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

• Published in: Ageing research reviews 2023-08, Vol.89, p.101982-101982, Article 101982
• Main Authors: Bapteste, Eric, Huneman, Philippe, Keller, Laurent, Teulière, Jérôme, Lopez, Philippe, Teeling, Emma C., Lindner, Ariel B., Baudisch, Annette, Ludington, William B., Franceschi, Claudio
• Format: Article
• Language: English
• Subjects: Aging - genetics; Biological Evolution; Evolutionary theory of ageing; Humans; Life Sciences; Microbiomes; Networks; Pluralism; Symbioses; Units of selection
• ISSN: 1568-1637; 1872-9649; 1872-9649
• DOI: 10.1016/j.arr.2023.101982

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. •Ageing organisms belong to networks of molecular, ecological and social interactions.•How surrounding or nested systems impact organismal ageing is yet to be characterized.•Focusing on hybridization, (endo)symbioses and social interactions raises open issues.•Using concepts of individuality, unit of selection and fitness measures raises issues.•Network analyses may help understand the evolution of ageing across the Web of Life.