Differences in masticatory loads impact facial bone surface remodeling in an archaeological sample of South American individuals

https://doi.org/10.1016/j.jasrep.2021.103034Get rights and content

Highlights

  • Cranial form variation among past populations has been linked to dietary differences.

  • Signs of diet in bony remains are useful in reconstructing life history.

  • Facial strains during biting were compared with bone remodeling patterns.

  • Bone remodeling data correlate with predicted masticatory strains.

  • Mechanical loading can enhance the variation in human craniofacial morphology.

Abstract

The reduction of masticatory strains is considered one of the main factors that led to a pronounced morphological variation of the facial skeleton among modern humans. Although the archaeological record has provided evidence of bone remodeling activity being linked to craniofacial variation, its link with subsistence strategies has been proposed but not yet tested. Here, we evaluate the relationship between the strains arising from masticatory loads in the facial bones and the observed surface bone remodeling activity in adults and subadults from archaeological sites from South America that exerted different masticatory loads during life. We simulated the impact of mechanical loading during I1 and M1 bite using finite element analysis in six skulls from two archaeological samples, one of hunter-gatherers from Patagonia and the other of horticulturists from Northwest Argentina. The extension and distribution of bone formation and resorption were registered by a periosteal bone surface analysis on facial bones. We found a similar spatial distribution of high and low strains between samples and across ages, but different magnitudes. In general, compression strains corresponded with resorption activity, while tension strains corresponded with formation activity. Our results show a relationship between mechanical bone response to masticatory loading and bone remodeling activity, which can ultimately shape cranial morphology. We propose that although there are differences in skull morphology among populations that are established early in ontogeny, mechanical loading produced during mastication can enhance such differences. These results then support the idea that craniofacial morphology can contribute to reconstructing the history of past populations.

Introduction

Assessing the skull shape in skeletal remains has been essential for researchers aiming to reconstruct the history of ancient populations (Neves and Hubbe, 2005, Pucciarelli et al., 2006, Sardi et al., 2006, Hubbe et al., 2015, Kuzminsky et al., 2017, von Cramon-Taubadel et al., 2017). Many of such studies rely on the assumption that skull shape is primarily controlled by neutral evolutionary factors (Weaver et al., 2007) but bone plasticity, i.e. changes in bone morphology during the lifespan of an individual, can also play a crucial role in craniofacial variation. This poses an interesting question regarding the utility of craniofacial traits in reconstructing the history of individuals in an archaeological context.

Bones grow and develop in a complex process that goes through different morphological events. Mechanical, hormonal and local signals regulate bone acquisition and maintenance, and thereby determine the interaction between bone formation and resorption through the activity of osteoblasts and osteoclasts (Enlow and Hans, 1996, Herring, 2011, Stout and Crowder, 2012). Bone remodeling activity (i.e. bone formation and resorption) underlying morphological variation can be assessed by the identification of microstructural features on bone surface. Among modern humans a similar pattern of remodeling activity in the facial skeleton has been found, consisting in mainly bone formation in the upper and the middle face, with the exception of the inferior orbital margin, the anterior surface of the zygomatic bone and the alveolar process of maxilla, where resorption activity has been found to be more relevant (Enlow and Bang, 1965, Kurihara et al., 1980, McCollum, 2008, Martinez-Maza et al., 2013, Schuh et al., 2019). However, the information is limited mostly to contemporary samples and it is not extensive to prehistoric populations. Differences found in anatomical areas that are associated to chewing and muscle insertions in individuals from South America suggest an important role of the masticatory loading in bone remodeling patterns led from the subsistence strategy (Brachetta-Aporta et al., 2019). Considering the recent occupation of the continent (17,000–14,000 cal BP; Perez et al., 2016) and the high levels of craniofacial variation, ecological factors have been proposed to be relevant in determining facial shape variation in native populations from South America (González-José et al., 2005, Perez and Monteiro, 2009, Menéndez et al., 2014). Facial bone plasticity, in particular the reduction of masticatory strains due to the adoption of softer and less abrasives diets is generally accepted as a factor leading to morphological variation among populations (e.g. Paschetta et al., 2016, Eyquem et al., 2019, Toro-Ibacache et al., 2019). Accordingly, adults from farming groups have been characterized to have small skulls and gracile facial structures –glabella, supraorbital arch, and zygo-maxillary region-, while hunter-gatherer groups have been described as having marked craniofacial robusticity, with a greater development of supraorbital and superciliary arches (González-José et al., 2005, Sardi et al., 2006, Perez and Monteiro, 2009, Menéndez et al., 2014, Paschetta et al., 2016). These morphological variations would be already established in early ages and becomes more pronounced among adults (Gonzalez et al., 2010, Gonzalez et al., 2011, Barbeito-Andrés et al., 2011). However, despite the relevance recognized for mechanical loading in determining craniofacial variation in South American populations, there is a lack of comparative studies assessing how loading relates to the remodeling activity of the bone surface, ultimately responsible of form variation.

Since mechanical loads are considered one of the most important epigenetic factors that affect bone morphology (Herring, 2011), it is compulsory to understand how surface bone remodeling data and external strains arising from the muscular impact are linked. Size, shape and rate of growing bone can be modified directly by the mechanical properties of food items. While nutrients from dietary intake are metabolically important to achieve and/or maintain the peak bone and muscle mass, how muscle and teeth strain the jaws during intraoral food processing can modify bone form (Helm and German, 1996, Herring, 2011, Weaver et al., 2016). Mechanical loading can stimulate or inhibit bone cell differentiation and activity, generating changes in the location, extension and activity rate of bone remodeling fields (Enlow and Hans, 1996, Oda et al., 1996, O'HIGGINS and JONES, 1998, Huang, 2017). Nevertheless, the impact of mechanical loading on bone shape can vary according to the magnitude of the strains, the moment that they take place and the number of stimulation cycles (Frost, 1987, Oda et al., 1996, Gosman, 2012).

Aiming to test the assumption that masticatory loads play an important role in craniofacial variation in prehistoric individuals, we assessed the relationship between bone strains derived from biting and the remodeling activity of facial bone surfaces. Since bone remodeling activity can in turn be a direct consequence of mechanical loading, we specifically evaluated whether low/high strain magnitudes occur in the areas of deposition or resorption of bone. We used as study model the crania of adults and subadults from native populations from the southernmost region of South America with dietary differences. The impact of mechanical loading in terms of strains distribution patterns was simulated by finite element (FE) methods. FE analyses are mainly used to predict deformations, strains and stress in skull as consequences of the effect of muscle and bite forces (Richmond et al., 2005, Rayfield, 2007, Toro-Ibacache and O'Higgins, 2016), as well as to predict craniofacial shape changes during growth (Libby et al., 2017, Barbeito-Andrés et al., 2020). Surface remodeling data of the individuals (i.e. bone formation and resorption activity on facial bones) was assessed by periosteal bone surface analysis, which shows the microscopic marks derived from the response of bone cells to different stimuli including mechanical loading, hormonal signals and pathologies (O’Higgins et al., 1991, Enlow and Hans, 1996, Brachetta-Aporta et al., 2018, Brachetta-Aporta et al., 2019).

Section snippets

Sample

Six skulls of subadults and adults from two archaeological samples were used for this study (Table 1). The samples are from sites of Pampa Grande (1720 ± 50 years BP; Salta province, Northwestern Argentina) and the lower valley of the Chubut river (2600–200 years BP; Chubut province, Argentine Patagonia), and are deposited in the Anthropology Division of Museo de La Plata (Buenos Aires, Argentina). Both samples represent the extremes of the craniofacial morphology variation for the southern

Strain distribution and magnitudes

Contour maps of strain were obtained for I1 and M1 biting (Fig. 3a,b). We did not simulate I1 biting of the youngest individual from Pampa Grande, in which the permanent incisors were close to erupt but still within the alveolar bone. This individual probably did not undergo mechanical loading at the front teeth.

In general, the patterns of von Mises strains are similar across ages and between samples for each simulated bite. The highest strains are found in the maxillary and zygomatic bones,

Discussion

We tested the assumption that masticatory loads play an important role in craniofacial variation in prehistoric individuals, by comparing bone strains produced during biting and bone remodeling patterns of individuals from two prehistoric populations with dietary differences. These allowed us to explore osteological responses to mechanical loading in the facial skeleton by employing state-of-the-art tools in the field of the bioarchaelogy, i.e. FE analysis and surface bone remodeling analysis (

CRediT authorship contribution statement

Natalia Brachetta-Aporta: Conceptualization, Formal analysis, Investigation, Methodology, Validation, Visualization, Writing - original draft, Writing - review & editing. Viviana Toro-Ibacache: Resources, Supervision, Validation, Writing - original draft, Writing - review & editing.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We thank the staff of the División Antropología (Facultad de Ciencias Naturales y Museo, UNLP) for allowing and facilitating access to the samples. We also thank Professor Paul O’Higgins and Dr. Phil Cox (University of York) for facilitating access to VoxFE and the FEA solver system, and Professor Timothy Bromage (New York University) for interesting discussions during the realization of this study.

This work was supported by the Dirección Nacional de Cooperación Internacional (Ministerio de

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  • 1

    Address: Instituto de Investigación en Paleobiología y Geología (IIPG), Universidad Nacional de Río Negro. CONICET. Río Negro, Argentina.

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