species than one that could evolve more quickly with a shorter lifespan and more rapidly turned-over population. Hence whilst an individual may evolve a longer lifespan, a species will pay for it.

The result is we tend to see animals lower in the food chain with shorter life spans. But when you evolve a really good defense like flight, a shell or great intelligence, you can start to become 'predator proof', and can then evolve a longer lifespan without danger you'll pay for it later.

If this is what is called 'group selection' these days, then so be it. To be it's just common sense and I see no need to tie myself in knots trying to come up with a theory that avoids selection at higher than the individual level.

Posted by: Mark at June 11th, 2018 7:50 AM

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