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      Parental age at conception on mouse lemur’s offspring longevity: Sex-specific maternal effects

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          Abstract

          Parental age at conception often influences offspring’s longevity, a phenomenon referred as the “Lansing effect” described in large variety of organisms. But, the majority of the results refer to the survival of juveniles, mainly explained by an inadequate parental care by the elderly parents, mostly the mothers. Studies on the effect of parental age on offspring’s longevity in adulthood remain few, except in humans for whom effects of parental age vary according to statistical models or socioeconomic environments. In a small primate in which the longevity reaches up to 13 years, we investigated the effects of parental age at conception on the longevity of offspring (N = 278) issued from parents with known longevity. None of the postnatal parameters (body mass at 30 and 60 days after birth, size and composition of the litter) influenced offspring’s longevity. Mothers’ age at conception negatively affected offspring’s longevity in males but not in females. By contrast, fathers’ age at conception did not influence offspring’s longevity. Finally, the longevity of female offspring was significantly positively related to the longevity of both parents. Compared with current studies, the surprisingly minor effect of fathers ‘age was related to the high seasonal reproduction and the particular telomere biology of mouse lemurs.

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          Comparative biology of mammalian telomeres: hypotheses on ancestral states and the roles of telomeres in longevity determination.

          Progressive telomere shortening from cell division (replicative aging) provides a barrier for human tumor progression. This program is not conserved in laboratory mice, which have longer telomeres and constitutive telomerase. Wild species that do/do not use replicative aging have been reported, but the evolution of different phenotypes and a conceptual framework for understanding their uses of telomeres is lacking. We examined telomeres/telomerase in cultured cells from > 60 mammalian species to place different uses of telomeres in a broad mammalian context. Phylogeny-based statistical analysis reconstructed ancestral states. Our analysis suggested that the ancestral mammalian phenotype included short telomeres (< 20 kb, as we now see in humans) and repressed telomerase. We argue that the repressed telomerase was a response to a higher mutation load brought on by the evolution of homeothermy. With telomerase repressed, we then see the evolution of replicative aging. Telomere length inversely correlated with lifespan, while telomerase expression co-evolved with body size. Multiple independent times smaller, shorter-lived species changed to having longer telomeres and expressing telomerase. Trade-offs involving reducing the energetic/cellular costs of specific oxidative protection mechanisms (needed to protect < 20 kb telomeres in the absence of telomerase) could explain this abandonment of replicative aging. These observations provide a conceptual framework for understanding different uses of telomeres in mammals, support a role for human-like telomeres in allowing longer lifespans to evolve, demonstrate the need to include telomere length in the analysis of comparative studies of oxidative protection in the biology of aging, and identify which mammals can be used as appropriate model organisms for the study of the role of telomeres in human cancer and aging. © 2011 The Authors. Aging Cell © 2011 Blackwell Publishing Ltd/Anatomical Society of Great Britain and Ireland.
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            Telomere Length as a Marker of Biological Age: State-of-the-Art, Open Issues, and Future Perspectives

            Telomere shortening is a well-known hallmark of both cellular senescence and organismal aging. An accelerated rate of telomere attrition is also a common feature of age-related diseases. Therefore, telomere length (TL) has been recognized for a long time as one of the best biomarkers of aging. Recent research findings, however, indicate that TL per se can only allow a rough estimate of aging rate and can hardly be regarded as a clinically important risk marker for age-related pathologies and mortality. Evidence is obtained that other indicators such as certain immune parameters, indices of epigenetic age, etc., could be stronger predictors of the health status and the risk of chronic disease. However, despite these issues and limitations, TL remains to be very informative marker in accessing the biological age when used along with other markers such as indices of homeostatic dysregulation, frailty index, epigenetic clock, etc. This review article is aimed at describing the current state of the art in the field and at discussing recent research findings and divergent viewpoints regarding the usefulness of leukocyte TL for estimating the human biological age.
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              Sex differences in telomeres and lifespan.

              Males and females often age at different rates resulting in longevity 'gender gaps', where one sex outlives the other. Why the sexes have different lifespans is an age-old question, still fiercely debated today. One cellular process related to lifespan, which is known to differ according to sex, is the rate at which the protective telomere chromosome caps are lost. In humans, men have shorter lifespans and greater telomere shortening. This has led to speculation in the medical literature that sex-specific telomere shortening is one cause of sex-specific mortality. However, telomere shortening may be a cause for and/or a consequence of the processes that govern survival, and to infer general principles from single-taxon studies may be misleading. Here, we review recent work on telomeres in a variety of animal taxa, including those with reverse sexual lifespan dimorphism (i.e., where males live longer), to establish whether sex-specific survival is generally associated with sex differences in telomere dynamics. By doing this, we attempt to tease apart the potential underlying causes for sex differences in telomere lengths in humans and highlight targets for future research across all taxa. © 2011 The Authors. Aging Cell © 2011 Blackwell Publishing Ltd/Anatomical Society of Great Britain and Ireland.

                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Writing – original draft
                Role: Data curation
                Role: Editor
                Journal
                PLoS One
                PLoS One
                plos
                PLOS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                29 December 2022
                2022
                : 17
                : 12
                : e0265783
                Affiliations
                [001] UMR 7179, Adaptive mechanisms and Evolution, MECADEV, Brunoy, France
                University of Massachusetts Medical School, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0002-3801-0453
                Article
                PONE-D-22-05796
                10.1371/journal.pone.0265783
                9799291
                36580457
                4992e16f-c31e-41b4-a292-7aa00a9577f1
                © 2022 Martine, Aude

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 7 March 2022
                : 22 November 2022
                Page count
                Figures: 3, Tables: 1, Pages: 12
                Funding
                The authors received no specific funding for this work.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Primates
                Prosimians
                Lemurs
                Biology and Life Sciences
                Zoology
                Animals
                Vertebrates
                Amniotes
                Mammals
                Primates
                Prosimians
                Lemurs
                Biology and Life Sciences
                Cell Biology
                Chromosome Biology
                Chromosomes
                Chromosome Structure and Function
                Telomeres
                Telomere Length
                People and Places
                Population Groupings
                Families
                Mothers
                People and Places
                Population Groupings
                Families
                Fathers
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
                Natural Selection
                Reproductive Success
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Primates
                Biology and Life Sciences
                Zoology
                Animals
                Vertebrates
                Amniotes
                Mammals
                Primates
                Biology and Life Sciences
                Cell Biology
                Chromosome Biology
                Chromosomes
                Chromosome Structure and Function
                Telomeres
                Biology and Life Sciences
                Psychology
                Behavior
                Animal Behavior
                Animal Sexual Behavior
                Social Sciences
                Psychology
                Behavior
                Animal Behavior
                Animal Sexual Behavior
                Biology and Life Sciences
                Zoology
                Animal Behavior
                Animal Sexual Behavior
                Custom metadata
                Data are available on request from the IBISA Platform (UMR 7179, F-91800 Brunoy, mail to fabienne.aujard@ 123456mnhn.fr ).

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