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Interspecific Interactions That Affect Ageing

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Interspecific interactions that affect ageing: age-distorters manipulate host ageing to their own evolutionary benefits Jérôme Teulière, Charles Bernard, Eric Bapteste To cite this version: Jérôme Teulière, Charles Bernard, Eric Bapteste. Interspecific interactions that affect ageing: age- distorters manipulate host ageing to their own evolutionary benefits. Ageing Research Reviews - ARR, Elsevier Masson, 2021, pp.101375. 10.1016/j.arr.2021.101375. hal-03250121 HAL Id: hal-03250121 https://hal.sorbonne-universite.fr/hal-03250121 Submitted on 4 Jun 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Journal Pre-proof Interspecific interactions that affect ageing: age-distorters manipulate host ageing to their own evolutionary benefits Jer´ omeˆ Teuli`ere, Charles Bernard, Eric Bapteste PII: S1568-1637(21)00122-7 DOI: https://doi.org/10.1016/j.arr.2021.101375 Reference: ARR 101375 To appear in: Ageing Research Reviews Received Date: 27 January 2021 Revised Date: 22 May 2021 Accepted Date: 26 May 2021 Please cite this article as: Teuli`ere J, Bernard C, Bapteste E, Interspecific interactions that affect ageing: age-distorters manipulate host ageing to their own evolutionary benefits, Ageing Research Reviews (2021), doi: https://doi.org/10.1016/j.arr.2021.101375 This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier. Interspecific interactions that affect ageing: age-distorters manipulate host ageing to their own evolutionary benefits Jérôme Teulièrea, Charles Bernarda, Eric Baptestea,*. aInstitut de Systématique, Evolution, Biodiversité (ISYEB), Sorbonne Université, CNRS, Museum National d'Histoire Naturelle, EPHE, Université des Antilles, Paris, France. *Corresponding author. E-mail address: [email protected] Highlights Genetic causes of cell/organismal ageing external to a focal species may be neglected Many age-distorters may interfere with ageing in other species for their own interest Co-evolution/arms races with age-distorters would affect genetics of ageing evolution Genes in viruses, (endo)parasites/symbionts may often turn hosts into disposable soma Modelling age-distorters can expand the scope of major non adaptive theories of ageing Abstract Genetic causes for ageing are traditionally investigated within a species. Yet, the lifecycles of many organisms intersect. Additional evolutionary and genetic causes of ageing, external to a focal species/organism, may thus be overlooked. Here, we introduce the phrase and concept of age-distorters and its evidence. Age-distorters carry ageing interfering genes, used to manipulate the biological age of other entities upon which the reproduction of age-distorters relies, e.g. age-distorters bias the reproduction/maintenance trade-offs of cells/organisms for their own evolutionary interests. Candidate age-distorters include viruses, parasites and symbionts, operating through specific, genetically encoded interferences resulting from co- evolution and arms race between manipulative non-kins and manipulable species. This interference results in organismal ageing when age-distorters prompt manipulated organisms to favor their reproduction at the expense of their maintenance, turning these hosts into expanded disposable soma. By relying on reproduction/maintenance trade-offs affecting disposable entities, which are left ageing to the reproductive benefit of other physically connected lineages with conflicting evolutionary interests, the concept of age-distorters expands the logic of the Disposable Soma theory beyond species with fixed germen/soma distinctions.Journal Moreover, acknowledging age-distorters Pre-proof as external sources of mutation accumulation and antagonistic pleiotropic genes expands the scope of the mutation accumulation and of the antagonistic pleiotropy theories. Keywords Antagonistic pleiotropy; Disposable soma theory; Mutation accumulation theory ; virus ; evolutionary conflict; symbiont; parasite; coevolution Introduction A broad range of cellular organisms, from microbes to animals and plants, have been shown to age physiologically and even replicatively, prompting the search for the proximal and ultimate causes of ageing across increasingly larger portions of the Tree of Life. Accordingly, diverse kinds of biochemical, ecological and evolutionary processes and events have been proposed to contribute to ageing, but these explanations remain incomplete. Importantly, mainstream explanations of ageing that adopt an evolutionary perspective (Kirkwood and Holliday, 1979; Medawar, 1952; Williams, 1957) have always considered conspecific organisms as the relevant units of selection, i.e. the entities in which longevity genes, antagonistic pleiotropic genes, genes involved in trade-offs that indirectly lead to ageing, or late-expressed deleterious mutations may evolve. In other words, the genetic causes for ageing have been and still are commonly searched for within a given species, and even within a kin (Bourke, 2007; Hamilton, 1966; Kirkwood and Holliday, 1979; Medawar, 1952; Williams, 1957), but seldom outside the focal ageing lineage (Johnson et al., 2019). Indeed, the three mutually non-exclusive major evolutionary theories of ageing (Johnson et al., 2019) rest on a common argument: all organisms inevitably die from extrinsic sources, be it by accident, predation, disease outbreak or due to exceptionally harsh conditions (Reichard, 2017). Since no individual is immortal, irrespectively of the existence of ageing, as progressively fewer individuals within populations escape these extrinsic sources of mortality and are thus able to experience the effects of natural selection, the later periods of any organism’s lives are predicted to be less important from an evolutionary viewpoint than their early periods (Reichard, 2017). Thus, the Mutation Accumulation theory of ageing (MA) (Medawar, 1952) predicts that late-expressed deleterious mutations will accumulate in organismal genomes, when the strength of natural selection has diminished so much that it is insufficient to purge the older members of the populations from their “rotten” late-expressed genes and to further postpone these genes expressions later in the course of the organisms’ lifetime. Hence, senescence, the gradual decrease in biological functions, occurs when such detrimental genes contribute to the decline of organisms late in their lives. The Antagonistic Pleiotropy theory of ageing (AP) (Williams, 1957), proposed by Williams shortly after MA, also fundamentally explains senescence by the decreasing strength of natural selection acting on chronologically ageing individuals. As external death is inevitable, the selection for genes that benefit organisms should be more active early in their lives, even when these genes with early positive fitness effects impair the survival ofJournal their bearers later in their lives. Such Pre-proof genes with positive fitness effects early in life, but negative fitness effects later, are therefore called antagonistic pleiotropic genes. Consequently, organismal ageing results from trade-offs favoring the reproduction of individuals over their long-term survival. Finally, the Disposable Soma theory (DS) developed by Kirkwood (Kirkwood and Holliday, 1979; Kirkwood, 1977) stresses that, because resources are limited, most organisms will be evolutionarily more successful if they invest their finite energy into their germline (i.e., the sperm, eggs and their precursor cells) and into their reproduction rather than into the maintenance of their soma (i.e., their other cells, doomed to form temporary bodies that contain, protect and help to propagate the genetic information they share with the germ cells) (Reichard, 2017). Thus, DS principally differs from AP by explicitly assuming optimal dynamical allocation of resources within the life history trade-offs (reproduction, survival) to maximize lifetime fitness (Reichard, 2017). Consequently, both the antagonistic pleiotropy and disposable soma theories expect a trade- off between ageing and fecundity (Johnson et al., 2019). While these approaches and their conclusions are sound and important, it also strikes us that searching for the causes of ageing solely within kin or within a species may obfuscate some additional genetic causes of organismal ageing, which would be external to the focal species, yet directly related to organismal ageing. We agree with Johnson et al. (Johnson et al., 2019), who recently stressed that “the trend in all three theories has been to designate the organism as the
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