Abstract
The classical evolutionary theories of aging suggest that aging evolves due to insufficient selective pressure against it. In these theories, declining selection pressure with age leads to aging through genes or resource allocations, implying that aging could potentially be stalled were genes, resource allocation, or selection pressure somewhat different. While these classical evolutionary theories are undeniably part of a description of the evolution of aging, they do not explain the diversity of aging patterns, and they do not constitute the only possible evolutionary explanation. Without denying selection pressure a role in the evolution of aging, we argue that the origin and diversity of aging should also be sought in the nature and evolution of organisms that are, from their very physiological make up, unmaintainable. Drawing on advances in developmental biology, genetics, biochemistry, and complex systems theory since the classical theories emerged, we propose a fresh evolutionary-mechanistic theory of aging, the Danaid theory. We argue that, in complex forms of life like humans, various restrictions on maintenance and repair may be inherent, and we show how such restrictions are laid out during development. We further argue that there is systematic variation in these constraints across taxa, and that this is a crucial factor determining variation in aging and lifespan across the tree of life. Accordingly, the core challenge for the field going forward is to map and understand the mosaic of constraints, trade-offs, chance events, and selective pressures that shape aging in diverse ways across diverse taxa.
Highlights
An evolutionary theory of aging should answer two key questions
We call our theory the “Danaid theory of aging” because we propose that organismal biology and physiology are like the leaky vessels of the Danaids, unable to hold life in them eternally due to constraints in their basic structure
This metaphor creates a clear contrast with programmed theories of aging, and with classical evolutionary theories relying on trade-offs and selection pressure
Summary
An evolutionary theory of aging should answer two key questions. First, why could aging evolve, given that, all else being equal, an individual’s fitness should be maximized by living as long as possible? Second, why do patterns of aging vary across the tree of life the way they do (Omotoso et al, 2021)? The classical evolutionary theories of aging have long provided a convincing answer to the first question (Medawar, 1952; Williams, 1957; Hamilton, 1966; Kirkwood, 1977). We propose a novel theory, The Danaid Theory of aging, that builds on existing theory, links mechanisms with evolution, and can simultaneously answer both questions. It integrates the previous theories with a modern understanding of development, aging biology, complex systems, and genetic control, contextualizing when previous theories may be key drivers, and when other forces may dominate the evolution of aging and lifespan. We propose a framework in which specific types of mechanistic constraints complement the declining force of selection to explain the diversity of aging patterns, showing that evolutionary and mechanistic theories are inextricably intertwined. We consider how this theory interacts with our knowledge about the diversity of aging processes across taxa
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