Disentangling the Evolution of Early and Late Life History Traits in Humans

Evolutionary Biology

Volumn 39, Issue 4, 2012, Pages 638-649

  Kachel, A Friederike ^a   Premo, L S ^a,b  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Allocare; Grandmothering; Human evolution; Longevity; Menopause; Weaning

Indexed keywords

HOMINOIDEA; PRIMATES;

EID: 84870783498     PISSN: 00713260     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11692-012-9169-4     Document Type: Review

References (121)

1. Allman, J., Rosin, A., Kumar, R., & Hasenstaub, A. (1998). Parenting and survival in anthropoid primates: Caretakers live longer. Proceedings of the National Academy of Sciences of the United State of America, 95(12), 6866-6869.
2. Alvarez, H. P. (2000). Grandmother hypothesis and primate life histories. American Journal of Physical Anthropology, 113(3), 435-450.
3. Amundsen, D. W., & Diers, C. J. (1970). Age of menopause in classical Greece and Rome. Human Biology, 42(1), 79-86.
4. Amundsen, D. W., & Diers, C. J. (1973). Age of menopause in medieval Europe. Human Biology, 45(4), 605-612.
5. Andersen, A.-M. N., Wohlfahrt, J., Christens, P., Olsen, J., & Melbye, M. (2000). Maternal age and fetal loss: Population based register linkage study. BMJ, 320(7251), 1708-1712.
6. Austad, S. N. (1994). Menopause: An evolutionary perspective. Experimental Gerontology, 29(3-4), 255-263.
7. Beise, J., & Voland, E. (2002). A multilevel event history analysis of the effects of grandmothers on child mortality in a historical German population (Krummhörn, Ostfriesland, 1720-1874). Demographic Research, 7(13), 469-498.
8. Bellino, F. L., & Wise, P. M. (2003). Nonhuman primate models of menopause workshop. Biology of Reproduction, 68(1), 10-18.
9. Blurton Jones, N. G., Hawkes, K., & O'Connell, J. F. (2002). Antiquity of postreproductive life: Are there modern impacts on hunter-gatherer postreproductive life spans? American Journal of Human Biology, 14(2), 184-205.
10. Bogin, B. (1990). The evolution of human childhood. BioScience, 40(1), 16-25.
11. Bogin, B. (1997). Evolutionary hypotheses for human childhood. American Journal of Physical Anthropology, 104(S25), 63-89.
12. Bogin, B. (2006). Modern human life history-the evolution of human childhood and fertility. In K. Hawkes & R. R. Paine (Eds.), The evolution of human life history (pp. 197-230). Santa Fe: School of American Research Press.
13. Bogin, B. (2009). Childhood, adolescence, and longevity: A multilevel model of the evolution of reserve capacity in human life history. American Journal of Human Biology, 21(4), 567-577.
14. Bogin, B., & Smith, B. H. (1996). Evolution of the human life cycle. American Journal of Human Biology, 8(6), 703-716.
15. Brass, W. (1975). Methods for estimating fertility and mortality from limited and defective data. Chapel Hill, N. C.: International Program of Laboratories for Population Statistics.
16. Bribiescas, R. G. (2006). Reproductive physiology and human evolution. International Congress Series, 1296, 127-137.
17. Broadfield, D. C. (2010). Grandparental investment and the epiphenomenon of menopause in recent human history. The Behavioral and Brain Sciences, 33(1), 19-20.
18. Brody, J. A., Grant, M. D., Frateschi, L. J., Miller, S. C., & Zhang, H. W. (2000). Reproductive longevity and increased life expectancy. Age and Ageing, 29(1), 75-78.
19. Cant, M. A., & Johnstone, R. A. (2008). Reproductive conflict and the separation of reproductive generations in humans. Proceedings of the National Academy of Sciences of the United State of America, 105(14), 5332-5336.
20. Caro, T. M., Sellen, D. W., Parish, A., Frank, R., Brown, D. M., Voland, E., et al. (1995). Termination of reproduction in nonhuman and human female primates. International Journal of Primatology, 16(3), 205-220.
21. Caspari, R., & Lee, S.-H. (2004). Older age becomes common late in human evolution. Proceedings of the National Academy of Sciences of the United State of America, 101(30), 10895-10900.
22. Charnov, E. L. (1993). Life history invariants: Some explorations of symmetry in evolutionary ecology (p. 167). New York: Oxford University Press.
23. Chrastil, E. R., Getz, W. M., Euler, H. A., & Starks, P. T. (2006). Paternity uncertainty overrides sex chromosome selection for preferential grandparenting. Human Behavior and Evolution, 27(3), 206-223.
24. Christensen, K., & Vaupel, J. W. (1996). Determinants of longevity: Genetic, environmental and medical factors. Journal of Internal Medicine, 240(6), 333-341.
25. Cleland, J. G., & Sathar, Z. A. (1984). The effect of birth spacing on childhood mortality in Pakistan. Population Studies - Journal Demography, 38(3), 401-418.
26. Cohen, A. A. (2004). Female post-reproductive lifespan: A general mammalian trait. Biological Reviews, 79(4), 733-750.
27. de Bruin, J. P., Bovenhuis, H., van Noord, P. A. H., Pearson, P. L., van Arendonk, J. A. M., te Velde, E. R., et al. (2001). The role of genetic factors in age at natural menopause. Human Reproduction, 16(9), 2014-2018.
28. Derry, P. S. (2002). What do we mean by "The biology of menopause"? Sex Roles, 46(1), 13-23.
29. Ellison, P. T. (1994). Advances in human reproductive ecology. Annual Review of Anthropology, 23(1), 255-275.
30. Ellison, P. T. (2010). Life historical perspectives on human reproductive aging. Annals of the New York Academy of Sciences, 1204(1), 11-20.
31. Emery Thompson, M., Jones, J. H., Pusey, A. E., Brewer-Marsden, S., Goodall, J., Marsden, D., et al. (2007). Aging and fertility patterns in wild chimpanzees provide insights into the evolution of menopause. Current Biology, 17(24), 2150-2156.
32. Euler, H. A., & Michalski, R. L. (2007). Grandparental and extended kin relationships. In C. A. Salmon & T. K. Shackelford (Eds.), Family relationships: An evolutionary perspective (pp. 230-255). New York: Oxford University Press.
33. Finch, C. E., & Holmes, D. J. (2010). Ovarian aging in developmental and evolutionary contexts. Annals of the New York Academy of Sciences, 1204(1), 82-94.
34. Finch, C. E., & Tanzi, R. E. (1997). Genetics of aging. Science, 278(5337), 407-411.
35. Fox, M., Sear, R., Beise, J., Ragsdale, G., Voland, E., & Knapp, L. A. (2010). Grandma plays favourites: X-chromosome relatedness and sex-specific childhood mortality. Proceedings of the Royal Society of London. Series B: Biological Sciences, 277, 567-573.
36. Gage, T. B. (2001). Age-specific fecundity of mammalian populations: A test of three mathematical models. Zoo Biology, 20(6), 487-499.
37. Galdikas, B. M. F., & Wood, J. W. (1990). Birth spacing patterns in humans and apes. American Journal of Physical Anthropology, 83(2), 185-191.
38. Gibson, M. A., & Mace, R. (2005). Helpful grandmothers in rural Ethiopia: A study of the effect of kin on child survival and growth. Human Behavior and Evolution, 26(6), 469-482.
39. Gosden, R. G. (1985). Biology of menopause: The causes and consequences of ovarian ageing. London: Academic Press, Inc.
40. Gosden, R. G. (1987). Follicular status at the menopause. Human Reproduction, 2(7), 617-621.
41. Gosden, R. G., & Telfer, E. (1987). Numbers of follicles and oocytes in mammalian ovaries and their allometric relationships. Journal of Zoology (Lond), 211, 169-175.
42. Gould, K. G., Flint, M., & Graham, C. E. (1981). Chimpanzee reproductive senescence: A possible model for evolution of the menopause. Maturitas, 3(2), 157-166.
43. Graham, C. E. (1979). Reproductive function in aged female chimpanzees. American Journal of Physical Anthropology, 50(3), 291-300.
44. Gurven, M., & Kaplan, H. (2007). Longevity among hunter-gatherers: A cross-cultural examination. Population and Development Review, 33(2), 321-365.
45. Hames, R. (1997). Comment on "Hadza women's time allocation, offspring provisioning, and the evolution of long postmenopausal life spans". Current Anthropology, 38(4), 567-568.
46. Hamilton, W. D. (1966). Moulding of senescence by natural selection. Journal of Theoretical Biology, 12(1), 12-45.
47. Hawkes, K. (2003). Grandmothers and the evolution of human longevity. American Journal of Human Biology, 15(3), 380-400.
48. Hawkes, K., & Bliege, B. R. (2002). Showing off, handicap signaling, and the evolution of men's work. Evolutionary Anthropology, 11(2), 58-67.
49. Hawkes, K., & O'Connell, J. F. (2005). How old is human longevity? Journal of Human Evolution, 49(5), 650-653.
50. Hawkes, K., O'Connell, J. F., & Blurton Jones, N. G. (1989). Hardworking Hadza Grandmothers. In V. Standen & R. A. Foley (Eds.), Comparative socioecology: The behavioural ecology of humans and other mammals (pp. 341-366). Oxford: Blackwell.
51. Hawkes, K., O'Connell, J. F., & Blurton Jones, N. G. (1997). Hadza women's time allocation, offspring provisioning, and the evolution of long postmenopausal life spans. Current Anthropology, 38(4), 551-577.
52. Hawkes, K., O'Connell, J. F., Blurton Jones, N. G., Alvarez, H., & Charnov, E. L. (1998). Grandmothering, menopause, and the evolution of human life histories. Proceedings of the National Academy of Sciences of the United State of America, 95(3), 1336-1339.
53. Hawkes, K., & Smith, K. R. (2010). Do women stop early? Similarities in fertility decline in humans and chimpanzees. Annals of the New York Academy of Sciences, 1204(1), 43-53.
54. Hawkes, K., Smith, K. R., & Robson, S. L. (2009). Mortality and fertility rates in humans and chimpanzees: How within-species variation complicates cross-species comparisons. American Journal of Human Biology, 21(4), 578-586.
55. Hill, K., Boesch, C., Goodall, J., Pusey, A., Williams, J., & Wrangham, R. (2001). Mortality rates among wild chimpanzees. Journal of Human Evolution, 40(5), 437-450.
56. Hill, K., & Hurtado, A. (1991). The evolution of premature reproductive senescence and menopause in human females: An evaluation of the "grandmother hypothesis". Human Nature, 2(4), 313-350.
57. Hill, K., & Hurtado, A. M. (2009). Cooperative breeding in South American hunter-gatherers. Proceedings of the Royal Society of London. Series B: Biological Sciences, 276(1674), 3863-3870.
58. Hill, K. R., Walker, R. S., Božičević, M., Eder, J., Headland, T., Hewlett, B., et al. (2011). Co-residence patterns in hunter-gatherer societies show unique human social structure. Science, 331(6022), 1286-1289.
59. Hobcraft, J., McDonald, J. W., & Rutstein, S. (1983). Child-spacing effects on infant and early child mortality. Population Index, 49(4), 585-618.
60. Hobcraft, J. N., McDonald, J. W., & Rutstein, S. O. (1985). Demographic determinants of infant and early child mortality: A comparative analysis. Population Studies - Journal Demography, 39(3), 363-385.
61. Hrdy, S. B. (2007). Evolutionary context of human development: The cooperative breeding model. In C. A. Salmon & T. K. Shackelford (Eds.), Family relationships: An evolutionary perspective (pp. 39-68). New York: Oxford University Press.
62. Hrdy, S. B. (2009). Mothers and others: The evolutionary origins of mutual understanding (p. 422). Cambridge, Mass.: Belknap Press of Harvard University Press.
63. Humphrey, L. T. (2010). Weaning behaviour in human evolution. Seminars in Cell & Developmental Biology, 21(4), 453-461.
64. Jamison, C. S., Cornell, L. L., Jamison, P. L., & Nakazato, H. (2002). Are all grandmothers equal? A review and a preliminary test of the 'grandmother hypothesis' in Tokugawa Japan. American Journal of Physical Anthropology, 119(1), 67-76.
65. Johnstone, R. A., & Cant, M. A. (2010). The evolution of menopause in cetaceans and humans: The role of demography. Proceedings of the Royal Society of London. Series B: Biological Sciences, 277(1701), 3765-3771.
66. Jones, K. P., Walker, L. C., Anderson, D., Lacreuse, A., Robson, S. L., & Hawkes, K. (2007). Depletion of ovarian follicles with age in chimpanzees: Similarities to humans. Biology of Reproduction, 77(2), 247-251.
67. Judge, D. S., & Carey, J. R. (2000). Postreproductive life predicted by primate patterns. Journals of Gerontology Series a-Biological Sciences and Medical Sciences, 55(4), B201-B209.
68. Kachel, A. F., Premo, L. S., & Hublin, J.-J. (2011a). Grandmothering and natural selection. Proceedings of the Royal Society of London. Series B: Biological Sciences, 278(1704), 384-391.
69. Kachel, A. F., Premo, L. S., & Hublin, J.-J. (2011b). Grandmothering and natural selection revisited. Proceedings of the Royal Society of London. Series B: Biological Sciences, 278(1714), 1939-1941.
70. Kachel, A. F., Premo, L. S., & Hublin, J.-J. (2011c). Modeling the effects of weaning age on length of female reproductive period: Implications for the evolution of human life history. American Journal of Human Biology, 23(4), 479-487.
71. Kaplan, H., Hill, K., Lancaster, J., & Hurtado, A. M. (2000). A theory of human life history evolution: Diet, intelligence, and longevity. Evolutionary Anthropology, 9(4), 156-185.
72. Kaplan, H., Lancaster, J., & Robson, A. (2003). Embodied capital and the evolutionary economics of the human life span. Population and Development Review, 29, 152-182.
73. Kaplan, H. S., & Robson, A. J. (2002). The emergence of humans: The coevolution of intelligence and longevity with intergenerational transfers. Proceedings of the National Academy of Sciences of the United State of America, 99(15), 10221-10226.
74. Kasuya, T., & Marsh, H. (1984). Life history and reproductive biology of the short-finned pilot whale, Globicephala macrorhynchus, of the Pacific coast of Japan. Reports of the International Whaling Commission(Special Issue 6): 259-310.
75. Kirkwood, T. B. L. (1987). Immortality of the germ-line versus disposability of the soma. In A. D. Woodhead & K. H. Thompson (Eds.), Evolution of longevity in animals: A comparative approach (pp. 209-218). New York: Plenum Publishing Corporation.
76. Kirkwood, T. B. L., & Shanley, D. P. (2010). The connections between general and reproductive senescence and the evolutionary basis of menopause. Annals of the New York Academy of Sciences, 1204(1), 21-29.
77. Kramer, K. L. (2005). Children's help and the pace of reproduction: Cooperative breeding in humans. Evolutionary Anthropology, 14(6), 224-237.
78. Lahdenperä, M., Lummaa, V., Helle, S., Tremblay, M., & Russell, A. F. (2004). Fitness benefits of prolonged post-reproductive lifespan in women. Nature, 428(6979), 178-181.
79. Larke, A., & Crews, D. E. (2006). Parental investment, late reproduction, and increased reserve capacity are associated with longevity in humans. Journal of Physiological Anthropology, 25(1), 119-131.
80. Lee, P. C. (1996). The meanings of weaning: Growth, lactation, and life history. Evolutionary Anthropology, 5(3), 87-98.
81. Lock, M. (1994). Menopause in cultural-context. Experimental Gerontology, 29(3-4), 307-317.
82. Mace, R., & Sear, R. (2005). Are humans cooperative breeders? In E. Voland, A. Chasiotis, & W. Schiefenhövel (Eds.), Grandmotherhood: The evolutionary significance of the second half of female life (pp. 143-159). New Jersey: Rutgers University Press.
83. Manda, S. O. M. (1999). Birth intervals, breastfeeding and determinants of childhood mortality in Malawi. Social Science and Medicine, 48(3), 301-312.
84. Melby, M. K., Lock, M., & Kaufert, P. (2005). Culture and symptom reporting at menopause. Human Reproduction Update, 11(5), 495-512.
85. Obermeyer, C. M. (2000). Menopause across cultures: A review of the evidence. Menopause, 7(3), 184-192.
86. Obermeyer, C. M., Reher, D., & Saliba, M. (2007). Symptoms, menopause status, and country differences: A comparative analysis from DAMES. Menopause, 14(4), 788-797.
87. O'Connell, J. F., Hawkes, K., & Jones, N. G. B. (1999). Grandmothering and the evolution of Homo erectus. Journal of Human Evolution, 36(5), 461-485.
88. Oeppen, J., & Vaupel, J. W. (2002). Broken limits to life expectancy. Science, 296(5570), 1029-1031.
89. Palloni, A., & Millman, S. (1986). Effects of inter-birth intervals and breastfeeding on infant and early childhood mortality. Population Studies - Journal Demography, 40(2), 215-236.
90. Pavard, S., Metcalf, C. J. E., & Heyer, E. (2008). Senescence of reproduction may explain adaptive menopause in humans: A test of the "mother" hypothesis. American Journal of Physical Anthropology, 136(2), 194-203.
91. Pavelka, M. S. M., & Fedigan, L. M. (1991). Menopause: A comparative life history perspective. Yearbook of Physical Anthropology, 34, 13-38.
92. Peccei, J. S. (1999). First estimates of heritability in the age of menopause. Current Anthropology, 40(4), 553-558.
93. Peccei, J. S. (2001a). Menopause: Adaptation or epiphenomenon? Evolutionary Anthropology, 10(2), 43-57.
94. Peccei, J. S. (2001b). A critique of the grandmother hypotheses: Old and new. American Journal of Human Biology, 13(4), 434-452.
95. Ragsdale, G. (2004). Grandmothering in Cambridgeshire, 1770-1861. Human Nature, 15(3), 301-317.
96. Richardson, S. J., Senikas, V., & Nelson, J. F. (1987). Follicular depletion during the menopausal transition: Evidence for accelerated loss and ultimate exhaustion. Journal of Clinical Endocrinology and Metabolism, 65(6), 1231-1237.
97. Robson, S. L., van Schaik, C. P., & Hawkes, K. (2006). The derived features of human life history. In K. Hawkes & R. R. Paine (Eds.), The evolution of human life history (pp. 17-44). Santa Fe: School of American Research Press.
98. Robson, S. L., & Wood, B. (2008). Hominin life history: Reconstruction and evolution. Journal of Anatomy, 212(4), 394-425.
99. Roff, D. A. (2002). Life history evolution (p. 527). Sunderland, Mass: Sinauer Associates, Inc.
100. Rogers, A. R. (1993). Why menopause? Evolutionary Ecology, 7(4), 406-420.
101. Schölmerich, A., Leyendecker, B., Citlak, B., Miller, A., & Harwood, R. (2005). Variability of Grandmother's roles. In E. Voland, A. Chasiotis, & W. Schiefenhövel (Eds.), Grandmotherhood: The evolutionary significance of the second half of female life (pp. 277-292). New Brunswick, New Jersey, London: Rutgers University Press.
102. Sear, R., & Mace, R. (2008). Who keeps children alive? A review of the effects of kin on child survival. Human Behavior and Evolution, 29(1), 1-18.
103. Sear, R., Mace, R., & McGregor, I. A. (2000). Maternal grandmothers improve nutritional status and survival of children in rural Gambia. Proceedings of the Royal Society of London. Series B: Biological Sciences, 267(1453), 1641-1647.
104. Sear, R., Mace, R., & McGregor, I. A. (2003). The effects of kin on female fertility in rural Gambia. Human Behavior and Evolution, 24, 25-42.
105. Sellen, D. W. (2001). Weaning, complementary feeding, and maternal decision making in a rural East African pastoral population. Journal of Human Lactation, 17(3), 233-244.
106. Sellen, D. W. (2007). Evolution of infant and young child feeding: Implications for contemporary public health. Annual Review of Nutrition, 27(1), 123-148.
107. Sellen, D. W. (2009). Evolution of human lactation and complementary feeding: Implications for understanding contemporary cross-cultural variation. In G. Goldberg, A. Prentice, A. Prentice, S. Filteau, & K. Simondon (Eds.), Breast-feeding: Early influences on later health (pp. 253-282). Netherlands, Dordrecht: Springer.
108. Shanley, D. P., & Kirkwood, T. B. L. (2001). Evolution of the human menopause. BioEssays, 23(3), 282-287.
109. Shanley, D. P., Sear, R., Mace, R., & Kirkwood, T. B. L. (2007). Testing evolutionary theories of menopause. Proceedings of the Royal Society of London. Series B: Biological Sciences, 274, 2943-2949.
110. Snieder, H., MacGregor, A. J., & Spector, T. D. (1998). Genes control the cessation of a woman's reproductive life: A twin study of hysterectomy and age at menopause. Journal of Clinical Endocrinology and Metabolism, 83(6), 1875-1880.
111. Stanford, J. L., Hartge, P., Brinton, L. A., Hoover, R. N., & Brookmeyer, R. (1987). Factors influencing the age at natural menopause. Journal of Chronic Diseases, 40(11), 995-1002.
112. Stearns, S. C. (1989). Trade-offs in life-history evolution. Functional Ecology, 3(3), 259-268.
113. Stearns, S. C. (1992). The evolution of life histories (p. 249). New York: Oxford University Press.
114. Te Velde, E. R., & Pearson, P. L. (2002). The variability of female reproductive ageing. Human Reproduction Update, 8(2), 141-154.
115. Thapa, S., Short, R. V., & Potts, M. (1988). Breast feeding, birth spacing and their effects on child survival. Nature, 335(6192), 679-682.
116. van Bodegom, D., Rozing, M., May, L., Kuningas, M., Thomese, F., Meij, H., et al. (2010). When grandmothers matter. Gerontology, 56(2), 214-216.
117. Vaupel, J. W. (1986). How change in age-specific mortality affects life expectancy. Population Studies - Journal Demography, 40(1), 147-157.
118. Videan, E. N., Fritz, J., Heward, C. B., & Murphy, J. (2006). The effects of aging on hormone and reproductive cycles in female chimpanzees (Pan troglodytes). Comparative Medicine, 56(4), 291-299.
119. Walker, M. L., & Herndon, J. G. (2008). Menopause in nonhuman primates? Biology of Reproduction, 79, 398-406.
120. Williams, G. C. (1957). Pleiotropy, natural selection, and the evolution of senescence. Evolution, 11(4), 398-411.
121. Wood, B. M. (2006). Prestige or provisioning? A test of foraging goals among the Hadza. Current Anthropology, 47(2), 383-387.