The bone is an adaptive tissue, with environmental factors leading to functional anatomical modifications (Harada & Rodan, 2003). Apart from biological and biochemical factors, the loading environment is a major factor at work in this adaptive system (Alliston, 2014). Multiple mechanical models have been suggested in the current literature, but their underlying mechanisms are still unclear (García-Aznar et al., 2021, Pearson and Lieberman, 2004). The mandible is a complex load-bearing bone due to its position, shape and multiple functions (chewing, swallowing, breathing, speaking, gripping). Several mandibular loading regimes and subsequent patterns of deformation have been identified from in vitro studies, including non-human primate studies (Daegling and Hylander, 1998, Hylander, 1984, Hylander et al., 1998, Panagiotopoulou et al., 2020, Smith et al., 2021, van Eijden, 2000). For example, in the mandibular corpus, unilateral molar biting at the working side results in a positive sagittal bending of the mandible, a negative anteroposterior torsion which consists in an inversion of the basal border, a positive sagittal shear and a lateral transverse bending, also referred to as wishboning (Hylander, 1984, Korioth et al., 1992, Panagiotopoulou et al., 2020, Smith et al., 2021, van Eijden, 2000). Positive sagittal bending leads to tension at the lower border and compression at the upper border of the corpus, and constitutes the predominant deformation occurring in the working side during unilateral biting (Korioth et al., 1992). On the balancing side, the corpus experiences negative sagittal bending, negative sagittal shear, lateral transverse bending and negative anteroposterior torsion, which, in this side, consists in an eversion of the basal border of the corpus (Hylander, 1984, Korioth et al., 1992, Panagiotopoulou et al., 2020, Smith et al., 2021, van Eijden, 2000). Negative sagittal bending leads to compression at the lower border and tension at the upper border of the corpus and this deformation is combined with the eversion of the basal border to constitute the predicted typical deformation: helically upward and towards the working side (van Eijden, 2000). In the current model, symphysis is hypothesised to experience positive frontal bending, frontal shear, lateral transverse bending or wishboning, and twisting (Dobson and Trinkaus, 2002, Hylander, 1979b, Hylander, 1984, Korioth et al., 1992, Panagiotopoulou et al., 2020, Smith et al., 2021, van Eijden, 2000). Lateral transverse bending, or “wishboning”, leads to a compression of the buccal part and tension in the lingual part of the symphysis. Frontal bending produces a compression of the alveolar part and tension in the inferior part, as well as torsion between the loaded and balancing sides, resulting in dorso-ventral and antero-posterior shear (Dobson and Trinkaus, 2002, Hylander, 1979b). Fig. 1 illustrates the different predicted deformations of the mandibular corpus and symphysis associated with the loading regimes of a unilateral molar biting model.

In this complex loading environment, several studies have identified specific external and internal anatomical modifications of the mandible (Daegling, 1989, Demes et al., 1984, Hylander, 1979b). For instance, in the Neandertal mandible from Regourdou (France), a particular pattern of cortical bone apposition was identified in the same areas where unusual premolar wear facets were identified (Fiorenza et al., 2019). Another feature is the consistently thicker buccal cortical bone compared to the lingual cortical bone in the post-canine corpus identified in several anthropoid genus (Daegling, 1992, Daegling, 2002, Daegling and Grine, 1991, Demes et al., 1984, Holmes and Ruff, 2011, Kanazawa and Kasai, 1998, Kasai et al., 1996, Masumoto et al., 2001). In a biomechanical model where cortical bone adapts its properties to compensate for loads, uniform loads between the buccal and lingual sides cannot explain this uneven distribution. In 1984, Demes et al. suggested that in the post-canine corpus and especially in the molar area, shear forces resulting from occlusal forces affect the buccal cortical bone, while mixed shear forces and counteracting torsional forces affect the lingual cortical bone. On the lingual side, the addition of shear forces and counteracting torsional forces results in reduced strain on the buccal side (Demes et al., 1984). This hypothesis is still debated to this day (Ichim et al., 2007). Thanks to methodological developments, testing the hypothesis of Demes et al. (1984) is possible in vitro (Daegling & Hotzman, 2003) and in virtual environments (Gröning et al., 2013, Ichim et al., 2007). Another opportunity to assess the importance of cortical bone distribution in the mandibular corpus and symphysis in a biomechanical framework is to compare human samples with known divergences in dietary or cultural habits (Holmes and Ruff, 2011, Kanazawa and Kasai, 1998). Findings obtained with these comparative studies are less accurate than those obtained in numerical predictions, only allowing the interpretation of variability in loading regimes in the light of broader cultural or dietary variations. However, these methods offer the opportunity to better understand the dynamics of biomechanical adaptations on a population scale by studying the morphological variability of the human mandible in large samples. Other protocols explore the cortical bone distribution in the framework of indirect mechanical parameters, for instance facial divergence assessment (Kasai et al., 1996, Masumoto et al., 2001). Indeed, facial divergences have been related to masticatory muscle cross-sectional dimensions, volume, activities and bite force measurements in numerous studies (Ingervall and Bitsanis, 1987, Ingervall and Helkimo, 1978, Ingervall and Minder, 1997, Ingervall and Thilander, 1974, Kubota et al., 1998, Raadsheer et al., 1996, Sondang et al., 2003, Tuxen et al., 1999, van Spronsen et al., 1989, van Spronsen et al., 1991, van Spronsen et al., 1992, Weijs and Hillen, 1984a, Weijs and Hillen, 1984b, Weijs and Hillen, 1986). Consequently, morphological analyses of cortical thickness in groups separated by their facial divergences provide a better understanding of the links between muscular activity level in the masticatory apparatus and distribution of this bone in large and modern samples.

An experimental study conducted on rabbits found that the mandibular cortical bone can develop environmental mechanical sensitivity long after skeletal maturity is achieved (Scott et al., 2014). The authors then hypothesised that this mechanism would be present in mammals in general (Scott et al., 2014). Numerous studies have investigated the interactions between loading regimes and the morphological adaptability of the mandibular bone in animal models with varying degrees of similarity to humans: Pan troglodytes (Smith et al., 2021), Pongo pygmaeus (Taylor, 2006, Vogel et al., 2014), Gorilla beringei (Taylor, 2006), Macaca fascicularis (Bouvier and Hylander, 1981a, Hylander, 1979a, Hylander, 1984, Hylander, 1986, Hylander et al., 1998, Hylander and Crompton, 1986, Panagiotopoulou and Cobb, 2011), Macaca mulatta (Bouvier and Hylander, 1981a, Bouvier and Hylander, 1981b, Ross et al., 2012), Cebus apella (Ross et al., 2012), Sapaju (Ross et al., 2016), Otolemur crassicaudatus (Bouvier and Hylander, 1981a, Hylander, 1979a, Hylander et al., 1998, Ravosa et al., 2000), Otolemur garnettii (Ravosa et al., 2000), Procolobus badius and Colobus polykomos (Daegling & McGraw, 2009), Callithrix jacchus, Saguinus fuscicollis and Saimiri sciureus (Vinyard & Ryan, 2006), Propithecus verreauxi (Hylander et al., 2011), Aotus trivirgatus (Hylander et al., 1998), Sus scrofa (Organ et al., 2006), Oryctolagus cuniculus (Ravosa et al., 2007, Ravosa et al., 2007, Scott et al., 2014, Terhune et al., 2020), Rattus norvegicus (Menegaz & Ravosa, 2017), Mus musculus (Ravosa et al., 2007, Ravosa et al., 2007). These studies mostly investigate the adaptability of the mandible within an evolutionary perspective. For instance, they may provide insights into the evolutionary significance of symphyseal fusion in adapting to new diets in primates (Hylander et al., 1998). Any study of the relationship between bone cortical distribution and loading regime in humans implies that the animal models must be comparable to humans, i.e., they must exhibit similar loading regimes. A study from 2020 suggests that these loading regimes are common to many anthropoids, and finds that the Macaca mulatta mandible shares similar pattern in terms of overall deformation with the human mandible (Panagiotopoulou et al., 2020). Furthermore, a similar pattern of uneven distribution of cortical bone in the post-canine corpus has been identified in other anthropoid genus (Daegling, 1992, Daegling, 2002, Daegling and Grine, 1991). Although a new study confirms that the overall deformation regimes in the mandibles of Macaca, Pan and humans are similar, the same study states that the orientation of particular muscle groups can influence interspecific differences in terms of loading regimes (Smith et al., 2021). For these authors, the Pan muscle configuration is a more suitable model for the study of mandibular biomechanics in hominids than the Macaca morphology (Smith et al., 2021). These differences are particularly observable in the anterior corpus (Smith et al., 2021). Other studies also highlight the unique aspect of the human mandible and its biomechanical environment (Daegling and Hotzman, 2003, Ichim et al., 2007, Ichim et al., 2006a, Ichim et al., 2006b). This specific environment could be the result of a unique pattern of masseter recruitment which differs from that of other anthropoids (Hylander et al., 1998, Hylander et al., 2000, Van Eijden et al., 1993). The unique aspect of the modern human mandible is also expressed in a more vertically oriented symphysis and the presence of a chin (Dobson & Trinkaus, 2002). Thus, although animal studies can control for confounding factors and provide accurate biomechanical interpretations, the human mandible, with its pattern of muscle recruitment, muscular orientations and symphyseal anatomy, exhibits specific characteristics that call for specific studies.

In this context, this review hypothesises that a process of environmental mechanical sensitivity is involved in the distribution of cortical bone in the mandibular corpus and symphysis in modern humans, and that loading regimes can influence this pattern of distribution, as in Demes et al.’s (1984) framework. Our work thus aims to answer the following question: “Is the distribution of cortical bone in the mandibular corpus and symphysis linked to the loading environment in modern humans?”.