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Comparative biology of mammalian telomeres: hypotheses on ancestral states and the roles of telomeres in longevity determination
Open accessAbstract
Summary: 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.
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“The programmed silencing of TERT, loss of telomerase activity and the resulting shortening of telomeres is not a universal phenomenon in mammals. Apparently, this tumour suppressor pathway is restricted to large animals with a reproductive strategy that requires a long lifespan28.”
From Telomeres in cancer: tumour suppression and genome instability (2017) · cites this paper as [28]
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“Taken together, it seems that the evolution of large body sizes and longevity is strongly associated with the evolution of short telomeres and telomerase suppression, presumably for tumour suppression (de Magalhaes, 2013; Gomes et al., 2011).”
From Stress, cell senescence and organismal ageing (2018) · cites this paper as Gomes et al., 2011
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“The enzyme telomerase acts to lengthen telomeres (Greider & Blackburn, 1985); in endothermic vertebrates, telomerase is expressed in germline cells throughout life, but is often repressed in adult somatic cells, particularly in larger bodied species (Gomes et al., 2011; Haussmann et al., 2007).”
BackgroundExercise as a Therapy to Maintain Telomere Function and Prevent Cellular Senescence
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A phylogenetic review of cancer resistance highlights evolutionary solutions to Peto’s Paradox
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“Across mammals, shorter telomeres and lower telomerase expression have been observed in larger, longer-lived species 62 .”
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“For example, using phylogenetically corrected data on telomeres from cultured fibroblast cells, collected from a range of tissues in over 60 species of mammals and grown in a variety of media, an impressive comparative study was carried out by Gomes et al. (2011).”
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“in large species [35]; as described in the introduc-”
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“By using these criteria, we noted that the 16 known or suggested TPE-OLD genes reported in the literature (9–12) appeared to be preserved at two telomeric positions in “replicatively aging species,” that is, in species which undergo TL-dependent replicative aging (18), including both primates and nonprimates (at 0.”
InfluentialHrdličková, R., Nehyba, J., Lim, S. L., Grützner, F., & Bose, H. R. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-216 · Cited by 14
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The heterochromatic chromosome caps in great apes impact telomere metabolism
Novo, C. L., Arnoult, N., Liu-Bordes, W.-Y., Castro‐Vega, L. J., Gibaud, A., Dutrillaux, B., Bacchetti, S., & Londoño‐Vallejo, A. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt169 · Cited by 13
Rejuvenation of Cardiac Tissue Developed from Reprogrammed Aged Somatic Cells
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“From an evolutionary point of view, short telomeres and repressed telomerase (as in human somatic tissues) have been suggested to coevolve with homeothermy and replicative aging in mammals (Gomes et al., 2011), while p66SHC with the metabolic adaptation to harsh energetic environments (i.”
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From zygote to a multicellular soma: Body size affects optimal growth strategies under cancer risk
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The TERB1 MYB domain suppresses telomere erosion in meiotic prophase I
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“While telomerase activity in humans is restricted to certain cell types, such as stem cells, germ cells, or cancer cells, and is not detectable in most somatic cells, laboratory mice have ubiquitous telomerase activity even in their somatic cells and thus have extremely long telomeres compared with other vertebrate sp…”
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“Telomerase repression in somatic tissues is not an universal phenomenon among mammals, and several small-sized species, which are characterized by a short lifespan, express telomerase in somatic cells (6).”
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“It is of interest that nonplacental mammals have interrupted telomeres where telomeric DNA frag ments of several kilobases in length alternate with DNA fragment containing nontelomeric DNA restriction sites [154].”
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Zhdanova, N. S., Drašković, I., Minina, J. M., Karamysheva, T. V., Novo, C. L., Liu-Bordes, W.-Y., Porreca, R. M., Gibaud, A., Zvereva, M. I., Skvortsov, D. A., et al. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.01697-13 · Cited by 11
“In fact, it appears that most of the species with telomeres whose lengths exceed 25 kb do not use replicative aging (8).”
BackgroundAdvanced paternal age and risk of cancer in offspring
Sun, Y., Li, X., Jiang, W., Fan, Y., Ouyang, Q., Shao, W., Alolga, R. N., Ge, Y., & Ma, G. (2020) · Aging · doi:10.18632/aging.202333 · Cited by 11
“Telomerase activity in mammals was found to be negatively correlated with body size [25, 26], while TL was negatively correlated with lifetime [27].”
BackgroundHuman chromosome 3p21.3 carries TERT transcriptional regulators in pancreatic cancer
Yagyu, T., Ohira, T., Shimizu, R., Morimoto, M., Murakami, Y., Hanaki, T., Kihara, K., Matsunaga, T., Yamamoto, M., Tokuyasu, N., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-94711-6 · Cited by 11
Telomerase as a possible key to bypass reproductive cost
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“The data on telomeres and telomerase were obtained from cultured cells derived from fibroblasts from skin, kidney, lung or cornea of the species (Gomes et al. 2011), or from spleen, lymph node, lung, and kidney (Fradiani et al.”
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Accelerated pathway evolution in mouse-like rodents involves cell cycle control
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“The study of telomere recovery suggested that ancestral mammals were relatively long-lived (Gomes et al. 2011).”
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“An alternative explanation for the telomere elongation pattern found in guppies relies in the anticancer hypothesis which states that telomerase suppression in senescent stage of life occurs as a mechanism to prevent cancer formation (Gomes et al., 2011).”
Backgroundvan Vuuren, A. J., Bolcaen, J., Engelbrecht, M., Burger, W., de Kock, M., Durante, M., Fisher, R., Martínez‐López, W., Miles, X., Rahiman, F., et al. (2023) · Animals · doi:10.3390/ani13142353 · Cited by 10
“Several studies have used elephant fibroblast cells from the San Diego Zoo to study the cancer suppression mechanisms in elephants [21,34,35].”
BackgroundMethodAccounting for phylogenetic relatedness in cross-species analyses of telomere shortening rates
Pepke, M. L., & Eisenberg, D. T. A. (2020) · Experimental Results · doi:10.1017/exp.2020.18 · Cited by 10
“Telomere shortening across species has been shown to be strongly influenced by phylogeny in birds (Tricola et al., 2018) and telomere length to be strongly influenced by phylogeny in mammals 2 Michael Le Pepke and Dan T.A. Eisenberg (Gomes et al., 2011).”
BackgroundPepke, M. L., Ringsby, T. H., & Eisenberg, D. T. A. (2023) · Molecular Ecology · doi:10.1111/mec.16907 · Cited by 9
“A similar magnitude of variation is found within mammals (Gomes et al., 2011), in which TL is shorter in larger and longer- lived species (Pepke & Eisenberg, 2022).”
BackgroundMethodInfluentialSilvestre, D. C., & Londoño‐Vallejo, A. (2012) · Genome dynamics · doi:10.1159/000337128 · Cited by 11
Divergent patterns of telomere shortening in tropical compared to temperate stonechats
Apfelbeck, B., Haussmann, M. F., Boner, W., Flinks, H., Griffiths, K., Illera, J. C., Mortega, K. G., Sisson, Z., Smiddy, P., & Helm, B. (2018) · Ecology and Evolution · doi:10.1002/ece3.4769 · Cited by 10
“In mammals, a comparative study found that short‐lived, small species have longer telomeres and higher telomerase expression than long‐lived, large species (Gomes et al., 2011).”
BackgroundTelomere length and oxidative stress variations in a murine model of Alzheimer’s disease progression
Martínez‐González, K., Islas‐Hernández, A., Martínez‐Ezquerro, J. D., Bermúdez‐Rattoni, F., & Garcia‐delaTorre, P. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14877 · Cited by 8
“different in mice [29].”
Zhang, F., Cheng, D., Porter, K. I., Heck, E. A., Wang, S., Zhang, H., Davis, C. J., Robertson, G. P., & Zhu, J. (2025) · Nature Communications · doi:10.1038/s41467-025-56559-6 · Cited by 11
Boccardi, V. (2025) · Biogerontology · doi:10.1007/s10522-025-10246-7 · Cited by 12
“Some determinants of telomere length are genetically programmed, while others are driven by lifestyle and environmental exposures (Bize et al. 2009; Gomes et al. 2011; Steenstrup et al. 2017; Shekhidem et al. 2019).”
Ingles, E. D., & Deakin, J. E. (2018) · Chromosome Research · doi:10.1007/s10577-018-9593-0 · Cited by 9
Two aspects of longevity are associated with rates of loss of telomeres in birds
Dobson, F. S., Schull, Q., & Criscuolo, F. (2022) · Ecology and Evolution · doi:10.1002/ece3.9364 · Cited by 9
Pérez-López, F. R., López-Baena, M. T., Ulloque‐Badaracco, J. R., & Benites-Zapata, V. A. (2023) · Reproductive Sciences · doi:10.1007/s43032-023-01306-9 · Cited by 9
“They are nucleoprotein complexes containing thousands of repetitive DNA sequences that protect the chromosomes from damage, senescence, and cell death [17, 18].”
BackgroundThe “telomereless” erythrocytes and telomere‐length dependent erythropoiesis
Aviv, A. (2023) · Aging Cell · doi:10.1111/acel.13997 · Cited by 8
“Namely, wild type mice live for about 2 years and most mice have long telomeres, that is, mean telomere length (mTL) ~ 30 kb (Calado & Dumitriu, 2013; Gomes et al., 2011).”
BackgroundRegulation of telomeric function by DNA methylation differs between humans and mice
Toubiana, S., Larom, G., Smoom, R., Duszynski, R. J., Godley, L. A., Francastel, C., Velasco, G., & Selig, S. (2020) · Human Molecular Genetics · doi:10.1093/hmg/ddaa206 · Cited by 9
ORS‐Pred: An optimized reduced scheme‐based identifier for antioxidant proteins
Feng, C., Wei, H., Yang, D., Feng, B., Ma, Z., Han, S., Zou, Q., & Shi, H. W. (2021) · PROTEOMICS · doi:10.1002/pmic.202100017 · Cited by 9
Life Expectancy in Marine Mammals Is Unrelated to Telomere Length but Is Associated With Body Size
Buddhachat, K., Brown, J. L., Kaewkool, M., Poommouang, A., Kaewmong, P., Kittiwattanawong, K., & Nganvongpanit, K. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.737860 · Cited by 9
Zane, L., Ensminger, D. C., & Vázquez-Medina, J. (2021) · bioRxiv · doi:10.1371/journal.pone.0257370 · Cited by 7
Li, K.-Q., 中国科学院昆明动物研究所, 中., Liu, G.-J., Liu, X., Chen, Q.-F., Huang, X.-Y., Tu, Q., Zhang, J., Chang, Q., Xie, Y., et al. (2023) · 动物学研究 · doi:10.24272/j.issn.2095-8137.2022.531 · Cited by 9
Gong, H., Zhu, W. Z., Zhang, J., Li, X., Meng, Q., Zhou, G., Wang, M., Wang, H., Miao, L., Qin, Q., et al. (2015) · Insect Molecular Biology · doi:10.1111/imb.12163 · Cited by 9
“Telomerase activity has been studied in a variety of organisms (Gomes et al., 2011).”
BackgroundKhan, A. M., Idrees, M., Perera, C. D., Haider, Z., Joo, M., Kang, J.-S., Lee, S. L., & Kong, I. (2023) · Reproduction Fertility and Development · doi:10.1071/rd22280 · Cited by 8
Telomere Dynamics in Livestock
Zhang, N., Baker, E. C., Welsh, T. H., & Riley, D. G. (2023) · Biology · doi:10.3390/biology12111389 · Cited by 8
“The range of TL is about 3 to 18 kb for H. sapiens [10] and ranges from 6 to 30 kb for Bos taurus [11] and 7 to 21 kb for Equus caballus [12].”
BackgroundHigh-throughput single telomere analysis using DNA microarray and fluorescent in situ hybridization
Zheng, Y., Wu, X., Williams, M., Verhulst, S., Lin, J., Takahashi, Y., Ma, J., & Wang, Y. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae812 · Cited by 8
He, S., Li, Y., Chen, Y., Zhu, Y., Zhang, X., Xia, X., & Sun, H. (2015) · Cytotechnology · doi:10.1007/s10616-015-9903-8 · Cited by 8
Concetti, F., Carpi, F. M., Nabissi, M., Picciolini, M., Santoni, G., & Napolioni, V. (2014) · European Journal of Human Genetics · doi:10.1038/ejhg.2014.102 · Cited by 9
Telomeres, cancer & aging: live long & prosper?
Eissenberg, J. C. (2013) · Europe PMC (PubMed Central) · Cited by 7
Influence of Donor Age and Species Longevity on Replicative Cellular Senescence
Lorenzini, A., & Maier, A. B. (2016) · Healthy ageing and longevity · doi:10.1007/978-3-319-26239-0_4 · Cited by 9
“(Gomes et al. 2011).”
BackgroundInfluentialWard, S. J., Hill, A. M., Buckley, J. D., Banks, S., Dhillon, V. S., Holman, S. L., Morrison, J. L., & Coates, A. M. (2021) · British Journal Of Nutrition · doi:10.1017/s0007114521001549 · Cited by 12
“Telomerase, a ribonucleoprotein capable of synthesising telomere repeats, may restore TL; however, its activity is either down-regulated or absent inmost somatic cells(6,12).”
BackgroundTelomeres and telomerase: active but complex players in life-history decisions
Frydrychová, R. Č., Konopová, B., Peška, V., Brejcha, M., & Sábová, M. (2023) · Biogerontology · doi:10.1007/s10522-023-10060-z · Cited by 8
“…length demonstrates remarkable divergence, extending anywhere from 0.5 kb to 3 Mb. Finally, mammalian telomere length usually ranges from 5 kb to in excess of 50 kb (Gomes et al. 2011); extremely long telomeres, reaching up to 300 kb, have been detected in Sorex granarius (Zhdanova et al. 2005).”
InfluentialContributions of Telomere Biology to Human Age-Related Disease
Yang, T.-L., Song, S., & Johnson, F. B. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-411596-5.00007-1 · Cited by 9
Telomere regulation during ageing and tumorigenesis of the grey mouse lemur
Trochet, D., Mergui, X., Ivković, I., Porreca, R. M., Gerbault‐Seureau, M., Sidibe, A., Richard, F. A., Londoño‐Vallejo, A., Perret, M., Aujard, F., et al. (2015) · Biochimie · doi:10.1016/j.biochi.2015.04.002 · Cited by 10
Bowman, J. D., & Lynch, V. J. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.02.27.582135 · Cited by 9
Vogt, G. (2015) · CRC Press eBooks · doi:10.1201/b18723-9 · Cited by 7
Active telomerase during leaf growth and increase of age in plants from Agave tequilana var. Azul
la Torre-Espinosa, Z. Y. D., Barredo-Pool, F., Castaño, E., & Sánchez‐Teyer, L. F. (2020) · Physiology and Molecular Biology of Plants · doi:10.1007/s12298-020-00781-7 · Cited by 7
Telomere Length is a Susceptibility Marker for Tasmanian Devil Facial Tumor Disease
Smith, L. E., Jones, M. E., Hamede, R., Risques, R. A., Patton, A. H., Carter, P. A., & Storfer, A. T. (2020) · EcoHealth · doi:10.1007/s10393-020-01491-y · Cited by 7
“Indeed in mammals, telomere length is positively correlated with maximum lifespan (Gomes 2011).”
BackgroundTelomere recombination in normal mammalian cells
Zhdanova, N. S., & Рубцов, Н. Б. (2016) · Russian Journal of Genetics · doi:10.1134/s1022795416010142 · Cited by 6
“In the majority of mammals, it varies from several to thousands of kilobase pairs [8].”
BackgroundMammalian chromosome–telomere length dynamics
Klegarth, A. R., & Eisenberg, D. T. A. (2018) · Royal Society Open Science · doi:10.1098/rsos.180492 · Cited by 7
“[31] dataset with the outlier,Muntiacus muntjak, removed.”
BackgroundMethodInfluentialTelomeric small RNAs in the genus Caenorhabditis
Frenk, S., Lister‐Shimauchi, E. H., & Ahmed, S. C. (2019) · RNA · doi:10.1261/rna.071324.119 · Cited by 7
Characterization of tree shrew telomeres and telomerase
Sun, J., Liu, W., Guo, Y., Zhang, H., Jiang, D., Luo, Y., Liu, R., & Chen, C. (2021) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2021.06.004 · Cited by 8
Swan, M. (2011) · Rejuvenation Research · doi:10.1089/rej.2011.1216 · Cited by 7
“Replicative aging (progressive telomere shortening from cell division, possibly for the purpose of conferring cancer protection) could have evolved from repressed telomerase.(11) Cancer, telomere length, and telomerase are connected: Short telomeres are present in almost all preneoplastic lesions, critically short tel…”
Vázquez, J. M., Kraft, M., & Lynch, V. J. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.09.07.506958 · Cited by 10
“…We gathered population doubling times from previously published studies (Burkard et al., 2019, 2015; Carvan et al., 1994; Chen et al., 2009; Gomes et al., 2011; Mancia et al., 2012; Rajput et al., 2018; Seluanov et al., 2008; Wang et al., 2011, 2021; Wise et al., 2011, 2008; Yajing et al.,…”
MethodNatural diversity of telomere length distributions across 100 Saccharomyces cerevisiae strainsPreprint
Garrido, C., Gómez-Muñoz, C., Kornobis, É., Agier, N., Ilioaia, O., Fischer, G., & Xu, Z. (2026) · Genome Research · doi:10.1101/gr.281132.125 · Cited by 8
The house mouse maintains constant telomere length throughout life
Smoom, R., Lichtental, D., Kaestner, K. H., & Tzfati, Y. (2025) · Nucleic Acids Research · doi:10.1093/nar/gkaf830 · Cited by 6
“In mammals, telomeric restriction fragments (TRFs) range in length from a few kilobases (kb) to several tens of kb, and up to 150 kb in the house mouse Mus musculus [ 2–4 ].”
Influential
Metadata
- Authors
- Gomes, N. M. V., Ryder, O. A., Houck, M. L., Charter, S. J., Walker, W., Forsyth, N. R., Austad, S. N., Venditti, C., Pagel, M., Shay, J. W., & Wright, W. E.
- Affiliations
- University of Lisbon (PT)
- The University of Texas Southwestern Medical Center (US)
- Keele University (GB)
- University of Hull (GB)
- Santa Fe Institute (US)
- Corresponding author
- Wright, Woodring E.
- ORCID
- Venue
- Aging Cell
- Publisher
- Wiley
- Published
- 2011-06
- Volume
- 10
- Issue
- 5
- Pages
- 761-768
- ISSN
- 1474-9718 (ISSN-L)
- 1474-9726
- PMC
- PMC3387546
- OpenAlex
- W1483456062
- Cited by
- 464
- References
- 63
- Citations by year
- 2026: 18 · 2025: 33 · 2024: 34 · 2023: 33 · 2022: 36 · 2021: 41 · 2020: 40 · 2019: 39 · 2018: 39 · 2017: 30 · 2016: 24 · 2015: 26 · 2014: 19 · 2013: 24 · 2012: 24
- FWCI
- 15.26
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Aging Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- CentAUR (University of Reading) (acceptedVersion)
- Funders
- W. M. Keck Foundation
- National Marine Sanctuary Foundation
- European Commission
- Engineering and Physical Sciences Research Council (EP/H028277/1)
- Natural Environment Research Council (NE/C51992X/1)
- National Institute on Aging (AG 01228, R01AG001228)
- National Cancer Institute (P50CA070907)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Keywords
- telomeres, telomerase, mammalian evolution, ancestral states, replicative senescence, lifespan, telomere length, homeothermy, mutational burden, body size, cancer, comparative biology, phylogenetic analysis
- MeSH terms
- Aging, Animals, Cell Division, Cell Line, Enzyme Repression, Fibroblasts, Genetic Vectors, Humans, Longevity, Mammals, Oxidation-Reduction, Phenotype, Phylogeny, Regression Analysis, Transfection, Telomere, Telomerase, Evolution, Molecular, Body Size, Cell Cycle Checkpoints, Telomere Shortening
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