Original Research Article

Ontogenetic Changes in Intralimb Proportions in a Romano-Christian Period

Sample from the Dakhleh Oasis, Egypt
MICHELE M. BLEUZE,
1
* SANDRA M. WHEELER,
2
LANA J. WILLIAMS,
2
AND TOSHA L. DUPRAS
2
1
Department of Anthropology, The University at Albany, State University of New York, Albany, New York 12222
2
Department of Anthropology, University of Central Florida, Orlando, Florida 32816
ABSTRACT: Objectives: The purpose of this study is to document the appearance of adult patterns in intralimb
indices during ontogeny in a skeletal sample from the Kellis 2 cemetery, Dakhleh Oasis, Egypt. In addition, this study
explores evolvability in intralimb indices to understand relative differences in sensitivity to ecogeographic variables.
Methods: Brachial and crural indices were compared across age cohorts with Welchs ANOVA tests and post-hoc
Dunnett-Tukey-Kramer (DTK) pairwise multiple comparison tests. Spearmans rank correlation coefcients were used
to examine developmental conservation and evolvability in intralimb proportions.
Results: Brachial and crural indices are greatest in the fetus/perinate cohort as compared to all other cohorts,
decrease during infancy and early childhood, and increase during middle/late childhood. The adult pattern in the
brachial index is rst evident in infancy, but is not maintained throughout development. Conversely, the adult pattern
in the crural index appears during early childhood and is maintained throughout development. The brachial index
shows a higher degree of evolvability than the crural index in utero.
Conclusions: The shifting pattern in intralimb proportions during development in the Kellis 2 sample is similar to
that previously reported from globally diverse samples, which likely reects the differential growth acceleration of proxi-
mal and distal intralimb skeletal elements during ontogeny. The brachial index may be more responsive to climatic condi-
tions while the crural index may be more conserved due to functional demands. The data indicate that Kellis 2 juveniles
were under strong selective pressures from climatic factors. Am. J. Hum. Biol. 26:221228, 2014. VC
2014 Wiley Periodicals, Inc.
Several studies have shown that ecogeographic varia-
tion in adult human relative limb length generally follows
Allens rule where cold-adapted, high latitude populations
tend to display relatively shorter limb lengths as com-
pared to warm-adapted, low latitude populations (Allen,
1877; Fukase et al., 2012; Holliday and Hilton, 2010;
Kurki et al., 2008; Ruff, 1994; Temple et al., 2008; Wein-
stein, 2005). Decreasing limb length minimizes the sur-
face area to body mass ratio, which conserves heat and is
advantageous in cold climates, while increasing limb
length maximizes the surface area to body mass ratio,
which aids in heat dissipation (Ruff, 1994; Schreider,
1951).
Although environmental conditions (e.g., poor nutri-
tion) may negatively impact limb length, intralimb pro-
portions still maintain a fairly strong correlation with
latitude and mean annual temperature (Ruff, 1994; Trin-
kaus, 1981). The maintenance of intralimb proportions
along a latitudinal gradient despite suboptimal nutri-
tional conditions suggests intense selective pressures
operating on this aspect of skeletal morphology. While
variation in adult intralimb proportions has been well
studied among geographically diverse populations, varia-
tion in intralimb proportions during ontogeny is less clear.
The few published studies on ecogeographic patterning in
juveniles [(the term juvenile is used throughout this
study as a general term referring to nonadult individuals
14.9 years of age and younger (Scheuer and Black,
2000a)] suggest that population-specic intralimb propor-
tions are present very early in ontogeny, intralimb propor-
tions are genetically conserved, and correlations between
latitude and intralimb proportions are just as strong in
juveniles as they are in adults (Cowgill et al., 2012; Frelat
and Mittereocker, 2011; Temple et al., 2011; Warren et al.,
2002).
Changes in intralimb proportions during ontogeny have
been linked to allometric changes in somatic growth (Fre-
lat and Mittereocker, 2011; Temple et al., 2011). For
instance, the greater growth velocity in intralimb proxi-
mal elements relative to distal elements during early and
middle childhood, and the deceleration in proximal ele-
ments relative to distal elements in utero, infancy, and at
the onset of puberty (Buschang, 1982; Schultz, 1923;
Smith and Buschang, 2004, 2005) likely explain the lower
brachial and crural indices in children as compared to
fetuses, infants, and adolescents (Cowgill et al., 2012).
Despite proportional changes during development,
juveniles must still maintain appropriate ecogeographic
intralimb proportions for their given environment since
they are vulnerable to thermal stress. Mortality during
infancy and early childhood can routinely be attributed to
exposure to extreme temperatures (Bissinger and Anni-
bale, 2010; Thomas, 1994; Wells and Cole, 2002). Indeed,
the vulnerability of very young individuals to thermal
stress may be related to their underdeveloped thermoreg-
ulatory system, large surface area to body mass ratio, and
relatively large head, which promotes signicant heat loss
through radiation (Price and Gwin, 2007; Rowland, 2008;
Contract grant sponsor: Social Science and Humanities Research Coun-
cil; Contract grant number: 501603-0500; Contract grant sponsors: the
Department of Anthropology, Western University, SSHRCC, and the CRC
of Canada.
*Correspondence to: Dr. Michele Bleuze, Department of Anthropology,
The University at Albany, State University of New York, 1400 Washington
Ave., Albany, NY 12222. E-mail: mbleuze@albany.edu
Received 15 June 2013; Revision received 20 December 2013; Accepted
27 December 2013
DOI: 10.1002/ajhb.22505
Published online in Wiley Online Library (wileyonlinelibrary.com).
VC
2014 Wiley Periodicals, Inc.
AMERICAN JOURNAL OF HUMAN BIOLOGY 26:221228 (2014)
Sinclair and Dangereld, 1998). Infants and young chil-
dren must rely on different physiological mechanisms to
thermoregulate than adults. For instance, vasoconstric-
tion and vasodilation are relatively well developed in
infants allowing them to redirect the distribution of heat
from the core to the periphery and vice versa (Adamsons
and Towell, 1965; Hackman, 2001). Thermoregulation in
children is more efcient than in neonates and infants,
but less efcient than in adults. Children can dissipate
heat via sweating, but their sweat glands are smaller and
produce less sweat per gland than adults (Falk, 1998).
The high surface area to body mass ratio in children how-
ever, enables them to lose dry heat via radiation (Falk,
1998; Rowland, 2008).
Thermoregulation in utero is also critical. Although
subcutaneous fat is rst laid down in the fetus at 34
weeks gestation and continues to increase until reaching
a peak at 9 months after birth, a fetus cannot generate
heat via nonshivering thermogenesis (NST) because the
thermogenic capacity of brown adipose tissue remains low
throughout gestation (Symonds and Lomax, 1992; Tanner,
1990). Furthermore, adenosine and prostaglandin E2
from the placenta inhibit NST in the fetus (Asakura,
2004). Instead, heat is generated via metabolic processes
heavily dependent on the availability of oxygen from the
mother (e.g., an increase in oxygen consumption leads to
an increase in heat production) (Adamsons and Towell,
1965; Asakura, 2004; Laburn et al., 2002). A fetus dissi-
pates heat mainly via umbilical circulation, but heat is
also lost through the skin to the amnion (Asakura, 2004).
It is crucial for a fetus to dissipate heat since hyperther-
mia may lead to temperature induced cellular and genetic
effects, which impede fetal growth and development (Asa-
kura, 2004; Gericke et al., 1989).
While body proportions and thermoregulatory mecha-
nisms are changing throughout development, juveniles
must still maintain appropriate ecogeographic intralimb
proportions for their given environment since they are
under selective pressures from climate (Cowgill et al.,
2012). An examination of ontogenetic changes in intra-
limb proportions will help clarify when and how the adult
morphology is eventually attained.
This study examines brachial and crural indices in a
large ontogenetic skeletal sample (fetal through adult)
from the Kellis 2 cemetery, Dakhleh Oasis, Egypt to inves-
tigate ecogeographic morphology during development. It
has been shown that changing patterns in intralimb pro-
portions during ontogeny (at least up until puberty)
reect human growth patterns in intralimb proximal and
distal skeletal element lengths (Frelat and Mittereocker,
2011; Temple et al., 2011). We expect shifting patterns in
intralimb proportions during ontogeny in the Kellis 2
sample to match patterns found in other populations.
That is, intralimb proportions are expected to be greatest
in infancy, decline during early childhood, and increase
again at the onset of puberty. Given the extreme climatic
conditions in the Dakhleh Oasis, the less efcient thermo-
regulatory mechanisms in juveniles as compared to
adults, and evidence suggesting that intralimb propor-
tions are genetically conserved, adult patterns in brachial
and crural indices are expected to be present in early
ontogeny and maintained throughout development. We
will also explore developmental conservation and evolv-
ability in juvenile intralimb proportions. The term
evolvability has multiple meanings in evolutionary
developmental biology, but in this study evolvability
refers to the ability of random variations to produce new,
heritable phenotypes, which can then be the targets of
selection (Houle, 1992; Wagner and Altenberg, 1996). If
intralimb proportions show a high degree of evolvability,
then this would suggest that the ability to evolve ecogeo-
graphic morphologies (i.e., brachial and crural indices) is
under selection. The large sample of fetuses will allow
pre- and postnatal comparisons, which will add to the cur-
rent data documenting ecogeographic patterns in
juveniles.
MATERIALS AND METHODS
The Dakhleh Oasis (25

31N, 28

57E) is located in the

Western Desert of Egypt 550 km south-southwest of
Cairo (Fig. 1). The Western Desert experiences excep-
tional uctuations in seasonal temperatures throughout
the year. Winter temperatures average near or slightly
below freezing before sunrise and 20

to 25

C by mid-
day; and, summer temperatures average 19

C in the
evening and between 40

and 50

C by midday (Giddy,
1987; Sutton, 1950). Mean annual rainfall (0.3 mm/year)
and humidity are moderately low in the Oasis (Dupras
and Schwarcz, 2001; Sutton, 1947). These climatic condi-
tions are very similar to those during the Romano-
Christian period from which the Kellis 2 cemetery sample
derives, although precipitation in the Oasis was greater
during the Romano-Christian period than today (Giddy,
1987; Stewart et al., 2003).
The arid conditions, low acidity of the soil in the West-
ern Desert, and the consistent mortuary practices
observed within the Kellis 2 cemetery have created ideal
conditions for the exceptional preservation of skeletal
remains, including the preservation of fetal and perinate
individuals. Archaeological evidence from the associated
ancient village of Kellis suggests occupation from AD 50
360 (Hope, 2003); however, numerous radiocarbon dates
from the Kellis 2 cemetery indicate use between AD 100
and 450 (Stewart et al., 2003). At present, 770 individuals
of an estimated 30004000 burials have been excavated,
and of those 725 have been analyzed. Approximately 35%
of the recovered individuals are adults, while the remain-
ing 65% are juveniles (Wheeler, 2009). The mortality pro-
le at Kellis 2 is similar to that expected in a natural
mortality distribution in preindustrial populations
(Tocheri et al., 2005). This study utilizes a cross-sectional
sample of 301 individuals spanning the fetal/perinate
through adult years (Table 1).
Skeletal measurements
Standard skeletal metrics were collected from all indi-
viduals as part of the basic osteological data collection
procedures of the Dakhleh Oasis Project Bioarchaeology
Research Team. A subset of skeletal measurements used
to calculate intralimb proportions was selected for this
study. Data from left-sided elements were examined; how-
ever, right-sided elements were included when the left
side was missing or damaged. Unilateral analyses are
deemed appropriate in this study since ecogeographic pat-
terns in intralimb proportions are likely to affect the body
symmetrically. However, it should be noted that bilateral
asymmetry in limb long bone lengths exists in utero, but
differences between left-sided and right-sided elements
are not statistically signicant (Bagnall et al., 1982).
222 M.M. BLEUZE ET AL.
American Journal of Human Biology
Maximum lengths for the major long bones in the upper
and lower limbs have also been found to show low levels of
bilateral asymmetry in a large, geographically and tempo-
rally diverse sample of modern humans (Auerbach and
Ruff, 2006). Maximum diaphyseal lengths for the
humerus (HL), radius (RL), femur (FL), and tibia (TL)
were measured in individuals with unfused proximal and
distal epiphyses to the nearest tenth of a millimeter using
digital sliding calipers, or to the nearest millimeter using
a standard osteometric board. Maximum bone lengths for
the same four long bones were measured in individuals
with fused proximal and distal epiphyses to the nearest
millimeter using a standard osteometric board following
standard long bone measurement protocols (Buikstra and
Ubelaker, 1994). Maximum bone lengths were converted
to maximum diaphyseal lengths to maintain consistency
in comparing juvenile and adult data (Ruff, 2007). Brach-
ial and crural indices were derived from the maximum
diaphyseal lengths following standard formulae: brachial
index 5maximum radius length/maximum humerus
length 3 100; and, crural index 5maximum tibia length/
maximum femur length 3 100.
Sex and age estimation
Reliable estimations of sex in juvenile skeletal remains
are problematic; therefore, sex estimation was not
attempted for the juvenile sample (Scheuer and Black,
2000a,b). This may limit interpretations of the data since
there are known sex differences in limb long bone growth
velocities and timings, which may ultimately contribute
to sex differences in adult intralimb proportions
(Buschang, 1982; Holliday, 1999; Smith and Buschang,
2004, 2005).
Fig. 1. Map of Dakhleh Oasis and the Kellis 2 site, Egypt.
TABLE 1. Samples
Age cohort Age range N brachial N crural
Fetal/Perinate 941 weeks
a
24 23
Infant 0.00.9 year 62 69
Child 1 (C1) 1.04.9 years 30 34
Child 2 (C2) 5.010.9 years 15 16
Child 3 (C3)
b
11.014.9 years 4 3
Adult female 15.01 years 89 87
Adult male 15.01 years 64 69
Total 288 301
a
While the fetal cohort includes individuals beginning at nine weeks gestation
(Scheuer and Black, 2000a), the youngest individuals in this study are estimated
at 24 weeks gestation.
b
Because of the small sample size, the C3 cohort was combined with the C2
cohort. Mean intralimb proportions are not signicantly different between the
groups, and C3 individuals in this study are all aged near the lower end of the
C3 age range (i.e., 11.011.4 years).
ONTOGENETIC CHANGES IN INTRALIMB PROPORTIONS 223
American Journal of Human Biology
The dentition provides the most reliable estimation of
chronological age in juveniles; however, inter- and intra-
population variation in dental formation and eruption
times exist and different dental aging methods have vari-
ous degrees of accuracy depending on the sample popula-
tion (Foti et al., 2003; Liversidge, 1994; Liversidge and
Molleson, 2004; Saunders, 2000; Smith, 1991). Juveniles
in this study were aged using dental calcication tables
(Moorrees et al., 1963a,b; Smith, 1991). Age estimates
were based on macroscopic examinations of the dentition
since radiographic equipment was not available in the
eld. Multiple teeth from each individual were examined
and suggested age and age ranges were based on crown or
root formation. The assigned dental age was recorded as
the mean of all available ages suggested by each tooth.
When dentition was absent, juvenile age estimates were
based on epiphyseal development and fusion, pars basila-
ris morphology, and fusion of cranial elements (Krogman
and Iscan, 1986; Scheuer and Black, 2000a). Fetal and
perinate age was estimated using a combination of basioc-
ciput metrics, development and fusion of cranial ele-
ments, and long bone diaphyseal lengths (Scheuer et al.,
1980; Scheuer and MacLaughlin-Black, 1994; Sherwood
et al., 2000).
Age terminology used to describe juveniles is inconsis-
tent in the literature and often varies depending on the
objectives of the research (e.g., biological, social) (Hal-
crow and Tayles, 2008). In this study, we use the clinical
pediatric/developmental osteology age terminology to
provide a biological basis for comparisons. Fetus
includes individuals aged nine weeks gestation to birth,
perinate is from 24 weeks gestation to seven postnatal
days (or around the time of birth), infant is from birth
to the end of the rst postnatal year (i.e., 0.00.9 year),
and child is from 1.0 to 14.9 years of age (Halcrow and
Tayles, 2008; Scheuer and Black, 2000a,b). The fetus
and perinate cohorts were pooled since age ranges over-
lap in these groups. Since signicant growth and devel-
opmental changes occur during childhood, we further
divided this cohort to examine shifts in intralimb propor-
tions at a ner scale. Child 1 (C1) encompasses the age
range between 1.0 and 4.9 years of age (early childhood),
child 2 (C2) encompasses the age range between 5.0
and 10.9 years of age (middle childhood), and child 3
(C3) encompasses the age range between 11.0 and 14.9
years of age (late childhood). These subdivisions match
important somatic growth spurts and physiological develop-
ments that occur during childhood (Bogin, 1999; Lewis,
2007), and therefore serve as the rationale for further sub-
dividing the childhood cohort. Because of small sample size,
however, individuals in the C3 cohort were combined with
the C2 cohort. Mean intralimb indices are not signicantly
different between the C2 and C3 groups, and the C3 indi-
viduals in this study were all aged closer to the lower end of
the C3 age range (i.e., 11.011.4 years of age).
Sex estimation for adult skeletal remains was based on
standard osteological techniques using morphological fea-
tures in the skull and pelvis (Buikstra and Ubelaker,
1994). Pubic symphysis morphology based on the Suchey-
Brooks method and sternal rib standards were used to esti-
mate age in adults (Brooks and Suchey, 1990; Iscan and
Loth, 1986). In this study, adults are identied based on
full epiphyseal fusion in the humerus and radius, or full
epiphyseal fusion in the femur and tibia.
Statistical analyses
Brachial and crural indices were compared across age
cohorts with Welchs ANOVA tests since the data is nor-
mally distributed, but the assumption of homogeneity of
the variances is violated (McDonald, 2008). Dunnett-
Tukey-Kramer (DTK) pairwise multiple comparison tests
with family-wise error adjusted for unequal variances and
unequal sample sizes were conducted post-hoc to deter-
mine which groups signicantly differed (Lau, 2009).
Adult sexes were analyzed separately since intralimb pro-
portions have been shown to be a sexually dimorphic trait
(Holliday, 1999). Intralimb indices are graphically repre-
sented in box-and-whisker plots (Figs. 2 and 3). The box
represents the interquartile range and the upper and
lower whiskers represent the maximum and minimum
values, respectively. The median is denoted as the line
within the box. Spearmans rank correlation coefcients
(q) with Fishers z-transformations were calculated
between intralimb skeletal elements (i.e., RL vs. HL and
TL vs. FL) in each age cohort to explore developmental
conservation and evolvability in the brachial index and
crural index. Fishers z-transformations were used to cal-
culate 95% condence intervals for the correlation coef-
cients, and dependent t-tests were used to compare
Fishers z-transformations of correlation coefcients in
the upper and lower limbs within each cohort (Sheskin,
2004). A greater correlation between intralimb elements
Fig. 2. Box-plot of brachial index. Means and standard deviations
as follows: fetus/perinate 582.4462.73, infant 579.05 62.48,
C1 576.1561.17, C2/C3577.2062.25, adult female 578.50 62.55,
and adult male 580.2862.53.
Fig. 3. Box-plot of crural index. Means and standard deviations as
follows: fetus/perinate 587.43 61.32, infant 584.87 62.28,
C1 582.5961.52, C2/C3 583.5661.63, adult female 582.94 62.07,
and adult male 583.4362.18.
224 M.M. BLEUZE ET AL.
American Journal of Human Biology
suggests reduced evolvability, while a lower correlation
suggests greater evolvability (Young et al., 2010). Statisti-
cal signicance is set at P<0.05 and all statistical analy-
ses were carried out using R-Studio.
RESULTS
The mean brachial index is signicantly different among
the age cohorts (F5 25.96, P<0.00). It is greatest during
early ontogeny, declines during early childhood, and
increases again during middle/late childhood (Fig. 2). The
fetus/perinate cohort has a signicantly greater brachial
index than all other groups, and the infant cohort has a sig-
nicantly greater brachial index than the C1 cohort. The
brachial index does not signicantly change during child-
hood. Children in the C1 cohort have a signicantly lower
brachial index than female and male adults, while children
in the C2 cohort have a signicantly lower brachial index
than male adults only (Table 2). The adult pattern is rst evi-
dent during infancy, but is not maintained during childhood.
The mean crural index is signicantly different among
the age cohorts (F537.97, P<0.00). It is greatest in the
fetus/perinate cohort, decreases during infancy and early
childhood, and increases, albeit nonsignicantly, during
middle/late childhood (Fig. 3). The fetus/perinate cohort
has a signicantly greater crural index than all other
groups. Infants have a signicantly greater crural index
than the C1 and adult cohorts. The crural index does not
signicantly change during childhood (Table 2). The adult
pattern is rst evident during early childhood and is
maintained from this point forward.
A signicantly lower correlation is observed between RL
and HL as compared to TL and FL in the fetus/perinate
cohort, and a signicantly greater correlation is observed
between RL and HL as compared to TL and FL in the C1
cohort. The correlations between RL and HL as compared
to TL and FL are not signicantly different in the other age
cohorts (Table 3). We pooled our postnatal juvenile sample
(ages 0.011.4 years) in order to compare the Kellis 2 juve-
niles with published data from Jomon period juveniles
(Temple et al., 2011). The correlations between RL and HL
as compared to TL and FL are not signicantly different in
the Kellis 2 sample (z 50.23, P50.81), which contrasts
with results from Temple et al. (2011).
DISCUSSION
The primary objective of this study was to describe
changes in intralimb proportions during development in
the Kellis 2 sample from the Dakhleh Oasis, Egypt. The
adult pattern in the brachial index is rst evident in
infancy, but is not maintained throughout development.
Conversely, the adult pattern in the crural index appears
during early childhood and is maintained throughout
development. Thus, while adult intralimb proportions are
not present in utero they do appear very early in ontogeny.
This lends further support to the long held view that
intralimb proportions are genetically conserved traits
(Holliday, 1999; Schultz, 1923; Temple et al., 2011).
It has been shown that brachial and crural indices dur-
ing ontogeny are strongly correlated with latitude despite
shifting values over the course of development such that
relative ecogeographic patterns among geographically
diverse populations are maintained during development
(Cowgill et al., 2012; Ruff, 2007). In other words, there are
signicant differences in absolute mean brachial and cru-
ral indices among age-matched cohorts across geographi-
cally diverse populations despite similarities in shifting
patterns throughout development. Shifting patterns in
intralimb proportions during ontogeny are often linked to
differences in growth velocities of intralimb proximal and
distal elements (Cowgill et al., 2012; Temple et al., 2011).
In the Kellis 2 sample, the intralimb proportions are
greatest in the fetus/perinate and infant cohorts, decrease
during early childhood, and increase again during middle/
late childhood. Our results are consistent with previous
work and extend the pattern to the fetus/perinate period.
Since hyperthermia in utero may impede fetal growth and
development, high intralimb proportions may be under
strong selective pressures even before postnatal life (Ger-
icke et al., 1989; Xu et al., 2012). During the rst year of
life, intralimb proportions are signicantly lower than in
utero, but signicantly greater than in early childhood.
These results suggest that accelerated growth velocities of
distal elements relative to proximal elements do not carry
over into infancy.
We hypothesized that adult patterns in intralimb indi-
ces would appear early in ontogeny and be maintained
throughout development. This hypothesis is partially sup-
ported by the results. While mean brachial indices are not
signicantly different between infants and adults, chil-
dren have signicantly lower brachial indices than adults
(barring C2 children and adult females). This may reect
the high growth velocity of the humerus relative to the
radius during childhood and adolescence (Smith and
TABLE 2. P-values from Dunnett-Tukey-Kramer pairwise multiple
comparisons post hoc tests
Brachial index
Infant C1 C2 Adult female Adult male
Fetus/perinate 0.00 0.00 0.00 0.00 0.00
Infant 0.00 0.05 0.76 0.13
C1 0.69 0.00 0.00
C2 0.29 0.00
Adult female 0.00
Crural index
Infant C1 C2 Adult female Adult male
Fetus/perinate 0.00 0.00 0.00 0.00 0.00
Infant 0.00 0.93 0.00 0.00
C1 0.06 0.97 0.44
C2 0.11 0.59
Adult female 0.72
TABLE 3. Spearmans rank correlation coefcients
Cohort Comparison q Fisher-z 95% CI z-value P
Fetal/Perinate RL vs. HL 0.909 1.527 0.8640.941 2.09 0.04
TL vs. FL 0.972 2.092 0.9540.980
Infant RL vs. HL 0.973 2.092 0.9510.982 0.71 0.48
TL vs. FL 0.979 2.298 0.9680.988
C1 RL vs. HL 0.989 2.647 0.9780.995 2.57 0.01
TL vs. FL 0.958 1.946 0.9200.980
C2 RL vs. HL 0.956 1.946 0.8970.985 0.50 0.62
TL vs. FL 0.969 2.993 0.9220.989
Adult ($) RL vs. HL 0.822 1.157 0.7380.878 0.10 0.92
TL vs. FL 0.827 1.188 0.7510.886
Adult (#) RL vs. HL 0.794 1.071 0.6750.867 0.03 0.98
TL vs. FL 0.796 1.099 0.6950.872
ONTOGENETIC CHANGES IN INTRALIMB PROPORTIONS 225
American Journal of Human Biology
Buschang, 2004, 2005). It has been demonstrated that the
brachial index is more strongly correlated with mean
annual temperature than the crural index in adults (Trin-
kaus, 1981), and that the brachial index has a stronger
correlation with latitude in adults than in juveniles (Cow-
gill et al., 2012). Since adult patterns in the brachial index
are not maintained during childhood, the results suggest
that selective pressures from climate acting on the brach-
ial index may be weaker in children than in infants and
adults. The high surface area to body mass ratio in chil-
dren, which enables them to lose dry heat, may ease selec-
tive pressures on the brachial index (Falk, 1998;
Rowland, 2008). Adult patterns in the crural index appear
in early childhood and are maintained throughout middle
and late childhood. It is possible that this reects func-
tional constraints placed on the lower limbs (Temple
et al., 2011; Young et al., 2010).
Correlation analyses indicate a signicantly lower cor-
relation between RL and HL (i.e., greater evolvability)
than between TL and FL in the fetus/perinate cohort,
which suggests that the crural index is more genetically
conserved than the brachial index in utero. These results
are in accordance with previous studies suggesting
greater genetic conservation of the crural index as com-
pared to the brachial index in postnatal life (Frelat and
Mittereocker, 2011; Temple et al., 2011). The greater cor-
relation between lower limb elements as compared to
upper limb elements is not maintained throughout devel-
opment. During early childhood, RL and HL have a signif-
icantly greater correlation than TL and FL. Growth rates
of proximal and distal segments are more variable in the
lower limbs as compared to the upper limbs during child-
hood (ages 310 years), which may explain the signi-
cantly greater correlation between RL and HL as
compared to TL and FL in the C1 cohort (Smith and
Buschang, 2004). The high degree of variation in growth
of the tibia is particularly evident during early childhood,
and may further contribute to the signicantly greater
correlation between RL and HL as compared to TL and
FL (Smith and Buschang, 2004). Animal studies have
shown that exercise increases limb length by increasing
the amount of nutritional solute delivery to growth plates
in weight-bearing limb bones (Jurvelin et al., 1988; Serrat
et al., 2007, 2010). Since children in the early childhood
phase are beginning to walk, the lower correlation of TL
and FL relative to RL and HL may reect growth devia-
tions from the biomechanical demands of bipedalism.
Greater variation in growth rates of lower limb elements
as compared to upper limb elements during early child-
hood coupled with lower limb skeletal element elongation
from increased loading due to the start of walking behav-
iors may explain the greater correlation between RL and
HL as compared to TL and FL in the C1 cohort.
It was previously shown that RL and HL have a signi-
cantly lower correlation than TL and FL in a Jomon
period juvenile sample (Temple et al., 2011). Our pooled
Kellis 2 postnatal juvenile sample does not follow this pat-
tern since the correlations between RL and HL as com-
pared to TL and FL are not signicantly different. These
contrasting results may reect differences in sample con-
struction since the Jomon juvenile sample largely con-
sisted of individuals between 2.1 and 10.9 years of age,
while infants (ages 0.00.9) slightly outnumbered chil-
dren (1.011.4 years of age) in the pooled postnatal Kellis
2 juvenile sample.
Given the climatic extremes experienced in the Dakh-
leh Oasis it is not unexpected to nd elevated intralimb
indices in the Kellis 2 juvenile sample. The Kellis 2 sam-
ple is similar to other warm-adapted populations in this
regard. While cross-sample comparisons are approached
with caution because of differences in age cohort construc-
tion, Kellis 2 juveniles have similar mean intralimb pro-
portions as those reported for similarly age-matched
juveniles from Kulubnarti, Upper Nubia (21

N), and Kel-

lis 2 juveniles have lower mean intralimb proportions
than those reported for similarly age-matched juveniles
from Point Hope, Alaska (68

N) (Cowgill et al., 2012).

Seasonal mortality for the Kellis 2 population was
derived using the solar alignment of the graves and iso-
topic analysis of hair (Williams, 2008, Williams et al.,
2011). Fifty-one percent of juvenile graves at Kellis 2 are
aligned with warmer seasons (late March/early April to
August/September), 47% of which are infants (Williams,
2008). Alignment of 38% of fetuses and 46% of perinates
are also represented in this portion of the year (Williams,
2008). This warmer season is associated with sandstorms,
temperature extremes, food shortages, and seasonal infec-
tious disease outbreaks that may have contributed to the
increased juvenile deaths during these times (Alpin, 1980;
Bagnall, 1993; Williams, 2008). The tendency towards
greater fetus and perinate mortality in the warm season
observed at Kellis 2 is comparable to historical and mod-
ern Egyptian rural populations from Upper and Lower
Egypt (Alpin, 1980; El-Nomrosi, 1981; Shaw, 1996). Given
the high mortality rate of Kellis 2 juveniles during the
warm season, it is possible that we are observing a juve-
nile sample with intralimb proportions that were selected
against. An important factor to consider when investigat-
ing a juvenile skeletal sample is that the sample may not
reect the normal, healthy population from which it was
drawn precisely because it is a skeletal sample (Johnston,
1962; Wood et al., 1992). With regard to the Kellis 2 juve-
nile sample, the low to moderate prevalence of physiologi-
cal markers of stress (e.g., cribra orbitalia, enamel
hypoplasia) and the low prevalence of trauma suggest an
overall improvement in health when compared to pre-
Roman populations (Fairgrieve and Molto, 2000) and a
contemporaneous Nubian sample from Kulubnarti
(Wheeler, 2012). In addition, the lack of relationship
between the number of observable skeletal and dental
stressors and growth patterns suggests that physiological
stressors did not negatively affect growth patterns in the
Kellis 2 juveniles (Wheeler, 2009). On the basis of these
ndings, it is reasonable to surmise that growth patterns
in our juvenile sample may not have been appreciably dis-
rupted by the presence of physiological stressors; there-
fore, the sample likely represents a plausible estimate of
true ontogenetic patterns.
While the effects of nutrition and overall health cannot
be ignored in analyses dealing with skeletal growth, it has
been suggested that the negative impact of such factors
(e.g., malnutrition) may have a minimal impact on intra-
limb proportions (Ruff, 1994; Frelat and Mittereocker,
2011). For instance, Pinhasi et al. (2013) found that intra-
limb proportions were not signicantly different in a skel-
etal sample of children from medieval cemeteries in two
regions of Croatia despite nutritional differences between
the groups. Stable isotopic analyses have shown a consist-
ent diet after weaning in the Kellis 2 juvenile sample
(Dupras, 1999; Dupras et al., 2001). Thus, ontogenetic
226 M.M. BLEUZE ET AL.
American Journal of Human Biology
changes in intralimb proportions in the Kellis 2 juvenile
sample are likely not biased by nutritional status.
CONCLUSIONS
This study examined ontogenetic changes in intralimb
proportions in a sample of Romano-Christian period indi-
viduals from the Kellis 2 cemetery, Dakhleh Oasis, Egypt.
Adult patterns in brachial and crural indices are present
early in ontogeny. While adult patterns in the brachial
index are not maintained throughout childhood, the adult
pattern in the crural index is maintained from early child-
hood onwards. Intralimb proportions, especially the cru-
ral index, have a strong developmental component. These
results suggest that, like adults, juveniles are under
strong selective pressures from climatic factors.
Selective pressures acting on human populations are
generally examined among adults despite the fact that
the adult morphology is the end result of biological and
environmental factors occurring throughout development.
Selective pressures and the adaptive signicance of juve-
nile morphology must be examined to better understand
the processes that lead to the adult form.
ACKNOWLEDGMENTS
The authors would like to thank the Egyptian Ministry
of State for Antiquities for their continued support of the
Dakhleh Oasis Project, Anthony Mills for his dedication
to the DOP, and all the members of the Dakhleh Oasis
Bioarchaeology team, especially Dr. Peter Sheldrick. The
authors would also like to thank Dr. J. E. Molto for the
use of the Kellis 2 adult osteometric data and the two
anonymous reviewers for their helpful comments.
LITERATURE CITED
Adamsons K, Towell ME. 1965. Thermal homeostasis in the fetus and new-
born. Anesthesiology 26:531548.
Allen JA. 1877. The inuence of physical conditions in the genesis of spe-
cies. Radical Rev 1:108140.
Alpin P. 1980. La medicine des Egyptiens, 15811584 par Prosper Alpin.
Cairo: Institut Francais deArcheologie Orientale du Cairo.
Asakura H. 2004. Fetal and neonatal thermoregulation. J Nipon Med Sch
71:360370.
Auerbach BM, Ruff CB. 2006. Limb bone bilateral asymmetry: variability
and commonality among modern humans. J Hum Evol 50:203218.
Bagnall KM, Harris PF, Jones PRM. 1982. A radiographic study of the lon-
gitudinal growth of primary ossication centers in limb long bones of
the human fetus. Anat Rec 203:293299.
Bagnall RS. 1993. Egypt in late antiquity. Princeton: Princeton University
Press.
Bissinger RL, Annibale DJ. 2010. Thermoregulation in very low birth-
weight infants during the golden hour. Adv Neonatal Care 10:230238.
Bogin B. 1999. Patterns of human growth. Cambridge: Cambridge Univer-
sity Press.
Brooks S, Suchey JM. 1990. Skeletal age determination based on the os
pubis: a comparison of the Acs adi-Nemeskeri and Suchey-Brooks meth-
ods. Hum Evol 5:227238.
Buikstra JE, Ubelaker DH. 1994. Standards for data collection from
human skeletal remains. Fayetteville: Arkansas Archaeological Survey
Research Series no. 44.
Buschang PH. 1982. Differential long bone growth of children between
two months and eleven years of age. Am J Phys Anthropol 58:291295.
Cowgill LW, Eleazer CD, Auerbach BM, Temple DH, Okazaki K. 2012.
Developmental variation in ecogeographic body proportions. Am J Phys
Anthropol 148:557570.
Dupras TL. 1999. Dining in the Dakhleh Oasis, Egypt: determination of
diet from documents and stable isotope analysis. PhD Dissertation.
Hamilton, Ontario: McMaster University.
Dupras TL, Schwarcz HP. 2001. Strangers in a strange land: stable isotope
evidence for human migration in the Dakhleh Oasis, Egypt. J Archaeol
Sci 28:11991208.
Dupras TL, Schwarcz HP, Fairgrieve SI. 2001. Infant feeding and weaning
practices in Roman Egypt. Am J Phys Anthropol 115:204212.
El-Nomrosi MM. 1981. Analytical study of fertility and mortality tenden-
cies in Egypt during the period 19501980. Pop Studies 59:38.
Fairgrieve SI, Molto JE. 2000. Cribra orbitalia in two temporally disjunct
population samples form the Dakhleh Oasis, Egypt. Am J Phys Anthro-
pol 111:319331.
Falk B. 1998. Effects of thermal stress during rest and exercise in the
paediatric population. Sports Med 25:221240.
Foti B, Lalys L, Adalian P, Giustiniani J, Maczel M, Signoli M, Dutour O,
Leonetti G. 2003. New forensic approach to age determination in chil-
dren based on tooth eruption. Forensic Sci Int 132:4956.
Frelat MA, Mittereocker P. 2011. Postnatal ontogeny of tibia and femur
form in two human populations: a multivariate morphometric analysis.
Am J Hum Biol 23:796804.
Fukase H, Wakebe T, Tsurumoto T, Saiki K, Fujita M, Ishida H. 2012. Geo-
graphic variation in body form of prehistoric Jomon males in the Japa-
nese archipelago: its ecogeographic implications. Am J Phys Anthropol
149:125135.
Gericke GS, Hofmeyr GJ, Laburn HP, Isaacs H. 1989. Does heat damage
fetuses? Med Hypoth 29:275278.
Giddy LL. 1987. Egyptian oases: Bahariya, Dakhla, Farafara and Kharga
during pharaonic times. London: Aris and Phillips Ltd.
Hackman PS. 2001. Recognizing and understanding the cold-stressed
term infant. J Neonat Nurs 20:3541.
Halcrow SE, Tayles N. 2008. The bioarchaeological investigation of child-
hood and social age: problems and prospects. J Archaeol Method Theory
15:190215.
Holliday TW. 1999. Brachial and crural indices of European Late Upper
Paleolithic and Mesolithic humans. J Hum Evol 36:549566.
Holliday TW, Hilton CE. 2010. Body proportions of circumpolar peoples as
evidenced from skeletal data: Ipiutak and Tigara (Point Hope) versus
Kodiak Island Inuit. Am J Phys Anthropol 142:287302.
Hope CA. 2003. The excavations at Ismant el-Kharab from 20002002. In:
Bowen GE, Hope CA, editors. The oasis papers III: the proceedings of
the third international conference of the Dakhleh Oasis Project. Oxford:
Oxbow Books. p 207289.
Houle D. 1992. Comparing evolvability and variability of quantitative
traits. Genetics 130:195204.
Iscan MY, Loth SR. 1986. Estimation of age and determination of sex from
the sternal rib. In: Reichs KJ, editor. Forensic osteology: advances in the
identication of human remains. Springeld: C.C. Thomas. p 6889.
Johnston FE. 1962. Growth of the long bones of infants and young children
at Indian Knoll. Am J Phys Anthropol 20:249254.
Jurvelin J, Lahtinen T, Kiriranta I, Arnala I, Lappalainen R, Tammi M,
Helminen HJ. 1988. Blood ow, histomorphology and elemental compo-
sition of the canine femur after physical training or immobilization.
Acta Physiol Scand 132:385389.
Krogman WM, Iscan MY. 1986. The human skeleton in forensic medicine.
Springeld: Charles C. Thomas.
Kurki HK, Ginter JK, Stock JT, Pfeiffer S. 2008. Adult proportionality in
small-bodied foragers: a test of ecogeographic expectations. Am J Phys
Anthropol 136:2838.
Laburn HP, Faurie A, Goelst K, Mitchell D. 2002. Effects on fetal and
maternal body temperature of exposure of pregnant ewes to heat, cold,
and exercise. J Appl Physiol 92:802808.
Lau MK. 2009. DTK: Dunnett-Tukey-Kramer Pairwise Multiple Compari-
son Test Adjusted for Unequal Variances and Unequal Sample Sizes. R
package version 3.0. http://CRAN.R-project.org/package5DTK.
Lewis ME. 2007. The bioarchaeology of children: perspectives from biologi-
cal and forensic anthropology. Cambridge: Cambridge University Press.
Liversidge HM. 1994. Accuracy of age estimation from developing teeth of
a population of known age (05.4 years). Int J Osteoarchaeol 4:3745.
Liversidge HM, Molleson T. 2004. Variation in crown and root formation and
eruption of human deciduous teeth. AmJ Phys Anthropol 123:172180.
McDonald JH. 2008. Handbook of biological statistics. Baltimore: Sparky
House.
Moorrees CFA, Fanning EA, Hunt EE. 1963a. Age variation of formation
stages for ten permanent teeth. J Dent Res 42:14901502.
Moorrees CFA, Fanning EA, Hunt EE. 1963b. Formation and resorption of
three deciduous teeth in children. Am J Phys Anthropol 21:205213.
Pinhasi R, Timpson A, Thomas M,

Slaus M. 2013. Bone growth, limb pro-
portions and non-specic stress in archaeological populations from Cro-
atia. Ann Hum Biol (early online) 112.
Price DL, Gwin JF. 2007. Pediatric nursing: an introductory text, 10th ed.
St. Louis: Saunders.
Rowland T. 2008. Thermoregulation during exercise in the heat in chil-
dren: old concepts revisited. J Appl Physiol 105:718724.
Ruff CB. 1994. Morphological adaptation to climate in modern and fossil
hominids. Yrbk Phys Anthropol 37:65107.
ONTOGENETIC CHANGES IN INTRALIMB PROPORTIONS 227
American Journal of Human Biology
Ruff CB. 2007. Body size prediction from juvenile skeletal remains. Am J
Phys Anthropol 133:698716.
Saunders SR. 2000. Subadult skeletons and growth-related studies. In:
Katzenberg MA, Saunders SR, editors. Biological anthropology of the
human skeleton. New York: Wiley-Liss. p 135161.
Scheuer JL, MacLaughlin-Black SM. 1994. Age estimation from the pars
basilaris of the fetal and juvenile occipital bone. Int J Osteoarchaeol 4:
377380.
Scheuer JL, Musgrave JH, Evans SP. 1980. The estimation of late fetal
and perinatal age from limb bone length by linear and logarithmic
regression. Ann Hum Biol 7:257265.
Scheuer L, Black S. 2000a. Developmental juvenile osteology. San Diego:
Academic Press.
Scheuer L, Black S. 2000b. Development and ageing of the juvenile skele-
ton. In: Cox M, Mays S, editors. Human osteology in archaeology and
forensic science. New York: Cambridge University Press. p 921.
Schreider E. 1951. Anatomical factors of body-heat regulation. Nature
167:823824.
Schultz AH. 1923. Fetal growth in man. Am J Phys Anthropol 4:389399.
Serrat MA, Lovejoy CO, King D. 2007. Age-and site-specic decline in
insulin-like growth factor-I receptor expression s correlate with differen-
tial growth plate activity in the mouse hindlimb. Anat Rec 290:375381.
Serrat MA, Williams RM, Farnum CE. 2010. Exercise mitigate the stunt-
ing effect of cold temperature on limb elongation in mice by increasing
solute delivery to the growth plate. J Appl Physiol 109:18691879.
Shaw B. 1996. Seasons of death: aspects of mortality in Imperial Rome. J
Rom Studies 86:100138.
Sherwood RJ, Meindl RS, Robinson HB, May RL. 2000. Fetal age: methods
of estimation and effects of pathology. Am J Phys Anthropol 113:305315.
Sheskin DJ. 2004. Handbook of parametric and non-parametric statistical
procedures, 3rd ed. Boca Raton: CRC Press LLC.
Sinclair D, Dangereld P. 1998. Human growth after birth, 6th ed. Oxford:
Oxford University Press.
Smith BH. 1991. Standards of human tooth formation and dental age
assessment. In: Kelley MA, Larsen CS, editors. Advances in dental
anthropology. New York: Wiley-Liss. p 143168.
Smith SL, Buschang PH. 2004. Variation in longitudinal diaphyseal long bone
growth in children three to ten years of age. Am J Hum Biol 16:648657.
Smith SL, Buschang PH. 2005. Longitudinal models of long bone growth
during adolescence. Am J Hum Biol 17:731645.
Stewart JD, Molto JE, Reimer PJ. 2003. The chronology of Kellis 2: the
interpretative signicance of radiocarbon dating of human remains. In:
Bowen GE, Hope CA, editors. The oasis papers 3: proceedings of the
third international conference of the Dakhleh Oasis Project. Oxford:
Oxbow Books. p 373378.
Sutton LJ. 1947. Rainfall in Egypt: statistics, storms, run-off. Cairo: Gov-
ernment Press.
Sutton LJ. 1950. The climate of Egypt. Weather 5:5962.
Symonds ME, Lomax MA. 1992. Maternal and environmental inuences
on thermoregulation in the neonate. Proc Nutritional Soc 51:165172.
Tanner JM. 1990. Fetus into man. Cambridge: Harvard University Press.
Temple DH, Auerbach BM, Nakatsukasa M, Sciulli PW, Larsen CS. 2008.
Variation in limb proportions between Jomon foragers and Yayoi agri-
culturalists from prehistoric Japan. Am J Phys Anthropol 137:164174.
Temple DH, Okazaki K, Cowgill LW. 2011. Ontogeny of limb proportions in
late through nal Jomon period foragers. Am J Phys Anthropol 145:
415425.
Thomas K. 1994. Thermoregulation in neonates. Neonat Network 13:
1525.
Tocheri MW, Dupras TL, Sheldrick P, Molto JE. 2005. Roman period fetal
skeletons from the East Cemetery (Kellis 2) of Kellis, Egypt. Int J Osteo-
archaeol 15:326341.
Trinkaus E. 1981. Neandertal limb proportions and cold adaptation. In:
Stringer CB, editor. Aspects of human evolution. London: Taylor and
Francis. p 187224.
Wagner GP, Altenberg L. 1996. Complex adaptation and the evolution of
evolvability. Evolution 50:967976.
Warren MW, Holliday TW, Cole TM. 2002. Ecogeographical patterning in
the human fetus. Am J Phys Anthropol (Suppl) 117:161.
Weinstein KJ. 2005. Body proportions in ancient Andeans from high and
low altitudes. Am J Phys Anthropol. 128:569585.
Wells JCK, Cole TJ. 2002. Birth weight and environmental heat load: a
between-population analysis. Am J Phys Anthropol 119:276282.
Wheeler SM. 2009. Bioarchaeology of infancy and childhood at the Kellis 2
cemetery, Dakhleh Oasis, Egypt. PhD Dissertation. London, Ontario:
The University of Western Ontario.
Wheeler SM. 2012. Nutritional and disease stress of juveniles from the
Dakhleh Oasis, Egypt. Int J Osteoarchaeol 22:219234.
Williams LJ. 2008. Investigating seasonality of death at Kellis 2 cemetery
using solar alignment and isotopic analysis of mummied tissues. PhD
Dissertation. London, Ontario: The University of Western Ontario.
Williams LJ, White CD, Longstaffe FJ. 2011. Improving stable isotopic
interpretations made from human hair through reduction of growth
cycle error. Am J Phys Anthropol 145:125136.
Wood JW, Harpending HC, Weiss KM, Milner GR. 1992. The osteological
paradox: problems of inferring prehistoric health from skeletal samples.
Curr Anthropol 33:343370.
Xu Z, Etzel RA, Su H, Huang C, Guo Y, Tong S. 2012. Impact of ambient
temperature on childrens health: a systematic review. Environ Res 117:
120131.
Young NM, Wagner GP, Hallgrimmson B. 2010. Development and evolv-
ability of human limbs. Proc Nat Acad Sci USA 107:34003405.
228 M.M. BLEUZE ET AL.
American Journal of Human Biology