FLUCTUATING DENTAL ASYMMETRY AT THE IMPERIAL ROMAN
NECROPOLIS OF VELIA
Morgan LaFleur
B.A., University of North Carolina, Chapel Hill, 2002
THESIS
Submitted in partial satisfaction of
The requirements for the degree of
MASTER OF ARTS
in
ANTHROPOLOGY
at
CALIFORNIA STATE UNIVERSITY, SACRAMENTO
Fall
2011
FLUCTUATING DENTAL ASYMMETRY AT THE IMPERIAL ROMAN
NECROPOLIS OF VELIA
A Thesis
by
Morgan LaFleur
Approved by:
_______________________________________, Committee Chair
Samantha M. Hens, Ph.D.
_______________________________________, Second Reader
Martin Biskowski, Ph.D.
____________________
Date
ii
Student: Morgan LaFleur
I certify that this student has met the requirements for format contained in the University
format manual, and that this thesis is suitable for shelving in the Library and credit is to
be awarded for the thesis.
____________________________, Graduate Coordinator _______________
Michael Delacorte, Ph.D.
Date
Department of Anthropology
iii
Abstract
of
FLUCTUATING DENTAL ASYMMETRY AT THE IMPERIAL ROMAN
NECROPOLIS OF VELIA
by
Morgan LaFleur
Fluctuating asymmetry is frequently used as an indicator of developmental stress.
This study assesses asymmetry in a Roman Imperial sample from the coast of Italy. The
purpose of this investigation was to analyze asymmetry in the adult dentition of 54
individuals from the necropolis of Velia in order to record overall magnitude of FA and
the presence or absence of directional asymmetry and antisymmetry. The data was
evaluated for patterns such as sex and size differences in FA frequencies, differences
between maxillary and mandibular teeth, differences between the mesiodistal and
buccolingual dimensions, differences between posterior and anterior teeth, and
correspondence to field theory. Tests showed that the Velia sample had no directional
asymmetry or antisymmetry present. Analyses of fluctuating asymmetry revealed that
Velia males consistently have more asymmetry than females. No significant differences
were noted between dimensions, however significantly higher asymmetry was noted for
the posterior teeth, and for the maxillary teeth in both sexes. The asymmetry frequencies
loosely correspond to dental field theory for both males and females. Evidence of skeletal
and dental pathology from Velia and similar Imperial Roman samples indicate that stress
during growth and development was common. The presence of fluctuating asymmetry at
iv
Velia confirms that fluctuating dental asymmetry is a useful indicator of developmental
instability.
______________________________, Committee Chair
Samantha M. Hens, Ph.D.
____________________
Date
v
ACKNOWLEDGEMENTS
Special thanks to Luca Bondioli for access to the Velia collection at the L. Pigorini
National Museum of Prehistory and Ethnography. I am particularly grateful to Samantha
M. Hens, Ph.D. for her support, generosity, inspiration, and invaluable ideas and advice.
Thanks also to Martin Biskowski, Ph.D. for his helpful input on this manuscript. Finally,
I would like to thank my husband, Alan, for his patience and encouragement.
vi
TABLE OF CONTENTS
Page
Acknowledgements……………………………………………………………………. vi
List of Tables………………………………………………………………………….... ix
List of Figures…………………………………………………………………………... x
Chapter
1.
INTRODUCTION………………………………………………………………… 1
Project Specifications…………………………………………………………... 8
2.
LITERARY REVIEW…………………………………………………………….. 9
Directional Asymmetry and Antisymmetry……………………………………. 9
Fluctuating Asymmetry……………………………………………………….. 15
Asymmetry in Non-Dental Structures………………………………………… 26
Common Problems and Error in Studies of FA……………………………..… 30
Patterns of Dental FA……………………………………………………..…… 35
Italian Literature…………………………………………………………..…… 38
Project Details…………………………………………………………..……... 47
3.
MATERIALS AND METHODS………………………………………..……....... 49
4.
RESULTS……………………………………………………………...………..... 55
5.
FINDINGS AND INTERPRETATIONS……………………………...………… 67
Discussion…………………………………………………………...………… 67
Conclusion…………………………………………………………...……….... 71
Appendix A: Abbreviations Used in Study………...………………………………….. 72
vii
Page
Appendix B: Sample of Scatter Plots Showing Outliers……………………………….. 74
Appendix C: Quantile-Quantile Plots of Normality for the Velia Sample………..……. 80
References………………………………………………………………………..……... 84
viii
LIST OF TABLES
Page
1. Tooth Pair Sample Size by Tooth, Arcade, Sex, and Crown Diameter………......... 53
2. Summary Statistics of |L – R| for Velia Females……….…..…………………..….. 56
3. Summary Statistics of |L – R| for Velia Males………….………...………………... 56
4. ANOVA Results for Male and Female Differences using Transformed Data
(L-R)/2 and the Absolute Value of L-R………..……..…………………….…....… 57
5. Test for Female Skew and Kurtosis…………………...…………..………….......... 58
6. Test for male Skew and Kurtosis………..………….…………………………….... 58
7. Kolmogorov-Smirnov Test Results………………………………………….......... 59
8. Mean Values and Standard Deviation for Subsets of Data Tested for DA……...... 60
9. Mixed-model ANOVA Results Testing for DA………………………………..…. 60
10. Comparisons of Female and Male Mean by Arcade…………...…………..….… 61
11. Two-Way ANOVA Results for Sex and Tooth Dimensions, Considered
Separately for Each Arcade……………..…….………………………….…...…. 61
12. ANOVA Results for Sex and Tooth Dimension, Arcades Pooled……….…...…. 62
13. ANOVA Results for Sex and Tooth Dimension, Considering Each Arcade....…. 62
14. Pooled ANOVA Results for the Main Variables……...………………………..... 63
15. Pooled Mean Values for FA……….……...…………………………………...... 63
16. ANOVA of the Male and Female Anterior and Posterior Teeth……..….…....… 64
17. Mean Values of FA by Tooth for the Arcades and Sexes…………………...….. 66
ix
LIST OF FIGURES
Page
1. Approximate Location of Velia in Relation to Modern Italian Cities and the
Imperial Roman Necropolis of Isola Sacra...…………………...…….…………...49
x
1
Chapter 1
INTRODUCTION
Fluctuating asymmetry (FA), coined by the German biologist Wilhelm Ludwig in
his 1932 paper (Van Valen, 1962), has been the focus of much recent work. Fluctuating
asymmetry is considered a measure of developmental stability, and has been used to
make inferences about the general health of populations during growth and development.
Fluctuating asymmetry is defined as random, independent deviations from bilateral
symmetry in a particular trait or character (Palmer and Strobeck, 1986; Van Valen, 1962).
FA involves the measurement of the same structure on two sides of an organism and
determining the variance in the right minus left values. Measures of asymmetry assess
developmental precision, or the ability of an organism to develop according to the genetic
goal of perfect bilateral symmetry (Van Valen, 1962). Most researchers have found a
positive correlation between instability during development, in the form of genetic or
environmental stress, and the ability for an organism to develop symmetrically (Debat
and David, 2001). Genetic and environmental stressors that cause disruptions in
developmental stability can therefore manifest as bilateral asymmetry. Studies assessing
the magnitude of asymmetry in structures have been used in numerous different scientific
fields, many of which have attempted to associate fluctuating asymmetry with a number
of environmental and genetic factors on a wide variety of species, both extant and
archeological.
2
Many researchers have found fluctuating asymmetry in a variety of structures,
including skeletal and dental traits, to be useful as an indirect measure of environmental
stress in archaeological human populations (Albert and Greene, 1999; DeLeon, 2007;
Hoover et al., 2005; Kujanova et al., 2008; Perzigian, 1977; Sciulli, 1978; Stojanowski et
al., 2007; Suarez, 1974). Clinical and medical studies have found increased FA
associated with wide array of behavioral and physical disorders such as schizophrenia,
Down syndrome, mental retardation, cleft lip, cleft palate, chemical or toxin exposure in
utero, fragile X syndrome, strabismus, and tempromandibular disorders (Angelopoulou
et al., 2009; Barden, 1980; Benderlioglu et al., 2004; Benderlioglu and Nelson, 2003;
Fushima et al., 1999; Heikkinen et al., 2002; Kieser et al., 1997; Livshits et al., 1988;
Naugler and Ludman, 1996; Peretz et al., 2005). In studies of laboratory rats and mice,
researchers have found connections between a variety of developmental and
environmental stressors and increased FA, including extreme exposure to heat, cold,
noise, reduced protein consumption, and intrauterine stress (Sciulli et al., 1979; Siegel
and Doyle, 1975). Increased FA has also been well documented in human inbred
populations (Hershkovitz et al., 1993; Niswander and Chung, 1965; Schaefer et al., 2006;
Suarez, 1974) and in stressed contemporary populations (Baume and Crawford, 1980;
Harris and Nweeia, 1980; Townsend and Brown, 1983). Additionally, studies of FA can
be used equally as well in non-human animals and plants (Falk et al., 1988; Hallgrimsson
et al., 2002; Helsen and Van Dongen 2009; Kark et al., 2001; Lens and Van Dongen,
2000; Swaddle and Witter, 1994)
3
These studies show that fluctuating asymmetry and stress are related, although
specific environmental disturbances that may cause bilateral asymmetries in the dentition
and skeleton of man are not well understood (DiBennardo and Bailit, 1978; Leamy and
Klingenberg, 2005; Lens and Van Dongen, 2000; Palmer and Strobeck, 1986). The
mechanisms, processes, and interaction of developmental stability and buffering capacity
in the face of environmental stress are a confounding presence, and are still debated in the
scientific community. Despite the fact that little is known about the underlying
mechanisms causing FA, most studies have successfully linked FA and increased
environmental stress, leading to the generally accepted study of FA as an indicator of
developmental instability (Leamy and Klingenberg, 2005).
The correlation with stress during development has made FA a popular subject for
studies of humans because of its potential for revealing information about the health of
past populations and its potential to act as an indicator of developmental disorders in
clinical settings (DeLeon, 2007; Palmer and Strobeck, 1986). Of the ways in which to
measure the magnitude of FA in humans, using dental measurements is perhaps the most
common method. Numerous studies have considered fluctuating dental asymmetry as an
indirect measure of environmental and genetic stress in various prehistoric and living
human populations (Barden, 1980; DiBennardo and Bailit, 1978; Doyle and Johnston
1977; Guatelli-Steinberg et al., 2006; Harris and Nweeia, 1980; Hershkovitz et al., 1993;
Townsend and Brown, 1983).
The practical advantages for using dental remains over skeletal remains for FA
analysis are numerous. The human dentition is well studied and well understood, from
4
pathology to development. Teeth begin formation early in life and continue throughout
childhood, providing a relatively long period for stress to be recorded. Once crown
formation is complete, teeth are minimally phenotypically plastic, unlike bone (GuatelliSteinberg et al., 2006; Rose et al., 1985). Lesions and growth disturbances on the
dentition will remain long after the stress episode has occurred. The static nature of teeth
after development provide the perfect setting for measuring minute differences between
sides (FA) and for measuring other pathologies, such as enamel hypoplasia, size
variation, and anomalies. Additionally, the dentition is observable in both adults and subadults, allowing for the study and comparison of permanent and deciduous dentition and
a wide variety of age ranges (Guatelli-Steinberg et al., 2006; Heikkinen et al., 2002;
Sciulli, 1978). Another added benefit is that teeth tend to preserve very well in
archaeological settings. In clinical settings, dental molds can be made that preserve
information the moment the mold was created, acting as a dental snapshot, and allowing
for comparisons to be made later in life or at specific time intervals for the same
individual.
In studies of FA, teeth are welcoming to study because they are bilaterally
symmetrical structures in which the genetic information is the same for both sides,
leading the right and left sides to develop as mirror images under ideal circumstances
(Potter and Nance, 1976). The dentition is thought of as being under tight genetic control,
more likely lending bilateral deviations to environmental stress rather than genetics, and
less likely to be influenced by directional asymmetry (Albert and Greene, 1999;
5
Stojanowski et al., 2007). Yet at the same time, dental tissues are considered sensitive
and seem to respond quickly to stress (Albert and Greene, 1999; Hoover et al., 2005).
Measures of dental asymmetry are easily obtained using the relatively simple
measurements of buccolingual and mesiodistal crown diameters taken with calipers
(Sciulli, 1978). Also commonly known as maximum crown dimensions, this
measurement requires that the tooth be fully erupted. The buccolingual (BL) diameter is
taken from the maximum crown breadth from the cheek (buccal), to the tongue (lingual).
The mesiodistal diameter is measured as the maximum crown breadth front to back, or
from the most mesial to the most distal points on the side of the crown, perpendicular to
the buccolingual diameter (Hillson et al., 2005; Sciulli et al., 1979). For determining
magnitude of FA, both left and right tooth antimeres must be present, tooth wear and
dental calculus should be minimal, and teeth with pathological lesions and anomalies
should be not be considered.
Studies of FA have been employed as an indirect measure of environmental stress
in a variety of archaeological and extant human populations. Modern day examples are
far ranging and include the Inuit, Australian whites and Australian Aboriginals, Japanese,
North Americans, Central and South Americans, Africans, and Europeans. Studies of FA
in archaeological samples include Native Americans, Neanderthals, early American slave
populations, medieval Nubians, prehistoric Japanese, and medieval Central Europeans.
Some asymmetry is normal and expected in human populations (Noss et al., 1983).
Comparative studies of FA must discern developmental stress as opposed to normal
6
human variation; however, normal human variation should not yield statistically
significant bilateral asymmetry (Albert and Greene 1999).
To date, only one study exists including analysis of fluctuating dental asymmetry
in an Imperial Roman population, although there have been an abundance of studies
assessing the stress and diet of Imperial Roman archaeological samples. Hoover et al.
(2005) measured FA in a sample from the necropolis of the Imperial Roman port of Isola
Sacra, dating from the 1st – 3rd century AD, located on the western coast of Italy just
outside of the city of Rome. They were most interested in testing for a correlation
between enamel hypoplasia incidence and severity and dental asymmetry, including FA
and directional asymmetry. Hoover and workers collected data on the teeth most
susceptible to each defect, which included the incisors and canines for enamel
hypoplasia, and the first and second molars for asymmetry. The results of the study failed
to find a significant relationship between enamel hypoplasia and asymmetry for Isola
Sacra. They were able to note the trend that the maxillary teeth were more asymmetrical
than the mandibular teeth for their sample, a similar finding to other published studies of
FA (Groeneveld and Kieser, 1991; Harris and Nweeia, 1980; Kieser et al., 1986; Schaefer
et al., 2006; Sciulli et al., 1979). Hoover and colleagues mention several possibilities as
to why no correlation was found between FA and enamel hypoplasia but state that more
research must be done. They point to the possibility that different timing and growth
sequences might not record growth disturbances in certain teeth, and suggest that
comparing asymmetry and hypoplasia in the same tooth might better capture a correlation
between the two indicators of developmental instability (Hoover et al., 2005). The
7
authors also mention that hypoplasia and asymmetry might be recording different
stresses. For instance, hypoplasia has been shown to have a strong nutritional etiology
while asymmetry has not been found to correlate to a specific stressor (Hoover et al.,
2005). Additionally, the authors note that it is possible that one indicator is more sensitive
to developmental stressors than the other. It may take a very large destabilizing force to
cause enamel hypoplasia, while asymmetry measures smaller, less significant stress
episodes, or vice versa. Lastly, the authors mention differential genetic susceptibility as a
possible factor in their results.
The study of FA, enamel hypoplasia, and stress on Isola Sacra by Hoover et al.
(2005) leaves many questions about the nature of FA in Imperial Roman populations.
Their choice to use only teeth most susceptible to each of the pathologies does not tell us
much about the patterns of fluctuating asymmetry in Imperial Roman samples. Recent
work by Craig et al. (2009) on the diet at the Imperial Roman town of Velia, a coastal
town contemporaneous with Isola Sacra, opens up the opportunity to learn more about
dental asymmetry in Imperial Roman samples and to discover more about the population
of Velia and the developmental instability they may have faced. The necropolis of Velia,
located on the west coast of Italy, with interments dating from the 1st – 2nd century AD, is
an excellent comparison to Isola Sacra. The Romans took control of Velia and it a Roman
trading center and important sea port (Craig et al., 2009; Prowse et al., 2005). Similarly,
Isola Sacra was also a port city. Accounts have described a decline in the welfare of Velia
upon Roman rule (Craig et al., 2009). Tombs and grave inclusions suggest social
congruence between Isola Sacra and Velia, although Craig and colleagues (2009)
8
reported stable isotope analyses of the adults from Velia in which they determined that
Velia citizens had less access to meat and fish than Isola Sacra, with Velia relying more
heavily upon cereals as a staple of their diet. Their heavier reliance on agricultural goods
and cereals will likely have implications on their health status. Both Isola Sacra and Velia
samples are known to have experienced early childhood stress, evidenced by high infant
mortality rates, and previous research recording dental and skeletal pathologies common
throughout the samples (Hoover et al., 2005, Craig et al., 2009).
Project Specifications
This study expects to uphold the positive association of stress and asymmetry by
assessing fluctuating dental asymmetry in a sample of individuals from the necropolis of
Velia in Southern Italy. The purpose was to analyze asymmetry in the adult dentition of a
sample from Velia to record overall magnitude of FA and the presence or absence of
directional asymmetry and antisymmetry. The data were evaluated for patterns such as
sex and size differences in FA frequencies, differences between maxillary and
mandibular teeth, differences between the mesiodistal and buccolingual dimensions, and
correspondence to field theory. The analysis of FA should reveal information about the
health status of the Velia sample, adding to what is already known about this and other
Imperial Roman populations.
9
Chapter 2
LITERARY REVIEW
Directional Asymmetry and Antisymmetry
There are three types of bilateral asymmetry: fluctuating asymmetry,
antisymmetry and directional asymmetry, and of these, only fluctuating asymmetry is
widely regarded as an indicator of developmental instability (Palmer and Strobeck, 1986;
Van Valen, 1962). Because more than one type of asymmetry can be present in a
population, it is important to know which asymmetries are present and what that may
indicate about a sample (Naugler and Ludman, 1996). Directional asymmetry (DA) is
present when there is greater development of a structure on one side over the other. Van
Valen (1962) mentions the mammalian heart as an example of directional asymmetry,
where typically the left side of the heart is larger than the right side. DA is measured as
the signed difference between two sides and is characterized by a nonzero mean with a
normal distribution (Palmer and Strobeck, 1986; Roff and Reale, 2004). Many studies
have related directional asymmetry to purely genetic factors, determining that it is not
reflective of environmental stress, and therefore not an indicator of developmental
instability (Little et al., 2002; Van Valen, 1962). In some cases, directional asymmetry
can also be adaptive, developmentally determined, or mechanically produced, e.g.
handedness (Van Valen, 1962, Falk et al., 1988; Roy et al., 1994).
Many papers on skeletal asymmetry, especially of the limb and hand bones, are
interested in DA because what it infers about natural side preferences and the
10
biomechanical mechanisms of sidedness or handedness (Falk et al., 1988; Roy et al.,
1994). However, a relationship between directional asymmetry and environmental stress
has been linked in a few samples known to have large amounts of stress. This reflects the
possibility that DA may indicate or coincide with extreme stress events and FA, although
this is not well understood or explained by current models and requires more study
(Boklage, 1987; Kujanova et al., 2008; Palmer and Strobeck, 1986; Schaefer et al., 2006).
For example, Schaefer et al. (2006) found significant directional asymmetry to cooccur with fluctuating asymmetry in a highly stressed sample and proposed that
directional asymmetry itself might be a potential indicator of developmental instability.
Schaefer et al. (2006) assessed FA in the dental arch of a reproductively isolated Adriatic
community on the island of Hvar, where inbreeding was common. Their reference
sample, located just off the island on the mainland in Zagreb, while having the same
basic healthcare, was far more heterozygous and therefore could serve as a control for
environmental stress on the island. The authors used early-mixed to complete permanent
dentition of 222 children aged 7-15 years from Hvar and 31 children aged 8-16 years in
the Zagreb reference sample, all in the form of dental casts. They carefully selected
individuals in both samples so that the distribution of dentition and occlusal traits would
match. Schaefer et al. also did an endogamy assessment for all the participating children
to assess the degree of inbreeding and to sort the children into an out bred group, a more
endogamous group, and a less endogamous group, for the purpose of the study. They then
digitized 26 different non-occlusal landmarks and conducted a geometric morphometric
based statistical analysis. The authors noted that shape change during growth is not
11
associated with changes in asymmetry, and that there was no correlation between total
FA and age, overall size of the jaw, or sex in either population. The Hvar sample showed
highly significant directional asymmetry when compared with the Zagreb sample, which
presents no significant DA. As expected, the study found significantly lower FA present
in the Zagreb sample as compared to Hvar, and amongst the Hvar samples, the most
inbred group had the highest FA.
The authors present some interesting findings: they suggest that DA might itself
be an indicator of stress and that the upper jaw appears better buffered than the lower
jaw, which fared worse in almost all the samples. Their findings support the contention
that inbreeding increases FA, and perhaps DA, and that environmental circumstances,
such as poor medical care, likely increase asymmetry (Schaefer et al., 2006). The authors
note that one cannot know, based from this study, whether the increased amounts of FA
and DA are in fact due to stress related to or caused by inbreeding, or by some other
mechanism. Schaefer et al. (2006) speculate that DA might represent population-level
stress, and FA might better signify individual-level stress.
Another example of a project that included the study of DA, coupled with FA, is
the work done by Kujanova et al. (2008). They analyzed limb bone asymmetry in two
samples: a medieval Slavonic sample from the 9th-12th century AD, and a Bohemian
population from the first half of the 20th century. In this case, the more modern sample
was subject to more environmental stress due to low socioeconomic status and other
studies confirming poor general health, than the older but less socioeconomically
impaired medieval Slavonic sample. The authors hypothesized that the modern sample
12
would see increased amounts of asymmetry as compared to the medieval sample.
Kujanova and colleagues found significant amounts of DA in both samples, with an
especially high amount of DA in the upper limb bones, much of which they attributed to
handedness. However, there was a significant increase in DA in both the upper and lower
limb bones of the recent, more environmentally stressed sample, along with significantly
greater amounts of FA. Like Schaefer et al. (2006), this may reflect that DA had a role in
the expression of environmental stress.
In contrast, many researchers have also encountered isolated communities or
highly stressed populations and did not find any significant directional asymmetry,
although FA amounts were considered to be high (Noss et al., 1983; Perzigian, 1977;
Townsend and Brown, 1983). Other studies outline the ambiguous nature of the
relationship between FA and DA. For example, Little et al. (2002) compared Mexican
school children living under chronic mild to moderate undernutrition to a white urban
middle class sample from Texas. They determined FA and DA for numerous different
anthropometric traits, including the long bones of the arm. Values of asymmetry were
actually lower in the chronically undernourished Mexican sample than in the wellnourished Texas sample. The values of DA were overall significantly higher for the
modern Texas sample. The finding of increased DA was perhaps due to the more athletic
and active middle class children in relation to sports and handedness. The authors
attribute the findings in this study to an apparent lack of an effect of environmental stress
on asymmetry, which they feel is consistent with the large genetic component in
measures of asymmetry. Little et al. (2002), Schaefer et al. (2006), and Kujanova et al.
13
(2008) emphasize the equivocal role of directional asymmetry as a potential tool for
measuring developmental instability. Clearly, the position of DA as an indirect indicator
of developmental stress requires further study and attention for future works and
applications.
Whereas FA is largely understood to be an indicator of developmental stability
and DA may or may not be a similarly useful measure in certain characters or
populations, antisymmetry is not employed for such a task. Antisymmetry (AS) is defined
as a situation where asymmetry is present in all individuals, but whether the right or the
left side is greater varies at random among individuals (Naugler and Ludman, 1996; Van
Valen, 1962). An apt example can be found in the signaling claws of male fiddler crabs,
where the large signaling claw, which is significantly larger than the opposing one,
occurs in equal frequencies on both the right and left sides in the population (Palmer and
Strobeck, 1986). Antisymmetry is characterized by a bimodal distribution of R – L,
indicating a negative correlation between two sides, with a mean of zero (Kellner and
Alford, 2003). It is more commonly accepted that antisymmetry has a strong genetic
basis, and is therefore not considered an indicator of developmental instability (Palmer
and Strobeck, 1986).
A different perspective is offered in Lens and Van Dongen (2000), in which the
authors suggest that the three types of asymmetries should be considered interrelated and
may reflect developmental instability in particular environmental conditions. Lens and
Van Dongen (2000), found evidence that very high levels of developmental instability
may not only increase FA, but will transition from FA to an admixture of other
14
asymmetries. While their study on natural bird populations exposed to different levels of
habitat disturbance found AS to be rare, they note experimental studies that have shown a
more complex relationship between the asymmetries. Lens and Van Dongen feel that
more attention should be paid to the interactions of the different asymmetries, rather than
simply discarding or correcting for them.
More research must be done in order to better understand the relationship between
the asymmetries and to determine if antisymmetry or directional asymmetry are useful as
estimates of developmental instability. However, as of yet, there is not an unequivocal
environmental basis for antisymmetry, and only a potential, weak, or poorly understood
environmental connection for directional asymmetry. Only FA is considered a reliable
indicator of developmental instability. In order to determine true FA in a sample, tests for
FA must first consider the presence of antisymmetry and DA, as these asymmetries can
have a confounding effect on measures of FA. Common practice is to statistically correct
for traits exhibiting DA in order to determine true FA, and in the case of antisymmetry,
such traits are simply discarded from the analysis of studies of FA since no mathematical
correction exists (Palmer and Strobeck, 1986). Antisymmetry and DA are not commonly
found in studies of the human dentition and would not be expected in any significant
values in the Velia sample. For the purposes of this paper in determining the nature of the
health status of the necropolis at Velia, FA warrants deeper discussion.
15
Fluctuating Asymmetry
Fluctuating asymmetry is minor, random, non-directional deviations from
bilateral symmetry (Van Valen, 1962). It has been established since the 1950s as a
measure of developmental instability, also commonly termed ‘developmental noise’ (Van
Valen, 1962). Genetic studies have shown that minor, random deviations from bilateral
symmetry have little or no genetic basis, indicating that bilateral symmetry differs from
most other morphological attributes in its lack of a heritable basis (Palmer and Strobeck,
1986; Potter and Nance, 1976). While the heritability of FA itself is generally considered
low or absent (Leamy and Klingenberg 2005; Potter and Nance, 1976; Potter et al.,
1976), FA is not a simple measure of environmental insult, since studies have shown that
the likelihood and degree to which an individual departs from bilateral symmetry, in
either direction, has a strong genetic basis (Naugler and Ludman, 1996; Potter and Nance,
1976; Potter et al., 1976). Genetic factors certainly influence the canalization and
developmental stability of an organism. Individuals respond to stressors differently and
there are inherent individual and populational differences in resisting the effects of
developmental stress (Van Valen, 1962). Any study of asymmetry must consider that
canalization and developmental stability are at play in the expression of asymmetry, and
therefore, one cannot separate out the influence of genetics on the study of FA (Palmer
and Strobeck, 1986; Van Valen, 1962). For this reason, comparisons between populations
should be made only between genetically similar populations.
The ability of an organism to buffer against insult appears to be strongly of
genetic composition (Palmer and Strobeck, 1986). Central to the mechanism behind
16
asymmetry are the components of developmental homeostasis, canalization, and
developmental stability (Clarke 1993; Debat and David 2001). Canalization is the process
by which a consistent phenotype is produced despite variable genetic and environmental
factors. Canalization acts as a stabilizing force, enacting mechanisms that keep the
phenotype consistent in spite of disturbances, therefore working to maintain
developmental homeostasis (Clarke 1993; Debat and David 2001; Van Valen, 1962).
Destabilizing forces interact with stabilizing forces and influence the expression of the
phenotype, and depending on how well buffered an individual is, developmental stresses
can interfere with the phenotype so that skeletal and dental features deviate from their
ideal genetic form to varying degrees (Naugler and Ludman, 1996; Van Valen, 1962).
Destabilizing forces can be genetic in nature, such as the homozygosity of deleterious
alleles, or any number of environmental factors, such as malnutrition, poor prenatal and
maternal conditions, socioeconomic level, disease, parasite load, and toxin exposure.
There are several important older studies that lay the foundation for the inclusion
of FA as an indirect indicator of developmental instability. One of the pioneering works
was Van Valen’s 1962 study of fluctuating asymmetry. Van Valen (1962) was among the
first to clearly define the three types of asymmetry, directional, fluctuating, and
antisymmetry. The study measured a variety structures in three different species, fruit
flies, deer mice, and an extinct horse species. The latter two were analyzed by dental
measurements and traits. Van Valen assessed FA in terms of buffering ability and
attempted to measure correlations between the three species. The study found uniformity
in the lack of control for the buffering of developmental noise, indicating that FA was
17
present in all three species (Van Valen, 1962). The theory behind the measurement of
asymmetry which Van Valen so eloquently elaborated in this paper led the way for other
workers to begin to analyze FA on a variety of samples and traits.
Niswander and Chung (1965) hoped to learn more about the environmental and
genetic factors affecting tooth size. Using a large Japanese sample with family relation
mapped, Niswander and Chung measured the mesiodistal dimension of the central
incisors. They found increased variation in tooth size among first cousin marriages,
which constitute low levels of inbreeding. They also found significant dental asymmetry
that could not be accounted for by inbreeding. The authors suggest the possibility that
inbred individuals are more poorly buffered during development and therefore more
subject to fluctuating asymmetry (Niswander and Chung, 1965).
Garn et al. (1966) examined dental asymmetries on modern Ohio whites to see if
asymmetries follow field theory of dentition, a hypothesis of dental patterning describing
the differing stability of individual teeth. They analyzed the mesiodistal dimension of
unworn teeth in Ohio whites and found an increase in FA in the maxillary teeth, and a
correlation between increased size and increased FA. Although they looked, they found
no significant correlation of asymmetrical variation between adjacent teeth. Their
findings are one of the first of many that are consistent with field theory as it concerns
FA.
Starting in the 1960’s, examinations of FA branched out and researchers began
looking at a diverse lot of traits and organisms, comparing the study of asymmetry to
other known indicators of instability, determining genetic influence, and conducting
18
experiments attempting to isolate FA causing stressors. Much experimental laboratory
work with rats and mice was done in this time period. Bader (1965) found that inbred
lines of mice have greater asymmetry than wild or random bred mice populations. Leamy
and Bader (1968) determined the variance of the widths of the second and third molars in
a wild-derived population of the white-footed mouse. Their sample size was large and
spread over three generations, and the authors were able to determine heritability
estimates. They found that approximately 11% of M2 and 5% of M3 variance was
attributable to fluctuating asymmetry. Higher amounts of variation could be attributed to
heritability and maternal effects (Leamy and Bader, 1968). Leamy and Bader note that
the amounts of FA found are similar to the amounts found in other mouse species and in
man. In an attempt to isolate specific stressors that cause developmental instability
leading to FA, Siegel and Smookler (1973) produced an increase in the magnitude of FA
in rats exposed to audiogenic stress. Shortly thereafter, Siegel and Doyle (1975) found an
increase in the magnitude of FA with prolonged cold stress in mice. Sciulli et al. (1979)
designed an experiment in which pregnant rats were stressed using combinations of heat,
cold, noise, and protein deprivation. While no directional asymmetry was found, all of
the protocols significantly elevated FA in the young (Sciulli et al., 1979). They were also
able to determine that not all tooth dimensions respond to stress to the same degree. In
this study, mandibular M1 appeared most stable. These researchers all postulated that
increased dental FA is a developmental response of the animal to stress, and that stress
causes the deviations from symmetry in the dentition.
19
Another pioneering work was done by Potter and Nance using Australian twin
pairs (1976). They set out to estimate three parameters within monozygotic and dizygotic
twin pairs, discordance, asymmetry, and mirror imagery (Potter and Nance, 1976). Potter
and Nance showed that dizygotic twins had greater discordance in all the variables
studied, lending credence to the strong genetic control of the dental dimensions, namely
the buccolingual and mesiodistal measurements used in this study. However, the results
for mirror imagery and asymmetry found that there was no evidence for a genetic
etiology of asymmetry on tooth dimensions (Potter and Nance, 1976). The authors
therefore attributed the FA to developmental noise from environmental factors. This
determination helped to pave the way for the popularity of FA since there was now
seemingly little question about FA’s environmental etiology, and its ability to indicate
developmental instability from environmental perturbations. The twin studies of Potter
and Nance (1976) have shown that human odontometric asymmetry itself is not
genetically inherited.
Potter and colleagues followed this study up with another using the same twin
data. In this second paper Potter et al. (1976) assessed the genetic determinants of the
maxillary and the mandibular dentition. They concluded that the maxillary dentition and
the mandibular dentition appear to be relatively independent of each other. Potter and
colleagues also feel their results suggest a differential degree of stability between the
maxillary and mandibular dentition, as evidenced repeatedly in a variety of studies of FA,
where most often, the maxillary teeth show greater variability (Garn et al., 1966; Harris
and Nweeia, 1980; Potter et al., 1976).
20
Perzigian (1977) analyzed and compared odontometric fluctuating asymmetry in
three different North American archaeological sites, Indian Knoll, Campbell, and Larson,
and compares these with a Caucasian portion of the Hamann – Todd collection. These
samples differ socio-economically and nutritionally as the Indian Knoll sample is made
up of hunters-gatherers, while Campbell and Larson represent samples from farming
based subsistence, and Hamann – Todd is a modern sample of Ohio whites. Perzigian
found no directional asymmetry and no differences between the sexes, but the huntergathering Indian Knoll sample was shown to have increased asymmetry while there were
no significant differences between Campbell, Larson, and Hamann – Todd (Perzigian,
1977). The author expected these results because of the accompanying prevalence of
skeletal and dental paleopathological data from the Indian Knoll sample. Taking this one
step further, the author analyzed femur length and asymmetry in the Indian Knoll sample,
comparing asymmetry in a group of individuals with shorter femurs versus a group with
larger femurs. Femur length is tied into stature, and decreased stature can be due to
nutritional stress and poor condition. Perzigian found a clear relationship between shorter
femur length and increased odontometric FA. The author expressed a confident link
between FA and environmental conditions.
Similarly, Doyle and Johnston (1977) and Suarez (1974) analyzed native
Americans, Eskimos, Ohio whites, and Neanderthals for dental asymmetry, finding, as
expected, less asymmetry in the modern Ohio sample than in the other populations.
Suarez argued for particularly significant asymmetry in Neanderthal data due to a
21
proposed increase in environmental stress. However, this conclusion is weak due to
problems with sample size in the Neanderthal collection.
Harris and Nweeia (1980) wrote an excellent example of a relatively simple older
study of FA in dentition. Harris and Nweeia measure the maximum mesiodistal (MD) and
buccolingual (BL) crown diameters for all permanent teeth in 57 extant Ticuna adults.
Based on earlier medical examinations of the Ticuna, and of knowledge about their diet
and social structure, Harris and Nweeia hypothesize that dental FA will be higher
amongst Ticuna than contemporary Western standards and that Ticuna females will have
more FA than Ticuna males (Harris and Nweeia, 1980). The authors employ a simple
equation that measures the difference between the left and right antimeres while negating
the effects of size differences among teeth. The mean is analyzed and is found not to be
significantly different than zero in any of the measurements, indicating that there is no
directional asymmetry at play and establishing that only random side differences exist.
Harris and Nweeia then compare the Ticuna data with three other groups, contemporary
white Americans, prehistoric Hopi Indians, and prehistoric Alaskan Eskimo. The Ticuna
exhibit less FA than either of the two prehistoric groups, all three of which have
significantly more FA than the contemporary American Whites, as expected (Harris and
Nweeia, 1980). For the within-population analysis, Harris and Nweeia employ a three
way analysis of variance to gain insight on FA differences in sex, arcade, and tooth. They
find that the MD measurement is the most statistically significant in all three variables,
whereas only tooth type differences are significant with BL breadths. Females had
significantly higher FA than males, but only for the MD diameter, and both arcades have
22
significant asymmetry differences, with the maxillary teeth having increased FA as
compared to the mandibular teeth (Harris and Nweeia, 1980). Interestingly, among the
different individual teeth, sex is not significant in either MD or BL diameters and there
are markedly higher rates of FA among M2 and M3 than among M1, P3, P4, C, I1 and I2.
The canines appear the most stable, having the lowest frequency of FA than any of the
teeth. The trend of maxillary teeth being more asymmetric overall continues for the tooth
by tooth analysis. The authors note that tooth morphology might be a significant variable
in these measurements where the variability of a cusp, for instance, will affect molar
breadth and length. Major conclusions from this study include that, at least for the
Ticuna, maxillary teeth are more asymmetric, especially with the mesiodistal
measurement. Also, there appears to be significant differences in tooth type, reflecting
that some teeth may be more susceptible to asymmetry than others. Finally, tooth
morphology must not go without consideration when using simple measurements such as
BL and MD diameters.
Several studies examined FA in conjunction with morphological variation or
discrete dental traits. Noss et al. (1983) addresses asymmetry in MD and BL crown
diameters in addition to asymmetry in morphological traits. The authors consider
measurements of asymmetry only in the maxillary and mandibular M1 and M2. They are
particularly interested in learning more about the relationship, if any, between
morphological asymmetry and asymmetry in dental dimensions in addition to learning
more about dental asymmetries in the Pima Indians of Arizona. They measured BL and
MD diameters in casts of 738 males and 790 females and scored for grades of
23
morphological trait expression. The authors found that DA was not present and no
differences between males and females were detected with either measurement, however
M2 was found to have higher FA frequencies as compared to M1 (Noss et al., 1983).
Noss and coworkers found no evidence of a relationship between morphological
asymmetry and measurements of FA for the Pima Indians. They mention the possibility
that timing of tooth formation and mineralization, as well as individual buffering, or
perhaps the different mechanisms of each combined might cause the lack of relationship
between FA and morphological asymmetry. It is interesting to note that the authors found
an abnormal distribution in dimensional and morphological measurements and traits,
indicating that the Pima Indians might have asymmetries resulting from several different
sources.
Townsend and Brown (1983) were interested in size differences and
morphological variation and their potential effect on analyses and measurements of
asymmetry. Other studies, such as Albert and Greene (1999) and Harris and Nweeia
(1980), have disagreements as to whether differences in size and morphology affect
measurements of FA. In their study, Townsend and Brown (1983) assessed contemporary
Australian Aboriginals for molar size sequencing and asymmetry. The authors measured
MD diameters, BL diameters, and crown areas (product of the diameters) for differences
in sizing of M1, M2 and M3, and for asymmetry. They had a large sample size of males
and females, and used dental casts to gather measurements. The authors note that
variability in tooth size can be of genetic and environmental etiology, and that recent and
historic Aboriginal populations tend to display considerable variation in tooth size
24
(Townsend and Brown, 1983). Frequency of asymmetry in molar size sequence was
measured for individuals for M1 and M2 and also for all three molars in a quadrant. For
the total sample, the authors found that the frequencies of M2 > M1 were lower in the
mandible. For a comparison of the sexes within the MD measurement, there were no
statistically significant differences between the sexes in the frequency of M2 > M1
sequence of maxillary molars, but this sequence was significantly more frequent in
females in the mandibular dentition. For the BL measurement, the M2 > M1 sequence
was significantly more frequent in males in both the upper and lower jaws. The
consideration of all three molars yielded high rates of asymmetry within all factors
(mandibular, maxillary, BL, and MD), with the M1 showing the least asymmetry.
Asymmetry for the sequences was high, but no analysis was attempted to determine FA
from the left and right variability in the sample or to distinguish FA from DA as this was
not the focus of the study. This paper lends credence to the stability of M1 and notes the
importance of tooth morphology on MD and BL based measurements for determining
tooth sequence, variation, and asymmetry.
Not all researchers have found a clear connection between FA and environmental
stress. DiBennardo and Bailit (1978) noted that the critical period of dental development
falls during prenatal life, when teeth are beginning to form in the womb. This is the time
in which asymmetries from developmental disruptions would begin to take shape. To
determine the effect of stress on dental asymmetry, they chose to look at several factors
during and after gestation, such as birth weight, gestational age, sex, maternal age, and
socioeconomic factors, in a Japanese sample after widespread radiation from the atomic
25
bomb in Hiroshima and Nagasaki (DiBennardo and Bailit, 1978). They found that dental
asymmetry did not relate to prenatal stress as they had hoped to capture it with the
numerous factors they assessed. They concluded that the level of individual asymmetry
does not reflect individual fitness or risk. The authors felt that FA as a measure of
buffering ability or fitness was equivocal and they suggest future research be conducted
to pinpoint the specific environmental causes of asymmetry. Similarly, Angelopoulou et
al. (2009) could not find a significant correlation between radiation exposure from the
Chernobyl accident and fluctuating asymmetry in their study of FA in Greek children.
While environmental radioactivity is considered a health risk and increased radionuclides
were found in human tissue samples from Greece after the Chernobyl accident, the
experimental group did not have significantly different amounts of FA than the control
group (Angelopoulou et al., 2009).
Other workers have also had mixed results. Black (1980) assessed dental FA in
white children from Michigan. Black determined that FA was higher in the Michigan
children than in Hamann and Indian Knoll population despite the fact that his sample was
not stressed. Jantz (1975) looked at digital ridge-counts for several groups from diverse
racial backgrounds and found considerable population variation, leading him to suggest
genetic control rather than environmental basis for all asymmetrical variation.
26
Asymmetry in Non-Dental Structures
In addition to non-human experiments, researchers began measuring a variety of
traits to study FA. Several key studies have successfully assessed FA using skeletal traits.
In addition to Little et al. (2002), Schaefer et al. (2006), and Kujanova et al. (2008) which
have already been described, Albert and Greene (1999) examined FA in the epiphyseal
union intending to show that FA is an indicator of environmental stress. The authors
looked at a population previously identified as under developmental stress, the Medieval
Kulubnarti from Nubia. The skeletal sample was comprised of an earlier period, called
the early Christian period, and a later period called the late Christian period. The authors
speculated that the earlier period samples would show increased asymmetry as compared
to the later period. Like the Schaefer et al. (2006), this analysis will also involve FA as an
indicator of stress in a sub-adult sample, this time assessing epiphyseal union in paired
bones. The authors note that in past studies, the normal amount of human variation in
skeletal maturation has not produced statistically significant differences in bilateral
asymmetry (Albert and Greene, 1999). Their sample size totaled 90, 36 individuals in the
early Christian period and 54 individuals comprising the late period sample with age
variation between 11 and 31 years. Four stages of epiphyseal union were outlined and the
sample was scored for epiphyseal union of the long bones, iliac crests, ischial
tuberosities, and medial clavicler epiphyses (they listed either proximal or distal or both).
Individuals were scored for right and left sides and this score was statistically analyzed.
For the entire sample, the authors found statistically significant bilateral asymmetry, and
tested separately, the early period was found to have significantly more asymmetry than
27
the late period (Albert and Greene, 1999). This is consistent with earlier findings from
Kulubnarti showing that the earlier period inhabitants were under more stress. There were
no significant differences in asymmetry between males and females in either sample,
however, the study found interesting differences in epiphyseal union between right and
left sides in the early period sample. This suggests that there were asymmetries in skeletal
growth and maturation for the early sample. It seems unlikely that such phenomena
would be from a biomechanics related cause, such as right-handedness for example, since
one sample did not present as statistically significant but the other did. From this, the
authors feel that the skeletal asymmetry evidenced in this study is most likely due to
environmental stress. Since it has been documented that both of these samples were under
stress, albeit one greater than the other, the findings suggest that asymmetry might not be
expressed in epiphyseal union except under a very pronounced degree of environmental
stress (Albert and Greene, 1999).
DeLeon (2007) analyzed fluctuating asymmetry in the craniofacial skeleton. The
sample consisted of two diachronic Nubian cemeteries from Kulubnarti, an earlier and
more developmentally stressed group, termed the “S” cemetery, and a later group
considered to be in better overall health, termed the “R” cemetery. DeLeon notes the
numerous bioarchaeological studies comparing the two different samples stress levels and
health status. The author expects to see increased magnitude of FA in the earlier Nubian
population as compared to the later, healthier population. Choosing thirty adult skeletons
of comparable age and sex from each population for a total sample size of 60 individuals,
DeLeon used three-dimensional coordinate data from the measurement of 48 midline and
28
bilateral landmarks of the skull and analyzed this data using EDMA. She tested for
measurement error and for directional asymmetry. The results showed that more
landmarks showed FA in the earlier group than in the late period group, and that the
earlier group also had significantly greater levels of FA, findings which support
DeLeon’s original hypothesis. The author looked further and noticed that presence and
amount of FA was dependent upon which landmark was being analyzed, with little FA
showing in either population along the midline landmarks. This indicates that FA is trait
specific. In other words, DeLeon found that certain landmarks are more sensitive
indicators of stress than others. She proceeds to discuss several mechanisms which might
explain this phenomena: the functionality hypothesis, which postures that natural
selection would reduce FA where it is involved in important biological functions relevant
to the fitness of an organism, the signaling hypothesis, in which natural selection would
work to reduce FA in the most visible areas for the importance of signaling and sexual
selection, and the complexity hypothesis, where traits of greater complexity would be
expected to have lower levels of FA relative to simple traits because complex traits are
made up of multiple components that may or may not be influenced by FA (DeLeon,
2007). DeLeon notes which areas of the skull would be considered simple traits, such as
the neurocranium due to its fewer osteogenic sites, and which would be complex traits,
like the facial skeleton because the face is formed from multiple osteogenic sites. As it
concerns the data, DeLeon finds that the complexity hypothesis does not quite accurately
explain the results because of the relatively high levels of FA in the complex landmarks
that extend from the cranial vault to the face. Of the other two hypotheses, the author
29
feels that the signaling hypothesis best explains the pattern of FA in the study. Areas of
the face close to the midline, important for both function and signaling, showed
significantly less FA while areas not involved with signaling, but heavily involved with
function, such as the cranial base, did not have low FA. DeLeon notes that additional
work should be done to further test these hypotheses as they relate to differential levels of
FA and trait specificity and feels that the results presented provide support for the use of
FA as an indicator of developmental instability and stress.
Hoover and Matsumura (2008) looked at a group of prehistoric Japanese
archaeological samples and conducted a comparison of FA from cranial traits with a
dental lesion called linear enamel hypoplasia, also considered an indirect indicator of
stress during tooth development. The authors note that previous studies have only found a
weak link between odontometric FA and enamel hypoplasia, despite both being of the
dentition, and both being widely considered indicators of developmental instability
(Corruccini et al. 2005; Hoover et al., 2005). Using DeLeon’s study (2007) as evidence
for the stress based etiology for FA in cranial landmarks, Hoover and Matsumura
measured upper facial breadth, orbital breadth, and orbital height and compared their
findings to enamel hypoplasia data from the maxillary and mandibular anterior dentitions.
They expected that individuals with hypoplasia would have greater overall FA. In this
sampling, they found a weak, albeit significant, association between FA and enamel
hypoplasia. Additionally, the findings did not corroborate their hypothesis, which
supposed that increased magnitude of fluctuating asymmetry would be found in the more
stressed group, while, on the other hand, the enamel hypoplasia increased dramatically
30
within this highly stressed group. Hoover and Matsumura note that their sample sizes
were small, perhaps confounding their results, but feel that their data support the
hypothesis that greater FA occurs in individuals with nutritionally based enamel defects
(Hoover and Matsumura, 2008).
Common Problems and Error in Studies of FA
Analysis of fluctuating asymmetry is subject to certain unique issues and
concerns. MD and BL measurements can easily be affected by various morphological
traits and dental pathology such as the buildup of dental calculus, caries, and LEH
(Corruccini et al. 2005; Harris and Nweeia, 1980; Hillson et al., 2005). Researchers have
to be careful to remove affected teeth from consideration in the study. Additionally,
unlike many skeletal traits used in the study of FA, teeth suffer from relatively poorly
defined landmarks, making them subject to greater measurement error and operator bias
(Falk and Corruccini, 1982).
Early studies of asymmetry tended to focus on the connection between FA and
environmental stress. In these early studies, workers measuring asymmetry in the
dentition tended to view tooth pairs as independent variables and did not remove the
effect of tooth size differences in their computation or analysis of asymmetry. Many early
researchers failed to recognize the relationship between increased tooth size and
increased metric variation. It would be expected that larger teeth would have greater FA;
since crowns grow at a constant rate, a larger tooth will have a longer growth period
(Garn et al., 1966; Rose et al., 1985). Longer growth periods allow for additional
31
episodes of childhood or maternal stress to be recorded in the teeth (Garn et al., 1966).
Additionally, character size differences often occur within populations and between
populations. It is well understood that there is sexual dimorphism in crown diameters.
Generally researchers have since decided that tooth size should be considered in studies
of FA where there is an apparent size-asymmetry relationship, and have scaled
differences by dividing by average tooth size (Harris and Nweeia, 1980; Palmer and
Strobeck, 1986; Smith et al., 1982). This eliminates the measurement differences between
the sexes and between tooth size differences so that one can better compare FA between
individuals, sexes, and between different sample populations.
Additionally, many early works only measured one variable. Leung et al. (2000)
convincingly demonstrated via computer simulation that it is more effective to use
multiple traits for the analysis of FA as an indicator of environmental stress. Since FA is
rare and occurs in very small amounts when compared to trait size, it can be difficult to
detect using a single paired trait (Leung et al., 2000). Employing the right set of traits is
also of importance, since one would want to avoid a trait showing tendencies for DA and
antisymmetry, which reflect heritable variation instead of variation from developmental
instability (Palmer, 1994). Using multiple traits and appropriate analyses for those traits
can help to maximize the reliability of FA as an indirect measure of developmental stress.
Smith and coworkers (1982) pointed out the numerous problems with the models
and statistics of many of the studies that predate their own. Since then, Greene (1984) has
also spoken out about how easily measurement error can confound FA data. Others have
voiced criticisms of dental FA as well. Buschang and Demirjian (1989) and Naugler and
32
Ludman (1996) feel that studies of dental FA suffer due to the prolonged developmental
time frame of teeth, which might obscure links between increased FA and episodes of
specific insult. Others are apt to point out that deciduous teeth, which form much faster
than permanent dentition, appear neither better or less buffered against developmental
instability in numerous studies (Guatelli-Steinberg et al., 2006; Hershkovitz et al., 1993),
indicating that the length of time for tooth development does not affect the magnitude of
FA.
Because differences in FA among samples are typically very small, antisymmetry,
DA, and measurement error can make up a sizable portion of the between-sides, or within
individual, variance in a sample (Palmer and Strobeck, 1986). Since FA is very small
compared to the size of the trait being measured, typically around 1% of trait size,
measurement error is of particular concern (Greene, 1984; Palmer and Strobeck, 1986).
In 1965, Bader determined that measurement error accounted for up to 25% of dental
fluctuating asymmetry counts in a wild mouse population and Greene (1984) found
similar results in human studies. It has been strongly suggested that measurements should
be replicated and tested to discern true asymmetry from measurement error (Greene,
1984; Palmer and Strobeck, 1986; Swaddle et al., 1994).
Smith et al. (1982) argue that differences in dental asymmetry could be explained
by sampling effects on the small sample sizes typically used. Additionally, they note that
measurement error itself can mimic FA and that sampling effects can obscure true FA if
the average amounts of FA are small (Smith et al., 1982). It has been shown that the
index chosen can also have an effect on true measures of FA.
33
Palmer and Strobeck (1986), interested in obtaining the best estimate of FA,
review the various indices used for the analysis of FA and survey the differences between
the indices, as well as suggest a recommended course of statistical analysis for obtaining
the best estimates of FA while checking for DA, measurement error, and antisymmetry.
Palmer and Strobeck are also interested in determining how the various indices account
for and deal with variation in character size. Such a wide variety of measures of FA are
used in literature, each with different strengths, weaknesses, and underlying assumptions.
At the time their paper was written, the authors counted 22 different indices used in
previous studies and determined that these 22 are variants of 9 main indices. They assess
the 9 main indices for their ability to detect true differences in FA frequencies among a
random sample. Palmer and Strobeck simulated 2 samples for which the differences in
FA were known. The samples did not contain any antisymmetry but do consider two
variations: FA independent of size, and FA proportional to size. In testing the 9 indices,
the authors varied the range of character size, the proportionality of FA to character size,
DA, and FA, while maintaining the mean character size as constant. A sample size of 20
was chosen because the authors found that to be a common sample size in studies of FA.
The tests were repeated 100 times using different distributions of random numbers. They
found that indices based on unsigned R – L differences were least able to distinguish true
FA differences, while indices based on the variance of R – L are more useful for
detecting true differences in FA. The authors then analyze the effect of character size
variation among the indices when FA is independent of size and when FA increases
proportionally to size, finding that indices scaling out character size were more reliable
34
for both. The various indices also handled DA differently, some not registering DA while
other indices were found to be very sensitive to DA.
Based on their findings, Palmer and Strobeck (1986) make recommendations as to
what index to use depending on the pattern of size variation within a sample. Firstly, they
recommend testing for a relationship between the magnitude of FA and the character size.
Since increased character size often correlates to increases in FA, the authors stress the
importance of scaling for size variation. To determine true FA from measurement error,
antisymmetry, and DA within samples, Palmer and Strobeck suggest using a two-way
mixed-model analysis of variance with repeated measurements of each side. The authors
state that this method is best used in sample sizes greater than 25. Finally, Palmer and
Strobeck also discuss tests and patterns of heterozygosity as it relates to FA. They noted a
lack of consistency among studies of FA, and emphasize that FA as a measure of
developmental stability is easy confounded by the fact that differences in FA among
samples are generally very small, and as such, the measurement of FA is easily
confounded by antisymmetry, DA, and measurement error.
Patterns of Dental FA
There appears to be very few intra-population consistencies with the measured
presence of FA, as noted by Black (1980), Palmer and Strobeck (1986), and others. Some
researchers have found MD measurements to show more FA, while others have found BL
measurements to do so. Some individuals can have FA in one tooth dimension and none
or a different amount in the other dimension in the exact same tooth. Similarly it seems to
35
be sample dependent as to whether the maxillary or mandibular teeth are found to show
more FA, or what quadrants and tooth classes are better buffered against stress during
development. Indeed, this is where the genetic complexity of the dentition is underscored,
at the level of both the individual and the population. Lack of patterns in tooth type,
arcade, and FA support the contention that tooth dimensions along the two arcades are
primarily independently determined (Kieser at al., 1986; Stojanowski, 2007). Townsend
and colleagues (2009) describe the varying nature of the molecular signaling in the upper
and lower jaw, suggesting, along with twin data, the independent genetic determination
of maxillary and mandibular dentition (Townsend et al., 2009). The bucco-lingual and
mesio-distal measurements themselves might have innate differences, with the BL
dimension perhaps more affected by environmental factors than the MD dimension,
possibly due to the spatial constraints on the MD dimension (Kolakowski and Bailit,
1981; Perzigian, 1977).
In some cases where, for instance, it was expected that females would have more
FA due to historically known increased stress, this was in fact not found to be the case, or
not the case in both dimensions or some tooth classes. Most researchers have not found
significant differences in FA between the sexes, and those studies that have significant
differences in FA between the sexes might in part be noticing that trend because of
cultural differences in the raising of children or in biological population differences (Noss
et al., 1983). Notable exceptions to this are Harris and Nweeia (1980), who found
statistically significant differences between males and females, as did Garn et al. (1966)
and Niswander and Chung (1965).
36
One of the few consistencies in the analyses of dental FA is that asymmetry often
conforms to dental field theory, a theory explaining the patterning and regional
specialization of teeth. Field theory, according to Dahlberg (1945), who first adapted the
idea of field theory to the adult human dentition, states that a tooth growing in the center
of a field, also known as the pole or key tooth, would be expected to show less
phenotypic variation than the teeth on either side. The further from the center in a
particular field, the more variable the teeth should be. In humans, four fields have been
identified: incisor, canine, premolar, molar (Dahlberg, 1945). Within the fields, the upper
central incisor, lower lateral incisor, canine, first premolar and first molar have been
identified as the pole teeth. Pole teeth are presumed to be the most stable teeth in each
field and would be expected to be better buffered against environmental perturbations
(Townsend et al., 2009). While field theory has a complex developmental etiology that is
still debated, few disagree that this order or patterning exists within the human dentition
(Townsend et al., 2009). Dental crown size, variability, and asymmetry have often been
found to conform to field theory (Aas and Risnes, 1979; Barden, 1980; Garn et al., 1966;
Garn et al., 1967; Groeneveld and Kieser, 1991; Kieser et al., 1986; Mayhall and
Saunders, 1986; Townsend et al., 2009). Interestingly, some other indirect indicators of
developmental stress, such as linear enamel hypoplasia, seem to present most often in the
pole teeth, central incisors, canines, and the first molar (Hoover et al. 2005).
In most studies of dental FA, there are fairly consistent findings that pole teeth
generally seem to be less influenced by systemic developmental stress as measured by
fluctuating asymmetry. The existence of the developmental patterning of pole-teeth and
37
non pole-teeth most likely represent the relative amount of time that each developing
tooth germ spends in the soft tissue phase of growth, prior to mineralization (Townsend
et al., 2009). The longer the soft tissue phase, the more time there is for epigenetic and
environmental factors to influence the tooth’s final shape and size. There appears to be no
relationship with FA between adjacent teeth or patterning indicating the necessary
increase of FA distally in the arcade (Townsend et al., 2009). Serial increases in FA
frequency across the arcade or between pole teeth and their neighbors have also not been
shown, and asymmetry in tooth dimensions has not been shown to influence the size of a
neighboring tooth (Townsend et al., 2009).
There also seems to be consistency that the molars, particularly the second and
third molars, show increased amounts of FA as compared to other teeth. However, higher
rates of FA in the molars more likely represent at least in part, some bias of the
measurement since they are also the most morphologically variable (Mayhall and
Saunders, 1986; Noss et al., 1983; Townsend and Brown, 1983; Townsend et al., 2009),
and it is widely agreed that certain morphological characteristics can influence MD and
BL measurements, as already discussed. Third molars are the last teeth to erupt and their
eruption time is the most variable of any tooth (Townsend et al., 2009). Their
morphology is highly variable, more than any other tooth, and they are also the most
commonly cogenitally missing tooth (Townsend et al., 2009). As such, for the purposes
of assessing FA, third molar measurements are often omitted altogether or are considered
of limited usefulness.
38
Italian Literature
Many skeletal samples from the Imperial Roman era have been well documented
and studied and can shed light on typical health status, socioeconomic status, and diet of
samples from the same time period. The skeletal sample from Isola Sacra, an Imperial
Roman necropolis, dating to the 1st through 3rd century AD has been well studied. There
is a large amount of data available to assist in the characterization of Isola Sacra,
including its similarities to other Roman or Italian samples, genetic composition, diet,
health status, social habits, and demography (Bondioli et al., 2004; Cucina et al., 2005;
Manzi et al., 1991; Manzi et al., 1997; Manzi et al., 1999; Prowse, 2001, Prowse et al.,
2007; Prowse et al., 2008). These characterizations can assist with expectations for the
study of FA in a sample from Velia, which is from the same time period and is
socioeconomically and genetically similar to the Isola Sacra sample.
Manzi et al. (1997) and Prowse et al. (2007) describe the homogeneity and
immigration patterns from Isola Sacra and other Imperial Roman samples. Manzi and
workers examined dental size and shape at Isola Sacra and another site in close proximity
to Rome, Lucus Feroniae, both of which date to the 1st – 3rd century A.D. (Manzi et al.,
1997). Isola Sacra is considered by the authors to represent a middle-class urban sample
while the sample at Lucus Feroniae is more rural and suggests humble origins such as
slaves, farmers, and war veterans. The authors took BL and MD measurements for the
permanent dentition and the teeth were also scored for nonmetric traits. The authors feel
that analysis of both dental dimensions and morphology will provide a basis for the
39
characterization of dental variation in Italian samples from the Roman Imperial age.
Analysis determined that these two Roman samples are rather homogeneous in their
dental morphology, and there is a noted absence of rare phenotypic variants. Both
samples were found to have very small dental dimensions in general, and the authors
correlate this to the trend of dental size reduction in human populations. Another
possibility for the small dental dimensions found in both samples is the possibility that
they were undergoing metabolic disturbances during growth and development, which has
been shown in other populations to reduce dental dimensions (Manzi et al., 1997). The
authors point out that stress markers on the bones and teeth, such as linear enamel
hypoplasia and Harris lines, can be found in similarly high quantities in both samples.
Enamel hypoplasia is found in greater quantities in the males of both samples. Despite
this, Manzi et al. note that Isola Sacra was less variable than Lucus Feroniae in both
dental morphology and in dental dimensions, suggesting that the gene pool of the Isola
Sacra sample was more homogeneous than that of Lucus Feroniae. While this study helps
determine that the sample of Isola Sacra is fairly homogeneous compared to its neighbor
Lucus Feroniae, and that the dentition during this time period show marked progression
towards reduction, a series of studies by Prowse and colleagues more aptly describe the
basic tenants of the sample of Isola Sacra, including immigration and diet.
Prowse et al. (2007) analyzed the Isola Sacra sample for patterns of migration and
geographic provenience using oxygen stable isotope ratios measured in tooth enamel.
Oxygen stable isotopes are acquired from drinking water, and record the water sources
available during a particular time and place. The authors analyzed oxygen ratios of the
40
first permanent molar and the third permanent molar in both upper and lower dentitions.
Due to the timing of the formation of the M1 and M3 tooth crowns, analyses of ratios in
these teeth represent a record of available water sources during infancy and into late
childhood or adolescence. Prowse et al. note that the infant mortality rates at Isola Sacra
were very high, and that its position as the main port of Rome, requiring a constant
workforce to supply the city of Rome, would require immigration. To test this theory,
stable isotope ratios of a sample from Isola Sacra were compared to ratios of a modern
indigenous Roman sample whose purpose was to act as a control sample, establishing
baseline Rome area ratios. For analysis of M1, Prowse and colleagues found that one
third of the Isola Sacra sample had isotopic signatures that indicated that they were born
outside the region of Rome (33%). The remaining 67% have signatures that correspond to
modern day Roman samples, indicating these individuals were from the area around
Rome and Isola Sacra. Analysis of M3 shows that a significant portion of these
individuals migrated to Isola Sacra during childhood; local isotope signature for M3
shifts to 75% of sample and outsider signatures drop to 25%. The authors state that it was
unexpected to encounter the migration of children, and presumably their families, as it
was previously thought migration during Imperial Roman times was an activity of adult
males. The high rates of immigration support the author’s hypothesis that, due to the high
mortality rates in Isola Sacra, immigration must be high to maintain population levels.
Other studies from Prowse (2001), Prowse et al. (2005) and Prowse et al. (2008)
employ isotopic evidence to characterize diet, differential access to resources, and
childhood feeding practices for the Isola Sacra sample. In 2001, Prowse examined dietary
41
patterns inferred from isotopic analysis and dental health data in the Isola Sacra sample.
Using isotopic data, Prowse was able to describe the diet of Isola Sacra to be 60%
territorial and 40% marine, with males showing higher consumption rates of marine
foods in their diet. The author found very little isotopic variation between different burial
types in the necropolis (Prowse, 2001). According to the study, infant weaning began
around 3 months of age and continued until 2 years of age, and they were fed a largely
grain based weaning diet (Prowse, 2001). Prowse also analyzed dental health data for the
sample, including caries, tooth wear, antemortem tooth loss (AMTL), abscesses, and
calculus. It was noted that the data indicate a good level of oral health in the Isola Sacra
sample, as consistent with evidence from other Roman skeletal samples from this time
period (Prowse, 2001). Similar to the isotopic data, Prowse notes that there were no
significant relationships between burial type and dental health. Differences between
males and females can be seen in the dental health data, where males have higher
incidences of calculus, caries, and tooth wear, and females have higher amounts of
AMTL. In the deciduous dentition, tooth wear started as early as 1.5 years, and
pathological lesions began to appear around 2.5 years, indicating that there was stress
during early childhood.
In 2005, Prowse and coworkers looked more closely at age related variations in
diet from isotopic evidence, and found a pattern in food consumption where adult males
consumed more proteins, especially in the form of marine foods, than females or
subadults. This is in agreement with known status and social habits of Romans, in which
males were of higher status then females and children, so they would be more likely to
42
consume food related to prestige such as meat and fish (Prowse et al., 2005). The authors
also found that the older age portion of the sample consumed more meats and fish than
those in younger age classes. Prowse and colleagues suggest that this trend could indicate
that individuals who regularly consumed a diet rich in protein also survived to an older
age. A dietary pattern was also found among the data from the subadult sample, in which
subadults were found to be depleted in both isotopes analyzed as compared to adults.
Since the subadult diet was largely comprised of plant foods, the authors imply that the
subadult diet was lacking in nutritional adequacy.
This trend was explored further in Prowse et al. (2008), which described the
weaning and feeding practices of infants and young children from Isola Sacra looking at a
combination of isotopic, paleopathological, and historical data. From isotopic analysis of
the deciduous dentition, they determined that the weaning period began at about one year
of age, at which point there was addition of complementary food items other than breast
milk. This transitional weaning diet was likely carbohydrate in nature and was probably
not nutritionally beneficial. Prowse and workers found caries, calculus, and tooth wear
that began shortly after the deciduous teeth erupted, consistent with the transitional diet
of the Isola Sacra subadults.
The isotopic studies done by Prowse et al. (2008, 2005) do not attempt to analyze
paleopathological data for implications of the health of Isola Sacra, however, they do hint
at an inadequate transitional feeding diet during weaning. A study by FitzGerald et al.
(2006) provides some information about the health of infants from Isola Sacra. In this
study, the authors analyze Wilson bands in deciduous teeth to determine ages of
43
formation and duration of defects based on methods of evaluating crown development
and incremental growth markers. High infant death rates make deciduous teeth, which
form between 13-16 weeks in the fetus, to about 11 months after birth, likely candidates
for assessing defects in enamel microstructure. Even if death is avoided, markers can still
show up in the enamel. FitzGerald and workers document and evaluate the prevalence of
Wilson bands in the first year of life in the deciduous dentition of specimens from Isola
Sacra. Age at death ranged from birth to about 13 years based on dental and skeletal
standards. Nearly forty percent of the sample was found to have at least one Wilson
Band, of which canines most commonly exhibited the dental defect (FitzGerald et al.,
2006). Concerning age at death, the authors found that individuals with Wilson bands
have a higher average age at death than those without, 4.8 years versus 3.8 years.
FitzGerald and colleagues feel that this may be an indication that these two different
groups, those with Wilson bands and those without, do not share the same frailty or
buffering capability. Additionally, the authors were able to pick out peaks in enamel
defect occurrence, the first between months 2 and 5, and the second beginning at month 6
and extending until month 9. This pattern may correspond to infant feeding practices
during the classical Roman period, and corresponds well to what Prowse et al. (2008) and
Prowse (2001) found with isotopic data in the same sample. Interestingly, those from the
group displaying no Wilson bands in the first year of life had a very high mortality rate in
that first year, more than double that of infants presenting with Wilson bands (FitzGerald
et al., 2006).
44
The determination of the frequency and age distribution of Wilson bands by
FitzGerald and coworkers indicate that the sub-adults of Isola Sacra were experiencing
some amount of stress. Other workers have also assessed the Isola Sacra dentition for
signs of stress. Manzi et al. (1999) analyzed dental lesions in three different skeletal
samples in Italy, two from the Roman Imperial age, Isola Sacra and Lucas Feroniae, and
a third sample from the early medieval site of La Selvicciola. The authors chose these
samples because they are well documented historically and archeologically. The samples
will make interesting comparisons because it has been well established that Isola Sacra is
mostly urban middle class, while Lucas Feroniae was known to be of poorer social status,
and the sample of La Selvicciola, from the early middle ages, is a rural community that
has been historically and archeologically shown to be under stress due to political strife,
high incidence of disease, and general decline during this time period. Dental lesions for
the three samples were diagnosed via macroscopic examination and included caries, ante
mortem tooth loss, calculus, periodontal lesions (retraction of the alveolar bone from the
cementoenamal junction), linear enamel hypoplasia (LEH), and dental attrition. It is
interesting to note that the individual results showed lower amounts of caries, abscesses,
tooth loss, calculus, resorption, but high rates of LEH for Isola Sacra. The high rate of
LEH was not an expected result of the study. Generally, Lucas Feroniae held an
intermediate position with Isola Sacra presenting less pathology and La Selvicciola
presenting the most pathology (Manzi et al., 1999). When analyzing only LEH, this
pattern is reversed. To this, the authors note the possible different susceptibility of the
Roman samples versus the Lombards of La Selvicciola due to genetic differences. Manzi
45
et al. (1999) also mention that high frequencies of infant mortality in the Isola Sacra and
Lucas Feroniae samples, while infant mortality was significantly lower for La
Selvicciola. After two years of age, this trend reverses and La Selvicciola has
significantly higher mortality rates. This finding suggests that subadults are under stress
at Isola Sacra. Bondioli and coworkers found a similar discovery when analyzing Wilson
bands from the Isola Sacra skeletal collection (2004). They showed that Wilson band
prevalence was higher for Isola Sacra than modern samples and they were able to
correlate peak occurrence with an age of nine and ten months steadily decreasing through
50 months of age. Like Prowse et al. (2008) and FitzGerald et al. (2006), this suggests
that the young of Isola Sacra faced challenges to their overall health.
To date, there has been one published study of fluctuating asymmetry done on a
portion of the Isola Sacra sample. In 2005, Hoover and colleagues investigated the
relationship between FA and enamel hypoplasia. Although their study was not done at the
populational level, and does not permit population-wide conclusions, they noted
interesting findings. The authors found only a very weak correlation between LEH and
FA, although these are both considered non-specific indicators of stress. Hoover et al.
(2005) note the possibility that the lack of relationship between the two might be due to
the longer length of time asymmetry takes to develop. This infers that FA is potentially
more sensitive to prolonged general stressors during growth and development, whereas
LEH is more specific to particular insults (Hoover et al., 2005). Hoover and colleagues
speculate that the differing etiology between the two defects might also be at play, noting
46
FA perhaps has a more complex and generalized etiology while LEH is linked to having
a strong nutritional etiology.
While Isola Sacra is relatively well studied and researchers have a good idea of
population stress, diet, immigration, and other cultural facts, the necropolis of Velia,
although understood to be very similar to Isola Sacra in many ways, is less well
documented and studied. Craig et al. (2009) have analyzed Velia for stable isotope
evidence of diet. The first published study on Velia to date, Craig and colleagues
analyzed stable isotopes extracted from bone collagen from every adult interred from the
Velia necropolis. The sample was comprised of 117 individuals. Carbon and nitrogen
stable isotope analyses were performed to gain insight into the diet of individuals from
Velia. The data was consistent with a diet primarily comprised of cereals, and with only
modest contributions of meat and fish. However, the authors noted substantial variation
within the population, and noted that it appears that some males had greater access to
marine resources, similarly indicated in the stable isotope analysis of the Isola Sacra
sample (Prowse, 2001; Prowse et al., 2005). Craig and coworkers compared this data to
tomb type and grave inclusions and found no significant differences between these
elements and isotope values. They also compare age at death with the isotopic values and
again found no correlation, providing no evidence that adults who lived longer ate a diet
richer in marine resources. Interesting to note, individuals from Velia consumed less
marine resources than compared with the contemporaneous population of Isola Sacra.
Because of the variation seen in the isotopic values, Craig and workers suggest, as one
possible explanation, the possibility of immigration or high population mobility, that
47
perhaps Velia was at least partially comprised of individuals that would have had diets
that were different than the rest of the population. The authors conclude that Velia likely
revolved around agriculture, supplemented by the raising of livestock, with only a
minority of the population involved in the gathering of marine resources. They find the
isotopic data from the Velia sample to be consistent with the historical and archaeological
findings, namely that the diet was high in cereals but lower in the consumption of meat
and fish for the majority of Velia citizens.
Project Details
The study of stable isotopes by Craig and workers (2009) provides a peek into
what the diet would have been like at Velia. Although similar to Isola Sacra in many
ways, Velia also differs in important ways. Their heavier reliance on agricultural goods
and cereals might have a greater impact on health status, especially among the young.
Accounts suggest that Velia was under some amount of stress and percentages at the
necropolis suggest a high infant mortality rate of 31% (Craig et al., 2009). The objective
of this study was to analyze fluctuating dental asymmetry in a sample of individuals from
the necropolis of Velia in Southern Italy. Documentation from other Roman Imperial
studies with similar samples from the same time period, and the work of Craig and
colleagues, suggest that FA should be present in the dentition of the Velia sample. This
study was undertaken to analyze asymmetry in adult dentition to record overall
magnitude of FA, presence or absence of DA and antisymmetry, and to evaluate the data
for patterns such as sex differences in FA frequencies, differences between maxillary and
48
mandibular teeth, differences between the MD and BL dimensions, and correspondence
to field theory.
49
Chapter 3
MATERIALS AND METHODS
Velia is the name that the Romans gave to the ancient village of Elea, founded in
540 BC by the Greeks fleeing the Persian invasion of Ionia (Craig et al., 2009). Velia is
located on the west coast of Italy, south of the modern day town of Salerno. The Romans
controlled the city of Velia from the late third century BC. It was a trading center and
known for its port facilities (Craig et al., 2009).
Figure 1. Approximate Location of Velia in Relation to Modern Italian Cities and the
Imperial Roman Necropolis of Isola Sacra.
50
The people of Velia would have been comprised of citizens who were traders or
employed in the construction and repair of ships. They would have fished the seas,
practiced small scale permanent cultivation, and likely operated a fish preservation
industry (Craig et al., 2009). The area is hilly with narrow river valleys giving way to
mountainous territory and would not be considered particularly suited for farming.
A long series of excavations have taken place at Velia, with the most recent field
campaign focused on the exploration of the necropolis. Workers uncovered over 230
burials spanning the first and second centuries AD, the zenith of the Imperial Roman
period (Craig et al., 2009). The necropolis at Velia contained both inhumations and
cremations, and a variety of tomb types, although none were indicative of particularly
high prestige (Craig et al., 2009). The skeletal remains were remarkably complete and
well preserved, making it possible to determine age at death and sex for large percentage
of individuals. Craig and colleagues (2009) recently analyzed stable isotopes for evidence
of diet in the Velia adults and provided basic sex and age at death estimations. They
sexed the individuals according to Acsadi and Nemenskeri (1970) and Phenice (1969).
They estimated age at death using Burns (1999), Iscan and Loth (1986), Lovejoy (1985),
Meindl and Lovejoy (1985), and Todd (1920). Nearly 54% of the individuals uncovered
from the Velia necropolis were subadults, and the infant mortality rate for Velia was
found to be particularly high at 31% (Craig et al., 2009). There was a slight
predominance of males to females in the overall adult sample, with 64 males to 51
females (Craig et al., 2009).
51
While the sample from Velia is generally well preserved and in good condition,
some factors, such as extreme tooth wear, AMTL, and dental calculus, limited the sample
size for the study of FA. The sample uncovered at Velia contains the remains of more
than 100 individuals, however only 54 individuals had dentition intact or well preserved
enough to be considered for this study.
Prior to the measurement of crown diameters, obvious skeletal and dental
pathologies were noted for each individual, including the presence of enamel hypoplasia,
cribra orbitalia, dental caries, abscesses, anti-mortem tooth loss (AMTL), tooth wear,
buildup of dental calculus, and anomalous traits. Approximately 35 out of the 54
individuals examined in this study had enamel hypoplasia lesions; caries, AMTL, active
and healed abscesses, and tooth wear were also common. A great majority of the 54
individuals measured had light to moderate tooth wear.
For analysis of FA, buccolingual (BL) and mesiodistal (MD) crown diameters
were taken of emerged upper and lower permanent teeth in 54 individuals comprised of
28 females, 21 males, and 5 of undeterminable sex. The age range of the 54 individuals
assessed for dental asymmetry varied from approximately ten years of age (where mixed
dentition allowed some permanent teeth to be accessible) to adults over the age of fifty.
Tooth pairs totaled 1040, made up of 527 female tooth pairs, 429 male tooth pairs, and 84
tooth pairs of unknown sex. Table 1 contains the exact sample sizes by tooth class, sex,
crown diameter, and arcade. Any tooth pairs where the presence of caries, lesions,
fractures, buildup of calculus, or heavy wear that would affect the dimensions were
52
excluded. Third molars were excluded from study. Only complete right and left pairs
were considered for the study.
All measurements were taken by the author. The first 13 individuals measured
were re-taken on a different day, as increased familiarity with the sample, the dimensions,
and the calipers lead to more accurate and repeatable measurements of the BL and MD
dimensions. The first set of measurements for those 13 individuals were discarded from
study and only the second set of measurements was used for those individuals.
The tooth diameters were carefully measured using sharp-pointed Mitutoyo
digital calipers, with an accuracy of 0.001mm. The MD diameter of the tooth was defined
as the maximum width of the tooth crown in the mesiodistal plane (Sciulli, 1979). The
BL diameter of a tooth was taken as the widest diameter of the tooth measured
perpendicular to the mesiodistal plane (Sciulli, 1979).
Differences in character size have been shown to confound measurements of FA
(Harris and Nweeia, 1980; Palmer and Strobeck, 1986). Some researchers transform their
data to eliminate size differences among teeth (Harris and Nweeia, 1980). One common
method, which was employed in this study, is to divide the absolute value of the side
difference (L – R) by the mean size of the left and the right teeth:
|𝐿 − 𝑅|
𝐿+𝑅
2
Table 1. Tooth Pair Sample Size by Tooth, Arcade, Sex, and Crown Diameter.
Tooth Class
MD I1
MD I2
MD C
MD P1
MD P2
MD M1
MD M2
Total MD Tooth Pairs
BL I1
BL I2
BL C
BL P1
BL P2
BL M1
BL M2
Total BL Tooth Pairs
Maxillary Teeth
Mandibular Teeth
Female Male Unknown Total Female Male Unknown Total
13
15
3
31
16
14
5
35
15
14
3
32
23
15
5
43
19
18
2
39
23
19
0
42
20
15
4
39
26
18
2
46
21
16
3
40
25
17
2
44
15
4
4
23
18
15
5
38
18
14
2
34
19
19
2
40
121
96
21
238
150
117
21
288
13
15
3
31
14
15
5
34
15
14
3
32
22
15
5
42
18
18
2
38
22
19
0
41
19
15
4
38
25
18
2
45
19
16
3
38
25
17
2
44
13
5
4
22
17
15
5
37
15
15
2
32
19
19
2
40
112
98
21
231
144
118
21
283
53
54
Descriptive statistics were generated for meaningful subsets of data, including
mean size and standard deviation. Antisymmetry was assessed by testing for the
normality of the R – L distributions with a Kolmogorov-Smirnov test, and also included
tests for kurtosis and skewness. To detect DA, a two-way analysis of variance (ANOVA)
was used to test for significant differences between mean L and mean R in the Velia
sample. Analyses of within-group distributions of FA for Velia were done by conducting
two-way and one-way ANOVA procedures (Palmer and Strobeck, 1986). However,
sample size limitations of less than 25 individuals prevented the use of mixed-model
ANOVA in most subsets of data. The statistics were calculated using Microsoft Excel
(2010) and the statistics software ‘R’, version 2.11.1. The frequency of FA was
calculated for males and females separately, and for the total group. Comparisons were
made to discern FA frequency differences between the sexes, the BL and MD
dimensions, the mandibular and maxillary dentition, and for analysis of differences
between the posterior and anterior teeth, and between tooth classes within the Velia
sample.
55
Chapter 4
RESULTS
Data was first carefully inspected for bad raw measurements, data entry errors,
outliers, and aberrant individuals. Differences between sides in some individuals might
be artificially inflated due to injury, wear, extreme phenotypic plasticity, anomalous teeth
etc. (Palmer and Strobeck, 2003). Palmer and Strobeck suggest the careful visual
inspection of scatter plots to identify outliers and errors. The data from Velia was
grouped into subsets of tooth, dimension, sex, and arcade and scatter plots of each subset
were used to identify extreme measurements. Scatter plots of the Velia data revealed
several measurements that appear to be outliers. It was noted that these extreme
measurements were not from the same individual, but had numerous sources and were
most likely single tooth anomalies. Outliers were determined by testing L – R
measurements for deviations from the sample mean by more than three times the standard
deviation. Exclusion of outliers via this method required careful consideration as
removing outliers can further reduce the already small sample size of some of the Velia
data subsets, and some outliers might represent real variation within the sample.
However, outliers can confound FA values and can also affect the normal distribution of
the data (Palmer and Strobeck, 2003). The inability to take replicate measures and fully
test for measurement error and the inability to re-measure upon finding an anomalous
measurement or statistical outlier made the author err on the side of caution. All
statistical outliers were removed from the sample and the end result provides a working
56
sample size consisting of 937 tooth pairs. Tables 2 and 3 present a summary of statistics
of |L – R| for males and females by arcade and dimension for the Velia sample.
Table 2. Summary Statistics of |L – R| for Velia Females.
Velia Females
MD
n
Maxilla
mean
BL
SD
N
mean
SD
118 0.133 0.109
111 0.122 0.105
Mandible 147 0.117 0.107
141 0.121 0.105
SD = Standard Deviation; n = number of tooth pairs
Table 3. Summary Statistics of |L – R| for Velia Males.
Velia Males
MD
n
Maxilla
94
mean
BL
SD
0.177 0.184
Mandible 114 0.136 0.120
n
96
mean
SD
0.141 0.120
116 0.125 0.102
SD = Standard Deviation; n = number of tooth pairs
Palmer and Strobeck (2003) and Palmer (1994) have recommended that the data
should be checked for a size dependence and asymmetry relationship, and if one is found,
only then should one transform the data. Palmer (1994) has determined that the arbitrary
correction for presumed size dependence in studies of FA can create artificial differences
among samples. Additionally, Palmer points out that size differences among samples
57
may reflect real differences in condition, which is correlated with FA, and eliminating all
size dependence of FA could potentially obscure associations between condition and FA
(Palmer, 1994; Palmer and Strobeck, 2003). Meaningful subsets of data from Velia were
checked for a size-FA relationship using scatter plots relating |L – R| to mean individual
sizes of L and R (L +R/2). There was no apparent relationship between |L – R| and size
for the Velia sample. Furthermore, an analysis of variance using transformed data
provided the similar results for differences between males and females as the untransformed data, shown in Table 4. As such, the size difference between left and right
antimeres (L – R) was used as the measure of asymmetry in this study, with |L – R| used
to measure fluctuating asymmetry.
Table 4. ANOVA Results for Male and Female Differences Using Transformed Data
(L-R)/2 and the Absolute Value of L-R.
|L – R|
(L-R)/2
F Value
18.0903
p-value
0.0001
F Value
6.7789
p-value
0.00937
Antisymmetry is thought to have a genetic basis and testing the sample for the
presence of antisymmetry is of importance because where antisymmetry is present, L – R
variation would not solely be due to developmental instability. Antisymmetry is tested for
by analyzing the sample for departures from normality. Per the recommendations of
Palmer (1994), quantile-quantile plots were used to visually inspect the data for
departures from normality for the Velia sample, with subsets broken down by sex, arcade,
58
and dimension. Quantile-Quantile plots were used to compare the shapes of distributions,
providing a graphical view of how properties such as location, scale, and skewness are
similar or different (Appendix B). The linearity of the points for the Velia subsamples
suggests that the data are normally distributed. Skew and kurtosis were measured for each
subset of data, and Kolmogorov-Smirnov tests were employed to test each subset for
departures from normality. The results of these tests are presented in Tables 5, Table 6,
and Table 7. None of these tests found statistically significant departures from normality.
Table 5. Test for Female Skew and Kurtosis.
Maxilla
MD
Mandible
BL
n
118
111
Mean
0.01876
-0.01571
SD
0.196874
0.169348
Skew
-0.01549
-0.62816
Kurtosis
1.850948
0.643869
n = sample number; SD = standard deviation
MD
BL
147
-0.0274
0.19125
-1.37376
4.4514
141
-0.00175
0.174196
-0.27507
1.99662
Table 6. Test for Male Skew and Kurtosis.
Maxilla
MD
BL
n
94
96
Mean
0.004167
-0.02643
SD
0.29326
0.200701
Skew
-0.39618
0.163452
Kurtosis
2.894567
1.798893
n = sample number; SD = standard deviation
Mandible
MD
114
0.006239
0.211268
0.255884
2.209209
BL
116
-0.0141
0.177769
0.99711
3.951975
59
Table 7. Kolmogorov-Smirnov Test Results.
Maxilla
Female
Male
D
p-value
D
p-value
MD
0.3517
0.0001
0.2883
0.0001
BL
0.377
0.0001
0.3528
0.0001
Mandible
MD
BL
0.3621
0.3555
0.0001
0.0001
0.3317
0.3556
0.0001
0.0001
Similarly to antisymmetry, tests for the presence of DA should be conducted in
studies of FA due to the fact that in characters exhibiting DA, some of the between sides
differences may have a genetic basis and not be the result of developmental instability
(Palmer, 1994). Finding DA in a sample would confound FA values. Mean and standard
deviation were assessed for the arcades, tooth dimensions, and the sexes separately, and
are presented in Table 8. A two-way analysis of variance was also used to test for
significant differences between mean left values and mean right values in the Velia
sample, the results of which can be seen in Table 9. While Table 9 shows some factors
from the two-way ANOVA testing for DA are significant, only the differences between
sides are important for determining if DA is present, and in none of the data subsets
tested was the mean of left and right significantly different from zero. None of the
differences between left and right is even as large as the standard deviation presented in
Table 8.
Tests for DA and antisymmetry confirm that the major source of variation of (L –
R) in the Velia sample is attributable to fluctuating asymmetry. Previous studies of FA
have shown that maxillary and mandibular teeth may respond differently to stress, that
60
females and males can present with differences in FA, and that the mesiodistal and
buccolingual dimensions may also respond differently to stress (Garn et al., 1967; Harris
and Nweeia 1980; Siegel and Doyle 1975). The Velia sample was analyzed for these
potential relationships.
Table 8. Mean Values and Standard Deviation for Subsets of Data Tested for DA.
Mean
SD
n
Maxilla
8.202784
1.625946
934
Mandible
7.681567
1.835851
1136
MD
7.542906
1.760642
1046
BL
8.301025
1.682116
1024
Female
7.754743
1.68133
1052
Male
8.09473
1.795688
852
n = sample number; SD = standard deviation
Table 9. Mixed-Model ANOVA Results Testing for DA.
Source of Variation
F Value
P Value
Arcade
45.7236
0.0001
Side*
0.0083
0.9276
Arcade:Side*
0.0001
0.9924
Sex
18.0903
0.0001
Side*
0.0084
0.9272
Sex:Side*
0.0001
0.9994
Dimension
100.1685
0.0001
Side*
0.0076
0.9304
Dimension:Side*
0.0159
0.8997
* For the purposes of analyses of DA, between sides differences are of primary
importance
Examined by a one-way ANOVA, pooling tooth type, arcade, and dimensions,
males and females were found to have statistically significant differences in magnitude of
61
FA, with males being more asymmetric (n = 937, p = 0.00937; see Table 10). Further
observations of a two-way analysis of variance with the two factors being sex and tooth
dimension (MD and BL) run separately for each arcade revealed that significant
differences between males and females are found only in the maxillary teeth (n = 419, p =
0.01485, Table 11). Table 10 charts the differences for mean and standard deviation by
sex and arcade, and Table 11 presents the results of the two-way ANOVA for sex and
dimension considering each arcade separately.
Table 10. Comparisons of Female and Male Mean by Arcade.
Maxilla
Number of Tooth Pairs 419
Female Mean
0.142167
Male Mean
0.145382
Standard Deviation
0.129925
Mandible
518
0.119201
0.130435
0.108096
Table 11. Two-Way ANOVA Results for Sex and Tooth Dimensions, Considered
Separately for Each Arcade.
Sum
Mean
F
Sq
Sqr
Value
Sex
0.0993 0.099337 5.9846
Maxilla
Dimension
0.0512 0.051247 3.0874
Sex:Dimension
0.0169 0.016939 1.0205
Sex
0.0161 0.016137 1.3785
Mandible Dimension
0.0008 0.00083
0.0709
Sex:Dimension
0.0074 0.007355 0.6283
* indicates statistical significance at a 95% confidence level
P
0.01485 *
0.07964
0.31299
0.2409
0.7901
0.4283
62
There was no significant difference for mandibular teeth, for FA differences
between the MD and BL dimensions, or for the interaction of sex and the dimensions.
Within the dimensions, with the arcades pooled, male and female differences between left
and right were statistically significant in the MD dimension (n = 473, p =0.01193) but not
in the BL dimension, as shown in Table 12. A one-way ANOVA testing the female
maxillary MD dimension and the male maxillary MD dimension also showed significant
differences between males and females, with males having higher amounts of FA, while
all other combinations of arcade and dimension did not (Table 13). The analyses all
indicate that males have significantly higher FA in the maxillary MD dimension than
females.
Table 12. ANOVA Results for Sex and Tooth Dimension, Arcades Pooled.
Number Sum Sq Mean Sqr
Female MD vs. Male MD 473
0.1072 0.107203
Female BL vs. Male BL
464
0.0124 0.012433
* indicates statistical significance at a 95% confidence level
F Value
6.3713
1.127
P
0.01193 *
0.289
Table 13. ANOVA Results for Sex and Tooth Dimension, Considering Each Arcade.
Maxilla
Mandible
Number
P
Number
P
Female MD vs. Male MD
212
0.03101 * 261
0.1826
Female BL vs. Male BL
207
0.2179
257
0.778
* indicates statistical significance at a 95% confidence level
63
Evaluations for FA frequencies in the arcades using one-way ANOVA, pooling
sex and dimension, suggested that there was a statistically significant difference between
FA in the mandible and the maxilla (Table 14), with the maxillary FA frequencies being
higher (Table 15). Comparing upper and lower teeth within each sex and within each
dimension produced no significant results, although comparisons of the male maxillary
and mandibular MD was significant at the 90% confidence level. Across the sample
subsets, the maxillary dentition showed greater levels of FA as compared to the
mandibular dentition. Pooled data of the entire sample tested for distinction in the dental
dimensions yielded no significance. Differences within the sexes between the MD and
BL dimension had the same results, although the MD mean was consistently higher,
suggesting increased FA in this dimension, but not to a statistically significant degree.
Table 14. Pooled ANOVA Results for the Main Variables.
Number SD
Sum Sq Mean Sqr
MD/BL
937
0.118617 0.0281 0.028101
Maxilla/Mandible 937
0.118617 0.0725 0.072538
Female/Male
937
0.118617 0.0948 0.094795
* indicates statistical significance at a 95% confidence level
Table 15. Pooled Mean Values for FA.
MD
BL
Maxilla
Mandible
Female
Male
Mean
0.135544
0.126138
0.141885
0.124189
0.123037
0.143262
F Value
1.9993
5.1785
6.7789
P
0.1577
0.02309*
0.00937*
64
A series of one-way ANOVA also revealed significant differences between the
anterior teeth (incisors and canine) and the posterior teeth (premolars and molars) within
and between the sexes. The results are presented in Table 16.
Table 16. ANOVA of the Male and Female Anterior and Posterior Teeth.
Source of Variation
Sum Sq
Mean Sq
Male Maxillary Anterior/Male
0.3567 0.35674
Maxillary posterior
Male Mandibular Anterior/Male
0.05578 0.055785
Mandibular Posterior
Female Maxillary Anterior/Female
0.00288 0.002882
Maxillary Posterior
Female Mandibular Anterior/Female 0.0429 0.042912
Mandibular Posterior
Male Mandibular Anterior/Female
0.00275 0.002746
Mandibular Anterior
Male Maxillary Posterior/Female
0.3063 0.306349
Maxillary Posterior
Female Mandibular Posterior/Male
0.015
0.015026
Mandibular Posterior
Female Maxillary Anterior/Male
0.01098 0.010985
Maxillary Anterior
* indicates statistical significance at a 95% confidence level
F Value
P
15.775
0.0001014*
4.6147
0.03275 *
0.2513
0.6166
3.8715
0.05008
0.3036
0.5822
16.537
0.0001*
1.1356
0.2874
0.8588
0.3553
Comparisons of the male anterior and posterior teeth for both the mandible and
the maxilla showed that the posterior teeth were significantly more variable than the
anterior teeth. This was especially true for the maxilla, in which the posterior teeth
present marked increases in FA as compared to the anterior teeth (n = 191, p =
0.0001014). Differences between the maxillary female and male posterior teeth were
highly significant (p=0.0001), although differences in the maxillary anterior teeth
65
between the sexes were not significant. Female comparisons of anterior and posterior
teeth did not show the same trends as the males, and in fact, although not statistically
significant, they had the higher frequencies of FA in the anterior maxillary teeth than in
the posterior maxillary teeth.
Individual teeth were assessed for FA by pooling the MD and BL measurements
for two reasons: the diameters were not found to differ significantly in their frequencies
of FA, and to permit a better sample size for individual teeth. Tooth types were separated
by sex and by arcade for the study, and they were analyzed for patterns and
correspondence to field theory and other known patterns of odontometic asymmetry.
Means, indicating FA frequencies, for both males and females and the upper and lower
teeth are presented by individual tooth in Table 17. Mean differences between female
maxillary and mandibular tooth types suggest nearly complete congruency with field
theory. In the female maxillary dentition, the tooth with the least amount of FA was the
first molar, followed closely by the canine. Mean differences in the lower teeth showed
the first lower incisor to have the lowest magnitude of FA. In both the upper and lower
teeth, M2 was found to have the largest amount of FA. Females showed no statistically
significant differences between tooth types.
Tooth type and FA analysis in males yielded significant differences between teeth
for magnitude of FA. As already noted, statistically significant values were found in the
maxilla, but not in the mandible. The male mandibular teeth followed expectations of
field theory with the exception of M2, which showed remarkably small amounts of FA.
The male maxillary dentition also loosely conformed to field theory, with the exception
66
of I1 having more asymmetry than I2. The largest mean values of asymmetry were
present in the male maxillary teeth, with M2, P2, and I1 having larger means than any
other subset measured. In the male sample, the canine appeared to be the most stable
maxillary tooth and the I2 was the most stable in the lower teeth.
Table 17. Mean Values of FA by Tooth for the Arcades and Sexes.
Tooth
I1
I2
C
P1
P2
M1
M2
Female Means
Maxilla
Mandible
0.128855 0.076923
0.133083 0.107442
0.115405 0.116818
0.124706 0.1218
0.127353 0.133469
0.11075
0.124857
0.146889 0.138108
Male Means
Maxilla
Mandible
0.142667 0.112414
0.107407 0.107143
0.101714 0.114595
0.150333 0.141714
0.200313 0.167353
0.186667 0.154667
0.268571 0.113784
67
Chapter 5
FINDINGS AND INTERPRETATIONS
Discussion
Craig et al. (2009) and other workers have documented that Velia and similar
communities in existence during the Imperial Roman period were under stress, especially
at a young age (Craig et al., 2009; Cucina et al., 2005; FitzGerald et al., 2006; Hoover et
al., 2005; Manzi et al., 1999; Manzi et al., 1997; Manzi et al., 1991; Prowse, 2001;
Prowse et al., 2008; Prowse et al., 2007; Prowse et al., 2005). As expected, tests
established the presence of FA in the Velia population, and confirmed a lack of DA and
antisymmetry, making the sample ideal for discerning patterns of FA variation.
Tests of asymmetry frequencies for the Velia data have consistently provided the
following trends: the maxillary teeth have greater amounts of FA than mandibular teeth,
the MD dimension showed increased FA as compared to the BL measurement, posterior
teeth showed more asymmetry, and males had higher FA means than females, with
greatest asymmetry occurring in the male maxillary posterior teeth.
Past research has shown that there is some evidence that fluctuating asymmetry is
not expressed uniformly across sexes and populations. While it is not surprising that there
should be differences between males and females in the Velia population, given the
evidence of differential access to nutritional foods, it is surprising that males should have
higher FA amounts than females. In the Velia sample, male frequencies of FA were
especially significant in the posterior maxillary dentition and for the maxillary MD
68
dimension. Generally, mean FA amounts were greater for males across all Velia subsets,
indicating greater variation and increased asymmetry in males. This finding should not be
an artifact of a tooth size and asymmetry relationship, as tests on the Velia sample
showed a consistent lack of correlation between tooth size and asymmetry. To ensure this
assumption was not mistaken, male and female differences were analyzed using
transformed data, to eliminate any possible effect of a size-asymmetry correlation. The
results from the ANOVA using transformed data matched the results from the same test
on non-transformed data.
Differences between the sexes are fairly rare among studies of odontometric FA.
Harris and Nweeia (1980) found that females were significantly more asymmetric than
males for the MD diameter in the modern-day Amazonian Ticuna Indians. Garn et al.
(1967), found in their sample of modern Ohio whites, that males were more asymmetric,
but for the BL dimension. While most studies do not find significant differences between
the sexes, it is widely believed that females are better buffered against developmental
instability due to their double X chromosome (Guatelli-Steinberg et al., 2006; Harris and
Nweeia, 1980). This could certainly be the case for Velia. What is known from research
on other Imperial Roman collections seem to indicate that females would experience
more stress given their dietary, cultural, and behavioral differences. It has been
convincingly reported that males had greater access to marine and mammal resources
(Craig et al., 2009; Prowse, 2001; Prowse et al., 2005). However, the explanation of the
findings from Velia would seem to indicate that males were under greater developmental
stress. One possible explanation is that Velia males could be comprised of a good portion
69
of immigrants, as Craig et al. (2009) speculated that Velia had high population mobility.
Prowse et al. (2007) had a similar finding for the sample from Isola Sacra. Both noted
that males rather than females were more likely to immigrate. Immigrants were often
more socioeconomically challenged, perhaps consisting of a slave class or laborer, and
thus would perhaps be more apt to experience stress during development. Comparative
analysis of stable isotopes and FA might be an avenue for further investigation on this
hypothesis.
Analysis of the dental dimensions within and between the sexes and arcades
showed only a significant difference in the MD dimension for the male maxillary teeth.
Differences in the magnitude of FA in the Velia sample suggest that the MD dimension is
a more sensitive measure of developmental instability. The MD and BL dimensions both
showed increased asymmetry in the maxillary teeth, lending to evidence for an arcadedimension effect sometimes found in studies of dental FA (Garn et al., 1967; Harris and
Nweeia, 1980; Siegel and Doyle, 1975).
Previous studies have often found the maxillary teeth to be more asymmetric than
mandibular teeth (Garn et al., 1967; Harris and Nweeia, 1980; Hoover et al., 2005; Potter
et al., 1976; Siegel and Doyle, 1975). The Velia data find the maxillary teeth to be more
asymmetric for both sexes and for both dimensions. Pooled data indicate a statistically
significant difference in FA between the maxilla and mandible. Further investigation
showed marked FA in the male posterior maxillary teeth. Consistent differences between
the upper and lower teeth suggest that the two arcades function independently in their
buffering ability to genetic and environmental disturbances. Hoover and colleagues
70
(2005), assessed asymmetry on a sample from Isola Sacra, and also found increased FA
in the maxillary dentition.
The positive association between asymmetry and the dental patterning as
described by field theory is evident in the FA measurements from the Velia sample. The
female maxillary dentition show complete agreement with field theory, in which the pole
teeth I1, C, P1 and M1 have the least asymmetry, and I2, P2, and M2 appear to be less
well buffered. The mandibular teeth do not show this pattern as cleanly, since the lower
I1 tooth was found to have the least asymmetry, whereas the pole tooth would be
expected to be I2. All other female mandibular teeth followed the description of field
theory, in which the pole teeth, considered most stable, have less variation and
asymmetry. Males follow a similar trend, with the exception of the upper I1 in and lower
M2.
Velia females had no significant differences amongst the seven tooth types in
either arcade or for either dimension. Differences in the magnitude of FA between female
anterior and posterior teeth were also not significant. Analysis of male tooth types and
comparison of anterior and posterior teeth offered a different pattern. For males, pooling
the dimensions, there were no statistically significant FA differences within tooth classes.
However, comparisons of the male anterior and posterior teeth yielded significant results
for both arcades, strongly indicating more variability in the posterior dentition.
Discussion of tooth type asymmetry from Velia should be interpreted with some caution.
Sample sizes were small, even with the dimensions (MD and BL) pooled.
71
Conclusion
The present study supports the contention that fluctuating dental asymmetry is a
useful measure of developmental instability. The sample from Velia, as evidenced from
skeletal and dental pathologies, experienced stress during growth and development
leading to deviations from bilateral symmetry in the adult dentition. Males were found to
be more asymmetric than females, and maxillary teeth were more asymmetric, especially
for the MD dimension. Asymmetry was also found to vary in accordance with tooth
position, where typically the most stable tooth in each field, or pole tooth, was least
asymmetric.
The lack of patterning and agreement in the various FA investigations conducted
over the years suggest that fluctuating asymmetry is not expressed uniformly across
populations, sexes, arcades, tooth classes, or dimensions. Without investigating
genetically similar comparative samples, it is impossible to know whether FA analyses
from Velia reflect trends of FA variation also seen in other Imperial Roman collections.
Further investigation is recommended to better understand the nature of fluctuating
asymmetry in Roman Imperial populations.
72
APPENDIX A
Abbreviations Used in Study
AMTL – Antemortem Tooth Loss
BL – Buccolingual Tooth Dimension
DA – Directional Asymmetry
C – Canine
FA – Fluctuating Asymmetry
I1 – Central Incisor
I2 – Lateral Incisor
L – Left
LEH – Linear Enamel Hypoplasia
MD – Mesiodistal Tooth Dimension
M1 – First Molar
M2 – Second Molar
M3 – Third Molar
P1 – First Premolar
73
P2 – Second Premolar
R – Right
74
APPENDIX B
Sample of Scatter Plots Showing Outliers
Scatter plot of |L – R| and (L-R)/2 for the female maxillary mesiodistal I1.
0.6
Absolute Value of L-R
0.5
0.4
0.3
0.2
0.1
0
7.5
8
8.5
(L-R)/2
9
9.5
Scatter plot of |L – R| and (L-R)/2 for the female maxillary mesiodistal P1.
0.7
Absolute Value of L-R
0.6
0.5
0.4
0.3
0.2
0.1
0
5.5
6
6.5
7
(L-R)/2
7.5
8
75
Scatter plot of |L – R| and (L-R)/2 for the female maxillary mesiodistal P2.
0.7
Absolute Value of L-R
0.6
0.5
0.4
0.3
0.2
0.1
0
5.5
6
6.5
7
7.5
8
(L-R)/2
Scatter plot of |L – R| and (L-R)/2 for the female maxillary mesiodistal M1.
0.7
Absolute Value of L-R
0.6
0.5
0.4
0.3
0.2
0.1
0
9
9.5
10
(L-R)/2
10.5
11
76
Scatter plot of |L – R| and (L-R)/2 for the male maxillary mesiodistal I2.
1.2
Absolute Value of L-R
1
0.8
0.6
0.4
0.2
0
5.5
6
6.5
7
7.5
8
(L-R)/2
Scatter plot of |L – R| and (L-R)/2 for the male maxillary mesiodistal P2.
0.9
Absolute Value of L-R
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
5.5
6
6.5
7
(L-R)/2
7.5
8
77
Scatter plot of |L – R| and (L-R)/2 for the male maxillary buccolingual canine.
0.8
Absolute Value of L-R
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
7
7.5
8
8.5
9
9.5
(L-R)/2
Scatter plot of |L – R| and (L-R)/2 for the female mandibular mesiodistal canine.
1
Absolute Value of L-R
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
5.5
6
6.5
(L-R)/2
7
7.5
78
Scatter plot of |L – R| and (L-R)/2 for the male mandibular mesiodistal M2.
0.8
Absolute Value of L-R
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
9.5
10
10.5
11
11.5
12
(L-R)/2
Scatter plot of |L – R| and (L-R)/2 for the female mandibular buccolingual I2.
1.6
Absolute Value of L-R
1.4
1.2
1
0.8
0.6
0.4
0.2
0
5.6
5.8
6
6.2
6.4
(L-R)/2
6.6
6.8
7
79
Scatter plot of |L – R| and (L-R)/2 for the male mandibular buccolingual I2.
1.8
Absolute Value of L-R
1.6
1.4
1.2
1
0.8
0.6
0.4
0.2
0
5.5
6
6.5
(L-R)/2
7
7.5
Scatter plot of |L – R| and (L-R)/2 for the male mandibular buccolingual canine.
0.9
Absolute Value of L-R
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
6.5
7
7.5
8
(L-R)/2
8.5
9
80
APPENDIX C
Quantile-Quantile Plots of Normality for the Velia Sample
Normality distribution of the female maxillary MD dimension.
0.8
0.6
0.4
0.2
0
-3
-2
-1
Female Max MD
0
1
2
3
-0.2
-0.4
-0.6
-0.8
Normality distribution of the female maxillary BL dimension.
0.4
0.3
0.2
0.1
0
-3
-2
-1
-0.1
-0.2
-0.3
-0.4
-0.5
-0.6
-0.7
0
1
2
3
Female Max BL
81
Normality distribution of the female mandibular MD dimension.
0.6
0.4
0.2
0
-3
-2
-1
0
1
2
3
-0.2
Female Mand MD
-0.4
-0.6
-0.8
-1
Normality distribution of the female mandibular BL dimension.
0.6
0.4
0.2
0
-3
-2
-1
Female Mand BL
0
-0.2
-0.4
-0.6
-0.8
1
2
3
82
Normality distribution of the male maxillary MD dimension.
1.5
1
0.5
0
-3
-2
-1
Male Max MD
0
1
2
3
-0.5
-1
-1.5
Normality distribution of the male maxillary BL dimension.
0.6
0.4
0.2
0
-3
-2
-1
Male Max BL
0
-0.2
-0.4
-0.6
1
2
3
83
Normality distribution of the male mandibular MD dimension.
0.8
0.6
0.4
0.2
0
-3
-2
-1
Male Mand MD
0
1
2
3
-0.2
-0.4
-0.6
-0.8
Normality distribution of the male mandibular BL dimension.
1
0.8
0.6
0.4
0.2
Male Mand BL
0
-3
-2
-1
0
-0.2
-0.4
-0.6
1
2
3
84
REFERENCES
Aas IHM, Risnes S. 1979. The depth of the lingual fossa in permanent incisors of
Norwegians. Am J Phys Anthropol 50:341-348.
Acsadi G, Nemeskeri J. 1970. History of human life span and mortality. Budapest:
Akademiai Kiado.
Albert AM, Greene DL. 1999. Bilateral asymmetry in skeletal growth and maturation as
an indicator of environmental stress. Am J Phys Anthropol 110:341-349.
Angelopoulou MV, Vlachou V, Halazonetis DJ. 2009. Fluctuating molar asymmetry in
relation to environmental radioactivity. Archives of Oral Biology 54:666-670.
Bader RS. 1965. Fluctuating asymmetry in the dentition of the house mouse. Growth
29:291-300.
Barden HS. 1980. Fluctuating dental asymmetry: a measure of developmental instability
in Down Syndrome. Am J Phys Anthropol 52:169-173.
Baume RM, Crawford MH. 1980. Discrete dental trait asymmetry in Mexican and
Belizean groups. Am J Phys Anthropol 52:315-321.
Benderlioglu Z, Nelson RJ. 2003. Season of birth and fluctuating asymmetry. American
Journal of Human Biology 16:298-310.
Benderlioglu Z, Sciulli PW, Nelson RJ. 2004. Fluctuating asymmetry predicts human
reactive aggression. American Journal of Human Biology 16:458-469.
Black TK. 1980. An exception to the apparent relationship between stress and fluctuating
dental asymmetry. J Dent Res 59:1168-1169.
Boklage CE. 1987. Developmental differences between singletons and twins in
distributions of
dental diameter asymmetries. Am J Phys Anthropol 74:319-322.
Bondioli L, Coppa A, FitzGerald C, Nava A, Macchiarelli R. 2004. Individual
chronology of enamel dental microdefects in the juvenile segment of the Portus Romae
community. [Abstract]. Am J Phys Anthropol 123:65-66.
Burns KR. 1999. Forensic anthropology training manual. Englewood Cliffs, NJ: Prentice
Hall.
85
Buschang PH, Demirjian A. 1989. Technical error of mesiodistal diameters for the
permanent and deciduous dentition. Am J Hum Biol 1:741-746.
Clarke GM. 1993. The genetic basis of developmental stability: relationships between
stability, heterozygosity and genomic coadaptation. Genetica 89:15-23.
Corruccini RS, Townsend GC, Schwerdt W. 2005. Correspondence between enamel
hypoplasia and odontometric bilateral asymmetry in Australian twins. Am J Phys
Anthropol 126:177-182.
Craig OE, Biazzo M, O’Connell TC, Garnsey P, Martinez-Labarga C, Lelli R, Salavadei
L, Tartaglia G, Nava A, Reno L, Fiammenghi A, Rickards O, Bondioli L. 2009. Stable
isotopic evidence for diet at the Imperial Roman coastal site of Velia (1st and 2nd
centuries AD) in southern Italy. Am J Phys Anthropol 139:572-583.
Cucina A, Vargiu R, Mancinelli D, Ricci R, Santandrea E, Catalano P, Coppa A. 2005.
The necropolis of Vallerano (Rome, 2nd-3rd century AD): an anthropological perspective
on the ancient Romans in the Suburbium. International Journal of Osteoarchaeology
16:104-117.
Dahlberg AA. 1945. The changing dentition of man. Journal of the American Dental
Association 32:676-690.
Debat V, David P. 2001. Mapping phenotypes: canalization, plasticity, and
developmental stability. Trends in Ecology and Evolution 16:555-561.
DeLeon VB. 2007. Fluctuating asymmetry and stress in a medieval Nubian population.
Am J Phys Anthropol 132:520-534.
DiBennardo R, Bailit HL. 1978. Stress and dental asymmetry in a population of Japanese
children. Am J Phys Anthropol 48:89-94.
Doyle WJ, Johnston O. 1977. On the meaning of increased fluctuating dental asymmetry:
a cross populational study. Am J Phys Anthropol 46:127-134.
Falk D, Corruccini R. 1982. Efficacy of cranial versus dental measurements for
separating human populations. Am J Phys Anthropol 57:123-127.
Falk D, Pyne L, Helmkamp RC, DeRousseau CJ. 1988. Directional asymmetry in the
forelimb of Macaca mulatta. Am J Phys Anthropol 77:1-6.
FitzGerald C, Saunders S, Bondioli L, and Macchiarelli R. 2006. Health of infants in an
86
Imperial Roman skeletal sample: perspective from dental microstructure. Am J Phys
Anthropol 130:179-189.
Fushima K, Inui M, Sato S. 1999. Dental asymmetry in temporomandibular disorders.
Journal of Oral Rehabilitation 26:752-756.
Garn SM, Lewis AB, Kerewsky RS. 1966. The meaning of bilateral asymmetry in the
permanent dentition. Angle Orthod 36:55-62.
Garn, SM, Lewis AB, Kerewsky RS. 1967. Buccolingual size asymmetry and its
developmental meaning. Angle Orthod. 37:186-193.
Greene DL. 1984. Fluctuating dental asymmetry and measurement error. Am J Phys
Anthropol 65:283-289.
Groeneveld HT, Kieser JA. 1991. A new perspective on fluctuating odontometric
asymmetry in South African Negroes. Am J Hum Biol 3:655-661.
Guatelli-Steinberg D, Sciulli PW, Edgar HHJ. 2006. Dental fluctuating asymmetry in the
Gullah: tests f hypotheses regarding developmental stability in deciduous vs. permanent
and male vs. female teeth. Am J Phys Anthropol 129:427-434.
Hallgrimsson B, Willmore K, Hall BK. 2002. Canalization, developmental instability,
and morphological integration in primate limbs. Yearbook of Physical Anthropology
45:131-158.
Harris EF, Nweeia MT. 1980. Dental Asymmetry as a measure of environmental stress in
the Ticuna Indians of Columbia. Am J Phys Anthropol 53:133-142.
Heikkinen T, Alvesalo L, Tienari J. 2002. Deciduous tooth crown size and asymmetry in
strabismic children. Orthod Craniofacial Res 5:195-204.
Helsen P, Van Dongen S. 2009. The normal distribution as appropriate model of
developmental instability in Opuntia cacti flowers. Journal of Evolutionary Biology
22:1346-1352.
Hershkovitz I, Livshits G, Moskona D, Arensburg B, Kobyliansky E. 1993. Variables
affecting dental fluctuating asymmetry in human isolates. Am J Phys Anthropol 91:349365.
Hillson S, FitzGerald C, Flinn H. 2005. Alternative dental measurements: proposals and
relationships with other measurements. Am J Phys Anthropol 126:413-426.
87
Hoover KC, Corruccini RS, Bondioli L, Macchiarelli R. 2005. Exploring the relationship
between hypoplasia and odontometric asymmetry in Isola Sacra, an Imperial Roman
necropolis. Am J Hum Biol 17:752-764.
Hoover KC, Matsumura H. 2008. Temporal variation and interaction between nutritional
and developmental instability in prehistoric Japanese populations. Am J Phys Anthropol
137:469-478.
Iscan MY, Loth SR. 1986. Estimation of age and determination of sex from the sterna rib.
In: Reichs KJ, editor. Forensic osteology: advances in the identification of human
remains. Springfield: Thomas. p 68-89.
Jantz RL. 1975. Population variation in asymmetry and diversity from finger to finger for
digital ridge-counts. Am J Phys Anthropol 42:215-224.
Kark A, Safriel UN, Tabarroni C, Randi E. 2001. Relationship between heterozygosity
and asymmetry: a test across the distribution range. Heredity 86:119-127.
Kellner JR, Alford RA. 2003. The ontogeny of fluctuating asymmetry. The American
Naturalist 161:931-947.
Kieser JA, Groeneveld HT, Da Silva PCF. 1997. Dental asymmetry, maternal obesity,
and smoking. Am J Phys Anthropol 102:133-140.
Kieser JA, Groeneveld HT, Preston CB. 1986. Fluctuating dental asymmetry as a
measure of odontogenic canalization in man. Am J Phys Anthropol 71:437-444.
Kolakowski D, Bailit HL. 1981. A differential environmental effect on human
anterior tooth size. Am J Phys Anthropol 54:377-381.
Kujanova M, Bigoni L, Veleminska J, Veleminsky P. 2008. Limb bones asymmetry and
stress in Medieval and recent populations of Central Europe. International Journal of
Osteoarchaeology 18:476-491.
Leamy LJ, Bader RS. 1968. Components of variance of odontometric traits in a wildderived population of Peromyscus leucopus. Evolution 22:826-834.
Leamy LJ, Klingenberg CP. 2005. The genetics and evolution of fluctuating asymmetry.
Annual Review of Ecology, Evolution, and Systematics 36:1-21.
Lens L, Van Dongen S. 2000. Fluctuating and directional asymmetry in natural bird
populations exposed to different levels of habitat disturbance, as revealed by mixture
analysis. Ecology Letters 3:516-522.
88
Leung B, Forbes MR, Houle D. 2000. Fluctuating asymmetry as a bioindicator of stress:
comparing efficacy of analyses involving multiple traits. The American Naturalist
155:101-115.
Little BB, Buschang PH, Malinas RM. 2002. Anthropometric asymmetry in
chronologically undernourished children from Southern Mexico. Ann Hum Biol 29:526537.
Livshits G, Davidi L, Kobyliansky E, Ben-Amitai D, Levi Y, Merlob P, Optiz JM,
Reynolds JF. 1988. Decreased developmental stability as assessed by fluctuating
asymmetry of morphometric traits in preterm infants. Am J Hum Genet 29:793-805.
Lovejoy CO. 1985. Dental wear in the Libben population: its functional pattern and role
in the determination of adult skeletal age at death. Am J Phys Anthropol 68:447-456.
Manzi G, Salvadei L, Vienna A, Passarello P. 1999. Discontinuity of life conditions at
the transition from the Roman Imperial age to the early middle ages: Examples from
Central Italy evaluated by pathological dento-alveolar lesions. Am J Hum Biol 11:327341.
Manzi G, Santandrea E, Passarello P. 1997. Dental size and shape in the Roman Imperial
age: two examples from the area of Rome. Am J Phys Anthropol 102:469-479.
Manzi G, Sperduti A, Passarello P. 1991. Behavior-induced auditory exostoses in
Imperial Roman society: evidence from coeval urban and rural communities near Rome.
Am J Phys Anthropol. 85:253-260.
Mayhall JT, Saunders SR. 1986. Dimensional and discrete dental trait asymmetry
relationships. Am J Phys Anthropol 69:403-411.
Meindl RS, Lovejoy CO. 1985. Ectocranial suture closure: a revised method for the
determination of skeletal age at death based on the later-anterior sutures. Am J Phys
Anthropol 68:57-66.
Naugler CT, Ludman MD. 1996. Fluctuating asymmetry and disorders of developmental
origin. American Journal of Medical Genetics 66:15-20.
Niswander JD, Chung CS. 1965. The effects of inbreeding on tooth size in Japanese
children. American Journal of Human Genetics 17:390-398.
Noss JF, Scott GR, Potter RHY, Dahlberg AA. 1983. Fluctuating asymmetry in molar
dimensions and discrete morphological traits in Pima Indians. Am J Phys Anthropol
61:437-445.
89
Palmer AR. 1994. Fluctuating asymmetry analysis: a primer. In: Markow TA (ed)
Developmental Instability: its Origin and Evolutionary Implications. Kluwer Academic:
Netherlands. pp 335–364.
Palmer AR, Strobeck C. 1986. Fluctuating asymmetry: measurement, analysis, patterns.
Annual Review of Ecology and Systematics 17:391-421.
Palmer AR, Strobeck C. 2003. Fluctuating asymmetry analyses revisited. In: Polak M
(ed) Developmental instability: causes and consequences. Oxford University Press:
Oxford. pp 279–319.
Peretz B, Ever-Hadani P, Casamassimo P, Eidelman E, Shellhart C, Hagerman R. 2005.
Crown size asymmetry in males with fra (X) or Martin-Bell syndrome. American Journal
of Medical Genetics 30:185-190.
Perzigian AJ. 1977. Fluctuating dental asymmetry: variation among skeletal populations.
Am J Phys Anthropol 47:81-88.
Phenice TW. 1969. A newly developed visual method of sexing in the Os Pubis. Am J
Phys Anthropol 30:297-301.
Potter RH, Nance WE. 1976. A twin study of dental dimension: discordance, asymmetry,
and mirror imagery. Am J Phys Anthropol 44:391-396.
Potter RH, Nance WE, Yu P, Davis WB. 1976. A twin study of dental dimension:
independent genetic determinants. Am J Phys Anthropol 44:391-396.
Prowse, TL. 2001. Isotopic and dental evidence for diet from the necropolis of Isola
Sacra (1st-3rd centuries AD), Italy [Dissertation]. Hamilton, ON, Canada: McMaster
Univeristy.
Prowse TL, Saunders SR, Schwartcz HP, Garnsey P, Macchiarelli R, Bondioli L. 2008.
Isotopic and dental evidence for infant and young child feeding practices in an Imperial
Roman skeletal sample. Am J Phys Anthropol 137:294-308.
Prowse TL, Schwarcz HP, Garnsey P, Knyf M, Macchiarelli R, Bondioli L. 2007.
Isotopic evidence for age-related immigration to Imperial Rome. Am J Phys Anthropol
132:510-519.
Prowse TL, Schwarcz HP, Garnsey P, Saunders SR, Macchiarelli R, Bondioli L. 2005.
Isotopic evidence for age-related variation in diet from Isola Sacra, Italy. Am J Phys
Anthropol 128:2-13.
90
Roff D, Reale D. 2004. The quantitative genetics of fluctuating asymmetry: a comparison
of two models. Evolution 58:47-58.
Rose JC, Condon KW, Goodman AH. 1985. Diet and dentition: developmental
disturbances. In: R. I. Gilbert and J. H. Mielke, Editors. The Analysis of Prehistoric
Diets. New York: Academic Press. p 281-305.
Roy TA, Ruff CB, Plato CC. 1994. Hand dominance and bilateral asymmetry in the
structure of the second metacarpal. Am J Phys Anthropol 94:203-211.
Schaefer K, Lauc T, Mitteroecker P, Gunz P, Bookstein FL. 2006. Dental arch
asymmetry in an isolated Adriatic community. Am J Phys Anthropol 129:132-142.
Sciulli PW. 1978. Developmental abnormalities of the permanent dentition in prehistoric
Ohio Valley Amerindians. Am J Phys Anthropol 48:193-198.
Sciulli PW. 1979. Size and morphology of the permanent dentition in prehistoric Ohio
Valley Amerindians. Am J Phys Anthropol 50:615-628.
Sciulli PW, Doyle WJ, Kelley C, Siegel P, Siegel MI. 1979. The interaction of stressors
in the induction of increased levels of fluctuating asymmetry in the laboratory rat. Am J
Phys Anthropol 50:279-284.
Siegel MI, Doyle WJ. 1975. The effects of cold stress on fluctuating asymmetry in the
dentition of the mouse. J Exp Zool 193:385-389.
Siegel MI, Smookler G. 1973. Fluctuating dental asymmetry and audiogenic stress.
Growth 37:35-19.
Smith BH, Garn SM, Cole PE. 1982. Problems of sampling and inference in the study of
fluctuating dental asymmetry. Am J Phys Anthropol 58:281-289.
Stojanowski CM. 2007. Comment on “Alternative Dental Measurements” by Hillson et
al. Am J Phys Anthropol 132:234-237.
Stojanowski CM, Larson CS, Tung TA, McEwan BG. 2007. Biological structure and
health implications from tooth size at Mission San Luis de Apalachee. Am J Phys
Anthropol 132:207-222.
Suarez BK. 1974. Neandertal dental asymmetry and the probable mutation effect. Am J
Phys Anthropol 41:411-416.
Swaddle JP, Witter MS. 1994. Food, feathers, and fluctuating asymmetries. Proceedings
of the Royal Society of London B: Biological Sciences 255:147-152.
91
Swaddle JP, Witter MS, Cuthill IC. 1994. The analysis of fluctuating asymmetry. Animal
Behaviour 48:986-989.
Todd TW. 1920. Age changes in the pubis bone. I. The white male pubis. Am J Phys
Anthropol 3:467-470.
Townsend GC, Brown T. 1983. Molar size sequence in Australian Aboriginals. Am J
Phys Anthropol 60:69-74.
Townsend GC, Harris EF, Lesot H, Clauss F, Brook A. 2009. Morphogenetic fields
within the human dentition: a new, clinically relevant synthesis of an old concept.
Archives of Oral Biology 54S:S34-S44.
Van Valen L. 1962. A study of fluctuating asymmetry. Evolution 16:125-142.