Shallow-water habitats as sources of fallback foods for hominins

Underground storage organs (USOs) have been proposed as critical fallback foods for early hominins in savanna, but there has been little discussion as to which habitats would have been important sources of USOs. USOs consumed by hominins could have included both underwater and underground storage organs, i.e., from both aquatic and terrestrial habitats. Shallow aquatic habitats tend to offer high plant growth rates, high USO densities, and relatively continuous USO availability throughout the year. Baboons in the Okavango delta use aquatic USOs as a fallback food, and aquatic or semiaquatic USOs support high-density human populations in various parts of the world. As expected given fossilization requisites, the African early- to mid-Pleistocene shows an association of Homo and Paranthropus fossils with shallow-water and flooded habitats where high densities of plant-bearing USOs are likely to have occurred. Given that early hominins in the tropics lived in relatively dry habitats, while others occupied temperate latitudes, ripe, fleshy fruits of the type preferred by African apes would not normally have been available year round. We therefore suggest that water-associated USOs were likely to have been key fallback foods, and that dry-season access to aquatic habitats would have been an important predictor of hominin home range quality. This study differs from traditional savanna chimpanzee models of hominin origins by proposing that access to aquatic habitats was a necessary condition for adaptation to savanna habitats. It also raises the possibility that harvesting efficiency in shallow water promoted adaptations for habitual bipedality in early hominins. Am J Phys Anthropol 140:630–642, 2009. © 2009 Wiley-Liss, Inc.     

Adaptation to hard-object feeding in sea otters and hominins

The large, bunodont postcanine teeth in living sea otters (Enhydra lutris) have been likened to those of certain fossil hominins, particularly the ’robust’ australopiths (genus Paranthropus). We examine this evolutionary convergence by conducting fracture experiments on extracted molar teeth of sea otters and modern humans (Homo sapiens) to determine how load-bearing capacity relates to tooth morphology and enamel material properties. In situ optical microscopy and x-ray imaging during simulated occlusal loading reveal the nature of the fracture patterns. Explicit fracture relations are used to analyze the data and to extrapolate the results from humans to earlier hominins. It is shown that the molar teeth of sea otters have considerably thinner enamel than those of humans, making sea otter molars more susceptible to certain kinds of fractures. At the same time, the base diameter of sea otter first molars is larger, diminishing the fracture susceptibility in a compensatory manner. We also conduct nanoindentation tests to map out elastic modulus and hardness of sea otter and human molars through a section thickness, and microindentation tests to measure toughness. We find that while sea otter enamel is just as stiff elastically as human enamel, it is a little softer and tougher. The role of these material factors in the capacity of dentition to resist fracture and deformation is considered. From such comparisons, we argue that early hominin species like Paranthropus most likely consumed hard food objects with substantially higher biting forces than those exerted by modern humans.     

Variation in enamel thickness within the genus Homo

Recent humans and their fossil relatives are classified as having thick molar enamel, one of very few dental traits that distinguish hominins from living African apes. However, little is known about enamel thickness in the earliest members of the genus Homo, and recent studies of later Homo report considerable intra- and inter-specific variation. In order to assess taxonomic, geographic, and temporal trends in enamel thickness, we applied micro-computed tomographic imaging to 150 fossil Homo teeth spanning two million years. Early Homo postcanine teeth from Africa and Asia show highly variable average and relative enamel thickness (AET and RET) values. Three molars from South Africa exceed Homo AET and RET ranges, resembling the hyper thick Paranthropus condition. Most later Homo groups (archaic European and north African Homo, and fossil and recent Homo sapiens) possess absolutely and relatively thick enamel across the entire dentition. In contrast, Neanderthals show relatively thin enamel in their incisors, canines, premolars, and molars, although incisor AET values are similar to H. sapiens. Comparisons of recent and fossil H. sapiens reveal that dental size reduction has led to a disproportionate decrease in coronal dentine compared with enamel (although both are reduced), leading to relatively thicker enamel in recent humans. General characterizations of hominins as having ‘thick enamel’ thus oversimplify a surprisingly variable craniodental trait with limited taxonomic utility within a genus. Moreover, estimates of dental attrition rates employed in paleodemographic reconstruction may be biased when this variation is not considered. Additional research is necessary to reconstruct hominin dietary ecology since thick enamel is not a prerequisite for hard-object feeding, and it is present in most later Homo species despite advances in technology and food processing.     

Abrasive, silica phytoliths and the evolution of thick molar enamel in primates, with implications for the diet of Paranthropus boisei

Background

Primates—including fossil species of apes and hominins—show variation in their degree of molar enamel thickness, a trait long thought to reflect a diet of hard or tough foods. The early hominins demonstrated molar enamel thickness of moderate to extreme degrees, which suggested to most researchers that they ate hard foods obtained on or near the ground, such as nuts, seeds, tubers, and roots. We propose an alternative hypothesis—that the amount of phytoliths in foods correlates with the evolution of thick molar enamel in primates, although this effect is constrained by a species'' degree of folivory.

Methodology/Principal Findings

From a combination of dietary data and evidence for the levels of phytoliths in plant families in the literature, we calculated the percentage of plant foods rich in phytoliths in the diets of twelve extant primates with wide variation in their molar enamel thickness. Additional dietary data from the literature provided the percentage of each primate''s diet made up of plants and of leaves. A statistical analysis of these variables showed that the amount of abrasive silica phytoliths in the diets of our sample primates correlated positively with the thickness of their molar enamel, constrained by the amount of leaves in their diet (R² = 0.875; p<.0006).

Conclusions/Significance

The need to resist abrasion from phytoliths appears to be a key selective force behind the evolution of thick molar enamel in primates. The extreme molar enamel thickness of the teeth of the East African hominin Paranthropus boisei, long thought to suggest a diet comprising predominantly hard objects, instead appears to indicate a diet with plants high in abrasive silica phytoliths.     

The role of character displacement in the molarization of hominin mandibular premolars

Closely related species are likely to experience resource competition in areas where their ranges overlap. Fossil evidence suggests that hominins in East Africa c. 2–1.5 million years ago may have lived synchronically and sympatrically, and that competition may have contributed to the different tooth sizes observed in Homo and Paranthropus. To assess the likelihood that these taxa overlapped, we applied a character displacement model to the postcanine tooth size of fossil hominins and validated this model in populations of living primates. Mandibular fourth premolar (P₄) crown size was measured from fossil taxa and from living primate species where dietary overlap is established. Dimensions of the P₄ crown were fitted to a character matrix and described as the response variables of a generalized linear model that took taxon and location as input variables. The model recovered significant divergence in samples of closely related, living primates. When applied to fossil hominins the same model detected strong indications of character displacement between early Homo and Paranthropus (P = 0.002) on the basis of their P₄ crown size. Our study is an example of how ecologically informed morphologies measured in appropriate extant referents can provide a comparative context for assessing community and ecological evolution in the fossil record.     

Early and Middle Pleistocene hominins from Atapuerca (Spain) show differences in dental developmental patterns

The Bayesian statistical approach considers teeth as forming a developmental module, as opposed to a tooth-by-tooth analysis. This approach has been employed to analyze Upper Pleistocene hominins, including Neandertals and some anatomically modern humans, but never earlier populations. Here, we show its application on five hominins from the TD6.2 level of the Gran Dolina site (Homo antecessor, Early Pleistocene) and the Sima de los Huesos site (Middle Pleistocene) of the Sierra de Atapuerca (Burgos, northern Spain). Our results show an advanced development of the third molars in both populations with respect to modern Homo sapiens. In addition, the Sima de los Huesos hominins differ from H. sapiens and H. antecessor in the relatively advanced development of their second molar. The relative mineralization of I1/M1 in H. antecessor appears to be similar to that of modern humans, as opposed to that of Neandertals, which appear to be unique. These observations, combined with reduced enamel formation times and the advanced development of the third molars, appear to indicate a shorter ontogenetic period in the hominins from Gran Dolina and Sima de los Huesos in comparison to modern human average.     

Bite force and occlusal stress production in hominin evolution

Maximum bite force affects craniofacial morphology and an organism's ability to break down foods with different material properties. Humans are generally believed to produce low bite forces and spend less time chewing compared with other apes because advances in mechanical and thermal food processing techniques alter food material properties in such a way as to reduce overall masticatory effort. However, when hominins began regularly consuming mechanically processed or cooked diets is not known. Here, we apply a model for estimating maximum bite forces and stresses at the second molar in modern human, nonhuman primate, and hominin skulls that incorporates skeletal data along with species‐specific estimates of jaw muscle architecture. The model, which reliably estimates bite forces, shows a significant relationship between second molar bite force and second molar area across species but does not confirm our hypothesis of isometry. Specimens in the genus Homo fall below the regression line describing the relationship between bite force and molar area for nonhuman anthropoids and australopiths. These results suggest that Homo species generate maximum bite forces below those predicted based on scaling among australopiths and nonhuman primates. Because this decline occurred before evidence for cooking, we hypothesize that selection for lower bite force production was likely made possible by an increased reliance on nonthermal food processing. However, given substantial variability among in vivo bite force magnitudes measured in humans, environmental effects, especially variations in food mechanical properties, may also be a factor. The results also suggest that australopiths had ape‐like bite force capabilities. Am J Phys Anthropol 151:544–557, 2013. © 2013 Wiley Periodicals, Inc.     

Variations in the mechanical properties of Alouatta palliata molar enamel

Teeth have provided insights into many topics including primate diet, paleobiology, and evolution, due to the fact that they are largely composed of inorganic materials and may remain intact long after an animal is deceased. Previous studies have reported that the mechanical properties, chemistry, and microstructure of human enamel vary with location. This study uses nanoindentation to map out the mechanical properties of Alouatta palliata molar enamel on an axial cross‐section of an unworn permanent third molar, a worn permanent first molar, and a worn deciduous first molar. Variations were then correlated with changes in microstructure and chemistry using scanning electron microscopy and electron microprobe techniques. The hardness and Young's modulus varied with location throughout the cross‐sections from the occlusal surface to the dentin‐enamel junction (DEJ), from the buccal to lingual sides, and also from one tooth to another. These changes in mechanical properties correlated with changes in the organic content of the tooth, which was shown to increase from ～6% near the occlusal surface to ～20% just before the DEJ. Compared to human enamel, the Alouatta enamel showed similar microstructures, chemical constituents, and magnitudes of mechanical properties, but showed less variation in hardness and Young's modulus, despite the very different diet of this species. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

Stretching the time span of hominin evolution at Kromdraai (Gauteng,South Africa): Recent discoveries

The Plio-Pleistocene locality of Kromdraai B has yielded the type specimen of Paranthropus robustus, as well as 27 additional fossil hominin specimens. In a number of both cranial and dental features, the states shown by the Kromdraai Paranthropus are more conservative when compared to the more derived conditions displayed by both South African conspecifics and the post-2.3 Ma eastern African Paranthropus boisei. Since 2014, we excavated the earliest known infilling of the Kromdraai cave system in a previously unexplored area. This new locality provided as yet 2200 identifiable macrovertebrate fossils, including 22 hominins, all tied in the earliest part of the stratigraphic sequence, representing three distinct depositional periods. Since we report here, for the first time, the occurrence of fossil hominins in Members 1 and 2, our discoveries stretch the time span of hominin evolution at Kromdraai and contribute to a better understanding of the origin of Paranthropus in southern Africa.     

First Early Hominin from Central Africa (Ishango,Democratic Republic of Congo)

Despite uncontested evidence for fossils belonging to the early hominin genus Australopithecus in East Africa from at least 4.2 million years ago (Ma), and from Chad by 3.5 Ma, thus far there has been no convincing evidence of Australopithecus, Paranthropus or early Homo from the western (Albertine) branch of the Rift Valley. Here we report the discovery of an isolated upper molar (#Ish25) from the Western Rift Valley site of Ishango in Central Africa in a derived context, overlying beds dated to between ca. 2.6 to 2.0 Ma. We used µCT imaging to compare its external and internal macro-morphology to upper molars of australopiths, and fossil and recent Homo. We show that the size and shape of the enamel-dentine junction (EDJ) surface discriminate between Plio-Pleistocene and post-Lower Pleistocene hominins, and that the Ishango molar clusters with australopiths and early Homo from East and southern Africa. A reassessment of the archaeological context of the specimen is consistent with the morphological evidence and suggest that early hominins were occupying this region by at least 2 Ma.     

Experimental perspective on fallback foods and dietary adaptations in early hominins

The robust jaws and large, thick-enameled molars of the Plio–Pleistocene hominins Australopithecus and Paranthropus have long been interpreted as adaptations for hard-object feeding. Recent studies of dental microwear indicate that only Paranthropus robustus regularly ate hard items, suggesting that the dentognathic anatomy of other australopiths reflects rare, seasonal exploitation of hard fallback foods. Here, we show that hard-object feeding cannot explain the extreme morphology of Paranthropus boisei. Rather, analysis of long-term dietary plasticity in an animal model suggests year-round reliance on tough foods requiring prolonged postcanine processing in P. boisei. Increased consumption of such items may have marked the earlier transition from Ardipithecus to Australopithecus, with routine hard-object feeding in P. robustus representing a novel behaviour.     

Enamel microarchitecture of a tribosphenic molar

The tribosphenic molar is a dental apomorphy of mammals and the molar type from which all derived types originated. Its enamel coat is expected to be ancestral: a thin, evenly distributed layer of radial prismatic enamel. In the bat Myotis myotis, we reinvestigated the 3D architecture of the dental enamel using serial sectioning combined with scanning electron microscopy analyses, biometrics of enamel prisms and crystallites, and X‐ray diffraction. We found distinct heterotopies in enamel thickness (thick enamel on the convex sides of the crests, thin on the concave ones), angularity of enamel prisms, and in distribution of particular enamel types (prismatic, interprismatic, aprismatic) and demonstrated structural relations of these heterotopies to the cusp and crest organization of the tribosphenic molar. X‐ray diffraction demonstrated that the crystallites composing the enamel are actually the aggregates of much smaller primary crystallites. The differences among particular enamel types in degree of crystallite aggregation and the variation in structural microstrain of the primary crystallites (depending upon the duration and the mechanical context of mineralization) represent factors not fully understood as yet that may contribute to the complexity of enamel microarchitecture in a significant way. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

Flexible feeding on cultivated underground storage organs by rainforest-dwelling chimpanzees at Bossou, West Africa

It has been proposed that exploitation of underground storage organs (USOs) played an important role in the evolution of the genus Homo, these items serving as ‘fallback foods’ during periods of low food availability. The use of USOs as food by wild chimpanzees is infrequent and seen mostly in populations inhabiting relatively arid environments, such as the savanna. Here, we specifically test the hypothesis that chimpanzees (Pan troglodytes verus) inhabiting tropical wet forest at Bossou (Republic of Guinea, West Africa) exploit USOs as a fallback food during periods of fruit scarcity. Chimpanzees were never observed feeding on wild USOs, that is, those that were never cultivated, and rarely on other underground plant parts. However, direct observations revealed regular consumption of the USOs of cultivated cassava (Manihot esculenta), a spatially abundant and continuously available plant, although the chimpanzees did not use tools when acquiring and feeding on cassava. In agreement with the fallback foods hypothesis, our results show that chimpanzees exploited cassava USOs more frequently when both wild and cultivated fruits were scarce, and consumption patterns of cassava paralleled those of wild fallback foods. These seasonal extractive USO foraging strategies by chimpanzees can strengthen attempts to construct a clearer picture of the importance of USO feeding in hominoid evolution.     

Tooth use and the physical properties of food

For decades, natural historians and comparative anatomists have acknowledged the form/function relationship between an animal's dentition and its food. Historically, anthropologists have cited this relationship to explain adaptations observed in modern species as well as to infer the diets of extinct animals found in the fossil record. Anthropologists have described morphological differences between species that permit dietary niche partitioning which allows closely related primates to co-exist within a single ecosystem. For example, Robinson¹ postulated that the anatomical differences between Australopithecus and Paranthropus are the result of their adaptations to different diets. Jolly's² seed-eating hypothesis suggested that early hominids' morphological divergence from apes resulted from their specialized feeding on small and hard grass seeds. Early work by Kay³ suggested that Sivapithecus' thick molar enamel was an adaptation to habitually eating resistant food items such as hard nuts or seeds enclosed in tough pods.     

Functional ecology and evolution of hominoid molar enamel thickness: Pan troglodytes schweinfurthii and Pongo pygmaeus wurmbii

The divergent molar characteristics of Pan troglodytes and Pongo pygmaeus provide an instructive paradigm for examining the adaptive form-function relationship between molar enamel thickness and food hardness. Although both species exhibit a categorical preference for ripe fruit over other food objects, the thick enamel and crenulated occlusal surface of Pongo molar teeth predict a diet that is more resistant to deformation (hard) and fracture (tough) than the diet of Pan. We confirm these predictions with behavioral observations of Pan troglodytes schweinfurthii and Pongo pygmaeus wurmbii in the wild and describe the mechanical properties of foods utilized during periods when preferred foods are scarce. Such fallback foods may have exerted a selective pressure on tooth evolution, particularly molar enamel thinness, which is interpreted as a functional adaptation to seasonal folivory and a derived character trait within the hominoid clade. The thick enamel and crenulated occlusal surface of Pongo molars is interpreted as a functional adaptation to the routine consumption of relatively tough and hard foods. We discuss the implications of these interpretations for inferring the diet of hominin species, which possessed varying degrees of thick molar enamel. These data, which are among the first reported for hominoid primates, fill an important empirical void for evaluating the mechanical plausibility of putative hominin food objects.     

Dental wear,wear rate,and dental disease in the African apes

The African apes possess thinner enamel than do other hominoids, and a certain amount of dentin exposure may be advantageous in the processing of tough diets eaten by Gorilla. Dental wear (attrition plus abrasion) that erodes the enamel exposes the underlying dentin and creates additional cutting edges at the dentin‐enamel junction. Hypothetically, efficiency of food processing increases with junction formation until an optimal amount is reached, but excessive wear hinders efficient food processing and may lead to sickness, reduced fecundity, and death. Occlusal surfaces of molars and incisors in three populations each of Gorilla and Pan were videotaped and digitized. The quantity of incisal and molar occlusal dental wear and the lengths of dentin–enamel junctions were measured in 220 adult and 31 juvenile gorilla and chimpanzee skulls. Rates of dental wear were calculated in juveniles by scoring the degree of wear between adjacent molars M1 and M2. Differences were compared by principal (major) axis analysis. ANOVAs compared means of wear amounts. Pearson correlation coefficients were calculated to compare the relationship between molar wear and incidence of dental disease. Results indicate that quantities of wear are significantly greater in permanent incisors and molars and juvenile molars of gorillas compared to chimpanzees. The lengths of dentin–enamel junctions were predominantly suboptimal. Western lowland gorillas have the highest quantities of wear and the most molars with suboptimal wear. The highest rates of wear are seen in Pan paniscus and Pan t. troglodytes, and the lowest rates are found in P.t. schweinfurthii and G. g. graueri. Among gorillas, G. b. beringei have the highest rates but low amounts of wear. Coefficients between wear and dental disease were low, but significant when all teeth were combined. Gorilla teeth are durable, and wear does not lead to mechanical senescence in this sample. Am. J. Primatol. 72:481–491, 2010. © 2010 Wiley‐Liss, Inc.     

Decreased levels of Cx43 gap junctions result in ameloblast dysregulation and enamel hypoplasia in Gja1Jrt/+ mice

Coordinated differentiation of the ameloblast cell layer is essential to enamel matrix protein deposition and subsequent mineralization. It has been hypothesized that this process is governed by Cx43‐based gap junctional intercellular communication as oculodentodigital dysplasia (ODDD) patients harboring autosomal‐dominant mutations in Cx43 exhibit enamel defects typically resulting in early adulthood tooth loss. To assess the role of Cx43 in tooth development we employ a mouse model of ODDD that harbors a G60S Cx43 mutant, Gja1^Jrt/+, and appears to exhibit tooth abnormalities that mimic the human disease. We found that total Cx43 plaques at all stages of ameloblast differentiation, as well as within the supporting cell layers, were greatly reduced in Gja1^Jrt/+ incisors compared to wild‐type littermate controls. To characterize the Gja1^Jrt/+ mouse tooth phenotype, mice were sacrificed prior to tooth eruption (postnatal day 7), weaning (postnatal day 21), and adulthood (2 months postnatal). A severely disorganized Gja1^Jrt/+ mouse ameloblast layer and abnormal accumulation of amelogenin were observed at stages when the cells were active in secretion and mineralization. Differences in enamel thickness became more apparent after tooth eruption and incisor exposure to the oral cavity suggesting that enamel integrity is compromised, leading to rapid erosion. Additional analysis of incisors from mutant mice revealed that they were longer with a thicker dentin layer than their wild‐type littermates, which may reflect a mechanical stress response to the depleted enamel layer. Together, these data show that reduced levels of Cx43 gap junctions result in ameloblast dysregulation, enamel hypoplasia, and secondary tissue responses. J. Cell. Physiol. 223:601–609, 2010. © 2010 Wiley‐Liss, Inc.     

Interspecific and intraspecific relationships between tooth size and jaw size in primates

The association between mandibular robusticity, postcanine megadontia, and canine reduction in hominins has led to speculation that large and robust jaws might be required to spatially accommodate large canine and molar teeth in hominins and other primates. If so, then variations in mandibular form that are generally regarded as biomechanical adaptations to masticatory demands might instead be incidental effects of functional requirements of tooth support. While the association between large teeth and deep, robust jaws in hominins is well known, the relationship between tooth size and jaw size has not been systematically evaluated in a comparative sample of primates. We evaluate the relationships between molar tooth size, canine tooth size, and mandibular corpus and symphyseal dimensions in a sample of adult anthropoids in interspecific (n=84 species) and intraspecific (n=36 species) contexts. For intraspecific comparisons, tooth size and jaw size are correlated, but for a majority of species this is a function of sexual size dimorphism. Interspecific comparisons lend little direct support to the hypothesis that jaw breadth directly covaries with molar tooth breadth, but they do support the hypothesis that mandibular depth is associated with canine tooth size in males. The latter observation suggests that if there is a causal association between canine size and mandibular depth, it is subject to a threshold effect. In contrast, neither corpus nor symphyseal robusticity, measured as a shape index of breadth/height, are correlated with tooth size. Our results suggest that further studies of the relationship between tooth size and corpus morphology should focus on tooth root size and corpus bony architecture, and that species-specific factors should have a strong impact on such relationships.     

Hard-object feeding in sooty mangabeys (Cercocebus atys) and interpretation of early hominin feeding ecology

Morphology of the dentofacial complex of early hominins has figured prominently in the inference of their dietary adaptations. Recent theoretical analysis of craniofacial morphology of Australopithecus africanus proposes that skull form in this taxon represents adaptation to feeding on large, hard objects. A modern analog for this specific dietary specialization is provided by the West African sooty mangabey, Cercocebus atys. This species habitually feeds on the large, exceptionally hard nuts of Sacoglottis gabonensis, stereotypically crushing the seed casings using their premolars and molars. This type of behavior has been inferred for A. africanus based on mathematical stress analysis and aspects of dental wear and morphology. While postcanine megadontia, premolar enlargement and thick molar enamel characterize both A. africanus and C. atys, these features are not universally associated with durophagy among living anthropoids. Occlusal microwear analysis reveals complex microwear textures in C. atys unlike those observed in A. africanus, but more closely resembling textures observed in Paranthropus robustus. Since sooty mangabeys process hard objects in a manner similar to that proposed for A. africanus, yet do so without the craniofacial buttressing characteristic of this hominin, it follows that derived features of the australopith skull are sufficient but not necessary for the consumption of large, hard objects. The adaptive significance of australopith craniofacial morphology may instead be related to the toughness, rather than the hardness, of ingested foods.