Sexual Dimorphism in Prehispanic Populations of the Cochabamba Valleys, Bolivia

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

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

Email: #jcocilovo@exa.unrc.edu.ar

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

Introduction

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).

#Corresponding author.

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

traits.

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

Figure 1.

Location of the Cochabamba samples from the eastern valleys of Bo-

livia.

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,

1938).

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.

Results

Table 1 shows the sample distribution according to sex and

age; a net predominance of female individuals is observed and

J. A. COCILOVO ET AL.

Figure 2.

Example of adult male from the Mojocoya site,

Cochabamba.

Figure 3.

Example of adult female from the Mojocoya site,

Cochabamba.

Table 1.

Distribution of the Cochabamba sample by age and sex.

Sex

Age Male Female

Total

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 (

), standard

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

Table 2.

Composition of the Cochabamba sample by sex and artificial defor-

mation type*.

Artificial Deformation

Sex TE TO CO ND

Total

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

Figure 7).

Discussion

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

Atacama.

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-

J. A. COCILOVO ET AL.

Table 3.

Cochabamba, statistics for each variable and test the difference between mean values (ANOVA) by sex.

Sex Male Female

Variable N

se N

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.

COCHABAMBA

MALE FEMALE

164

166

168

170

172

174

176

178

180

Maxim um Cr ania l Length

SEXUAL DIMORPHISM

Figure 4.

Sexual dimorphism, Maximum Cranial Length. Vertical bars indicate

95% confidence interval of the mean distribution.

COCHABAMBA

MALE FEMALE

130

131

132

133

134

135

136

137

138

139

140

Maximum Cranial Breadth

SEXUAL DIMORFISM

Figure 5.

Sexual dimorphism, Maximum Cranial Breadth. Vertical bars indicate

95% confidence interval of the mean distribution.

COCHABAMBA

MALE FEMALE

126

127

128

129

130

131

132

133

134

135

Maximum Cranial H eig ht

SEXUAL DIMORPHISM

Figure 6.

Sexual dimorphism, Maximum Cranial Height. Vertical bars indicate

95% confidence interval of the mean distribution.

Cochabamba

Sexual dimorphism

Canonical discriminant I

Frecuency

-5 -4 -3 -2 -10123456

MALE FEMALE

Figure 7.

Discriminant analysis, distribution of individuals of each sex for the

canonical discriminant function I.

Table 4.

Cochabamba, reclassification of individuals by sex based on discrimi-

nant function.

Assigned Total

Sex

(%) 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

al., 2007).

Acknowledgements

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-

J. A. COCILOVO ET AL.

ciate the access to the skeletal collections granted by David

Pereira and Ramon Sanzetenea (Museo Arqueológico del Uni-

versidad Mayor de San Simon, Cochabamba, Bolivia) and Ed-

mundo Salinas (Museo Arqueológico de la Universidad de

Chuquisaca, Sucre, Bolivia).

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