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Sexual dimorphism of body composition

Article in Best Practice & Research: Clinical Endocrinology & Metabolism · October 2007
DOI: 10.1016/j.beem.2007.04.007 · Source: PubMed

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Best Practice & Research Clinical Endocrinology & Metabolism
Vol. 21, No. 3, pp. 415–430, 2007
doi:10.1016/j.beem.2007.04.007
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Sexual dimorphism of body composition

Jonathan C.K. Wells *

Reader in Pediatric Nutrition Childhood Nutrition Research Centre, Institute of Child Health, 30 Guilford Street,
London WC1N 1EH, UK

Sexual dimorphism in human body composition is evident from fetal life, but emerges primarily
during puberty. At birth, males have a similar fat mass to females but are longer and have greater
lean mass. Such differences remain detectable during childhood; however, females enter puberty
earlier and undergo a more rapid pubertal transition, whereas boys have a substantially longer
growth period. After adjusting for dimorphism in size (height), adult males have greater total
lean mass and mineral mass, and a lower fat mass than females. These whole-body differences
are complemented by major differences in tissue distribution. Adult males have greater arm
muscle mass, larger and stronger bones, and reduced limb fat, but a similar degree of central
abdominal fat. Females have a more peripheral distribution of fat in early adulthood; however,
greater parity and the menopause both induce a more android fat distribution with increasing
age. Sex differences in body composition are primarily attributable to the action of sex steroid
hormones, which drive the dimorphisms during pubertal development. Oestrogen is important
not only in body fat distribution but also in the female pattern of bone development that pre-
disposes to a greater female risk of osteoporosis in old age. Disorders of sex development are
associated with significant abnormalities of body composition, attributable largely to their im-
pact on mechanisms of hormonal regulation.

Key words: Fat mass; Fat distribution; Lean mass; Bone mass.

As in many animal species, humans show significant average sex differences in body
size, though the magnitude of these differences varies with population. From an
evolutionary perspective, such differences can be related to divergent reproductive
strategies. However, unlike in many animal species, humans also show significant aver-
age sex differences in body composition. These can be attributed to specific aspects of
human biology, as will be discussed in more detail at the end of this article. Overall,
therefore, the two sexes in our species pursue contrasting patterns of growth and
development. Whilst these represent a normal aspect of human biology, they have
major implications for sex differences in the risk of various diseases. This review

* Tel.: þ44 207 905 2389; Fax: þ44 207 831 9903.
E-mail address: j.wells@ich.ucl.ac.uk
1521-690X/$ - see front matter ª 2007 Elsevier Ltd. All rights reserved.
 Author's personal copy
416 J. C. K. Wells

will discuss the three major tissue components, fat-free mass (used synonymously in
this chapter with lean mass), fat mass, and bone mineral mass. Other components
of body composition, such as the size of individual organs, also show dimorphism
but data remain scarce.

DIMORPHISM IN SIZE AND PHYSIQUE

Differences in adult body size are best illustrated by stature, which averages around 7%
greater in males but also varies significantly between populations.1,2 This dimorphism
emerges primarily during postnatal growth, with male neonates only 1% longer than fe-
males at birth.3 During childhood, size dimorphism remains relatively minor until the
onset of puberty. Here the two sexes take increasingly divergent pathways, with girls
passing through puberty earlier and ceasing to grow at a younger age.4 In terms of
body size, therefore, sexual dimorphism is primarily a secondary sexual characteristic.
The evaluation of differences in body composition requires this size dimorphism to
be addressed, for a number of reasons. First, total body composition is generally
assessed as tissue masses, and these (like weight) can only be compared after the
influence of body size is taken into account. Traditionally, body fat has been expressed
as a percentage of weight in order to allow for body size; however, this approach has
several limitations.5 Second, the sex difference in stature can be attributed primarily to
differences in leg length, and hence in addition to size dimorphism there is also dimor-
phism in body proportions. This influences allometric relationships between size and
body composition and may confound comparisons of regional body composition. This
issue requires attention because the regional distribution of body components is often
of greater importance for health than their total amounts. Third, body size has a com-
plex association with bone mineralization, which is poorly addressed by the main mea-
surement method, dual energy x-ray absorptiometry (DXA).6 Hence comparisons of
bone phenotype in particular require the effects of body size to be taken into account.

SHAPE DIMORPHISM

Simple indices of shape indicate that the regional distribution of body weight likewise
differs considerably between the sexes, although the magnitude of such differences
varies in relation to age. The close association between pubertal development and re-
gional body composition accounts for the emergence during adolescence of significant
shape dimorphism. By early adulthood, sex differences in body shape are maximal, with
females tending towards an hourglass body shape whilst males tend towards an inverted
triangle with broad shoulders and a narrow waist.7 Because fat and lean deposition is di-
rected towards different body locations, body shape conveys valuable information about
body composition. For example, the circumference of the waist is primarily influenced
by abdominal fatness, whereas breadth of the shoulders is more closely related to phy-
sique and lean mass. With increasing age the sex differences vanish, due primarily to
changes in female shape.7 Whilst male shape is relatively stable across decades, in
women weight is shifted upwards from the thigh to the waist and bust. By the seventh
or eighth decades of life, sexual dimorphism in shape is markedly reduced with both
sexes having lost the key characteristics of their early adulthood shape.7
Sex differences in body composition are also minimized at opposite ends of the
spectrum of body weight. Eating disorders, which tend to be far more common in fe-
males, prevent post-pubertal tissue accretion and hence the expression of body shape.
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Sexual dimorphism of body composition 417

Eating disorders could until recently be considered a Western phenomenon, but are
now emerging in modernizing populations such as in southern Brazil, where those
with low body mass index (BMI) are now disproportionately young educated women.8
This finding illustrates that social concerns with body shape are a key element in sec-
ular trends in body composition. At the other end of the spectrum, obesity in both
sexes results in a more android fat distribution and again decreases shape dimorphism.

DIMORPHISM IN TOTAL BODY COMPOSITION

The simplest model of body composition divides body weight into two components:
the fat and lean masses. Adjusting these components for size can be undertaken in dif-
ferent ways, many of which fail to achieve their purpose.9 They are now conventionally
adjusted for height by dividing by height squared, producing two indices: the lean mass
index (lean mass/height2) and the fat mass index (fat mass/height2).10 These indices
have the advantage that they provide discrete indices for the two components of
weight, each adjusted for an independent component of size. In most cases they pro-
vide sufficient adjustment for size, although in some cases more complex approaches
are required.11
Figure 1 illustrates sex differences in relation to age in these two indices. Boys are
heavier than girls at birth and during early infancy, a difference that can be attributed to
increased lean mass, whereas fat mass is similar between the sexes.12,13 Proportionally,
therefore, females are fatter than males at birth, and tend to have slightly higher mean
skin-fold thicknesses.3,14 Thus even at this early age, the two sexes appear to have dif-
fering developmental strategies, and these differences may be related to greater male
vulnerability in the newborn period.15
The two sexes show broad consistency over the first decade in terms of lean
mass12,16, but differ in their accretion of fat.17,18 Both sexes show relative decreases
in body fat between 1 and 6 years of age; however, whereas girls then begin to increase
in fatness again, increases in weight in boys are primarily attributable to lean mass.12,19
These contrasting growth patterns diverge further during adolescence, with girls gain-
ing considerable amounts of fat but relatively little lean, and boys showing the opposite
strategy.20–22 These changes are primarily hormonally driven (see below); however, re-
duced energy expenditure in girls during puberty may also be important.23 The end
result by early adulthood is that while the sexes have relatively similar weight for
height (BMI), the ratio of lean to fat is much greater in males than females.24 These
data illustrate the inadequacy of BMI as an index of body composition during growth.
Whereas increases in BMI are generally attributed to greater fatness, Figure 1 demon-
strates that most of the age-associated increase in BMI, particularly in boys, can be at-
tributed to increments in lean mass rather than fat.19,20
The attainment of adulthood is therefore marked by considerable dimorphism in
total body composition, with women having substantially greater mean percentage
fat and relatively less lean mass. This sex difference holds across all ethnic groups
and has been observed in all populations, although its magnitude is influenced by ethnic
genetic factors and environmental conditions. Percentage fat averages 10–15% in males
in most populations, but can attain 30% in some Polynesian populations. The typical
range in females is 20–30%, but up to 45% in Polynesians.25 Complementing these pop-
ulation differences in percentage fat are differences in relative lean mass; however,
these have generally received much less attention, despite their importance for func-
tional work capacity and long-term health.
 Author's personal copy
418 J. C. K. Wells

(a) 20
Male

Fat-free mass index (kg/m2)

Female
18

16

14

12

10
0 2 4 6 8 10 12 14 16 18 20
Age (years)

(b) 6
Male
Female
Fat mass index (kg/m2)

1
0 2 4 6 8 10 12 14 16 18 20
Age (years)

Figure 1. The relationship between age and (a) relative fat-free mass and (b) relative fatness during the life
course, using data from the reference child and adolescent.12,22 In each case, lean or fat mass has been ad-
justed for height by dividing by height squared. The resulting values, termed fat-free mass index and fat mass
index, are expressed in the same kg/m2 units as body mass index (BMI). During early life, boys and girls have
similar fatness, but boys have more lean mass and are therefore heavier. During childhood, both sexes lose
fatness, but boys gain relatively more lean mass. During adolescence, boys gained primarily lean and little fat,
whereas girls gain little lean but substantial fat. In adulthood, men show substantially less body fatness and
greater relative lean mass than women in all human populations. Note that the ‘kink’ in the profile of body
fatness at around 10–14 years may in part be due to merging two idealized data sets.

The main source of evidence concerning skeletal size and bone mass is DXA. This is
a two-dimensional imaging method which measures the length and width of bones but
not their depth.6 The degree of attenuation of photons during their transmission
through bone is a function of the bone mineral content. Larger bones with greater
volume attenuate more photons, but this does not imply greater bone density. Young
adult males therefore have greater bone mass due to their larger body size, but their
bone density is similar to that in females, and this applies likewise to earlier develop-
mental periods.26,27 The sex difference in bone mineral mass and size emerges during
puberty27,28 and can be attributed to several factors, including the longer prepubertal
growth period of boys compared to girls, and the inhibitory effect of oestrogen on
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Sexual dimorphism of body composition 419

periosteal apposition in girls.6 Recent studies indicate that gender differences in bone
mass emerge at around 15–17 years, with the larger size of male bones then conferring
greater strength.29 Thus whereas mineral mass is very similar between the sexes at
birth12, by the start of adulthood skeletal weight is around 4 kg in men and 2.8 kg
in women.30
Dimorphism in total body composition does not remain stable in adulthood. Males
maintain their lean mass into the fifth decade of life, but then begin to lose muscle
mass31 due to both hormonal changes and decline in activity levels. Females show
a similar decline in lean mass, but often illustrate greater gains in fatness32, even
when weight-stable.33 Such changes continue into old age34, but are strongly influ-
enced by the quality of the environment. Whereas those from industrialized popula-
tions tend to gain weight with age, in non-industrialized populations the elderly are
frequently malnourished.35,36 Since the decline in lean mass is relatively universal,
weight gain with age in all populations can be attributed primarily to fat.31
Ageing also influences skeletal phenotype. Bone size and content are influenced in
contrasting ways by the processes of growth and development. The effect of growth is
to increase the size of the bone, whereas that of ageing is to resorb bone from the
cortex while offsetting this process with periosteal apposition which enlarges the
bone.6 The process of trabecular bone loss can occur either by thinning or by loss
of connectivity, and the influence of these two processes differs between the sexes,
which can be attributed to the effect of oestrogen deficiency occurring at menopause.6
Age-associated periosteal bone formation also differs between the sexes, being
greater in men. The net effect of these two sex differences is to confer greater
strength on male bones in old age, and hence predispose to a marked sex difference
in the risk of fracture.6
Recent research has emphasized the influence of reproductive maturity on the pro-
file of female fatness. The timing of onset of puberty is itself associated with baseline
body fatness37, while those entering puberty earlier tend to maintain high levels of fat-
ness throughout adulthood.38 Pregnancy is associated with marked gains in lean mass
and body fat39, and fatness also increases and becomes more central with parity, since
postpartum fat accretion occurs disproportionately in the abdomen.40 Thus the mag-
nitude of sexual dimorphism can be related to patterns of reproductive maturation
and fertility. However, calcium depletion related to lactation is only temporary.41
Sexual dimorphism in total tissue masses is of importance in several contexts: for
example, when calculating energy requirements or the dosages of some drug treat-
ments and dialysis. It also exerts strong effects on some aspects of function, such as
work capacity. However, it is regional body composition that is most strongly impli-
cated in sex differences in the risk of diseases.

REGIONAL BODY COMPOSITION

Lean

The increased lean mass of males can be attributed disproportionately to muscle mass.
Based on magnetic resonance imaging (MRI) measurements of healthy adults, the ratio
of muscle mass to total lean mass was 0.53 in males and 0.47 in females42, with this sex
difference declining with age. However, this dimorphism is strongly influenced by age.
Dissection studies demonstrate that around 40% of total musculature is located in the
head and trunk at birth, but only 25–30% by adulthood.30,43 In turn, lower-limb muscle
 Author's personal copy
420 J. C. K. Wells

mass increases from around 40% of the total at birth to 55% by maturity.30,43 Thus, sex
differences emerge within the context of this change with age.
Due to historical difficulties in measuring regional muscle mass in vivo, most data
relate to the estimated muscle areas calculated using anthropometry. The most com-
monly applied approach is the adjustment of mid-upper-arm circumference for skin-
fold thicknesses, with a similar approach being applied less often to the calf.30 Whilst
this approach tends to overestimate muscle area relative to radiographic measure-
ments44, it is sufficient for identifying broad sex differences in relation to age. Such
studies indicate relatively close similarity between the sexes until the beginning of pu-
berty, when males gain substantially more muscle area, particularly in the arm but also
in the leg.45 These dimorphisms appear consistent across ethnic groups in both chil-
dren and adults, despite within-sex ethnic differences.30,45
More recent radiographic imaging studies are consistent with the larger anthropo-
metric literature. Taking into account the influence of peak height velocity, muscle
widths in the arm and calf were similar in UK boys and girls until 14–15 years,
when boys increased in both parameters but especially in the arm.46 In contemporary
populations, this sex difference may emerge earlier due to the trend towards earlier
sexual maturation in girls. However, more sophisticated techniques reveal a significant
dimorphism in muscle mass prior to puberty. In a study using computed tomography
(CT) scanning of children 5–10 years of age closely matched for age, weight and height,
approximately 10% greater muscle mass was observed in boys.17 This finding requires
confirmation in non-white ethnic groups, and there is a need for more data on the de-
velopment of muscle mass.
Other radiographic imaging studies using DXA, CT, MRI or ultrasound consistently
indicate that adult sex differences in arm muscle mass exceed those in the leg.47–51
However, one study suggested that whereas the arm dimorphism persists after adjust-
ment for stature, that in the thigh does not.48 Collectively, these studies support the
concept of greater muscularization of the upper body in men compared to women,
with this difference representing a secondary sexual characteristic.

Fat

As discussed above, sexual dimorphism in regional fatness is clearly evident in body

shape. However, radiographic imaging techniques are now revealing with greater
sophistication these differences in fat distribution, and are highlighting for example sig-
nificant differences in subcutaneous versus internal adipose tissue. Fat can be differen-
tiated into essential fat and storage fat.52 Essential fat, located in bone marrow, the
heart, lungs, liver, kidneys, intestines, muscles and central nervous system, comprises
around 3% of body mass in men and 9% in women.52 It comprises both triglycerides
and other compounds such as phospholipids, and is considered higher in women due
to fat located in the breast and pelvic region. Storage fat comprises around 12% and
15% of body mass in men and women, respectively.52
Sex differences in the distribution of adipose tissue have been known for decades
through simple measures of skin-fold thickness, and waist and hip girths. Typically, such
data are expressed in the form of ratios, for example the waist/hip ratio or the ratio of
central to peripheral skin-fold thicknesses. Such differences are already apparent at
birth: for example, the ratio of triceps þ biceps/subscapular þ suprailiac is around 3%
greater in females compared to males.3 Further studies consistently demonstrate
that skin-fold ratios diverge markedly between the sexes at puberty53,54, with these
 Author's personal copy
Sexual dimorphism of body composition 421

differences maintained into the fifth decade of life (see Figure 2). These differences can
be attributed to a tendency for increased peripheral fat accumulation in females but
not males, with this pattern reported in all the major ethnic groups.30 Data on the
waist/hip ratio likewise show marked sex differences, being consistently greater in
males, especially in early adulthood. These differences are generally conceptualized
as android (upper body, trunk) versus gynoid (hip and thigh) distributions of adipose
tissue.
Nevertheless, the validity of skin-fold ratios for assessing regional adiposity in indi-
viduals has been criticized. At later ages, large data sets demonstrate a non-linear
relationship between central and peripheral skin-fold thicknesses, indicating that vari-
ability in the ratio is an unreliable index of relative central fat distribution.5 This issue
may likewise influence between-sex comparisons due to differing body proportions.
Furthermore, more sophisticated measurement techniques are now capable of dis-
cerning internal non-subcutaneous adipose tissue, demonstrating that skin-fold ratios

80
Boys
Sum of four skinfolds (mm)

70 Girls

60

50

40

30

20
0 2 4 6 8 10 12 14 16 18 20
Age (years)
Ratio of trunk to peripheral skinfolds

1.6
Boys
1.4 Girls

1.2

1.0

0.8

0.6

0.4
0 2 4 6 8 10 12 14 16 18 20
Age (years)

Figure 2. Developmental patterns of subcutaneous fatness, assessed using the ratio of central to peripheral
skin-fold thicknesses. The data illustrate marked differences in fat distribution only emerge with puberty;
however, the magnitude of the difference may be confounded by sex differences in size and physique.53
 Author's personal copy
422 J. C. K. Wells

provide an incomplete picture of sex differences in adiposity. Thus, while there is little
doubt that puberty is associated with significant regional differences in fat distribution
between males and females, more subtle differences can be discerned at younger age
groups and the process of ageing is likewise associated with more complex effects.
Comparisons of regional fatness by DXA demonstrate substantially increased fat
mass in females in the limbs, but a much smaller increase in the trunk (see Figure 3).55
These authors adjusted the sex differences for body weight, and reported the persis-
tence of increased leg fatness in women, but a lack of significant differences for the arm
and the trunk. As discussed above, it would be more appropriate to adjust sex differ-
ences for stature rather than weight, given that fat mass is a component of weight. Few
studies of body composition address size adjustment appropriately, and further inves-
tigations of this issue are required in both adults and children.
Several studies have assessed visceral versus subcutaneous adiposity in the abdo-
men using MRI or CT scanning. These studies collectively indicate the emergence of
increased visceral adiposity in males during adolescence, with this difference increasing
through adulthood56–59, but the magnitude of these dimorphisms may be confounded
by differences in body size. Using MRI scanning, Kuk and colleagues60 found that, for
a given waist circumference, there were significant sex differences in the total amount
of adipose tissue in the abdomen, and in its visceral and subcutaneous components.
Whereas women had greater subcutaneous fat, men had significantly greater visceral
fat, with this sex difference increasing at larger waist circumference. Thus differences
in regional adiposity must be distinguished from differences in waist circumference per
se. In general, males show greater accumulation of visceral fat with age than women;
however, this difference decreases when older men are compared with postmeno-
pausal women.61

30

20
% Difference

10

-10

-20
Leg lean

Trunk lean

Leg fat

Trunk fat

Arm bone

Leg bone

Trunk bone
Arm lean

Arm fat

Figure 3. Regional body composition data obtained in 120 adults using dual energy x-ray absorptiometry
(DXA). Adjusting for body size, women have similar amounts of lean mass in the legs and trunk, but around
10% less than men in the arms. They have a similar amount of fat in the trunk, but around 10% more in the
arms and 30% more in the legs. They have a similar amount of bone mineral in the leg, but around 10% more
in the trunk and 20% less in the arm.55
 Author's personal copy
Sexual dimorphism of body composition 423

Few high-quality studies are available on fat distribution at younger ages. However
in a study of prepubertal children matching for age, weight and height, visceral fat was
similar between the sexes, whereas girls had significantly greater subcutaneous and
total fat mass.17

Bone

Regional bone characteristics show negligible sex differences prior to adolescence.

Bone mineral content in the limbs and trunk is consistent between the sexes up until
around 16 years of age.62 However, from around this age significant sex differences in
bone mineral content emerge in all body regions27,63, with the increased mineral mass
of males being especially apparent in the appendicular skeleton. Consequently, adult
males have a smaller proportion of total bone mineral mass in the head.
During puberty the two sexes diverge both in their growth patterns and in the ef-
fects of these patterns on bone maturation. Boys enter puberty approximately 2 years
later than girls, and continue the pubertal growth spurt for approximately 1 year lon-
ger.4 The effect of this is to increase size dimorphism and leg length, with significant
effects on bone size and hence total bone mass. In boys, puberty stimulates periosteal
apposition but not endocortical expansion, and hence increases bone diameter, corti-
cal thickness and medullary diameter, particularly in the extremities.6 Oestrogen
inhibits periosteal apposition but stimulates endocortical bone formation, hence in
girls increasing cortical thickness occurs with a decrease in medullary diameter and
little increase in periosteal diameter.6 The combination of these effects results in sig-
nificant gender differences in bone strength from puberty onwards. Because of the
contrasting effects of puberty in the two sexes, the influence of delayed puberty like-
wise differs between the sexes, and leads to reduced bone size in boys but normal or
larger bone size in girls.6
The age-associated loss of bone mineral content is greater in females than males in
all skeletal regions, but the magnitude of this difference varies by skeletal site, being
greatest in the spine and pelvis.64

HORMONAL CONTRIBUTIONS

The major contribution of pubertal development to the aetiology of sexual dimor-

phism in body composition can be attributed to the effects of sex hormones acting
during this period. The endocrine event termed adrenarche represents an increase
in the secretion of adrenal androgen hormones which produce an acceleration in
growth in height, a transient acceleration of bone maturation, and the development
of secondary sexual characteristics and fat distribution.4 Sex steroid hormones like-
wise play important roles in the accumulation, metabolism and distribution of adipose
tissue: for example, testosterone and oestrogen facilitate fat deposition in the abdom-
inal and gluteo-femoral regions respectively.52 However, the effects of oestrogen may
be mediated by androgen levels, and lipoprotein lipase may also contribute to sex dif-
ferences in fat distribution. Testosterone is also important for the increase in lean mass
that occurs during puberty, especially in boys.4 Whilst sex steroid hormones exert
their strongest effects during puberty, there is growing evidence that exposure to
them in fetal life may have long-term effects on phenotype. Studies using the ratio
of second to fourth digit as a proxy for fetal exposure to sex hormones have shown
 Author's personal copy
424 J. C. K. Wells

associations between this ratio and markers of android fat distribution in

adulthood.65,66
Sex hormones – especially oestrogen – are of particular importance in the devel-
opment of bone mass. Oestrogen acts to conserve bone mass, suppress bone turn-
over, and maintain balanced rates of bone formation and bone resorption, whilst
also influencing the functional activity of bone cells.67 In turn, testosterone reduces
bone resorption and increases periosteal apposition of bone. The contrasting effects
of these hormones during puberty largely account for the larger skeletal size achieved
by the male. Puberty involves increases in the gonadal secretion of sex steroids which
act in coordinated fashion to support the pubertal growth spurt.67 Of these, serum
oestrogen is particularly important: firstly for initiating the growth spurt, and secondly
for bringing it to an end by inducing epiphyseal closure.67 Testosterone also contrib-
utes, but fails to exert its effects in the absence of oestrogen. Recent studies suggest
that the loss of bone begins well before menopause, and the latter event simply accel-
erates the process due to the associated decline in sex steroid levels.67
As adulthood progresses, sex steroid levels decline due to an increase in sex-hor-
mone binding proteins which reduce the concentration of the free form.6 These de-
clines influence both lean mass and bone. Overall, the menopause is associated with
a 90% increase in bone resorption but only a 45% increase in bone formation68, leading
to an acceleration in bone loss in women, particularly on the endosteal surface. This is
followed by a slower phase of bone loss, probably due to age-related abnormalities in
calcium homeostasis, which also occurs in elderly men.67 Indeed, recent studies sug-
gest that declining testosterone levels with ageing exert their own influence on
bone loss in men.67
Adipose tissue contains receptors for oestrogen, androgens and progesterone;
however, the expression of these receptors differs between visceral and subcutaneous
depots.69 Androgen receptors are more dense in visceral tissue in both males and fe-
males, whereas oestrogen receptors are reduced in visceral tissue in males but not
females. Oestrogen is strongly implicated in the increased fatness and gynoid fat dis-
tribution of females, and the cessation of gonadal oestrogen production at menopause
is associated with the emergence of a more android fat distribution.69
The sexes also differ significantly in circulating leptin concentrations. Some of this
difference can be attributed to sex differences in fat distribution; however, even within
specific adipose tissue depots, the expression of leptin is greater in women.69 Leptin
plays an important role in female reproductive function, signalling the availability of
energy for conception, and also contributes to the regulation of satiety. It is now
thought that circulating concentrations of gonadal steroids mediate the sex difference
in the association between leptin and fat mass.

GENERAL HEALTH IMPLICATIONS

Sex differences in body composition have various implications for health and the risk
of disease. In many cases both sexes illustrate consistent relationships between body
composition phenotype and health outcome. Abdominal fat is generally considered the
most harmful adipose tissue depot. Recent studies have attributed high metabolic ac-
tivity to visceral fat in particular, suggesting that such activity is associated with cardio-
vascular damage and perturbations in blood sugar control. Consequently, the android
pattern of fat distribution is associated in men and women with an increased risk of
cardiovascular disease, type 2 diabetes, and certain cancers, and hormone replacement
 Author's personal copy
Sexual dimorphism of body composition 425

therapy in women and testosterone therapy in men can be used to reduce central obe-
sity and therefore decrease these risks.70,71
However, dimorphism in circulating leptin concentrations is not accounted for by
differences in adipose tissue distribution69, suggesting a sex-specific association medi-
ated by hormonal levels. The association between total and central adiposity and
markers of infection is likewise stronger in women than in men72, whereas increases
in body fat are more strongly associated with insulin sensitivity in men.73
A variety of techniques is now available for body composition assessment in all age
groups74, and reference data are increasingly available. Body composition evaluation
requires appropriate adjustment for size in order to differentiate tissue masses and
distributions from size and physique.75 Even simple approaches are valuable, and mea-
surements of regional body composition may offer the best indication of health
status.74

SEX CHROMOSOME DEFECTS AND OTHER DISORDERS OF

SEX DEVELOPMENT

Individuals with sex chromosome defects or other disorders of sex development show
significant abnormalities of body composition. These are due in part to abnormalities
in sex hormone profile, but may also be influenced by other consequences of chromo-
somal abnormality.
Individuals with Klinefelter syndrome have an extra X chromosome but live as men.
The extra X chromosome is associated with reduced testosterone levels during pu-
berty, resulting in low levels of lean mass and bone density, and a predisposition to
truncal obesity.76,77 Tall height and female breast development may also occur. The
body composition abnormalities contribute to a major increase in risk of the metabolic
syndrome, although not high blood pressure. Testosterone treatment can at least par-
tially address these issues77 and predisposes to normal bone health if conducted
appropriately.
Individuals with Turner syndrome are females who lack one X chromosome. This
abnormality is associated with reduced height and lean mass, and poor development
of the ovaries and breasts, while total and visceral fat are increased.78 Treatment
with oestrogen and growth hormone is used to resolve the deficit in height and nor-
malize body composition. Such treatment does not appear to exert detrimental effects
on bone health.79 Once again, the syndrome is associated with a major increase in the
risk of cardiovascular disease, the enhanced visceral fat being considered to be an im-
portant underlying mechanism.78
Ovarian hyperandrogenism occurs in girls with polycystic ovary syndrome. The
masculinizing hormones predispose to insulin resistance and high levels of truncal
fat80, which again greatly increases risk of the metabolic syndrome.81 Treatment in-
volves a variety of approaches to androgen reduction, along with weight loss to ad-
dress the truncal fat.
A variety of other disorders of sex development impact on the ratio of fat to lean,
and on fat distribution, largely through disorders of hormonal regulation. In addition to
their effects on cardiovascular disease risk, such abnormalities in body composition
have implications for gender identity and reproductive function. Whereas in many con-
ditions gender can be readily ascribed and treatment addresses physiological symp-
toms, in some conditions – such as androgen insensitivity syndromes – gender itself
is ambiguous, and gender assignment is a component of management. Diagnosis is
 Author's personal copy
426 J. C. K. Wells

often difficult, and may involve a variety of approaches, including karyotyping, hor-
monal assessments and abdomino-pelvic imaging. Recent attempts to clarify the clas-
sification of disorders of sex development by differentiating between chromosomal
and hormonal bases82 may improve understanding of the effects of these different bi-
ological levels on body composition and its development. Such knowledge may then
improve the sensitivity with which hormonal treatments can be matched to individual
patients’ phenotypes.

EVOLUTIONARY PERSPECTIVE

Sexual dimorphism in any trait poses the question of what selective pressures might
account for the differences. In the case of body size, for example, we might ask
whether selection has favoured bigger males or smaller females. In general there is
very little difference between males and females in any given species in birth weight.83
Typically, dimorphism emerges just before sexual maturity, with the larger sex demon-
strating either a more rapid growth, or an extension of the growth phase during this
period.83 Whilst larger male size may be relevant to male–male competition, reduced
female size may be relevant to the high energy costs of lactation. In most other spe-
cies, further dimorphisms in body fatness are small or absent.52
Humans therefore differ from other species in demonstrating a profound dimor-
phism in adult body composition that begins to emerge from fetal life onwards. In pri-
mates in general, detailed consideration of the relationship between brain and body
size dimorphism suggests that selection has favoured reduced body size in females,
rather than increased body size in males.52 This would be consistent with the high en-
ergy costs of the large primate brain, which are paid for primarily by the mother
through lactation. In humans, the ratio of brain volume to body size is the greatest
in any primate. These characteristics result in the brain dominating energy require-
ments during early life, which is also the period during which energy requirements
are met by maternal metabolism. High levels of body fatness in adolescent females
and young adult women can therefore be attributed to the high energy demands of
lactation24, whereas the additional lean mass of men, which is only acquired around
17 years of age, is associated with greater physical work capacity.4
In addition to their reproductive implications, the sex differences in body compo-
sition have other functional implications. The greater body fatness of women confers
on them significantly greater capacity to survive famine conditions, as is evident from
studies of wartime Europe.52 Body composition also plays a key role in sexual selec-
tion. Female fat distribution is signalled by the waist/hip ratio. Recent studies have
shown firstly that this ratio distinguishes menstruating, premenarchal, pregnant and
postmenopausal women84, and that those with a lower waist/hip ratio find it easier
to conceive.85 Men in all cultures appear attracted to a low waist/hip ratio, whereas
women favour low levels of body fat in men which reveal male physique.84

CONCLUSIONS

Humans demonstrate significant sexual dimorphism in body composition in relation to

lean, fat and bone masses, a scenario that appears relatively unusual in the animal king-
dom. The sex differences can be attributed to profound differences in reproductive
strategy, which in turn stem from the disproportionate contribution of females to
the nutritional requirements of the large brain in human offspring. In contemporary
 Author's personal copy
Sexual dimorphism of body composition 427

populations, these sex differences have implications for the relationship between
weight status and the risk of diseases such as heart disease, type 2 diabetes, hyperten-
sion, cancers and osteoporosis. Females tolerate higher levels of body fat due to a less
central fat distribution, but are at greater risk of obesity due to an increased propen-
sity to gain fat. Disorders of normal sex development exert significant effects on body
composition and tend to be associated with major increases in risk of the metabolic
syndrome.
Future research is likely to elucidate in greater detail the ontogenetic development
of body composition, and sex differences in this process. Future studies should also
direct greater attention to non-Western populations, since body composition is sen-
sitive to both ethnic genetic factors and ecological conditions, and sexual dimorphisms
are predicted likewise to vary according to circumstances.

Practice points

 sex differences in body composition are present very early in life but emerge
most dramatically during puberty
 a variety of techniques is now available for assessment of paediatric body com-
position, and age- and sex-specific reference data are also emerging
 evaluation of body composition requires appropriate adjustment for body size,
particularly when addressing the period of pubertal development

Research agenda

 ethnic variability on body composition requires further attention, particularly

in relation to reference data
 more research is required on regional body composition and body shape,
which show the strongest association with disease risk
 inadequate attention has been directed to lean mass, which is emerging as an
important health outcome independent of adiposity

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