Spatio‐temporal variation in lifelong telomere dynamics in a long‐term ecological study

Abstract Understanding individual‐level variation in response to the environment is fundamental to understanding life‐history evolution and population dynamics. Telomeres, the protective caps at the ends of chromosomes, shorten in response to oxidative stress, and telomere shortening is correlated with reduced survival and life span. Investigating telomere dynamics may help us quantify individual variation in the costs experienced from social and ecological factors, and enhance our understanding of the dynamics of natural populations. Here, we study spatio‐temporal variation in lifelong telomere dynamics in the Seychelles warbler, Acrocephalus sechellensis. We combine long‐term life history and ecological data with a large longitudinal dataset of mean telomere lengths, consisting of 1,808 samples from 22 cohorts born between 1993 and 2014. We provide a detailed analysis of how telomere dynamics vary over individual life spans and cohorts, and with spatio‐temporal variation in the social and ecological environment. We found that telomere length decreases with cross‐sectional and longitudinal measures of age, and most rapidly very early in life. However, both cross‐sectional and longitudinal data suggested that against this overall pattern of shortening, bouts of telomere length increase occur in some individuals. Using a large number of repeated measurements we show statistically that these increases are unlikely to be explained solely by qPCR measurement error. Telomere length varied markedly among cohorts. Telomere length was positively associated with temporal variation in island‐wide insect abundance—a key resource for the insectivorous Seychelles warbler—suggesting that the costs associated with living in harsher environments can be studied by investigating telomere dynamics. We also found evidence for sex‐specific relationships between telomeres and tarsus length, potentially reflecting differential costs of growth. Our long‐term data show that in a natural population, telomere dynamics vary in a complex manner over individual life spans, and across space and time. Variance in telomere dynamics among individuals is the product of a wide array of genetic, parental and environmental factors. Explaining this variation more fully will require the integration of comprehensive long‐term ecological and genetic data from multiple populations and species.

[1]  J. Komdeur,et al.  Conserving the Seychelles Warbler Acrocephalus sechellensis by translocation: a transfer from Cousin Island to Aride Island , 1991, Bird Conservation International.

[2]  L. Keller,et al.  Mother–offspring and nest-mate resemblance but no heritability in early-life telomere length in white-throated dippers , 2015, Proceedings of the Royal Society B: Biological Sciences.

[3]  David R. Anderson,et al.  AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons , 2011, Behavioral Ecology and Sociobiology.

[4]  N. Metcalfe,et al.  Sex-dependent effects of nutrition on telomere dynamics in zebra finches (Taeniopygia guttata) , 2015, Biology Letters.

[5]  M. Bateson.  Cumulative stress in research animals: Telomere attrition as a biomarker in a welfare context? , 2015, BioEssays : news and reviews in molecular, cellular and developmental biology.

[6]  S. Bensch,et al.  Hidden costs of infection: Chronic malaria accelerates telomere degradation and senescence in wild birds , 2015, Science.

[7]  C. M. Lessells,et al.  The Evolution of Life Histories , 1994 .

[8]  B. Moe,et al.  Migration and stress during reproduction govern telomere dynamics in a seabird , 2014, Biology Letters.

[9]  Y. Handrich,et al.  Starting with a handicap: phenotypic differences between early‐ and late‐born king penguin chicks and their survival correlates , 2014 .

[10]  T. Burke,et al.  The impact of reproductive investment and early‐life environmental conditions on senescence: support for the disposable soma hypothesis , 2013, Journal of evolutionary biology.

[11]  D. Bates,et al.  Linear Mixed-Effects Models using 'Eigen' and S4 , 2015 .

[12]  J. Komdeur,et al.  The role of group size and environmental factors on survival in a cooperatively breeding tropical passerine. , 2006, The Journal of animal ecology.

[13]  Martijn van de Pol,et al.  A simple method for distinguishing within- versus between-subject effects using mixed models , 2009, Animal Behaviour.

[14]  P. Bize,et al.  Red blood cells open promising avenues for longitudinal studies of ageing in laboratory, non-model and wild animals , 2015, Experimental Gerontology.

[15]  J. Komdeur,et al.  Assessing the Cost of Helping: The Roles of Body Condition and Oxidative Balance in the Seychelles Warbler (Acrocephalus sechellensis) , 2011, PloS one.

[16]  Simon Verhulst,et al.  Nestling telomere shortening, but not telomere length, reflects developmental stress and predicts survival in wild birds , 2014, Proceedings of the Royal Society B: Biological Sciences.

[17]  J. Komdeur.  Influence of age on reproductive performance in the Seychelles warbler , 1996 .

[18]  Lewis G. Spurgin,et al.  Museum DNA reveals the demographic history of the endangered Seychelles warbler , 2014, Evolutionary applications.

[19]  C. Vleck,et al.  Calibrating the telomere clock in common terns, Sterna hirundo , 2003, Experimental Gerontology.

[20]  J. Pemberton,et al.  Data from: Sex differences in leukocyte telomere length in a free-living mammal , 2017 .

[21]  Lea Harrington,et al.  Lifelong leukocyte telomere dynamics and survival in a free‐living mammal , 2015, Aging cell.

[22]  A. McQuarrie,et al.  Regression and Time Series Model Selection , 1998 .

[23]  F. Angelier,et al.  Age and Heat Stress as Determinants of Telomere Length in a Long-Lived Fish, the Siberian Sturgeon , 2016, Physiological and Biochemical Zoology.

[24]  D. Richardson,et al.  Sex differences in telomeres and lifespan , 2011, Aging cell.

[25]  David M. Richardson,et al.  Sex‐specific associative learning cues and inclusive fitness benefits in the Seychelles warbler , 2003, Journal of evolutionary biology.

[26]  H. Watson,et al.  Variation in early-life telomere dynamics in a long-lived bird: links to environmental conditions and survival , 2015, The Journal of Experimental Biology.

[27]  Y. Moodley,et al.  Telomere dynamics in free-living edible dormice (Glis glis): the impact of hibernation and food supply , 2016, Journal of Experimental Biology.

[28]  S. Bensch,et al.  Maternal and genetic factors determine early life telomere length , 2015, Proceedings of the Royal Society B: Biological Sciences.

[29]  T. Burke,et al.  Spatio-temporal variation in territory quality and oxidative status: a natural experiment in the Seychelles warbler (Acrocephalus sechellensis) , 2011, The Journal of animal ecology.

[30]  H. Kao,et al.  Telomeres and Early-Life Stress: An Overview , 2013, Biological Psychiatry.

[31]  Simon Verhulst,et al.  Measuring telomere length and telomere dynamics in evolutionary biology and ecology , 2014, Methods in ecology and evolution.

[32]  T. Burke,et al.  Telomere length and dynamics predict mortality in a wild longitudinal study , 2013, Molecular ecology.

[33]  T. Burke,et al.  GRANDPARENT HELPERS: THE ADAPTIVE SIGNIFICANCE OF OLDER, POSTDOMINANT HELPERS IN THE SEYCHELLES WARBLER , 2007, Evolution; international journal of organic evolution.

[34]  M. Bateson,et al.  The telomere lengthening conundrum – it could be biology , 2016, Aging cell.

[35]  Pat Monaghan,et al.  An experimental demonstration that early-life competitive disadvantage accelerates telomere loss , 2015, Proceedings of the Royal Society B: Biological Sciences.

[36]  J. Komdeur,et al.  Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles warbler , 1992, Nature.

[37]  T. Burke,et al.  Seychelles warblers: Complexities of the helping paradox , 2016 .

[38]  Shinichi Nakagawa,et al.  A general and simple method for obtaining R2 from generalized linear mixed‐effects models , 2013 .

[39]  Hermann Brenner,et al.  A systematic review of leukocyte telomere length and age in adults , 2013, Ageing Research Reviews.

[40]  Robert M. Bachoo,et al.  Telomere dysfunction and Atm deficiency compromises organ homeostasis and accelerates ageing , 2003, Nature.

[41]  Paul C. Johnson.  Extension of Nakagawa & Schielzeth's R2GLMM to random slopes models , 2014, Methods in ecology and evolution.

[42]  S. Verhulst,et al.  Absolute standards as a useful addition to the avian quantitative PCR telomere assay , 2012 .

[43]  S. Wanless,et al.  Parental age influences offspring telomere loss , 2016 .

[44]  Lewis G. Spurgin,et al.  Senescence in the wild: Insights from a long-term study on Seychelles warblers , 2015, Experimental Gerontology.

[45]  L. Spurgin,et al.  Telomere length reveals cumulative individual and transgenerational inbreeding effects in a passerine bird , 2016, Molecular ecology.

[46]  J. Lindström,et al.  Early development and fitness in birds and mammals. , 1999, Trends in ecology & evolution.

[47]  T. Clutton‐Brock,et al.  Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. , 2010, Trends in ecology & evolution.

[48]  P. Bize,et al.  Immediate and delayed effects of growth conditions on ageing parameters in nestling zebra finches , 2015, Journal of Experimental Biology.

[49]  M. Simons.  Questioning causal involvement of telomeres in aging , 2015, Ageing Research Reviews.

[50]  B T Grenfell,et al.  Age, sex, density, winter weather, and population crashes in Soay sheep. , 2001, Science.

[51]  Clifford M. Hurvich,et al.  Regression and time series model selection in small samples , 1989 .

[52]  R. Griffiths,et al.  A DNA test to sex most birds , 1998, Molecular ecology.

[53]  E. Susser,et al.  Commentary: The reliability of telomere length measurements , 2015, International journal of epidemiology.

[54]  J. Komdeur.  Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles warbler , 1992, Nature.

[55]  D. Penn,et al.  Stress impacts telomere dynamics , 2007, Biology Letters.

[56]  E. Blackburn,et al.  Telomere length is paternally inherited and is associated with parental lifespan , 2007, Proceedings of the National Academy of Sciences.

[57]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[58]  E. Blackburn,et al.  The rate of telomere sequence loss in human leukocytes varies with age. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[59]  J. Komdeur,et al.  Helpers at the Nest Improve Late-Life Offspring Performance: Evidence from a Long-Term Study and a Cross-Foster Experiment , 2012, PloS one.

[60]  Pat Monaghan,et al.  Telomere length in early life predicts lifespan , 2012, Proceedings of the National Academy of Sciences.

[61]  J. Komdeur.  The effect of kinship on helping in the cooperative breeding Seychelles warbler (Acrocephalus sechellensis) , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[62]  Shinichi Nakagawa,et al.  A statistical approach to distinguish telomere elongation from error in longitudinal datasets , 2013, Biogerontology.

[63]  T. von Zglinicki.  Oxidative stress shortens telomeres. , 2002, Trends in biochemical sciences.

[64]  J. Campisi.  Cellular senescence and apoptosis: how cellular responses might influence aging phenotypes , 2003, Experimental Gerontology.

[65]  A. Aviv,et al.  The telomere lengthening conundrum—artifact or biology? , 2013, Nucleic acids research.

[66]  J. Komdeur,et al.  Why Seychelles Warblers fail to recolonize nearby islands : unwilling or unable to fly there? , 2004 .

[67]  T. Ruf,et al.  Telomeres are elongated in older individuals in a hibernating rodent, the edible dormouse (Glis glis) , 2016, Scientific Reports.

[68]  E. Blackburn,et al.  Recognition and elongation of telomeres by telomerase. , 1989, Genome.

[69]  P. Monaghan.  Organismal stress, telomeres and life histories , 2014, Journal of Experimental Biology.

[70]  K. Yoda,et al.  Environmental perturbations influence telomere dynamics in long-lived birds in their natural habitat , 2013, Biology Letters.

[71]  T. Burke,et al.  Plant ecology (communication arising): Tree-species competition and coexistence , 2003, Nature.

[72]  P. Bize,et al.  Investigating how telomere dynamics, growth and life history covary along an elevation gradient in two passerine species , 2016 .

[73]  S. Schreiber,et al.  Why intraspecific trait variation matters in community ecology. , 2011, Trends in ecology & evolution.