The Origins of Aging: Evidence that Aging is an Adaptive Phenotype

Aging can be defined as the time-related decline in biological functions which ultimately results in organismal death. Beyond the stage of reproductive maturity as fertility declines, cell and tissue functions come under reduced selection pressure since organismal survival is considered no longer an evolutionary priority. Repair mechanisms become less robust and the resulting stochastic accumulation of tissue and genomic damage is believed to underlie the aging process. The objective of this review is to challenge this construct and to present evidence that aging represents a species-specific adaptive developmental program.

Through a review of published data, the cellular aging programs of both single cell and multicellular organisms are described. Since all organisms live in communities (ecosystems) of diverse species, the role of multi-level selection is discussed within this context and a proposal is advanced that aging represents an adaptive phenotype.

Single cell organisms evolved an aging phenotype in which the primary feature was replicative arrest prior to cell death. The evolution of multicellularity represented the emergence of a new level of biological organization. Multicellularity required cell-cell cooperation as well as a division of labor. In simple multicellular organisms aging was rooted in an age-related decline in stem cell function (renewal and differentiation). In complex multicellular organisms cellular aging/ death programs (senescence, autophagy, apoptosis) were used as a form of cell "altruistic" suicide carried out for the benefit of the whole organism (morphogenesis, tissue repair and maintenance). Organisms do not live in isolation. Species occupy ecological niches and communities of diverse species comprise an ecosystem. Ecosystems are highly regulated and structured biological organizations. The effective functioning and productivity of an ecosystem is determined by its biological diversity and relative species densities. Multilevel selection acts to balance optimal functioning of both the whole ecosystem and its compositional species/organisms.

Organismal aging and death programs are adaptive; these programs provide a mechanism for regulating species population densities within the constraints imposed by the ecosystem organization. A unique feature of humans has been the development of a second inheritance system, culture. Through cultural practices, humans have expanded our ecological niche to be global in size. Our technology enriched urban ecosystem is very different from natural ecosystems. Our future evolution, including aging and lifespan, will be determined by our unique urban ecosystem through geneculture co-evolution.