Phenoptosis and the Evolution of Ageing

Abstract

Phenoptosis describes ageing as the evolved product of a genome‐based program to limit lifespan and thereby favour evolution. Previously, programmed ageing was deemed incompatible with Darwinian dogma that population evolution depends upon genetic diversity resulting from selection of traits that provide individual benefit. To avoid this conflict, phenoptosis employs evolvability, an alternative theory of evolution through which biological systems can acquire novel functions that enhance population evolution without individual benefit. This article analyses the claim that ‘programmed’ ageing evolved de novo, specifically to limit lifespan exclusively under the cloak of evolvability, and if certain assumptions in phenoptosis theory are valid. A brief historic perspective of its origins will be followed by considerations of ‘when’, ‘why’ and ‘how’ it evolved. An alternative ‘programmatic’ theory that presents a mechanism for the coincidental evolution of ageing with the developmental program will be compared and contrasted with phenoptosis.

Key Concepts

  • Individual benefit is incompatible with phenoptosis (programmed ageing) theory, but compatible with development/ageing continuum (programmatic ageing) theory.
  • Immortal/nonageing animals preceded the evolution of phenoptosis.
  • Phenoptosis relies exclusively upon ‘evolvability’ to explain the evolution of ageing, yet ageing promotes ‘evolvability’ thereafter.
  • In nonsenescing populations (presumably existing before phenoptosis), evolution would be stifled by low adult death rate.
  • Natural selection in immortal populations causes unchecked birth rates, overpopulation and subsequent extinctions. Phenoptosis then emerges as an adaptation.
  • Phenoptosis evolved by the process of ‘supra‐individual’ selection.
  • Selection for ecological homeostasis counterbalances selection for expanding individual reproductive fitness and keeps growth rates in check.
  • Scheduled death increases individual turnover, provides more chances for evolution of diverse genotypes and thereby, increases evolvability.
  • Programmatic ageing is a product of coincidental evolution resulting from post‐maturational decay of the developmental program and of second‐order selection for population benefit.
  • Ageing is initiated and accelerated by progressive loss of temporal organisation within the whole organism, not by any individual or few factors affecting single metabolic or physiologic functions.

Keywords: phenoptosis; programmed ageing; evolvability; development‐ageing continuum; programmatic ageing; coincidental evolution; second‐order selection; circadian rhythms; temporal order; homeodynamics

Figure 1. Structure of the circadian system. The retina captures photic information and transmits signals to the hypothalamic suprachiasmatic nucleus (SCN) which serves as the circadian coordinating center. It integrates light/dark cycles and nutrient cues from the environment, then relays appropriate signals to peripheral clocks. Cross talk between extrinsic signals and the clock network leads to oscillation of metabolites, ROS, hormones, etc. which taken together constitute individual “body time” and establish overall physiological homeodynamics of throughout life. Desynchronization and decay of the clock network initiates and exacerbates aging over time, ultimately causing intrinsic disease and death. Source: https://www.intechopen.com/books/molecular‐mechanisms‐of‐the‐aging‐process‐and‐rejuvenation/circadian‐clock‐gene‐regulation‐in‐aging‐and‐drug‐discovery. Licensed under CC by 3.0.
Figure 2. Examples of circadian rhythms in older adults relative to rhythms in younger adults. In the 24‐h cycle, documented changes include rhythms of waking activity; core body temperature; SCN firing; release of hormones; and fasting plasma glucose levels. In older adults, amplitude of many rhythms dampen and in some cases, the peak of the rhythm also advances. Reproduced with permission from Hood and Amir . © American Society for Clinical Investigation.
Figure 3. Hallmark processes of aging. This diagram summarizes the hallmark processes that are typically affected by dysregulation of integrated circadian rhythms during aging. Source: https://www.frontiersin.org/articles/10.3389/fneur.2015.00043/full. Licensed under CC by 4.0.
Figure 4. Decay of the circadian system begins and accelerates at the end of development as part of the aging process. Upon completion of development when stringent regulation of homeodynamics ends, there is a progressive loss of temporal order that is expressed initially as loss of vitality then accelerates through progressively waning physical performance to intrinsic diseases and ultimately to death. Reproduced with permission from Tevy et al. . © Elsevier.
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Walker, Richard F(Dec 2018) Phenoptosis and the Evolution of Ageing. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028293]