Grandmothers and the evolution of human longevity: A review of findings and future directions

Evolutionary Anthropology

Volumn 22, Issue 6, 2013, Pages 294-302

  Hawkes, Kristen ^a   Coxworth, James E ^a  

^a NONE

Author keywords

Cooperative child rearing; Infant psychology; Life history evolution; Male male competition; Senescence

Indexed keywords

ANIMAL; ANTHROPOLOGY; ARTICLE; COOPERATIVE CHILD REARING; EVOLUTION; FEMALE; HOMINID; HUMAN; INFANT PSYCHOLOGY; LIFE HISTORY EVOLUTION; LONGEVITY; MALE-MALE COMPETITION; MOTHER; POSTMENOPAUSE; SENESCENCE;

COOPERATIVE CHILD REARING; INFANT PSYCHOLOGY; LIFE HISTORY EVOLUTION; MALE-MALE COMPETITION; SENESCENCE;

ANIMALS; ANTHROPOLOGY; BIOLOGICAL EVOLUTION; FEMALE; HOMINIDAE; HUMANS; LONGEVITY; MOTHERS; POSTMENOPAUSE;

EID: 84890646069     PISSN: 10601538     EISSN: 15206505     Source Type: Journal    
DOI: 10.1002/evan.21382     Document Type: Article

References (102)

1. Robson SL, van Schaik CP, Hawkes K. 2006. The derived features of human life history. Hawkes K, Paine RR, editors. The evolution of human life history. Sante Fe, NM: School of Advanced Research Press. p 17-44.
2. Goodall J. 1986. The chimpanzees of Gombe: patterns of behavior. Cambridge, MA: Belknap Press of Harvard University Press.
3. Hill K, Boesch C, Goodall J, et al. 2001. Mortality rates among wild chimpanzees. J Hum Evol 40:437-450.
4. Howell N. 1979. Demography of the Dobe!Kung. New York: Academic Press.
5. Hill K, Hurtado AM. 1996. Aché life history: the ecology and demography of a foraging people. New York: Aldine de Gruyter.
6. Blurton Jones NG, Hawkes K, O'Connell JF. 2002. Antiquity of postreproductive life: are there modern impacts on hunter-gatherer postreproductive life spans? Am J Hum Biol 14:184-205.
7. Levitis DA, Burger O, Lackey LB. 2013. The human post-fertile lifespan in comparative evolutionary context. Evol Anthropol 22:66-79.
8. Hawkes K, O'Connell JF, Blurton Jones NG, et al. 1998. Grandmothering, menopause, and the evolution of human life histories. Proc Natl Acad Sci USA 95:1336-1339.
9. O'Connell JF, Hawkes K, Blurton Jones NG. 1999. Grandmothering and the evolution of Homo erectus. J Hum Evol 36:461-485.
10. Alvarez HP. 2000. Grandmother hypothesis and primate life histories. Am J Phys Anthropol 113:435-450.
11. Hawkes K. 2003. Grandmothers and the evolution of human longevity. Am J Hum Biol 15(3):380-400.
12. Kim PS, Coxworth JE, Hawkes K. 2012. Increased longevity evolves from grandmothering. Proc R Soc London B 279:4880-4884.
13. Kirkwood TBL, Rose MR. 1991. Evolution of senescence: late survival sacrificed for reproduction. Philos Trans R Soc B 332:15-24.
14. Williams GC. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11(4): 398-411.
15. Medawar PB. 1952. An unsolved problem of biology. London: HK Lewis.
16. Graham CE. 1986. Endocrinology of reproductive success. Dukelow WR, Erwin J, editors. Comparative primate biology, vol 3: reproduction and development. New York: Alan R. Liss. p 93-99.
17. Herndon JG, Paredes J, Wilson ME, et al. 2012. Menopause occurs late in life in the captive chimpanzee (Pan troglodytes). Age 34:1145-56.
18. vom Saal FS, Finch CE, Nelson JF. 1994. Natural history and mechanisms of reproductive aging in humans, laboratory rodents, and other selected vertebrates. Knobil E, Neill J, editors. The physiology of reproduction. New York: Raven. p 1213-1314.
19. Gosden R, Telfer E. 1987. Numbers of follicles and oocytes in mammalian ovaries and their allometric relationships. J Zool 211:169-175.
20. Moss CJ. 2001. The demography of an African elephant (Loxodonta africana) population in Amboseli, Kenya. J Zool 255:145-156.
21. Mizroch SA. 1981. Analyses of some biological parameters in the Antarctic fin whale. Report Int Whaling Commission 31:425-434.
22. Jones KP, Walker LC, Anderson D, et al. 2007. Depletion of ovarian follicles with age in chimpanzees: similarities to humans. Biol Reprod 77:247-251.
23. Hawkes K, Smith KR. 2010. Do women stop early? Similarities in fertility decline in humans and chimpanzees. Ann NY Acad Sci 1204:43-53.
24. Caspari R, Lee S-H. 2004. Older age becomes common late in human evolution. Proc Natl Acad Sci USA 101:10895-10900.
25. Hawkes K, O'Connell J. 2005. How old is human longevity? J Hum Evol 49:650-653.
26. Caspari R, Lee S-H. 2005. Are OY ratios invariant? A reply to Hawkes and O'Connell (2005). J Hum Evol 49:654-659.
27. Hawkes K, Blurton Jones NG. 2005. Human age structures, paleodemography, and the grandmother hypothesis. Voland E, Chasiotis A, Schiefenhovel W, editors. Grandmotherhood: the evolutionary significance of the second half of female life. New Brunswick, NJ: Rutgers University Press. p 118-140.
28. Oeppen J, Vaupel JW. 2002. Broken limits to life expectancy. Science 296:1029.
29. Gurven M, Kaplan H. 2007. Longevity among hunter-gatherers: a cross-cultural examination. Popul Dev Rev 33:321-365.
30. Hamilton WD. 1966. The moulding of senescence by natural selection. J Theor Biol 12:12-45.
31. Hamilton WD. 1964. The genetical evolution of social behaviour. II. J Theor Biol 7:17-52.
32. Hawkes K, O'Connell JF, Blurton Jones NG. 1997. Hadza women's time allocation, offspring provisioning, and the evolution of long postmenopausal life spans. Curr Anthropol 38:551-577.
33. Charnov EL. 1993. Life history invariants: some explorations of symmetry in evolutionary ecology. Oxford: Oxford University Press.
34. Hawkes K. 2006. Slow life histories and human evolution. Hawkes K, Paine R, editors. The evolution of human life history. Santa Fe: SAR Press. p 95-126.
35. Charnov EL, Berrigan D. 1993. Why do female primates have such long lifespans and so few babies? Or life in the slow lane. Evol Anthropol 1:191-194.
36. Kim PS, McQueen JS, Coxworth JE, et al n.d. Grandmothering drives the evolution of longevity in a probabilistic model. Submitted.
37. Hawkes K, O'Connell JF, Blurton Jones NG. 1995. Hadza children's foraging: juvenile dependency, social arrangements, and mobility among hunter-gatherers. Curr Anthropol 36:688-700.
38. Lee R. 2008. Sociality, selection, and survival: simulated evolution of mortality with intergenerational transfers and food sharing. Proc Natl Acad Sci USA 105:7124-7128.
39. Lee RD. 2003. Rethinking the evolutionary theory of aging: transfers, not births, shape senescence in social species. Proc Natl Acad Sci USA 100:9637-9642.
40. Kaplan H, Robson A. 2002. The emergence of humans: the coevolution of intelligence and longevity with intergenerational transfers Proc Natl Acad Sci USA 99;10221-10226.
41. Kaplan H, Gurven M, Winking J, et al. 2010. Learning, menopause, and the human adaptive complex. Ann NY Acad Sci 1204:30-42.
42. Kachel AF, Premo L, Hublin J-J. 2011. Grandmothering and natural selection. Proc R Soc London B 278: 384-391.
43. Hawkes K, Kim PS, Kennedy B, et al. 2011. A reappraisal of grandmothering and natural selection. Proc R Soc London B 278:1936-1938.
44. Bentley GR, Mace R. 2012. Substitute parents: biological and social perspective on alloparenting across human societies: New York:Berghahn Books.
45. Lahdenperä M, Lummaa V, Helle S, et al. 2004. Fitness benefits of prolonged post-reproductive lifespan in women. Nature 428:178-181.
46. Sear R, Mace R. 2008. Who keeps children alive? A review of the effects of kin on child survival. Evol Hum Behav 29:1-18.
47. Hill K, Hurtado AM. 2009. Cooperative breeding in South American hunter-gatherers. Proc R Soc B 276:3863-3870.
48. Blurton Jones NG, Hawkes K, O'Connell JF. 2005. Hadza grandmothers as helpers: residence data. Voland E, Chasiotis A, Schiefenhovel W, editors. Grandmotherhood: the evolutionary significance of the second half of female life. Piscataway, NJ: Rutgers University Press. p 160-176.
49. Voland E, Chasiotis A, Schiefenhovel W, editors. 2005. Grandmotherhood: the evolutionary significance of the second half of female life. Piscataway, NJ: Rutgers University Press.
50. Strassmann BL, Garrard WM. 2011. Alternatives to the grandmother hypothesis. Hum Nat 22:201-222.
51. Voland E, Beise J. 2002. Opposite effects of maternal and paternal grandmothers on infant survival in historical Krummhörn. Behav Ecol Sociobiol 52:435-443.
52. Lahdenperä M, Gillespie DO, Lummaa V, et al. 2012. Severe intergenerational reproductive conflict and the evolution of menopause. Ecol Lett 15:1283-1290.
53. Leonetti DL, Nath DC, Hemam NS, et al. 2005. Kinship organization and the impact of grandmothers on reproductive success among the matrilineal Khasi and patrilineal Bengali of Northeast India. Voland E, Chasiotis A, Schiefenhovel W, editors. Grandmotherhood: The evolutionary significance of the second half of female life. New Brunswick: Rutgers University Press. p 194-214.
54. Sear R. 2008. Kin and child survival in rural Malawi. Hum Nat 19:277-293.
55. Hrdy SB. 1999. Mother nature: a history of mothers, infants, and natural selection. New York: Pantheon Books.
56. Fox M, Sear R, Beise J, et al. 2010. Grandma plays favourites: X-chromosome relatedness and sex-specific childhood mortality. Proc R Soc London B 277:567-573.
57. Cant MA, Johnstone RA. 2008. Reproductive conflict and the separation of reproductive generations in humans. Proc Natl Acad Sci USA 105:5332-5336.
58. Koenig A, Borries C. 2012. Hominoid dispersal patterns and human evolution. Evol Anthropol 21:108-112.
59. Wrangham RW. 1987. The significance of African apes for reconstructing human social evolution. Kinzey W, editor. The evolution of human behavior: Primate models. Albany: SUNY Press. p 55-71.
60. Alvarez HP. 2004. Residence groups among hunter-gatherers: a view of claims and evidence. Berman C, Chapais B, editors. Kinship and behavior in primates. Oxford: Oxford University Press. p 420-442.
61. Marlowe FW. 2004. Marital residence among foragers. Curr Anthropol 45:277-284.
62. Hill KR, Walker RS, Božičević M, et al. 2011. Co-residence patterns in hunter-gatherer societies show unique human social structure. Science 331:1286-1289.
63. Labrie F, Martel C, Balser J. 2011. Wide distribution of the serum dehydroepiandrosterone and sex steroid levels in postmenopausal women: role of the ovary? Menopause 18:30-43.
64. Finch CE. 2010. Evolution of the human lifespan and diseases of aging: roles of infection, inflammation, and nutrition. Proc Natl Acad Sci USA 107(suppl 1):1718-1724.
65. Labrie F. 1991. Intracrinology. Moll Cell Endocrinol 78:C113-C118.
66. Lane MA, Ingram DK, Ball SS, et al 1997. Dehydroepiandrosterone sulfate: a biomarker of primate aging slowed by calorie restriction. J Clin Endocr Metab 82:2093-2096.
67. Ingram D, Nakamura E, Smucny D, et al. 2001. Strategy for identifying biomarkers of aging in long-lived species. Exp Gerontol 36:1025-1034.
68. Blevins JK, Coxworth JE, Herndon JG, et al 2013. Brief communication: adrenal androgens and aging: female chimpanzees (Pan troglodytes) compared with women. Am J Phys Anthropol 151:643-648.
69. Bernstein RM, Sterner KN, Wildman DE. 2012. Adrenal androgen production in catarrhine primates and the evolution of adrenarche. Am J Phys Anthropol 147:389-400.
70. Lasley BL, Chen J, Stanczyk FZ, et al. 2012. Androstenediol complements estrogenic bioactivity during the menopausal transition. Menopause19:650.
71. Shay JW, Wright WE. 2007. Hallmarks of telomeres in ageing research. J Pathol 211:114-123.
72. Haussmann MF, Marchetto NM. 2010. Telomeres: linking stress and survival, ecology and evolution. Curr Zool 56:714-727.
73. Tackney J, Cawthon RM, Coxworth JE, et al. 2013. Blood cell telomere lengths and shortening rates of chimpanzee and human females. Submitted.
74. Gomes N, 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.
75. Alberts SC, Altmann J, Brockman DK, et al. 2013. Reproductive aging patterns in primates reveal that humans are distinct. Proc Natl Acad Sci USA 110:13440-13445.
76. Wrangham RW. 2007. The cooking enigma. Ungar P, editor. Evolution of the human diet: the known, the unknown, and the unknowable. Oxford: Oxford University Press. p 308-323.
77. Wrangham RW. 2009. Catching fire: how cooking made us human. New York: Basic Books.
78. Wrangham R, Carmody R. 2010. Human adaptation to the control of fire. Evol Anthropol 19:187-199.
79. Wrangham RW, Jones JH, Laden G, et al. 1999. The raw and the stolen. Curr Anthropol 40:567-594.
80. Organ C, Nunn CL, Machanda Z, et al. 2011. Phylogenetic rate shifts in feeding time during the evolution of Homo. Proc Natl Acad Sci USA 108:14555-14559.
81. Jaeggi AV, Van Schaik CP. 2011. The evolution of food sharing in primates. Behav Ecol Sociobiol 65:2125-2140.
82. Kramer KL, Ellison PT. 2010. Pooled energy budgets: resituating human energy allocation trade-offs. Evol Anthropol 19:136-147.
83. Leonetti DL, Chabot-Hanowell B. 2011. The foundation of kinship. Hum Nat 22:16-40.
84. Hrdy SB. 2009. Mothers and others: the evolutionary origins of mutual understanding. Cambridge, MA: Belknap Press of Harvard University Press.
85. Tomasello M, Carpenter M, Call J, et al. 2005. Understanding and sharing intentions: the origins of cultural cognition. Behav Brain Sci 28:675-91;691-735.
86. Tomasello M. 2008. Origins of human communication. Cambridge, MA: MIT Press.
87. Hrdy SB. 2013. Development + social selection in the emergence of "emotionally modern" humans. Meehan CL, Crittenden AN, editors. Origins and implications of the evolution of childhood. Santa Fe: SAR Press.
88. Hawkes K. 2013. Primate sociality to human cooperation: why us and not them? Hum Nat 25. DOI 10.1007/s12110-013-9184-x.
89. Plooij FX. 1984. The behavioral development of free-living chimpanzee babies and infants. Norwood, NJ: Ablex.
90. Tomonaga M, Tanaka M, Matsuzawa T, et al. 2004. Development of social cognition in infant chimpanzees (Pan troglodytes): face recognition, smiling, gaze, and the lack of triadic interactions. Jpn Psychol Res 46:227-235.
91. Hawkes K. 2006. Life history theory and human evolution: a chronicle of ideas and findings. Hawkes K, Paine R, editors. The evolution of human life history. Santa Fe: SAR Press. p 45-94.
92. Morton RA, Stone JR, Singh RS. 2013. Mate choice and the origin of menopause. PLoS Comput Biol 9:e1003092.
93. Jones D. 1996. An evolutionary perspective on physical attractiveness. Evol Anthropol 5:97-109.
94. Muller MN, Thompson ME, Wrangham RW. 2006. Male chimpanzees prefer mating with old females. Curr Biol 16:2234-2238.
95. Marlowe FW, Berbesque JC. 2012. The human operational sex ratio: effects of marriage, concealed ovulation, and menopause on mate competition. J Hum Evol 63:834-842.
96. Blurton Jones NG, Marlowe FW, Hawkes K, et al. 2000. Paternal investment and hunter-gatherer divorce rates. Cronk L, Chagnon N, Irons W, editors. Adaptation and human behavior: an anthropological perspective. New York: Aldine de Gruyter. p 31-55.
97. Coxworth JE. 2013. First among equals: male-male competition among the Bardi of northwestern Australia and its implications for human evolution. Ph.D. dissertation. Salt Lake City: University of Utah.
98. Chapais B. 2008. Primeval kinship: how pair-bonding gave birth to human society. Cambridge: Harvard University Press.
99. de Waal F. 2011. What is an animal emotion? Ann NY Acad Sci 1224:191-206.
100. de Waal FB. 2012. The antiquity of empathy. Nature 336:874-876.
101. Darwin C. 1871. The descent of man, and selection in relation to sex. New York: D. Appleton.
102. Blurton Jones NG. 2013. Hadza demography and sociobiology. http://www.sscnet.ucla.edu/anthro/faculty/blurton-jones/hadza-part-1.pdf.