A unified framework for evolutionary genetic and physiological theories of aging

Jean François Lemaître; Jacob A. Moorad; Jean-Michel Gaillard; Alexei A Maklakov; Daniel H Nussey

doi:10.1371/journal.pbio.3002513

A unified framework for evolutionary genetic and physiological theories of aging

Jean François Lemaître^*, Jacob A. Moorad, Jean-Michel Gaillard, Alexei A Maklakov, Daniel H Nussey

^*Corresponding author for this work

School of Biological Sciences

Research output: Contribution to journal › Article › peer-review

Abstract / Description of output

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.

Original language	English
Article number	e3002513
Number of pages	38
Journal	PLoS Biology
Volume	22
Issue number	2
DOIs	https://doi.org/10.1371/journal.pbio.3002513
Publication status	Published - 27 Feb 2024

Access to Document

10.1371/journal.pbio.3002513

journal.pbio.3002513Final published version, 2.01 MBLicence: Creative Commons: Attribution (CC-BY)

Cite this

@article{7237f9268af54c31b5c6777356f88871,

title = "A unified framework for evolutionary genetic and physiological theories of aging",

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.",

author = "Lema{\^i}tre, {Jean Fran{\c c}ois} and Moorad, {Jacob A.} and Jean-Michel Gaillard and Maklakov, {Alexei A} and Nussey, {Daniel H}",

note = "Funding Information: 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. Authorship was ordered by random draw. Publisher Copyright: {\textcopyright} 2024 Lema{\^i}tre et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.",

year = "2024",

month = feb,

day = "27",

doi = "10.1371/journal.pbio.3002513",

language = "English",

volume = "22",

journal = "PLoS Biology",

issn = "1545-7885",

publisher = "Public Library of Science",

number = "2",

}

TY - JOUR

T1 - A unified framework for evolutionary genetic and physiological theories of aging

AU - Lemaître, Jean François

AU - Moorad, Jacob A.

AU - Gaillard, Jean-Michel

AU - Maklakov, Alexei A

AU - Nussey, Daniel H

N1 - Funding Information: 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. Authorship was ordered by random draw. Publisher Copyright: © 2024 Lemaître et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

PY - 2024/2/27

Y1 - 2024/2/27

N2 - 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.

AB - 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.

U2 - 10.1371/journal.pbio.3002513

DO - 10.1371/journal.pbio.3002513

M3 - Article

C2 - 38412150

SN - 1545-7885

VL - 22

JO - PLoS Biology

JF - PLoS Biology

IS - 2

M1 - e3002513

ER -

A unified framework for evolutionary genetic and physiological theories of aging

Abstract / Description of output

Access to Document

Fingerprint

Cite this