Are reproductive and somatic senescence coupled in humans? Late, but not early, reproduction correlated with longevity in historical Sami women

Proceedings of the Royal Society B: Biological Sciences

Volumn 272, Issue 1558, 2005, Pages 29-37

  Helle, Samuli ^a   Lummaa, Virpi ^b   Jokela, Jukka ^c  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF OULU   (Finland)

Author keywords

Evolution; Homo sapiens; Life history; Longevity; Natural selection

Indexed keywords

NATURAL SELECTION;

ARTICLE; CHILDBIRTH; EVOLUTION; FEMALE; FERTILITY; HUMAN; LIFE HISTORY; LIFESPAN; LONGEVITY; MAJOR CLINICAL STUDY; MATERNAL MORTALITY; MORTALITY; NATURAL SELECTION; PRIORITY JOURNAL; REPRODUCTION; SCANDINAVIA; SENESCENCE; SURVIVAL;

HOMO SAPIENS;

EID: 14544303395     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2004.2944     Document Type: Article

References (83)

1. Allison, P. D. 1995 Survival analysis using the SAS system: a practical guide. Cary, NC: SAS Institute Inc.
2. Arantes-Oliveira, N., Apfeld, J., Dillin, A. & Kenyon, C. 2002 Regulation of life-span by germ-line stem cells in Caenorhabditis elegans. Science 295, 502-505.
3. Arnold, S. J. & Wade, M. J. 1984 On the measurement of natural selection and sexual selection: theory. Evolution 38, 709-719.
4. Beeton, M., Yule, G. U. & Pearson, K. 1900 Data for the problem of evolution in man V: on the correlation between duration of life and number of offspring. Proc. R. Soc. 67, 159-179.
5. Bell, A. G. 1918 The duration of life and conditions associated with longevity: a study of the Hyde genealogy. Washington, DC: Genealogical Record Office.
6. Bideau, A. 1986 Fertility and mortality at ages 45 and over. The contribution of research in historical demography. Population 41, 59-72.
7. Carey, J. R., Liedo, P., Harshman, L., Liu, X., Müller, H.-G., Partridge, L. & Wang, J.-L. 2002 Food pulses increase longevity and induce cyclical egg production in Mediterranean fruit flies. Funct. Ecol. 16, 313-325.
8. Collett, D. 2003 Modelling survival data in medical research, 2nd edn. Boca Raton, FL: Chapman & Hall/CRC.
9. Cooper, G. S. & Sandler, D. P. 1998 Age at natural menopause and mortality. Ann. Epidemiol. 8, 229-235.
10. Doblhammer, G. 2000 Reproductive history and mortality later in life: a comparative study of England and Wales and Austria. Popul. Stud. 54, 169-176.
11. Doblhammer, G. & Oeppen, J. 2003 Reproduction and longevity among the British peerage: the effect of frailty and health selection. Proc. R. Soc. B 270, 1541-1547. (doi: 10.1098/rspb.2003.2400)
12. Dorn, H. F. & McDowell, A. J. 1939 The relationship between fertility and longevity. Am. Soc. Rev. 4, 234-246.
13. Dribe, M. 2004 Long-term effects of childbearing on mortality. Popul. Stud. 58, 297-310.
14. Egan, K. M., Giovanucci, E., Titus-Ernstoff, L., Newcomb, P. & Stampfer, M. 1997 Mixed blessing for middle-aged mothers. Nature 389, 922.
15. Ellison, P. 2001 On fertile ground. Cambridge, MA: Harvard University Press.
16. Eogan, M. A., Geary, M. P., O'Connell, M. P. & Keane, D. P. 2003 Effect of fetal sex on labour and delivery: retrospective review. Br. Med. J. 326, 137.
17. Freeman, B. C. 1935 Fertility and longevity in married women dying after the end of reproductive period. Hum. Biol. 7, 392-418.
18. Friedlander, N. J. 1996 The relation of lifetime reproduction to survivorship of women and men: a prospective study. Am. J. Hum. Biol. 8, 771-783.
19. Gargill, S. L., Carey, J. R., Müller, H.-G. & Anderson, G. 2003 Age of ovary determines remaining life expectancy in old ovariectomized mice. Aging Cell 2, 185-190.
20. Gavrilov, L. A. & Gavrilova, N. S. 2001 Epidemiology of human longevity: the search for appropriate methodology. J. Anti-Aging Med. 4, 13-30.
21. Gavrilova, N. S., Gavrilov, L. A., Semyonova, V. G. & Evdokushkina, G. N. 2004 Does exceptional human longevity come with a high cost of infertility? Ann. NY Acad. Sci. 1019, 513-517.
22. Hamilton, W. D. 1966 The moulding of senescence by natural selection. J. Theor. Biol. 12, 12-45.
23. Hatcher, L. 1994 A step-by-step approach to using SAS© for factor analysis and structural equation modeling. Gary, NC: SAS Institute Inc.
24. Hawkes, K., O'Connell, J. F. Jones, N. G., Alvarez, H. & Charnov, E. L. 1998 Grandmothering, menopause, and the evolution of human life histories. Proc. Natl Acad. Sci. USA 95,1336-1339.
25. Helle, S., Käär, P. & Jokela, J. 2002 Human longevity and early reproduction in pre-industrial Sami populations. J. Evol. Biol. 15, 803-807.
26. Helle, S., Lummaa, V. & Jokela, J. 2004a Selection for increased brood size in historical human populations. Evolution 52, 430-436.
27. Helle, S., Lummaa, V. & Jokela, J. 2004b Accelerated immunosenescence in preindustrial twin mothers. Proc. Natl Acad. Sci. USA 101, 12 391-12 396.
28. Hill, K. & Hurtado, A. M. 1996 Ache life history: the ecology and demography of a foraging people. Hawthorne, NY: Aldine de Gruyter.
29. Holman, D. J. & Wood, J. W. 2001 Pregnancy loss and fecundibility in women. In Reproductive ecology and human evolution (ed. P. T. Ellison), pp. 15-38. Hawthorne, NY: Aldine de Gruyter.
30. Hosmer, D. W. & Lemenshow, S. 1994 Applied logistic regression. New York: Wiley.
31. Houston, A. I. & McNamara, J. M. 1999 Models of adaptive behaviour. Cambridge University Press.
32. Hsin, H. & Kenyon, C. 1999 Signals from the reproductive system regulate the lifespan of C. elegans. Nature 399, 362-366.
33. Itkonen T. 1948 The Lapps of Finland, vol. 2. Provoo, Finland: WSOY.
34. Jacobsen, B. K., Knutsen, S. F. & Fraser, G. E. 1999 Age at natural menopause and total mortality and mortality from ischemic heart disease: the Adventist health study. J. Clin. Epidemiol. 52, 303-307.
35. Jacobsen, B. K., Heuch, I. & Kvåle, G. 2003 Age at natural menopause and all-cause mortality: a 37-year follow-up of 19 731 Norwegian women. Am. J. Epidemiol. 157, 923-929.
36. Käär, P., Jokela, J., Helle, T. & Kojola, I. 1996 Direct and correlative phenotypic selection on life-history traits in three pre-industrial human populations. Proc. R. Soc. B 263, 1475-1480.
37. Kaplan, H. K. 1994 Evolutionary and wealth flows theories of fertility: empirical tests and emerging models. Popul. Dev. Rev. 20, 753-791.
38. Kemkes-Grottenthaler, A. 2004 God, faith, and death: the impact of biological and religious correlates on mortality. Hum. Biol. 75, 897-915.
39. Kinsolver, J. G. & Schemske, D. W. 1991 Path analyses of selection. Trends Evol. Ecol. 6, 276-280.
40. Kirk, K. M., Blomberg, S. P., Duffy, D. L., Heath, A. C., Owens, I. P. F. & Martin, N. G. 2001 Natural selection and quantitative genetics of life-history traits in western women: a twin study. Evolution 55, 423-435.
41. Kirkwood, T. B. L. & Austad, S. N. 2000 Why do we age? Nature 408, 233-238.
42. Kirkwood, T. B. L. & Rose, M. R. 1991 Evolution of senescence: late survival sacrificed for reproduction. Phil. Trans. R. Soc. B 332, 15-24.
43. Knodel, J. E. 1988 Demographic behavior in the past. New York: Cambridge University Press.
44. Korpelainen, H. 2000 Fitness, reproduction and longevity among European aristocratic and rural Finnish families in the 1700s and 1800s. Proc. R. Soc. B 267, 1765-1770. (doi: 10.1098/rspb.2000.1208)
45. Korpelainen, H. 2003 Human life histories and the demographic transition: a case study from Finland, 1870-1949. Am. J. Phys. Anthropol. 120, 384-390.
46. Kumle, M. & Lund, E. 2000 Patterns of childbearing and mortality in Norwegian women. A 20-year follow-up of women aged 40-96 in the 1970 Norwegian census. In Sex and longevity: sexuality, gender, reproduction, parenthood (ed. J. M. Robine, T. B. L. Kirkwood & M. Allard), pp. 117-128. Berlin: Springer.
47. Lahdenperä, M., Lummaa, V., Helle, S., Tremblay, M. & Russell, A. F. 2004 Fitness benefits of prolonged post-reproductive lifespan in women. Nature 428, 178-181.
48. Lande, R. & Arnold, S. J. 1983 The measurement of selection on correlated characters. Evolution 37, 1210-1226.
49. Le Bourg, E., Thon, B., Légaré, J., Desjardinds, B. & Charbonneau, H. 1993 Reproductive life of French-Canadians in the 17-18th centuries: a search for a trade-off between early fecundity and longevity. Exp. Gerontol. 28, 217-232.
50. Lee, R. 2003 Rethinking the evolutionary theory of aging: transfers, not births, shape senescence in social species. Proc. Natl Acad. Sci. USA 100, 9637-9642.
51. Lycett, J. E., Dunbar, R. I. M. & Voland, E. 2000 Longevity and the costs of reproduction in a historical human population. Proc. R. Soc. B 267, 31-35. (doi:10.1098/rspb.2000.0982)
52. McCulloch, C. E. & Searle, S. R. 2001 Generalized, linear, and mixed models. New York: Wiley.
53. Manor, O., Eisenbach, Z., Israeli, A. & Friedlander, Y. 2000 Mortality differentials among women: the Israel longitudinal mortality study. Soc. Sci. Med. 51, 1175-1188.
54. Medawar, P. B. 1952 An unsolved problem of biology. London: H. K. Lewis.
55. Menken, J., Duffy, L. & Kühn, R. 2003 Childbearing and women's survival: new evidence from rural Bangladesh. Popul. Dev. Rev. 29, 405-426.
56. Mikkola, M. S. & Clarkson, T. B. 2002 Estrogen replacement therapy, atherosclerosis, and vascular function. Cardiovasc. Res. 53, 605-619.
57. Mitchell, R. J. 1993 Path analysis: pollination. In Design and analysis of ecological experiments (ed. S. M. Scheiner & J. Gurevitch), pp. 211-231. New York: Chapman & Hall.
58. Mostafa, G. & van Ginneken, J. K. 2000 Trends in and determinants of mortality in the elderly population of Matlab, Bangladesh. Soc. Sci. Med. 50, 763-771.
59. Müller, H.-G., Chiou, J., Carey, J. R. & Wang, J. 2002 Fertility and lifespan: late children enhance female longevity. J. Gerontol. A Biol. Sci. Med. Sci. 57, B202-B206.
60. Partridge, L. & Barton, N. H. 1993 Optimality, mutation and the evolution of ageing. Nature 362, 305-311.
61. Partridge, L. & Gems, D. 2002 Mechanism of ageing: public or private? Nature Rev. Genet. 3, 165-175.
62. Perls, T. T. & Fretts, R. C. 2001 The evolution of menopause and human lifespan. Ann. Hum. Biol. 28, 237-245.
63. Perls, T. T., Alpert, L. & Fretts, R. C. 1997 Middle-aged mothers live longer. Nature 339, 133.
64. Petraitis, P. S., Dunham, A. E. & Niewiarowski, P. H. 1996 Inferring multiple causality: the limitations of path analysis. Funct. Ecol. 10, 421-431.
65. Philippe, P. & Yelle, L. 1976 Effect of family size and mother's longevity. Ann. Hum. Biol. 3, 429-431.
66. Powys, A. O. 1905 Data for the problem of evolution in man: on fertility, duration of life and reproductive selection. Biometrika 4, 233-285.
67. Scheiner, S. M., Mitchell, R. J. & Callahan, H. S. 2000 Using path analysis to measure natural selection. J. Evol. Biol. 13, 423-433.
68. Smith, K. R., Mineau, G. P. & Bean, L. L. 2003 Fertility and post-reproductive longevity. Soc. Biol. 49, 55-75.
69. Snowdon, D. A., Kane, R. L. & Beeson, W. L. 1989 Is early natural menopause a biological marker of health and ageing? Am. J. Pub. Hlth 79, 709-714.
70. Tarin, J., Brines, J. & Cano, A. 1998 Long-term effects of delayed parenthood. Hum. Reprod. 13, 2371-2376.
71. Thomas, F., Teriokhin, A. T., Renaud, F., De Meeûs, T. & Guégan, J. F. 2000 Human longevity at the cost of reproductive success: evidence from global data. J. Evol. Biol. 13, 409-414.
72. Tuljapurkar, S. 1990 Delayed reproduction and fitness in variable environments. Proc. Natl Acad. Sci. USA 87, 1139-1143.
73. van der Schouw, Y. T., van der Graff, Y., Steyerberg, E. W., Eijkemans, M. J. C. & Banga, J. D. 1996 Age at menopause and a risk factor for cardiovascular mortality. Lancet 347, 714-718.
74. van Noordwijk, A. J. & de Jong, G. 1986 Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat. 128, 137-142.
75. Voland, E. & Engel, C. 1986 Ist das postmenopausale sterbealter variable einer fitness-maximierender reproduktionssttategie? Anthropol. Anz. 44, 19-34.
76. Voland, E. & Engel, C. 1989 Women's reproduction and longevity in a premodern population Ostfriesland, Germany, 18th century. In The sociobiology of sexual and reproductive strategies (ed. A. E. Rasa, C. Vogel & E. Voland), pp. 194-205. London: Chapman & Hall.
77. Westendorp, R. G. J. & Kirkwood, T. B. L. 1998 Human longevity at the cost of reproductive success. Nature 396, 743-746.
78. Williams, G. C. 1957 Pleiotropy, natural selection and the evolution of senescence. Evolution 11, 398-411.
79. Wolf, D. A. 1994 The eldery and their kin: patterns of availability and access. In Demography of aging (ed. L. G. Martin & S. H. Perston), pp. 146-194. Washington, DC: National Academy Press.
80. Wood, J. M. 1994 Dynamics of human reproduction: biology, biometry, demography. Hawthorne, NY: Aldine de Gruyter.
81. Wrigley, E. A., Davies, R. S., Oeppen, J. E. & Schofield, R. S. 1997 English population history from family reconstitution 1580-1837. Cambridge University Press.
82. Zeger, S. L. & Liang, K. Y. 1986 Longitudinal data analysis for discrete and continuous outcomes. Biometrics 42, 121-130.
83. Zeng, Y. & Vaupel, J. W. 2004 Association of late childbearing with healthy longevity among the oldest-old in China. Popul. Stud. 58, 37-53.