Bleuze Et Al Ontogenetic Changes in Intralimb Proportions in a Romano-Christian Period Sample From the Dakhleh Oasis Egypt-libre

Original Research Article

Ontogenetic Changes in Intralimb Proportions in a Romano-Christian PeriodSample from the Dakhleh Oasis, Egypt

MICHELE M. BLEUZE,1* SANDRA M. WHEELER,2 LANA J. WILLIAMS,2 AND TOSHA L. DUPRAS2

1Department of Anthropology, The University at Albany, State University of New York, Albany, New York 122222Department 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 Welch’s ANOVA tests and post-hoc

Dunnett-Tukey-Kramer (DTK) pairwise multiple comparison tests. Spearman’s rank correlation coefficients 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 first 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 reflects 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. 26:221–228, 2014. VC 2014 Wiley Periodicals, Inc.

Several studies have shown that ecogeographic varia-tion in adult human relative limb length generally followsAllen’s rule where cold-adapted, high latitude populationstend 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 isadvantageous in cold climates, while increasing limblength 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 withlatitude and mean annual temperature (Ruff, 1994; Trin-kaus, 1981). The maintenance of intralimb proportionsalong a latitudinal gradient despite suboptimal nutri-tional conditions suggests intense selective pressuresoperating on this aspect of skeletal morphology. Whilevariation in adult intralimb proportions has been wellstudied among geographically diverse populations, varia-tion in intralimb proportions during ontogeny is less clear.The few published studies on ecogeographic patterning injuveniles [(the term “juvenile” is used throughout thisstudy as a general term referring to nonadult individuals14.9 years of age and younger (Scheuer and Black,2000a)] suggest that population-specific intralimb propor-tions are present very early in ontogeny, intralimb propor-tions are genetically conserved, and correlations betweenlatitude and intralimb proportions are just as strong injuveniles as they are in adults (Cowgill et al., 2012; Frelatand Mittereocker, 2011; Temple et al., 2011; Warren et al.,2002).

Changes in intralimb proportions during ontogeny havebeen linked to allometric changes in somatic growth (Fre-lat and Mittereocker, 2011; Temple et al., 2011). Forinstance, the greater growth velocity in intralimb proxi-mal elements relative to distal elements during early andmiddle childhood, and the deceleration in proximal ele-ments relative to distal elements in utero, infancy, and atthe onset of puberty (Buschang, 1982; Schultz, 1923;Smith and Buschang, 2004, 2005) likely explain the lowerbrachial and crural indices in children as compared tofetuses, infants, and adolescents (Cowgill et al., 2012).

Despite proportional changes during development,juveniles must still maintain appropriate ecogeographicintralimb proportions for their given environment sincethey are vulnerable to thermal stress. Mortality duringinfancy and early childhood can routinely be attributed toexposure to extreme temperatures (Bissinger and Anni-bale, 2010; Thomas, 1994; Wells and Cole, 2002). Indeed,the vulnerability of very young individuals to thermalstress may be related to their underdeveloped thermoreg-ulatory system, large surface area to body mass ratio, andrelatively large head, which promotes significant heat lossthrough radiation (Price and Gwin, 2007; Rowland, 2008;

Contract grant sponsor: Social Science and Humanities Research Coun-cil; Contract grant number: 50–1603-0500; Contract grant sponsors: theDepartment of Anthropology, Western University, SSHRCC, and the CRCof Canada.

*Correspondence to: Dr. Michele Bleuze, Department of Anthropology,The University at Albany, State University of New York, 1400 WashingtonAve., Albany, NY 12222. E-mail: [email protected]

Received 15 June 2013; Revision received 20 December 2013; Accepted27 December 2013

DOI: 10.1002/ajhb.22505Published online in Wiley Online Library (wileyonlinelibrary.com).

VC 2014 Wiley Periodicals, Inc.

AMERICAN JOURNAL OF HUMAN BIOLOGY 26:221–228 (2014)

Sinclair and Dangerfield, 1998). Infants and young chil-dren must rely on different physiological mechanisms tothermoregulate than adults. For instance, vasoconstric-tion and vasodilation are relatively well developed ininfants allowing them to redirect the distribution of heatfrom the core to the periphery and vice versa (Adamsonsand Towell, 1965; Hackman, 2001). Thermoregulation inchildren is more efficient than in neonates and infants,but less efficient than in adults. Children can dissipateheat via sweating, but their sweat glands are smaller andproduce 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. Althoughsubcutaneous fat is first laid down in the fetus at �34weeks gestation and continues to increase until reachinga peak at �9 months after birth, a fetus cannot generateheat via nonshivering thermogenesis (NST) because thethermogenic capacity of brown adipose tissue remains lowthroughout gestation (Symonds and Lomax, 1992; Tanner,1990). Furthermore, adenosine and prostaglandin E2from the placenta inhibit NST in the fetus (Asakura,2004). Instead, heat is generated via metabolic processesheavily dependent on the availability of oxygen from themother (e.g., an increase in oxygen consumption leads toan 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 isalso 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 geneticeffects, which impede fetal growth and development (Asa-kura, 2004; Gericke et al., 1989).

While body proportions and thermoregulatory mecha-nisms are changing throughout development, juvenilesmust still maintain appropriate ecogeographic intralimbproportions for their given environment since they areunder selective pressures from climate (Cowgill et al.,2012). An examination of ontogenetic changes in intra-limb proportions will help clarify when and how the adultmorphology is eventually attained.

This study examines brachial and crural indices in alarge ontogenetic skeletal sample (fetal through adult)from the Kellis 2 cemetery, Dakhleh Oasis, Egypt to inves-tigate ecogeographic morphology during development. Ithas been shown that changing patterns in intralimb pro-portions during ontogeny (at least up until puberty)reflect human growth patterns in intralimb proximal anddistal skeletal element lengths (Frelat and Mittereocker,2011; Temple et al., 2011). We expect shifting patterns inintralimb proportions during ontogeny in the Kellis 2sample to match patterns found in other populations.That is, intralimb proportions are expected to be greatestin infancy, decline during early childhood, and increaseagain at the onset of puberty. Given the extreme climaticconditions in the Dakhleh Oasis, the less efficient thermo-regulatory mechanisms in juveniles as compared toadults, and evidence suggesting that intralimb propor-tions are genetically conserved, adult patterns in brachialand crural indices are expected to be present in earlyontogeny and maintained throughout development. Wewill 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 evolvabilityrefers to the ability of random variations to produce new,heritable phenotypes, which can then be the targets ofselection (Houle, 1992; Wagner and Altenberg, 1996). Ifintralimb 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) isunder selection. The large sample of fetuses will allowpre- and postnatal comparisons, which will add to the cur-rent data documenting ecogeographic patterns injuveniles.

MATERIALS AND METHODS

The Dakhleh Oasis (25�31’N, 28�57’E) is located in theWestern Desert of Egypt �550 km south-southwest ofCairo (Fig. 1). The Western Desert experiences excep-tional fluctuations in seasonal temperatures throughoutthe year. Winter temperatures average near or slightlybelow freezing before sunrise and �20� to 25�C by mid-day; and, summer temperatures average �19�C in theevening 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 (Duprasand Schwarcz, 2001; Sutton, 1947). These climatic condi-tions are very similar to those during the Romano-Christian period from which the Kellis 2 cemetery samplederives, although precipitation in the Oasis was greaterduring 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 practicesobserved within the Kellis 2 cemetery have created idealconditions for the exceptional preservation of skeletalremains, including the preservation of fetal and perinateindividuals. Archaeological evidence from the associatedancient village of Kellis suggests occupation from AD 50–360 (Hope, 2003); however, numerous radiocarbon datesfrom the Kellis 2 cemetery indicate use between AD 100and 450 (Stewart et al., 2003). At present, 770 individualsof an estimated 3000–4000 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-file at Kellis 2 is similar to that expected in a naturalmortality distribution in preindustrial populations(Tocheri et al., 2005). This study utilizes a cross-sectionalsample of 301 individuals spanning the fetal/perinatethrough adult years (Table 1).

Skeletal measurements

Standard skeletal metrics were collected from all indi-viduals as part of the basic osteological data collectionprocedures of the Dakhleh Oasis Project BioarchaeologyResearch Team. A subset of skeletal measurements usedto calculate intralimb proportions was selected for thisstudy. Data from left-sided elements were examined; how-ever, right-sided elements were included when the leftside was missing or damaged. Unilateral analyses aredeemed appropriate in this study since ecogeographic pat-terns in intralimb proportions are likely to affect the bodysymmetrically. However, it should be noted that bilateralasymmetry in limb long bone lengths exists in utero, butdifferences between left-sided and right-sided elementsare not statistically significant (Bagnall et al., 1982).

222 M.M. BLEUZE ETAL.

American Journal of Human Biology

Maximum lengths for the major long bones in the upperand lower limbs have also been found to show low levels ofbilateral asymmetry in a large, geographically and tempo-rally diverse sample of modern humans (Auerbach andRuff, 2006). Maximum diaphyseal lengths for thehumerus (HL), radius (RL), femur (FL), and tibia (TL)were measured in individuals with unfused proximal anddistal epiphyses to the nearest tenth of a millimeter using

digital sliding calipers, or to the nearest millimeter usinga standard osteometric board. Maximum bone lengths forthe same four long bones were measured in individualswith fused proximal and distal epiphyses to the nearestmillimeter using a standard osteometric board followingstandard long bone measurement protocols (Buikstra andUbelaker, 1994). Maximum bone lengths were convertedto maximum diaphyseal lengths to maintain consistencyin comparing juvenile and adult data (Ruff, 2007). Brach-ial and crural indices were derived from the maximumdiaphyseal lengths following standard formulae: brachialindex5maximum radius length/maximum humeruslength 3 100; and, crural index5maximum tibia length/maximum femur length3 100.

Sex and age estimation

Reliable estimations of sex in juvenile skeletal remainsare problematic; therefore, sex estimation was notattempted for the juvenile sample (Scheuer and Black,2000a,b). This may limit interpretations of the data sincethere are known sex differences in limb long bone growthvelocities and timings, which may ultimately contributeto 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 9–41 weeksa 24 23Infant 0.0–0.9 year 62 69Child 1 (C1) 1.0–4.9 years 30 34Child 2 (C2) 5.0–10.9 years 15 16Child 3 (C3)b 11.0–14.9 years 4 3Adult female 15.01 years 89 87Adult male 15.01 years 64 69Total 288 301

aWhile the fetal cohort includes individuals beginning at nine weeks gestation(Scheuer and Black, 2000a), the youngest individuals in this study are estimatedat 24 weeks gestation.bBecause of the small sample size, the C3 cohort was combined with the C2cohort. Mean intralimb proportions are not significantly different between thegroups, and C3 individuals in this study are all aged near the lower end of theC3 age range (i.e., 11.0–11.4 years).

ONTOGENETIC CHANGES IN INTRALIMB PROPORTIONS 223


The dentition provides the most reliable estimation ofchronological age in juveniles; however, inter- and intra-population variation in dental formation and eruptiontimes 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 andMolleson, 2004; Saunders, 2000; Smith, 1991). Juvenilesin this study were aged using dental calcification tables(Moorrees et al., 1963a,b; Smith, 1991). Age estimateswere based on macroscopic examinations of the dentitionsince radiographic equipment was not available in thefield. Multiple teeth from each individual were examinedand suggested age and age ranges were based on crown orroot formation. The assigned dental age was recorded asthe mean of all available ages suggested by each tooth.When dentition was absent, juvenile age estimates werebased on epiphyseal development and fusion, pars basila-ris morphology, and fusion of cranial elements (Krogmanand Iscan, 1986; Scheuer and Black, 2000a). Fetal andperinate 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; Sherwoodet al., 2000).

Age terminology used to describe juveniles is inconsis-tent in the literature and often varies depending on theobjectives of the research (e.g., biological, social) (Hal-crow and Tayles, 2008). In this study, we use the clinicalpediatric/developmental osteology age terminology toprovide a biological basis for comparisons. “Fetus”includes individuals aged nine weeks gestation to birth,“perinate” is from 24 weeks gestation to seven postnataldays (or around the time of birth), “infant” is from birthto the end of the first postnatal year (i.e., 0.0–0.9 year),and “child” is from 1.0 to 14.9 years of age (Halcrow andTayles, 2008; Scheuer and Black, 2000a,b). The “fetus”and “perinate” cohorts were pooled since age ranges over-lap in these groups. Since significant growth and devel-opmental changes occur during childhood, we furtherdivided this cohort to examine shifts in intralimb propor-tions at a finer scale. “Child 1” (C1) encompasses the agerange between 1.0 and 4.9 years of age (early childhood),“child 2” (C2) encompasses the age range between 5.0and 10.9 years of age (middle childhood), and “child 3”(C3) encompasses the age range between 11.0 and 14.9years 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 withthe C2 cohort. Mean intralimb indices are not significantlydifferent between the C2 and C3 groups, and the C3 indi-viduals in this study were all aged closer to the lower end ofthe C3 age range (i.e., 11.0–11.4 years of age).

Sex estimation for adult skeletal remains was based onstandard 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 andLoth, 1986). In this study, adults are identified based onfull epiphyseal fusion in the humerus and radius, or fullepiphyseal fusion in the femur and tibia.

Statistical analyses

Brachial and crural indices were compared across agecohorts with Welch’s ANOVA tests since the data is nor-mally distributed, but the assumption of homogeneity ofthe variances is violated (McDonald, 2008). Dunnett-Tukey-Kramer (DTK) pairwise multiple comparison testswith family-wise error adjusted for unequal variances andunequal sample sizes were conducted post-hoc to deter-mine which groups significantly 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 boxrepresents the interquartile range and the upper andlower “whiskers” represent the maximum and minimumvalues, respectively. The median is denoted as the linewithin the box. Spearman’s rank correlation coefficients(q) with Fisher’s z-transformations were calculatedbetween intralimb skeletal elements (i.e., RL vs. HL andTL vs. FL) in each age cohort to explore developmentalconservation and evolvability in the brachial index andcrural index. Fisher’s z-transformations were used to cal-culate 95% confidence intervals for the correlation coeffi-cients, and dependent t-tests were used to compareFisher’s z-transformations of correlation coefficients inthe 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 deviationsas follows: fetus/perinate5 82.446 2.73, infant579.0562.48,C15 76.156 1.17, C2/C35 77.206 2.25, adult female578.5062.55,and adult male5 80.286 2.53.

Fig. 3. Box-plot of crural index. Means and standard deviations asfollows: fetus/perinate587.4361.32, infant584.8762.28,C15 82.596 1.52, C2/C35 83.566 1.63, adult female582.9462.07,and adult male5 83.436 2.18.



suggests reduced evolvability, while a lower correlationsuggests greater evolvability (Young et al., 2010). Statisti-cal significance is set at P< 0.05 and all statistical analy-ses were carried out using R-Studio.

RESULTS

The mean brachial index is significantly different amongthe age cohorts (F5 25.96, P< 0.00). It is greatest duringearly ontogeny, declines during early childhood, andincreases again during middle/late childhood (Fig. 2). Thefetus/perinate cohort has a significantly greater brachialindex than all other groups, and the infant cohort has a sig-nificantly greater brachial index than the C1 cohort. Thebrachial index does not significantly change during child-hood. Children in the C1 cohort have a significantly lowerbrachial index than female and male adults, while childrenin the C2 cohort have a significantly lower brachial indexthanmale adults only (Table 2). The adult pattern is first evi-dent during infancy, but is not maintained during childhood.

The mean crural index is significantly different amongthe age cohorts (F5 37.97, P< 0.00). It is greatest in thefetus/perinate cohort, decreases during infancy and earlychildhood, and increases, albeit nonsignificantly, duringmiddle/late childhood (Fig. 3). The fetus/perinate cohorthas a significantly greater crural index than all othergroups. Infants have a significantly greater crural indexthan the C1 and adult cohorts. The crural index does notsignificantly change during childhood (Table 2). The adultpattern is first evident during early childhood and ismaintained from this point forward.

A significantly lower correlation is observed between RLand HL as compared to TL and FL in the fetus/perinatecohort, and a significantly greater correlation is observedbetween RL and HL as compared to TL and FL in the C1cohort. The correlations between RL and HL as comparedto TL and FL are not significantly different in the other agecohorts (Table 3). We pooled our postnatal juvenile sample(ages 0.0–11.4 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 HLas compared to TL and FL are not significantly different inthe Kellis 2 sample (z5 0.23, P50.81), which contrastswith results from Temple et al. (2011).

DISCUSSION

The primary objective of this study was to describechanges in intralimb proportions during development inthe Kellis 2 sample from the Dakhleh Oasis, Egypt. Theadult pattern in the brachial index is first evident ininfancy, but is not maintained throughout development.Conversely, the adult pattern in the crural index appearsduring early childhood and is maintained throughoutdevelopment. Thus, while adult intralimb proportions arenot present in utero they do appear very early in ontogeny.This lends further support to the long held view thatintralimb 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 despiteshifting values over the course of development such thatrelative ecogeographic patterns among geographicallydiverse populations are maintained during development(Cowgill et al., 2012; Ruff, 2007). In other words, there aresignificant differences in absolute mean brachial and cru-ral indices among age-matched cohorts across geographi-cally diverse populations despite similarities in shiftingpatterns throughout development. Shifting patterns inintralimb proportions during ontogeny are often linked todifferences in growth velocities of intralimb proximal anddistal elements (Cowgill et al., 2012; Temple et al., 2011).In the Kellis 2 sample, the intralimb proportions aregreatest in the fetus/perinate and infant cohorts, decreaseduring early childhood, and increase again during middle/late childhood. Our results are consistent with previouswork and extend the pattern to the fetus/perinate period.Since hyperthermia in utero may impede fetal growth anddevelopment, high intralimb proportions may be understrong selective pressures even before postnatal life (Ger-icke et al., 1989; Xu et al., 2012). During the first year oflife, intralimb proportions are significantly lower than inutero, but significantly greater than in early childhood.These results suggest that accelerated growth velocities ofdistal elements relative to proximal elements do not carryover into infancy.

We hypothesized that adult patterns in intralimb indi-ces would appear early in ontogeny and be maintainedthroughout development. This hypothesis is partially sup-ported by the results. While mean brachial indices are notsignificantly different between infants and adults, chil-dren have significantly lower brachial indices than adults(barring C2 children and adult females). This may reflectthe high growth velocity of the humerus relative to theradius during childhood and adolescence (Smith and

TABLE 2. P-values from Dunnett-Tukey-Kramer pairwise multiplecomparisons post hoc tests

Brachial index

Infant C1 C2 Adult female Adult male

Fetus/perinate 0.00 0.00 0.00 0.00 0.00Infant 0.00 0.05 0.76 0.13C1 0.69 0.00 0.00C2 0.29 0.00Adult female 0.00

Crural index

Infant C1 C2 Adult female Adult male

Fetus/perinate 0.00 0.00 0.00 0.00 0.00Infant 0.00 0.93 0.00 0.00C1 0.06 0.97 0.44C2 0.11 0.59Adult female 0.72

TABLE 3. Spearman’s rank correlation coefficients

Cohort Comparison q Fisher-z 95% CI z-value P

Fetal/Perinate RL vs. HL 0.909 1.527 0.864–0.941 2.09 0.04TL vs. FL 0.972 2.092 0.954–0.980

Infant RL vs. HL 0.973 2.092 0.951–0.982 0.71 0.48TL vs. FL 0.979 2.298 0.968–0.988

C1 RL vs. HL 0.989 2.647 0.978–0.995 2.57 0.01TL vs. FL 0.958 1.946 0.920–0.980

C2 RL vs. HL 0.956 1.946 0.897–0.985 0.50 0.62TL vs. FL 0.969 2.993 0.922–0.989

Adult ($) RL vs. HL 0.822 1.157 0.738–0.878 0.10 0.92TL vs. FL 0.827 1.188 0.751–0.886

Adult (#) RL vs. HL 0.794 1.071 0.675–0.867 0.03 0.98TL vs. FL 0.796 1.099 0.695–0.872



Buschang, 2004, 2005). It has been demonstrated that thebrachial index is more strongly correlated with meanannual temperature than the crural index in adults (Trin-kaus, 1981), and that the brachial index has a strongercorrelation with latitude in adults than in juveniles (Cow-gill et al., 2012). Since adult patterns in the brachial indexare not maintained during childhood, the results suggestthat selective pressures from climate acting on the brach-ial index may be weaker in children than in infants andadults. 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 appearin early childhood and are maintained throughout middleand late childhood. It is possible that this reflects func-tional constraints placed on the lower limbs (Templeet al., 2011; Young et al., 2010).

Correlation analyses indicate a significantly 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 geneticallyconserved than the brachial index in utero. These resultsare in accordance with previous studies suggestinggreater genetic conservation of the crural index as com-pared to the brachial index in postnatal life (Frelat andMittereocker, 2011; Temple et al., 2011). The greater cor-relation between lower limb elements as compared toupper 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 ratesof proximal and distal segments are more variable in thelower limbs as compared to the upper limbs during child-hood (ages 3–10 years), which may explain the signifi-cantly greater correlation between RL and HL ascompared to TL and FL in the C1 cohort (Smith andBuschang, 2004). The high degree of variation in growthof the tibia is particularly evident during early childhood,and may further contribute to the significantly greatercorrelation between RL and HL as compared to TL andFL (Smith and Buschang, 2004). Animal studies haveshown that exercise increases limb length by increasingthe amount of nutritional solute delivery to growth platesin weight-bearing limb bones (Jurvelin et al., 1988; Serratet al., 2007, 2010). Since children in the early childhoodphase are beginning to walk, the lower correlation of TLand FL relative to RL and HL may reflect growth devia-tions from the biomechanical demands of bipedalism.Greater variation in growth rates of lower limb elementsas compared to upper limb elements during early child-hood coupled with lower limb skeletal element elongationfrom increased loading due to the start of walking behav-iors may explain the greater correlation between RL andHL as compared to TL and FL in the C1 cohort.

It was previously shown that RL and HL have a signifi-cantly lower correlation than TL and FL in a Jomonperiod juvenile sample (Temple et al., 2011). Our pooledKellis 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 significantly different. Thesecontrasting results may reflect 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 0.0–0.9) slightly outnumbered chil-dren (1.0–11.4 years of age) in the pooled postnatal Kellis2 juvenile sample.

Given the climatic extremes experienced in the Dakh-leh Oasis it is not unexpected to find elevated intralimbindices in the Kellis 2 juvenile sample. The Kellis 2 sam-ple is similar to other warm-adapted populations in thisregard. While cross-sample comparisons are approachedwith caution because of differences in age cohort construc-tion, Kellis 2 juveniles have similar mean intralimb pro-portions as those reported for similarly age-matchedjuveniles from Kulubnarti, Upper Nubia (21�N), and Kel-lis 2 juveniles have lower mean intralimb proportionsthan those reported for similarly age-matched juvenilesfrom Point Hope, Alaska (68�N) (Cowgill et al., 2012).

Seasonal mortality for the Kellis 2 population wasderived 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 arealigned with warmer seasons (late March/early April toAugust/September), 47% of which are infants (Williams,2008). Alignment of �38% of fetuses and 46% of perinatesare 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 theincreased juvenile deaths during these times (Alpin, 1980;Bagnall, 1993; Williams, 2008). The tendency towardsgreater fetus and perinate mortality in the warm seasonobserved at Kellis 2 is comparable to historical and mod-ern Egyptian rural populations from Upper and LowerEgypt (Alpin, 1980; El-Nomrosi, 1981; Shaw, 1996). Giventhe high mortality rate of Kellis 2 juveniles during thewarm season, it is possible that we are observing a juve-nile sample with intralimb proportions that were selectedagainst. An important factor to consider when investigat-ing a juvenile skeletal sample is that the sample may notreflect the normal, healthy population from which it wasdrawn 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, enamelhypoplasia) and the low prevalence of trauma suggest anoverall improvement in health when compared to pre-Roman populations (Fairgrieve and Molto, 2000) and acontemporaneous Nubian sample from Kulubnarti(Wheeler, 2012). In addition, the lack of relationshipbetween the number of observable skeletal and dentalstressors and growth patterns suggests that physiologicalstressors did not negatively affect growth patterns in theKellis 2 juveniles (Wheeler, 2009). On the basis of thesefindings, it is reasonable to surmise that growth patternsin 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 oftrue ontogenetic patterns.

While the effects of nutrition and overall health cannotbe ignored in analyses dealing with skeletal growth, it hasbeen 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 significantly different in a skel-etal sample of children from medieval cemeteries in tworegions of Croatia despite nutritional differences betweenthe 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



changes in intralimb proportions in the Kellis 2 juvenilesample are likely not biased by nutritional status.

CONCLUSIONS

This study examined ontogenetic changes in intralimbproportions 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 presentearly in ontogeny. While adult patterns in the brachialindex are not maintained throughout childhood, the adultpattern in the crural index is maintained from early child-hood onwards. Intralimb proportions, especially the cru-ral index, have a strong developmental component. Theseresults suggest that, like adults, juveniles are understrong selective pressures from climatic factors.

Selective pressures acting on human populations aregenerally examined among adults despite the fact thatthe adult morphology is the end result of biological andenvironmental factors occurring throughout development.Selective pressures and the adaptive significance of juve-nile morphology must be examined to better understandthe processes that lead to the adult form.

ACKNOWLEDGMENTS

The authors would like to thank the Egyptian Ministryof State for Antiquities for their continued support of theDakhleh Oasis Project, Anthony Mills for his dedicationto the DOP, and all the members of the Dakhleh OasisBioarchaeology team, especially Dr. Peter Sheldrick. Theauthors would also like to thank Dr. J. E. Molto for theuse of the Kellis 2 adult osteometric data and the twoanonymous reviewers for their helpful comments.

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Bleuze Et Al Ontogenetic Changes in Intralimb Proportions in a Romano-Christian Period Sample From the Dakhleh Oasis Egypt-libre