ARTICLES
https://doi.org/10.1038/s41559-018-0567-6
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
1
Department of Anthropology, University of Durham, Durham, UK.
2
Department of Obstetrics and Gynecology, Feinberg School of Medicine, Northwestern
University, Chicago, IL, USA.
3
Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA.
4
Department of
Pathology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA.
5
Department of Anthropology, University of Chittagong,
Chittagong, Bangladesh. *e-mail: kesson.magid@durham.ac.uk
G
lobally, men in wealthy, developed regions generally have
higher testosterone than those living in less affluent ones
1–3
.
While some researchers link such variation to ‘ethnic’, ‘racial’
or genetic traits
4–6
, ecological and behavioural variables associ-
ated with energy availability, such as abundant nutritional intake,
pathogen load and sedentary lifestyles, also potentially contrib-
ute to interpopulation differences in reproductive phenotypes
7–12
.
Developmental exposure to energetic variables during childhood
may further explain adult variation in reproductive steroid hormones.
Evidence supporting this ‘developmental hypothesis’ connects early
infancy, pre-birth or childhood experience with sex steroid levels in
later infancy
13,14
, developmental timing as measured by adult height
and pubertal age
15–18
, or adult reproductive function
3,18–21
.
Migration studies support the developmental hypothesis.
Children migrating from less to more affluent regions show rapid
postnatal growth and earlier sexual maturation
19,22,23
. Levels of
salivary progesterone, ovulation rates and menopausal age of
Bangladeshi women who reached adulthood in more ecologically
constrained environments were lower compared with those who
migrated to a less challenging one
19,24,25
, and early-childhood migra-
tion (age 0–8 versus 9–16 years) was associated with more robust
ovarian function
19,23
.
We lack comparable migrant studies among men, but—based
on the above findings—we predicted that men with different life
histories would express varying degrees of reproductive investment
depending on differential developmental conditions. We expected
that males encountering improved ecologies before or during devel-
opmental transitions would invest in more costly reproductive effort
associated with competition and/or sexual signalling, mediated by
testosterone
26–28
. Based on ecological developmental histories, we
presumed that individual trade-offs between testosterone-mediated
traits and other energetic demands would lead to population-level
differences. Considering male variation in reproductive function,
hormonal variations in non-clinical populations are unlikely to
impact fecundity
29,30
, but instead relate to trade-offs between traits
associated with survivorship and reproductive effort
2,3,31–34
.
We therefore designed a cross-cultural study to distinguish
whether global variations in male reproductive phenotypes (mea-
sured by salivary testosterone levels, pubertal age and stature)
reflect: (1) developmentally plastic, organizational responses to
childhood ecology or (2) current, activational responses to local
ecology. We selected a generally homogenous, ethno-cultural group
of Bangladeshis of Bengali ethnic origin, some of whom migrated
from a less to more affluent region (specifically, Sylhet, northeast
Bangladesh to London, United Kingdom).
We assumed that there would be fewer ecological constraints on
males in the United Kingdom compared with Bangladesh. Despite
improvements, Bangladesh still ranks globally among the poor-
est quartile of countries, with high indicators of maternal under-
nutrition and stunting (36%) among children aged <5 years
35,36
.
However, the Bangladeshi populations studied here originate from
the land-owning, middle-class not normally subject to nutritional
Childhood ecology influences salivary
testosterone, pubertal age and stature of
Bangladeshi UK migrant men
Kesson Magid
1
*, Robert T. Chatterton
2,3,4
, Farid Uddin Ahamed
5
and Gillian R. Bentley
1
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 var-
ies 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 ecol-
ogy 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, declin-
ing 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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