AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 134:520528 (2007)

Dental Indicators of Health and Stress in Early Egyptian and Nubian Agriculturalists: A Difcult Transition and Gradual Recovery
Anne P. Starling* and Jay T. Stock
Leverhulme Centre for Human Evolutionary Studies, Department of Biological Anthropology, University of Cambridge, Cambridge, UK CB2 1QH KEY WORDS linear enamel hypoplasia; subsistence transition; Nile valley; Badari interruption. The prevalence of LEH was highest in the proto-agricultural (pastoralist) Badari population, with a gradual decline throughout the late Predynastic and early Dynastic periods of state formation. This suggests that the period surrounding the emergence of early agriculture in the Nile valley was associated with high stress and poor health, but that the health of agriculturalists improved substantially with the increasing urbanization and trade that accompanied the formation of the Egyptian state. This evidence for poor health among protoand early agriculturalists in the Nile valley supports theories that agricultural intensication occurred as a response to ecological or demographic pressure rather than simply as an innovation over an existing stable subsistence strategy. Am J Phys Anthropol 134:520528, 2007. V 2007 Wiley-Liss, Inc.
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ABSTRACT Although agriculture is now the globally predominant mode of food production, studies of the skeletal remains of early agriculturalists have indicated high levels of physiological stress and poor health relative to hunter-gatherers in similar environments. Previous studies identifying this trend in different regions prompt further research of the causes and effects of subsistence transitions in human societies. Here, 242 dentitions from ve ancient Egyptian and Nubian populations are examined: 38 individuals from Jebel Sahaba (Upper Paleolithic), 56 from Badari (Predynastic), 54 from Naqada (Predynastic), 47 from Tarkhan (Dynastic), and 47 from Kerma (Dynastic). These populations span the early period of agricultural intensication along the Nile valley. Skeletal remains were scored for the presence of linear enamel hypoplasia (LEH) of the dentition, an established indicator of physiological stress and growth

The ancient history of the Nile valley is well-studied and has fascinated historians and archaeologists for centuries. The Predynastic period has received a great deal of recent attention as the time when the foundations of the Pharaonic state were established (Wilkinson, 1999). Over a relatively short period of time, ancient Egyptian and Nubian populations transformed from primarily nomadic pastoralist communities to settled agricultural proto-city-states (Kemp, 1989). Immediately following this subsistence transition was the emergence of the worlds rst nation-state, a highly hierarchical and centralized bureaucratic polity. This subsistence transition has been well-documented, and therefore provides a unique opportunity to study the health consequences of increasing sedentism and dependence on agriculture. This study examines the conditions of this transition in Egypt and Nubia through a bioculturally-integrated paleopathological approach. The prevalence of linear enamel hypoplasia (LEH) of the dentition, an indicator of physiological stress, is examined in ve populations spanning the temporal range of 13000 1500 B.C., including the Neolithic transition.

hierarchical civilization and social complexity (Childe, 1936; Cohen, 1989). However, the paradox that continues to attract researchers of human biology and history to questions surrounding the origins of agriculture is how little this progress seemed to benet the earliest food producers (Larsen, 2006). Despite the intuitive sense that increased social complexity has produced increased quality of life, most studies have shown a decline in health in the earliest agriculturalists (e.g. Cohen and Armelagos, 1984; Cohen, 1989; Steckel and Rose, 2002; Steckel et al., 2002; Larsen, 2006). While cultivating rather than gathering plant resources is frequently cited as a means of increasing food security (Smith, 1995; Larsen, 2006), it is also a risky investment if the crops fail. In addition, the concentration of food resources can be viewed as a liability rather than an advantage to early hunter-gatherers adopting domestication, as these food stores may become
Grant sponsor: Leverhulme Trust *Correspondence to: Anne Starling, Department of Biological Anthropology and Anatomy, Duke University, 08 Biological Sciences Bldg., Box 90383, Durham, NC 27708-0383. E-mail: aps4@duke.edu Received 18 October 2006; accepted 20 July 2007 DOI 10.1002/ajpa.20700 Published online 4 September 2007 in Wiley InterScience (www.interscience.wiley.com).

AGRICULTURE AND THE NEOLITHIC REVOLUTION

It is undeniable that the transition from a nomadic foraging lifestyle to a sedentary agricultural one has had signicant consequences for the human adaptive niche. This transition has been viewed, historically and recently, as the crucial shift leading to modern human
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DENTAL STRESS MARKERS IN EARLY AGRICULTURALISTS a target for aggressive neighbors (Cohen, 1989). These interactions with other human populations, as well as interactions with the external environment and the internal dynamics of human societies, must be considered in evaluating the effects of plant and animal domestication on the earliest agriculturalists. It is clear that the advent of agriculture is associated with population growth among most Neolithic societies (Dumond, 1975). However, it is not clear if this population growth has been a cause or effect of agricultural intensication. One proposed causal link between agriculture and population growth is that sedentism reduces the interbirth interval, presumably due to reduced physical activity or greater reliability of food resources (Roth, 1985), but this association has been questioned by subsequent researchers and empirical evidence for the link between sedentism and interbirth interval is weak (Pennington, 1992). An inuential work by Boserup (1965) attempted to reverse this view of causality and to posit population growth as the independent variable driving technological and subsistence change. From this perspective, endogenous population pressure would eventually make a foraging lifestyle less viable and cause the need for a shift in subsistence (Cohen, 1977). By extension of this theory, all of the subsequent steps of urbanization and state formation can also be seen as inevitable consequences of pressures to support a burgeoning population. The archaeological record can be used to assess whether the transition to agriculture emerged gradually as an adaptation over a previously successful strategy, or as a result of environmental or demographic stress. In this context, the analysis of skeletal remains can tell us whether agriculture improved the quality of life of the earliest farmers, and whether this relationship is consistent through time and space. Previous analyses of these questions have largely focused on stress and disease though paleopathological markers, as these provide general indicators of poor quality of life (Cohen and Armelagos, 1984; Beckett and Lovell, 1994; Larsen, 1995, 2006; Keita and Boyce, 2001; Pechenkina et al., 2002; Steckel and Rose, 2002; Keita, 2003). Stressful stimuli recorded in human skeletal remains include disease and parasite load, dietary deciencies, and synergistic effects between the two (Scrimshaw et al., 1968; Stephenson and Holland, 1987; Keita, 2003). In this study, we investigate the patterns of disease and dietary health over the course of the Neolithic in the Nile valley, via a commonly studied indicator of general physiological stress, LEH of the dentition (Kreshover, 1940, 1944; Sarnat and Schour, 1941). This analysis is used to test whether the patterns of LEH are consistent across the agricultural transition, and through a time scale that includes not only the early Neolithic, but also the growth and expansion of the Egyptian and Nubian states. The patterns of health and disease that emerge are interpreted within the context of the causes and consequences of agricultural intensication in the Nile valley.

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1981; Hummert, 1983; Hummert and Van Gerven, 1983; Martin et al., 1984). However, this sample is notably lacking material from the Neolithic period in the Nile valley. The Nile valley is not considered to be an independent point of origin of agriculture. The traditional view, still commonly cited (Smith, 1995), is that domesticated crops and animals arrived gradually in the area from the fertile crescent. Evidence is accumulating, however, for early African domestication of cattle and grains in the Eastern Sahara and Western Desert regions, and these areas may also have served as sources of domesticated crops for the Nile valley Neolithic (Warfe, 2003). Archaeological evidence of cattle domestication in the Eastern Sahara (Wendorf et al., 1984) has been supported by genetic comparisons of 50 African cattle breeds (Hanotte et al., 2002), which suggest that cattle were independently domesticated in North Africa prior to interbreeding with domesticated cattle from the Near East. In addition, some researchers have emphasized the inuence of Lower Egypt and the Delta region on the Upper Egyptian Neolithic (Holmes, 1992; Warfe, 2003). Studies comparing modern and ancient DNA of domesticates, support a combination model involving multiple origins of agriculture with subsequent localized diffusions (Jones and Brown, 2000). The rst denitive food-producing sites in the Nile valley are from the Badari civilization, at 4500 B.C. Agricultural products at these sites consisted of barley, cattle, and sheep or goats (Arkell and Ucko, 1965). The lack of evidence of permanent dwellings and the relatively thin layer of animal droppings at this site are interpreted to mean that the settlement was not inhabited for very long; the Badarians were likely still seminomadic pastoralists rather than full-time farmers (Hassan, 1988). Regardless of its rst origins, it is undisputed that agricultural intensication in Egypt proceeded in earnest through the early Predynastic period, and by the beginning of the 1st Dynasty the Nile valley region was comprised of several sedentary communities, loosely united under the rst pharaohs (Kemp, 1989). This study examines the prevalence of LEH in ve Nile valley populations which surround the temporal span of the Neolithic, from late Paleolithic hunter-gatherers to the inhabitants of the hierarchical Nubian Kerma civilization. Based on past studies of other geographical regions, which show increases in skeletal stress and disease indicators in early agriculturalists as compared with contemporaneous foragers (Cohen and Armelagos, 1984; Pechenkina et al., 2002) it is hypothesized that the earliest proto-agricultural population, the Badari, will show the highest levels of nonspecic stress, as evidenced by the percentage of individuals with LEH of the dentition. Later populations are predicted to show some evidence of recovery and improved health, as urbanization and social complexity increased and food shortages were buffered by trade relationships (Hassan, 1988; Keita and Boyce, 2001; Zakrzewski, 2006).

The Northeast African context of agriculture

There has been relatively little study of the human biology of the agricultural transition in Africa. One prominent exception is a series of populations from Wadi Halfa in Sudanese Nubia which have been studied extensively for over 30 years (Armelagos, 1969; Vagn Nielsen, 1970; Armelagos et al., 1972; Van Gerven et al.,

MATERIALS AND METHODS

The skeletal remains used in this study were from ve chronologically distinct populations along the Nile in Egypt and Nubia between 13000 and 1500 B.C. (Table 1). The ve populations existed during three separate epochs: one in the Upper Paleolithic period, two in the

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Population Jebel Sahaba (Upper Paleolithic) Badari (Predynastic) Naqada (Predynastic) Tarkhan (Early Dynastic) Kerma (Late Dynastic) Total Time period

A.P. STARLING AND J.T. STOCK the sensitivity and specicity is largely unknown (Goodman and Rose, 1990). Formation of LEH bands has been associated with severe childhood diseases (Hillson, 1996) and childhood nutritional inadequacy (Rose et al., 1985), but no effort to relate enamel hypoplasia formation to a specic medical cause has yet been successful (Goodman and Rose, 1990). Studies of living populations have examined the association of LEH with other dental diseases and dental caries, as well as with childhood and congenital diseases (Enwonwu, 1973; Goodman et al., 1988; Lunardelli and Peres, 2005). The presence of LEH has been associated with rickets, congenital syphilis, and tuberculosis (Ortner and Putschar, 1981; Knick, 1982). Infectious or parasitic disease and malnutrition often have synergistic effects that may create a more serious disruption of health, which is then recorded in the bone and dental enamel (Stephenson and Holland, 1987; Keita, 2003). In summary, the presence of LEH is a useful non-specic indicator of physiological stress experienced in childhood. Therefore the frequency of this indicator in a population will here be considered to be inversely related to the overall health of the population.

TABLE 1. Origins and sample sizes of the study subjectsa N dentition 38 56 54 47 47 242

130009000 B.C. 50004000 40003100 31002686 21001500 B.C. B.C. B.C. B.C.

a All dates are approximate, based primarily on Kemp (1989) and Zakrzewski (2003).

Predynastic, and two in the Dynastic (or Pharaonic) period. The presence or absence and eruption status of all permanent and deciduous teeth was recorded according to criteria adapted from an earlier system (Moorrees et al., 1963). Each of the 32 permanent teeth (and 20 deciduous teeth, if present) was scored as unerupted, emerging, in occlusion, missing (for unknown reason), postmortem tooth loss, or antemortem tooth loss. If the tooth crown was greater than 50% complete, included a complete section from tip to cemento-enamel junction, and was not obscured by calculus, sediment, or other materials, it was considered scorable. The number of scorable teeth was noted for each individual. Loose teeth associated with an individual were not scored unless they t completely into a crypt in the mandible or maxilla.

Data collection
Scorable teeth were evaluated for the presence or absence and position of LEH by visual examination of the buccal surface of each crown, where the defect is most frequently observable (Goodman and Rose, 1990; Facchini et al., 2004). Enamel hypoplasia was operationally dened here according to the developmental defects of enamel (DDE) Index as a quantitative defect of enamel visually and morphologically identied as involving the surface of the enamel (an external defect) and associated with a reduced thickness of enamel (FDI, 1982). The type of defect examined here (and those most frequently referred to in the literature as LEH) falls under the FDIs Type 4 defects, horizontal grooves (see Goodman and Rose 1990, for a critical assessment of this denition). The presence or absence of LEH bands was recorded for each tooth in the dentition for each individual, due to previous reports of differential susceptibility of different tooth types to enamel defects (Goodman and Armelagos, 1985). It has been noted in several studies that the anterior teeth, particularly the maxillary incisors and mandibular canines, are more susceptible to LEH than are the more posterior molars and premolars (Goodman and Armelagos, 1985; Goodman and Rose, 1990; Berti and Mahaney, 1995). This has led some authors to select particular teeth for controlled observation. For example, Keita and Boyce (2001) intentionally used posterior (premolar) teeth in their study as they reasoned that these defects would indicate only the most severe disruptions of growth. However, due to the fragmentary nature of many of the ancient specimens in this study, all teeth positively attributed to a skull were scored for the presence or absence of LEH. Statistical measures were employed to compensate for the differential preservation of the different samples. The frequency of LEH in each population was then examined separately for each tooth type to address the potential for bias in susceptibility.

Linear enamel hypoplasia, a nonspecic stress indicator

LEH is a well-established indicator of individual past episodes of poor health and growth disturbance (Sarnat and Schour, 1941; Kreshover, 1940, 1944; Goodman and Rose, 1990; King et al., 2005). The enamel of permanent teeth forms during childhood and does not subsequently remodel (Skinner and Goodman, 1992). Intense periods of disease and nutritional stress can cause interruptions in the enamel formation, producing a band of reduced enamel thickness, or hypoplasia (Harris and Ponitz, 1980). This indicator has been examined in skeletal samples in order to test archaeological theories; for example, to examine the health effects of increasing urbanization (Keita and Boyce, 2001) or socioeconomic disparities (Cucina and Iscan, 1997), or to search for evidence of historical events such as famine (Lovell and Whyte, 1999). The most common current use of LEH data is to compare the levels of physiological stress in past populations, including modern humans (Cucina, 2002; King et al., 2005; Pechenkina and Delgado, 2006; Boldsen, 2007), Neandertals (Guatelli-Steinberg et al., 2004), nonhuman primates (Guatelli-Steinberg and Lukacs, 1999; Lukacs, 1999; Lukacs, 2001), and human ancestors (Skinner, 1996). The primary causes of enamel hypoplasia are heredity, localized trauma, and systemic metabolic stress (Goodman and Rose, 1990). Linear hypoplasias result from disturbances that last between several weeks to a few months (Rose et al., 1985). Among archaeological populations, systemic stress appears to be the most common cause of this disorder (Goodman et al., 1980; Goodman and Rose, 1990; Skinner and Goodman, 1992). While LEH has been accepted as a general indicator of systemic disturbances in development (Hillson, 1996),

Data analysis
v tests were used to analyze the differences in prevalence of LEH between populations. Complications
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Fig. 1. Percentage of individuals with one or more linear enamel hypoplasia bands anywhere in the dentition, by population.

encountered in the analysis included the marked differences in tooth preservation between populations, and the association between the number of teeth observed and the likelihood of observing LEH (Corruccini et al., 1985; Ogilvie et al., 1989). As the number of scorable teeth was not normally distributed, nonparametric tests were used. Biases in the data were examined using a KruskallWallis test to compare the number of teeth preserved between populations, and a MannWhitney Utest to compare the number of teeth preserved in individuals with and without LEH present. To address the preservation bias, the prevalence of LEH was also analyzed as a percentage of teeth rather than as a percentage of individuals. In addition, different tooth types were analyzed separately to examine their differential susceptibility, a factor discussed in previous studies (Goodman and Rose, 1990). Of particular interest to this study is the presence or absence of chronological trends in the frequency of skeletal stress indicators. The ve populations were ranked from earliest to latest and Kendalls tau correlation was used to examine the association between the presence of the indicators and chronological order. This was considered to be more appropriate to this particular association than a Spearman R test because the Kendalls tau tests the probability that the data are in the same order for the two variables. Therefore it makes no assumptions about the proportional distances between the ranked items.

Fig. 2. Mean number of scorable teeth per individual in each population.

Fig. 3. Mean number of scorable teeth present in individuals with and without one or more LEH bands anywhere in the dentition (Z 5 25.331; P < 0.001; Mann-Whitney U-test).

RESULTS
The overall frequency for the presence of LEH in one or more teeth was 42.1% of 242 individuals. There were signicant differences between the populations in the percentage of individuals with one or more LEH bands anywhere in the dentition (v2 5 27.594; df 5 4; P \ 0.001; Fig. 1). The highest frequency of LEH was found in the early agriculturalists at Badari (69.6%), although this population also had the highest level of tooth preservation; a correlation discussed in more detail below. A Kendalls tau test showed signicant correlations between population number (chronologically ranked) and presence of LEH (P \ 0.001). There was a negative correlation between these variables (T 5 20.202), meaning that as population rank increased through time, the prevalence of LEH decreased. Although the samples were collected in such a way that the number of scorable dentitions were roughly sim-

ilar among the populations (see Methods, Table 1), tooth preservation had considerable inuence on the prevalence of LEH. The number of teeth preserved per individual was not normally distributed. The mean number of teeth preserved per individual also varied signicantly between populations (v2 5 114.295; df 5 4; P \ 0.001; KruskallWallis test; Fig. 2). Individuals in the earlier (Jebel Sahaba and Badari) populations had higher mean numbers of teeth per individual than did the later populations. Previous studies have noted that LEH and other dental defects are frequently underestimated in skeletal populations because the likelihood of observing defects is related to the number of teeth preserved (Corruccini et al., 1985; Ogilvie et al., 1989). This observation was conrmed in the present study: samples with higher mean number of teeth preserved and scorable showed greater frequencies of LEH (Z 5 25.331; P \ 0.001; Mann-Whitney U-test; Fig. 3). While this relationship was signicant for the entire sample, the association between the

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Fig. 5. Percentage of total teeth with one or more LEH bands, by population.

Fig. 4. Mean number of scorable teeth preserved in individuals with and without one or more LEH bands anywhere in the dentition, by population. TABLE 2. Percentage of teeth in each population with one or more LEH band Population Jebel Sahaba Type of tooth All teeth Molars Premolars Canines Incisors All teeth Molars Premolars Canines Incisors All teeth Molars Premolars Canines Inciscors All teeth Molars Premolars Canines Incisors All teeth Molars Premolars Canines Incisors All teeth Molars Premolars Canines Incisors N of teeth with LEH 44 7 12 9 16 146 39 45 38 24 36 26 6 3 1 43 11 8 8 16 17 14 2 1 0 286 97 73 59 57 Total N of teeth 676 272 168 94 142 851 382 240 95 134 237 186 42 7 2 463 221 121 27 52 279 219 46 6 8 2,506 1,280 625 247 354 % of Teeth with LEH 6.5 2.6 7.1 9.6 11.3 17.2 10.2 18.8 40.0 17.9 15.2 14.0 14.3 42.9 50.0 9.3 5.0 6.2 17.8 23.5 6.1 6.4 4.3 16.7 0.0 11.4 7.6 11.7 23.9 16.1 Fig. 6. Frequency of LEH by tooth type, entire sample.

Badari

Naqada

Tarkhan

Kerma

All Populations

number of teeth in an individuals dentition and the likelihood that one or more of those teeth would show an LEH band was inconsistent within populations. This relationship was signicant within the Jebel Sahaba, Badari, and Tarkhan populations, but nonsignicant within the Naqada and Kerma populations (Fig. 4). To resolve some of these complexities, results were separated by population, by tooth, and by tooth type. Examining the presence of LEH per tooth rather than

per individual reduces preservation bias to some degree, but this approach has residual inuences on results: LEH defects due to systemic stress are generally found on more than one tooth (Goodman and Rose, 1990) so individuals with many teeth preserved may have disproportionate inuence on the result. However, this analysis revealed patterns of differential susceptibility and preservation bias (Table 2). The patterning of the frequency of LEH per tooth was very similar to the pattern previously observed per individual, but the trend was even more pronounced (Fig. 5). The highest per tooth frequency of LEH was in the Badari population; this was substantially higher than in the earlier Jebel Sahaba population. There was a gradual decline in prevalence of LEH per tooth over the subsequent populations, with the lowest frequency found among the Kerma (Dynastic) population. The sample size of scorable teeth varied greatly for each tooth type. The largest sample was 164 for permanent left maxillary second molars while the smallest samples were 37, for both the permanent left and right mandibular rst incisors. The distribution of LEH frequencies by tooth type (Fig. 6) suggests that differential preservation may have led to underestimation in the overall frequencies of LEH, as the teeth most likely to show the defect were the anterior maxillary teeth which were least frequently preserved. In accordance with previous studies (reviewed in Goodman and Armelagos, 1990) the populations examined here had the highest rates of LEH in the anterior teeth. The highest frequency of LEH was found in the left mandibular canine (36.8% of 57 teeth). The lowest frequency of LEH was found in the left maxillary third molar (1.7% of 115). This trend was generally consistent within the populations; however, many of these sample sizes were too small for statistical analysis.

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Fig. 7. Frequency of LEH by population for each tooth type.

When different tooth types were examined separately, the same general trends were observed: rates of LEH were generally highest in the Predynastic populations and lower in the Dynastic ones and the prehistoric foragers (Fig. 7). The differences in LEH frequency between populations were signicant for molars (v2 5 29.956; df 5 4; P \ 0.001), premolars (v2 5 21.409; df 5 4; P \ 0.001), and canines (v2 5 26.639; df 5 4; P \ 0.001); and marginally nonsignicant for incisors (v2 5 8.795; df 5 4; P 5 0.0664), likely due to the very small sample size. A Kendalls tau correlation showed a signicant association between the prevalence of LEH and the chronological population rank (T 5 20.185; P \ 0.002). However, there appeared to be two separate trends in this data, an initial increase followed by a decrease in dental stress indicators. This was addressed by examining the initial transition to agriculture, from Jebel Sahaba to Badari, separately from the later progression of agricultural intensication, from Badari through Kerma. A v2 test conrmed a signicantly higher prevalence of LEH per individual in Badari than in Jebel Sahaba (v2 5 8.429; df 5 1; P \ 0.01). Separate Kendalls tau tests showed: (1) a signicant positive correlation between LEH and population rank for the earliest two populations (T 5 0.299; P \ 0.005), and (2) a signicant negative correlation for the latter four populations (T 5 20.288; P \ 0.001). In addition, a binomial logistic regression predicting the presence or absence of LEH based on population rank for the latter four populations successfully classied 68.1% of cases.

DISCUSSION
In this study, dental indicators of stress and disease were analyzed to evaluate the conditions of the transition to agricultural subsistence in the Nile valley. It was hypothesized that the earliest agricultural populations would show the highest levels of LEH, indicating the highest levels of physiological stress. The results supported this hypothesis by demonstrating that the earliest proto-agricultural population (Badari) had the highest levels of dental developmental interruptions. It is beyond the scope of this study to infer whether or not this stress was due to resource depletion, disease, or dietary insufciency as suggested by other researchers (Cohen, 1977). However, this nding does support the idea that the Neolithic subsistence transition was necessitated by ecological or demographic factors in the Nile valley. As in many other regions studied, the advent of food production appears to be associated with a decline in health for the earliest agriculturalists (Cohen and Armelagos, 1984; Steckel and Rose, 2002; Larsen, 2006).

The present study differs from previous studies in its broad time scale and inclusion of the oldest known preagricultural skeletal population in the area (Jebel Sahaba). This analysis suggests a substantial increase in stress at the origins of agriculture over late Upper Paleolithic foragers. LEH levels reached a peak in the earliest agriculturalists, followed by a decline during the period of intensication and state formation. This pattern persists when the analysis is restricted to like teeth to compensate for differences in susceptibility of different tooth types (Fig. 7). Of particular interest in Figure 7 is the LEH prevalence in premolars, which shows pattern very similar to the overall prevalence of LEH by tooth (Fig. 5). As premolars are less sensitive than incisors or canines to enamel defects, past researchers have argued for a conservative scoring procedure which includes only premolars (Keita and Boyce, 2001). Any comparative study of skeletal populations must approach the interpretation of differences with caution, in order to rule out the confounding role of underlying genetic variation. The populations examined here lived in roughly the same geographic area, but over a span of nearly 10,000 years. All populations shared an ecology that was dominated by the variable oods of the Nile, which suggests that the broad environmental context of the samples is relatively consistent. In addition, there is substantial evidence for contact and trade between populations along the Nile valley as far south as Lower Nubia, at least as early as the Predynastic period (Arkell and Ucko, 1965). The question of the genetic origins of ancient Egyptians, particularly those during the Dynastic period, is relevant to the current study. Modern interpretations of Egyptian state formation propose an indigenous origin of the Dynastic civilization (Hassan, 1988). Early Egyptologists considered Upper and Lower Egyptians to be genetically distinct populations, and viewed the Dynastic period as characterized by a conquest of Upper Egypt by the Lower Egyptians. More recent interpretations contend that Egyptians from the south actually expanded into the northern regions during the Dynastic state unication (Hassan, 1988; Savage, 2001), and that the Predynastic populations of Upper and Lower Egypt are morphologically distinct from one another, but not sufciently distinct to consider either nonindigenous (Zakrzewski, 2007). The Predynastic populations studied here, from Naqada and Badari, are both Upper Egyptian samples, while the Dynastic Egyptian sample (Tarkhan) is from Lower Egypt. The Dynastic Nubian sample is from Upper Nubia (Kerma). Previous analyses of cranial variation found the Badari and Early Predynastic Egyptians to be more similar to other African groups than to Mediterranean or European populations (Keita, 1990; Zakrzewski, 2002). In addition, the Badarians have been described as near the centroid of cranial and dental variation among Predynastic and Dynastic populations studied (Irish, 2006; Zakrzewski, 2007). This suggests that, at least through the Early Dynastic period, the inhabitants of the Nile valley were a continuous population of local origin, and no major migration or replacement events occurred during this time. Studies of cranial morphology also support the use of a Nubian (Kerma) population for a comparison of the Dynastic period, as this group is likely to be more closely genetically related to the early Nile valley inhabitants than would be the Late Dynastic Egyptians, who likely experienced signicant mixing with other Mediterranean

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A.P. STARLING AND J.T. STOCK Alternatively, lower LEH frequency in later populations studied may indicate that intensication and urbanization eventually provided greater health and quality of life for Egyptians. The evidence for improvements in health of these increasingly complex societies may be attributed to trade relationships and the centralization of food storage and distribution, enabling Predynastic and Dynastic societies to withstand seasonal food shortages which would have been highly disruptive to an isolated agricultural community (Hassan, 1988; Savage, 2001). This interpretation is supported by a recent nding that the stature of Nile valley inhabitants increased throughout the Predynastic period, without evidence of population discontinuity (Zakrzewski, 2006). Ironically, this very pooling of resources that may have initially improved health, enabled concentrations of power in hierarchical societies characterized by poor quality of life for those in the lower classes (Hassan, 1988). Because of the wide geographic and temporal span of the samples, the differences observed here must be interpreted as preliminary. The different histories of early agricultural intensication in Lower and Upper Egypt may have inuenced LEH manifestation. In addition, there may still be underlying unidentied differences between the populations which affect their susceptibilities to defects of dental enamel (Goodman and Rose, 1991). While the relative similarity between the Upper and Lower Egyptian morphologies is addressed above, underlying heterogeneity is most likely to be problematic for the Jebel Sahaba foragers, because of their temporal distance from the other populations. In addition, there is some evidence from dental morphology to suggest that these Paleolithic Nubians are of independent origin to the later Nubian populations (Irish, 2005). This study has identied changes in LEH frequency over time amongst hunter-gatherer, nomadic pastoralist and agricultural Dynastic populations of the Nile valley. Future research should investigate whether these trends are consistent within more nely resolved spatial and temporal contexts. Conducting more in-depth regional studies of the interrelationships of sedentism, social complexity, food supply, and social inequality will greatly enhance our understanding of the relationship between these factors. In Egypt, as in many other areas of the world, state formation followed closely on the heels of agricultural intensication, making this initially risky subsistence strategy more reliable and sustainable in the long run by facilitating the redistribution of resources. The earliest agriculturalists of this region, as in many others, bear the mark of a difcult transition between subsistence strategies.

populations (Zakrzewski, 2002). A craniometric study found the Naqada and Kerma populations to be morphologically similar (Keita, 1990). Given these and other prior studies suggesting continuity (Berry et al., 1967; Berry and Berry, 1972), and the lack of archaeological evidence of major migration or population replacement during the Neolithic transition in the Nile valley, we may cautiously interpret the dental health changes over time as primarily due to ecological, subsistence, and demographic changes experienced throughout the Nile valley region. The frequency of LEH in the proto-agriculturalist Badari population was signicantly higher than among earlier hunter-gatherers, and also higher than among later populations, during the period of state formation and increasing social complexity in Nile valley. Why, then, did the early Badarians become more sedentary and increase their dependence on agriculture when it did not immediately increase their health and tness? One possibility is that agricultural dependency may have been forced on a formerly hunting and gathering population by climatic changes or increased population density. Archaeological evidence suggests that the shortlived Badari civilization had higher population density than did other contemporaneous civilizations (Gabriel, 1987; Hassan, 1988). Increases in population may have been caused by immigration from the Western Desert as the climate there became more arid and less habitable around 5000 B.C. (Hassan, 1988, 1993). It is generally agreed that the techniques of agricultural domestication were adopted much later in the Nile valley than in the Near East or the Eastern Sahara, despite the likely interactions between the Nile valley inhabitants and these nearby agriculturalists (Wendorf et al., 1984, 1992; Holmes, 1993). This delay suggests that the previous subsistence pattern had to be rendered unstable before this transition would be desirable or widespread. This delay in Lower Egypt may be explained by the fact that soils in the Nile delta region may have been unsuitable for cultivation prior to increased silt deposition around 6,000 B.P. (Stanley and Warne, 1993). However, this does not seem to explain the reluctance of Upper Egyptians to adopt the grains domesticated by their Eastern Sahara neighbors as early as 8,000 B.P. (Wendorf et al., 1992). When the Neolithic began in the Nile valley, it does not seem to have been immediately benecial to human health. There are numerous costs associated with agricultural intensication, and the proto-agricultural Badari population likely suffered from many of these. A signicant nding, however, is that the relatively poor health of the Badarians does not appear to have slowed the pace of urbanization and increasing social complexity. Urbanism and increasing population density are almost universally associated with increases in infectious disease (Cohen, 1989; Stuart-Macadam and Kent, 1992; Steckel and Rose, 2002) and it is interesting that these changes, occurring throughout the late Predynastic and early Dynastic periods, are associated with decreasing frequencies of LEH disturbances. This may indicate that the kinds of disturbances recorded by LEH are more frequently those associated with seasonal food shortage rather than the epidemic diseases of urbanization. This subtlety of etiology is difcult to separate in modern clinical studies, where poverty inevitably brings both food insecurity and increased susceptibility to infectious disease.

ACKNOWLEDGMENTS
The authors would like to acknowledge the detailed and constructive comments of the editor and both reviewers, which resulted in signicant improvements to the manuscript. We would also like to thank John Taylor of the Department of Ancient Egypt and Sudan of the British Museum, London, UK, for access to the Jebel Sahaba remains. All other specimens were housed in the Duckworth Collection of the Leverhulme Center for Human Evolutionary Studies, at the University of Cambridge, UK, and we would like to extend our appreciation to Ms. Maggie Bellatti, for her assistance.

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