Abstract
Despite tremendous progress in recent years, our understanding of the evolution of ageing is still incomplete. A dominant paradigm maintains that ageing evolves due to the competing energy demands of reproduction and somatic maintenance leading to slow accumulation of unrepaired cellular damage with age. However, the centrality of energy trade-offs in ageing has been increasingly challenged as studies in different organisms have uncoupled the trade-off between reproduction and longevity. An emerging theory is that ageing instead is caused by biological processes that are optimized for early-life function but become harmful when they continue to run-on unabated in late life. This idea builds on the realization that early-life regulation of gene expression can break down in late life because natural selection is too weak to optimize it. Empirical evidence increasingly supports the hypothesis that suboptimal gene expression in adulthood can result in physiological malfunction leading to organismal senescence. We argue that the current state of the art in the study of ageing contradicts the widely held view that energy trade-offs between growth, reproduction, and longevity are the universal underpinning of senescence. Future research should focus on understanding the relative contribution of energy and function trade-offs to the evolution and expression of ageing.
Highlights
It is remarkable that after a seemingly miraculous feat of morphogenesis a complex metazoan should be unable to perform the much simpler task of merely maintaining what is already formed.—George C
It was originally believed that ageing is restricted only to humans, captive animals, and livestock because animals in nature die from predation, competition, and parasites before they senesce
Evolutionary biologists and biogerontologists have sought to understand why ageing evolves, what determines variation in lifespan and rates of ageing, what are the proximal causes of ageing, and are they evolutionarily conserved? Such an understanding requires an integrated approach in which evolutionary concepts are used to guide the research into the mechanisms of ageing, while knowledge of the mechanisms is used to support or reject different evolutionary theories
Summary
It is remarkable that after a seemingly miraculous feat of morphogenesis a complex metazoan should be unable to perform the much simpler task of merely maintaining what is already formed. There is a remarkable diversity in the patterns of ageing across the tree of life, with some species showing negligible rates of senescence in either age-specific reproduction, mortality, or both [4]. To explain this variation, evolutionary biologists and biogerontologists have sought to understand why ageing evolves, what determines variation in lifespan and rates of ageing, what are the proximal causes of ageing, and are they evolutionarily conserved? 2 age-specific gene effect fitness positive negative selection shadow lifespan neutral energy trade-offs negative age Figure 1. The colours along the selection gradient line represent the effect of an antagonistically pleiotropic (AP) allele on fitness across the life course, from positive green early in life to strongly negative red in late life. Under functional trade-offs, optimizing gene expression in adulthood improves both fitness and lifespan, without developmental costs. (Online version in colour.)
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