Advances in Anthropology
2013. Vol.3, No.1, 10-15
Published Online February 2013 in SciRes (http://www.scirp.org/journal/aa) http://dx.doi.org/10.4236/aa.2013.31002
Copyright © 2013 SciRes.
Sexual Dimorphism in Prehispanic Populations of the
Cochabamba Valleys, Bolivia*
José A. Cocilovo1#, María L. Fuchs1, Tyler G. O’Brien2, Héctor H. Varela1
1Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Química y Naturales,
Universidad Nacional de Río Cuarto, Río Cuarto, Argentina
2Department of Sociology, Anthropology and Criminology, University of Northern Iowa,
Cedar Falls, USA
Received November 17th, 2012; revised December 21st, 2012; accepted January 1st, 2013
The expression of sexual dimorphism may vary across time and space, as well as within and between
populations depending on genetic and environmental factors that influence growth and development. The
objective of the present work is to contribute to the knowledge of factors that determine the physical cha-
racteristics of ancient human groups in the eastern valleys of Cochabamba—a key region for cultural
development, inter-regional interaction with northern Chile and northwest Argentina, and their noticeable
role in the settlement of the south central Andean region. This paper analyzes the differences between
males and females crania representing ancient human groups that inhabited the eastern valleys of Co-
chabamba, Bolivia. Thirty-one craniometric variables are analyzed from a sample of 234 individuals.
Differences are evaluated using univariate analysis by ANOVA and multivariate discriminant analysis.
The results indicate the existence of higher mean values in males compared to females in most cranial
measurements (mean difference 5.3%). The discriminant analysis also reveals a significant morphological
difference exists between sexes. Furthermore, by means of the discriminant function, the reclassification
of correct sex was 99% of cases. This information indicates that members of this population could live in
optimal conditions, with adequate resources to ensure growth and development and normal expression of
the phenotype of each sex.
Keywords: Sexual Dimorphism; Growth and Development; Population Biology; Craniometrics
Sexual dimorphism is the result of the complex action of a
series of genetic and environmental factors linked to the growth
and development process of individuals. Although this charac-
teristic is already seen in the fetal development, this is much
more evident in the puberal stage of the vital cycle, affecting
the anatomy, physiology and behavior. In current populations,
normal growth tends to conclude with the development of the
secondary sexual characteristics around 16 years old in the
female and about 18 years old in the males, with the most con-
spicuous change being the overall difference in size. This diffe-
rence is produced by differential growth in regards to duration,
intensity and velocity. A complete synthesis of this theme, from
an evolutionary perspective, can be found in work by Frayer
and Wolpoff (1985). Additional work by Guntupalli and Baten
(2009) evaluates stature differences between both sexes from
historic and socioeconomic points of view.
Sexual differences manifest themselves at various levels in
respect to size and form of the tissue and organ. In particular,
the acquisition in the male of greater muscular mass also brings
about a greater development of the skeletal system. The bone
structure reflects these differences in conjunction with anatomic
traits. Such characteristics are currently employed in the dis-
crimination of sex in skeletal remains (Saunders, 1992).
The magnitude of sexual dimorphism constitutes a topic of
great interest because of its association with growth problems
produced by disease and malnutrition. In fact, in situations of
chronic stress a reduction of sexual dimorphism is expected but
at the expense of normal masculine growth. Males are more
ecosensitive and experience a much more marked response to
prolonged nutritional shortages (Frayer & Wolpoff, 1985;
Stinson, 1985). Three dramatic examples of the effects on
sexual dimorphism by way of nutritional shortages and ineffi-
cient sanitary conditions are evident in the cases of Heliconia,
Colombia (Stini, 1969), of the Villa IAPI, a poor village outside
of Buenos Aires, Argentina (Pucciarelli et al., 1993) and an-
other case in the Republic of Mali, Africa (Dettwyler, 1992).
However, in contrast, the Tehuelches and Mapuches, two in-
digenous groups of Chubut, Argentina, express normal rates of
sexual dimorphism in supposedly unfavorable economic and
environmental conditions because of the governmental assis-
tance they receive and the social cooperation that permits them
to reach an appropriate nutritional state (Pinotti et al., 2005).
This feature was evaluated in current native groups from la
Puna in Jujuy in a sample of 231 individuals, by means of 21
somatometric measurements. All the variables showed signifi-
cant differences between both sexes, and the male mean values
were higher than those of the females. This result was very
precise as the measurements were performed independently of
*The research for this work was supported by grants from Consejo Nacional
de Investigaciones Científicas y Técnicas (PIP 2405/08), Universidad Na-
cional de Río Cuarto (C18/328), Agencia Nacional de Promoción Científica
y Técnica (PICT 02210/07) of Argentina; Faculty Fellowship, University o
orthern Iowa; and Nacional Science Foundation’s doctoral dissertation
improvement grant (SBR 9903631).
J. A. COCILOVO ET AL.
the age effect or any micro-geographical variations (Varela et
al., 1990a). Similar results were obtained in native groups from
western Chaco (Matacos, Tobas, Chorotes and Chiriguanos)
(Priotto, 1990). A more recent work confirmed the results ob-
tained in these ethnic groups (Méndez & Ferrarini, 2006), in
which sexual dimorphism was explained based on the life his-
tory of each group, energy intake and utilization of resources.
In current populations, detailed research attests to the anato-
mical and physiological differences between both sexes. How-
ever, in ancient populations any indication of sexual dimor-
phism or its effects is more often associated with the simple
determination of sex from the bones and not the evaluation of
such traits as an adaptive process (Giles & Elliot, 1963; Coci-
lovo & Marcellino, 1974; Purkait & Chandra, 2002, 2004). An
earlier analysis of sexual dimorphism is in Keen’s (1950) work
on the human cranium. In his research, the statistical signi-
ficance of differences seen between males and females is
evaluated statistically by a set of metric variables and discrete
In many studies carried out on skeletal materials from vast
regions (Peru, Chile and Argentina), sexual dimorphism ex-
pressed across the entire cranium is typically verified to be the
main factor of variation (Cocilovo, 1975, 1978; Cocilovo et al.,
1982; Cocilovo & Baffi, 1985; Varela et al., 1990; Cocilovo et
al., 1994; Mendonça et al., 1994). Male individuals tend to
present systematically greater dimensions than females, while
general form of anatomical structures remains constant. For
example, statistical tests indicate significant differences exist
between sexes in the majority of metric variables, however,
indices (or the quotient between two variables), could not
always be verified.
In some cases, these facts suggest that major bony develop-
ment in males, in contrast to women, could be the result of a
normal rate of growth, but only in conditions of adequate nu-
trition and certain lifestyles of the distinct groups. However, a
situation in one case finds diametrically opposite results: Las
Pirguas (Pampa Grande, Salta, Argentina). Here the differences
between males and females are of a smaller magnitude. This
information, along with other indicators (low life expectancy at
birth, the prevalence of infectious and nutritional pathologies,
and social stress indicators), reflects the presence of rigorous
environmental circumstances and possibly more intense interac-
tion with other contemporary groups (Baffi & Cocilovo, 1989;
Baffi et al., 1996).
The study of sexual dimorphism is important to assess the
biological profile of a population, in respect to its adaptation to
specific socio-cultural and environmental conditions. The ob-
jective of the present work is to contribute to the knowledge of
factors that determine the physical characteristics of ancient
human groups in the eastern valleys of Cochabamba—a key
region for cultural development, inter-regional interaction with
northern Chile and northwest Argentina, and their noticeable
role in the settlement of the south central Andean region
(Cocilovo et al., 2009).
Materials and Methods
The series of skulls used for this project come from pre-
hispanic archaeological sites in the eastern valleys of Bolivia
around Cochabamba and Sucre. Sites from where skulls were
collected temporally range from the Middle Horizon to pre-
conquest (~0 - 1450 s AD) for the South Central Andean region.
Figure 1 illustrates the eastern valleys of the Cochabamba
Location of the Cochabamba samples from the eastern valleys of Bo-
region in geographic relation to the capital city of La Paz and
Lake Titicaca (O’Brien, 2003).
The observations and measurements were made by one of the
authors (TGB) in a set of 234 individuals, that were aged using
dental development, attrition patterns (Buikstra & Ubelaker,
1994; Lovejoy, 1985) and cranial suture obliteration (Masset
1989; Meindl & Lovejoy, 1985) and were sexed utilizing gross
morphological and diagnostic cranial features (Acsadi & Neme-
skeri, 1970; Bass, 1987; Buikstra & Ubelaker, 1994). Judgment
of whether or not a cranium was artificially modified was
based on previous work (Dingwall, 1931; Dembo & Imbelloni,
Cranial data, derived from 31 metric variables taken across
the vault, base and face, are statistically analyzed using a one-
way ANOVA analysis to evaluate the differences between male
and female skulls (see Figures 2 and 3). Subsequently, the
differences between both sexes were evaluated through discri-
minant analysis (Seber, 1984). Discriminant function analysis
verified the correct sex classification on individuals that pre-
sented complete data for all variables. For the explanation of
the magnitude of the sexual dimorphism, for each variable, an
index was calculated as the difference between the mean male
(MEDm) and the mean female (MEDf) value in relation to the
average female: [(MEDm − MEDf)/MEDf] expressed as a per-
centage. “Heteromorphic” are those variables which in the
ANOVA results showed significant differences between the
mean values of one and the other sex, and “isomorphic” those
who did not express that difference.
Table 1 shows the sample distribution according to sex and
age; a net predominance of female individuals is observed and
Copyright © 2013 SciRes. 11
J. A. COCILOVO ET AL.
Example of adult male from the Mojocoya site,
Example of adult female from the Mojocoya site,
Distribution of the Cochabamba sample by age and sex.
Age Male Female
Adult 43 (39%) 67 (61%) 110
Mature 50 (52%) 46 (48%) 96
Senile 7 (25%) 21 (75%) 28
Total 100 134 234
few senile individuals. Table 2 shows the distribution of both
sexes according to artificial cranial deformation. The majority
consists of non-deformed individuals (76%). The other types:
tabular erect (TE), tabular oblique (TO) and circular oblique
(CO) represent 24% of all cases. Table 3 displays each variable
separated by sex, number of cases (N), mean (
error (s.e.), and the test for sex differences between means (F).
All but three of the craniometric variables express a sig-
nificant difference between the sexes (p < 0.01). The three
exceptions are nasal breadth, orbit height and occipital chord.
Overall, males tend to present greater mean values than females
(see Figures 4-6). This difference, measured with regard to the
female value, is always positive and is distributed with a mean
of 4.9% (s.d. = 0.06%) in a range with a low of 2.3% (for the
frontal chord) and a high of 19.4% (for mastoid length). The
magnitude of the difference is smaller in measurements of the
Composition of the Cochabamba sample by sex and artificial defor-
Sex TE TO CO ND
Male 9 (9%) 8 (8%) 5 (5%) 78 (78%) 100
Female10 (7%)9 (7%) 16 (12%) 99 (74%) 134
Total 19 (8%)17 (7%)21 (9%) 176 (76%) 234
Note: row percentages. *TE = Tabular erect; TO = Tabular oblique; CO = Circular
oblique; ND = no deformation.
vault (mean = 4.4%) and greater in facial skull measurements
(mean = 5.4%).
In general, the adult male tends to possess greater growth and
development in the majority of the anatomical substructures of
the skull. The greater dimensions are most evident in the vault,
neurocranial base, foramen magnum, size of the face and fron-
tal, malar and palatine bones, wider orbits and longer nasal
length. Upon considering all the variables together, the results
of the discriminant analysis indicate that there is a significant
difference between sexes (Wilks’ Lambda = 0.21343, approxi-
mate F (31 and 47 df) = 5.5876, p < 0.0001). The reclassifica-
tion of individuals into the correct sex was 99% (Table 4). The
distributions of male and female agrees with the first canonical
discriminant variable accounting for 100% of the variance (see
The magnitude of sexual dimorphism depends on genetic
variation and local conditions such as the availability of food
resources to ensure adequate nutrition, in order to guarantee
normal growth and development. Such effects are often evident
in a metric examination of the skeleton. Results from the uni-
variate and multivariate tests, carried out on the crania in the
Cochabamba population, clearly demonstrate a difference exists
between the male and females phenotypes. In males, during the
process of body tissue differentiation, major skeletal develop-
ment enables greater and more functional muscle mass to form
than in females. This characteristic, constituting an important
property of the biological profile of the population, is charac-
terized by the notable constancy of the sexual dimorphic dif-
ferences across the cranial dimensions. Incidentally, in only
10% of the variables was it not possible to show this effect.
These facts are consistent with a normal growth and a later
development in male individuals in an environment with exten-
sive availability of nutritional resources.
Undoubtedly, the living conditions in prehispanic Cocha-
bamba surpassed that of other localities, where it was found
that the proportion of isomorphic variables was higher, ranging
between 13% and 62% of all measurements. In comparison,
values for pre-ceramic populations in northern Chile are 19% in
Morro de Arica and 13% in agro pastoral group of San Pedro de
More extreme values come from the site of Pisagua where
the absence of sexual dimorphism is determined from 38% of
the metric variables analyzed. Similarly, in Caleta Huelén 42,
45% of the variables were unaffected. In late ceramic groups of
northwest Argentina, like La Paya, in the Calchaqui Valleys,
27% of the variables do not manifest sexual dimorphic diffe-
Copyright © 2013 SciRes.
J. A. COCILOVO ET AL.
Copyright © 2013 SciRes. 13
Cochabamba, statistics for each variable and test the difference between mean values (ANOVA) by sex.
Sex Male Female
se F1 df
Maximum Cranial Length 100 175.52 0.66 133 168.64 0.64 ** 231
Maximum Cranial Breadth 98 137.08 0.70 133 134.56 0.53 ** 229
Maximum Cranial Height 93 132.49 0.55 125 129.4 0.53 ** 216
Minimum Frontal Breadth 98 92.02 0.46 131 89.10 0.33 ** 227
Maximum Frontal Breadth 96 113.92 0.57 127 110.67 0.51 ** 221
Upper Facial Breadth 100 103.78 0.45 131 99.83 0.34 ** 229
Upper Facial Height 87 72.33 0.64 115 67.63 0.69 ** 200
Bizygomatic Breadth 89 137.26 0.63 117 128.39 0.56 ** 204
External Palatal Length 65 53.2 0.33 82 50.29 0.35 ** 145
External Palatal Breadth 58 65.31 0.40 77 62.10 0.34 ** 133
Internal Palatal Length 64 47.55 0.37 87 44.87 0.30 ** 149
Internal Palatal Breadth 55 42.47 0.41 78 40.42 0.28 ** 131
Nasal Height 89 51.38 0.34 117 48.68 0.29 ** 204
Nasal Breadth 87 25.39 0.21 117 25.02 0.16 ns 202
Orbit Height 91 35.68 0.28 121 35.55 0.21 ns 210
Orbit Breadth 90 37.87 0.20 122 36.85 0.15 ** 210
Interorbit Breadth 89 23.42 0.24 127 21.94 0.20 ** 214
Biorbital Breadth 100 95.91 0.39 128 92.41 0.33 ** 226
Malar Length. Inferior 81 32.91 0.33 105 30.67 0.35 ** 184
Malar Length. Maximum 80 52.26 0.32 107 48.33 0.42 ** 185
Cheek Height. Minimum 91 24.35 0.29 121 22.10 0.22 ** 210
Biauricular Breadth 97 126.57 0.56 130 120.38 0.42 ** 225
Basion Prosthion Length 79 96.19 0.55 104 91.80 0.45 ** 181
Cranial Base Length 92 96.85 0.37 124 92.25 0.35 ** 214
Foramen Magnum Length 89 35.56 0.29 120 34.21 0.25 ** 207
Foramen Magnum Breadth 93 29.74 0.23 120 28.87 0.21 ** 211
Biasterion Breadth 97 107.10 0.51 132 103.71 0.47 ** 227
Mastoid Length 97 29.03 0.29 128 24.32 0.28 ** 223
Frontal Chord 97 111.24 0.57 133 108.75 0.57 ** 228
Parietal Chord 99 105.12 0.64 133 102.31 0.55 ** 230
Occipital Chord 91 100.66 0.70 120 99.13 0.69 ns 209
Age 100 39.30 0.81 134 37.65 0.89 ns 232
Note: F: test sex differences; **p < 0.01; ns = p > 0.05; df: denominator degree of freedom. Numerator degrees of freedom equal to 1.
rences (Cocilovo & Baffi, 1985). Also in Doncellas (Puna), a
cemetery of the Late Period, 26% of the variables did not differ
between sex (Mendonça et al., 1994). Finally, in Trelew, a
hunter and gatherer site in Patagonia, 15% of 41 variables do
not exhibit sexual dimorphism (Cocilovo, 1978).
Cochabamba unlike, Pampa Grande (Northwest Argentina),
represents a situation in which the differences between males
and females reach a minimum expression with 62% of isomor-
phic variables from 37 measurements. This fact clearly demon-
strates the life conditions based on a subsistence economy with
insufficient nutritional resources, which was already seen pre-
viously (Baffi & Cocilovo, 1989; Cocilovo et al., 1994).
The difficulty to establish morphometric differences between
both sexes for some variables is certainly caused by problems
related to experimental design and the quantity of observations
available in each case. Furthermore, assuming an adequate
design, the early cessation of growth in a particular region of
the skull, like the anatomical units that protect and contain the
visual and olfactory systems, can limit the expression of the
differences between sexes. For example, this could explain the
absence of sexual dimorphism in the dimensions of the orbit
and nose in several samples from northern Chile: Morro de
J. A. COCILOVO ET AL.
Maxim um Cr ania l Length
Sexual dimorphism, Maximum Cranial Length. Vertical bars indicate
95% confidence interval of the mean distribution.
Maximum Cranial Breadth
Sexual dimorphism, Maximum Cranial Breadth. Vertical bars indicate
95% confidence interval of the mean distribution.
Maximum Cranial H eig ht
Sexual dimorphism, Maximum Cranial Height. Vertical bars indicate
95% confidence interval of the mean distribution.
Canonical discriminant I
-5 -4 -3 -2 -10123456
Discriminant analysis, distribution of individuals of each sex for the
canonical discriminant function I.
Cochabamba, reclassification of individuals by sex based on discrimi-
(%) Male Female Observed
Male 100.0 37 0 37
Female 97.6 1 41 42
Total 98.7 38 41 79
Arica (Cocilovo et al., 1982), Pisagua (Cocilovo et al., 1999),
Caleta Huelén 42 (Cocilovo et al., 2005) and San Pedro of
Atacama (Varela et al., 1990b; Cocilovo et al., 1994; Varela et
al., 1996); and from northwestern Argentina: La Paya (Baffi &
Cocilovo, 1985), Puna (Mendonça et al., 1994) and Las Pirguas
(Baffi et al., 1996).
In summary, the study of sexual dimorphism in ancient
populations allows us to make inferences about the expression
of a genetic trait that is determined and conditioned by envi-
ronmental, economic and socio-cultural factors. The obtained
information constitutes a window into the past through which
we can observe important aspects of life history and the adap-
tive process experienced by individuals. This process is still
occurring uninterrupted, even today, offering a connection be-
tween ancient groups and the current populations who inhabit
the vast regions of South America. Besides works of this type,
others in the future will be able to integrate global databases,
similar to the living populations studied by Gustafsson and
Lindernfors (2004, 2009) to explain the biological variation
from a biogeographical point of view or to carry out analysis of
the evolution of sexual dimorphism across time (Gustafsson et
The authors would like to thank, not only the editors and re-
viewers of this manuscript, but also the following for their as-
sistance, support and encouragement on this research and the
diverse aspects of the job in general: Deborah Blom, Ingrid
Carlstein, William Isbell, and John Janusek. We greatly appre-
Copyright © 2013 SciRes.
J. A. COCILOVO ET AL.
Copyright © 2013 SciRes. 15
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Pereira and Ramon Sanzetenea (Museo Arqueológico del Uni-
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