Telomere dynamics in relation to experimentally increased locomotion costs and fitness in great tits.

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    • Source:
      Publisher: Blackwell Scientific Publications Country of Publication: England NLM ID: 9214478 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-294X (Electronic) Linking ISSN: 09621083 NLM ISO Abbreviation: Mol Ecol Subsets: MEDLINE
    • Publication Information:
      Original Publication: Oxford, UK : Blackwell Scientific Publications, c1992-
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    • Abstract:
      Evidence that telomere length (TL) and dynamics can be interpreted as proxy for 'life stress' experienced by individuals stems largely from correlational studies. We tested for effects of an experimental increase of workload on telomere dynamics by equipping male great tits (Parus major) with a 0.9 g backpack for a full year. In addition, we analysed associations between natural life-history variation, TL and TL dynamics. Carrying 5% extra weight for a year did not significantly accelerate telomere attrition. This agrees with our earlier finding that this experiment did not affect survival or future reproduction. Apparently, great tit males were able to compensate behaviourally or physiologically for the increase in locomotion costs we imposed. We found no cross-sectional association between reproductive success and TL, but individuals with higher reproductive success (number of recruits) lost fewer telomere base pairs in the subsequent year. We used the TRF method to measure TL, which method yields a TL distribution for each sample, and the association between reproductive success and telomere loss was more pronounced in the higher percentiles of the telomere distribution, in agreement with the higher impact of ageing on longer telomeres within individuals. Individuals with longer telomeres and less telomere shortening were more likely to survive to the next breeding season, but these patterns did not reach statistical significance. Whether successful individuals are characterized by losing fewer or more base pairs from their telomeres varies between species, and we discuss aspects of ecology and social organisation that may explain this variation.
      (© 2021 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)
    • References:
      Andrews, C., Zuidersma, E., Verhulst, S., Nettle, D., & Bateson, M. (2021). Exposure to food insecurity increases energy storage and reduces somatic maintenance in European starlings. Royal Society Open, in press.
      Atema, E., Mulder, E., van Noordwijk, A. J., & Verhulst, S. (2019). Ultra-long telomeres shorten with age in nestling great tits but are static in adults and mask attrition of short telomeres. Molecular Ecology Resources, 19, 648-658. https://doi.org/10.1111/1755-0998.12996.
      Atema, E., van Noordwijk, A. J., Boonekamp, J. J., & Verhulst, S. (2016). Costs of long-term carrying of extra mass in a songbird. Behavioral Ecology, 27, 1087-1096. https://doi.org/10.1093/beheco/arw019.
      Barha, C. K., Hanna, C. W., Salvante, K. G., Wilson, S. L., Robinson, W. P., Altman, R. M., & Nepomnaschy, P. A. (2016). Number of children and telomere length in women: a prospective, longitudinal evaluation. PLoS ONE, 11, 1-12. https://doi.org/10.1371/journal.pone.0146424.
      Bauch, C., Becker, P. H., & Verhulst, S. (2013). Telomere length reflects phenotypic quality and costs of reproduction in a long-lived seabird. Proceedings of the Royal Society B: Biological Sciences, 280, 20122540. https://doi.org/10.1098/rspb.2012.2540.
      Bauch, C., Becker, P. H., & Verhulst, S. (2014). Within the genome, long telomeres are more informative than short telomeres with respect to fitness components in a long-lived seabird. Molecular Ecology, 23, 300-310. https://doi.org/10.1111/mec.12602.
      Bauch, C., Gatt, M. C., Granadeiro, J. P., Verhulst, S., & Catry, P. (2020). Sex-specific telomere length and dynamics in relation to age and reproductive success in Cory's shearwaters. Molecular Ecology, 29, 1344-1357. https://doi.org/10.1111/mec.15399.
      Bauch, C., Riechert, J., Verhulst, S., & Becker, P. (2016). Telomere length reflects reproductive effort indicated by corticosterone levels in a long-lived seabird. Molecular Ecology, 25, 5785-5794. https://doi.org/10.1111/mec.13874.
      Beaulieu, M., Reichert, S., Le Maho, Y., Ancel, A., & Criscuolo, F. (2011). Oxidative status and telomere length in a long-lived bird facing a costly reproductive event. Functional Ecology, 25, 577-585. https://doi.org/10.1111/j.1365-2435.2010.01825.x.
      Blackburn, E. H. (1991). Telomeres. Trends in Biochemical Sciences, 16, 378-381. https://doi.org/10.1016/0968-0004(91)90155-O.
      Bouwhuis, S., Sheldon, B. C., Verhulst, S., & Charmantier, A. (2009). Great tits growing old: Selective disappearance and the partitioning of senescence to stages within the breeding cycle. Proceedings of the Royal Society B: Biological Sciences, 276, 2769-2777.
      Bouwhuis, S., Van Noordwijk, A. J., Sheldon, B. C., Verhulst, S., & Visser, M. E. (2010). Similar patterns of age-specific reproduction in an island and mainland population of great tits Parus major. Journal of Avian Biology, 41, 615-620. https://doi.org/10.1111/j.1600-048X.2010.05111.x.
      Chatelain, M., Drobniak, S. M., & Szulkin, M. (2019). The association between stressors and telomeres in non-human vertebrates: a meta-analysis. Ecology Letters, 99, 21-18.
      Eastwood, J. R., Hall, M. L., Teunissen, N., Kingma, S. A., Hidalgo Aranzamendi, H., Fan, M., Roast, M., Verhulst, S., & Peters, A. (2019). Early-life telomere length predicts lifespan and lifetime reproductive success in a wild bird. Molecular Ecology, 28, 1127-1137. https://doi.org/10.1111/mec.15002.
      Ens, B. J., Esselink, P., & Zwarts, L. (1990). Kleptoparasitism as a problem of prey choice: A study on mudflat-feeding curlews, Numenius arquata. Animal Behaviour, 39, 219-230. https://doi.org/10.1016/S0003-3472(05)80866-8.
      Houston, A. I., McNamara, J. M., & Hutchinson, J. M. C. (1993). General results concerning the trade-off between gaining energy and avoiding predation. Philosophical Transactions of the Royal Society B: Biological Sciences, 341, 375-397.
      Jimeno, B., Hau, M., & Verhulst, S. (2017). Strong association between corticosterone and temperature dependent metabolic rate in individual zebra finches. Journal of Experimental Biology, 220, 3280-3289. https://doi.org/10.1242/jeb.166124.
      Jimeno, B., Hau, M., & Verhulst, S. (2018). Corticosterone levels reflect variation in metabolic rate independent of ‘stress’. Scientific Reports, 8, 13020. https://doi.org/10.1038/s41598-018-31258-z.
      Kimura, M., Barbieri, M., Gardner, J. P., Skurnick, J., Cao, X., van Riel, N., Rizzo, M. R., Paoliso, G., & Aviv, A. (2007). Leukocytes of exceptionally old persons display ultra-short telomeres. American Journal of Physiology- Regulatory, Integrative and Comparative Physiology, 293, R2210-2217. https://doi.org/10.1152/ajpregu.00615.2007.
      Lane, J. E., Boutin, S., Speakman, J. R., & Humphries, M. M. (2010). Energetic costs of male reproduction in a scramble competition mating system. Journal of Animal Ecology, 79, 27-34. https://doi.org/10.1111/j.1365-2656.2009.01592.x.
      Le Vaillant, M., Viblanc, V. A., Saraux, C., Le Bohec, C., Le Maho, Y., Kato, A., Criscuolo, F., & Ropert-Coudert, Y. (2015). Telomere length reflects individual quality in free-living adult king penguins. Polar Biology, 2059-2067. https://doi.org/10.1007/s00300-015-1766-0.
      Olsson, M., Shine, R., & Wapstra, E. (2001). Costs of reproduction in a lizard species: A comparison of observational and experimental data. Oikos, 93, 121-125. https://doi.org/10.1034/j.1600-0706.2001.930113.x.
      Ouyang, J. Q., Sharp, P., Quetting, M., & Hau, M. (2013). Endocrine phenotype, reproductive success and survival in the great tit, Parus major. Journal of Evolutionary Biology, 26, 1988-1998.
      Pauliny, A., Wagner, R. H., Augustin, J., Szép, T., & Blomqvist, D. (2006). Age-independent telomere length predicts fitness in two bird species. Molecular Ecology, 15, 1681-1687. https://doi.org/10.1111/j.1365-294X.2006.02862.x.
      Plot, V., Criscuolo, F., Zahn, S., & Georges, J. Y. (2012). Telomeres, age and reproduction in a long-lived reptile. PLoS ONE, 7, e40855. https://doi.org/10.1371/journal.pone.0040855.
      Postma, E., & van Noordwijk, A. J. (2005). Gene flow maintains a large genetic difference in clutch size at a small spatial scale. Nature, 433, 65-68. https://doi.org/10.1038/nature03083.
      R Core and Team (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
      Salmón, P., Nilsson, J. F., Watson, H., Bensch, S., & Isaksson, C. (2017). Selective disappearance of great tits with short telomeres in urban areas. Proceedings of the Royal Society B: Biological Sciences, 284, 20171349-20171358. https://doi.org/10.1098/rspb.2017.1349.
      Salomons, H. M., Mulder, G. A., van de Zande, L., Haussmann, M. F., Linskens, M. H. K., & Verhulst, S. (2009). Telomere shortening and survival in free-living corvids. Proceedings of the Royal Society B: Biological Sciences, 276, 3157-3165. https://doi.org/10.1098/rspb.2009.0517.
      Snijders, L., van Rooij, E. P., Burt, J. M., Hinde, C. A., van Oers, K., & Naguib, M. (2014). Social networking in territorial great tits: slow explorers have the least central social network positions. Animal Behaviour, 98, 95-102. https://doi.org/10.1016/j.anbehav.2014.09.029.
      Sudyka, J. (2019). Does Reproduction Shorten Telomeres? Towards Integrating Individual Quality with Life-History Strategies in Telomere Biology. BioEssays, 32, 1900095-1900112. https://doi.org/10.1002/bies.201900095.
      Tinbergen, J. M., & Dietz, M. W. (1994). Parental energy expenditure during brood rearing in the great tit (Parus major) in relation to body mass, temperature, food availability and clutch size. Functional Ecology, 8, 563-572. https://doi.org/10.2307/2389916.
      Tinbergen, J. M., & Verhulst, S. (2000). A fixed energetic ceiling to parental effort in the great tit? Journal of Animal Ecology, 69, 323-334. https://doi.org/10.1046/j.1365-2656.2000.00395.x.
      Van de Pol, M., & Verhulst, S. (2006). Age-dependent traits: a new statistical model to separate within- and between-individual effects. The American Naturalist, 167, 766-773. https://doi.org/10.1086/503331.
      Van Noordwijk, A. J., Van Balen, J. H., & Scharloo, W. (1981). Genetic and environmental variation in clutch size of the Great tit Parus major. Netherlands Journal of Zoology, 31, 342-372.
      Verboven, N., Tinbergen, J. M., & Verhulst, S. (2001). Food, reproductive success and multiple breeding in the Great Tit Parus major”. Ardea, 89, 387-406.
      Verhulst, S., & Van Eck, H. M. (1996). Gene flow and immigration rate in an island population of great tits. Journal of Evolutionary Biology, 9, 771-782. https://doi.org/10.1046/j.1420-9101.1996.9060771.x.
      Wilbourn, R. V., Moatt, J. P., Froy, H., Walling, C. A., Nussey, D. H., & Boonekamp, J. J. (2018). The relationship between telomere length and mortality risk in non-model vertebrate systems: a meta-analysis. Philosophical Transactions of the Royal Society B: Biological Science, 373, 20160447-20160449. https://doi.org/10.1098/rstb.2016.0447.
    • Contributed Indexing:
      Keywords: TRF; birds; fitness; longitudinal; senescence
    • Publication Date:
      Date Created: 20210903 Date Completed: 20230201 Latest Revision: 20230209
    • Publication Date:
      20240628
    • Accession Number:
      PMC9786264
    • Accession Number:
      10.1111/mec.16162
    • Accession Number:
      34478576