Mother–offspring and nest-mate resemblance but no heritability in early-life telomere length in white-throated dippers

Proceedings of the Royal Society B: Biological Sciences

Volumn 282, Issue 1807, 2015, Pages

  Becker, Philipp J J ^a   Reichert, Sophie ^b,c,d   Zahn, Sandrine ^b,c   Hegelbach, Johann ^a   Massemin, Sylvie ^b,c   Keller, Lukas F ^a   Postma, Erik ^a   Criscuolo, François ^b,c  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b INSTITUT DE RECHERCHES SUBATOMIQUES   (France)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Bird; Heritability; Inbreeding; Maternal effect; Relative telomere length; Sex linkage

Indexed keywords

CHROMOSOME; ENVIRONMENTAL FACTOR; EVOLUTIONARY BIOLOGY; GENETIC STRUCTURE; GENETIC VARIATION; HERITABILITY; IMPRINTING; INBREEDING; PARENT-OFFSPRING INTERACTION; PASSERINE;

AVES; CINCLUS CINCLUS; EUKARYOTA;

ANIMAL; FEMALE; GENETICS; INHERITANCE; MALE; PASSERIFORMES; PHYSIOLOGY; REGRESSION ANALYSIS; SEX DIFFERENCE; TELOMERE;

ANIMALS; FEMALE; INHERITANCE PATTERNS; MALE; PASSERIFORMES; REGRESSION ANALYSIS; SEX FACTORS; TELOMERE;

EID: 84928905804     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.2924     Document Type: Article

References (64)

1. Blackburn EH. 2000 Telomere states and cell fates. Nature 408, 53–56. (doi:10.1038/35040500)
2. Blackburn EH. 2001 Switching and signaling at the telomere. Cell 106, 661–673. (doi:10.1016/S0092-8674(01)00492-5)
3. von Zglinicki T. 2000 Role of oxidative stress in telomere length regulation and replicative senescence. Ann. N. Y. Acad. Sci. 908, 99–110. (doi:10.1111/j.1749-6632.2000.tb06639.x)
4. Heidinger BJ, Blount JD, Boner W, Griffiths K, Metcalfe NB, Monaghan P. 2012 Telomere length in early life predicts lifespan. Proc. Natl Acad. Sci. USA 109, 1743–1748. (doi:10.1073/pnas.1113306109)
5. Bize P, Criscuolo F, Metcalfe NB, Nasir L, Monaghan P. 2009 Telomere dynamics rather than age predict life expectancy in the wild. Proc. R. Soc. B 276, 1679–1683. (doi:10.1098/rspb.2008.1817)
6. 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)
7. Haussmann MF, Winkler DW, Vleck CM. 2005 Longer telomeres associated with higher survival in birds. Biol. Lett. 1, 212–214. (doi:10.1098/rsbl.2005.0301)
8. 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)
9. Bauch C, Becker PH, Verhulst S. 2013 Telomere length reflects phenotypic quality and costs of reproduction in a long-lived seabird. Proc. R. Soc. B 280, 20122540. (doi:10.1098/rspb.2012.2540)
10. Gomes N, Shay JW, Wright WE. 2010 Telomere biology in Metazoa. FEBS Lett. 584, 3741–3751. (doi:10.1016/j.febslet.2010.07.031)
11. Graakjaer J, Pascoe L, Der-Sarkissian H, Thomas G, Kolvraa S, Christensen K, Londoño-Vallejo JA. 2004 The relative lengths of individual telomeres are defined in the zygote and strictly maintained during life. Aging Cell 3, 97–102. (doi:10.1111/j.1474-9728.2004.00093.x)
12. Slagboom PE, Droog S, Boomsma DI. 1994 Genetic determination of telomere size in humans: a twin study of three age groups. Am. J. Hum. Genet. 55, 876.
13. Broer L et al. 2013 Meta-analysis of telomere length in 19713 subjects reveals high heritability, stronger maternal inheritance and a paternal age effect. Eur. J. Hum. Genet. 21, 1163–1168. (doi:10.1038/ejhg.2012.303)
14. Njajou OT et al. 2007 Telomere length is paternally inherited and is associated with parental lifespan. Proc. Natl Acad. Sci. USA 104, 12 135–12 139. (doi:10.1073/pnas.0702703104)
15. Asghar M, Bensch S, Tarka M, Hansson B, Hasselquist D. 2015 Maternal and genetic factors determine early life telomere length. Proc. R. Soc. B 282, 20142263. (doi:10.1098/rspb.2014.2263)
16. Horn T, Robertson BC, Will M, Eason DK, Elliott GP, Gemmell NJ. 2011 Inheritance of telomere length in a bird. PLoS ONE 6, e17199. (doi:10.1371/journal.pone.0017199)
17. Olsson M, Pauliny A, Wapstra E, Uller T, Schwartz T, Blomqvist D. 2011 Sex differences in sand lizard telomere inheritance: paternal epigenetic effects increases telomere heritability and offspring survival. PLoS ONE 6, e17473. (doi:10.1371/journal.pone.0017473)
18. Reichert S, Rojas ER, Zahn S, Robin JP, Criscuolo F, Massemin S. 2015 Maternal telomere length inheritance in the king penguin. Heredity 114, 10–16. (doi:10.1038/hdy.2014.60)
19. Voillemot M, Hine K, Zahn S, Criscuolo F, Gustafsson L, Doligez B, Bize P. 2012 Effects of brood size manipulation and common origin on phenotype and telomere length in nestling collared flycatchers. BMC Ecol. 12, 17. (doi:10.1186/1472-6785-12-17)
20. Atema E, Mulder E, Dugdale HL, Briga M, Van Noordwijk AJ, Verhulst S. In press. Heritability of telomere length in the zebra finch. J. Ornithol. (doi:10.1007/s10336-015-1212-7)
21. Price T, Schluter D. 1991 On the low heritability of life-history traits. Evolution 45, 853–861. (doi:10.2307/2409693)
22. Postma E. 2014 Four decades of estimating heritabilities in wild vertebrate populations: improved methods, more data, better estimates. In Quantitative genetics in the wild, (eds A Charmantier, D Garant, LEB Kruuk), pp. 16–33. Oxford, UK: Oxford University Press.
23. Weigensberg I, Roff DA. 1996 Natural heritabilities: can they be reliably estimated in the laboratory? Evolution 50, 2149–2157. (doi:10.2307/2410686)
24. Kruuk LEB, Hadfield JD. 2007 How to separate genetic and environmental causes of similarity between relatives. J. Evol. Biol. 20, 1890–1903. (doi:10.1111/j.1420-9101.2007.01377.x)
25. Geiger S, Le Vaillant M, Lebard T, Reichert S, Stier A, Le Maho Y, Criscuolo F. 2012 Catching-up but telomere loss: half-opening the black box of growth and ageing trade-off in wild king penguin chicks. Mol. Ecol. 21, 1500–1510. (doi:10.1111/j.1365-294X.2011.05331.x)
26. Jennings B, Ozanne S, Dorling M, Hales C. 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)
27. Tarry-Adkins J, Martin-Gronert M, Chen J-H, Cripps R, Ozanne S. 2008 Maternal diet influences DNA damage, aortic telomere length, oxidative stress, and antioxidant defense capacity in rats. FASEB J. 22, 2037–2044. (doi:10.1096/fj.07-099523)
28. 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, 17 312–17 315. (doi:10.1073/pnas.0407162101)
29. 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)
30. Haussmann MF, Longenecker AS, Marchetto NM, Juliano SA, Bowden RM. 2012 Embryonic exposure to corticosterone modifies the juvenile stress response, oxidative stress and telomere length. Proc. R. Soc. B 279, 1447–1456. (doi:10.1098/rspb.2011.1913)
31. Nawrot TS, Staessen JA, Gardner JP, Aviv A. 2004 Telomere length and possible link to X chromosome. Lancet 363, 507–510. (doi:10.1016/S0140-6736(04)15535-9)
32. Nordfjäll K, Larefalk A°, Lindgren P, Holmberg D, Roos G. 2005 Telomere length and heredity: indications of paternal inheritance. Proc. Natl Acad. Sci. USA 102, 16 374–16 378. (doi:10.1073/pnas.0501724102)
33. Øigarden T, Borge T, Lifjeld JT. 2010 Extrapair paternity and genetic diversity: the white-throated dipper Cinclus cinclus. J. Avian Biol. 41, 248–257. (doi:10.1111/j.1600-048X.2009.04847.x)
34. Wright S. 1969 Evolution and the genetics of populations: vol. 2. The theory of gene frequencies. Chicago, IL: University of Chicago Press.
35. Morrissey MB, Wilson AJ. 2010 pedantics: an R package for pedigree-based genetic simulation and pedigree manipulation, characterization and viewing. Mol. Ecol. Resour. 10, 711–719. (doi:10.1111/j.1755-0998.2009.02817.x)
36. Arctander P. 1988 Comparative studies of avian DNA by restriction fragment length polymorphism analysis: convenient procedures based on blood samples from live birds. J. Ornithol. 129, 205–216. (doi:10.1007/BF01647289)
37. Bucher T, Wandeler P, Hegelbach J, Keller L. 2009 Development of microsatellite loci in the European dipper, Cinclus cinclus. Conserv. Genet. Resour. 1, 309–312. (doi:10.1007/s12686-009-9071-2)
38. Griffiths R, Double MC, Orr K, Dawson RJ. 1998 A DNA test to sex most birds. Mol. Ecol. 7, 1071–1075. (doi:10.1046/j.1365-294x.1998.00389.x)
39. Hoeck P, Bucher T, Wandeler P, Keller L. 2009 Microsatellite primers for the four Galápagos mockingbird species (Mimus parvulus, Mimus macdonaldi, Mimus melanotis and Mimus trifasciatus). Mol. Ecol. Resour. 9, 1538–1541. (doi:10.1111/j.1755-0998.2009.02704.x)
40. Cawthon RM. 2002 Telomere measurement by quantitative PCR. Nucleic Acids Res. 30, e47. (doi:10.1093/nar/30.10.e47)
41. Criscuolo F, Bize P, Nasir L, Metcalfe NB, Foote CG, Griffiths K, Gault EA, Monaghan P. 2009 Real-time quantitative PCR assay for measurement of avian telomeres. J. Avian Biol. 40, 342–347. (doi:10.1111/j.1600-048X.2008.04623.x)
42. Nussey DH et al. 2014 Measuring telomere length and telomere dynamics in evolutionary biology and ecology. Methods Ecol. Evol. 5, 299–310. (doi:10.1111/2041-210X.12161)
43. Smith S, Turbill C, Penn D. 2011 Chasing telomeres, not red herrings, in evolutionary ecology. Heredity 107, 372–373. (doi:10.1038/hdy.2011.14)
44. Pfaffl MW. 2001 A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 29, e45. (doi:10.1093/nar/29.9.e45)
45. Kruuk LEB. 2004 Estimating genetic parameters in natural populations using the ‘animal model’. Phil. Trans. R. Soc. B 359, 873–890. (doi:10.1098/rstb.2003.1437)
46. Gilmour AR, Gogel B, Cullis B, Thompson R. 2009 ASReml user guide release 3.0. Hemel Hempstead, UK: VSN International Ltd.
47. Meyer K. 2007 WOMBAT: a tool for mixed model analyses in quantitative genetics by restricted maximum likelihood (REML). J. Zhejiang Univ. Sci. B 8, 815–821. (doi:10.1631/jzus.2007.B0815)
48. de Boer I, van Arendonk J. 1992 Prediction of additive and dominance effects in selected or unselected populations with inbreeding. Theor. Appl. Genet. 84, 451–459. (doi:10.1007/BF00229506)
49. Hoeschele I, van Raden P. 1991 Rapid inversion of dominance relationship matrices for noninbred populations by including sire by dam subclass effects. J. Dairy Sci. 74, 557–569. (doi:10.3168/jds.S0022-0302(91)78203-9)
50. Willham R. 1972 The role of maternal effects in animal breeding: III. Biometrical aspects of maternal effects in animals. J. Anim. Sci. 35, 1288–1293.
51. Lynch M, Walsh B. 1998 Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer Associates.
52. Husby A, Schielzeth H, Forstmeier W, Gustafsson L, Qvarnström A. 2012 Sex chromosome linked genetic variance and the evolution of sexual dimorphism of quantitative traits. Evolution 67, 609–619. (doi:10.1111/j.1558-5646.2012.01806.x)
53. Schaeffer LR, Kennedy BW, Gibson JP. 1989 The inverse of the gametic relationship matrix. J. Dairy Sci. 72, 1266–1272. (doi:10.3168/jds.S0022-0302(89)79231-6)
54. Rivero MT, Mosquera A, Goyanes V, Slijepcevic P, Fernandez JL. 2004 Differences in repair profiles of interstitial telomeric sites between normal and DNA double-strand break repair deficient Chinese hamster cells. Exp. Cell Res. 295, 161–172. (doi:10.1016/j.yexcr.2003.12.031)
55. Ballen C, Healey M, Wilson M, Tobler M, Olsson M. 2012 Predictors of telomere content in dragon lizards. Naturwissenschaften 99, 661–664. (doi:10.1007/s00114-012-0941-1)
56. Haussmann MF, Marchetto NM. 2010 Telomeres: linking stress and survival, ecology and evolution. Curr. Zool. 56, 714–727.
57. Young RC, Kitaysky AS, Haussmann MF, Descamps S, Orben RA, Elliott KH, Gaston AJ. 2013 Age, sex, and telomere dynamics in a long-lived seabird with male-biased parental care. PLoS ONE 8, e0074931. (doi:10.1371/journal.pone.0074931)
58. Foote C, Gault E, Nasir L, Monaghan P. 2011 Telomere dynamics in relation to early growth conditions in the wild in the lesser black-backed gull. J. Zool. 283, 203–209. (doi:10.1111/j.1469-7998.2010.00774.x)
59. 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)
60. 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)
61. Andrew T et al. 2006 Mapping genetic loci that determine leukocyte telomere length in a large sample of unselected female sibling pairs. Am. J. Hum. Genet. 78, 480–486. (doi:10.1086/500052)
62. Keller LF, Waller DM. 2002 Inbreeding effects in wild populations. Trends Ecol. Evol. 17, 230–241. (doi:10.1016/S0169-5347(02)02489-8)
63. Manning EL, Crossland J, Dewey MJ, Van Zant G. 2002 Influences of inbreeding and genetics on telomere length in mice. Mammal. Genome 13, 234–238. (doi:10.1007/s003350020027)
64. O’Hare TH, Delany ME. 2009 Genetic variation exists for telomeric array organization within and among the genomes of normal, immortalized, and transformed chicken systems. Chromosome Res. 17, 947–964. (doi:10.1007/s10577-009-9082-6)