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

An Author Correction to this article was published on 23 July 2018

This article has been updated

Abstract

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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Fig. 1: Linear regression of standing height by age at recruitment and migration.
Fig. 2: Resident group least squares mean salivary testosterone values, adjusted for age and BMI.
Fig. 3: Composite recalled age at puberty by age at migration.
Fig. 4: Daily mean salivary testosterone by age at migration.

Change history

  • 23 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.

References

  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).

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Google Scholar 

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

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

  38. The World Factbook (Central Intelligence Agency, Washington DC, 2018); https://www.cia.gov/library/publications/the-world-factbook/geos/bg.html

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

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

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

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

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

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

  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).

    Article  CAS  PubMed  Google Scholar 

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

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Acknowledgements

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).

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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.

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Correspondence to Kesson Magid.

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Magid, K., Chatterton, R.T., Ahamed, F.U. et al. Childhood ecology influences salivary testosterone, pubertal age and stature of Bangladeshi UK migrant men. Nat Ecol Evol 2, 1146–1154 (2018). https://doi.org/10.1038/s41559-018-0567-6

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