Modalities of aging in organisms with different strategies of resource allocation

Abstract

Although the progress of aging research relies heavily on a theoretical framework, today there is no consensus on many critical questions in aging biology. I hypothesize that a systematic analysis of the intersection of different evolutionary mechanisms of aging with diverse resource allocation strategies in different organisms may reconcile aging hypotheses. The application of disposable soma, mutation accumulation, antagonistic pleiotropy, and life-history theory is considered across organisms with asexual reproduction, organisms with sexual reproduction and indeterminate growth in different conditions of extrinsic mortality, and organisms with determinate growth, with endotherms/homeotherms as a subgroup. This review demonstrates that different aging mechanisms are complementary to each other, and in organisms with different resource allocation strategies they form aging modalities ranging from immortality to suicidal programs. It also revamps the role of growth arrest in aging. Growth arrest evolved in many different groups of organisms as a result of resource reallocation from growth to reproduction (e.g., semelparous animals, holometabolic insects), or from growth to nutrient storage (endotherms/homeotherms). Growth arrest in different animal lineages has similar molecular mechanisms and similar consequences for longevity due to the conflict between growth-promoting and growth-suppressing programs and suppression of regenerative capacity.

Keywords: Determinate growth; Endotherm; Homeotherm; Iteroparity; MTOR; Semelparity.

Fig. 1.

Resource allocation strategies. A – in organisms with indeterminate growth and asexual reproduction, resources are converted into somatic growth. Given that offspring are produced from body parts of the parental organism, the use of resources for growth is equivalent to the use of resources for reproduction. B – organisms with indeterminate growth and sexual reproduction living in conditions of low extrinsic adult mortality. Most resources are used for growth and a small portion is regularly diverted to reproduction. C, D – semelparous organisms and holometabolic insects in which resources are used for growth in the early stage of life (C), and later diverted completely to reproduction (D). This strategy is associated with growth arrest upon maturation. E, F – homeothermic organisms (birds and mammals) in which resources are used for growth at the early stages of life (E) and later diverted to nutrient storage and reproduction. This strategy is also associated with growth arrest upon maturation.

Fig. 2.

Modalities of aging in organisms with indeterminate growth and sexual reproduction. Adult and juvenile survival (horizontal axis) determine reproductive strategies in a continuum ranging from extreme semelparity to iteroparity. In iteroparous organisms, aging trajectories are determined by age-dependent changes in fitness. If fitness is increasing with age, no evolutionary mechanisms of aging will work, and the organism may gain immortality. If fitness is decreasing or not changing with age, evolutionary mechanisms triggered by extrinsic mortality will result in entropy-driven aging.

Fig. 3.

Structure of aging mechanisms. The balance between entropy-driven damage (left) and somatic maintenance (right) determines organisms’ longevity. The efficiency of somatic maintenance mechanisms is limited by evolutionary constraints (center). Pro-aging factors are shown in testaceous, and anti-aging factors are shown in green.