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Trends in Ancient Populations’ Osteobiography during the Holocene: the Levantine Perspective

Israel Hershkovitz, Rachel Sarig et Hila May
p. 71-82

Résumés

Résumé. Les changements rapides de notre environnement au cours de l’Holocène mettent le corps humain au défi. L’étude actuelle, menée sur les populations du Pléistocène final et de l’Holocène du Levant, présente plusieurs exemples sur la manière dont les changements d’habitat et de régime alimentaire ont affecté les schémas pathologiques et la morphologie brute des os longs et des mandibules. Nos principales conclusions ont révélé que les populations préhistoriques du Natoufien (67 %) et celles protohistoriques du Chalcolithique (80 %) présentaient un taux d’inflammation de l’oreille (otite moyenne) beaucoup plus élevé que toutes les autres populations : néolithique, romaine/byzantine et ottomane (50 % ± 5 %). Une diminution générale continue et significative de la surface corticale relative de l’os fémoral entre le Natoufien (77,8 %) et l’époque actuelle (64,7 %) a pu être observée (la population chalcolithique étant l’exception). La forme de la mandibule a considérablement changé, principalement entre la population pré-agricole (le Natoufien) et les suivantes (c.-à-d., le ramus est devenu plus grand et plus étroit, le processus coronoïde plus haut et plus pointu, l’encoche mandibulaire plus étroite et plus profonde et le corps plus triangulaire). Les facteurs comportementaux, économiques et environnementaux possibles associés à ces changements sont discutés.

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The authors wish to thank the Dan David Foundation and the Israeli Science Foundation (grant no. 1116/16 and 2632/18) for their financial support. CT scans were carried out at the Shmunis Family Anthropology Institute, Tel Aviv University. We would like to thank Mr. Ariel Pokhojaev for his assistance in creating the figures and Rasha Abu-Jebel for preparing the manuscript for publication. Steve Manch edited the paper.

1For hundreds of thousands of years, our species has evolved, both anatomically and physiologically, into an efficient hunter-gatherer. When most of his “cousins” (e.g., Neanderthals, H. Denisovans, H. Floresiensis, and H. Lusonensis) disappeared, Homo sapiens continued to flourish and conquer new ecological niches, becoming undoubtedly the most successful representative of the genus Homo.

2Until the beginning of the Natufian period (ca. 15,000 years ago), the selection forces that acted on humans to adapt them to life as hunter-gatherers had fluctuated very little. However, this situation changed dramatically during the Natufian period: the old life style, which was practiced for hundreds of thousands of years and involved hunting and gathering, was quickly replaced by a sedentary life style that largely relied on farming (Bar-Yosef 1998; Belfer-Cohen and Goring-Morris 2011). Large communities were soon established, the demographic structure of the populations changed, a division of labor evolved, social stratification emerged, and cultures sometimes quickly changed (Hershkovitz and Gopher 2008; Belfer-Cohen and Goring-Morris 2011). From the Neolithic period onward, human populations underwent temporal and perhaps extreme changes in various aspects of their daily life (e.g., physical activity, diet, health, and demography; Hershkovitz and Gopher 1990, 2008; Eshed et al. 2004a, 2004b; May and Ruff 2016). Consequently, rapid fluctuations in selection pressure arose, requiring equivalent temporal changes in the population’s fitness and its ability to adapt to changes. However, the population’s biological adaptation could not occur at the same pace, leaving Holocene people seemingly trapped in the body of Upper Paleolithic hunter-gatherers. The social adaptation, however, was enforced through rules, prohibitions, and laws initiated by a newly evolved centralized political and economic system (Belfer-Cohen and Goring-Morris 2011).

3Many studies have been published on the terminal Pleistocene-early Holocene populations of the Levant: the Natufian (13,000 BC-9,500 BC) and the Pre-Pottery Neolithic (9,500 BC-6,400 BC). During this period, one of the most dramatic events in human evolution occurred, namely, the “Agricultural Revolution’. Changes in dental diseases as well as the attrition rates and patterns (Eshed et al. 2006), the prevalence of infectious diseases (Eshed et al. 2010) including the appearance of tuberculosis (Hershkovitz et al. 2008), physical loads (Eshed et al. 2004b; May and Ruff 2016), demography (Eshed et al. 2004a; Hershkovitz and Gopher 2008), physiognomy, and burial customs (Hershkovitz and Gopher 1990; Slon et al. 2014) have been reported. New ecological niches were conquered and people started to look for food not just on land, but also in the sea (Galili et al. 1993). For reasons not currently clear, the “golden age” of the Pre-Pottery Neolithic (PPN) culture in the Levant came to an end around 6,400 BC. The local populations started to flourish again in the Chalcolithic period (4,500 BC-3,900 BC), probably partially due to the introduction of new populations following migrations (probably from Anatolia) into the local population (Harney et al. 2018). This period became the prologue to some of the greatest achievements and milestones in human history including the “Secondary Products Revolution” (derivatives from animal sources such as wool, textiles, and dairy goods), metal production, the development of art and religion, and the emergence of specialized occupations and professions. The Chalcolithic period ended in Israel around 3,900 BC, with the rise of the Early Bronze civilization, marking the beginning of urbanization, the appearance of kingdoms and empires, and most importantly, writings (Gilead 1988).

4Studies of archeological populations that underwent changes in subsistence strategies from hunter-gathering to agriculture (Natufians vs. the Pre-Pottery Neolithic) have generally revealed a decline in health (Goodman et al. 1980, 1984; Angel 1984; Larsen 1995, 2006; Mummert et al. 2011). In the southern Levant, this was manifested by a decrease in the female life expectancy and an increase in the prevalence of infectious diseases and perhaps pandemics (Hershkovitz and Gopher 2008; Eshed et al. 2010).

5The aims of the current paper were to follow the temporal changes in the biological and morphological features of Levantine populations during the Holocene, and to examine them in light of known data regarding their living conditions, subsistence strategies, and environmental conditions.

Material and methods

6Various skeletal remains (i.e., petrous, mandible, and femur) of different populations including Natufian hunter-gatherers, Pre-Pottery Neolithic early farmers, Chalcolithic farmers, Roman/Byzantine farmers, Ottoman farmers housed at the Anthropological collection, the Dan David Center for Human Evolution and Biohistory Research, Sackler Faculty of Medicine, Tel Aviv University as well as recent populations (approved by the ethics board of the Carmel Medical Center, number: 0066-11-CMC) were examined (table 1).

Table 1 Skeletal remains examined in the study, by population.

Table 1               –        Skeletal remains examined in the study, by population.

7Estimating the presence of ear infection: The promontory of all petrous bones was examined using a flexible videoscope (PENTAX Medical VNL-CP, field 90¡, depth of field 5-50 mm, distal end width 3mm, deflection 120¡/120¡, LED illumination) and an optical microscope (Nikon SMZ745T magnification range: ×6.7 to ×50). Interruptions in the integrity of the promontory bony surface were recorded as either manifesting or not manifesting ear infection. These interruptions may appear either as bony bulges (appearing as isolated narrow bony crests or isolated bony spicules), or as zones of bone resorption (Folreanova et al. 2020).

8Estimation of physical load: Mid-shaft cross-sectional images were obtained from the CT scans of the femora (Brilliance 64 [Philips Medical Systems, Cleveland, Ohio]: slice thickness 0.8-1 mm, 140 kV, 150 mA, rotation time 0.75 s, Pitch 0.39, and Matrix 512 × 512). The amount of the cortical bone was measured in relation to the total area of the cross section (i.e., %CA = cortical area/Total area × 100) via a dedicated software developed for this purpose (May and Ruff 2016).

9Estimation of dietary quality: The relative size of the medullary cavity (medullary cavity diameter/total cross-sectional diameter) in long bones, mainly of the lower limbs can be used as indicator of food quality and the general health of a population (Garn et al. 1970; Ruff 1999; Heaney et al. 2000; Horocholyn and Brickley 2017). The medullary cavity diameters on the antero-posterior and medio-lateral axes were measured from the midshaft cross sections of the femur, obtained from CT. To control for body size, the AP and ML medullary cavity diameters were divided by the corresponding total diameter of the midshaft cross section.

10Estimation of dietary habits: Shape analysis of hemimandibles was carried out on mandibles that either underwent a high-resolution computerized tomography (CT) scan (Brilliance 64, Philips Medical Systems, Cleveland, Ohio: slice thickness 0.5-0.8 mm, 100 kV, 150 mAs, rotation time 0.75 s., pitch 0.39, and Matrix 768 × 768), or were surface scanned via a Space Spider portable 3D scanner (Artec Europe, Luxembourg). For mandibles that were scanned via CT, a 3D surface mesh of the mandibles was reconstructed from CT stacks using Amira 6.3 software (www.fei.com). A semi-automated segmentation of CT stacks was carried out, based on gray level thresholds. Manual segmentation was performed where needed. For those mandibles scanned by the surface scanner, the image processing and alignment were carried out via Artec Studio 13 software (Artec Europe, Luxembourg). The 3D shape of the mandible was analyzed using the Procrustes-based geometric morphometrics method, which included 52 landmarks (16) and semilandmarks (36) representing eight curves (Sella Tunis et al. 2018). Landmarks were placed by the same researcher on the 3D surface mesh of the mandible using Evan Toolbox software 1.72 (www.evan-society.org). Semilandmark sliding was carried out based on the minimum bending energy technique (Gunz and Mitteroecker 2013).

Changes in comorbidity throughout the Holocene: challenges as well as speculations

11In order to follow changes in disease prevalence over time, the disease must fulfil two a priori conditions, namely, it must leave distinct marks on the bones (many different diseases leave similar marks on the bones) and be common enough. Otitis media (OM), i.e., the inflammatory disease of the middle ear, fulfils these two basic requirements. Presently, acute otitis media affects about 11% of people each year (about 709 million cases), with half occurring in individuals below five years of age (Monasta et al. 2012). Chronic suppurative otitis media affects about 31 million, with 22.6% of these cases occurring annually in children under the age of five years (Monasta et al. 2012). The disease, regardless of type, may persist for months; this often leads to a remodeling of the osseous wall of the middle ear. The common cause of all forms of otitis media in children is dysfunction of the eustachian tube (Bluestone 2005).

12Our laboratory developed a reliable method for identifying ear infection in skeletal material (Floreanova et al. 2020; fig. 1), in which remodeling of the promontory surface, a preserved structure in the middle ear, which under normal conditions, undergoes little remodeling if any, is used as an indicator of infection. Analysis of the middle ear of six populations that lived in the southern Levant during the terminal Pleistocene-Holocene revealed that two populations exhibited a higher prevalence of OM: the prehistoric Natufian (67%) and the protohistoric Chalcolithic (80%) populations. All other populations (Neolithic, Roman/Byzantine, and Ottoman) showed a prevalence of 50% ± 5% (Folreanova et al. 2020). Our results fall within the variation of the mediaeval pre-antibiotic period from different regions (Flohr and Schultz 2009, Krenz-Niedbała and Łukasik 2016).

Fig. 1 – Ear infection diagnosis based on bone remodeling of the promontory surface (after Floreanova et al. 2020, modified bracket. A, B: No remodeling is evident; the surface is smooth when directly observed via a videoscope (PENTAX Medical VNL9-CP; A) and a light microscope (SMZ1270i, Nikon equipped with a digital camera DS-Fi3, Nikon; B); C, D: Isolated, bony overgrowths with clear margins appearing as a narrow bony crest (1) or a bony spicule (2) observed via videoscope (C) and a light microscope (D); E, F: Interruption of the integrity of the promontory bony surface observed via videoscope (E) and a light microscope (F).

Fig. 1 – Ear infection diagnosis based on bone remodeling of the promontory surface (after Floreanova et al. 2020, modified bracket. A, B: No remodeling is evident; the surface is smooth when directly observed via a videoscope (PENTAX Medical VNL9-CP; A) and a light microscope (SMZ1270i, Nikon equipped with a digital camera DS-Fi3, Nikon; B); C, D: Isolated, bony overgrowths with clear margins appearing as a narrow bony crest (1) or a bony spicule (2) observed via videoscope (C) and a light microscope (D); E, F: Interruption of the integrity of the promontory bony surface observed via videoscope (E) and a light microscope (F).

13What could explain the high prevalence of OM in these two populations that engaged in completely different lifestyles and dietary habits and that are more than 6,000 years apart? Why was morbidity so high in the Chalcolithic period? In our quest for possible answers, we examined several possibilities and present here what we think are the most likely ones.

14The Natufians were the last hunter-gatherer population in Israel that used caves and terraces in front for habitation. Many of the large Natufian sites in Israel (e.g., Hayonim, Nahal Oren, and Rakefet) are actually cave-based camps. Since cave-dwellers are exposed to smoke, i.e., indoor pollution, to a much greater extent than people living in open areas, this may explain the high prevalence of OM in this group. Indoor air pollution can cause upper respiratory infection as well as middle ear effusion because it irritates the mucus (Bruce et al. 2000). Many studies have shown that indoor air pollution (originating, for example, from smoking tobacco, cooking, and heating) places children at more risk for ear infections (Uhari et al. 1996; Ilicali et al. 1999; Bruce et al. 2000; Murphy 2006).

15Although it is tempting to use this argument for the Chalcolithic population as well, since at least in the southern part of Israel the people during this period dwelled in artificial caves, the abundance of open sites suggests that a definitive causal explanation is more complex. Whatever the cause, considering the very high prevalence of this disease, it must have been distressing.

16The Chalcolithic population, in contrast to their preceding populations, probably consumed dairy products (Gilead 1988; Evershed et al. 2008). Interestingly, the association between cow’s milk intake and recurrent ear infections in children has been documented in many studies (Juntti et al. 1999). Although there are rare cases of pathogens in milk directly causing ear infections, the link is thought to be due to milk allergies (Juntti et al. 1999). Ear infection is due to fluid building up in the respiratory passages, sinuses, and the eustachian tubes of the ears. Today, around 5% of children and adults seem to be either allergic or intolerant to milk (Ludman et al. 2013).

17An additional possible factor for the increase in the prevalence of ear infections during the Chalcolithic period is the unique climatic conditions. In contrast to the preceding and succeeding periods, the weather was colder and wetter during the Levantine Chalcolithic period (Litt et al. 2012). Cold and wet weather is also considered a risk factor for ear infections (Šprem and Branica 1993).

Fig. 2 – Prevalence of ear infections in various populations (adults only) during the terminal Pleistocene-Holocene Levant.

Fig. 2 – Prevalence of ear infections in various populations (adults only) during the terminal Pleistocene-Holocene Levant.

Changes in the physical burden over time

18Throughout life, bone modeling and remodeling have dramatically changed bone strength, which can be enhanced through functional loading (Seeman 2008). Following the Mechanostat approach (Frost 2003), when all else is equal, individuals who are physically active should have stronger bones than their less active peers would. However, in order for loading to generate sufficient strain on the bone to elicit a response, the following should occur: the loading should be of sufficient magnitude; it should be distributed to the skeleton in abnormal directions, and it should be exerted at a regular frequency (Schoenau 2005). Since the skeletal response to loading is site specific (Sugiyama et al. 2010), some habitual activities can be detected (see, for example, Eshed et al. 2004b). However, determining which activity is more labor intensive is sometimes not straightforward or is even unsuccessful.

19Since the majority of conventional weight-bearing exercises generate loading to the lower limbs, in the current study we examined changes in the relative cortical area (CA) of the femoral midshaft cross section during the Holocene. We preferred to present this parameter rather than other typically accepted cross-sectional geometry parameters because it includes information both on the strength of the bone as well as on its relative amount (Ruff et al. 2006). We noticed a general continuous significant decrease in %CA (cortical subperiosteal bone area/total cross-sectional area ×100) from the Natufian period (77.8%) to present times (64.7%); however, the Chalcolithic population was an exception (fig. 3). For reasons not presently known, the Chalcolithic population deviated from the general trend and exhibited a very high %CA, almost as high as the Natufian population (fig. 3).

Fig. 3 – Changes in the relative subperiosteal cortical bone area ([cortical area/total cross-sectional area at midshaft] ×100) in southern Levant populations during the Holocene.

Fig. 3 – Changes in the relative subperiosteal cortical bone area ([cortical area/total cross-sectional area at midshaft] ×100) in southern Levant populations during the Holocene.

20These results raised two intriguing questions: Is the general decrease in %CA due to an ongoing decrease in physical stress (mainly axial loading) over time? Why did the Chalcolithic population deviate so sharply from the general trend? As is well known, bone tissue is extremely dynamic, and continuously responds to diverse biochemical and physical stimuli, but to what stimuli?

21As for the first question, the answer would be affirmative if we assume that the Natufians had walked long distances and had run (characteristics of hunting and foraging), i.e., both types of activities require greater resistance to axial loads (large cross-sectional areas). It has been shown that (a) low levels of physical activity contribute to reduced bone strength (Ryan and Shaw 2015), and (b) runners increase periosteal apposition (which augments bone strength through greater resistance against bending forces), compared with elite swimmers and non-athletic individuals (Hind et al. 2010, 2012). Periosteal apposition reduces bone fragility by adding more bone mass to the skeleton; it increases stiffness and strength by adding bone farther away from the central axis (Turner 2003). Ryan and Shaw (2015) have shown that the femoral head of mobile foragers possesses a significantly higher bone volume fraction and significantly thicker trabeculae compared with agriculturalists, who are more sedentary.

22But what about the Chalcolithic population? Their lifestyle did not differ much from later populations. The only parameter common to both the Natufian and Chalcolithic populations examined in the current study was their residential environment (i.e., the geographic elevation), i.e., most of the Chalcolithic sample studied here were from the Peqi’in Cave in the Upper Galilee and most of the Natufian material was either from the Upper Galilee or the Carmel mountain. It has already been shown that people who live at high elevations have a better bone status than those who live at low elevations due to the chronically greater daily activity caused by steep slopes in rural mountainous areas (Takeda et al. 2015).

Changes in the diet quality over time

23Until the 1980s, the leading theory was that domestication of plants and animals resulted in improved nutritional status (i.e., the balance between the intake of nutrients by an organism and their expenditure in the processes of growth, reproduction, and health maintenance). However, Armelagos and Cohen (1984) revolutionized this line of thinking and claimed that the Neolithic transition brought about a decline in the food quality, which continued until the industrial revolution. Their arguments were mainly based on observations suggesting that the general health status of the population had declined, based on the tooth attrition rates and patterns, and the prevalence of various dental/oral diseases. The major drawback of the dental-based studies was that all of these markers can be used to gain insights on food consistency and preparation methods, but they often reveal very little about the quality of the diet.

24One of the markers that can be used for such a purpose is the relative size of the medullary cavity (medullary cavity diameter/total cross-sectional diameter) in long bones, mainly of the lower limbs. In populations that are malnourished or exposed to high systemic stress, low bone mass is expected, with an enlargement of the endosteal surface (Garn et al. 1970; Ruff 1999; Heaney et al. 2000; Horocholyn and Brickley 2017).

25The availability of CT femoral diaphysis images of the Holocene Levantine populations allowed us to follow changes in the medullary cavity’s relative size over time (changes in medullary cavity diameters along the antero-posterior and the medio-lateral axes of the femur in relation to the total cross-sectional diameters).

26Our results clearly show a temporal increase during the terminal Pleistocene-Holocene Levant in the medullary cavity space, regarding the cortical bone thickness area (excluding the Chalcolithic population; fig. 4). The femora from the Chalcolithic period displayed a relatively small medullary cavity, similar to that of the Natufian femora. The overall increase in the relative medullary cavity size and consequently, a decrease in the relative cortical bone thickness imply a greater rate of endosteal resorption over time. This may indicate that nutritional factors, among other factors, may have been involved. Previous studies, based on skeletal and dental remains, suggested that in the Levant, nutrition deteriorated following the agricultural revolution (Smith and Peretz 1986; Hershkovitz and Gopher 2008). This may have been due to many factors, non-dietary (e.g., higher population density and reduced hygiene, and increased parasite load) and dietary factors (e.g., the transition to monotypic diets based on a few domesticated animals and plants bracket; Smith et al. 1984; Larsen 1995, 2003, 2006; Bar-Yosef 1998; Cordain et al. 2005; Lucock et al. 2014). Low intake of calcium and vitamin D, along with lower levels of dietary proteins as well as a decline in the health status, could have caused an imbalance in bone remodeling, leading to bone resorption and reduced cortical bone thickness (Garn et al. 1964; Garn 1970; Himes et al. 1975; Freudenheim et al. 1986; Owsley 1991; Hirota et al. 1992; Larsen 1995; Hannan et al. 2000).

Fig.  4 – Relative medullary cavity breadth measured at the femoral mid-shaft cross section in samples from various periods during the terminal Pleistocene-Holocene Levant.

Fig.  4 – Relative medullary cavity breadth measured at the femoral mid-shaft cross section in samples from various periods during the terminal Pleistocene-Holocene Levant.

27What could have occurred in the Chalcolithic period to have caused the diet quality to improve so much? It is probably a combination of two factors: climate and the type of food consumed. Litt et al. (2012) suggested that the Levant underwent several climate change cycles throughout the Holocene, i.e., arid and warm weather in the early Holocene period (∼10-6.5 ka cal. BP), wetter and colder weather in the mid Holocene (6.3-3.3 ka cal. BP), and drier and warmer weather in the late Holocene (∼3.2 ka cal. BP to the present). Being an agrarian culture in nature, the Chalcolithic population greatly benefited from increased precipitation and consequently, a better, more diverse, and well-balanced diet. Their subsistence was based on farming crops—chiefly wheat, barley, and lentils—and on livestock: sheep, goats, and cattle. The livestock was also used for producing wool and dairy products. People of the Chalcolithic period were also the first, in Israel, to grow cultivated fruit-bearing trees, such as date palms, olive trees, and pomegranates (Gilead 1988).

Food consistency and preparation methods

28The transition to food production was followed by changes in the food preparation techniques (e.g., grinding vs. pounding, and the introduction of cookware and other utensils; Gopher et al. 1992; Goren and Gopher 1995; Eshed et al. 2006). Changes in the cooking methods resulted in reduced stiffness of the food and therefore, in reduced mastication forces required for processing the food. Previous studies have shown that mandibular shape is associated with mastication loadings (Sella-Tunis et al. 2018). Accordingly, mandibles associated with high mastication loadings are associated with a wider, more trapezoidal-shaped ramus, a more massive coronoid (wide and low), and a rectangular body. In contrast, mandibles with lower mastication loadings are characterized by a tall and narrow ramus (more like a parallelogram), a pointed coronoid (narrow and tall), and a triangular body. We have demonstrated (Pokhojaev et al. 2019) that during the terminal Pleistocene-Holocene Levant mandibular shape had changed considerably, mainly between the pre-agricultural population (the Natufian) and the succeeding ones, and between the pre-industrial and the post-industrial populations. A tendency for a reduction in mandibular size was identified between the pre-agricultural population and the farmers. Changes in mandibular shape that correspond to mastication loadings are presented in figure 5.

Fig.  5 – Patterns of mandibular shape transformation from Natufian hunter-gatherers to the present time. The magnitude of the shape transformation between the warped surfaces of the mean shape is presented via a color map (the lowest value is in blue and the highest is in red). Note that the coronoid process shape and the mandibular angle regions exhibit the highest change over time.

Fig.  5 – Patterns of mandibular shape transformation from Natufian hunter-gatherers to the present time. The magnitude of the shape transformation between the warped surfaces of the mean shape is presented via a color map (the lowest value is in blue and the highest is in red). Note that the coronoid process shape and the mandibular angle regions exhibit the highest change over time.

29Variance of mandibular shape, captured by 52 landmarks and semilandmarks, indicated that throughout the first PC (explaining 19.7% of variance), the mandibular shape changed from the pre-agricultural population (the Natufian) to the post-industrial population (the Modern), mainly regarding the mandibular body and ramus. The mandibular body became more triangular (a reduction in its posterior height, relative to its anterior one); the mandibular ramus became narrower, elongated, and posteriorly tilted; the coronoid process became narrower and elongated, extending beyond the condyle height, and the mandibular notch became narrower and deeper. The third PC (explaining about 11.1% of the variance) differentiated between the post-agricultural revolution populations (Neolithic, Chalcolithic, and Roman/Byzantine) and the post-industrial populations (the recent population) that exhibit mainly an increase in chin projection, a narrowing of the coronoid, and a lengthening of the condyle (fig. 6).

Fig.  6 – Principal component analysis of the hemimandibular shape by population (using a set of 52 landmarks). Purple: Natufian; green: PPNC; blue: Chalcolithic; orange: Roman/Byzantine; brown: recent population. A: The first two principal components (PCs) explain 31.7% of the variance; B: The first and third PCs explain 30.8% of the variance (figure modified from Pokhojaev et al. 2019).

Fig.  6 – Principal component analysis of the hemimandibular shape by population (using a set of 52 landmarks). Purple: Natufian; green: PPNC; blue: Chalcolithic; orange: Roman/Byzantine; brown: recent population. A: The first two principal components (PCs) explain 31.7% of the variance; B: The first and third PCs explain 30.8% of the variance (figure modified from Pokhojaev et al. 2019).

30Although the impact of dietary changes on mandibular morphology was recognized in previous studies (Pinhasi et al. 2008; Cramon-Taubadel 2011; Galland et al. 2016; Katz et al. 2017), our study (Pokhojaev et al. 2019) is the only one that meticulously followed these changes in a series of Levantine populations. These changes in mandibular shape can be explained by the masticatory-functional hypothesis (Proffit et al. 2014; Sella Tunis et al. 2018); therefore, they can be reliably used as indicators of changes in dietary habits.

Summary and conclusions

31There is no doubt that Holocene populations experienced, in a relatively short time period, dramatic changes in almost all behavioral and cultural aspects. The transition from the Stone Age to the Apollo 13 landing on the moon took less than 12,000 years. It is still debated what triggered this dramatic change, but once humans abandoned their old life style of hunting and gathering, which was practiced for more than 2 my, and they adopted a food-producing behavior, the point of no return was crossed, and their lives changed forever. The abundance of well-dated skeletal remains from all periods, the relatively homogeneous (biologically and culturally) nature of the populations having their roots in the Natufians, the small geographical areas, and the similar environmental conditions, make the prehistoric populations of Israel ideal for testing the impact technological innovations had on human biology. Nonetheless, reconstructing trends overtime in body physique, life style, and health, and their possible causes must take into consideration, even when on a small scale, population dynamics (e.g., migration, population mixture). For example, we recently generated a genome-wide ancient DNA study from 22 individuals from Peqi’in Cave (Harney et al. 2018), a Chalcolithic site in northern Israel. Interestingly, we discovered that people from this site were part of a homogeneous population that can be modeled as deriving ~57% of their ancestry from groups related to individuals from the local Levant Neolithic, ~17% from groups related to individuals from the Iran Chalcolithic, and ~26% from groups related to Anatolian Neolithic individuals. It is therefore possible that population movements not only propelled cultural changes in the deep past, but also affected the biological characteristics of the local population. Our study of the skeleton and mandible of Levantine Holocene populations clearly shows a reduction in their size and general robusticity over time. With the changes in lifestyle, diet, and food preparation techniques, there was probably no longer a need to maintain a massive masticatory and locomotion system, which requires significant energy (De Paula and Rosen 2013). The dietary and physical changes experienced by Levantine Holocene populations had their toll, e.g., an increased incidence of dental anomalies and dental diseases with time, an increased incidence of bone fractures (mainly hip fractures), low back pain, obesity, and many other physical and health hazards. 

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Table des illustrations

Titre Table 1 Skeletal remains examined in the study, by population.
URL http://0-journals-openedition-org.catalogue.libraries.london.ac.uk/paleorient/docannexe/image/907/img-1.jpg
Fichier image/jpeg, 74k
Titre Fig. 1 – Ear infection diagnosis based on bone remodeling of the promontory surface (after Floreanova et al. 2020, modified bracket. A, B: No remodeling is evident; the surface is smooth when directly observed via a videoscope (PENTAX Medical VNL9-CP; A) and a light microscope (SMZ1270i, Nikon equipped with a digital camera DS-Fi3, Nikon; B); C, D: Isolated, bony overgrowths with clear margins appearing as a narrow bony crest (1) or a bony spicule (2) observed via videoscope (C) and a light microscope (D); E, F: Interruption of the integrity of the promontory bony surface observed via videoscope (E) and a light microscope (F).
URL http://0-journals-openedition-org.catalogue.libraries.london.ac.uk/paleorient/docannexe/image/907/img-2.jpg
Fichier image/jpeg, 272k
Titre Fig. 2 – Prevalence of ear infections in various populations (adults only) during the terminal Pleistocene-Holocene Levant.
URL http://0-journals-openedition-org.catalogue.libraries.london.ac.uk/paleorient/docannexe/image/907/img-3.jpg
Fichier image/jpeg, 47k
Titre Fig. 3 – Changes in the relative subperiosteal cortical bone area ([cortical area/total cross-sectional area at midshaft] ×100) in southern Levant populations during the Holocene.
URL http://0-journals-openedition-org.catalogue.libraries.london.ac.uk/paleorient/docannexe/image/907/img-4.jpg
Fichier image/jpeg, 46k
Titre Fig.  4 – Relative medullary cavity breadth measured at the femoral mid-shaft cross section in samples from various periods during the terminal Pleistocene-Holocene Levant.
URL http://0-journals-openedition-org.catalogue.libraries.london.ac.uk/paleorient/docannexe/image/907/img-5.jpg
Fichier image/jpeg, 48k
Titre Fig.  5 – Patterns of mandibular shape transformation from Natufian hunter-gatherers to the present time. The magnitude of the shape transformation between the warped surfaces of the mean shape is presented via a color map (the lowest value is in blue and the highest is in red). Note that the coronoid process shape and the mandibular angle regions exhibit the highest change over time.
URL http://0-journals-openedition-org.catalogue.libraries.london.ac.uk/paleorient/docannexe/image/907/img-6.jpg
Fichier image/jpeg, 113k
Titre Fig.  6 – Principal component analysis of the hemimandibular shape by population (using a set of 52 landmarks). Purple: Natufian; green: PPNC; blue: Chalcolithic; orange: Roman/Byzantine; brown: recent population. A: The first two principal components (PCs) explain 31.7% of the variance; B: The first and third PCs explain 30.8% of the variance (figure modified from Pokhojaev et al. 2019).
URL http://0-journals-openedition-org.catalogue.libraries.london.ac.uk/paleorient/docannexe/image/907/img-7.jpg
Fichier image/jpeg, 283k
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Israel Hershkovitz, Rachel Sarig et Hila May, « Trends in Ancient Populations’ Osteobiography during the Holocene: the Levantine Perspective »Paléorient, 47-1 | 2021, 71-82.

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Israel Hershkovitz, Rachel Sarig et Hila May, « Trends in Ancient Populations’ Osteobiography during the Holocene: the Levantine Perspective »Paléorient [En ligne], 47-1 | 2021, mis en ligne le 01 décembre 2021, consulté le 05 novembre 2024. URL : http://0-journals-openedition-org.catalogue.libraries.london.ac.uk/paleorient/907 ; DOI : https://0-doi-org.catalogue.libraries.london.ac.uk/10.4000/paleorient.907

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Auteurs

Israel Hershkovitz

Department of Anatomy and Anthropology, Sackler Faculty of Medicine, Shmunis Family anthropology Institute, The Dan David Center for Human Evolution and Biohistory Research, Tel Aviv University – Israel

Rachel Sarig

Department of Oral Biology, The Maurice and Gabriela Goldschleger School of Dental Medicine, Sackler Faculty of Medicine, Shmunis Family anthropology Institute, The Dan David Center for Human Evolution and Biohistory Research, Tel Aviv University – Israel

Hila May

Department of Anatomy and Anthropology, Sackler Faculty of Medicine, Shmunis Family anthropology Institute, The Dan David Center for Human Evolution and Biohistory Research, Tel Aviv University – Israel

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