Telomere length reflects phenotypic quality and costs of reproduction in a long-lived seabird

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1752, 2013, Pages

  Bauch, Christina ^a   Becker, Peter H ^a   Verhulst, Simon ^b  

^a INSTITUTE OF AVIAN RESEARCH VOGELWARTE HELGOLAND   (Germany)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Age; Arrival; Common tern; Individual quality; Lifestyle; Reproductive performance

Indexed keywords

ARRIVAL DATE; BROOD REARING; FOOD PROVISIONING; LIFE EXPECTANCY; NEST; PHENOTYPIC PLASTICITY; REPRODUCTIVE COST; REPRODUCTIVE POTENTIAL; REPRODUCTIVE SUCCESS; SEABIRD; SENESCENCE;

EID: 84870771744     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.2540     Document Type: Article

References (63)

1. Blackburn EH. 1991 Structure and function of telomeres. Nature 350, 569-573. (doi:10.1038/350569a0)
2. Cawthon RM, Smith KR, O'Brien E, Sivatchenko A, Kerber RA. 2003 Association between telomere length in blood and mortality in people aged 60 years or older. Lancet 361, 393-395. (doi:10.1016/S0140-6736(03)12384-7)
3. Chang S, Multani AS, Cabrera NG, Naylor ML, Laud P, Lombard D, Pathak S, Guarente L, DePinho RA. 2004 Essential role of limiting telomeres in the pathogenesis of Werner syndrome. Nat. Genet. 36, 877-882. (doi:10.1038/ng1389)
4. Hofer AC, Tran RT, Aziz OZ, Wright W, Novelli G, Shay J, Lewis M. 2005 Shared phenotypes among segmental progeroid syndromes suggest underlying pathways of aging. J. Gerontol. A Biol. Sci. Med. Sci. 60, 10-20. (doi:10.1093/gerona/60.1.10)
5. Monaghan P. 2010 Telomeres and life histories: the long and the short of it. Ann. NY Acad. Sci. 1206, 130-142. (doi:10.1111/j.1749-6632.2010.05705.x)
6. Aviv A. 2006 Telomeres and human somatic fitness. J. Gerontol. A Biol. Sci. Med. Sci. 61, 871-873. (doi:10.1093/gerona/61.8.871)
7. Olovnikov AM. 1973 A theory of marginotomy: the incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J. Theor. Biol. 41, 181-190. (doi:10.1016/0022-5193(73)90198-7)
8. von Zglinicki T. 2000 Role of oxidative stress in telomere length regulation and replicative senescence. Ann. NY Acad. Sci. 908, 99-110. (doi:10.1111/j.1749-6632.2000.tb06639.x)
9. von Zglinicki T. 2002 Oxidative stress shortens telomeres. Trends Biochem. Sci. 27, 339-344. (doi:10.1016/S0968-0004(02)02110-2)
10. Houben JMJ, Moonen HJJ, van Schooten FJ, Hageman GJ. 2008 Telomere length assessment: biomarker of chronic oxidative stress? Free Rad. Bio. Med. 44, 235-246. (doi:10.1016/j.freeradbiomed. 2007.10.001)
11. Karlseder J, Smogorzewska A, de Lange T. 2002 Senescence induced by altered telomere state, not telomere loss. Science 295, 2446-2449. (doi:10. 1126/science.1069523)
12. Greider CW. 1996 Telomere length regulation. Annu. Rev. Biochem. 65, 337-365. (doi:10.1146/annurev. bi.65.070196.002005)
13. Brümmendorf TH, Mak J, Sabo KM, Baerlocher GM, Dietz K, Abkowitz JL, Lansdorp PM. 2002 Longitudinal studies of telomere length in feline blood cells: implications for hematopoietic stem cell turnover in vivo. Exp. Hematol. 30, 1147-1152. (doi:10.1016/S0301-472X(02)00888-3)
14. Aviv A, Chen W, Gardner JP, Kimura M, Brimacombe M, Cao X, Srinivasan SR, Berenson GS. 2009 Leukocyte telomere dynamics: longitudinal findings among young adults in the Bogalusa heart study. Am. J. Epidemiol. 169, 323-329. (doi:10.1093/aje/kwn338)
15. Hall ME, Nasir L, Daunt F, Gault EA, Croxall JP, Wanless S, Monaghan P. 2004 Telomere loss in relation to age and early environment in long-lived birds. Proc. R. Soc. Lond. B 271, 1571-1576. (doi:10.1098/rspb.2004.2768)
16. Pauliny A, Wagner RH, Augustin J, Szép T, Blomqvist D. 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)
17. Salomons HM, Mulder GA, van de Zande L, Haussmann MF, Linskens MHK, Verhulst S. 2009 Telomere shortening and survival in free-living corvids. Proc. R. Soc. B 276, 3157-3165. (doi:10.1098/rspb.2009.0517)
18. Slagboom PE, Droog S, Boomsma DI. 1994 Genetic determination of telomere size in humans: a twin study of 3 age-groups. Am. J. Hum. Genet. 55, 876-882.
19. Bakaysa SL, Mucci LA, Slagboom PE, Boomsma DI, McClearn GE, Johansson B, Pedersen NL. 2007 Telomere length predicts survival independent of genetic influences. Aging Cell 6, 769-774. (doi:10.1111/j.1474-9726.2007.00340.x)
20. Jennings BJ, Ozanne SE, Dorling MW, Hales CN. 1999 Early growth determines longevity in male rats and may be related to telomere shortening in the kidney. FEBS Lett. 448, 4-8. (doi:10.1016/S0014-5793(99)00336-1)
21. Epel ES, Blackburn EH, Lin J, Dhabhar FS, Adler NE, Morrow JD, Cawthon RM. 2004 Accelerated telomere shortening in response to life stress. Proc. Natl Acad. Sci. USA 101, 17312-17315. (doi:10.1073/pnas.0407162101)
22. Valdes AM, Andrew T, Gardner JP, Kimura M, Oelsner E, Cherkas LF, Aviv A, Spector TD. 2005 Obesity, cigarette smoking, and telomere length in women. Lancet 366, 662-664. (doi:10.1016/S0140-6736(05)66630-5)
23. Cherkas LF, Aviv A, Valdes AM, Hunkin JL, Gardner JP, Surdulescu GL, Kimura M, Spector TD. 2006 The effects of social status on biological aging as measured by white-blood-cell telomere length. Aging Cell 5, 361-365. (doi:10.1111/j.1474-9726. 2006.00222.x)
24. Kotrschal A, Ilmonen P, Penn DJ. 2007 Stress impacts telomere dynamics. Biol. Lett. 3, 128-130. (doi:10.1098/rsbl.2006.0594)
25. Dijkstra C, Bult A, Bijlsma S, Daan S, Meijer T, Zijlstra M. 1990 Brood size manipulations in the kestrel (Falco tinnunculus): effects on offspring and parent survival. J. Anim. Ecol. 59, 269-285. (doi:10.2307/5172)
26. Monaghan P, Haussmann MF. 2006 Do telomere dynamics link lifestyle and lifespan? Trend. Ecol. Evol. 21, 47-53. (doi:10.1016/j.tree.2005.11.007)
27. Verhulst S. 1998 Multiple breeding in the great tit II. The costs of rearing a second clutch. Funct. Ecol. 12, 132-140. (doi:10.1046/j.1365-2435.1998.00165.x)
28. Bauch C, Kreutzer S, Becker PH. 2010 Breeding experience affects condition: blood metabolite levels over the course of incubation in a seabird. J. Comp. Physiol. B 180, 835-845. (doi:10.1007/s00360-010-0453-2)
29. Hamel S, Gaillard J.-M., Yoccoz NG, Loison A, Bonenfant C, Descamps S. 2010 Fitness costs of reproduction depend on life speed: empirical evidence from mammalian populations. Ecol. Lett. 13, 915-935. (doi:10.1111/j.1461-0248.2010.01478.x)
30. Haussmann MF, Salomons HM, Verhulst S. 2011 Telomere measurement tools: Telometric produces biased estimates of telomere length. Heredity 107, 371-371. (doi:10.1038/hdy.2011.10)
31. Olsson M, Pauliny A, Wapstra E, Uller T, Schwartz T, Miller E, Blomqvist D. 2011 Sexual differences in telomere selection in the wild. Mol. Ecol. 20, 2085-2099. (doi:10.1111/j.1365-294X.2011.05085.x)
32. Becker PH, Wendeln H, González-Solís J. 2001 Population dynamics, recruitment, individual quality and reproductive strategies in common terns marked with transponders. Ardea 89, 241-252.
33. Becker PH, Dittmann T, Ludwigs J-D, Limmer B, Ludwig SC, Bauch C, Braasch A, Wendeln H. 2008 Timing of initial arrival at the breeding site predicts age at first reproduction in a long-lived migratory bird. Proc. Natl Acad. Sci. USA 105, 12349-12352. (doi:10.1073/pnas.0804179105)
34. Wendeln H, Becker PH. 1999 Effects of parental quality and effort on the reproduction of common terns. J. Anim. Ecol. 68, 205-214. (doi:10.1046/j. 1365-2656.1999.00276.x)
35. Wiggins DA, Morris RD. 1987 Parental care of the common tern Sterna hirundo. Ibis 129, 533-540. (doi:10.1111/j.1474-919X.1987.tb08241.x)
36. Becker PH, Finck P. 1985 Witterung und Ernährungssituation als entscheidende Faktoren des Bruterfolgs der Flussseeschwalbe (Sterna hirundo). J. Ornithol. 126, 393-404. (doi:10.1007/BF01643404)
37. Bollinger PB. 1994 Relative effects of hatching order, egg-size variation, and parental quality on chick survival in common terns. Auk 111, 263-273. (doi:10.2307/4088591)
38. Szostek KL, Becker PH. 2011 Terns in trouble: demographic consequences of low breeding success and recruitment on a common tern population in the German Wadden Sea. J. Ornithol. 153, 313-326. (doi:10.1007/s10336-011-0745-7)
39. Kikker U. 1995 Wachstumsrate von Flussseeschwalbenküken in Abhängigkeit von brutbiologischen Faktoren und der Qualität der Altvögel. Diploma Thesis, University of Oldenburg, Germany.
40. Wiggins DA. 1989 Consequences of variation in brood size on the allocation of parental care in common terns (Sterna hirundo). Can. J. Zool. 67, 2411-2413. (doi:10.1139/z89-341)
41. Becker PH, Wendeln H. 1997 A new application for transponders in population ecology of the common tern. Condor 99, 534-538. (doi:10.2307/1369963)
42. Becker PH, Ezard THG, Ludwigs J-D, Sauer-Gürth H, Wink M. 2008 Population sex ratio shift from fledging to recruitment: consequences for demography in a philopatric seabird. Oikos 117, 60-68. (doi:10.1111/j.2007.0030-1299.16287.x)
43. Christians JK, Evanson M, Aiken JJ. 2001 Seasonal decline in clutch size in European starlings: a novel randomization test to distinguish between the timing and quality hypotheses. J. Anim. Ecol. 70, 1080-1087. (doi:10.1046/j.0021-8790.2001.00566.x)
44. Ezard THG, Becker PH, Coulson T. 2007 Correlations between age, phenotype and individual contribution to population growth in common terns. Ecology 88, 2496-2504. (doi:10.1890/06-2020.1)
45. Verhulst S, Nilsson J-Å. 2008 The timing of a birds' breeding seasons: a review of experiments that manipulated timing of breeding. Phil. Trans. R. Soc. B 363, 399-410. (doi:10.1098/rstb.2007.2146)
46. Becker PH, Wink M. 2002 Geschlechtsabhängige Größenunterschiede von Flügglingen der Flussseeschwalbe (Sterna hirundo). J. Ornithol. 143, 51-56. (doi:10.1007/BF02465458)
47. Becker PH, Voigt CC, Arnold JM, Nagel R. 2006 A non-invasive technique to bleed incubating birds without trapping: a blood-sucking bug in a hollow egg. J. Ornithol. 147, 115-118. (doi:10.1007/s10336-005-0027-3)
48. Lessels CM, Boag PT. 1987 Unrepeatable repeatabilities: a common mistake. Auk 104, 116-121. (doi:10.2307/4087240)
49. Arnold JM, Oswald SA, Voigt CC, Palme R, Braasch A, Bauch C, Becker PH. 2008 Taking the stress out of blood collection: comparison of field blood-sampling techniques for analysis of baseline corticosterone. J. Avian Biol. 39, 588-592. (doi:10. 1111/j.0908-8857.2008.04265.x)
50. Delany ME, Krupkin AB, Miller MM. 2000 Organization of telomere sequences in birds: evidence for arrays of extreme length and for in vivo shortening. Cytogenet. Cell Genet. 90, 139-145. (doi:10.1159/000015649)
51. Haussmann MF, Vleck CM, Nisbet ICT. 2003 Calibrating the telomere clock in common terns, Sterna hirundo. Exp. Gerontol. 38, 787-789. (doi:10.1016/S0531-5565(03)00109-8)
52. 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)
53. Tinbergen JM, Verhulst S. 2000 A fixed energetic ceiling to parental effort in the great tit? J. Anim. Ecol. 69, 323-334. (doi:10.1046/j1365-2656.2000.00395.x)
54. 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. Funct. Ecol. 25, 577-585. (doi:10.1111/j.1365-2435.2010.01825.x)
55. Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, Sorci G. 2004 Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol. Lett. 7, 363-368. (doi:10.1111/j.1461-0248. 2004.00594.x)
56. Wiersma P, Selman C, Speakman JR, Verhulst S. 2004 Birds sacrifice oxidative protection for reproduction. Proc. R. Soc. Lond. B 271, S360-S363. (doi:10.1098/rsbl.2004.0171)
57. Voituron Y, de Fraipont M, Issartel J, Guillaume O, Clobert J. 2011 Extreme lifespan of the human fish (Proteus anguinus): a challenge for ageing mechanisms. Biol. Lett. 7, 105-107. (doi:10.1098/rsbl.2010.0539)
58. Clutton-Brock TH. 1988 Reproductive success: studies of individual variation in contrasting breeding systems. Chicago, IL: University of Chicago Press.
59. Weladji RB, Loison A, Gaillard J-M, Holand Ø, Mysterud A, Yoccoz NG, Nieminen M, Stenseth NC. 2008 Heterogeneity in individual quality overrides costs of reproduction in female reindeer. Oecologia 156, 237-247. (doi:10.1007/s00442-008-0961-x)
60. Hamel S, Côté SD, Gaillard J-M, Festa-Bianchet M. 2009 Individual variation in reproductive costs of reproduction: high-quality females always do better. J. Anim. Ecol. 78, 143-151. (doi:10.1111/j.1365-2656.2008.01459.x)
61. Becker PH, Zhang H. 2011 Renesting of common terns (Sterna hirundo) in the life history perspective. J. Ornithol. 152, 213-225. (doi:10.1007/s10336-010-0639-0)
62. Hofer H, East ML. 1996 The components of parental care and their fitness consequences: a life history perspective. Verhandlungen der Deutschen Zoologischen Gesellschaft 89, 149-164.
63. Rebke M, Coulson T, Becker PH, Vaupel JW. 2010 Reproductive improvement and senescence in a long-lived bird. Proc. Natl Acad. Sci. USA 107, 7841-7846. (doi:10.1073/pnas.1002645107)