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Native human populations from South America display high levels of craniofacial variation encompassing gracile and robust skulls. Nevertheless, the processes of bone modeling by which morphological variation among populations were attained, remain poorly understood. Here we analyze the relationship between patterns of bone formation and resorption and morphometric variation in the upper face of adults belonging to farmers and hunter-gatherers from northwestern and south Argentina. Our analyses reveal a common pattern of bone modeling of the malar bone characterized by the presence of formation areas. Thus, the larger size and greater development of malar bone exhibited by hunter-gatherers would be linked to a greater magnitude of bone formation activity. Conversely, the glabella and the superciliary arch presented both formation and resorption areas with a variable distribution among individuals. In the extreme corresponding to more robust morphologies, the great development of the glabella is related to the presence of large formation fields, both in the upper region and toward the frontonasal suture. The less robust morphologies show resorption fields at the upper margin of the glabella, which would contribute to the weaker development of this region. The superciliary arch showed a complex relationship between its morphometric and histological variation; the individuals located at both extremes of the shape space presented large resorption areas located on its upper margin. Overall, our results show the existence of intraspecific variation in the patterns of bone modeling in the human upper face. Anat Rec, 297:1829–1838, 2014. © 2014 Wiley Periodicals, Inc.
Native human populations from southern South America are characterized by their high level of craniofacial morphological variation. Several works have shown the existence of a pattern of variation in adult individuals whose extremes are occupied by small skulls with gracile facial structures—glabella, supraorbital arch, and zygo-maxillary region—corresponding to individuals from farming groups, and larger skulls with more robust facial features corresponding to hunter-gatherer groups (González José et al., 2005; Sardi et al., 2005; Pucciarelli et al., 2006; Perez and Monteiro, 2009; Perez et al., 2011). Moreover, recent analyses suggest that the pattern of interpopulation variation in shape and size is evident at the age of 5 years, although it becomes more pronounced among adults (González et al., 2010, 2011; Barbeito Andrés et al., 2011). So far, these studies focused at the macroanatomical scale, and thus they allowed only a partial and indirect approach to the study of the processes that act at the cellular level and which are essential to understand the mechanisms underlying the craniofacial morphology of adult individuals (e.g. Enlow, 1963; Kurihara et al., 1980; Bromage, 1989; Enlow and Hans, 1996; McCollum, 2008; Lieberman, 2011; Lacruz et al., 2013; Martinez-Maza et al., 2013).
According to the Enlow's counterpart principle (Enlow et al., 1969; Enlow and Hans, 1996) and the functional matrices theory (Moss and Young, 1960; Moss and Rankow, 1968; Moss and Salentijn, 1969; Moss, 1997a,b), the skull grows through interrelated complex processes involving the growth by bone modeling mechanism and displacements of its skeletal elements to maintain a functional and structural balance (e.g. Moss and Young, 1960; Moss and Salentijn, 1969; Enlow and Hans, 1996; McCollum, 2008; Lieberman, 2011). The bone modeling mechanism (a process also termed as remodeling; Enlow and Hans, 1996; see discussion in Martinez-Maza et al., 2006) consists in the coordinated and uncoupled activity of two cellular groups, osteoblasts (bone forming cells) and osteoclasts (bone resorbing cells). During development, bone growth is influenced by many factors including different genetic, biomechanical and hormonal factors (Enlow and Hans, 1996; O'Higgins et al., 1991) as well as by the growth of the functional spaces (cranial, orbital, nasal, and oral cavities) and the soft tissues in which they are embedded (e.g., brain, muscles, connective tissues) (Moss and Young, 1960; Enlow and Hans, 1996; see also Lieberman, 2011 and cites there in). Consequently, craniofacial bones change their size and shape as well as their relative position within the craniofacial system maintaining the proper bone alignment, function and proportionate growth (by means of drift, displacement, and rotation; Moss and Young, 1960; Björk, 1969; Björk and Skieller, 1972, 1976; Enlow and Hans, 1996; see also a review in Martínez-Maza et al., 2006). These factors ultimately regulate the onset, offset and rate of activity as well as the spatial distribution of the areas of bone formation and resorption (Enlow and Hans, 1996; Martin, 2000; Robling et al., 2006). Changes in any of these parameters will contribute to the morphological differences observed among species and populations (Lieberman, 2011).
One of the approaches to study the dynamics of bone modeling that underlie morphological variation, is based on the identification of microstructural features generated by the cellular activities of tissue formation and resorption on the surface of bone (Enlow, 1963; Boyde, 1972; Bromage, 1989; Enlow and Hans, 1996; Martinez-Maza et al., 2010). Such data are used to build maps of bone modeling that show the distribution of areas of cellular activity, whose interpretation in the field of craneofacial biology provides insight regarding the directions of growth in the various bone regions (Enlow and Hans, 1996). The development of a specific nondestructive methodology for these types of studies has allowed the analysis of the craniofacial complex of fossil and living primates, and the particular pattern of each species has been established (e.g., Bromage, 1989; O'Higgins et al., 1991; McCollum, 1999, 2008; Rosas and Martinez-Maza, 2010; see also a review of these works in Martinez-Maza et al., 2006; Martinez-Maza et al., 2011, 2013). It has also been suggested that some differences among human populations exist, although the available data come exclusively from a reduced number of recent populations of European origin, and thus the range of variation of the species remains poorly understood (Kurihara et al., 1980; Hans et al., 1995; McCollum, 2008; Martinez-Maza et al., 2013).
The main goal of this work is to explore the relationship between patterns of bone modeling in periosteal surfaces and morphometric variation, in the upper region of the face of adult individuals belonging to populations from northwestern and south Argentina, which represent the extremes of morphological variation described for South America. In particular, the individuals that show greatest differentiation in the morphometric analyses are also expected to exhibit the greatest differences regarding the distribution of fields of bone modeling. To describe the axes of greatest variation of the shape and size of craniofacial structures, we used multivariate statistical analyses derived from geometric morphometrics. The microstructure of the bone surface was studied using high resolution bone replicas that were analyzed under incident-light microscope. Bone modeling maps made from these data were compared with the pattern of morphometric variation at macroanatomical level.
- Top of page
- MATERIAL AND METHODS
- LITERATURE CITED
Craniofacial morphological variation is related to differences in the distribution of bone formation and resorption fields that indicate different growth dynamics (e.g., Bromage, 1989; Enlow and Hans, 1996; McCollum, 2008; Martinez-Maza et al., 2013; Lacruz et al., 2013). Until now, studies on this subject have shown the existence of a particular bone modeling pattern for each species, but its role regarding intraspecific variation has been scarcely studied (McCollum, 2008; Martinez-Maza et al., 2013). In this sense, the present work represents a first approach to the study of the cellular mechanisms involved in the morphometric variation of human populations from southern South America. This study is highly interesting for studies of craniofacial morphology in general, because it is the first analysis of the morphological variation of a single sample by two integrated complementary approaches, i.e., geometric morphometric analysis and study of bone modeling patterns.
The morphometric analysis of the facial structures of Pampa Grande and Chubut samples agrees with the general pattern documented for South American populations, with larger size and stronger development of the glabella and superciliary arch in the hunter-gatherer adults than in the farmers (Sardi et al., 2005; Perez and Monteiro, 2009). A reduction in size and robusticity of cranial traits associated with an increased consumption of domesticated plants has been found in other geographic regions, although the patterns seemed to vary according to the populations being as compared (Carlson and Van Gerven, 1977; Paschetta et al., 2010; von Cramon-Taubadel, 2011). On the other hand, the analysis of bone surface allowed to characterize the distribution of bone formation and resorption fields in the three facial structures studied here. In particular, the bone modeling of the malar bone showed a common pattern in all individuals characterized by the presence of bone formation areas. Conversely, the glabella and the superciliary arch presented both formation and resorption areas, but the distribution of the respective fields varied between the Pampa Grande and Chubut individuals.
The relationship between facial variation summarized in the form space and the bone modeling maps suggests that the differences in malar form among individuals would not be attributable to variations in the distribution of bone formation and resorption areas, because all the individuals showed bone formation. Consequently, the larger size of the malar and the development of its frontal and zygomatic processes in Chubut individuals would be linked to greater magnitude of bone formation activity. Unbalance favoring bone formation results in an increase of size during growth (Enlow and Hans, 1996), and therefore, differences in bone formation rates could explain the size and shape variation among adult individuals. The glabella and the superciliary arch displayed greater disparity in the patterns of bone modeling among individuals. In the extreme condition corresponding to the more robust individuals from the Chubut population, the great development of the glabella is related to the presence of large formation fields, both in the upper region and toward the frontonasal suture. On the contrary, the less robust morphologies from Pampa Grande show resorption fields at the upper margin of the glabella, which would contribute to the weaker development of this region. The superciliary arch display a complex relationship between its morphometric and histological variation, since the individuals at both extremes of the shape space present large resorption areas on the upper margin of this structure.
The combined analysis of facial morphometric variation at anatomical level and of bone modeling patterns performed here contributes to the discussion regarding the mechanisms responsible for the variation observed among adult individuals. Previous research on native South American populations were aimed at establishing whether the shape and size differences between populations entailed changes in allometric trajectories, in the age of cessation of growth, or in the rate of growth (González et al. 2010, 2011; Barbeito Andrés et al., 2011). The presence of bone formation fields in the malar of adult individuals of similar age that differ markedly in the size of this structure suggests that such morphological differences would have more probably resulted from variation in the rate of bone formation, rather than from the prolongation of bone formation activity. In this sense, the larger size of the masticatory component in hunter-gatherers since early ontogenetic stages (Barbeito Andrés et al., 2011) also supports the hypothesis that differences in growth rate would account for interpopulational variation.
Assessing whether the pattern of bone modeling described here is a particular feature of the adult individuals of the populations under study, or reflects the variability of the species, requires the comparison of a larger number of samples. The scarcity of studies of craniofacial bone modeling in adult Homo sapiens restricts comparison of the results obtained here. Until now, the only reference about variation in the bone modeling pattern of facial structures is the work by Martinez-Maza et al. (2013). The sample analyzed by these authors comes from the anthropological collection of Identified Skeletons belonging to Universidade de Coimbra (Portugal) consisting of individuals dated between the late 19th century and early 20th century (Matos Fernandes, 1985). This collection has detailed information for each individual (age, sex, employment, cause of death, and geographical origin). Comparison of the present results with those from the Coimbra sample indicates that the bone modeling patterns of the glabella and superciliary arch of Chubut and Pampa Grande resemble those recorded for the adult sample in Coimbra. Unlike the condition observed in South American individuals, the pattern of the malar in the Coimbra sample displays bone resorption along its entire lower margin and its temporal process up to the temporal-zygomatic suture, as well as on the infraorbitary margin in the area of contact between glabella and superciliary arch.
Taking into account observations from previous studies (Kurihara et al., 1980; Enlow and Hans, 1996; McCollum, 2008), differences observed in the facial regions may be attributable to environmental factors or to the evolutionary history of populations. Particularly, the mechanical loads exerted on bone tissue are among the most important factors to stimulate bone formation (Robling et al., 2006); thus, the structures directly involved in food processing are expected to present more extensive bone formation fields. Numerous studies have shown that the zygomatic arch region is strongly influenced by forces exerted during mastication, whereas stress is very low on the glabella and superciliary arch (Hylander and Johnson, 1997; Ravosa et al., 2000; Vinyard and Smith, 2001; Ross and Metzger, 2004; Wroe et al., 2010; Athreya, 2012). This could explain the predominance of bone formation in the malar compared to the other structures analyzed, as well as the differences in modeling patterns of malar bone between the Coimbra and South American samples. On the other hand, the differential hardness of consumed foods would not be enough to explain the degree of robusticity of the supraorbital region. As an alternative hypothesis, a positive association between skull size and development of this region has been suggested, which would be related to systemic factors (e.g., increase in circulating growth hormone) that result in greater cortical robusticity (Lieberman, 2011; Athreya, 2012). Such factors have been previously proposed to explain differences in robusticity between South American populations (Bernal et al., 2007).
Our goals for the future include more in-depth studies through the histological analysis of ontogenetic, in order to describe the changes in bone modeling that take place during development. The combination of these data with the description of morphological changes from three-dimensional morphometric analyses will allow the generation of development models and the assessment of hypotheses regarding the ontogenetic mechanisms involved in interpopulational variation.