Individual variation in rates of senescence: Natal origin effects and disposable soma in a wild bird population

Journal of Animal Ecology

Volumn 79, Issue 6, 2010, Pages 1251-1261

  Bouwhuis, Sandra ^a,b   Charmantier, Anne ^c   Verhulst, Simon ^a   Sheldon, Ben C ^b  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

Author keywords

Ageing; Cost of reproduction; Disposable soma; Great tit; Immigrant status; Life history; Parus major; Senescence; Trade off

Indexed keywords

AGING POPULATION; BIRD; BREEDING POPULATION; FITNESS; IMMIGRANT POPULATION; LIFE HISTORY TRAIT; PLEIOTROPY; PROBABILITY; REPRODUCTIVE COST; REPRODUCTIVE SUCCESS; SENESCENCE; SONGBIRD; SURVIVAL; TRADE-OFF; WILD POPULATION;

AGING; ANIMAL; ARTICLE; ECOSYSTEM; FEMALE; PHYSIOLOGY; REPRODUCTION; SONGBIRD;

AGING; ANIMALS; ECOSYSTEM; FEMALE; REPRODUCTION; SONGBIRDS;

AVES; PARUS MAJOR; VERTEBRATA;

EID: 77956652008     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/j.1365-2656.2010.01730.x     Document Type: Article

References (69)

1. Alonso-Alvarez, C., Bertrand, S., Devevey, G., Prost, J., Faivre, B., Chastel, O. & Sorci, G. (2006) An experimental manipulation of life-history trajectories and resistance to oxidative stress. Evolution, 60, 1913-1924.
2. Bouwhuis, S., Sheldon, B.C., Verhulst, S. & Charmantier, A. (2009) Great tits growing old: selective disappearance and the partitioning of senescence to stages within the breeding cycle. Proceedings of the Royal Society of London Series B-Biological Sciences, 276, 2769-2777.
3. Bouwhuis, S., Charmantier, A., Verhulst, S. & Sheldon, B.C. (2010) Trans-generational effects on ageing in a wild bird population. Journal of Evolutionary Biology, 23, 636-642.
4. Brommer, J.E., Wilson, A.J. & Gustafsson, L. (2007) Exploring the genetics of aging in a wild passerine bird. American Naturalist, 170, 643-650.
5. Browne, W.J., Goldstein, H. & Rasbash, J. (2001) Multiple memberships multiple classification (MMMC) models. Statistical Modelling, 1, 103-124.
6. Browne, W.J., McCleery, R.H., Sheldon, B.C. & Pettifor, R.A. (2007) Using cross-classified multivariate mixed response models with application to life history traits in great tits (Parus major). Statistical Modelling, 7, 217-238.
7. Cam, E., Monnat, J.Y. & Hines, J.E. (2003) Long-term fitness consequences of early conditions in the kittiwake. Journal of Animal Ecology, 72, 411-424.
8. Charmantier, A., Perrins, C., McCleery, R.H. & Sheldon, B.C. (2006a) Age-dependent genetic variance in a life-history trait in the mute swan. Proceedings of the Royal Society B-Biological Sciences, 273, 225-232.
9. Charmantier, A., Perrins, C., McCleery, R.H. & Sheldon, B.C. (2006b) Quantitative genetics of age at reproduction in wild swans: support for antagonistic pleiotropy models of senescence. Proceedings of the National Academy of Sciences of the United States of America, 103, 6587-6592.
10. Clobert, J., Perrins, C.M., McCleery, R.H. & Gosler, A.G. (1988) Survival rate in the great tit Parus major in relation to sex, age, and immigration status. Journal of Animal Ecology, 57, 287-306.
11. Descamps, S., Boutin, S., Berteaux, D. & Gaillard, J.M. (2008a) Age-specific variation in survival, reproductive success and offspring quality in red squirrels: evidence of senescence. Oikos, 117, 1406-1416.
12. Descamps, S., Boutin, S., Berteaux, D., Mcadam, A.G. & Gaillard, J.M. (2008b) Cohort effects in red squirrels: the influence of density, food abundance and temperature on future survival and reproductive success. Journal of Animal Ecology, 77, 305-314.
13. 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. Journal of Animal Ecology, 59, 269-285.
14. Doligez, B. & Pärt, T. (2008) Estimating fitness consequences of dispersal: a road to 'know-where'? Non-random dispersal and the underestimation of dispersers' fitness. Journal of Animal Ecology, 77, 1199-1211.
15. Doligez, B., Clobert, J., Pettifor, R.A., Rowcliffe, M., Gustafsson, L., Perrins, C.M. & McCleery, R.H. (2002) Costs of reproduction: assessing responses to brood size manipulation on life-history and behavioural traits using multi-state capture-recapture models. Journal of Applied Statistics, 29, 407-423.
16. Finkel, T. & Holbrook, N.J. (2000) Oxidants, oxidative stress and the biology of ageing. Nature, 408, 239-247.
17. Garant, D., Kruuk, L.E.B., McCleery, R.H. & Sheldon, B.C. (2004) Evolution in a changing environment: a case study with great tit fledging mass. American Naturalist, 164, E115-E129.
18. Grøtan, V., Saether, B.E., Engen, S., Van Balen, J.H., Perdeck, A.C. & Visser, M.E. (2009) Spatial and temporal variation in the relative contribution of density dependence, climate variation and migration to fluctuations in the size of great tit populations. Journal of Animal Ecology, 78, 447-459.
19. Gustafsson, L. & Sutherland, W.J. (1988) The costs of reproduction in the collared flycatcher Ficedula albicollis. Nature, 335, 813-815.
20. Hamel, S., Gaillard, J.M., Festa-Bianchet, M. & Cote, S.D. (2009) Individual quality, early-life conditions, and reproductive success in contrasted populations of large herbivores. Ecology, 90, 1981-1995.
21. Harman, D. (1956) Aging - a theory based on free-radical and radiation-chemistry. Journal of Gerontology, 11, 298-300.
22. Harvey, P.H., Greenwood, P.J. & Perrins, C.M. (1979) Breeding area fidelity of great tits (Parus major). Journal of Animal Ecology, 48, 305-313.
23. Jones, O.R., Gaillard, J.M., Tuljapurkar, S., Alho, J.S., Armitage, K.B., Becker, P.H., Bize, P., Brommer, J., Charmantier, A., Charpentier, M., Clutton-Brock, T., Dobson, F.S., Festa-Bianchet, M., Gustafsson, L., Jensen, H., Jones, C.G., Lillandt, B.G., McCleery, R., Merila, J., Neuhaus, P., Nicoll, M.A.C., Norris, K., Oli, M.K., Pemberton, J., Pietiainen, H., Ringsby, T.H., Roulin, A., Saether, B.E., Setchell, J.M., Sheldon, B.C., Thompson, P.M., Weimerskirch, H., Wickings, E.J. & Coulson, T. (2008) Senescence rates are determined by ranking on the fast-slow life-history continuum. Ecology Letters, 11, 664-673.
24. Julliard, R., Perret, P. & Blondel, J. (1996) Reproductive strategies of philopatric and immigrant blue tits. Acta Oecologica-International Journal of Ecology, 17, 487-501.
25. Kirkwood, T.B.L. (1977) Evolution of aging. Nature, 270, 301-304.
26. Kirkwood, T.B.L. & Rose, M.R. (1991) Evolution of senescence - late survival sacrificed for reproduction. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 332, 15-24.
27. De Kogel, C.H. (1997) Long-term effects of brood size manipulation on morphological development and sex-specific mortality offspring. Journal of Animal Ecology, 66, 168-178.
28. Koivula, M., Koskela, E., Mappes, T. & Oksanen, T.A. (2003) Cost of reproduction in the wild: manipulation of reproductive effort in the bank vole. Ecology, 84, 398-405.
29. McCleery, R.H. & Clobert, J. (1990) Differences in recruitment of young by immigrant and resident great tits in Wytham Wood. Population Biology of Passerine Birds: An Integrated Approach (eds J. Blondel, A.G. Gosler, J.D. Lebreton & R.H. McCleery), pp. 423-440. Springer-Verlag, Berlin.
30. McCleery, R.H., Clobert, J., Julliard, R. & Perrins, C.M. (1996) Nest predation and delayed cost of reproduction in the great tit. Journal of Animal Ecology, 65, 96-104.
31. McCleery, R.H., Pettifor, R.A., Armbruster, P., Meyer, K., Sheldon, B.C. & Perrins, C.M. (2004) Components of variance underlying fitness in a natural population of the great tit Parus major. American Naturalist, 164, E62-E72.
32. Medawar, P.B. (1952) An Unsolved Problem in Biology. H.K. Lewis & Co. Ltd, London.
33. Metcalfe, N.B. & Monaghan, P. (2003) Growth versus lifespan: perspectives from evolutionary ecology. Experimental Gerontology, 38, 935-940.
34. Monaghan, P., Charmantier, A., Nussey, D.H. & Ricklefs, R.E. (2008) The evolutionary ecology of senescence. Functional Ecology, 22, 371-378.
35. Moyes, K., Coulson, T., Morgan, B.J.T., Donald, A., Morris, S.J. & Clutton-Brock, T.H. (2006) Cumulative reproduction and survival costs in female red deer. Oikos, 115, 241-252.
36. Nakagawa, S. & Freckleton, R.P. (2008) Missing inaction: the dangers of ignoring missing data. Trends in Ecology & Evolution, 23, 592-596.
37. Newton, I. & Marquiss, M. (1983) Dispersal of sparrowhawks between birthplace and breeding place. Journal of Animal Ecology, 52, 463-477.
38. Nussey, D.H., Kruuk, L.E.B., Donald, A., Fowlie, M. & Clutton-Brock, T.H. (2006) The rate of senescence in maternal performance increases with early-life fecundity in red deer. Ecology Letters, 9, 1342-1350.
39. Nussey, D.H., Kruuk, L.E.B., Morris, A. & Clutton-Brock, T.H. (2007) Environmental conditions in early life influence ageing rates in a wild population of red deer. Current Biology, 17, R1000-R1001.
40. Nussey, D.H., Coulson, T., Festa-Bianchet, M. & Gaillard, J.M. (2008a) Measuring senescence in wild animal populations: towards a longitudinal approach. Functional Ecology, 22, 393-406.
41. Nussey, D.H., Wilson, A.J., Morris, A., Pemberton, J., Clutton-Brock, T. & Kruuk, L.E.B. (2008b) Testing for genetic trade-offs between early- and late-life reproduction in a wild red deer population. Proceedings of the Royal Society B-Biological Sciences, 275, 745-750.
42. Oksanen, T.A., Koivula, M., Koskela, E. & Mappes, T. (2007) The cost of reproduction induced by body size at birth and breeding density. Evolution, 61, 2822-2831.
43. Orell, M. & Belda, E.J. (2002) Delayed cost of reproduction and senescence in the willow tit Parus montanus. Journal of Animal Ecology, 71, 55-64.
44. Pärt, T. (1990) Natal dispersal in the collared flycatcher - possible causes and reproductive consequences. Ornis Scandinavica, 21, 83-88.
45. Perrins, C.M. (1979) British Tits. Collins, London.
46. Pettifor, R.A., Perrins, C.M. & McCleery, R.H. (2001) The individual optimization of fitness: variation in reproductive output, including clutch size, mean nestling mass and offspring recruitment, in manipulated broods of great tits Parus major. Journal of Animal Ecology, 70, 62-79.
47. Van De Pol, M. & Verhulst, S. (2006) Age-dependent traits: a new statistical model to separate within- and between-individual effects. American Naturalist, 167, 766-773.
48. Van De Pol, M., Bruinzeel, L.W., Heg, D., Van der Jeugd, H.P. & Verhulst, S. (2006) A silver spoon for a golden future: long-term effects of natal origin on fitness prospects of oystercatchers (Haematopus ostralegus). Journal of Animal Ecology, 75, 616-626.
49. Rasbash, J., Steele, F., Browne, W. & Prosser, B. (2005) A User's Guide to MLwiN - Version 2.0. Centre for Multilevel Modelling, University of Bristol, London.
50. Reed, T.E., Kruuk, L.E.B., Wanless, S., Frederiksen, M., Cunningham, E.J.A. & Harris, M.P. (2008) Reproductive senescence in a long-lived seabird: rates of decline in late-life performance are associated with varying costs of early reproduction. American Naturalist, 171, E89-E101.
51. Reid, J.M., Bignal, E.M., Bignal, S., McCracken, D.I. & Monaghan, P. (2003) Environmental variability, life-history covariation and cohort effects in the red-billed chough Pyrrhocorax pyrrhocorax. Journal of Animal Ecology, 72, 36-46.
52. Reznick, D.N., Bryant, M.J., Roff, D., Ghalambor, C.K. & Ghalambor, D.E. (2004) Effect of extrinsic mortality on the evolution of senescence in guppies. Nature, 431, 1095-1099.
53. Riddington, R. & Gosler, A.G. (1995) Differences in reproductive success and parental qualities between habitats in the great tit Parus major. Ibis, 137, 371-378.
54. Roulin, A. (2002) Short- and long-term fitness correlates of rearing conditions in barn owls Tyto alba. Ardea, 90, 259-267.
55. Stearns, S.C. (1992) The Evolution of Life Histories. Oxford University Press, Oxford.
56. Svensson, L. (1994) Identification Guide to European Passerines. Fingraf AB, Sweden.
57. Szulkin, M. & Sheldon, B.C. (2007) The environmental dependence of inbreeding depression in a wild bird population. PLoS ONE, 2, e1027.
58. Tinbergen, J.M. & Boerlijst, M.C. (1990) Nestling weight and survival in individual great tits (Parus major). Journal of Animal Ecology, 59, 1113-1127.
59. Verhulst, S. (1998) Multiple breeding in the great tit, II. The costs of rearing a second clutch. Functional Ecology, 12, 132-140.
60. Verhulst, S., Holveck, M.J. & Riebel, K. (2006) Long-term effects of manipulated natal brood size on metabolic rate in zebra finches. Biology Letters, 2, 478-480.
61. Verhulst, S., Perrins, C.M. & Riddington, R. (1997) Natal dispersal of great tits in a patchy environment. Ecology, 78, 864-872.
62. Verhulst, S. & Van Eck, H.M. (1996) Gene flow and immigration rate in an island population of great tits. Journal of Evolutionary Biology, 9, 771-782.
63. Visser, M.E. & Verboven, N. (1999) Long-term fitness effects of fledging date in great tits. Oikos, 85, 445-450.
64. Wilkin, T.A. & Sheldon, B.C. (2009) Sex differences in the persistence of natal environmental effects on life-histories. Current Biology, 19, 1998-2002.
65. Wilkin, T.A., Garant, D., Gosler, A.G. & Sheldon, B.C. (2006) Density effects on life-history traits in a wild population of the great tit Parus major: analyses of long-term data with GIS techniques. Journal of Animal Ecology, 75, 604-615.
66. Williams, G.C. (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution, 11, 398-411.
67. Williams, G.C. (1966) Natural selection costs of reproduction and a refinement of Lack's principle. American Naturalist, 100, 687-690.
68. Wilson, A.J., Charmantier, A. & Hadfield, J.D. (2008) Evolutionary genetics of ageing in the wild: empirical patterns and future perspectives. Functional Ecology, 22, 431-442.
69. Wilson, A.J., Nussey, D.H., Pemberton, J.M., Pilkington, J.G., Morris, A., Pelletier, F., Clutton-Brock, T.H. & Kruuk, L.E.B. (2007) Evidence for a genetic basis of aging in two wild vertebrate populations. Current Biology, 17, 2136-2142.