Sex differences in leucocyte telomere length in a free-living mammal

Molecular Ecology

Volumn 26, Issue 12, 2017, Pages 3230-3240

  Watson, Rebecca L ^a   Bird, Ellen J ^a   Underwood, Sarah ^a   Wilbourn, Rachael V ^a   Fairlie, Jennifer ^a   Watt, Kathryn ^a   Salvo Chirnside, Eliane ^a   Pilkington, Jill G ^a   Pemberton, Josephine M ^a   McNeilly, Tom N ^b   Froy, Hannah ^a   Nussey, Daniel H ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b MOREDUN RESEARCH INSTITUTE   (United Kingdom)

Author keywords

granulocyte; lymphocyte; Ovis aries; polygyny; sexual selection; Soay sheep

Indexed keywords

ANIMAL; CROSS-SECTIONAL STUDY; FEMALE; GENETICS; LEUKOCYTE; MALE; SEXUAL CHARACTERISTICS; SHEEP; TELOMERE; TELOMERE SHORTENING; ULTRASTRUCTURE;

ANIMALS; CROSS-SECTIONAL STUDIES; FEMALE; LEUKOCYTES; MALE; SEX CHARACTERISTICS; SHEEP; TELOMERE; TELOMERE SHORTENING;

EID: 85011347235     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.13992     Document Type: Article

References (68)

1. Akkad A, Hastings R, Konje J et al. (2006) Telomere length in small-for-gestational-age babies. BJOG: An International Journal of Obstetrics & Gynaecology, 113, 318–323.
2. Andersson M (1994) Sexual Selection. Princeton University Press, Princeton, New Jersey.
3. Armanios M, Blackburn EH (2012) The telomere syndromes. Nature Reviews Genetics, 13, 693–704.
4. Asghar M, Hasselquist D, Hansson B et al. (2015) Hidden costs of infection: chronic malaria accelerates telomere degradation and senescence in wild birds. Science, 347, 436–438.
5. Asghar M, Palinauskas V, Zaghdoudi-Allan NG et al. (2016) Parallel telomere shortening in multiple body tissues owing to malaria infection. Proceedings of the Royal Society London, Series B, 283, 20161184.
6. Aubert G, Baerlocher GM, Vulto I, Poon SS, Lansdorp PM (2012) Collapse of telomere homeostasis in hematopoietic cells caused by heterozygous mutations in telomerase genes. PLoS Genetics, 8, e1002696.
7. Aviv A, Shay J, Christensen K, Wright W (2005) The longevity gender gap: are telomeres the explanation? Science's SAGE KE, 2005, pe16.
8. Baerlocher GM, Rice K, Vulto I, Lansdorp PM (2007) Longitudinal data on telomere length in leukocytes from newborn baboons support a marked drop in stem cell turnover around 1 year of age. Aging Cell, 6, 121–123.
9. Bain BJ (2014) Blood Cells: a Practical Guide. John Wiley & Sons, Oxford.
10. Barrett ELB, Richardson DS (2011) Sex differences in telomeres and lifespan. Aging Cell, 10, 913–921.
11. Barrett ELB, Burke TA, Hammers M, Komdeur J, Richardson DS (2013) Telomere length and dynamics predict mortality in a wild longitudinal study. Molecular Ecology, 22, 249–259.
12. Bauch C, Becker PH, Verhulst S (2013) Telomere length reflects phenotypic quality and costs of reproduction in a long-lived seabird. Proceedings of the Royal Society London B, 280, 20122540.
13. 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.
14. Beirne C, Delahay R, Hares M, Young A (2014) Age-related declines and disease-associated variation in immune cell telomere length in a wild mammal. PLoS ONE, 9, e108964.
15. Berglund K, Reynolds CA, Ploner A et al. (2016) Longitudinal decline of leukocyte telomere length in old age and the association with sex and genetic risk. Aging, 8, 7.
16. Bize P, Criscuolo F, Metcalfe NB, Nasir L, Monaghan P (2009) Telomere dynamics rather than age predict life expectancy in the wild. Proceedings of the Royal Society London B, 276, 1679–1683.
17. Blackburn EH (1991) Structure and function of telomeres. Nature, 350, 569–573.
18. Blackburn EH, Epel ES, Lin J (2015) Human telomere biology: a contributory and interactive factor in aging, disease risks, and protection. Science, 350, 1193–1198.
19. Cawthon RM (2002) Telomere measurement by quantitative PCR. Nucleic Acids Research, 30, e47.
20. 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. The Lancet, 361, 393–395.
21. Cherif H, Tarry J, Ozanne S, Hales C (2003) Ageing and telomeres: a study into organ- and gender-specific telomere shortening. Nucleic Acids Research, 31, 1576–1583.
22. Clutton-Brock TH, Pemberton JM (2004) Soay Sheep: Dynamics and Selection in an Island Population. Cambridge University Press, Cambridge.
23. Coviello-McLaughlin GM, Prowse KR (1997) Telomere length regulation during postnatal development and ageing in Mus spretus. Nucleic Acids Research, 25, 3051–3058.
24. Daniali L, Benetos A, Susser E et al. (2013) Telomeres shorten at equivalent rates in somatic tissues of adults. Nature Communications, 4, 1597.
25. De Lange T (2004) T-loops and the origin of telomeres. Nature Reviews Molecular Cell Biology, 5, 323–329.
26. Epel ES, Blackburn EH, Lin J et al. (2004) Accelerated telomere shortening in response to life stress. Proceedings of the National Academy of Sciences of the United States of America, 101, 17312–17315.
27. Factor-Litvak P, Susser E, Kezios K et al. (2016) Leukocyte telomere length in newborns: implications for the role of telomeres in human disease. Pediatrics, 137, e20153927.
28. Fairlie J, Holland R, Pilkington JG et al. (2016) Life-long leukocyte telomere dynamics and survival in a free-living mammal. Aging Cell, 15, 140–148.
29. Gardner JP, Kimura M, Chai W et al. (2007) Telomere dynamics in Macaques and humans. Journals of Gerontology Series A-Biological Sciences And Medical Sciences, 62, 367–374.
30. Gardner M, Bann D, Wiley L et al. (2014) Gender and telomere length: systematic review and meta-analysis. Experimental Gerontology, 51, 15–27.
31. Giefing-Kröll C, Berger P, Lepperdinger G, Grubeck-Loebenstein B (2015) How sex and age affect immune responses, susceptibility to infections, and response to vaccination. Aging Cell, 14, 309–321.
32. 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.
33. Gulland FMD, Fox M (1992) Epidemiology of Nematode Infections of Soay Sheep (Ovis aries L) on St-Kilda. Parasitology, 105, 481–492.
34. Hayward AD, Wilson AJ, Pilkington JG, Pemberton JM, Kruuk LEB (2009) Ageing in a variable habitat: environmental stress affects senescence in parasite resistance in St Kilda Soay sheep. Proceedings of the Royal Society of London B, 276, 3477–3485.
35. Heidinger BJ, Blount JD, Boner W et al. (2012) Telomere length in early life predicts lifespan. Proceedings of the National Academy of Sciences of the United States of America, 109, 1743–1748.
36. Hemann MT, Strong MA, Hao L-Y, Greider CW (2001) The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell, 107, 67–77.
37. Ilmonen P, Kotrschal A, Penn DJ (2008) Telomere attrition due to infection. PLoS ONE, 3, e2143.
38. Johnston SE, Gratten J, Berenos C et al. (2013) Life history trade-offs at a single locus maintain sexually selected genetic variation. Nature, 502, 93–95.
39. Kimura M, Gazitt Y, Cao X et al. (2010) Synchrony of telomere length among hematopoietic cells. Experimental Hematology, 38, 854–859.
40. Lapham K, Kvale MN, Lin J et al. (2015) Automated assay of telomere length measurement and informatics for 100,000 subjects in the Genetic Epidemiology Research on Adult Health and Aging (GERA) cohort. Genetics, 200, 1061–1072.
41. Linton PJ, Dorshkind K (2004) Age-related changes in lymphocyte development and function. Nature Immunology, 5, 133–139.
42. Monaghan P (2010) Telomeres and life histories: the long and the short of it. Annals of the New York Academy of Science, 1206, 130–142.
43. Monaghan P (2014) Organismal stress, telomeres and life histories. Journal of Experimental Biology, 217, 57–66.
44. Monaghan P, Haussmann MF (2006) Do telomere dynamics link lifestyle and lifespan? Trends in Ecology & Evolution, 21, 47–53.
45. Moore SL, Wilson K (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science, 297, 2015–2018.
46. Nussey DH, Watt K, Pilkington JG, Zamoyska R, McNeilly TN (2012) Age-related variation in immunity in a wild mammal population. Aging Cell, 11, 178–180.
47. Okuda K, Bardeguez A, Gardner JP et al. (2002) Telomere length in the newborn. Pediatric Research, 52, 377–381.
48. Olsson M, Pauliny A, Wapstra E et al. (2011) Sexual differences in telomere selection in the wild. Molecular Ecology, 20, 2085–2099.
49. Pawelec G, Larbi A, Derhovanessian E (2010) Senescence of the human immune system. Journal of Comparative Pathology, 142, S39–S44.
50. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29, e45.
51. R Core Development Team (2012) R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria.
52. Reichert S, Criscuolo F, Verinaud E, Zahn S, Massemin S (2013) Telomere length correlations among somatic tissues in adult zebra finches. PLoS ONE, 8, e81496.
53. Reichert S, Stier A, Zahn S et al. (2014) Increased brood size leads to persistent eroded telomeres. Frontiers in Ecology and Evolution, 2, 9.
54. Rode L, Nordestgaard BG, Bojesen SE (2015) Peripheral blood leukocyte telomere length and mortality among 64 637 individuals from the general population. Journal of the National Cancer Institute, 107, djv074.
55. Ruijter JM, Ramakers C, Hoogaars WMH et al. (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Research, 37, e45.
56. Salomons HM, Mulder GA, van de Zande L et al. (2009) Telomere shortening and survival in free-living corvids. Proceedings of the Royal Society London B, 276, 3157–3165.
57. Seeker LA, Holland R, Underwood S et al. (2016) Method specific calibration corrects for DNA extraction method effects on relative telomere length measurements by quantitative PCR. PLoS ONE, 11, e0164046.
58. Shalev I (2012) Early life stress and telomere length: investigating the connection and possible mechanisms. BioEssays, 34, 943–952.
59. Shi-Ni L, Yahya Z, Zeegers D et al. (2013) Distribution of telomere length in the cord blood of Chinese newborns. British Journal of Medicine and Medical Research, 3, 1004.
60. Smith DL, Mattison JA, Desmond RA et al. (2011) Telomere dynamics in rhesus monkeys: no apparent effect of caloric restriction. Journals of Gerontology Series A-Biological Sciences and Medical Sciences, 66, 1163–1168.
61. Stindl R (2004) Tying it all together: telomeres, sexual size dimorphism and the gender gap in life expectancy. Medical Hypotheses, 62, 151–154.
62. Sudyka J, Arct A, Drobniak S et al. (2014) Experimentally increased reproductive effort alters telomere length in the blue tit (Cyanistes caeruleus). Journal of Evolutionary Biology, 27, 2258–2264.
63. Tarry-Adkins JL, Ozanne SE, Norden A, Cherif H, Hales CN (2006) Lower antioxidant capacity and elevated p53 and p21 may be a link between gender disparity in renal telomere shortening, albuminuria, and longevity. American Journal of Physiology-Renal Physiology, 290, F509–F516.
64. Voillemot M, Hine K, Zahn S et al. (2012) Effects of brood size manipulation and common origin on phenotype and telomere length in nestling collared flycatchers. BMC Ecology, 12, 17.
65. Watson RL, McNeilly TN, Watt KA et al. (2016) Cellular and humoral immunity in a wild mammal: Variation with age & sex and association with over-winter survival. Ecology & Evolution, 6, 8695–8705.
66. Weng N-P (2001) Interplay between telomere length and telomerase in human leukocyte differentiation and aging. Journal of Leukocyte Biology, 70, 861–867.
67. Wilson K, Grenfell BT, Pilkington JG, Boyd HEG, Gulland FM (2004) Parasites and their impact. In: Soay Sheep: Dynamics and Selection in an Island Population (eds Clutton-Brock TH, Pemberton JM), pp. 113–165. Cambridge University Press, Cambridge.
68. von Zglinicki T (2002) Oxidative stress shortens telomeres. Trends in Biochemical Sciences, 27, 339–344.