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Childhood ecology influences salivary testosterone, pubertal age and stature of Bangladeshi UK migrant men

Nature Ecology & Evolutionvolume 2pages11461154 (2018) | Download Citation


Male reproductive investment is energetically costly, and measures of human reproductive steroid hormones (testosterone), developmental tempo (pubertal timing) and growth (stature) correlate with local ecologies at the population level. It is unclear whether male reproductive investment in later life is ‘set’ during childhood development, mediated through adulthood, or varies by ethnicity. Applying a life-course model to Bangladeshi migrants to the United Kingdom, here we investigate plasticity in human male reproductive function resulting from childhood developmental conditions. We hypothesized that childhood ecology shapes adult trade-offs between reproductive investment and/or other fitness-related traits. We predicted correspondence between these traits and developmental timing of exposure to ecological constraints (Bangladesh) or conditions of surplus (United Kingdom). We compared: Bangladesh sedentees (n = 107); Bangladeshi men who migrated in childhood to the United Kingdom (n = 59); migrants who arrived in adulthood (n = 75); second-generation UK-born and raised children of Bangladeshi migrants (n = 56); and UK-born ethnic Europeans (n = 62). Migration before puberty predicted higher testosterone and an earlier recalled pubertal age compared with Bangladeshi sedentees or adult migrants, with more pronounced differences in men who arrived before the age of eight. Second-generation Bangladeshis were taller, with higher testosterone than sedentees and adult migrants, and higher waking testosterone than Europeans. Age-related testosterone profiles varied by group, declining in UK migrants, increasing in sedentees, and having no significant relationship within UK-born groups. We conclude that male reproductive function apparently remains plastic late into childhood, is independent of Bengali or European ethnicity, and shapes physiological trade-offs later in life.

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  • 02 July 2018

    In the version of this Article originally published, the units for the ‘Weight’ column in Table 1 were incorrect; they should have been kg. This has now been corrected.


  1. 1.

    Bentley, G. R., Harrigan, A. M., Campbell, B. & Ellison, P. T. Seasonal effects on salivary testosterone levels among lese males of the Ituri forest, Zaire. Am. J. Hum. Biol. 5, 711–717 (1993).

  2. 2.

    Ellison, P. T. et al. Population variation in age-related decline in male salivary testosterone. Hum. Reprod. 17, 3251–3253 (2002).

  3. 3.

    Bribiescas, R. G. Testosterone levels among Aché hunter-gatherer men : a functional interpretation of population variation among adult males. Hum. Nat. 7, 163–188 (1996).

  4. 4.

    Richard, A. et al. Racial variation in sex steroid hormone concentration in black and white men: a meta-analysis. Andrology 2, 428–435 (2014).

  5. 5.

    Panizzon, M. S. et al. Genetic and environmental influences of daily and intra-individual variation in testosterone levels in middle-aged men. Psychoneuroendocrinology 38, 2163–2172 (2013).

  6. 6.

    Travison, T. G. et al. The heritability of circulating testosterone, oestradiol, oestrone and sex hormone binding globulin concentrations in men: the Framingham Heart Study. Clin. Endocrinol. 80, 277–282 (2014).

  7. 7.

    Muehlenbein, M. P., Alger, J., Cogswell, F., James, M. & Krogstad, D. The reproductive endocrine response to Plasmodium vivax infection in Hondurans. Am. J. Trop. Med. Hyg. 73, 178–187 (2005).

  8. 8.

    Trumble, B. C. et al. Age-independent increases in male salivary testosterone during horticultural activity among Tsimane forager-farmers. Evol. Hum. Behav. 34, 350–357 (2013).

  9. 9.

    Priskorn, L. et al. Is sedentary lifestyle associated with testicular function? A cross-sectional study of 1,210 men. Am. J. Epidemiol. 184, 284–294 (2016).

  10. 10.

    Cangemi, R., Friedmann, A. J., Holloszy, J. O. & Fontana, L. Long-term effects of calorie restriction on serum sex-hormone concentrations in men. Aging Cell 9, 236–242 (2010).

  11. 11.

    Boonekamp, J. J., Ros, A. H. F. & Verhulst, S. Immune activation suppresses plasma testosterone level: a meta-analysis. Biol. Lett. 4, 741–744 (2008).

  12. 12.

    Gettler, L. T., McDade, T. W., Agustin, S. S., Feranil, A. B. & Kuzawa, C. W. Testosterone, immune function, and life history transitions in Filipino males (Homo sapiens). Int. J. Primatol. 35, 787–804 (2014).

  13. 13.

    Thompson, A. L. & Lampl, M. Prenatal and postnatal energetic conditions and sex steroids levels across the first year of life. Am. J. Hum. Biol. 25, 643–654 (2013).

  14. 14.

    Xia, K. et al. Environmental and genetic contributors to salivary testosterone levels in infants. Front. Endocrinol. 5, 1–15 (2014).

  15. 15.

    Jardim-Botelho, A. et al. Age patterns in undernutrition and helminth infection in a rural area of Brazil: associations with ascariasis and hookworm. Trop. Med. Int. Heal. 13, 458–467 (2008).

  16. 16.

    Holmgren, A. et al. Pubertal height gain is inversely related to peak BMI in childhood. Pediatr. Res. 81, 448–454 (2016).

  17. 17.

    Villamor, E. & Jansen, E. C. Nutritional determinants of the timing of puberty. Annu. Rev. Public Health 37, 33–46 (2016).

  18. 18.

    Kuzawa, C. W., McDade, T. W., Adair, L. S. & Lee, N. Rapid weight gain after birth predicts life history and reproductive strategy in Filipino males. Proc. Natl Acad. Sci. USA 107, 16800–16805 (2010).

  19. 19.

    Núñez-de la Mora, A., Chatterton, R. T., Choudhury, O. A., Napolitano, D. A. & Bentley, G. R. Childhood conditions influence adult progesterone levels. PLoS Med. 4, e167 (2007).

  20. 20.

    Jasienska, G., Ziomkiewicz, A., Lipson, S. F., Thune, I. & Ellison, P. T. High ponderal index at birth predicts high estradiol levels in adult women. Am. J. Hum. Biol. 18, 133–140 (2006).

  21. 21.

    Ellison, P. T. Developmental influences on adult ovarian hormonal function. Am. J. Hum. Biol. 8, 725–734 (1996).

  22. 22.

    Parent, A. S. et al. Timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr. Rev. 24, 668–693 (2003).

  23. 23.

    Houghton, L. C. et al. Childhood environment influences adrenarcheal timing among first-generation Bangladeshi migrant girls to the UK. PLoS ONE 9, e109200 (2014).

  24. 24.

    Murphy, L. et al. Life course effects on age at menopause among Bangladeshi sedentees and migrants to the UK. Am. J. Hum. Biol. 25, 83–93 (2013).

  25. 25.

    Begum, K. et al. Ethnicity or environment: effects of migration on ovarian reserve among Bangladeshi women in the United Kingdom. Fertil. Steril. 105, 744.e1–754.e1 (2016).

  26. 26.

    Geary, D. C. Evolution of sex differences in trait- and age-specific vulnerabilities. Perspect. Psychol. Sci. 11, 855–876 (2016).

  27. 27.

    Hamilton, W. D. & Zuk, M. Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387 (1982).

  28. 28.

    Kokko, H., Brooks, R., McNamara, J. M. & Houston, A. I. The sexual selection continuum. Proc. R. Soc. B 269, 1331–1340 (2002).

  29. 29.

    Andersen, A. et al. Serum levels of testosterone do not provide evidence of selection bias in studies of male reproductive health. Epidemiology 11, 232–234 (2000).

  30. 30.

    Bhasin, S. et al. Testosterone dose–response relationships in healthy young men. Am. J. Physiol. Endocrinol. Metab. 281, E1172–E1181 (2001).

  31. 31.

    Bribiescas, R. G. Reproductive ecology and life history of the human male. Am. J. Phys. Anthropol. 44, 148–176 (2001).

  32. 32.

    Alvergne, A., Faurie, C. & Raymond, M. Variation in testosterone levels and male reproductive effort: insight from a polygynous human population. Horm. Behav. 56, 491–497 (2009).

  33. 33.

    Vitzthum, V. J. et al. Seasonal and circadian variation in salivary testosterone in rural Bolivian men. Am. J. Hum. Biol. 21, 762–768 (2009).

  34. 34.

    Campbell, B., Leslie, P. & Campbell, K. Age-related changes in testosterone and SHBG among Turkana males. Am. J. Hum. Biol. 18, 71–82 (2006).

  35. 35.

    Ahmed, T. et al. Nutrition of children and women in Bangladesh: trends and directions for the future. J. Heal. Popul. Nutr. 30, 1–11 (2012).

  36. 36.

    Human Development Report 2016: Human Development for Everyone (United Nations Development Programme, New York, 2016).

  37. 37.

    Bangladesh Demographic and Health Survey 2014 (National Institute of Population Research and Training (NIPORT), Dhaka, and Mitra and Associates, Rockville, 2014).

  38. 38.

    The World Factbook (Central Intelligence Agency, Washington DC, 2018);

  39. 39.

    Howard, G. & Bartram, J. Domestic Water Quantity Service Level and Health (World Health Organisation, Geneva, 2003).

  40. 40.

    Das, S. & Gulshan, J. Different forms of malnutrition among under five children in Bangladesh: a cross sectional study on prevalence and determinants. BMC Nutr. 3, 1–12 (2017).

  41. 41.

    Stanton, B. F. & Clemens, J. D. Socioeconomic variables and rates of diarrhoeal disease in urban Bangladesh. Trans. R. Soc. Trop. Med. Hyg. 81, 278–282 (1987).

  42. 42.

    Alam, M. J. B., Rahman, M. H., Khan, S. K. & Munna, G. M. Unplanned urbanization: assessment through calculation of environmental degradation index. Int. J. Environ. Sci. Technol. 3, 119–130 (2006).

  43. 43.

    Kenway, P. & Palmer, G. Poverty Among Ethnic Groups: How and Why Does it Differ? (Joseph Rowntree Foundation, York, 2007).

  44. 44.

    Kaiser, J. & Gruzelier, J. H. The Adolescence Scale (AS-ICSM): a tool for the retrospective assessment of puberty milestones. Acta Paediatr. Suppl. 88, 64–68 (1999).

  45. 45.

    Morley, J. E. et al. Longitudinal changes in testosterone, luteinizing hormone, and follicle-stimulating hormone in healthy older men. Metabolism 46, 410–413 (1997).

  46. 46.

    Harman, M. S., Metter, J. E., Tobin, J. E., Pearson, J. & Blackman, M. R. Longitudinal effects of aging on serum total and free testosterone levels in healthy men. J. Clin. Endocrinol. Metab. 86, 724–731 (2001).

  47. 47.

    Allen, N. E., Appleby, P. N., Davey, G. K. & Key, T. J. Lifestyle and nutritional determinants of bioavailable androgens and related hormones in British men. Cancer Causes Control 13, 353–363 (2002).

  48. 48.

    Mantzoros, C. S. & Georgiadis, E. I. Body mass and physical activity are important predictors of serum androgen concentrations in young healthy men. Epidemiology 6, 432–435 (1995).

  49. 49.

    Mazur, A. The age–testosterone relationship in black, white, and Mexican-American men, and reasons for ethnic differences. Aging Male 12, 66–76 (2009).

  50. 50.

    Wingfield, J. C., Hegner, R. E., Dufty Jr, A. M. & Ball, G. F. The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating system, and breeding strategies. Am. Nat. 136, 829–846 (1990).

  51. 51.

    Archer, J. Testosterone and human aggression: an evaluation of the challenge hypothesis. Neurosci. Biobehav. Rev. 30, 319–345 (2006).

  52. 52.

    Muehlenbein, M. P. & Watts, D. P. The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees. Biopsychosoc. Med. 4, 21 (2010).

  53. 53.

    Sapolsky, R. M. Testicular function, social rank and personality among wild baboons. Psychoneuroendocrinology 16, 281–293 (1991).

  54. 54.

    Mazur, A. & Booth, A. Testosterone and dominance in men. Behav. Brain Sci. 21, 353–397 (1998).

  55. 55.

    Carré, J. M. & Olmstead, N. A. Social neuroendocrinology of human aggression: examining the role of competition-induced testosterone dynamics. Neuroscience 286, 171–186 (2015).

  56. 56.

    Book, A. S., Starzyk, K. B. & Quinsey, V. L. The relationship between testosterone and aggression: a meta-analysis. Aggress. Violent Behav. 6, 579–599 (2001).

  57. 57.

    Trumble, B. C. et al. Physical competition increases testosterone among Amazonian forager-horticulturalists: a test of the ‘challenge hypothesis’. Proc. Biol. Sci. 279, 2907–2912 (2012).

  58. 58.

    Gray, P. B., Campbell, B. C., Marlowe, F. W., Lipson, S. F. & Ellison, P. T. Social variables predict between-subject but not day-to-day variation in the testosterone of US men. Psychoneuroendocrinology 29, 1153–1162 (2004).

  59. 59.

    Gray, P. B., McHale, T. S. & Carré, J. M. A review of human male field studies of hormones and behavioral reproductive effort. Horm. Behav. 91, 52–67 (2017).

  60. 60.

    Gettler, L. T. Becoming DADS: considering the role of cultural context and developmental plasticity for paternal socioendocrinology. Curr. Anthropol. 57, S38–S51 (2016).

  61. 61.

    Bogin, B., Smith, P., Orden, A. B., Silva, M. I. V. & Loucky, J. Rapid change in height and body proportions of Maya American children. Am. J. Hum. Biol. 14, 753–761 (2002).

  62. 62.

    Mascie-Taylor, C. G. N. & Little, M. A. History of migration studies in biological anthropology. Am. J. Hum. Biol. 16, 365–378 (2004).

  63. 63.

    Wang, C., Plymate, S., Nieschlag, E. & Paulsen, C. A. Salivary testosterone in men: further evidence of a direct correlation with free serum testosterone. J. Clin. Endocrinol. Metab. 53, 1021–1024 (1981).

  64. 64.

    Ellison, P. T. Endocrinology, energetics, and human life history: a synthetic model. Horm. Behav. 91, 97–106 (2017).

  65. 65.

    Kuzawa, C. W., Georgiev, A. V., McDade, T. W., Bechayda, S. A. & Gettler, L. T. Is there a testosterone awakening response in humans? Adapt. Hum. Behav. Physiol. 2, 166–183 (2016).

  66. 66.

    Zemel, B. S., Kawchak, D. A., Ohene-Frempong, K., Schall, J. I. & Stallings, V. A. Effects of delayed pubertal development, nutritional status, and disease severity on longitudinal patterns of growth failure in children with sickle cell disease. Pediatr. Res. 61, 607–613 (2007).

  67. 67.

    Chisholm, J. S. Death, hope, and sex: life-history theory and the development of reproductive strategies. Curr. Anthropol. 34, 1–24 (1993).

  68. 68.

    Del Giudice, M., Angeleri, R. & Manera, V. The juvenile transition: a developmental switch point in human life history. Dev. Rev. 29, 1–31 (2009).

  69. 69.

    Herdt, G. & Mcclintock, M. The magical age of 10. Arch. Sex. Behav. 29, 587–606 (2000).

  70. 70.

    Hochberg, Z. Evo-devo of child growth II: human life history and transition between its phases. Eur. J. Endocrinol. 160, 135–141 (2009).

  71. 71.

    Palmert, M. R. et al. The longitudinal study of adrenal maturation during gonadal suppression: evidence that adrenarche is a gradual process. J. Clin. Endocrinol. Metab. 86, 4536–4542 (2001).

  72. 72.

    Peach, C. South Asian migration and settlement in Great Britain, 1951–2001. Contemp. S. Asia 15, 133–146 (2006).

  73. 73.

    Koo, M. M. & Rohan, T. E. Accuracy of short-term recall of age at menarche. Ann. Hum. Biol. 24, 61–64 (1997).

  74. 74.

    Cooper, R. et al. Validity of age at menarche self-reported in adulthood. J. Epidemiol. Community Health 60, 993–997 (2006).

  75. 75.

    Casey, V. A. et al. Accuracy of recall by middle-aged participants in a longitudinal study of their body size and indices of maturation earlier in life. Ann. Hum. Biol. 18, 155–166 (1991).

  76. 76.

    Gilger, J. W., Geary, D. C. & Eisele, L. M. Reliability and validity of retrospective self-reports of the age of pubertal onset using twin, sibling, and college student data. Adolescence 26, 41–53 (1991).

  77. 77.

    Flinn, M. V., Ponzi, D. & Muehlenbein, M. P. Hormonal mechanisms for regulation of aggression in human coalitions. Hum. Nat. 23, 68–88 (2012).

  78. 78.

    Jasienska, G., Bribiescas, R. G., Furberg, A. S., Helle, S. & Núñez-de la Mora, A. Human reproduction and health: an evolutionary perspective. Lancet 390, 510–520 (2017).

  79. 79.

    Alvarado, L. C. Do evolutionary life-history trade-offs influence prostate cancer risk? A review of population variation in testosterone levels and prostate cancer disparities. Evol. Appl. 6, 117–133 (2013).

  80. 80.

    Kaufman, J. M. & Vermeulen, A. The decline of androgen levels in elderly men and its clinical and therapeutic implications. Endocr. Rev. 26, 833–876 (2005).

  81. 81.

    Worthman, C. M. & Kuzara, J. Life history and the early origins of health differentials. Am. J. Hum. Biol. 17, 95–112 (2005).

  82. 82.

    Walvoord, E. C. The timing of puberty: is it changing? Does it matter? J. Adolesc. Health 47, 433–439 (2010).

  83. 83.

    Handelsman, D. J. Global trends in testosterone prescribing, 2000–2011: expanding the spectrum of prescription drug misuse. Med. J. Aust. 199, 548–551 (2013).

  84. 84.

    The Bangladeshi Muslim Community in England: Understanding Muslim Ethnic Communities (Change Institute, London, 2009).

  85. 85.

    Núñez-De La Mora, A., Bentley, G. R., Choudhury, O. A. & Napolitano, D. A. The impact of developmental conditions on adult salivary estradiol levels: why this differs from progesterone? Am. J. Hum. Biol. 20, 2–14 (2008).

  86. 86.

    Vittek, J., L’Hommedieu, D. G., Gordon, G. G., Rappaport, S. C. & Southren, A. L. Direct radioimmunoassay (RIA) of salivary testosterone: correlation with free and total serum testosterone. Life Sci. 37, 711–716 (1985).

  87. 87.

    Frisancho, A. R. Anthropometric Standards for the Assessment of Growth and Nutritional Status (Univ. Michigan Press, Ann Arbor, 1990).

  88. 88.

    Hair, J. F., Anderson, R. E., Tatham, R. L. & Black, W. C. Multivariate Data Analysis (Pearson Education International, Uppersaddle River, 2010).

  89. 89.

    Feldman, H. A. et al. Age trends in the level of serum testosterone and other hormones in middle-aged men: longitudinal results from the Massachusetts Male Aging Study. J. Clin. Endocrinol. Metab. 87, 589–598 (2002).

  90. 90.

    R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2017).

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The authors thank K. Begum, O. Choudhury, A. Chowdhury, D. Lawson, Z. Salehin, T. Sharmeen and students of Shahjalal University of Science and Technology for assistance with recruitment, translation and data collection, and the Bengali Workers Association, Chadswell Community Centre and Bengali Football Association for providing facilities and promotion. We thank L. Houghton, R. Mace and A. Núñez-de la Mora for advice on study implementation, and H. Colleran and A. Alvergne for comments on previous drafts. This work was supported by the Economic and Social Research Council (PTA-030-2005-00706), Prostate Research Campaign UK (G2003-07), and a Royal Society University Research Fellowship (to G.R.B., UF951006).

Author information


  1. Department of Anthropology, University of Durham, Durham, UK

    • Kesson Magid
    •  & Gillian R. Bentley
  2. Department of Obstetrics and Gynecology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA

    • Robert T. Chatterton
  3. Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA

    • Robert T. Chatterton
  4. Department of Pathology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA

    • Robert T. Chatterton
  5. Department of Anthropology, University of Chittagong, Chittagong, Bangladesh

    • Farid Uddin Ahamed


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K.M. and G.R.B. designed the study and drafted the manuscript. K.M. carried out all data and laboratory analysis. K.M. and F.U.A. supervised and performed the data collection. R.T.C. designed, advised and assisted with laboratory analysis.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Kesson Magid.

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    Supplementary Sections 1–3, including Supplementary Figures 1–2, Supplementary Tables 1–21, Supplementary Analysis, Supplementary References

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  3. Supplementary Section 4

    R script to perform all analyses and to create all plots and tables

  4. Supplementary Section 5

    Data file used in all analyses

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