Evolutionary Ecology

, Volume 31, Issue 4, pp 571–584 | Cite as

Environmental, not individual, factors drive markers of biological aging in black bears

  • Rebecca Kirby
  • Mathew W. Alldredge
  • Jonathan N. Pauli
Original Paper

Abstract

Aging negatively affects individual survival and reproduction; consequently, characterizing the factors behind aging can enhance our understanding of fitness in wild populations. The drivers of biological age are diverse, but often related to factors like chronological age or sex of the individual. Recently, however, environmental factors have been shown to strongly influence biological age. To explore the relative importance of these influences on biological aging in a free-ranging and long-lived vertebrate, we quantified the length of telomeres—highly conserved DNA sequences that cap the ends of eukaryotic chromosomes and a useful molecular marker of biological age—for black bears sampled throughout Colorado, and measured a variety of environmental variables (habitat productivity, human development, latitude, elevation) and individual characteristics (age, sex, body size, genetic relatedness). Our extensive sampling of bears (n = 245) revealed no relationships between telomere length and any individual characteristics. Instead, we found a broad-scale latitudinal pattern in telomere length, with bears in northern Colorado possessing shorter telomeres. Our results suggest that environmental characteristics overwhelm individual ones in determining biological aging for this large carnivore.

Keywords

Biological aging Landscape variation Stress Telomere Ursus americanus 

References

  1. Alldredge MW (2008) Cougar demographics and human interactions along the urban-exurban Front Range of Colorado. Wildlife Research Report, Mammals Research, Colorado Parks and WildlifeGoogle Scholar
  2. Angelier F, Vleck CM, Holberton RL, Marra PP (2013) Telomere length, non-breeding habitat and return rate in male American redstarts. Funct Ecol 27:342–350. doi:10.1111/1365-2435.12041 CrossRefGoogle Scholar
  3. Aydos SE, Elhan AH, Tükün A (2005) Is telomere length one of the determinants of reproductive life span? Arch Gynecol Obstet 272:113–116CrossRefPubMedGoogle Scholar
  4. Baldwin RA (2008) Population demographics, habitat utilization, critical habitats, and condition of black bears in Rocky Mountain National Park. Dissertation, New Mexico State UniversityGoogle Scholar
  5. Baldwin RA, Bender LC (2009) Survival and productivity of a low-density black bear population in Rocky Mountain National Park, Colorado. Human-Wildl Confl 3:271–281Google Scholar
  6. Baldwin RA, Bender LC (2010) Denning chronology of black bears in Eastern Rocky Mountain National Park, Colorado. West N Am Nat 70:48–54. doi:10.3398/064.070.0106 CrossRefGoogle Scholar
  7. Barrett ELB, Richardson DS (2011) Sex differences in telomeres and lifespan. Aging Cell 10:913–921. doi:10.1111/j.1474-9726.2011.00741.x CrossRefPubMedGoogle Scholar
  8. Baruch-Mordo S, Wilson KR, Lewis DL et al (2014) Stochasticity in natural forage production affects use of urban areas by black bears: implications to management of human-bear conflicts. Plos One 9:1–10. doi:10.1371/journal.pone.0085122 CrossRefGoogle Scholar
  9. Beckmann JP, Berger J (2003) Rapid ecological and behavioural changes in carnivores: the responses of black bears (Ursus americanus) to altered food. J Zool 261:207–212. doi:10.1017/S0952836903004126 CrossRefGoogle Scholar
  10. Beirne C, Delahay R, Hares M et al (2014) Age-related declines and disease-associated variation in immune cell telomere length in a wild mammal. Plos One 9:e108964. doi:10.1371/journal.pone.0108964 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Benetos A, Kimura M, Labat C et al (2011) A model of canine leukocyte telomere dynamics. Aging Cell 10:991–995CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bize P, Criscuolo F, Metcalfe NB et al (2009) Telomere dynamics rather than age predict life expectancy in the wild. Proc R Soc B Biol Sci 276:1679–1683. doi:10.1098/rspb.2008.1817 CrossRefGoogle Scholar
  13. Bonier F, Martin PR, Moore IT, Wingfield JC (2009) Do baseline glucocorticoids predict fitness? Trends Ecol Evol 24:634–642. doi:10.1016/j.tree.2009.04.013 CrossRefPubMedGoogle Scholar
  14. Bonneaud C, Mazuc J, Chastel O et al (2004) Terminal investment induced by immune challenge and fitness traits associated with major histocompatibility complex in the house sparrow. Evolution 58:2823–2830. doi:10.1111/j.0014-3820.2004.tb01633.x CrossRefPubMedGoogle Scholar
  15. Bridges AS, Fox JA, Olfenbuttel C, Vaughan MR (2004) American black bear denning behavior: observations and applications using remote photography. Wildl Soc Bull 32:188–193. doi:10.2193/0091-7648(2004)32 CrossRefGoogle Scholar
  16. Broussard D, Risch T, Dobson F, Murie J (2003) Senescence and age-related of female reproduction Columbian ground squirrels. J Anim Ecol 72:212–219CrossRefGoogle Scholar
  17. Brown SK, Hull JM, Updike DR et al (2009) Black bear population genetics in California: signatures of population structure, competitive release, and historical translocation. J Mammal 90:1066–1074CrossRefGoogle Scholar
  18. Bryant MJ, Reznick D (2004) Comparative studies of senescence in natural populations of guppies. Am Nat 163:55–68. doi:10.1086/380650 CrossRefPubMedGoogle Scholar
  19. Buffenstein R, Edrey YH, Yang T, Mele J (2008) The oxidative stress theory of aging: embattled or invincible? Insights from non-traditional model organisms. Age 30:99–109. doi:10.1007/s11357-008-9058-z CrossRefPubMedPubMedCentralGoogle Scholar
  20. Callicott RJ, Womack JE (2006) Real-time PCR assay for measurement of mouse telomeres. Comp Med 56:17–22PubMedGoogle Scholar
  21. Cassidy A, De Vivo I, Liu Y et al (2010) Associations between diet, lifestyle factors, and telomere length in women. Am J Clin Nutr 91:1273–1280. doi:10.3945/ajcn.2009.28947.INTRODUCTION CrossRefPubMedPubMedCentralGoogle Scholar
  22. Cawthon RM (2002) Telomere measurement by quantitative PCR. Nucleic Acids Res 30:e47CrossRefPubMedPubMedCentralGoogle Scholar
  23. Cawthon RM (2009) Telomere length measurement by a novel monochrome multiplex quantitative PCR method. Nucleic Acids Res 37:e21. doi:10.1093/nar/gkn1027 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Cichoń M, Sendecka J, Gustafsson L (2003) Age-related decline in humoral immune function in Collared Flycatchers. J Evol Biol 16:1205–1210. doi:10.1046/j.1420-9101.2003.00611.x CrossRefPubMedGoogle Scholar
  25. Costello C, Jones D, Inman R et al (2003) Relationship of variable mast production to American black bear reproductive parameters in New Mexico. Ursus 14:1–16Google Scholar
  26. Daniala L, Benetos A, Susser E, Kark JD et al (2013) Telomeres shorten at equivalent rates in somatic tissues of adults. Nat Commun 4:1597CrossRefGoogle Scholar
  27. Dunshea G, Duffield D, Gales N et al (2011) Telomeres as age markers in vertebrate molecular ecology. Mol Ecol Resour 11:225–235. doi:10.1111/j.1755-0998.2010.02976.x CrossRefPubMedGoogle Scholar
  28. Epel ES, Blackburn EH, Lin J et al (2004) Accelerated telomere shortening in response to life stress. Proc Natl Acad Sci USA 101:17312–17315. doi:10.1073/pnas.0407162101 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Fairlie J, Holland R, Pilkington JG et al (2016) Lifelong leukocyte telomere dynamics and survival in a free-living mammal. Aging Cell 15:140–148CrossRefPubMedGoogle Scholar
  30. Fedorov VB, Goropashnaya AV, Tøien O et al (2009) Elevated expression of protein biosynthesis genes in liver and muscle of hibernating black bears (Ursus americanus). Physiol Genomics 37:108–118. doi:10.1152/physiolgenomics.90398.2008 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247CrossRefPubMedGoogle Scholar
  32. Gilbert ER, Wong EA, Vaughan M, Webb KE (2007) Distribution and abundance of nutrient transporter mRNA in the intestinal tract of the black bear, Ursus americanus. Comp Biochem Physiol Part B 146:35–41CrossRefGoogle Scholar
  33. Gomes NMV, Ryder OA, Houck ML et al (2011) Comparative biology of mammalian telomeres: hypotheses on ancestral states and the roles of telomeres in longevity determination. Aging Cell 10:761–768. doi:10.1111/j.1474-9726.2011.00718.x CrossRefPubMedPubMedCentralGoogle Scholar
  34. Haussmann MF, Winkler DW, O’Reilly KM et al (2003) Telomeres shorten more slowly in long-lived birds and mammals than in short-lived ones. Proc R Soc B Biol Sci 270:1387–1392. doi:10.1098/rspb.2003.2385 CrossRefGoogle Scholar
  35. Hilderbrand GV, Schwartz CC, Robbins CT et al (1999) The importance of meat, particularly salmon, to body size, population productivity, and conservation of North American brown bears. Can J Zool 77:132–138. doi:10.1139/cjz-77-1-132 CrossRefGoogle Scholar
  36. Horn T, Robertson BC, Gemmell NJ (2010) The use of telomere length in ecology and evolutionary biology. Heredity 105:497–506. doi:10.1038/hdy.2010.113 CrossRefPubMedGoogle Scholar
  37. Horn T, Robertson BC, Will M et al (2011) Inheritance of telomere length in a bird. Plos One 6:e17199. doi:10.1371/journal.pone.0017199 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Houben JMJ, Moonen HJJ, van Schooten FJ, Hageman GJ (2008) Telomere length assessment: biomarker of chronic oxidative stress? Free Radic Biol Med 44:235–246. doi:10.1016/j.freeradbiomed.2007.10.001 CrossRefPubMedGoogle Scholar
  39. Izzo C, Hamer DJ, Bertozzi T et al (2011) Telomere length and age in pinnipeds: the endangered Australian sea lion as a case study. Mar Mamm Sci 27:841–851CrossRefGoogle Scholar
  40. Jacoby ME, Hilderbrand GV, Servheen C et al (1999) Trophic relations of brown and black bears in several western North American ecosystems. J Wildl Manag 63:921–929CrossRefGoogle Scholar
  41. Johnson KG, Pelton MR (1980) Environmental relationships and the denning period of black bears in Tennessee. J Mammal 61:653–660CrossRefGoogle Scholar
  42. Kirby R, Alldredge MW, Pauli JN (2016) The diet of black bears tracks the human footprint across a rapidly developing landscape. Biol Cons 200:51–59CrossRefGoogle Scholar
  43. Kotrschal A, Ilmonen P, Penn DJ (2007) Stress impacts telomere dynamics. Biol Lett 3:128–130. doi:10.1098/rsbl.2006.0594 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Laske TG, Garshelis DL, Iaizzo PA (2011) Monitoring the wild black bear’s reaction to human and environmental stressors. BMC Physiol 11:13. doi:10.1186/1472-6793-11-13 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Leri A, Malhotra A, Liew C et al (2000) Telomerase activity in rat cardiac myocytes is age and gender dependent. J Mol Cell Cardiol 32:385–390CrossRefPubMedGoogle Scholar
  46. Lewin N, Treidel LA, Holekamp KE et al (2015) Socioecological variables predict telomere length in wild spotted hyenas. Biol Lett 11:20140991CrossRefPubMedPubMedCentralGoogle Scholar
  47. Liker A, Szekely T (2005) Mortality costs of sexual selection and parental care in natural populations of birds. Evolution 59:890–897CrossRefPubMedGoogle Scholar
  48. Lyman CP, Brien RCO, Greene GC, Papafrangos ED (1981) Hibernation and longevity in the Turkish hamster Mesocricetus brandi. Science 212:668–670CrossRefPubMedGoogle Scholar
  49. Mackenzie DK, Bussière LF, Tinsley MC (2011) Senescence of the cellular immune response in Drosophila melanogaster. Exp Gerontol 46:853–859. doi:10.1016/j.exger.2011.07.004 CrossRefPubMedGoogle Scholar
  50. Melvin RG, Andrews MT (2009) Torpor induction in mammals: recent discoveries fueling new ideas. Trends Endocrinol Metab 20:490–498. doi:10.1016/j.tem.2009.09.005 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Meyne J, Ratiliff RL, Moyzis RK (1989) Conservation of the human telomere sequence (TTAGGG)n among vertebrates. Proc Natl Acad Sci USA 86:7049–7053CrossRefPubMedPubMedCentralGoogle Scholar
  52. Mizutani Y, Tomita N, Niizuma Y, Yoda K (2013) Environmental perturbations influence telomere dynamics in long-lived birds in their natural habitat. Biol Lett 9:20130511. doi:10.1098/rsbl.2013.0511 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Monaghan P (2010a) Telomeres and life histories: the long and the short of it. Ann N Y Acad Sci 1206:130–142. doi:10.1111/j.1749-6632.2010.05705.x CrossRefPubMedGoogle Scholar
  54. Monaghan P (2010b) Crossing the great divide: telomeres and ecology. Heredity 105:574–575. doi:10.1038/hdy.2010.120 CrossRefPubMedGoogle Scholar
  55. Monaghan P, Haussmann MF (2006) Do telomere dynamics link lifestyle and lifespan? Trends Ecol Evol 21:47–53. doi:10.1016/j.tree.2005.11.007 CrossRefPubMedGoogle Scholar
  56. Nakagawa S, Gemmell NJ, Burke T (2004) Measuring vertebrate telomeres: applications and limitations. Mol Ecol 13:2523–2533. doi:10.1111/j.1365-294X.2004.02291.x CrossRefPubMedGoogle Scholar
  57. Noyce K, Garshelis D (1994) Body size and blood characteristics as indicators of condition and reproductive performance in black bears. Int Conf Bear Res Manag 9:481–496Google Scholar
  58. Nussey DH, Froy H, Lemaitre J-F et al (2013) Senescence in natural populations of animals: widespread evidence and its implications for bio-gerontology. Ageing Res Rev 12:214–225. doi:10.1016/j.arr.2012.07.004 CrossRefPubMedGoogle Scholar
  59. Olsen MT, Bérubé M, Robbins J, Palsbøll PJ (2012) Empirical evaluation of humpback whale telomere length estimates; quality control and factors causing variability in the singleplex and multiplex qPCR methods. BMC Genet 13:77. doi:10.1186/1471-2156-13-77 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Olsson M, Pauliny A, Wapstra E et al (2011) Sexual differences in telomere selection in the wild. Mol Ecol 20:2085–2099. doi:10.1111/j.1365-294X.2011.05085.x CrossRefPubMedGoogle Scholar
  61. Paetkau D, Strobeck C (1994) Microsatellite analysis of genetic variation in black bear populations. Mol Ecol 3:489–495CrossRefPubMedGoogle Scholar
  62. Patel R, McIntosh L, McLaughlin J et al (2002) Disruptive effects of glucocorticoids on glutathione peroxidase biochemistry in hippocampal cultures. J Neurochem 82:118–125CrossRefPubMedGoogle Scholar
  63. Pauli JN, Whiteman JP, Marcot BG et al (2011) DNA-based approach to aging martens (Martes americana and M. caurina). J Mammal 92:500–510. doi:10.1644/10-MAMM-A-252.1 CrossRefGoogle Scholar
  64. Pauliny A, Wagner RH, Augustin J et al (2006) Age-independent telomere length predicts fitness in two bird species. Mol Ecol 15:1681–1687. doi:10.1111/j.1365-294X.2006.02862.x CrossRefPubMedGoogle Scholar
  65. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29:e45CrossRefPubMedPubMedCentralGoogle Scholar
  66. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multi-locus genotype data. Genetics 255:945–959Google Scholar
  67. Punzo F, Chavez S (2003) Effect of aging on spatial learning and running speed in the shrew (Cryptotis parva). J Mammal 84:1112–1120. doi:10.1644/BWG-106 CrossRefGoogle Scholar
  68. Radeloff VC, Stewart SI, Hawbaker TJ et al (2010) Housing growth in and near United States protected areas limits their conservation value. Proc Natl Acad Sci 107:940–945. doi:10.1073/pnas.0911131107 CrossRefPubMedGoogle Scholar
  69. Ringsby TH, Jensen H, Parn H et al (2015) On being the right size: increased body size is associated with reduced telomere length under natural conditions. Proc R Soc B Biol Sci 282:20152331CrossRefGoogle Scholar
  70. Robbins CT, Schwartz CC, Felicetti LA (2004) Nutritional ecology of ursids: a review of newer methods and management implications. Ursus 15:161–171CrossRefGoogle Scholar
  71. Robinson MR, Mar KU, Lummaa V (2012) Senescence and age-specific trade-offs between reproduction and survival in female Asian elephants. Ecol Lett 15:260–266. doi:10.1111/j.1461-0248.2011.01735.x CrossRefPubMedGoogle Scholar
  72. Rogers L (1987) Effects of food supply and kinship on social behavior, movements, and population growth of black bears in northeastern Minnesota. Wildl Monogr 97:3–72Google Scholar
  73. Ruijter JM, Ramakers C, Hoogaars WMH et al (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37:e45. doi:10.1093/nar/gkp045 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Schwartz CC, Keating KA, Reynolds HV et al (2003) Reproductive maturation and senescence in the female brown bear. Ursus 14:109–119Google Scholar
  75. Scott NM, Haussmann MF, Elsey RM et al (2006) Telomere length shortens with body length in Alligator mississippiensis. Southeast Nat 5:685–692. doi:10.1656/1528-7092(2006)5[685:TLSWBL]2.0.CO;2 CrossRefGoogle Scholar
  76. Seluanov A, Chen Z, Hine C (2007) Telomerase activity coevolves with body mass, not lifespan. Aging Cell 6:45–52. doi:10.1111/j.1474-9726.2006.00262.x CrossRefPubMedGoogle Scholar
  77. Shi Q, Hubbard GB, Kushwaha RS et al (2007) Endothelial senescence after high-cholesterol, high-fat diet challenge in baboons. Am J Physiol Hear Circ Physiol 292:H2913–H2920. doi:10.1152/ajpheart.01405.2006 CrossRefGoogle Scholar
  78. Smith DL, Mattison JA, Desmond RA et al (2011a) Telomere dynamics in rhesus monkeys: no apparent effect of caloric restriction. J Gerontol A Biol Sci Med Sci 66:1163–1168CrossRefPubMedGoogle Scholar
  79. Smith S, Turbill C, Penn DJ (2011b) Chasing telomeres, not red herrings, in evolutionary ecology. Heredity 107:372–373CrossRefPubMedPubMedCentralGoogle Scholar
  80. Stevenson RD, Woods WA (2006) Condition indices for conservation: new uses for evolving tools. Integr Comp Biol 46:1169–1190. doi:10.1093/icb/icl052 CrossRefPubMedGoogle Scholar
  81. Tarlow EM, Blumstein DT (2007) Evaluating methods to quantify anthropogenic stressors on wild animals. Appl Anim Behav Sci 102:429–451. doi:10.1016/j.applanim.2006.05.040 CrossRefGoogle Scholar
  82. Tøien Ø, Blake J, Edgar DM et al (2011) Hibernation in black bears: independence of metabolic suppression from body temperature. Science 331:906–909. doi:10.1126/science.1199435 CrossRefPubMedGoogle Scholar
  83. Tøien Ø, Blake J, Barnes BM (2015) Thermoregulation and energetics in hibernating black bears: metabolic rate and the mystery of multi-day body temperature cycle. J Comp Physiol B 185:447. doi:10.1007/s00360-015-0891-y CrossRefPubMedGoogle Scholar
  84. Turbill C, Bieber C, Ruf T (2011) Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proc R Soc B Biol Sci 278:3355–3363. doi:10.1098/rspb.2011.0190 CrossRefGoogle Scholar
  85. Turbill C, Smith S, Deimel C, Ruf T (2012) Daily torpor is associated with telomere length change over winter in Djungarian hamsters. Biol Lett 8:304–307. doi:10.1098/rsbl.2011.0758 CrossRefPubMedGoogle Scholar
  86. Turbill C, Ruf T, Smith S, Bieber C (2013) Seasonal variation in telomere length of a hibernating rodent. Biol Lett 9:20121095CrossRefPubMedPubMedCentralGoogle Scholar
  87. Ujvari B, Madsen T (2009) Short telomeres in hatchling snakes: erythrocyte telomere dynamics and longevity in tropical pythons. Plos One 4:e7493CrossRefPubMedPubMedCentralGoogle Scholar
  88. von Zglinicki T (2002) Oxidative stress shortens telomeres. Trends Biochem Sci 27:339–344CrossRefGoogle Scholar
  89. Watson JD (1972) Origin of concatameric T4 DNA. Nature 239:197–201CrossRefGoogle Scholar
  90. Wiegand T, Naves J, Garbulsky MF, Fernández N (2008) Animal habitat quality and ecosystem functioning: exploring seasonal patterns using NDVI. Ecol Monogr 78:87–103. doi:10.1890/06-1870.1 CrossRefGoogle Scholar
  91. Wilkinson GS, South JM (2002) Life history, ecology and longevity in bats. Aging Cell 1:124–131CrossRefPubMedGoogle Scholar
  92. Willey C (1974) Aging black bears from first premolar tooth sections. J Wildl Manag 38:97–100CrossRefGoogle Scholar
  93. Young RC, Kitaysky AS, Haussmann MF et al (2013) Age, sex, and telomere dynamics in a long-lived seabird with male-biased parental care. Plos One 8:e74931. doi:10.1371/journal.pone.0074931 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Young RC, Kitaysky AS, Barger CP et al (2015) Telomere length is a strong predictor of foraging behavior in a long-lived seabird. Ecosphere 6:1–26CrossRefGoogle Scholar
  95. Yu L, Li Q, Ryder OA, Zhang Y (2004) Phylogeny of the bears (Ursidae) based on nuclear and mitochondrial genes. Mol Phylogenet Evol 32:480–494. doi:10.1016/j.ympev.2004.02.015 CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.Department of Forest and Wildlife EcologyUniversity of Wisconsin – MadisonMadisonUSA
  2. 2.Mammals Research SectionColorado Parks and WildlifeFort CollinsUSA

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