The contribution of subsistence to global human cranial variation

Abstract

Diet-related cranial variation in modern humans is well documented on a regional scale, with ample examples of cranial changes related to the agricultural transition. However, the influence of subsistence strategy on global cranial variation is less clear, having been confirmed only for the mandible, and dietary effects beyond agriculture are often neglected. Here we identify global patterns of subsistence-related human cranial shape variation. We analysed a worldwide sample of 15 populations (n = 255) with known subsistence strategies using 3-D landmark datasets designed to capture the shape of different units of the cranium. Results show significant correlations between global cranial shape and diet, especially for temporalis muscle shape and general cranial shape. Importantly, the differences between populations with either a plant- or an animal-based diet are more pronounced than those between agriculturalists and hunter-gatherers, suggesting that the influence of diet as driver of cranial variation is not limited to Holocene transitions to agricultural subsistence. Dental arch shape did not correlate with subsistence pattern, possibly indicating the high plasticity of this region of the face in relation to age, disease and individual use of the dentition. Our results highlight the importance of subsistence strategy as one of the factors underlying the evolution of human geographic cranial variation.

Introduction

Modern human geographic cranial diversity is well documented (Howells, 1973, Lahr, 1996), but the mechanisms underlying it remain unclear (Lieberman, 2008). Although masticatory stress is generally accepted as a major driver of regional human cranial variation (Carlson and Van Gerven, 1977, Hylander, 1977a, Paschetta et al., 2010), the influence of subsistence on global cranial morphological variation is a matter of debate (Lieberman, 2011, von Cramon-Taubadel, 2011a). Regional studies comparing agriculturalists with non-agriculturalists have found that this dietary difference affects the shape, size and positioning of the masticatory muscle attachments, mandible, zygomatic bone, neurocranium and the dental arch (Carlson and Van Gerven, 1977, Hylander, 1977a, Hylander, 1977b, Varrela, 1992, Larsen, 1995, González-José et al., 2005, Sardi et al., 2006, Pinhasi et al., 2008, Paschetta et al., 2010). On a global scale, however, such diet-related variation has only been confirmed for the mandible (von Cramon-Taubadel, 2011a). This is unexpected, as modern humans inhabit many different ecosystems where the types of food available, and consequently the strains posed on the cranium during mastication, can differ significantly. The possible influence of subsistence strategy on the pattern of global cranial variation therefore remains unclear.

Studies investigating the effects of diet on modern human cranial variation have mainly focused on differences between agriculturalists and hunter-gatherers. Nevertheless, dietary adaptations have been documented throughout the hominin fossil record. Diet is considered an important driver of cranial variation among early hominins (e.g., Teaford and Ungar, 2000), while the inclusion of meat in the diet likely marked an important step in human evolution (e.g., Stanford and Bunn, 2001). Among Pleistocene Homo, Neanderthals are often considered to have relied heavily on meat from medium and large size terrestrial mammals on the basis of both isotopic and zooarchaeological data (e.g., Hockett and Haws, 2005, Bocherens, 2009, Richards and Trinkaus, 2009; but see Henry et al., 2010), while modern humans might have had a more flexible subsistence strategy (e.g., Stiner, 2001, Hockett and Haws, 2005, Richards and Trinkaus, 2009). Food types have therefore been important throughout human evolution both in terms of the strain they posed on the cranium as well as the nutritional value they added. In order to understand possible effects of diet on the evolution of modern human cranial diversity it is thus important to study the relationship between cranial shape and detailed differences in diets, testing not only for effects of agriculture, but also for effects of animal- versus plant-based food intake.

Here we study a sample of 15 worldwide populations of Homo sapiens with different subsistence strategies. In addition to testing for correlations between diet and shape of particular cranial regions (upper dental arch, masseter and temporalis muscle, general cranium), we discuss overlap in effects of diet, climate and population history on global human cranial variation as well as the functionality of observed diet-related cranial variation.

Central to the hypothesis that subsistence strategy affects global human cranial shape is the notion that differences in subsistence patterns result in different diets and therewith in different food types consumed. Diets including tougher and harder food items are generally thought to require more masticatory effort to break them down compared with tender and soft agricultural products that have a high component of processed grains (Carlson, 1976, Carlson and Van Gerven, 1979, Kohyama et al., 2004). With a more mechanically demanding diet, cranial adaptations are expected that enhance the production and dissipation of high bite forces (Hylander, 1972). The size of the masticatory muscles and the three-dimensional arrangement of those muscles are particularly relevant in this respect (e.g., Wroe et al., 2010). Proposed adaptations for the generation of high bite forces, needed for processing more mechanically resistant food items, include a more anterior positioning of the masticatory muscles (temporalis and masseter) and posterior position of the dental arch to enhance the mechanical advantage of the chewing muscles (Hylander, 1977a, Lieberman, 2011), as well as overall enlarged masticatory muscles, traceable on the cranium by enlarged attachment sites on the zygomatic arch (masseter) and lateral side of the cranium (temporalis), and a larger cross-section of the infratemporal fossa (temporalis) (Weijs and Hillen, 1984, Weijs and Hillen, 1986, Demes and Creel, 1988). Dissipation of masticatory stress and reduction of bending moments occurs via enlarged vertical facial dimensions (Hylander, 1977a), flaring of the cheekbones and thicker alveolar processes (Lieberman, 2011).

Changes in diet are also shown to relate to changes in cranial size (Sardi et al., 2006, Perez et al., 2011), where less demanding diets correlate with smaller sized crania. In Nubian populations with a soft, agricultural diet, the size of the face decreased relative to total cranium size (Carlson and Van Gerven, 1977). Perez et al. (2011) found that in South American populations, the effect of diet on size is larger than the effect of diet on facial and neurocranial shape variation. Size differences are thus to be expected between groups with different subsistence patterns.

Importantly, not only adaptation, but also cranial plasticity might play an important role in diet-related shape variation. Studies on non-human mammals have indicated cranial shape changes induced by differences in food types during rearing (e.g., Lieberman et al., 2004, Menegaz et al., 2010, Ravosa et al., 2010). Human cranial regions under masticatory stress (zygotemporal and palatomaxilla) show higher variability than regions less affected by mastication (basicranium, upper face, vault), which might indicate higher plasticity in the masticatory regions of the cranium (von Cramon-Taubadel, 2009a). Nevertheless, the masticatory regions have been found to be equally reliable for inferring population history patterns (von Cramon-Taubadel, 2009a). Although environmental plasticity and adaptation to diet can be difficult to disentangle (O'Higgins et al., 2006), it has been shown in humans that typical diet related morphology of the mandible can already be traced in children before they start on their adult foods (Fukase and Suwa, 2008) and that population differentiation in craniofacial shape is already detectable at an early ontogenetic stage (e.g., Viðarsdóttir et al., 2002, Viðarsdóttir and Cobb, 2004, Gonzalez et al., 2010).

Beyond such considerations relating cranial shape to masticatory behaviour, there is clear evidence that population history has a significant influence on global patterning of cranial morphology (e.g., Relethford, 1994, Roseman, 2004, Roseman and Weaver, 2004, Harvati and Weaver, 2006a, Harvati and Weaver, 2006b, Hubbe et al., 2009, Smith, 2009, Smith, 2011, von Cramon-Taubadel, 2011b). Regions of the human cranium have been found to preserve the signal of population history to varying extents, also depending on how the cranium is divided into separately studied compartments (von Cramon-Taubadel, 2014). Overall cranial shape reflects population history, and specifically the regions of the basicranium and the temporal bone shape show a very clear correlation with neutral genetic data (Harvati and Weaver, 2006a, Harvati and Weaver, 2006b, Smith, 2009, von Cramon-Taubadel, 2009a, von Cramon-Taubadel, 2009b). The vault shows varying results, depending on the populations studied and the landmarks included, being either strongly (Harvati and Weaver, 2006a, Harvati and Weaver, 2006b, von Cramon-Taubadel, 2009b) or weakly (Smith, 2009) related to neutral genetic distances. The mandible, maxilla, zygomatic bone and occipital bone are generally considered to perform less well as indicators of past population history (Smith, 2009, von Cramon-Taubadel, 2009b, von Cramon-Taubadel, 2014), which might be related to the fact that these parts of the cranium are involved in shaping overall facial morphology and/or relate to muscle attachment sites (masseter, temporalis and nuchal muscles) (von Cramon-Taubadel, 2014). The overall face and especially the region around the nasal opening shows stronger influences from climate (Roseman and Weaver, 2004, Harvati and Weaver, 2006a, Harvati and Weaver, 2006b, Hubbe et al., 2009, Noback et al., 2011). Although neutral evolution thus plays an important role in human variation (Relethford, 1994), part of craniofacial variation remains unexplained (Roseman and Weaver, 2004, Smith, 2009, von Cramon-Taubadel, 2009b, von Cramon-Taubadel, 2014). Furthermore, observed population differences in cranial shape and size are too large to be caused by genetic drift alone (Perez and Monteiro, 2009, Perez et al., 2011).

In addition to population history, climate also plays an important role in cranial diversity. A relationship has been found between climatic factors and morphology of the face in general (Roseman, 2004, Harvati and Weaver, 2006a, Hubbe et al., 2009), the mid-face (Evteev et al., 2014), nasal aperture and cavity (e.g., Wolpoff, 1968, Noback et al., 2011), sinus volume (Shea, 1977; but see Rae et al., 2003, Butaric et al., 2010) and cranial size (Beals et al., 1984, Harvati and Weaver, 2006a), suggesting adaptive selection. This selection signal is strongly influenced by populations from extremely cold regions (Roseman, 2004, Harvati and Weaver, 2006a, Harvati and Weaver, 2006b, Hubbe et al., 2009). The latter observation is important, as Arctic populations are also linked with extreme dietary adaptations (Hylander, 1972). Global studies specifically focussed on effects of climate versus population history on cranial variation have generally not included factors of subsistence differences (e.g., Harvati and Weaver, 2006a, von Cramon-Taubadel, 2009b, Betti et al., 2010).

In order to detect diet-related cranial variation it is essential to correct for the effects of population history/genetic drift to prevent overestimating the effects of natural selection (Betti et al., 2010). As there is a very strong correlation between genetic and geographic distances (Manica et al., 2005, Ramachandran et al., 2005, Romero et al., 2008), geographic distance (when measured along land migration routes) can be used as a proxy for population history (Lawson Handley et al., 2007, Hubbe et al., 2009, Betti et al., 2010).

Corrections for effects of climate are also needed in the detection of diet-related cranial shape (e.g., von Cramon-Taubadel, 2011a). Diet, however, is expected to be highly dependent on climate. With increased latitudes, plant eating declines in hunter-gatherer populations (Cordain et al., 2000). The total amount of fishing, on the contrary, increases with higher latitudes (Cordain et al., 2000). This increase in animal foods towards the higher latitudes is especially problematic as climatic adaptations of the cranium are also expected for colder regions (e.g., Davies, 1932, Beals et al., 1984, Roseman, 2004, Harvati and Weaver, 2006a, Hubbe et al., 2009). Hylander (1977a) tackled the climate versus diet debate by making clear predictions about expected diet-related changes. This approach, combined with careful interpretation of the effects of climate and population history in correlation analyses, is necessary to study global diet-related shape variation.

We focus on three hypotheses: (1) there is a global effect of diet on cranial shape and size, (2) the observed diet-related cranial variation will be consistent with regional studies on masticatory adaptations, and (3) climate and population history influence the relationship between diet and cranial shape.

Regarding the first hypothesis, we predict (1a) significant correlations between measures of diet and datasets representing global variation in cranial shape and size. However, we also expect that the different regions of the cranium will be differentially affected by diet. The strains that are generated during chewing or paramasticatory behaviour are highest at the tooth row, the alveolar process, the attachment sites of the masticatory muscles and the palate, and decrease away with increased distance from the tooth row (Lieberman, 2011). Studies on non-human primates showed increased effects of high masticatory strains in the lower face, especially the occlusal plane. The middle and upper face were less affected (Hylander et al., 1991, Hylander et al., 1992). Finite element analyses on the human cranium showed highest strain directly above the point of load application (the alveolar/dental arcade) (Gross et al., 2001, Witzel and Preuschoft, 2002). We therefore predict that (1b) the strongest correlation between diet and shape will be found in the dental arch, (1c) the second strongest diet–shape correlation will be found in the temporalis and masseter muscle attachment sites (as well as the zygomatic bone), and (1d) that the lowest diet–shape correlation will be found in the general cranial shape. Regarding diet–size correlations, we expect (1e) to see strongest correlations between diet and size of the masticatory muscle attachments, as one important way of increasing masticatory power is by increasing muscle size (e.g., Hylander, 2006), as well as (1f) correlations between diet and size of the upper dental arch, as one way of resisting high masticatory loads is an increase in alveolar size (e.g., Lieberman, 2011).

Regarding the second hypothesis, the shape changes related to subsistence, we expect to see (2a) cranial morphology that enhances the generation and dissipation of high bite forces in populations with subsistence patterns (hunting, fishing, gathering) that include masticatorily demanding food items. We expect that diet-related shape variation on a global scale will follow trends observed in regional studies: (2b) the masseter muscle will show a more anterior positioning and a relatively larger attachment site; (2c) the temporalis muscle will show a more anterior positioning and will be thicker and larger, resulting in a larger cross-section of the infratemporal fossa and a higher and/or longer attachment site, (2d) the upper dental arch will show a relatively more posterior positioning as well as a more robust alveolar process. We furthermore predict (2e) that the relative positioning of the muscles and dentition is important in the context of dietary adaptation.

Last, considering the closely linked geographic patterns of population history, climate and subsistence patterns, we predict (3a) that correcting for climate and geographic distance will severely lower the correlation between cranial shape and diet. We also expect (3b) to see overlap between the explanatory variables in the percentage of cranial variation they explain.

In this study, we will first investigate possible correlations of cranial shape with diet using Mantel tests. We then correct for the effects of climate and population history by partial Mantel tests. We visualize the global diet-related functional shape changes of the human cranium using partial least squares analysis and surface warping. We discuss the possible overlap of dietary shape effects and those of population history and climate. Finally, we discuss implications of our results for understanding pre-Holocene human evolution.