Earliest evidence for caries and exploitation of starchy plant foods in Pleistocene hunter-gatherers from Morocco

Abstract

Dental caries is an infectious disease that causes tooth decay. The high prevalence of dental caries in recent humans is attributed to more frequent consumption of plant foods rich in fermentable carbohydrates in food-producing societies. The transition from hunting and gathering to food production is associated with a change in the composition of the oral microbiota and broadly coincides with the estimated timing of a demographic expansion in Streptococcus mutans, a causative agent of human dental caries. Here we present evidence linking a high prevalence of caries to reliance on highly cariogenic wild plant foods in Pleistocene hunter-gatherers from North Africa, predating other high caries populations and the first signs of food production by several thousand years. Archaeological deposits at Grotte des Pigeons in Morocco document extensive evidence for human occupation during the Middle Stone Age and Later Stone Age (Iberomaurusian), and incorporate numerous human burials representing the earliest known cemetery in the Maghreb. Macrobotanical remains from occupational deposits dated between 15,000 and 13,700 cal B.P. provide evidence for systematic harvesting and processing of edible wild plants, including acorns and pine nuts. Analysis of oral pathology reveals an exceptionally high prevalence of caries (51.2% of teeth in adult dentitions), comparable to modern industrialized populations with a diet high in refined sugars and processed cereals. We infer that increased reliance on wild plants rich in fermentable carbohydrates and changes in food processing caused an early shift toward a disease-associated oral microbiota in this population.

Dental caries involves progressive dissolution of the mineral component of dental tissues by organic acids produced during fermentation of food debris by bacteria in dental plaque. The development of carious lesions requires infection by disease-associated oral bacteria, as well as a suitable oral environment for their survival and proliferation (1). Examination of fossil and archeological human dentitions provides direct evidence for the prevalence of dental disease in the past. High caries rates are associated with sedentary food-producing societies that rely on foods rich in fermentable carbohydrates as staples (2⇓–4). Frequencies of carious lesions in archaeological populations range from 2.2–48.1% of teeth for agricultural populations, but only 0–14.3% for hunter-gatherers (4). Analysis of bacterial DNA from ancient calculus deposits provides direct evidence of the disease environment, with recent research pointing toward a shift toward a more disease-associated oral microbiota following the onset of food production (5).

Grotte des Pigeons at Taforalt (Fig. 1) was a key location for ritual and economic activities during the Middle Stone Age and Later Stone Age (Iberomaurusian) (6, 7). Archaeological deposits document a marked intensification in the use of the cave during the Later Stone Age, with the rapid accumulation of thick ashy midden layers, known as the Grey Series, between 15,000 and 12,600 cal B.P. (8). The extreme dryness of the deposits has favored the preservation of organic material, including animal and human bone and charred plant remains. The Grey Series deposits incorporate numerous closely spaced burials of adults, children, and infants in a spatially demarcated area toward the rear of the cave (7, 9, 10). The large number of burials and exceptional preservation of charred macrobotanical remains in contemporaneous occupational deposits provides an opportunity to evaluate both oral health and the role of wild plants in the diet of a preagricultural population.