Volume 297, Issue 11 p. 2121-2137
Special Article
Free Access

The Nasal Complex of Neanderthals: An Entry Portal to their Place in Human Ancestry

Samuel Márquez

Corresponding Author

Samuel Márquez

Department of Cell Biology, SUNY Downstate Medical Center, Brooklyn, New York

Department of Otolaryngology, SUNY Downstate Medical Center, Brooklyn, New York

Correspondence to: Samuel Márquez, Ph.D., Department of Cell Biology, SUNY Downstate Medical Center, 450 Clarkson Ave, Box 5, Brooklyn, NY 11203. E-mail: [email protected]Search for more papers by this author
Anthony S. Pagano

Anthony S. Pagano

Center for Anatomy and Functional Morphology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, New York

New York Consortium in Evolutionary Primatology (NYCEP), New York, New York

Department of Cell Biology, New York University School of Medicine, New York, New York

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Eric Delson

Eric Delson

New York Consortium in Evolutionary Primatology (NYCEP), New York, New York

Department of Anthropology, Lehman College and the Graduate School, City University of New York, New York

Department of Vertebrate Paleontology, American Museum of Natural History, New York, New York

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William Lawson

William Lawson

Department of Otolaryngology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, New York

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Jeffrey T. Laitman

Jeffrey T. Laitman

Center for Anatomy and Functional Morphology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, New York

New York Consortium in Evolutionary Primatology (NYCEP), New York, New York

Department of Otolaryngology, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, New York

Department of Medical Education, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, New York

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First published: 23 August 2014
Citations: 27

ABSTRACT

Neanderthals are one of the most intensely studied groups of extinct humans, as aspects of their phylogeny and functional morphology remain controversial. They have long been described as cold adapted but recent analyses of their nasal anatomy suggest that traits formerly considered adaptations may be the result of genetic drift. This study performs quantitative and qualitative analysis of aspects of the nasal complex (NC) in Neanderthals and other later Pleistocene fossils from Europe and Africa. A geographically diverse sample of modern human crania was used to establish an anatomical baseline for populations inhabiting cold and tropical climates. Nasofrontal angle, piriform aperture dimensions, and relative maxillary sinus volume were analyzed along with qualitative features of the piriform aperture rim. Results indicate that Neanderthals and other later Pleistocene Homo possessed NC's that align them with tropical modern humans. Thus comparison of Neanderthal nasal morphology with that of modern humans from cold climates may not be appropriate as differences in overall craniofacial architecture may constrain the narrowing of the piriform apertures in Neanderthals. They retain primitively long, low crania, large maxillary sinuses, and large piriform aperture area similar to mid-Pleistocene Homo specimens such as Petralona 1 and Kabwe 1. Adaptation to cold climate may have necessitated other adaptations such as bony medial projections at the piriform aperture rim and, potentially, midfacial prognathism. Nasal complex components of the upper respiratory tract remain a critical but poorly understood area that may yet offer novel insight into one of the greatest continuing controversies in paleoanthropology. Anat Rec, 297:2121–2137, 2014. © 2014 Wiley Periodicals, Inc.

The nose is a strategically placed “organ” that participates in a variety of important physiologic activities by serving as the entry portal of the upper respiratory system. The nose itself, apart from its function as an olfactory organ (but see Jankowski, 2011, 2013), plays a critical role in respiration as it prepares inspired air for the lungs by modifying its temperature, providing humidification and assisting in defense of its mucosa (Ewert, 1965; Cole, 1993). The nose, however, is not a single entity but rather comprised of a number of intricate structures that operate as a well-integrated functional unit during respiration (Márquez and Laitman, 2008; Márquez et al., 2014). Accordingly, the term nasal complex (Márquez et al., 1995, 2002, 2014; Márquez and Laitman, 2008) represents a morphophysiologic concept, which incorporates multiple components of the upper respiratory system. Among the factors contributing to this region's morphological and functional complexity are its osteocartilaginous framework, topographical orientation (e.g., Killian, 1903; Schaeffer, 1920; Patra et al., 1986), fluctuating intranasal pressures and gaseous composition (e.g., Suarez, 1952; Scharf, 1994; Mikula et al., 1995), the intricate morphology of the internal bony structures (Hillenius, 1992, 1994), and the different mucosal linings (e.g., stratified squamous, respiratory epithelium, transitional, and olfactory epithelium; Harkema, 1991; Harkema et al., 2006). The marked diversity of nasal shape among living human populations has long been considered a consequence of adaptation to a wide range of climatic conditions for optimizing respiratory heat and moisture exchange in the nasal mucosa, resulting in a rich history of study (Thomson and Buxton, 1923; Davies, 1932; Weiner, 1954; Negus, 1958; Wolpoff, 1968; Franciscus and Trinkaus, 1988; Yokley, 2009).

The nasal region of fossil crania has similarly received considerable attention with many studies attempting to reconstruct function and soft tissue anatomy (e.g., Coon, 1962). One particular fossil group, the Neanderthals, is considered the best known and most extensively studied but continues to perplex investigators (e.g., Trinkaus, 2006). Paleoanthropologists still debate the physiologic and evolutionary importance of aspects of their cranial morphology (e.g., Howell, 1952; Coon, 1962; Laitman et al., 1979; Wolpoff et al., 1981; Laitman and Heimbuch, 1982; Trinkaus, 1983, 1986, 1987, 1988, 2003, 2007; Rak, 1986; Demes, 1987; Smith and Paquette, 1989; Wolpoff, 1989; Stringer and Gamble, 1993; Antón, 1994; Laitman et al., 1996; Schwartz and Tattersall, 1996, 1999, 2010; Maureille and Houet, 1998; Franciscus, 1999, 2003; Schwartz et al., 1999, 2008; Rae et al., 2006; Holton and Franciscus, 2008; Tattersall and Schwartz, 2009; Holton et al., 2011; Clement et al., 2012). Among areas of debate are several components of the nasal complex, which have recently come under scrutiny (e.g., Rae et al., 2011; Holton et al. 2013). Selective forces may heavily influence each of these nasal structures as they together act as the primary means of conditioning inspired air. This requires modification to core body temperature and humidification to saturation before reaching the lungs to ensure proper cardiopulmonary function and maintain homeostasis (Negus, 1952, 1957). The physiological story of air-conditioning does not stop after inspiration but continues as expiratory air is passed subsequently through these same respiratory nasal passages, requiring that moisture be maintained in the membranes of the nasal walls, providing the opportunity for heat reclamation or dissipation to occur (Cole, 1993). It is thus likely that the specific form of the nasal complex was of great functional importance among the Neanderthals, who inhabited the cold, dry environments of later Middle Pleistocene-earlier Late Pleistocene Eurasia, and that it would have been subject to strong selective forces.

This study assesses the comparative morphology of the Neanderthal nasal complex relative to other later Pleistocene fossil hominins and a geographically diverse sample of contemporary humans. These data may permit placement of morphological variation among Neanderthals within an evolutionary context. We test for the presence of climatic adaptations using both quantitative and qualitative analyses of several nasal parametric traits. These external and internal measures include nasal bone orientation, nasal region indices and areas, maxillary sinus volumes and the medial bony projection character. Data from these different portions of the nasal complex may also aid in better defining the traits in which Neanderthals differ from modern humans.

This study quantitatively examined four craniofacial measures (i.e., 1—nasofrontal angle; 2—nasal index; 3—piriform aperture area; 4—maxillary sinus volume) and a qualitative character (i.e., the medial bony projection of Neanderthals residing within the internal nasal margin; see below). Each of these morphological parameters has been chosen to represent a different aspect of the nasal complex so that one may assess the manner in which its component structures are responding individually to climatic stresses. These measures were also chosen for their reproducibility and can be repeated on other samples to document patterns of diversity. A brief historical overview is offered for each of these measures so that the justification for its use can be placed in proper context.

BACKGROUND

Nasofrontal Angle

The nasofrontal angle (from glabella to nasion to rhinion) is a measure of nasal projection commonly used in forensic anthropology (Stephan et al., 2003; Rynn and Wilkinson, 2006; Anderson et al., 2008) and in otolaryngology during nasal reconstruction surgeries in cases involving trauma, pathology, and aesthetic rhinoplasty (e.g., Szychta et al., 2011; Webster et al., 1979; Milgrim et al., 1996). It is an important parameter of nasal profile evaluation in that it determines the visual projection of the nose from the face independent of the tip position (Mowlavi et al., 2004). Researchers have noted population differences in the nasofrontal angle and its relationship with soft tissue parameters, especially between Caucasian and non-Caucasian groups (e.g., Wang, 2003; Palma et al., 2003; Trenité, 2003). As Neanderthal faces have marked midfacial prognathism, an analysis of the nasofrontal angle might reveal similarities to some modern samples.

Nasal Index

The nasal index is arguably one of the most historically important anthropometric measures. Paul Broca formalized the definition of the nasal index in his classic work of 1872 as the maximum nasal breadth/nasal height × 100 (Broca, 1872), as one of several indices of the nasal and cranial region for classifying the various human population groups. The nasal index continues to be applied as a population-sensitive anthropometric index for distinguishing the geographic origin and sex of individuals whose identities are unknown (e.g., Oladipo et al., 2010; Eboh, 2011; Howale et al., 2012).

Holland (1902) reported on nasal index values of two groups of Kanet people living in distinct Indian habitats. He found the Kanets of Kullu, inhabiting the fertile valleys of the Punjab, presented a mean nasal index value of 74.1, while the Kanets of Lahoul, living along the barren sides of mountainous regions at an altitude of 10,000 feet, had a mean nasal index value of 66.4. These population differences could reflect physiologic adaptations, which arose in response to local climatic conditions, here manifested in the osteological construction of the nasal region (e.g., Franciscus and Long, 1991; Franciscus, 1995). Hrdlicka (1910) suggested that in Inuits a narrow nasal aperture was directly related to the effects of the Arctic cold, but he did not address the functional significance of this narrowing.

Piriform Aperture Area

The piriform aperture, considered the bony entry portal of the upper respiratory system, is the channel through which inspiratory and expiratory airflow must travel and whose air-conditioning process is under nervous system control (Cole, 1993). While the autonomic nervous system of the nasal cavity is intricate and not well understood (Nichani et al., 2010), there are now studies demonstrating the presence of different functional zones within the nasal mucosa (see Frasnelli et al., 2004; Scheibe et al., 2006) with the perception of chemosensory stimuli appearing to be most accurate in the anterior portion of the nasal fossa (Konstantinidis et al., 2010). In order for optimal nasal air conditioning function to be maintained, the width and stability of the osseous and cartilaginous nasal skeleton must be finely tuned to environmental ambient conditions (Hwang et al., 2005). Any disturbances to the soft or hard tissue anatomy of the region will have severe adverse effects on normal respiratory functioning and, ultimately, on survival. Studies have examined conformation of the fleshy nose to its osteological substrate and have reported population and sex differences (e.g., Schultz, 1918; Gower, 1923; Moreddu et al., 2013). Schmittbuhl et al. (1998) focused on piriform aperture morphology, concluding that its elongated shape in modern Homo sapiens may be a derived (apomorphic) feature. We include the piriform aperture area measure here to establish a modern human baseline of climatic variation against which the morphology of Neanderthals and other later Pleistocene hominins can be assessed.

Paranasal Sinuses

Although the processes and patterns of paranasal sinus pneumatization are not fully understood, the presence and extent to which these air-containing spaces invade the bony elements of the cranium has been an important consideration of hominoid phylogenetic analysis (Ward and Pilbeam, 1983; Begun, 1992; Arsuaga et al., 1997). Despite a long history of study, the function of the paranasal sinuses has remained elusive (Witmer, 1997; Rae and Koppe, 2004). In an effort to identify the exact role of the paranasal sinuses, investigators have examined various factors involved in the evolution of primate crania. Brain enlargement, facial and orbital orientation, basicranial flexion, tooth size and masticatory loads have all been considered, with the general conclusion that the observed differences in sinus morphology in various taxonomic groups cannot be explained by a single factor (Koppe et al., 1999). Although a general consensus is lacking as to the functional role of the paranasal sinuses, most investigators have taken one of three positions: (1) structural role; (2) evolutionary residual; or (3) physiological role. One proposal for the structural role function of paranasal sinuses was that they served as weight reducers of the skull for maintenance of equipoise of the head, but that was shown experimentally not to be the case (e.g., Biggs and Blanton, 1970). Others consider these special spaces of the skull as byproducts of facial growth, considering them as biological spandrels (e.g., Zollikofer et al., 2008). Still others contend that whatever role these sinuses may have played in evolutionary history, they no longer serve any function today and should be considered as excess baggage or evolutionary residuals (e.g., Márquez, 2008). Finally, other sinus researchers believe that the real function of these spaces may be related to the lower respiratory tract, playing a physiological rather than a structural role (e.g., Rae and Koppe, 2008). Recent physiologic studies of the paranasal sinuses have reaffirmed a non-structural explanation of sinus function (Lundberg et al., 1994, 1996; Lundberg and Alving, 1995), with some providing experimental evidence that the paranasal sinuses function as an integral element of an interactive mosaic of seemingly distinct anatomic units (Gannon et al., 1997). The discovery that the paranasal sinuses produce nitric oxide, a potent neurotransmitter with profound effects on the pulmonary vasculature and on tissue oxygenation, has altered the traditional explanations of sinus physiology (e.g., Sahin et al., 2011). The relative size of one or more sinuses (here we examine the maxillary) may provide information on the respiratory physiology of extant or extinct human groups.

Medial Projection

Schwartz and Tattersall (1996) reported a novel feature of the Neanderthal nose (as seen in Gibraltar 1), which they termed the medial projection and suggested to be an autapomorphic trait. They later (Schwartz et al., 1999, 2008) described this character state as a rim of raised bone that projects from the anterior nasal aperture (on both sides) just within its anterior edge and forms an internal secondary margin. The rim travels almost halfway up the inner nasal wall, where it expands and becomes “a wide, bluntly pointed mass that protrudes medially into the nasal cavity… fades superiorly into a low ridge that continues to frame the nasal cavity… and the vertical portion is bounded by an open lacrimal groove” (Schwartz and Tattersall, 1996, pg. 10852). The vertical portion is usually fully present only in adults. Others have questioned the validity of this character (e.g., Franciscus, 1999, 2003), with some claiming that medial projections have been observed in living human population groups (Wolpoff, 1999). We examined the Gibraltar 1 and Guattari 1 fossils to assess this feature.

MATERIALS AND METHODS

Both quantitative and qualitative analyses were undertaken, focusing on the nasal complex of dry crania of living and extinct humans. Quantitative measures include the nasofrontal angle, nasal index, piriform aperture area, and maxillary sinus volume, as detailed below. For each we used a different subset of dry crania selected from the human osteological collections at the Division of Anthropology at the American Museum of Natural History in New York (AMNH). Adult and subadult individuals were examined (as determined by the eruption of the third maxillary molar, and eruption of the second maxillary but not the third molar, respectively). Several human populations are represented in each sample; modern human crania represent a geographically diverse baseline against which Neanderthal morphology could be assessed. The Neanderthal fossils included here are Gibraltar Forbes' Quarry 1, Guattari 1, and Saccopastore 1. We also examined the geologically older crania Kabwe 1, Steinheim 1, Petralona 1 and Atapuerca 5 (studied from a cast). Many authors consider these fossils to represent Homo heidelbergensis, but that taxon is not consistently defined, so we prefer to use an informal term for this material. Following Wang (2011; see Athreya, 2007, for a slightly different concept) and also Xiao et al. (in press), we use the neutral term mid-Pleistocene Homo for specimens which are not readily identified as H. erectus, Neanderthal or modern human. This term is roughly equivalent to the outdated “archaic Homo sapiens,” but without its nomenclatural baggage.

Nasofrontal Angle

Material

The modern mixed-sex sample (Sample 1) of 130 includes individuals from: Alaska (n = 24), Northern Europe (n = 15), Southern Europe (n = 16), North Africa (n = 15), East Africa (n = 14), West Africa (n = 17), China (n = 10), and South East Asia (n = 19).

Method

Coordinate data for three craniofacial landmarks (glabella, nasion, and rhinion) were digitized using a Microscribe G2 digitizer on extant and extinct material. The nasofrontal angle was calculated from inter-landmark distances using the cosine rule: [Cos (γ) = (a2+b2−c2)/2ab] (see Fig. 1). The values for each human population group were contrasted via pairwise Student's T tests (with unadjusted Bonferroni Correction).

Details are in the caption following the image

A modern human cranium in frontal (A) and lateral (B) view demonstrating the locations of the landmarks comprising the nasofrontal angle and the lines intersecting them. The nasofrontal angle is measured at the intersection of the rhinion-nasion and nasion-glabella lines, representing the angulation of the nasal bones relative to the frontal bone. It has been used to quantify nasal projection among contemporary human populations in both anthropological and clinical contexts. Courtesy of the Division of Anthropology, AMNH.

Nasal Index, Piriform Aperture Area, and Maxillary Sinus Volume

Material

A mixed-sex sample (Sample 2) of 48 dry crania was used to assess the nasal index, piriform aperture, and maxillary sinus morphology. Populations represented include: Alaska (n = 14), Northern Europe (n = 15), East Africa (n = 8), West Africa (n = 2), and South Africa (n = 9) (see Fig. 2).

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Crania representing populations from cold climates (A–C) and warm climates (D–F) demonstrating different piriform aperture morphologies. Populations from cold climates exhibit tall, narrow piriform apertures while those from tropical climates exhibit short, broad piriform apertures. Note: The cold climate crania include (from left to right): Northern European (a; VL 193), Alaskan Inuit (b; 99/1476), and Northern European (C; VL 1466) individuals. The warm climate crania (from left to right) include: West African (D; VL 1921), San (E; 99/76), and West African (F; VL 2472) individuals. Courtesy of the Division of Anthropology, AMNH.

Methods

Nasal index was calculated as: (nasal width/nasal height) × 100. Nasal width (measured from alare to alare) is instrumentally determined, finding the maximum width at a right angle to nasal height (Hrdlicka, 1920). Nasal height is traditionally measured from the superior craniometric point of nasion to the base of the anterior nasal spine, or inferiorly to the middle of a line connecting the lowest points of the two nasal fossa (Hrdlicka, 1920). If instead of a border there is a gutter encountered, the measurement should be at the upper limiting line of the gutters (Hrdlicka, 1920). The technique employed here was to measure from nasion to the two separate lowest points of each piriform nasal fossa and record the mean (Hrdlicka, 1920). The modern human crania were measured with electronic calipers (i.e., Mitutoyo 500 series, 196-20 Absolute digimatic digital caliper with an accuracy to 0.02 mm) while the nasal width and height of fossil crania were quantified via three-dimensional landmark coordinate data (inter-landmark distance).

Piriform aperture areas were quantified for human dry crania and human fossils. For the human dry crania, a scale bar was placed at the root of the nose approximating the rhinion–anterior nasal spine plane of the piriform aperture. A digital photo was taken with a SONY DSL D200 camera fixed perpendicular to the rhinion–anterior nasal spine line. Piriform aperture areas were determined using ImageJ software, by outline tracing the aperture and determining area using a reference scale in the photo. The lateral edge of the piriform aperture is not planar but undulates in and out, making the area an estimated value. Notwithstanding this limitation, piriform aperture area does provide an approximate measure of the space through which inspiratory and expiratory airflow must travel. This airflow does not pass directly through the pear shaped opening at a perpendicular angle but rather follows certain trajectory patterns with specific channels and eddies constrained by nasal cavity structures (see Churchill et al., 2004 for review).

Piriform aperture areas for the fossils Gibraltar (Forbes' Quarry 1), Guattari 1 and Kabwe 1 were also calculated using ImageJ. The distance from rhinion to anterior nasal spine determined from 3D coordinate data (collected by A.S.P.) allowed scaling for area determination (i.e., distances between known points on the image were used to scale area from pixels to square centimeters).

Maxillary sinus volume determination on the human crania, Gibraltar Forbes Quarry 1 and Kabwe 1 fossils was conducted using the seed-filling method (Fig. 3). Data for the Guattari 1 (Monte Circeo) left maxillary sinus volume is reported in Rae et al. (2011).

Details are in the caption following the image

The Gibraltar Forbes' Quarry 1 and Kabwe 1 fossil specimens had their maxillary sinuses measured via the seed filling technique. The left maxillary sinus of Gibraltar and Kabwe's right maxillary sinus were filled with seeds and completely packed, which can be seen through the broken orbital floor of Kabwe shown above. The weight of the seeds was transformed to a volumetric measure by a regression formula.

The protocol for establishing maxillary sinus and endocranial volumes for this study has been reported in Márquez and Laitman (2008). Volume measurements on the modern human sample were obtained by the use of oil rapeseeds, chosen due to their small size and superior packing qualities. Other workers have used a similar technique for sinus volume determination (e.g., Shea, 1977). With each cranium positioned on its side, the seeds were introduced into the maxillary sinus via a funnel placed either through the choana or piriform aperture. Continual gentle tapping of the cranium was done throughout the filling process in order to ensure that the seeds packed and settled. Any seeds projecting through the opening of the medial wall of the maxillary sinus were leveled off and removed through the piriform aperture. Transillumination was required to confirm the complete filling of the sinus. Crania were weighed with a Sartorius scale (with an accuracy to 0.1 g) before and after seed-filling so the difference obtained represented the weight of the seeds alone. Data for weight (in grams) was then transformed to a volumetric measurement (in milliliters) by linear regression. Filling the cranium with seeds through the foramen magnum and then depositing the seeds into a graduated cylinder was the technique used to obtain endocranial volumes.

Medial Projection

Material

The nasal cavity was examined for presence of a medial projection in the combined adult modern samples 1 and 2, as well as sample 3 of 70 subadults from the AMNH collection, which showed eruption of second maxillary molar with third maxillary molars not fully erupted. Fossils examined were Gibraltar Forbes' Quarry 1, Guattari 1, Kabwe 1, Steinheim 1 and Petralona 1.

Method

The medial bony projection is identified by the combined presence of the following characters: (1) a pyramidally shaped swelling of bone intruding medially (in the coronal plane) into the nasal cavity; (2) a vertical strut of bone distinct from the maxilloturbinal; and (3) a prenasal fossa spanning the distance between the vertical strut of bone and the rim of the piriform aperture. Each specimen was scored for presence or absence.

Size Standardization and Statistical Methods

Endocranial volume was used to normalize all measures in this study, as this measure has been historically used to standardize measures to body/skull size differences and evaluated by a number of investigators (e.g., Bauchot and Stephan, 1969; Martin, 1993). Size standardization of linear measurements was undertaken by dividing each measurement by the cube root of endocranial volume. In the case of piriform aperture areas, the square root of this measure was divided by the cube root of endocranial volume. Maxillary sinus volume is directly divided by endocranial volume for each specimen as both measures are expressed in cubic centimeters. Standardizing measurements in this way transforms them into units that are comparable statistically. Some measures were also normalized with cranial (prosthion-opisthocranion) length.

Wilcoxon rank tests were used to compare modern human groups, and the Bonferroni adjustment was utilized. This method provides a conservative critical value for P relative to others such as the Sidak–Bonferroni, or Tukey–Kramer. As a further post hoc test, bootstrap resampling was performed. Once differences (or lack thereof) were identified, Z scores were calculated for each fossil relative to each modern human group.

RESULTS

Nasofrontal Angle

The nasofrontal angles of Northern and Southern European crania were significantly (P < 0.05) different from every other human group except North Africans and Southeast Asians, which in turn, were not significantly (P < 0.05) different from any other human population group (Figs. 4 and 5). Despite being a cold climate population, the Inuit were not significantly (P < 0.05) different from any human groups other than the Northern and Southern Europeans. The two “classic” Neanderthals (Guattari 1 and Gibraltar Forbes' Quarry 1) were within the ranges of all the human populations while Saccopastore 1 exhibited a nasofrontal angle greater than the maximum values of all populations except East Africans and North Africans, on which it overlapped the highest respective values. Most European and African mid-Pleistocene Homo (Kabwe, Steinheim, Petralona) were within the range of all human populations, but Atapuerca 5 exhibited an angle greater than the maximum Northern European value. Summary statistics for Sample 1 are shown in Table 1.

Details are in the caption following the image

The raw nasofrontal angle values among various human populations from sample 1 are shown. Note that each “+” represents the value derived from an individual cranium. Nasofrontal angle tends to distinguish the Northern and Southern European crania from all other populations except North Africans. This pattern is likely related to differences in external nasal projection in life.

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A box-whisker plot of nasofrontal angle values among several modern human populations and fossil crania. The fossils appear to span the full range of modern human morphology from extremely acute to obtuse angles. Petralona (P) was the lowest (falling at the low end of the European distribution), and Sacopastore 1 (Sa) was the highest value, falling at the upper limit of the East African sample. Other fossil crania (Atapuerca 5, A; Kabwe, K, Guattari, G, and Steinheim, St) overlap with many modern populations.

Table 1. Summary statistics for the nasofrontal angle measure in sample 1
Sample size Minimum value Maximum value Mean Standard deviation
Alaskan 24 123.60 154.40 143.45 7.98
Chinese 10 139.14 156.29 144.52 5.00
South East Asian 19 124.71 147.44 138.67 6.25
Northern European 15 117.35 141.72 130.84 7.93
Southern European 16 118.95 144.66 132.87 6.51
North African 15 116.46 170.32 140.66 14.43
West African 17 130.42 156.94 146.13 7.765
East African 14 129.39 173.283 148.37 11.90
  • Note that the North African sub-sample exhibits the highest standard deviation, likely as a result of greater variability in this measure.

Nasal Index

The nasal index was significantly lower (P < 0.05) among the European and Alaskan crania than the African specimens (Fig. 6). The latter group had values between 47.8 and 69.8 while the former ranged between 38.0 and 59.8 (Summary statistics for Sample 2 are shown in Table 2). The values of the European mid-Pleistocene Homo were within the African range, while Kabwe and Petralona overlapped the higher north European values. The Gibraltar Forbes' Quarry 1 Neanderthal cranium fell at the upper end of the African range, while Guattari 1 and Saccopastore 1 had values close to the overlap zone of all extant populations.

Details are in the caption following the image

The nasal index values from the population groups of sample 2 are represented in a box-whisker plot. Note that the “+” represents the mean and the vertical lines of the box represent (from bottom up) the 25th, 50th, and 75th quartiles. The upper- and lower-most whisker edges represented the maximum and minimum values, respectively. The fossils represented here are Atapuerca 5 (A), Gibraltar Forbes' Quarry 1 (F), Kabwe 1 (K), Saccopastore 1 (Sa), Petralona (P), Steinheim 1 (St), and Guattari 1 (G). Most of the fossil crania fall well within the African range of variation with Gibraltar Forbes' Quarry 1 and Steinheim 1 plotting at the upper range of the African sample exceeding all but two tropical African individuals.

Table 2. Summary statistics for nasal index in sample 2
Sample size Minimum value Maximum value Mean Standard deviation
Northern European 15 39.71 59.77 48.22 5.66
Alaskan 14 38.03 50.73 45.55 4.00
South African 9 47.78 64.86 57.25 5.45
Tropical African 10 53.69 69.80 58.58 5.79
  • Note the large difference in means among the cold climate groups (Northern Europeans and Alaskans) and the warm climate groups (South and tropical Africa).

Piriform Aperture Area and Maxillary Sinus Volume

Scaling measures

The cube root of endocranial volume and prosthion-opisthocranion lengths were both used to scale maxillary sinus volume (its cube root) and piriform aperture area (its square root). Prosthion-opisthocranion length was moderately and significantly (P < 0.05) correlated with maxillary sinus volume (r = 0.465; P = 0.000863) and piriform aperture area (r = 0.648; P < 0.0001) whereas endocranial capacity was not significantly (P > 0.05) correlated with either nasal complex measure. It thus appears that endocranial volume is more appropriate for size standardization due to the non-significance of its respective correlations with maxillary sinus volume and piriform aperture area (Fig. 7).

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Two crania in superior view demonstrating population differences in vault shape. On the left is a dolichocephalic West African cranium (VL 1921) and on the right is a brachycephalic Northern European cranium (VL 3560). Endocranial capacity and cranial length are the two most commonly used measures for size standardization. This figure illustrates a potential disadvantage of scaling nasal measures against cranial length in that two specimens with similar endocranial capacity can express markedly different cranial lengths, thus impacting quantification of nasal morphology. Courtesy of the Division of Anthropology, AMNH.

The piriform aperture and maxillary sinus dimensions exhibited no significant (P < 0.05) difference among population groups when scaled by cranial length (Figs. 8 and 9). When scaled by endocranial capacity, piriform aperture area (K–W P < 0.001) and maxillary sinus volume (K-W P = 0.002) revealed statistically significant differences of distribution across populations (Figs. 10 and 11; for summary statistics of Sample 2, see Tables 3 and 4). Two of the 10 sub-Saharan African specimens (VL/408 & VL/3272) are clearly outliers in terms of relative maxillary sinus volume (see Fig. 11): with these observations excluded, the K–W P value for that measure is <0.001. Overall, relative values for maxillary sinus volume and piriform aperture area tend to be higher among the African groups, but there is no significant difference (P < 0.05) between the South African and Northern European samples.

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Distribution of values for piriform aperture area (its square root) scaled over prosthion-opisthocranion (cranial) length among populations from cold and warm climates. The data are presented in a box-whisker plot. Note that scaling over cranial length failed to significantly (P < 0.05) distinguish human groups from cold and warm climates in a Wilcoxon Rank test with bootstrap resampling.

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Distribution of values for maxillary sinus volume (its cube root) scaled over prosthion-opisthocranion (cranial) length among populations from cold and warm climates. The data are presented in a box-whisker plot. Scaling maxillary sinus volume over cranial length did not result in any significant (P < 0.05) group differences in a Wilcoxon Rank test with bootstrap resampling.

Details are in the caption following the image

Distribution of values for piriform aperture area (its square root) scaled over the cube root of endocranial volume among populations from cold and warm climates. The data are presented in a box-whisker plot. This measure distinguished human populations from warm and cold climates while also distinguishing Neanderthals from most modern human groups. The Neanderthal specimen with the lowest value (Saccopastore 1; Sa) overlapped modern Europeans at their extreme range but was close to the tropical African mean. The Gibraltar Forbes' Quarry 1 cranium (F) overlapped with the highest tropical African values, while Guattari 1 (G) exceeded all sampled humans. The other fossils (K, Kabwe; S, Steinheim; P, Petralona; A, Arago), which are typically assigned to Homo heidelbergensis, all fall within the range of Neanderthals.

Table 3. Summary statistics for scaled piriform aperture area (square root of this value scaled over the cube root of endocranial volume) in sample 2
Sample size Minimum value Maximum value Mean Standard deviation
Northern European 15 0.19 0.26 0.23 0.02
Alaskan 14 0.20 0.25 0.22 0.01
South African 9 0.23 0.28 0.25 0.02
Tropical African 10 0.24 0.29 0.26 0.01
  • Note that the tropical African sub-sample exhibited the highest mean value and the Alaskan sample exhibited the lowest.
Table 4. Summary statistics for maxillary sinus volume scaled over endocranial volume in sample 2
Sample size Minimum value Maximum value Mean Standard deviation
Northern European 15 0.27 0.28 0.25 0.02
Alaskan 14 0.19 0.28 0.24 0.02
South African 9 0.24 0.31 0.28 0.02
Tropical African 10 0.24 0.34 0.29 0.03
  • Note that the tropical African sub-sample exhibited the highest mean value while the lowest was the Alaskan sub-sample.
Details are in the caption following the image

Distribution of values for maxillary sinus volume scaled over endocranial volume among populations from cold and warm climates. The data are presented in a box-whisker plot. This measure significantly (P < 0.05) distinguished cold and warm climate human populations while the Neanderthals ranged from nearly overlapping the tropical African mean (Gibraltar Forbes' Quarry 1, F) to exceeding all modern humans sampled (Guattari 1, G). Kabwe (K) is intermediate between the two fossils, exhibiting sinus volume that overlapped tropical Africans at their extreme upper range.

With respect to scaled piriform aperture area, the later or “classic” Neanderthals (Gibraltar and Guattari) were completely above the range of any modern human group while the earlier Saccopastore 1 was under a single standard deviation from the respective tropical African and South African means. European mid-Pleistocene Homo also exhibited this pattern of diversity, whereby the Petralona and Atapuerca 5 crania were above the range of all modern humans, and Steinheim 1 was below one standard deviation from the tropical African and South African means. The Kabwe cranium also overlapped with the African sample, but was outside the range of the Europeans and Alaskans.

The scaled maxillary sinus size of Gibraltar Forbes' Quarry 1 exceeded the maximum values for the Northern Europeans and Alaskans, falling 1.821 and 1.45 standard deviations from their means, respectively. Guattari 1 exceeded the maximum values of all the groups and was 2.69 standard deviations above the tropical African mean. The Kabwe cranium exceeded the maximum values of the European, Alaskan, and South African groups, falling at the periphery of the tropical African group (exceeded only by the maximum value) at 1.48 standard deviations above its mean.

For a summary of the values for each of the above measures calculated for the fossils, see Table 5.

Table 5. Values of the fossil specimens for each measure used in this study
Specimen Nasofrontal angle Nasal index Scaled piriform aperture area Scaled maxillary sinus volume
Kabwe 1 139.14 52.75 0.28 0.34
Petralona 1 125.78 58.31 0.32 N/A
Atapuerca 5 (cast) 144.76 63.38 0.29 N/A
Steinheim 1 134.69 67.89 0.26 N/A
Gibraltar Forbes' Quarry 1 134.35 66.64 0.29 0.28
Guattari 1 139.19 51.72 0.32 0.37
Saccopastore 1 160.41 47.61 0.26 N/A
  • Note that the fossils express marked variability in nasofrontal angle and nasal index but are all consistently higher than modern human mean values in scaled piriform aperture area (square root of this value scaled over the cube root of endocranial volume) and scaled maxillary sinus volume (scaled over endocranial volume).

Medial Projection

Gibraltar Forbes' Quarry 1 and Guattari 1 were the “classic” Neanderthal fossils examined for a medial projection. The Gibraltar specimen was found to exhibit all three of the components defining a medial projection. Additionally, an internal secondary crest of bone was found within the piriform aperture, situated posterior to the anterior rim of the nasal fossa. This secondary internal crest originates from the floor of the nasal aperture near the anterior nasal spine, where it begins to course in a lateral direction, forming a prenasal fossa. Upon reaching the lateral border of the piriform aperture, the internal secondary crest rises superiorly in the coronal plane, where it melds into a medially projected process, or medial projection (hereafter termed MP). Visualizing the MP as pyramidal in shape, its base is confluent with the lateral wall of the nasal cavity, while the apex projects medially towards the midline. The inferior portion of the base is continuous with the internal secondary crest, while its superior portion continues to rise toward the orbit. Most of the posterior side of the base broadens in the parasagittal plane, particularly its superior portion, as it becomes confluent with the lateral wall of the piriform aperture. When viewing Gibraltar 1 from an anteroposterior perspective (in the Frankfurt Horizontal plane), the most superior portion of the MP base follows along the lateral internal portion of the frontal process of the maxilla, where it continues to rise well above the level of the inferior orbital rim (Fig. 12).

Details are in the caption following the image

(a) The Gibraltar Forbes' Quarry 1 external nasal aperture demonstrates the pyramidal shape of the medial projection (MP) with an apex extending medially toward the midline of the nasal aperture. The prenasal fossa and secondary internal nasal crest are also clearly visible. Note that the medial projection and prenasal fossa in Gibraltar 1 are expressed bilaterally. (b) Gibraltar 1 also exhibits an inferior border of the MP base that is continuous with the secondary internal crest.

For the Guattari 1 cranium, medial projections are visible from both sides in frontal view with the right being better preserved. This specimen exhibits a vertical strut of bone that projects medially into the nasal cavity and is continuous with a broken medial projection, with the superior- and anterior-most extent of the prenasal fossa still preserved between these structures and the piriform aperture rim (Fig. 13). Despite some damage to the anterior nasal wall and floor, it appears that Guattari 1 exhibited all three of the components defining an MP.

Details are in the caption following the image

The Guattari 1 cranium in oblique (A), frontal (B), and close-up oblique (C) views. Medial projections are visible on both sides in frontal view (A). Despite extensive damage to the right side of the face and erosion of the maxillae, the right piriform aperture margin and nasal fossa are better preserved than on the left side (white circle on left MP) (B). This specimen exhibits a vertical strut of bone that projects medially into the nasal cavity (whose broken apex is indicated by white arrow) and posteriorly bounds the nasal fossa (C). Photograph (A) copyright, © Jeffrey H. Schwartz, reproduced with permission; Photographs (B and C) copyright, © Anthony S. Pagano.

The Petralona 1 and Kabwe 1 fossil crania were examined for the presence of a medial projection. Despite a diminutive prenasal fossa in Kabwe 1, neither individual exhibited a well-expressed or incipient medial projection. Additionally, all three traits were absent among all the adult and subadult samples of the contemporary human crania used in this study. Despite exhibiting a wide range of piriform aperture morphology, none approached the medial projection condition found in our Neanderthal sample. Thus, all non-Neanderthal specimens were characterized by a sharp, uninflated lateral piriform margin as well as the absence of a vertical strut of bone associated with a medial bony projection.

DISCUSSION

Neanderthal Morphometric Results

Our results offer an overview of the Neanderthal nasal complex and insight into the morpho-physiologic nature of its components.

Nasofrontal Angle

Most of the contemporary human populations exhibited obtuse nasofrontal angles with the exception of the Europeans, which has been noted often in clinical studies (e.g., Romo and Abraham, 2003; Trenité, 2003; Wang, 2003). Additionally, the nasofrontal angle did not distinguish Neanderthals from any living population. Some, such as Gibraltar Forbes' Quarry 1 and Guattari 1, were close to the European mean value, while Saccopastore 1 was at the upper range of East Africans and exceeded the West Africans. Other later Pleistocene fossils also exhibited a wide range of morphologies with Atapuerca 5 falling close to the West African mean and Petralona falling among the most acutely angled European crania. This measure appears polymorphic among the fossil crania and is likely not related to climatic adaptation.

Nasal Index

The classic nasal index measure distinguishes modern humans ecogeographically while all European mid-Pleistocene Homo plotted among tropical and South African modern human crania. Kabwe 1 plotted at the lower range of modern South Africans and at the upper range of Northern Europeans despite its extremely short, broad piriform aperture. Nasal index values for the Neanderthals showed Gibraltar Forbes' Quarry 1 plotting at the upper periphery of the tropical African group, while Guattari 1 and Saccopastore 1 overlapped the range of living Europeans and South Africans. This variation in nasal index suggests that Neanderthals consistently exhibited relatively great nasal breadth but varied in the vertical distance between nasion and nasospinale. The low value of Kabwe 1 may also be attributable to its relatively great nasal bone length despite its apparently tropical piriform aperture shape. Such a pattern may be related to a different set of functional demands interacting with vertical height of the nasal cavity among the fossil crania than is true for modern humans.

Piriform Aperture

Comparison of human groups from cold and warm climates clearly illustrates piriform aperture area differences. This, in turn, may reflect adaptations that serve as a protective mechanism for the respiratory mucosa, the primary modifier of inspired air. Population differences in piriform aperture area were significant (P < 0.05) when scaled by endocranial volume but not cranial length (prosthion-opisthocranion distance). This latter measure may not be ideal for size standardization as it is moderately correlated with piriform aperture area and may not be an independent size metric. The prosthion-opisthocranion length may also be confounded by population differences in cranial length (i.e., brachycephalic crania occurring in higher frequencies among cold climates and dolichocephalic crania being more frequent in tropical climates) irrespective of endocranial volume. Indeed, a weak correlation (r = 0.39; P = 0.006) was found between the two measures. Additionally, Neanderthals and other later Pleistocene Homo exhibit long, low cranial vaults and greater prognathism relative to modern humans, potentially confounding measures scaled with prosthion-opisthocranion distance. Endocranial volume thus appeared a more reliable scaling factor, as it was not directly affected by neurocranial or facial shape. The quantitative data on the Neanderthal specimens did not ally them with modern human populations from cold climates. They instead resembled humans from warm, tropical climates in nearly all nasal dimensions and often exceeded the dimensions of living tropical Africans. This has led some to hypothesize that the cranial shape differences between Neanderthals and modern humans were not the result of cold adaptation but rather due to genetic drift (Weaver et al., 2007).

Maxillary Sinus Volume

The two Neanderthals studied (Gibraltar Forbes' Quarry 1 and Guattari 1) exhibited large relative maxillary sinus volumes compared to the modern human sample. The Gibraltar specimen is close (under one standard deviation) to the respective mean values of the tropical and South African groups and plots at the periphery of the European range but outside the Alaskan range. Guattari 1, however, exceeds the entire contemporary human sample. The maxillary sinus measure does distinguish among the contemporary population groups, sorting them by ecogeographic regions corroborating the results of Szilvássy et al. (1987) who stated they were able to sort population samples into Europeans, Asians and Africans on the basis of metric and sinus morphology.

These observations may shed some light into Neanderthal sinonasal and respiratory physiology. The relatively large sinuses of Neanderthals may have permitted greater quantities of nitric oxide (NO) production within the endothelial cells that line the paranasal sinus mucosa than are typically produced by modern Europeans and Alaskans. Recent physiologic and molecular studies have identified the paranasal sinuses as a prime site for the production of NO (e.g., Lundberg, 1995) and may also function as reservoirs for NO (Andersson et al., 2002). Lundberg (2008) demonstrated that NO acts as an aerocrine messenger between the upper and lower airways and may selectively reverse hypoxic pulmonary vasoconstriction without causing systemic vasodilation (Fig. 14). This type of respiratory physiology would have been ideal for the physiologic demands imposed by the hyperactive behavioral regime of Neanderthals as suggested by Berger and Trinkaus (1995). As NO production has been related to energy levels, it is possible that the potentially higher gas production in Neanderthals similarly reflects extensive respiratory activity, facilitating greater cardiopulmonary efficiency to supplement the estimated 3360 to 4480 kcal per day expenditure to support strenuous foraging strategies and cold resistance costs (Steegman et al., 2002). In an elegant “natural” experiment design, Beall et al. (2001) compared two far removed high altitude populations to a low-altitude reference sample and found the former groups to exhibit more than twice the NO levels than the latter group. The possible physiologic impact of the observed high NO concentration levels in the high altitude group may be to offset the ambient hypoxia by enhancing the uptake of oxygen from the lungs, with improved delivery to peripheral tissues (Beall et al., 2001). Such a physiologic mechanism may have benefited Neanderthals while actively hunting in seasonally cold habitats (e.g., Niven et al., 2012).

Details are in the caption following the image

Illustration showing nitric oxide gas production from the maxillary sinus. During inhalation, the gas is mixed with ambient air and transported to the lower respiratory tract (copyright, © Samuel Márquez).

Medial Projection

Both of the Neanderthal fossils used in this study exhibit clearly defined medial projections, corroborating the observations of Schwartz and Tattersall (1996, 2002; Schwartz et al., 1999, 2008). Physiologically, the MP may serve to increase the surface area available for the critical respiratory mucosa in the nasal cavity. It may have reduced the traumatic effect of cold air on the nasal mucosa by occupying a strategic location for receiving the initial impact of inspiratory airflow (Laitman et al., 1996). As observed by Keck et al. (2009), the majority of inspiratory heat and moisture exchange occurs in the anterior portion of the nasal cavity. Additionally, the medial projection could promote airflow turbulence on expiration, aiding in moisture retention and safeguarding against dehydration in cold, dry conditions. Such a function would supplement the role of the nasal conchae (e.g., Hillenius and Ruben, 2004).

Some of the strongest evidence in support of the autapomorphic nature of the Neanderthal MP may lie in its early presence among non-adult specimens. The examination of both modern human subadult material (upper third molar not erupted, n = 70) and non-adult Neanderthal specimens such as Roc de Marsal and Subalyuk 2 (e.g., Schwartz and Tattersall, 2002) suggests that Neanderthals developed medial swellings early in their ontogeny, while modern humans never exhibit this peculiar nasal anatomy at any stage of development. This evidence suggests that the growth trajectory of the modern human nasal complex is clearly distinct from that of Neanderthals. Taken together, the comparative anatomy and the developmental evidence strongly indicate that the Neanderthal internal nasal region is highly autapomorphic.

What does the Neanderthal Nose Know?

As the nose is the entry portal of the upper respiratory system so too may the Neanderthal nose be an entry portal to understanding their evolutionary trajectory. For example, focused comparisons of Neanderthals to modern human groups from cold, dry climates may not be appropriate as the dimensions of NC components may have an idiosyncratic functional importance in Neanderthals. Modern human populations exhibit climatic signatures associated with their ecogeographic provenance, which likely evolved independently along distinctive adaptive pathways (Hubbe et al., 2009). For example, cold-living populations from North America exhibit narrowing of the piriform aperture while Northern Europeans exhibit nasal projection in addition to tall, narrow piriform apertures (Hubbe et al., 2009). A lack of piriform aperture narrowing among Neanderthals does not necessarily indicate a lack of cold adaptation. Rather, their morphologic suite of overall nasal features may reflect a distinctive species-specific adaptation to cold that differed from the adaptive, respiratory modifications taken by present day humans.

Neanderthals differ from modern humans in a broad array of craniofacial features, rendering a different template upon which cold adaptation may act. The retention of the ancestral condition in Neanderthals of long, low crania and midfacial prognathism would suggest a different set of functional relationships involved in their evolutionary history than the modern human condition of a globular cranium with facial orthognathy. Indeed, a narrow, prognathic midface as in Neanderthals may require an inferiorly oriented, broad piriform aperture as a matter of biomechanical stability. Holton and Franciscus (2008) argue that piriform aperture dimensions share a close relationship with overall upper respiratory tract length (estimated as prosthion-basion distance), which is relatively longer among Neanderthals. Modern humans who lack this extreme prognathism and exhibit anteroposteriorly short upper respiratory tracts may permit a greater malleability in piriform aperture shape and orientation. This may also account for the similarities among Neanderthals and the specimens of mid-Pleistocene Homo in relative measures of piriform aperture area, sinus volume, and nasal index, suggesting the persistence of an ancestral morphology (which overlaps some of the warm-climate modern African samples). Taken together, Neanderthals' wide nasal breadths, large piriform aperture, uniquely derived bony medial projection and extensive paranasal sinus pneumatization suggest that they developed this suite of features while on a separate evolutionary trajectory from that of modern humans (Fig. 15).

Details are in the caption following the image

A hypothetical 3D model reconstruction of the Neanderthal nasal complex. The impressive armamentarium of this specialized upper respiratory apparatus was probably highly responsive to the environmentally challenging conditions during the Late Pleistocene cold intervals. Note, the MP is strategically positioned to confront the plume of cold air preparing the air for warming before it is mixed with nitric oxide gas, but causing turbulence during expiration for heat reclamation. (copyright©, Samuel Márquez).

Our findings suggest that it may be better not to regard the autapomorphic nasal complex of the Neanderthals—large noses, expansive sinuses, and medially projecting bony structures—as a single unit linked together through evolution, but rather as a set of anatomically related structures responsive to different stimuli. Still, the unique Neanderthal nasal complex functioned as a unit and was highly successful for a long time. Clearly it did not finally disappear, taking its subassemblies with it, because it (or any of its components) was adaptively inferior to its counterpart in Homo sapiens. It was Homo neanderthalensis as a whole that succumbed in the competition for ecological space with the newly arrived Homo sapiens.

ACKNOWLEDGEMENTS

The authors thank Blaire Van Valkenburgh, Timothy D. Smith and Brent Craven, guest editors of the special issue on the Vertebrate Nose: Evolution, Structure and Function, for inviting them to participate. They are excited to be part of an important special issue. They are indebted to Brent for his helpful suggestions and patience as “supervisor” to the manuscript. They also appreciate the thoughtful suggestions of the anonymous reviewers who greatly enhanced the focus of the report. They also recognize two individuals from SUNY Downstate Medical Center: Dr. Jeremy Weadon of Academic Computing for statistical suggestions and Mr. Vincent Garofalo of the Department of Cell Biology Media Lab for assistance in the preparation of the images and graphic design. Finally, they thank the following people who allowed access to the specimens used in this study: George D. Koufos, Department of Geology and Physical Geography, Laboratory of Geology and Palaeontology, Aristotle University of Thessaloniki, Greece; Luca Bondioli, Museo Nazionale Preistorico Etnografico Luigi Pigorini, Rome, Italy; Reinhard Ziegler, Staatliches Museum für Naturkunde, Stuttgart, Germany; Christopher B Stringer and Robert Kruszynski, Department of Paleontology, Natural History Museum, London, England; and Gisselle Garcia, Division of Anthropology, American Museum of Natural History, New York, USA.