Expanding evolutionary theories of ageing to better account for symbioses and interactions throughout the Web of Life

Abstract

How, when, and why organisms age are fascinating issues that can only be fully addressed by adopting an evolutionary perspective. Consistently, the main evolutionary theories of ageing, namely the Mutation Accumulation theory, the Antagonistic Pleiotropy theory, and the Disposable Soma theory, have formulated stimulating hypotheses that structure current debates on both the proximal and ultimate causes of organismal ageing. However, all these theories leave a common area of biology relatively under-explored. The Mutation Accumulation theory and the Antagonistic Pleiotropy theory were developed under the traditional framework of population genetics, and therefore are logically centred on the ageing of individuals within a population. The Disposable Soma theory, based on principles of optimising physiology, mainly explains ageing within a species. Consequently, current leading evolutionary theories of ageing do not explicitly model the countless interspecific and ecological interactions, such as symbioses and host-microbiomes associations, increasingly recognized to shape organismal evolution across the Web of Life. Moreover, the development of network modelling supporting a deeper understanding on the molecular interactions associated with ageing within and between organisms is also bringing forward new questions regarding how and why molecular pathways associated with ageing evolved. Here, we take an evolutionary perspective to examine the effects of organismal interactions on ageing across different levels of biological organisation, and consider the impact of surrounding and nested systems on organismal ageing. We also apply this perspective to suggest open issues with potential to expand the standard evolutionary theories of ageing.

Keywords: Evolutionary theory of ageing; Microbiomes; Networks; Pluralism; Symbioses; Units of selection.

Fig. 1.

Visual summary of some key sources of open issues about the evolution of ageing. The classic evolutionary theories of ageing are collectively highlighting numerous important issues about the evolution of ageing (yellow bulb), but several open issues (in black font, under lighter bulbs, in the grey area) could benefit from embracing a plurality of additional perspectives (in orange font, over the lighter bulbs). Embracing these perspectives more systematically could ultimately highlight several reticulate dimensions of the evolution of organismal ageing, consistently with a rich scientific literature showing that organismal ageing is affected by interactions from diverse biological systems surrounding the ageing organism and by interactions from biological systems nested within the ageing organism.