Programmed versus non-programmed evolution of aging. What is the evidence?

Pamplona, Reinald; Jové, Mariona; Gómez, José; Barja, Gustavo

doi:10.1016/j.exger.2023.112162

Cited by 7 publications

(1 citation statement)

References 118 publications

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“…This view has been disputed on several fronts. Demographers have undermined the claim that senescence is inevitable, both theoretically [ 9 – 11 ] and empirically [ 12 – 14 ], and several authors have recently turned to Weismann’s suggestion that programmed aging (i.e., that there are specific senescence genes), or the direct selection for a life end, can indeed evolve as an adaptation in its own right [ 15 – 19 ]. Contrarily to the claim by non-programmed aging theories ([ 20 ], p. 39) that “Death from senescence is itself in many species so rare an event in the wild state that failure to senesce early, or at all, has little value from the point of view of survival,” there is ample evidence that aging does happen in wild populations [ 21 – 26 ].…”

Section: Introductionmentioning

confidence: 99%

Directional selection coupled with kin selection favors the establishment of senescence

Szilágyi,

Czárán,

Santos

et al. 2023

BMC Biol

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Background Conventional wisdom in evolutionary theory considers aging as a non-selected byproduct of natural selection. Based on this, conviction aging was regarded as an inevitable phenomenon. It was also thought that in the wild organisms tend to die from diseases, predation and other accidents before they could reach the time when senescence takes its course. Evidence has accumulated, however, that aging is not inevitable and there are organisms that show negative aging even. Furthermore, old age does play a role in the deaths of many different organisms in the wild also. The hypothesis of programmed aging posits that a limited lifespan can evolve as an adaptation (i.e., positively selected for) in its own right, partly because it can enhance evolvability by eliminating “outdated” genotypes. A major shortcoming of this idea is that non-aging sexual individuals that fail to pay the demographic cost of aging would be able to steal good genes by recombination from aging ones. Results Here, we show by a spatially explicit, individual-based simulation model that aging can positively be selected for if a sufficient degree of kin selection complements directional selection. Under such conditions, senescence enhances evolvability because the rate of aging and the rate of recombination play complementary roles. The selected aging rate is highest at zero recombination (clonal reproduction). In our model, increasing extrinsic mortality favors evolved aging by making up free space, thereby decreasing competition and increasing drift, even when selection is stabilizing and the level of aging is set by mutation-selection balance. Importantly, higher extrinsic mortality is not a substitute for evolved aging under directional selection either. Reduction of relatedness decreases the evolved level of aging; chance relatedness favors non-aging genotypes. The applicability of our results depends on empirical values of directional and kin selection in the wild. Conclusions We found that aging can positively be selected for in a spatially explicit population model when sufficiently strong directional and kin selection prevail, even if reproduction is sexual. The view that there is a conceptual link between giving up clonal reproduction and evolving an aging genotype is supported by computational results.

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Section: Introductionmentioning

confidence: 99%

Directional selection coupled with kin selection favors the establishment of senescence

Szilágyi,

Czárán,

Santos

et al. 2023

BMC Biol

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Seven knowledge gaps in modern biogerontology

Rattan

2024

Biogerontology

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Hayflick 2007a). This declaration was their rebuttal to a much earlier paper by the Nobel Laureate Peter Medawar that ageing was the last unsolved problem in biology (Medawar 1952). Both Holliday and Hayflick had based their proclamations on the assumption that, by the end of the twentieth century, a detailed description of the ageing phenotype at all levels of the biological organization was already achieved, possible molecular-genetic processes of longevity assurance were understood, and that explanations for the evolution of ageing and longevity were generally accepted.Since then, a tsunami of ageing interventional research publications and associated industry news has been dominating the biogerontological scene, often with naïve extrapolations, overhyped claims and empty promises. Several biogerontologists, demographers and ethicists have repeatedly drawn the attention of scientists and the general public to the pros and cons, hype and reality, fact and fiction of the socalled "anti-ageing" industry (

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