Shaping the human face

International Congress Series 1296 (2006) 55 – 73

www.ics-elsevier.com

Shaping the human face Paul O’Higgins a,*, Markus Bastir a,b, Kornelius Kupczik a a

b

Hull York Medical School, The University of York, Heslington, York YO10 5DD, England, UK Department of Paleobiology, Museo Nacional de Ciencias Naturales, CSIC, 28006 Madrid, Spain

Abstract. The craniofacial skeleton carries out diverse functions served by hierarchically integrated developmental and functional modules. The craniofacial biologist is interested in how the skeleton of the cranium evolves and develops to integrate these functions while the clinician is more concerned with how function and development is altered in disease. The study of pathology is informative with respect to the control of development as is the study of normal variability. Particularly interesting are the paranasal sinuses which show marked variation within humans, in the human fossil record and among our close relatives. Their variations in humans are important clinically because they can be associated with increased susceptibility to disease and render sinus surgery more difficult. The extent and nature of variation within and between cranial structures is also informative with respect to normal developmental regulation since this can inform us about how their development is regulated. To fully understand the reasons we possess paranasal sinuses and why they vary it is necessary to relate their development to the temporally and spatially integrated development of the face from modules. Recent advances in morphometrics and mechanical modelling of the developing face have opened up new avenues of investigation likely to lead to such an understanding. They have the potential to test mechanical and spatial hypotheses of sinus ontogeny and so are likely to lead to new insights into craniofacial biology of importance to both evolutionary biologist and clinician. Resumen. Es esqueleto facial cumple una serie de funciones distintas que se llevan a cabo a trave´s de mo´dulos tanto funcionales como mo´dulos del desarrollo todos ellos organizados jera´rquicamente. Mientras que el bio´logo craneofacial esta´ interesado en conocer la evolucio´n y la ontogenia de la integracio´n de esto mo´dulos en el esqueleto craneofacial, el clı´nico se interesa mas por como la funcio´n y el desarrollo esta´n alterados por enfermedad. El estudio de las patologı´as y el de la variacio´n normal son interesantes en cuanto a los mecanismos de control ontoge´nico. Los senos paranasales que demuestran una variacio´n marcada en humanos modernos, homı´nidos fo´siles y nuestros parientes evolutivos ma´s cercanos, los simios, son especialmente interesantes. La variacio´n de los senos paranasales en humanos tiene elevada importancia clı´nica porque se asocia con una

* Corresponding author. Tel.: +44 1904 321752; fax: +44 1904 321696. E-mail address: [email protected] (P. O’Higgins). 0531-5131/ D 2006 Published by Elsevier B.V. doi:10.1016/j.ics.2006.03.036

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susceptibilidad elevada a infectarse y porque aumenta la dificultad de intervencio´n cirujana. El grado y la naturaleza de esta variacio´n entre determinadas mo´dulos craneofaciales y dentro de aquellos contienen tambie´n informacio´n sobre la regulacio´n ontoge´nica normal. Para un conocimiento completo de los motivos de la formacio´n de los senos paranasales y su variacio´n es necesario relacionar su desarrollo con las propiedades de la integracio´n espacio-temporal de los componentes craneofaciales a lo largo de la ontogenia. Avances recientes en morfometrı´a y en la modelizacio´n meca´nica de la cara durante su ontogenia han abierto nuevas perspectivas para la investigacio´n. Estas metodologı´as permiten testar hipo´tesis espaciales y funcionales de la ontogenia de los senos. Asimismo, contienen el potencial de incrementar nuestro conocimiento sobre la biologı´a craneofacial, algo tan importante para el bio´logo evolutivo como para el clı´nico. D 2006 Published by Elsevier B.V. Keywords: Paranasal sinus; Primate; Human variation; Modularity; Morphological integration; Geometric morphometrics; Finite element analysis; Biomechanics

1. Introduction The relationship between the development, evolution, morphology and function of the craniofacial skeleton is a key issue in mammalian biology because of its unique importance to the whole animal. The skull provides support for and integrates diverse structures that perform diverse tasks, including provision of support and protection for the brain, mastication, vision, respiration, olfaction, expression and display. From the clinicians’ perspective the cranial region of humans manifests many signs and symptoms of disease. This is an inevitable reflection of the complexity of roles subserved by the cranium. The cranium develops in a way that reflects its diverse functions with tightly genetically controlled patterning being responsible for the initial form of the cartilaginous and membranous parts of the skeleton, contents of the neurocranium, orbits, ears, nasal chamber and the diverse components of the oral system [1]. To a large degree the genetic control of (at least) the early development of many component structures is distinct yet during ontogeny and eventually in the adult they co-exist such that the functionality of each is preserved while they fit together to make a viable whole. Thus disparate components develop varying degrees of mutual interaction until the face is integrated as a whole whilst efficiently serving diverse functions. The result is that we usually develop functioning crania comprising different functional complexes (orbits, nasal, masticatory, etc.) that may incorporate and share with other complexes diverse structures under diverse developmental control. Of interest to evolutionary and developmental biologists is how these components are regulated and how they are integrated. In this paper we aim to consider the latter, integration in the skeleton of the cranium, and particularly the extent to which mechanical signals might be involved in effecting this during the later stages of ontogeny. It is not only from studies of the normal that insights can be gained into craniofacial ontogeny but also through the study of pathological development. Thus, people who have achondroplasia share some characteristics of facial form (including frontal bossing and midfacial hypoplasia) that reflect the underlying developmental controls and constraints in craniofacial development. Premature fusion of different cranial sutures in craniofacial

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synostoses leads to diverse consequences for the subsequent ontogeny of facial form. The consequences depend on the timing and nature of the primary lesion (e.g. which sutures close and when, bilateral or symmetrical, etc.; [2]). Such disorders serve to emphasise that cranial ontogeny is plastic and can compensate. Even following a disturbance of cartilage growth or bone displacement at sutures it can develop in a way that preserves functionality. A further interesting avenue is to study normal variability rather than static morphology. The extent to which regulation of ontogeny of a structure is intrinsically regulated or secondary to the development of other structures might be expected to be reflected in its variability. In some structures normal variations can be quite extreme, bordering on the pathological. One such set of dstructuresT is the paranasal sinuses which can vary between absent and present and show large degrees of asymmetry. These variations can be associated with ill health and cause problems for the clinician at surgery and in diagnosis. The paranasal sinuses also show large and unexpected patterns of variation between related species [3]. This leads us to ask what clinical and comparative perspectives on the sinuses can tell us about craniofacial ontogeny. 2. The paranasal sinuses: clinical significance The propensity of an individual to suffer recurrent and chronic sinus infections is in part related to the presence or absence of certain variations in the anatomy of their paranasal sinuses and associated nasal structures, particularly if they impede the freedom of flow of mucus through the sinus orifices. Surgery requires awareness of the complexities of sinus anatomy and is made difficult by the high incidence of sinus anomalies. A recent study [4] indicated frequent variations on CT examination of 400 patients; 10% showed ethmoidal sinus hypoplasia, 4% maxillary sinus hypoplasia and incidences of 2–4% were noted for other gross anomalies. Another study [5] of 110 CT scans of patients suffering inflammatory sinus disease identified anomalies of the paranasal sinuses in 20% and further anomalies of the nasal septum and middle nasal concha in more than 55%. Of particular note for the surgeon and of some interest to the craniofacial biologist, sinus variations can result in herniations of the orbital contents into the ethmoid sinuses and of other structures into other sinuses. Thus, the internal carotid artery which normally passes just lateral to the basisphenoid can come to bulge into or lie free within the sphenoidal air sinus as can the optic nerve [4]. This is interesting from a developmental point of view because it implies that there are few controls and constraints, other than the developmental historical ones of initial patterning and spatial organisation, on the relationship between nerves and vessels and the sinus walls. Other common anomalies include supraorbital recess 6%; concha bullosa 30%; pneumatisation of the anterior clinoid processes 12% [6]. The extent to which the maxillary sinus is pneumatised also varies greatly with some 10% of individuals possessing one or both maxillary sinuses larger in horizontal or vertical dimensions than 90% of the corresponding dimension of the orbit. This variable pneumatisation suggests that it is regulated as a secondary phenomenon, perhaps in response to cues such as the space available, rather than primarily with sinuses driving the growth of the enclosing bones. Asymmetry is common in the sinuses and it can be marked with one maxillary sinus being extensively pneumatised in 1% [7] and

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congenitally absent in rare cases [8]. Again this is interesting because it implies somewhat loose control of maxillary sinus ontogeny. 3. The paranasal sinuses: variation and evolution The paranasal sinuses develop from very specific parts of the lateral nasal walls and the original openings of the outgrowths persist as orifices with relatively fixed locations in adulthood, implying tight, probably genetic, regulation. This constancy of location is the basis for discerning homology in comparative studies of cranial pneumatisation [3,9,10]. The extent to which the morphology of the sinuses as a whole is consistent within and between geographical groups of humanity has been investigated by a number of authors. Most extensively studied is the frontal sinus because it can be imaged using plain radiography. Brothwell et al. [11] noted differences in frontal sinus morphology of Europeans, Africans and Australians and Buckland-Wright [12] has identified consistent differences in the frontal sinus between British Populations from different historical periods. Further Schuller [13] noted that within Australians of European extraction the frontal sinuses may be absent bilaterally in 5% and Greene and Scott [14] found the frontal sinuses to be absent in 95% of the Wadi Halfa Mesolithic population from Sudan. Additionally the frontal sinus is missing in a high proportion of native Australians and some arctic populations [3]. Greene and Scott [14] consider that this variability of frontal sinuses might in some way be related to how masticatory stress is distributed in the face (see later). Recent work by one of us has [15,16] has also demonstrated significant variations in frontal sinus morphology in a late Pleistocene–early Holocene (5–20,000 years ago) population using CT (Fig. 1). The evolutionary context of sinus morphology has most recently been reviewed by Rae and Koppe [3]. This review has brought to the fore some curious issues surrounding the evolution and function of the paranasal sinuses. The maxillary sinus is present in a wide range of mammals. Within primates it is found in all apes and many New World but no Old World Monkeys except macaques [3] and this, together with its absence in Victoriapithecus has led to the view that it has been reacquired in this group during evolution. In hominoids the volume of the maxillary sinus scales isometrically with measures of cranial size [17]. In atelines maxillary sinus volume also scales with cranial size but allometrically and in Alouatta caraya the maxillary sinus possesses one or more vertical septa (of potential relevance to load bearing) and may invade neighbouring bones such as the frontal and basisphenoid which do not possess true sinuses [18]. Interestingly maxillary sinus volume in Japanese macaques (Macaca fuscata) shows a relationship to latitude and temperature such that specimens from colder regions possess smaller sinuses possibly because of nasal cavity enlargement [19]. Similarly, small sinuses are reported for Eskimos [20]. In contrast to the maxillary sinus, true sphenoidal air sinuses are less widely distributed within primates. They are found in apes and possibly some platyrrhines while true ethmoidal and frontal sinuses are present only in hominoids [3]. However, as noted above the frontal sinus may be missing unilaterally or bilaterally in modern humans. There is debate about the phylogenetic significance of the distribution of paranasal sinuses in primates which is augmented by the difficulties in determining their homology and state in fossils [3,16,21]. Further, within modern humans variable absence of paranasal sinuses has

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led to debate about the relationship between them and climate. This is particularly important given that Neanderthals are heavily pneumatised [22] which has led to the speculation that the sinuses represent a cold adaptation. This is in direct contrast to the finding of diminished maxillary sinuses in humans and macaques that inhabit colder climates (see above) and of large sinuses in the archaic Homo from Broken Hill although in this fossil, scaling of the face according to the scaling relationship of modern humans may explain maxillary sinus volume [21]. 4. The paranasal sinuses: functional significance Given that frontal sinuses show considerable variability between modern human populations and that they are often massively expanded in fossil representatives of archaic Homo there is some debate about the relationship between the volume of this sinus, the morphology of the supraorbital torus and masticatory stress [3,23]. The key issue is whether or not the supraorbital torus is an adaptation to masticatory loads [24,99]. Prossinger and Bookstein [25], in a mathematical modeling study of the frontal sinus,

Fig. 1. Variation of paranasal sinus morphology in late Pleistocene/early Holocene humans as revealed by CT (3D rendering done with VOXEL-MAN; modified after Kupczik [15]).

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conclude that a mechanism with similarities in behavior to an autocatalytic reaction, could well dexplainT their ontogeny although their final size appears to be determined by other factors. This is consistent with a model in which the final size is determined by the available space and the sinuses are excavated in response to lack of bone loading. The issue of the relationship between facial mechanics and the architecture of the face including the paranasal sinuses is a key issue in human evolution and will be discussed in more detail below. The possible physiological functions of paranasal sinuses have led to a great deal of discussion. Possible functions include olfaction in some species, conditioning of inspired air, thermoregulation, contribution to vocal resonance among others ([3]; Table 1). These authors make the important distinction between the current functions that sinuses may serve and their evolutionary and ontogenetic origins. It is clear that absence of one or more paranasal sinuses in humans is no great burden and that they serve no critical function [3] that can satisfactorily explain their evolution in terms of natural selection. Thus increasing attention is being given to the possible role of mechanical loading and the consequent distribution of strains during ontogeny in the formation of sinuses. It has already been noted that the supraorbital region bears little masticatory strain in adult primates [26,99] but it is also noteworthy that the hollowing out of bone results in little loss of mechanical integrity while minimising the cost of maintaining bone and the weight of the cranium [27]. A problem with the discussions of paranasal sinus morphology and biomechanical function is that much of the data used to support or refute arguments is gathered from adults, yet the sinuses appear during post natal ontogeny as the various functional components (teeth, nose, orbits, jaws, etc.) of the cranium develop their adult sizes and shapes. Thus, if the cranium adapts to loading during ontogeny, we should expect the adult cranium to be well adapted in that, on average (rather than different bites of short duration), low strains will be present throughout. As the craniofacial skeleton develops its peculiar ridges, bumps and fossae in response to whatever stimuli and in relation to the various components of the head that serve specific functions we might expect regions of bone that are relatively insulated from stresses to be hollowed out either by sinuses or cancellous bone. This is not to imply that sinuses drive the growth of adjacent bone, but rather, under this model, they passively expand into newly available space. Preuschoft et al. [27] have recently reinforced this idea in a biomechanical analysis of model pneumatised spaces and spongy bone. Regarding the formation of the maxillary sinuses it is worth noting that they appear as the permanent dentition erupts and the maxillary dental row extends and shifts in its relative location to other modules (see later analysis of longitudinal data). It is possible therefore that a critical signal in the development of these sinuses relates to changes in the spatial relationships of developmental modules in the cranium. 5. The paranasal sinuses: modules, integration and facial mechanics Rae and Koppe ([3]: 218) indicate bit will be impossible to elucidate the dtrueT function of the paranasal sinuses without considering their relationship to all relevant components of the head during ontogeny and phylogenyQ. The ontogeny of sinuses cannot be

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considered in isolation from the ontogeny of the form and spatial relationships of other cranial components that might themselves be under somewhat more direct (genetic) control of developmental regulatory mechanisms related to their more critical functions. The integration of the craniofacial skeletal components depends to considerable degree on the adaptive response of the growing cranium to mechanical signals. In turn, if viewed from the perspective of the response of tissues to localized mechanical signals (or lack thereof) during the development of the paranasal sinuses then we might expect sinus morphology to be highly variable [27]. This mechanical regulation model is consistent with the clinical and comparative pictures described above but care should be exercised in accepting it as the whole picture. This is because, there is a dynamic hierarchy of interactions between developing cranial components (e.g. eruption and accommodation of the permanent dentition allowing maxillary expansion with consequent sinus expansion) which is as yet incompletely understood (see functional matrices, below). 6. Building a face from modules The face is a complex morphological structure constructed from several components or modules characterized by different levels of morphological integration [28]. These are to some degree anatomically distinct but they are arranged hierarchically and so overlap and intertwine both temporally during development and evolution and spatially within the same individual. At a higher level the modules have to dfitT and work together, i.e. become integrated. The physical links between them that integrate them (e.g. the maxilla between masticatory, visual and respiratory components) are influenced by their adjoining functional components. They accommodate and integrate their distinct functions. What is a module? Different definitions of modules have been suggested. Many authors use a developmental definition [29–36], e.g. those structures that are controlled by a specific group of genes, that share a common set of developmental constraints or which share locally acting self-regulatory developmental mechanisms [29,37–39]. A pragmatic approach to identifying modules has recently been suggested through the identification of bany subsystem manifesting some quasi-autonomous behaviorQ ([31]: 313). This definition is useful because it enables the identification of modularity from morphometric approaches (see Partial Least Squares below) [32,35,36] and opens up the possibility of linking developmental modules to units of phenotypic evolution. However with regard to such links von Dassow and Munro [31] point out that while a linear correspondence between genes, gene complexes, functional components, and morphological characters (homologies) may be naively thought of, there is not always a one-toone relationship between them. This is because of the multiple potential interactions between modules within and between hierarchical levels and it is known as the drepresentation problemT in the genotype–phenotype map (Fig. 2) [38]. In part then, the problem with identifying modules, particularly in a complex structure such as the cranium, arises because the modules interact spatially, temporally and hierarchically which means that their distinctiveness becomes blurred at each level [40]. The term modularity describes the decomposability of units into sub-units and so forth, as a hierarchical and nested concept, however we should not expect to be able to decompose structures into precisely delimited and independent modules.

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Fig. 2. A) Schematic relationships between genetic, developmental, morphological and functional levels of structural complexity. Pleiotropic effects account for character covariation; (i.e. formation of character complexes [c1–c4, or c5–c7] which contribute to a given function [F1, F2] (modified after Wagner and Altenberg [38]).

How then does the cranial skeleton which subserves and accommodates different modules come to function as coherent whole? The answer lies in great part with integration. Morphological integration refers to the ways in which these semi-autonomous (individualized) modules interact temporally, spatially and at different hierarchical levels [28,35,36,41]. Integration results in the fitting together of disparate modules in ways that preserve function of each and of the whole [28,32,35,41–47]. Relative independence of ontogenetic regulation between modules is an important precondition of mosaic evolutionary change because modifications in one functional system should not diminish the functional or structural integrity of others [39,48]. If integration were homogeneously pervasive, then morphological evolution would be severely constrained [49]. All parts would be affected simultaneously by modification of one specific component and this would be unlikely to produce viable biological results [38,48,50]. In order to understand the specific processes that lead to relative independence and subsequent integration of morphological units (modularization) it is essential to identify and delimit modules [35]. This identification might be by the elucidation of pathways of genetic and non-genetic regulation of functional structures [1], through the identification of suites of characters that show correlated development or evolution [32] or through comparative/functional analyses based on the functional matrix hypothesis [51]. This dhypothesisT posits an non-genetic model of craniofacial growth and development that assumes the existence of semi autonomous bfunctional cranial componentsQ with regard to their genetic and non-genetic ontogenetic control mechanisms [51–55]. 7. Control in craniofacial ontogeny: relationships between genetic and non-genetic systems Through ontogeny the relative importance of genetic and non-genetic growth controls varies. Genetic control is relatively more important early, especially during patterning, while non-genetic control becomes increasingly important later in ontogeny. One key

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aspect of non-genetic control is the response of skeletal tissues to their local biomechanical environments [56,57]; this is the basis of the functional matrix hypothesis [51]. Two types of functional matrices have been distinguished, periosteal and capsular [52,58]. These bear slightly different relationships to growth processes. The first, the periosteal matrix, provides a mechanism whereby the structures related to the periosteum influence its directly and locally related microskeletal units. The classical example of a periosteal functional matrix is the temporal muscle (soft tissue matrix) which regulates the formation and morphology of the mandibular coronoid process. The second, the capsular matrix [59] affects macroskeletal units, which are composites of different parts of bones. The capsular contents have a morphogenetic interaction with their enveloping bony capsule. Examples of capsular matrices include the nasopharyngeal space, the oropharyngeal space, the cranial cavity and the orbits [52]. Thus functional matrices bear some similarities to the notion of dmodulesT but differ in that they relate principally to later events in ontogeny and in that they may specifically act to integrate. Ranly [60] has criticized the Moss formulation of functional matrices in the degree to which it relies entirely on non-genetic interactions. Thus, chondrocranial growth is controlled by intrinsic genetic factors while desmocranial growth is controlled by non-genetic factors that originate from more tightly genetically regulated skull cartilage, the brain and other head tissues. The concepts of modularity and integration of functional cranial components also help in understanding morphological variation because different parts of the skull share functional and ontogenetic relationships with different systems of the organism. There are two essentially different organism systems and associated growth patterns that are relevant for facial variation, the neural and the somatic system. The maturation of both systems is reflected in the ontogenetic variation of the face. Facial growth is characterized by positive facial allometry (somatic growth pattern) while the neuro- and basicranium scale with negative allometry and follow the neural pattern. 8. Advances in methodology for studying craniofacial ontogeny If we are to make inroads into the analysis of how the cranium (or its parts such as the sinuses) changes in size and shape during ontogeny, how these changes relate to functional components of the cranium and how these components interact and become integrated into the whole we need technologies suited to the analysis of the size and shape of internal and external structures of the cranium. The use of radiographs to analyse facial growth is commonplace in orthodontics and craniofacial biology [53] but the advent of CT imaging is potentially revolutionary in that it allows us to visualize the details of both internal and external morphology in a way that preserves all spatial relationships [61]. When combined with recent advances in statistics and geometric morphometrics they have the potential to allow us to model and compare ontogenetic changes in the sizes and shapes of complex three-dimensional structures such as the cranium. Geometric morphometrics represents coordinate data within a nonEuclidean shape space [62] whose geometric and statistical properties are well defined and which has highly desirable statistical properties (reviewed by [63]). The methods offer considerable advantages in terms of visualisation and statistical analysis in comparison with all other morphometric approaches to the analysis of landmarks [64,65]. They allow

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us to directly compare ontogenetic trajectories between individuals, populations, species, etc. and they can be used to examine how variations in one structure are related to variations in another. This is particularly pertinent to the study of craniofacial ontogeny in that it naturally leads to studies of modularity and evolution. Finally the advent of powerful software and computers allows us to model the mechanical behavior of complex structures such as the cranium; using Finite Elements Analysis (FEA). Given that mechanical adaptation is widely believed to exert a considerable influence on craniofacial ontogeny (see functional matrices, above) and particularly in the post-natal period, this tool is of potential value in testing models of adaptation and integration. Below, we illustrate these methods by describing three example studies. 9. Example analyses 9.1. Denver growth study: non-linearity and modularity, linearity and integration A series of geometric morphometric studies has recently addressed the question of coincidence, parallelism or divergence in primate facial and craniofacial ontogenetic trajectories [66–71]. These investigations have focused on trying to explain the extent to which adult differences are established pre or postnatally and to investigate differences in ontogenetic shape and scaling trajectories [72–74] They have also investigated the extent to which allometric trajectories reflect phylogeny ([47,75]; contra [76]). Important conclusions of these studies are that the principal differences between species arise during the prenatal period, while postnatal ontogenetic shape trajectories only serve to accentuate and modify them. Cross sectional data have been used in many of these studies and a frequent finding among diverse primates is that the ontogenetic shape trajectory of the face is essentially linear, implying consistency of the underlying biological processes throughout the postnatal period. Subtle non-linearities have been noted however as a component of the development of sexual dimorphism, late in ontogeny and where analyses examine the whole cranium [66,77,100]. Given that the cranium comprises diverse modules and functional components we should be somewhat cautious about accepting the apparent linearities that emerge from cross sectional studies. It seems clear that their presence or absence can only be tested using longitudinal data. Several life history events would lead us to expect a certain irregularity in ontogenetic shape trajectories until some time between 5 and 7 years of age. These include the termination of the major expansive period of brain growth which fixes medio-lateral dimensions of the cranial base and upper facial dimensions [53]. The permanent incisors and first molars erupt, changing the relative proportions of the alveolar arch (lengths and heights) with respect to other facial structures [78,79]. The change from sutural to surface growth as the prevailing growth mechanism also occurs at this time [80,81] and leads to mechanical integration of most functional facial components. Beyond this period the face follows a somatic growth trajectory while the neurocranium does not. Thus further nonlinearities in the form of the cranium as a whole are expected as neural growth ceases and somatic growth spurts. The somatic growth trajectory of the face ties in well with the expansion of lung volumes and the nasal capsule [53] and facilitates functional physiological integration between the nasal capsule as the facial part of the respiratory system and the lungs as the postcranial part of the respiratory system.

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In ongoing work we have applied geometric morphometric methods to longitudinal data in order to examine the detail of post natal facial ontogenetic shape trajectories in humans using radiographs from the Denver Growth Study. We have studied 10 individuals, who were X-rayed periodically between birth and adulthood. Analyses of six common facial landmarks allow us to trace each individual along its ontogenetic shape trajectory and to test the null hypothesis of no significant difference between two time fractions of postnatal ontogeny (below and above 6 years) by Multivariate Analysis of Covariance [71,82] and Principal Component Analysis (PCA) [83]. The results indicate that linear models do not adequately describe postnatal ontogenetic trajectories. It appears that particularly the earlier ontogenetic period until 5–7 years is characterized by inconsistency within and between individuals in ontogenetic trajectories. This is followed by more stable and more linear ontogenetic trajectories (Fig. 3). Morphologically the first ontogenetic fraction is characterized by increasingly vertical growth, while the second fraction produces horizontal projection of the nasal bridge (nasion) and the alveolar arches (prosthion—possibly to accommodate the erupting permanent dentitions). The lack of stability in the early phase of post natal ontogeny may well reflect the

Fig. 3. Geometric morphometrics analysis of longitudinal cephalograms. A) PCAs showing highly irregular trajectories until the age of 6 and linear beyond. B) Left frame shows landmarks; middle frame—the first part of the allometric trajectory is characterized by vertical expansion of the face; right frame—the second part is characterized by horizontal expansion at the nasal bridge and the alveolar arches.

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lack of integration between the facial modules, whereas the later stabilisation might be attributed to the integrative effects of mechanical interlocking of sutures and subsequent coordination of facial structures with the somatic growth pattern. One immediate implication of these findings is that there is no reason to expect stable localizations of growth remodelling fields along the whole postnatal ontogenetic period. Some studies have identified subtle variations in these [84–86] and have made attempts to link these to ontogenetic events [66]. The current findings regarding linearity add further impetus to the need to link craniofacial ontogenetic size and shape trajectories to studies of facial remodelling, modularity and biomechanics. 9.2. Partial Least Squares analysis of cranial bases and faces Partial Least Squares analysis (PLS) can be turned to the study of landmark data in geometric morphometrics. It is a technique that examines the ways in which two or more

Fig. 4. PLS analysis of face based interactions. A) Indicates that PLS correlations are largest between the lateral base and face. B) Visualisation of the interaction between the midline base and face. C) Visualisation of the interaction between the lateral base and face.

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sets (blocks) of variables covary and has been turned to the analysis of landmark data with considerable effect [87–89]. In the context of morphological integration and modularity PLS can be used because it allows patterns of covariation between structures to be identified and visualized [32,35,36,89,90]. An example of the application of PLS to a significant problem in craniofacial biology comes from a recent study [91] in which it was applied to the study of morphological integration between basicranial and facial structures in humans. There is a long held view that midline base structures impact on facial and so, mandibular form and a less well defined view that the lateral base structures are also influential [53]. In order to test if the midline or the lateral base is the most significant Bastir et al. [91] used PCA to reveal apparent morphological covariation between the petrosal part of the temporal bone and the mandibular ramus [91] and were then able to show (Fig. 4) that the lateral base is actually more closely integrated with facial structures than is the midline [36]. 9.3. Modelling facial mechanics None of the advances in morphometrics leads to a direct understanding of the role of mechanical loading in driving changes in size and shape in craniofacial ontogeny. Even direct biomechanical analyses of facial function achieved by placing strain gauges on the face and assessing the distribution of strains during function (e.g. [92]) can only give us insights into what is happening where strain gauges can be viably bonded to the cranium. Finite Element Analysis of the cranium is a potential route to testing hypotheses about the ontogenetic regulation of its bony anatomical features. Finite Element Analysis can estimate the distribution of strains throughout the cranium. If FEA were iteratively combined with an algorithm that mimics the adaptive response of bone it would be useful in assessing the extent to which observed ontogenetic changes might be explained in biomechanical terms alone. Inconsistencies between such a model and reality would be due to errors of modelling and other influences unaccounted for in the model (e.g. as genetic regulation, the hormonal environment, etc.). There have been significant advances in FEA [93–96] and Fig. 5 presents an example analysis from ongoing work in our laboratory where we are using FEA to adapt a model of a loaded face [97]. In the example we have applied rather unphysiological loads (because

Fig. 5. Adaptive finite elements analysis in which loading results in morphological transformation. A) Initial loading of a catarrhine cranium by compressing it in the vertical direction. B) Adapted model after several iterations of the algorithm (see text for details). The colors represent strain energy density as estimated by FEA with red representing high and blue low values.

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of current software constraints) to compress a 3D reconstruction of a cranium. On the right is the same model after a few iterations of the FEA combined with adaptive simulations of bone response. Its form has changed in a way that is consistent with improved bearing of such a compressive load. The approach seems useful in the context of analyses of facial loadings and ontogeny but there is work yet to be done in extending and developing the software tools before they are of practical use. 10. Conclusions Variations of the paranasal sinuses can cause problems for both patient and clinician. Their very variability is, however, a stimulus to the evolutionary anthropologist to consider more closely how they arise, how they are distributed among our ancestors and near relatives and how they may lead to deeper insights into craniofacial ontogeny. That they are so variable both in morphology and phylogeny implies that neither their form nor their disposition is intrinsically controlled during ontogeny. Rather they develop as a consequence of the preceding hierarchical integration, form and spatial relations of related modules. This is further supported by the numerous investigations of paranasal sinuses that have failed to identify any critical function. Indeed where a function can be ascribed it is invariably secondary (e.g. the effect on vocal resonance, lightening of the skull), it happens because the sinuses are there; the sinuses are not present because of the function. In this sense sinuses are like spandrels, the often ornate, triangular spaces found between arches. In churches, they serve no primary function but are there as a consequence of constructional constraints [98]. Their function is dependent on the spatiotemporal integration of other modules higher in hierarchy. This leads us to consider how the craniofacial region is constructed from a series of hierarchically integrated but to some degree autonomous modules or components. The integration of these components is hierarchical and occurs in both temporal and spatial dimensions. We have described how some recent developments in imaging, morphometrics and mechanical modelling have brought new tools to bear on the analysis of post natal craniofacial ontogeny. A study of longitudinal ontogenetic shape trajectories leads us to identify at around 6 years a critical change in the way in which the shape of the face changes with time. This seems likely to be a reflection of increasing integration between developing modules at this time. A second analysis using PLS demonstrates how these methods can also be applied to studying the integration and interaction between modules. The morphometric approaches combined with modern imaging have considerable potential to enhance studies of craniofacial evolution and development. They also offer an exciting prospect in assessing pathological ontogeny and the outcomes of medical interventions. With regard to understanding how mechanical forces impact on craniofacial ontogeny, including that of the sinuses, there are significant advances being made in modelling using FEA. In turn these may eventually contribute to prediction of ontogenetic trajectories, something that will be of use to craniofacial biologists and clinicians planning interventions to modify pathological trajectories. These developments require further refinement but for now there is clear value for the evolutionary anthropologist in taking a closer look at the peculiarities of morphology, such as sinus variability, that commonly affect us and our doctors.

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Acknowledgements We would like to thank the following colleagues who have helped in various ways—by discussing and debating the ideas and methodologies we present, providing data for analyses or supervising research that has led to results that are incorporated in this chapter: Antonio Rosas, Kazuto Kuroe, Jose Maria Bermudez de Castro, Dan Lieberman, Charles Oxnard, John Currey, Todd Rae, Thomas Koppe, Fred Spoor, Chris Dean, Theya Molleson, Fred Bookstein, Gu¨nter Bra¨uer, Christoph Groden, Thomas Schiemann, Andreas Pommert, Robin Crompton, Michael Fagan, Christian Langton, Roger Phillips, Catherine Dobson, Tim Bromage, Sam Cobb and Andrew Parker. We would also like to thank The Leverhulme Trust (UK) for supporting the finite element modelling work (and through this the post of KK), the Ministerio de Educacion y Ciencia (Spanish Ministry of Science; MEC) for supporting MB. We also thank the Fundacio´n Ramo´n Areces for its considerable efforts in supporting the symposium on Integrative Approaches to Human Health and Evolution from which this chapter arose. Of course the symposium and the opportunity to write this paper would have not arisen without the efforts of the coordinators: Timothy G. Bromage, Anxo Vidal, Emiliano Aguirre, and Alejandro Pe´rez-Ochoa, to whom we also extend our thanks. References [1] Schilling TF, Thorogood PV. Development and evolution of the vertebrate skull. In: O’Higgins P, Cohn M, editors. Vertebrate Ontogeny and Phylogeny: implications for the Study of Hominid Skeletal Evolution. San Diego7 Academic Press; 2000. p. 57 – 84. [2] Ridgway EB, Weiner HL. Skull deformities. Pediatr Clin North Am 2004;51:359 – 87. [3] Rae TC, Koppe T. Holes in the head: evolutionary interpretations of the paranasal sinuses in cattarhines. Evol Anthropol 2004;13:211 – 23. [4] Meyers RM, Valvassori G. Interpretation of anatomic variations of computed tomography scans of the sinuses: a surgeon’s perspective. Laryngoscope 1998;108:422 – 5. [5] Perez-Pinas, Sabate J, Carmona A, Catalina-Herrera CJ, Jimenez-Castellanos J. Anatomical variations in the human paranasal sinus region studied by CT. J Anat 2000;197:221 – 7. [6] Arslan H, Aydinlioglu A, Bozkurt M, Egeli E. Anatomic variations of the paranasal sinuses: CT examination for endoscopic sinus surgery. Auris Nasus Larynx 1999;26:39 – 48. [7] Kalavagunta S, Reddy KT. Extensive maxillary sinus pneumatization. Rhinology 2003;41:113 – 7. ¨ zturk M, Erkan M. Maxillary Sinus Aplasia. Turk J Med Sci 2002;32: [8] Baykara M, Erdoan N, O 273 – 5. [9] Cave A, Haines R. The paranasal sinuses of the anthropoid apes. J Anat 1940;74:493 – 523. [10] Blanton P, Biggs N. Eighteen hundred years of controversy: the paranasal sinuses. Am J Anat 1969;124:135 – 48. [11] Brothwell DR, Molleson T, Metreweli C. Radiological aspects of normal variation in earlier skeletons: an exploratory study. In: Brothwell DR, editor. The skeletal biology of earlier human populations. New York7 Pergamon Press; 1968. p. 149 – 72. [12] Buckland-Wright. A radiographic examination of frontal sinuses in early British Populations. Man (NS) 1970;5:512 – 7. [13] Schuller A. A note on the identification of skulls by X-ray pictures of the frontal sinuses. Med J Aust 1943;25:554 – 6. [14] Greene DL, Scott L. Congenital frontal sinus absence in the Wadi Halfa Mesolithic population. Man 1973;8:471 – 4.

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