A unified framework for evolutionary genetic and physiological theories of aging

PLoS Biol. 2024 Feb 27;22(2):e3002513. doi: 10.1371/journal.pbio.3002513. eCollection 2024 Feb.

Abstract

Why and how we age are 2 intertwined questions that have fascinated scientists for many decades. However, attempts to answer these questions remain compartmentalized, preventing a comprehensive understanding of the aging process. We argue that the current lack of knowledge about the evolution of aging mechanisms is due to a lack of clarity regarding evolutionary theories of aging that explicitly involve physiological processes: the disposable soma theory (DST) and the developmental theory of aging (DTA). In this Essay, we propose a new hierarchical model linking genes to vital rates, enabling us to critically reevaluate the DST and DTA in terms of their relationship to evolutionary genetic theories of aging (mutation accumulation (MA) and antagonistic pleiotropy (AP)). We also demonstrate how these 2 theories can be incorporated in a unified hierarchical framework. The new framework will help to generate testable hypotheses of how the hallmarks of aging are shaped by natural selection.

MeSH terms

  • Biological Evolution*
  • Longevity* / genetics
  • Mutation Accumulation
  • Selection, Genetic

Grants and funding

J.-F. L. was supported by a grant from the Agence Nationale de la Recherche (EVORA - ANR-22-CE02-0021). J.-M.G. was supported by a grant from the Agence Nationale de la Recherche (DivInt - ANR-22- CE02-0020). A.A.M. was supported by a grant from ERC CoG (GermlineAgeingSoma 724909) and NERC (NE/W001020/1). J.A.M. was supported by nobody. D.H.N. and J.-F.L. were supported by a Royal Society International Exchange Grant (IEC\R2\181087). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.