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A Comparison of men’s Life History, Aging, and Testosterone Levels among Datoga Pastoralists, Hadza Foragers, and Qom Transitional Foragers

  • Louis Calistro AlvaradoEmail author
  • Claudia R. Valeggia
  • Peter T. Ellison
  • Caitlin L. Lewarch
  • Martin N. Muller
Original Article

Abstract

Objectives

Relative to industrialized populations, men from subsistence groups exhibit lower testosterone values and more modest declines with age. Limited energy availability has been hypothesized to suppress testosterone production, particularly during young adulthood when testosterone levels are highest, resulting in a flatter trajectory of age-decline. Energetic constraint, however, is not unique to the evolutionary ecology of humans, and yet significant age-related testosterone decline is observed in numerous species of wild primates. Conversely, human life history is distinguished by extensive bi-parental care and male provisioning. Because fathers show decreased testosterone with parenting effort, we argue that within more naturalistic and evolutionarily relevant ecologies, natural fertility and earlier reproduction suppresses testosterone in emerging adulthood such that a lower relative baseline dictates less age-decline across the remaining lifespan.

Methods

We examine men’s testosterone levels as contrasting functions of energetic status and paternal involvement across three traditional populations with substantial variability in men’s nutritional condition and parental investment. Anthropometric and demographic data along with saliva samples were collected from 70 Datoga, 29 Hadza, and 43 Qom men, ages 20–72 years.

Results

Population variation in salivary testosterone was greatest at younger ages and patterned so paternal involvement associated with lower morning and evening testosterone, along with diminished age-decline in both measures. Men’s energetic status as indicated by body mass index was not associated with testosterone values or age-related decline.

Conclusions

Within socioecological contexts of smaller scale society, these data suggest that blunted age-decline in men’s testosterone levels is primarily due to population variation in parental investment rather than energetic constraint.

Keywords

Men’s life course Aging Testosterone Smaller scale societies 

Notes

Acknowledgements

We thank Susan Lipson for providing laboratory assistance with hormone assays. We are also thankful to the Datoga, Hadza, and Qom men who participated in this study.

Compliance with Ethical Standards

Conflict of Interest

The authors declare no competing interests.

Supplementary material

40750_2019_116_MOESM1_ESM.docx (126 kb)
ESM 1 (DOCX 126 kb)

References

  1. Alfonso-Durruty, M. P., & Valeggia, C. R. (2016). Growth patterns among indigenous Qom children of the argentine Gran Chaco. American Journal of Human Biology, 28, 895–904.Google Scholar
  2. Alvarado, L. C. (2010). Population differences in the testosterone levels of young men are associated with prostate cancer disparities in older men. American Journal of Human Biology, 22, 449–455.CrossRefGoogle Scholar
  3. Alvarado, L. C. (2011). Total testosterone in young men is more closely associated than free testosterone with prostate cancer disparities. Therapeutic Advances in Urology, 3, 99–106.CrossRefGoogle Scholar
  4. Alvarado, L. C. (2013). Do evolutionary life-history trade-offs influence prostate cancer risk? A review of population variation in testosterone levels and prostate cancer disparities. Evolutionary Applications, 6, 117–133.CrossRefGoogle Scholar
  5. Alvarado, L. C., Muller, M. N., Emery, T. M., Klimek, M., Nenko, I., & Jasieńska, G. (2015). The paternal provisioning hypothesis: Effects of workload and testosterone production on Men’s musculature. American Journal of Physical Anthropology, 158, 19–35.CrossRefGoogle Scholar
  6. Alvergne, A., Faurie, C., & Raymond, M. (2009). Variation in testosterone levels and male reproductive effort: Insight from a polygynous human population. Hormones and Behavior, 56, 491–497.CrossRefGoogle Scholar
  7. Beall, C. M., Worthman, C. M., Stallings, J., Strohl, K. P., Brittenham, G. M., & Barragan, M. (1992). Salivary testosterone concentration of Aymara men native to 3600 m. Annals of Human Biology, 19, 67–78.CrossRefGoogle Scholar
  8. Beehner, J. C., Gesquiere, L., Seyfarth, R. M., Cheney, D. L., Alberts, S. C., & Altmann, J. (2009). Testosterone related to age and life-history stages in male baboons and geladas. Hormones and Behavior, 56, 472–480.CrossRefGoogle Scholar
  9. Bentley, G. R., Harrigan, A. M., Campbell, B., & Ellison, P. T. (1993). Seasonal effects on salivary testosterone levels among lese males of the Ituri Forest, Zaire. American Journal of Human Biology, 5, 711–717.CrossRefGoogle Scholar
  10. Bokony, V., Garamszegi, L. Z., Hirschenhauser, K., & Liker, A. (2008). Testosterone and melanin-based black plumage coloration: A comparative study. Behavioral Ecology and Sociobiology, 62, 1229–1238.CrossRefGoogle Scholar
  11. Bribiescas, R. G. (1996). Testosterone levels among Aché hunter-gatherer men : A functional interpretation of population variation among adult males. Human Nature, 7, 163–188.CrossRefGoogle Scholar
  12. Bribiescas R.G. (2001a). Reproductive ecology and life history of the human male. American Journal of Physical Anthropology, Supplement 33, 148–176.Google Scholar
  13. Bribiescas, R. G. (2001b). Reproductive physiology of the human male: An evolutionary and life history perspective. In P. T. Ellison (Ed.), Reproductive ecology and human evolution (pp. 107–135). New York: Aldine de Gruyter.Google Scholar
  14. Bribiescas, R. G. (2010). An evolutionary and life history perspective on human male reproductive senescence. Annals of the New York Academy of Sciences, 1204, 54–64.CrossRefGoogle Scholar
  15. Bribiescas, R. G. (2006). On the evolution of human male reproductive senescence: proximate mechanisms and life history strategies. Evolutionary Anthropology, 15, 132–141.Google Scholar
  16. Campbell, B., O'Rourke, M. T., & Lipson, S. F. (2003). Salivary testosterone and body composition among Ariaal males. American Journal of Human Biology, 15, 697–708.CrossRefGoogle Scholar
  17. Campbell, B., Leslie, P., & Campbell, K. (2006). Age-related changes in testosterone and SHBG among Turkana males. American Journal of Human Biology, 18, 71–82.CrossRefGoogle Scholar
  18. Christiansen, K. H. (1991). Serum and saliva sex hormone levels in !Kung san men. American Journal of Physical Anthropology, 86, 37–44.CrossRefGoogle Scholar
  19. Clutton-Brock, T. H. (1991). The evolution of parental care. Princeton: Princeton University Press.Google Scholar
  20. Ellis, L., & Nyborg, H. (1992). Racial/ethnic variations in male testosterone levels: a probable contributor to group differences in health. Steroids, 57, 72–75.Google Scholar
  21. Ellison, P. T., & Panter-Brick, C. (1996). Salivary testosterone levels among Tamang and kami males of Central Nepal. Human Biology, 68, 955–965.Google Scholar
  22. Ellison, P. T., Lipson, S. F., & Meredith, M. D. (1989). Salivary testosterone levels in males from the Ituri Forest of Zaïre. American Journal of Human Biology, 1, 21–24.CrossRefGoogle Scholar
  23. Ellison, P. T., Bribiescas, R. G., Bentley, G. R., Campbell, B. C., Lipson, S. F., Panter-Brick, C., & Hill, K. (2002). Population variation in age-related decline in male salivary testosterone. Human Reproduction, 17, 3251–3253.CrossRefGoogle Scholar
  24. Fernandez-Duque, E., Valeggia, C. R., & Mendoza, S. P. (2009). The biology of paternal care in human and nonhuman primates. Annual Review of Anthropology, 38, 115–130.CrossRefGoogle Scholar
  25. Gettler, L. T. (2014). Applying socioendocrinology to evolutionary models: Fatherhood and physiology. Evolutionary Anthropology, 23, 146–160.CrossRefGoogle Scholar
  26. Gettler, L. T., McDade, T. W., Feranil, A. B., & Kuzawa, C. W. (2011). Longitudinal evidence that fatherhood decreases testosterone in human males. PNAS, 108, 16194–16199.CrossRefGoogle Scholar
  27. Gray, P. B. (2003). Marriage, parenting, and testosterone variation among Kenyan Swahili men. American Journal of Physical Anthropology, 122, 279–286.CrossRefGoogle Scholar
  28. Gray, P. B., & Campbell, B. C. (2009). Human male testosterone, pair-bonding, and fatherhood. In P. T. Ellison & P. B. Gray (Eds.), Endocrinology of social relationships (pp. 270–293). Cambridge: Harvard University Press.Google Scholar
  29. Gray, P. B., & Crittenden, A. N. (2014). Father Darwin: Effects of children on men, viewed from an evolutionary perspective. Fathering, 12, 121–142.Google Scholar
  30. Gray, P. B., Kahlenberg, S. M., Barrett, E. S., Lipson, S. F., & Ellison, P. T. (2002). Marriage and fatherhood are associated with lower testosterone in males. Evolution and Human Behavior, 23, 193–201.CrossRefGoogle Scholar
  31. Gray, P. B., Kruger, A., Huisman, H. W., Wissing, M. P., & Vorster, H. H. (2006a). Predictors of south African male testosterone levels: The THUSA study. American Journal of Human Biology, 18, 123–132.CrossRefGoogle Scholar
  32. Gray, P. B., Yang, C. J., & Pope, H. G., Jr. (2006b). Fathers have lower salivary testosterone levels than unmarried men and married non-fathers in Beijing, China. Proceedings of the Royal Society B, 273, 333–339.CrossRefGoogle Scholar
  33. Gray, P. B., Parkin, J. C., & Samms-Vaughan, M. E. (2007). Hormonal correlates of human paternal interactions: A hospital-based investigation in urban Jamaica. Hormones and Behavior, 52, 499–507.CrossRefGoogle Scholar
  34. Gray, P. B., McHale, T. S., & Carré, J. M. (2017). A review of human male field studies of hormones and behavioral reproductive effort. Hormones and Behavior, 91, 52–67.CrossRefGoogle Scholar
  35. Gurven, M., & Hill, K. (2009). Why do men hunt? A re-evaluation of "man the hunter" and the sexual division of labor. Current Anthropology, 50, 51–74.CrossRefGoogle Scholar
  36. Hamilton, J. B., & Mestler, G. E. (1969). Mortality and survival: Comparison of eunuchs with intact men and women in a mentally retarded population. Journal of Gerontology, 24, 395–411.CrossRefGoogle Scholar
  37. Hill, K., & Hurtado, A. M. (1996). Ache life history: The ecology and demography of a foraging people. New York: de Gruyter.Google Scholar
  38. Hooper P.L. (2011). The structure of energy production and redistribution among Tsimane’ forager-horticulturalists. PhD Dissertation, Evolutionary Anthropology, University of New Mexico.Google Scholar
  39. Hu, H., Odedina, F. T., Reams, R. R., Lissaker, C. T., & Xu, X. (2015). Racial Differences in Age-Related Variations of Testosterone Levels Among US Males: Potential Implications for Prostate Cancer and Personalized Medication. Journal of Racial and Ethnic Health Disparities, 2, 69–76.Google Scholar
  40. Kaplan, H., & Lancaster, J. B. (2000). The evolutionary economics and psychology of the demographic transition to low fertility. In L. Cronk, N. Chagnon, & W. Irons (Eds.), Evolutionary biology and human behavior: 20 years later (pp. 283–322). New York: Aldine de Gruyter.Google Scholar
  41. Kaplan, H., Hill, K., Lancaster, J. B., & Hurtado, M. (2000). A theory of human life history evolution: Diet, intelligence, and longevity. Evolutionary Anthropology, 9, 156–185.CrossRefGoogle Scholar
  42. Kehinde, E. O., Akanji, A. O., Memon, A., Bashir, A. A., Daar, A. S., Al-Awadi, K. A., et al. (2006). Prostate cancer risk: The significance of differences in age related changes in serum conjugated and unconjugated steroid hormone concentrations between Arab and Caucasian men. International Urology and Nephrology, 38, 33–44.CrossRefGoogle Scholar
  43. Ketterson, E. D., & Nolan, V., Jr. (1992). Hormones and life histories: An integrative approach. American Naturalist, 140, s33–s62.CrossRefGoogle Scholar
  44. Ketterson, E. D., & Nolan, V., Jr. (1999). Adaptation, exaptation, and constraint: A hormonal perspective. American Naturalist, 154, S4–S25.CrossRefGoogle Scholar
  45. Klima, G. (1970). The Barabaig: East African cattle-herders. Prospect Heights: Waveland Press.Google Scholar
  46. Kraska-Miller, M. (2014). Nonparametric statistics for social and behavioral sciences. Boca Raton: CRC Press.Google Scholar
  47. Krause, W. (2006). Androgens in the demography of male life course - a review. Biodemography and Social Biology, 53, 4–12.CrossRefGoogle Scholar
  48. Kuzawa, C. W., Muller, M. N., Gettler, L., McDade, T. W., & Feranil, A. (2009). Fatherhood, pairbonding, and testosterone in the Philippines. Hormones and Behavior, 56, 429–435.CrossRefGoogle Scholar
  49. Lancaster, J. B. (1997). The evolutionary history of human parental Investment in Relation to population growth and social stratification. In P. A. Gowaty (Ed.), Feminism and evolutionary biology (pp. 466–489). New York: Chapman & Hall.CrossRefGoogle Scholar
  50. Lancaster, J. B., & Lancaster, C. S. (1983). Parental investment: The hominid adaptation. In D. Ortner (Ed.), How Humans Adapt: A Biocultural Odyssey. Proceedings of the Seventh International Smithsonian Symposium (pp. 33–66). Washington DC: Smithsonian Institution.Google Scholar
  51. Lancaster, J. B., Kaplan, H., Hill, K., & Hurtado, A. M. (2000). The Evolution of Life History, Intelligence, and Diet Among Chimpanzees and Human Foragers. In F. Tonneau & N. S. Thompson (Eds.), Perspectives in Ethology: Evolution, Culture and Behavior (Vol. 13, pp. 47–72). New York: Plenum Publishers.Google Scholar
  52. Lincoln, G. A. (1971). The seasonal reproductive changes in the red deer stag (Cervus elaphus). Journal of Zoology, 163, 105–123.CrossRefGoogle Scholar
  53. Lincoln, G. A. (1992). Biology of antlers. Journal of Zoology, 226, 517–528.CrossRefGoogle Scholar
  54. Lukas, W. D., Campbell, B. C., & Ellison, P. T. (2004). Testosterone, aging, and body composition in men from Harare, Zimbabwe. American Journal of Human Biology, 16, 704–712.CrossRefGoogle Scholar
  55. Magid, K., Chatterton, R. T., Ahamed, F. U., & Bentley, G. R. (2018). Childhood ecology influences salivary testosterone, pubertal age and stature of Bangladeshi UK migrant men. Nature Ecology & Evolution, 2, 1146–1154.CrossRefGoogle Scholar
  56. Marlowe, F. W. (1999). Showoffs or providers? The parenting effort of Hadza men. Evolution and Human Behavior, 20, 391–404.CrossRefGoogle Scholar
  57. Marlowe, F. W. (2000). Paternal investment and the human mating system. Behavioural Processes, 51, 45–61.CrossRefGoogle Scholar
  58. Marlowe, F. W. (2003). A critical period for provisioning by Hadza men. Implications for pair bonding. Evolution and Human Behavior, 24, 217–229.CrossRefGoogle Scholar
  59. Marlowe, F. W. (2010). The Hadza: Hunter-gatherers of Tanzania. Berkeley: University of California Press.Google Scholar
  60. Mendoza, M. (1999). The Western Toba: Family life and subsistence of a former hunter-gatherer society (pp.79-108). In E. S. Miller (Ed.), Peoples of the Gran Chaco. Westport: Bergin & Garvey.Google Scholar
  61. Min, K. J., Lee, C. K., & Park, H. N. (2012). The lifespan of Korean eunuchs. Current Biology, 22, R792–R793.CrossRefGoogle Scholar
  62. Muehlenbein, M. P., & Bribiescas, R. G. (2005). Testosterone-mediated immune functions and male life histories. American Journal of Human Biology, 17, 527–558.CrossRefGoogle Scholar
  63. Muehlenbein, M. P., Hirschtick, J. L., Bonner, J. Z., & Swartz, A. M. (2010). Toward quantifying the usage costs of human immunity: Altered metabolic rates and hormone levels during acute immune activation in men. American Journal of Human Biology, 22, 546–556.CrossRefGoogle Scholar
  64. Muller, M. N. (2017). Testosterone and reproductive effort in male primates. Hormones and Behavior, 91, 36–51.CrossRefGoogle Scholar
  65. Muller, M. N., & Emery, T. M. (2012). Mating, parenting, and male reproductive strategies. In J. C. Mitani, J. Call, P. M. Kappeler, R. A. Palombit, & J. B. Silk (Eds.), The evolution of primate societies (pp. 387–411). Chicago: University of Chicago Press.Google Scholar
  66. Muller, M. N., & Wrangham, R. W. (2004). Dominance, aggression and testosterone in wild chimpanzees: a test of the 'challenge hypothesis'. Animal Behaviour, 67, 113–123.Google Scholar
  67. Muller, M. N., & Wrangham, R. W. (2005). Testosterone and energetics in wild chimpanzees (Pan troglodytes schweinfurthii). American Journal of Primatology, 66, 119–130.CrossRefGoogle Scholar
  68. Muller, M. N., Marlowe, F. W., Bugumba, R., & Ellison, P. T. (2009). Testosterone and paternal care in east African foragers and pastoralists. Proceedings of the Royal Society B, 276, 347–354.CrossRefGoogle Scholar
  69. Nunes, S., Fite, J. E., & French, J. A. (2000). Variation in steroid hormones associated with infant care behaviour and experience in male marmosets (Callithrix kuhlii). Animal Behaviour, 60, 857–865.CrossRefGoogle Scholar
  70. Parent, A. S., Teilmann, G., Juul, A., Skakkebaek, N. E., Toppari, J., & Bourguignon, J. P. (2003). The timing of normal puberty and the age limits of sexual precocity: Variations around the world, secular trends, and changes after migration. Endocrine Reviews, 24, 668–693.CrossRefGoogle Scholar
  71. Perini, T., Ditzen, B., Fischbacher, S., & Ehlert, U. (2012). Testosterone and relationship quality across the transition to fatherhood. Biological Psychology, 90, 186–191.CrossRefGoogle Scholar
  72. Promislow, D. (1992). Cost of sexual selection in natural population of mammals. Proceedings of the Royal Society B, 247, 203–210.CrossRefGoogle Scholar
  73. Promislow, D., Montgomerie, R., & Martin, T. E. (1992). Mortality costs of sexual dimorphism in birds. Proceedings of the Royal Society B, 250, 143–150.CrossRefGoogle Scholar
  74. Roney, J. R. (2016). Theoretical frameworks for human behavioral endocrinology. Hormones and Behavior, 84, 97–110.CrossRefGoogle Scholar
  75. Santos, C. V., French, J. A., & Otta, E. (1997). Infant Carrying Behavior in Callitrichid Primates: Callithrix and Leontopithecus. International Journal of Primatology, 18, 889–907.Google Scholar
  76. Sellen, D. W. (1999). Polygyny and child growth in a traditional pastoral society: The case of the Datoga of Tanzania. Human Nature, 10, 329–371.CrossRefGoogle Scholar
  77. Shen, X., Wang, R., Yu, N., Shi, Y., Li, H., Xiong, C., Li, Y., Wells, E. M., & Zhou, Y. (2016). Reference ranges and Association of age and Lifestyle Characteristics with testosterone, sex hormone binding globulin, and luteinizing hormone among 1166 Western Chinese men. PLoS One, 11(10), e0164116.CrossRefGoogle Scholar
  78. Stiver, K. A., & Alonzo, S. H. (2009). Parental and mating effort: Is there necessarily a trade-off? Ethology, 115, 1101–1126.CrossRefGoogle Scholar
  79. Storey, A. E., Walsh, C. J., Quinton, R. L., & Wynne-Edwards, K. E. (2000). Hormonal correlates of paternal responsiveness in new and expectant fathers. Evolution and Human Behavior, 21, 79–95.Google Scholar
  80. Tecot, S. R., & Baden, A. L. (2018). Profiling caregivers: Hormonal variation underlying allomaternal care in wild red-bellied lemurs, Eulemur rubriventer. Physiology & Behavior, 193, 135–148.CrossRefGoogle Scholar
  81. Tehrani, F. R., Mansournia, M. A., Solaymani-Dodaran, M., Minooee, S., & Azizi, F. (2017). Serum variations of anti-mullerian hormone and total testosterone with aging in healthy adult Iranian men: A population-based study. PLoS One, 12(7), e0179634.CrossRefGoogle Scholar
  82. Travison, T. G., Araujo, A. B., O'Donnell, A. B., Kupelian, V., & McKinlay, J. B. (2007). A population-level decline in serum testosterone levels in American men. The Journal of Clinical Endocrinology and Metabolism, 92, 196–202.CrossRefGoogle Scholar
  83. Trumble, B. C., Cummings, D., von Rueden, C., O'Connor, K. A., Smith, E. A., Gurven, M., et al. (2012). Physical competition increases testosterone among Amazonian forager-horticulturalists: A test of the 'challenge hypothesis'. Proceedings of the Royal Society B, 279, 2907–2912.CrossRefGoogle Scholar
  84. Trumble, B. C., Blackwell, A. D., Stieglitz, J., Thompson, M. E., Suarez, I. M., Kaplan, H., & Gurven, M. (2016). Associations between male testosterone and immune function in a pathogenically stressed forager-horticultural population. American Journal of Physical Anthropology, 161, 494–505.CrossRefGoogle Scholar
  85. Valeggia, C. R., Lewarch, C. L., & Ellison, P. T. (2009). Testosterone, aging, and seasonality among Toba men of northern Argentina. American Journal of Physical Anthropology, 138, S48–S259.Google Scholar
  86. Valeggia, C. R., Burke, K. M., & Fernandez-Duque, E. (2010). Nutritional status and socioeconomic change among Toba and Wichí populations of the Argentinean Chaco. Economics and Human Biology, 8, 100–110.CrossRefGoogle Scholar
  87. Veile, A. (2018). Hunter-gatherer diets and human behavioral evolution. Physiology & Behavior, 193, 190–195.CrossRefGoogle Scholar
  88. Walker, R., Gurven, M., Hill, K., Migliano, A., Chagnon, N., De Souza, R., et al. (2006). Growth rates and life histories in twenty-two small-scale societies. American Journal of Human Biology, 18, 295–311.CrossRefGoogle Scholar
  89. Wingfield, J. C., Hegner, R. E., Dufty, A. M., Jr., & Ball, G. F. (1990). The "challenge hypothesis": Theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. American Naturalist, 136, 829–846.CrossRefGoogle Scholar
  90. Wood, J. W. (1994). Dynamics of human reproduction: Biology, biometry, demography. Hawthorne: Aldine de Gruyter Publishers.Google Scholar
  91. Wood, B. M., & Marlowe, F. (2013). Household and kin provisioning by Hadza men. Human Nature, 24, 280–317.Google Scholar
  92. Wynne-Edwards, K. E. (2001). Hormonal changes in mammalian fathers. Hormones & Behavior, 40, 139–145.CrossRefGoogle Scholar
  93. Ziegler, T. E. (2000). Hormones associated with non-maternal infant care: a review of mammalian and avian studies. Folia Primatologica, 71, 6–21.Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Louis Calistro Alvarado
    • 1
    Email author
  • Claudia R. Valeggia
    • 2
  • Peter T. Ellison
    • 3
  • Caitlin L. Lewarch
    • 4
  • Martin N. Muller
    • 5
  1. 1.Department of AnthropologyUniversity of PittsburghPittsburghUSA
  2. 2.Department of AnthropologyYale UniversityNew HavenUSA
  3. 3.Department of Human Evolutionary BiologyHarvard UniversityCambridgeUSA
  4. 4.Department of Molecular and Cellular BiologyHarvard UniversityCambridgeUSA
  5. 5.Department of AnthropologyUniversity of New MexicoAlbuquerqueUSA

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