Internal nasal floor configuration in Homo with special reference to the evolution of Neandertal facial form

Journal of Human Evolution 44 (2003) 701–729

Internal nasal floor configuration in Homo with special reference to the evolution of Neandertal facial form Robert G. Franciscus Department of Anthropology & The Neuroscience Graduate Program, 114 Macbride Hall, University of Iowa, Iowa City, IA 52242 USA Received 16 May 2002; accepted 7 April 2003

Abstract The presence of a steeply sloping or depressed nasal floor within the nasal cavity of Neandertals is frequently mentioned as a likely specialization or autapomorphy. The depressed nasal floor has also been seen as contributing to a relatively more capacious nasal cavity in Neandertals, which is tied to cold-climate respiratory adaptation and energetics. These observations have been limited largely to a relatively few intact crania, and the character states associated with this trait have not been as precisely codified or analyzed as those published for Plio-Pleistocene hominins (McCollum et al., 1993, J. Hum. Evol. 24, 87; McCollum, 2000, Am. J. Phys. Anthrop. 112, 275). This study examines the internal nasal floor topography in complete crania and isolated maxillae in European, west Asian, and African fossil Homo (n = 158) including 25 Neandertals, and a wide range of recent humans from Europe, the Near East, and Africa (n = 522). The configuration of the internal nasal floor relative to the nasal cavity entrance is codified as: 1) level, forming a smooth continuous plane; 2) sloped or mildly stepped; or 3) bilevel with a pronounced vertical depression. The frequency of these nasal floor configurations, and their relationship to both nasal margin cresting patterning and a comprehensive set of nasofacial metrics is examined. Neandertals show a high frequency of the bilevel (depressed) configuration in both adults and subadults (80%), but this configuration is also present in lower frequencies in Middle Pleistocene African, Late Pleistocene non-Neandertal (Skhul, Qafzeh), and European Later Upper Paleolithic samples (15%–50%). The bilevel configuration is also present in lower frequencies (ca. 10%) in all recent human samples, but attains nearly 20% in some sub-Saharan African samples. Across extinct and extant Homo (excluding Neandertals), internal nasal floor configuration is not associated with piriform aperture nasal margin patterning, but the two are strongly linked in Neandertals. Variation in internal nasal floor configuration in recent humans is primarily associated with internal nasal fossa breadth and nasal bridge elevation, whereas in fossil hominins, it is associated primarily with variation in facial height. Cold-climate and activity-related thermal adaptation as an explanation for the high frequency of pronounced nasal floor depression in Neandertals is inconsistent with all available data. Alternatively, variation in internal nasal floor configuration is more likely related to stochastically derived populational differences in fetal nasofacial growth patterns that do not sharply differentiate genus Homo taxa (i.e., cladistically), but do phenetically differentiate groups, in particular the Neandertals, especially when considered in combination with other nasofacial features.  2003 Elsevier Science Ltd. All rights reserved. Keywords: Pleistocene hominin evolution; Archaic humans; Subnasal morphology; Nasal cavity; Piriform aperture

E-mail address: [email protected] (R.G. Franciscus). 0047-2484/03/$ - see front matter  2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0047-2484(03)00062-9

702

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

Fig. 1. Internal nasal floor depression in Neandertals: (a) Shanidar 1, figure redrawn from Stewart (1959); (b) Shanidar 2 maxilla redrawn from Stewart (1961).

Introduction In his initial description of the Shanidar 1 Neandertal cranium, Stewart (1959:479) first directed attention to the unusually depressed, sloping internal nasal floor posterior to the nasal margin of the piriform aperture. Subsequently, Stewart (1961) described the same anatomy for the Shanidar 2 cranial remains (Fig. 1). The depressed internal nasal floor configuration was also noted in the Amud 1 Neandertal cranium by Suzuki (1970), who pointed out that this feature was also present in La Chapelle, La Quina (presumably La Quina 5), and La Ferrassie (presumably La Ferrassie 1). The trait was reiterated by Stewart (1977), who posited that facial size in modern humans was too reduced to accommodate the characteristic Neandertal internal nasal floor depression. Since then, the trait has been mentioned, and/or questioned, as a Neandertal autapomorphy frequently (Stringer and Trinkaus, 1981; Stringer, 1983; Trinkaus, 1983; Stringer et al., 1984; Franciscus

and Trinkaus, 1988; Hublin, 1991; Arsuaga et al., 1997; Churchill et al., 1999; Arsuaga et al., 1999). In addition to its potential as a species-specific trait, the depressed nasal floor in Neandertals has been further tied by others to two specific functional dynamics. First, the depressed floor has been seen as one reflection of an unusually large internal nasal fossa or chamber that is capacious in all its dimensions (Stringer and Trinkaus, 1981), an idea first elaborated by Coon (1962) who related this anatomy to a nasal radiator. Although Coon acknowledged the significance of warming and moistening inspired air in cold, dry climates with respect to lung tissue viability (see below), he primarily emphasized the need to warm inspired air in an enlarged, projecting nasal cavity given its proximity to the arterial supply to a temperature sensitive brain. Coon, in fact, argued that the characteristic midfacial projection of Neandertals, especially those from western Europe, was entirely due to the necessity of distancing the nasal chamber from the neurocranium, with the

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

anteriorly positioned dentognathic region being a mere passive byproduct. Large nasal cavities and nasal mucosa area have also been hypothesized to be involved in brain thermoregulation in terms of cooling rather than warming under conditions of heightened activity (Dean, 1988). Evidence exists for cerebral cooling that can be decoupled from hypothalamic control and significantly influenced by cavernous sinus venous/arterial heat exchange in mammals (including humans) that lack a carotid rete (Cabanac and Caputa, 1979a,b). For example, at an ambient temperature of 18.8( C, the trunk core temperature of a marathon runner can rise to 41.9( C with no clinical signs of heat stress (Maron et al., 1977). A commensurate rise in brain temperature (ca. 5( C) would rapidly impair cerebral integrating function (Cabanac and Caputa, 1979a). Ambient temperature and its effect on nasal respiratory mucosa is potentially important in cooling cerebral temperature via a complex system of venous and arterial plexi which anastomose with the internal and external jugular drainage (Steegman, 1970; Girgis and Turkel, 1984; Dean, 1988). A narrow thermal range for central nervous system viability (Wheeler, 1984) suggests that fitness may well be affected by extremes of nasal anatomy which deviate too far from tolerable temperature modification capacity, especially under conditions of heavy exercise in cool and moderate thermal conditions (Cabanac and Caputa, 1979a; Trinkaus, 1987a). Secondly, it has been suggested that the lowered, sloping nasal floor in Neandertals acted to enhance turbulent airflow during inspiration as opposed to laminar airflow that is induced in a smooth or unilevel internal fossa configuration (Franciscus and Trinkaus, 1988). Airflow through the nose, as in any tube, is defined as “turbulent” when it follows random paths, constantly changes velocities, and forms eddy currents and whorls. In contrast, “laminar” airflow is characterized by air movement that follows smooth predictable flow patterns (Courtiss et al., 1984). Turbulent air flow results in a larger portion of air coming into direct contact with the nasal mucosa during both inspiratory and expiratory cycles and therefore directly affects the efficiency of temperature and moisture

703

exchange in the nasal cavity (Franciscus and Long, 1991; Franciscus, 1995). An abrupt widening posterior to the constricture of the piriform aperture, due to a lowered internal nasal floor, would theoretically increase the rate of air flow in the nasal fossa facilitating turbulence following “Bernoulli’s principle” (Courtiss et al., 1984). This, in turn, would lead to greater nasal mucosal surface contact distal to the impingement (Proetz, 1951) and thus minimize the loss of body heat and moisture, especially in conditions of extremely cold and arid environments (Webb, 1951, 1955; Walker et al., 1961). These discussions of the possible functional and phylogenetic significance of internal nasal floor anatomy are particularly relevant to the wider discussion and debate regarding the tempo and mode of Neandertal craniofacial evolution and the apparent mosaic nature of that process (e.g., Hublin, 1998 vs. Hawks and Wolpoff, 2001). Focusing on Plio-Pleistocene hominins, McCollum et al. (1993) initially reported that a “stepped” internal nasal floor characterizes Australopithecus afarensis and A. africanus, which they considered to be the primitive pattern, while a “smooth” internal nasal floor characterized Australopithecus (P.) robustus, A.(P.) boisei and KNM-WT 17000, which they considered to be the derived pattern. A mixed pattern (both “stepped” and “smooth”) was evident in early Homo (KNM-ER 1470, 1805 and 1813; OH 24, 62, and Stw 53) and Homo erectus/ergaster (KNM-ER 3733 and SK 847) indicating the possibility of multiple species. A recent reassessment of this material (McCollum, 2000) has led to a refinement of categories that describe the topography of the nasal cavity entrance to include three classifications: “continuous-smooth”, “continuousdiscrete”, and “interrupted”. All early Homo with undamaged morphology have been reassigned to the “continuous-smooth” category. McCollum (1999) has further explored the growth dynamics of this and other subnasal and craniodental features in robust australopithecines, linking many apparent unique traits to a primary morphogenetic dynamic resulting from their unusual dental proportions. Finally, McCollum and Ward (1997) have also studied the comparative ontogeny of nasal floor topography in Hylobates, Pongo,

704

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

Gorilla, and recent humans and have shown that its configuration remains stable across developmental stages. No such comprehensive treatment, dealing specifically with the internal nasal floor configuration for later hominins, has been published despite its frequent mention in the literature. Moreover, the functional hypotheses linked to depressed internal nasal floors and more capacious nasal cavities in Neandertals reviewed above, have so far been based on a relatively small set of the more complete Neandertal crania, and have not included a wide range of comparative nonNeandertal specimens. This paper reports the results from the first comprehensive morphometric analysis of nasal floor configuration in Neandertals, non-Neandertal Pleistocene Homo, and a wide geographic range of recent modern human crania. The specific questions addressed here are: 1) Do Neandertals differ in the frequency of bilevel or depressed internal nasal floors to the extent that it constitutes an autapomorphy? 2) To what degree is internal nasal floor configuration, operationalized as a categorical variable, statistically associated with other internal and external nasofacial measurements in Neandertals and comparative samples? 3) To what extent is categorical variation in internal nasal floor form statistically associated with categorical variation in the lower border of the piriform aperture nasal margin in Neandertals and comparative samples? The results of these specific analyses are then discussed more generally in light of ongoing arguments relating to the evolution of Neandertal facial form and attendant ideas regarding nasofacial adaptive specialization and phylogenetic differentiation.

Materials The recent human adult sample consists of 522 completely intact, non-pathological crania deriving from several broad geographical regions, including western Europe, central Europe, the Mediterranean and Near East, northern Africa, and sub-Saharan Africa. They range temporally from the Neolithic time period to Nineteenth Century cemetery samples. Male and female sub-

Table 1 Recent human samples Sample

males

females

Western Europe Norse1 British Isles1,2 France3,4 Germany5

7 18 18 19

9 6 16 18

Central Europe Hungary5 Austria5 Czechoslovakia5

21 18 17

21 15 17

Mediterranean/Near East Greece5 Near East5

15 22

21 14

North Africa Egypt (Nagada)2 Egypt (Gizeh)2 N.W. Africa5

14 15 9

12 14 4

sub-Saharan Africa (Bantu) Tanzania2 Gabon3 Cameroon5 Zulu5,6

16 13 16 15

14 17 12 16

sub-Saharan Africa (Khoisan) Khoisan1,2,5,7,8

21

21

274

248

Total 1

Natural History Museum, London. Duckworth Laboratory, Cambridge. 3 Musee´ de l’Homme, Paris. 4 Institut de Pale´ontologie Humaine, Paris. 5 American Museum of Natural History, New York. 6 University of the Witwatersrand, Johannesburg. 7 South African Museum, Cape Town. 8 University of Cape Town, Cape Town. 2

samples within each of these regions are given in Table 1. Details of subsample composition, specimen selection, adult age determination, and sex determination can be found in Franciscus (1995). The fossil sample (Table 2) consists of 158 adult and subadult specimens from western and central Europe, the Near East and western Asia, North Africa and sub-Saharan Africa, for which internal nasal floor configuration could be coded. The majority of the fossil sample is from the later Pleistocene (including 25 Neandertals); however, it

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

705

Table 2 Fossil specimens and trait coding1 Specimen/sample

Sex/age

African Plio-Pleistocene KNM-ER 406 OH 5 KNM-ER 1470 KNM-ER 1813 OH 24 OH 62

Nasal floor configuration

Nasal margin configuration

level level ? ? ? level

? 2 (2) 2 2 3

African Early Pleistocene KNM-ER 3733 KNM-WT 15000

female male

sloped level

3,7 3,7

African Middle Pleistocene Bodo (cast)* Broken Hill 1 Broken Hill 2 (E687) Ndutu

male male ? female

(bilevel) bilevel level level

2 3 3 7

10.0–11.5 yrs male male 16.0–18.0 yrs 14.0 yrs female male

level level level level level bilevel bilevel

(3) ? 3 7 (7) 4 2

? ? ?

level level level

? 3 3

North African Late Pleistocene Jebel Irhoud 1 (cast)§ Rabat 1

male 14.0–15.0 yrs

sloped bilevel

? 3

African Archaic/Early Modern Klasies River Mouth AA43

male

level

Near Eastern Archaic/Early Modern Qafzeh 4 Qafzeh 6 Qafzeh 9 Qafzeh 11 Skhul 4

6.0–8.0 yrs male male 12.0–13.0 yrs male

bilevel sloped level level bilevel

4 4 4 4 3

European Neandertals Arcy-sur-Cure 3 (cast) La Chapelle 1 Devil’s Tower 1 Engis 2 La Ferrassie 1 La Ferrassie 2 Forbes’ Quarry Guattari 1 Krapina 47 Krapina 48

? male 5.0 yrs 5.0–6.0 yrs male female female male 9.0–10.0 yrs 15.0–16.0 yrs

bilevel bilevel bilevel bilevel (bilevel) bilevel bilevel bilevel sloped level

1 5 – 5 5 4 5 5 3 –

European Middle Pleistocene ATD6-69† Arago 21 (cast) Atapuerca 5‡ AT-1100+1111+1197+1198‡ AT-767+963‡ Montmaurin 4 Petralona 1 African Late Pleistocene Eliye Springs Florisbad Ngaloba (Laetoli 18)

–

706

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

Table 2 (continued) Specimen/sample

Sex/age

Nasal floor configuration

Nasal margin configuration

15.0–16.0 yrs 14.0–15.0 yrs female 6.0–7.0 yrs 2.5–4.0 yrs male 3.0 yrs female female

sloped bilevel bilevel (bilevel) bilevel bilevel bilevel sloped bilevel

2 5 4 5 5 1 5 5 5

male male male male 11.0–12.0 yrs female

bilevel bilevel bilevel bilevel bilevel sloped

1 ? ? 5 5 5

Near Eastern Early Modern Nahal Ein Gev 1 Ohalo 2

female male

level sloped

1

North African Early Modern Nazlet Khater 1 Tangiers 1

male 9.0 yrs

level sloped

3 3,7

European Early Upper Paleolithic Abri Pataud 1 Arene Candide 1 (“Prince”) Cro Magnon 1 Cro Magnon 2 Cro Magnon 4 Dolnı´ Veˇstonice 3 Dolnı´ Veˇstonice 13 Dolnı´ Veˇstonice 14 Dolnı´ Veˇstonice 15 Dolnı´ Veˇstonice 16 Grotte des Enfants 4 Grotte des Enfants 5 Grotte des Enfants 6 Lagar Velho 1 Mladecˇ 8 Pavlov 1

female male male female male female male male female male male female male 4.5–5.0 yrs male male

level level level level level level level level level level level level level sloped/bilevel? level level

4 5 ? 3 1 1 3 3 1 3 4 3 3 7 4 1

European Late Upper Paleolithic Arene Candide 1 Arene Candide 2 Arene Candide 4 Arene Candide 5 Arene Candide 6 Chancelade 1 Farincourt 3 Gough’s Cave 1 Gough’s Cave 22/87 Gough’s Cave 139 Obercassel 1

male male male male 2.5–4.0 yrs male <12.0 yrs male male female male

level sloped level level bilevel sloped sloped level level level sloped

1 2 1 3 3,7 3 7 – 3 3 1

Krapina 49 Ku˚lna 1 La Quina H5 La Quina H18 Roc de Marsal 1 Saint-Ce´saire 1 Subalyuk 2 Vindija 225 Vindija 259 Near Eastern Neandertals Amud 1 Shanidar 1¶ Shanidar 2> Shanidar 5 (cast)i Tabun B-1 Tabun C1

1

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

707

Table 2 (continued) Specimen/sample

Sex/age

Nasal floor configuration

Nasal margin configuration

Obercassel 2 Laugerie-Basse Mas d’Azil Montgaudier 3 Le Placard 56020 Le Placard 28 Rochereil 3 Romito 3 Romito 4 Svita´vka 1 Kone´prusy-Zlatu´ Ku˚nˇ 1

female <11.0 yrs 6.0–12.0 yrs 8.0–12.0 yrs female ? <6.0 yrs male female female female

sloped level bilevel level level level bilevel level level level level

3 4 1,7 – 1 4 7 3 3 – 2

North African Late Modern Afalou-2 Afalou-3 Afalou-5 Afalou-9 Afalou-10 Afalou-12 Afalou-15 Afalou-20 Afalou-24 Afalou-28 Afalou-29 Afalou-30 Afalou-31 Afalou-32 Afalou-34 Afalou-43 Afalou-46 Afalou-47 Afalou-48 Jebel Sahaba 117-4 Jebel Sahaba 117-9 Jebel Sahaba 117-10 Jebel Sahaba 117-15 Jebel Sahaba 117-18 Jebel Sahaba 117-19 Jebel Sahaba 117-22 Jebel Sahaba 117-23 Jebel Sahaba 117-26 Jebel Sahaba 117-28 Jebel Sahaba 117-31 Jebel Sahaba 117-33 Jebel Sahaba 117-34 Jebel Sahaba 117-35 Jebel Sahaba 117-38 Jebel Sahaba 117-42 Jebel Sahaba 117-44 Jebel Sahaba 117-101 Jebel Sahaba 117-106 Jebel Sahaba 117-X Jebel Sahaba 80-5 Jebel Sahaba 80-7

male male male male male male male male male male female male male female female male male male male female? 3.0–5.0 yrs male female male male female female female female male female female ? male male female 5.0 yrs male female male female

level level level sloped sloped sloped sloped bilevel sloped sloped level level level level level level level level sloped level level level sloped level level level level level level level level level level bilevel level level sloped level level level sloped

1 1 5 5 3 3 3 5 3 7 5 2 1 3 3 3 1 1 1 3,7 7 3,7 7 7 3,7 7 3,7 7 – 7 7 7 7 3,7 3 7 7 7 7 – 3

708

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

Table 2 (continued) Specimen/sample

Sex/age

Nasal floor configuration

Nasal margin configuration

Jebel Sahaba 80-12 Taforalt-1c Taforalt-8 Taforalt-8c Taforalt-9 Taforalt-11c1 Taforalt-12c1 Taforalt-12c3 Taforalt-12c4 Taforalt-15c2 Taforalt-15c4 Taforalt-15c5 Taforalt-16c1 Taforalt-17c1 Taforalt-20c1 Taforalt-20c2 Taforalt-24c1 Taforalt-25 Taforalt-25c1 Taforalt-27c3

? ? ? female male male male ? male ? male ? ? female ? female female male male ?

level level level level sloped level level sloped level level level sloped level level level level level level level sloped

3 2 2 6 3 6 5 3 2 1 3 5 5 3 1 7 1 7 5 1

African Late Modern Eland’s Bay UCT378 Eland’s Bay UCT374 Elmenteita A Naivasha 1 Oakhurst 185 Oakhurst 192

male female male female female female

level sloped sloped level level level

1 4 2 6 3 3,1

1

Unless otherwise specified, all observations taken by author on original specimens. In addition to sources cited here, and in Franciscus (1995), updated references to fossil specimens, and sex/age attributions can be found in Franciscus (2002). Double numbers under nasal margin configuration indicates that the coded state (first number) is very close to being categorized as the alternative second coded state. See text for definitions and explanations of variable coding. *Rightmire (1996). † Arsuaga et al. (1999). ‡ Arsuaga et al. (1997). § Hublin (1991). ¶ Stewart (1977). > Stewart (1961). i Trinkaus (1983).

also includes Early and Middle Pleistocene Homo and a small number of Plio-Pleistocene hominins. The Plio-Pleistocene specimens are included only to compare coding methodology with that of McCollum et al. (1993) and McCollum (2000), and are not included in subsequent analyses. The Archaic/Early Modern grouping for the Near East and sub-Saharan African samples reflects the relatively early radiometric dating for these specimens (i.e., y100 Ka), the mix of archaic vs.

modern features that many of these specimens exhibit (Kidder et al., 1992; Corruccini, 1992), and ongoing debate as to whether the total morphological pattern is best regarded as “archaic” or “modern” (e.g., Rightmire and Deacon, 1991; Smith, 1993; Bra¨uer and Singer, 1996; Wolpoff and Caspari, 1996). The Early Modern samples from Europe, the Near East, and northern Africa are composed of specimens associated with early Upper Paleolithic technology (including

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

European Aurignacian, Szeletian, Gravettian, and Proto-Magdalenian; Levantine Aurignacian; and northern African Aterian) dating to the early Upper Pleniglacial (ca.R20 Ka). The Late Modern samples from Europe, northern Africa and sub-Saharan Africa are composed of specimens associated with later Upper Paleolithic technology (including European Magdalenian and Epigravettian, northern African Fakhurian, Iberomaurusian, and Qadan; and sub-Saharan African LSA industries including: Elmenteitan, Stillbay, Capsian, Smithfield, and Wilton) dated to the late Upper Pleniglacial and Tardiglacial (y20– 10 Ka). The fossil samples include specimens which range in preservation from essentially complete crania to isolated maxillae. Further details regarding the fossil specimens including repository location, techno-cultural association, geological dating, age and sex estimation, state of preservation, and description references can be found in Franciscus (1995).

Methods The vast majority of measurements and observations were taken by the author on original fossil specimens (93%) and recent samples using a uniform protocol as described below. Given the developmental stability of internal nasal floor configuration across hominoids, including humans (McCollum and Ward, 1997), fossil subadults were included with adults for analyses of internal nasal floor scoring counts and percentages by sample, but they were not included when analyzing the relationship between internal nasal floor configuration and nasofacial metric measurements. Internal nasal floor configuration scoring Scoring of the internal nasal floor configuration was made by visual assessment, primarily from the perspective of the anterior piriform aperture (Figs. 2 and 3). Scoring was also verified, when possible, from the posterior choanae on intact crania, and from these and other orientations in the case of a single maxilla or isolated fused maxillae. Each specimen was scored according to a three stage

709

discrete scheme as: level, sloped, or bilevel based on the following criteria: 1. Level: the transition from the lowest point of the nasal margin (lateral to the incisive crest) to the internal nasal floor is smooth, forming a single plane. The predominant transverse plane of the internal nasal floor1 posterior to the nasal margin approximates the lowest point of the nasal margin relative to the Frankfurt Horizontal, or is occasionally even positioned slightly higher than the nasal margin. Emphasis is placed on the level in the posterior 2/3 portion of the internal nasal floor. A minimal depression will often be present posterior to the nasal margin and incisive crest in the vicinity of the incisive foramen; however, the majority of the internal nasal floor plane will be level or smoothly continuous with the nasal margin. 2. Sloped: the transition from the lowest point of the nasal margin (lateral to the incisive crest) to the internal nasal floor is not smooth or level. The predominant transverse plane of the internal nasal floor posterior to the nasal margin is positioned somewhat inferiorly (depressed) from the lowest point of the nasal margin relative to the Frankfurt Horizontal. The depression, however, is mild or postero-inferiorly sloping and not markedly stepped, usually attaining its most inferior point in the posterior 2/3 portion of the internal nasal floor. 3. Bilevel: the transition from the lowest point of the nasal margin (lateral to the incisive crest) to the internal nasal floor is stepped. The predominant transverse plane of the internal nasal floor is markedly depressed from the lowest point of the nasal margin relative to the Frankfurt Horizontal. Moreover, the depression often occurs in the anterior 1/3 portion of

1

The internal nasal floor is not always completely flat in a transverse plane. When viewed in A-P cross-section, it will often be mildly curved such that the lowest point is found in each half of the nasal fossa lateral to midline, and medial to the lateral wall (see Fig. 2c). Because of this, precise scoring using other techniques e.g., lateral CT-scans can be misleading if viewed only in the mid-sagittal plane.

710

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

Fig. 2. Landmarks and positional criteria for scoring internal nasal floor configuration: INF = internal nasal floor; ICR = incisive crest; IC = incisive canal; ANS = anterior nasal spine; PNS = posterior nasal spine; NM = nasal margin. Sagittal cross-section (a) showing key anatomical structures. Obliquely rotated sagittal section (b) with dotted line indicating general area that is scored lateral to the midline. Frontal view of nasal fossa posterior to the nasal margin and posterior incisive crest (c) showing nasal floor topography with dotted lines indicating general area that is scored as in (b).

the internal nasal floor, as well as in the 2/3 posterior portion. The coding scheme used here differs from the one used by McCollum et al. (1993) and McCollum (2000), and requires further elaboration. Initial pre-tests in a wide range of recent Homo, using a two state scheme similar to that originally used by McCollum and colleagues

(“smooth” vs. “stepped”), resulted in virtually no intraobserver error. However, this scheme resulted in a large range of variation in the non-“smooth” category being collapsed into the single “stepped” category, and was deemed too coarse to capture the full range of morphology for the present study. Pre-tests using an alternative four character state scheme (“level”, “sloped”, “bilevel”, and “strongly

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

711

Fig. 3. Internal nasal configuration scoring examples shown in anterior view (photos) and lateral view (illustrations): (a) level, (b) sloped, and (c) bilevel, all in recent humans, and (d) bilevel, in the Forbe’s Quarry Neandertal. Solid line in lateral views indicates the level of the nasal margin with respect to the Frankfurt Horizontal. Dotted line indicates the predominant plane of the nasal floor. In the level configuration (a) the two lines are coincident; in the sloped configuration (b) they are slightly separated in the posterior 2/3 portion of the nasal floor; in the bilevel configuration (c and d) they are separated to a greater degree, and for most of the length of the nasal floor. See text for elaboration of terminology and scoring criteria. Scale bar = 1 cm.

712

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

bilevel”) led to an unacceptably high degree of intraobserver error because it was too fine-grained to be repeatable. The three category scheme described above, and illustrated in Figs. 2 and 3, proved repeatable and accurate enough to convey the full range of variation manifested in all fossil and recent Homo. Independent coding on original specimens of a subset of the Plio-Pleistocene hominins coded by McCollum (2000), indicates congruence between her “continuous-smooth” category and the category level used here (Table 2). Based on the broader taxonomic patterning found in McCollum (2000:278), it is likely that the level and sloped categories used here fall within the “continuous smooth” category, while the bilevel category used here most closely corresponds to the “continuous-discrete” form. Differences between these two coding systems are not wholly unexpected since McCollum (2000) is partitioning variation across several genera, while the system employed here is based on the variation found only in Homo. Comparison of internal nasal floor configurations, as defined above, was assessed across sex and group categories using cross-tabulation frequency analysis. Finally, in response to some independent observers that the distinction between level and sloped required greater acclimation for scoring consistency relative to distinguishing either of these from the bilevel category, I compare results using both the three category system outlined above, and a more conservative two category case in which the level and sloped individuals are collapsed into a single group. Other observations and nasofacial measurements To analyze the relationships between internal nasal floor configuration and variation in other aspects of nasofacial morphology, general linear model analysis of variance (ANOVA), and discriminant function and canonical ariate analysis were conducted on a maximum of 39 metric variables using the three internal nasal configuration categories as the group variable. The 39 metric variables used here measure: 1) various elevations of the nasal bridge, 2) dimensions of the external nasal region adjacent to the nasal bridge, 3) dimen-

sions of the internal nasal fossa, posterior choanae and ectobasicranium, and 4) dimensions of the overall face (Table 3). All measurements were taken using a series of standard osteometric calipers, as well as a simometer (a modified coordinate caliper; Howells, 1973; Gill, 1984), and specialized internal dial calipers (Fowler: model numbers 52-553-101, and 52-553-103). The recent human samples are composed of complete data sets in which all 39 measurements and 1 of 3 nasal floor configuration scores were taken on each cranium (i.e., no missing data cells). The number of measurements available for fossil specimens varied in accordance with preservation, ranging from nearly complete measurement sets to only a few associated metric variables. Since internal nasal floor configuration is evaluated here relative to the nasal margin complex, it is necessary to understand the relationship between the two. From a spatial perspective, a depressed internal nasal floor could be the result of an inferiorly positioned floor relative to the nasal margin, the latter being a “relatively more fixed” landmark during heterochronic resorption and drift. Conversely, the floor might appear to be more depressed in some individuals because the nasal margin is relatively more elevated or pronounced (for example, in the case of a sharply raised nasal sill). In order to evaluate this, the three categories for internal nasal floor configuration were tested for their potential association with seven discrete classes of nasal margin patterning using cross-tabulation frequency analysis. The nasal margin categories used here (Fig. 4) correspond to the nomenclature and crest definitions of Gower (1923) and the specific coding system using this nomenclature employed by De Villiers (1968) and modified by Franciscus (1995). It is based on the presence/absence and conjoining configuration of up to three nasal margin crests (Fig. 4) as originally defined by Gower (1923): the lateral crest (originating from the lateral margin of the piriform aperture); the turbinal crest (originating from the anterior root of the attachment crest for the inferior turbinate); and the spinal crest (originating from the anterior nasal spine). The seven nasal margin categories based on these crests are:

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

713

Table 3 Nasofacial metric measurements Reference1

Measurement Nasal Bridge Elevation Interorbital width subtense at nasion - IOWS Naso-dacryal subtense - NDS Naso-zygoorbital subtense - NZS Naso-alpha subtense - NAS Simotic subtense - SIS Minimum nasal tip elevation - MNTE Inferior simotic subtense - ISIS Mid-orbital breadth subtense at rhinion - MOBSR Zygoorbitale-inferior nasomaxillary suture length - ZINMS Zygoorbitale-inferior nasomaxillary suture subtense - ZINMSS

Woo and Morant (1934) Howells (1973) Gill et al. (1988) Gill et al. (1988) Howells (1973) Franciscus (1995) Franciscus (1995) Woo and Morant (1934) Franciscus (1995) Franciscus (1995)

External Nasal Region Nasal breadth - NLB Nasal height - NLH Piriform aperture height - PAH Superior nasal bone width - SNBW Nasal bone height - NBH Simotic width - WNB Greatest breadth of nasal bones - GBNB Inferior nasal bone width - INBW

Martin Martin Martin Martin Martin Martin Martin Martin

Internal Nasal Fossa Internal nasal fossa length - INFL Internal nasal fossa breadth - INFB Basion-rhinion length - BRL Anterior nasal spine-staphylion length - ANSSL Superior ethmoidal breadth - SEB Inferior ethmoidal breadth - IEB Interorbital breadth - DKB Choanal height - CLH Choanal breadth - CLB Nasion-hormion length - NHL Basion-staphylion length - BSL Basion-staphylion hormion subtense - BSHS

Charles (1930) Charles (1930) Brace and Hunt (1990) Franciscus (1995) Martin No. 49.1 Martin No. 49.2 Martin No. 49a Martin No. 59 Martin No. 59.1 Charles (1930) Franciscus (1995) Franciscus (1995)

Facial Region Basion-prosthion length - BPL Nasion-prosthion height - NPH Bizygomatic breadth - ZYB Interorbital width - IOW Mid-orbital breadth - MOB Alpha cord - ALC Basion-subspinale length - BSS Basion-nasion length - BNL Intercanine breadth - ICB

Martin No. 40 Martin No. 48 Martin No. 45 Woo and Morant (1934) Woo and Morant (1934) Gill et al. (1988) Cameron (1933) Martin No. 5 Glanville (1969)

No. No. No. No. No. No. No. No.

54 55 55.1 57.2 56.2 57 57.1 57.3

1

Martin numbers refer to those found in Martin (1928) and Bra¨uer (1988). Detailed descriptions and notes regarding all measurements can be found in Franciscus (1995).

1. A single crest forming the inferior margin of the nasal aperture, i.e., fused lateral, spinal and turbinal crests.

2. Three crests forming the inferior margin of the nasal aperture, i.e., separate lateral, spinal and turbinal crests.

714

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

Fig. 4. Nasal margin categories based on the presence/absence and specific conjoining configuration of the a) lateral crest, b) turbinal crest, and c) spinal crest. An additional category not pictured here (category 7), shows no visible crests, i.e., a completely smooth nasal margin. See text for further details. Modified from De Villiers (1968).

3. Two crests forming the inferior margin of the nasal aperture, i.e., fused spinal and turbinal crests, and separate lateral crest. 4. Two crests forming the inferior margin of the nasal aperture, i.e., fused lateral and spinal crests, but separate turbinal crest. 5. Fused lateral and spinal crests, but partial fusion of spinal and turbinal crests resulting in the formation of a triangular fossa intranasalis. 6. Separate lateral crest, but partial fusion of spinal and turbinal crests resulting in the formation of the fossa intranasalis. 7. No visible crests present, or a completely smooth inferior nasal margin.

With respect to their potential relationship to internal nasal floor configuration, these seven specific nasal margin categories fall into what can be considered two broader morphological patterns (Franciscus, 1999c). Categories 1, 4 and 5 are grossly similar because they tend to delineate the interior of the piriform aperture from the external subnasoalveolar clivus by a distinct, often sharp, “raised” sill or sills. In contrast, categories 2, 3 and 6, are grossly similar because they tend to demarcate the transition between the internal nose and external clivus in a smoother, less marked, and frequently “lowered” or guttered form. Nasal margin variation in fossil Homo and recent humans,

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729 Table 4 Cross-tabulation results for internal nasal floor configuration frequencies by sex1 Total sample (fossils and recent combined; n = 638) Level Females Males Total

50.0 0.29 46.0 0.26 47.8 0.53 Total
2 = 2.00; Not significant

Sloped

Bilevel

Total
2

39.3 10.7 0.01 0.79 1.09 39.9 14.1 0.01 0.67 0.94 39.7 12.5 0.02 1.45 2.00 d.f. = 2; probability level = 0.3675;

1

For each sample, the top row is the frequency occurrence (in percent) for each internal nasal floor configuration; the bottom row is the
2 contribution for each frequency.

beyond what is considered here, including its characterization, coding, and relationship to metric and non-metric aspects of external nasofacial anatomy in fossil and recent Homo, is extraordinarily complicated (Lahr, 1994; Franciscus, 1995) and a detailed consideration is beyond the scope of this report. It will be treated comprehensively elsewhere (Franciscus, in prep.). All analyses were performed using NCSS (Hintze, 2001).

Results Internal nasal floor frequencies among samples Cross-tabulation results indicate no sex differences (p = 0.3675) in the respective frequencies of internal nasal margin patterning in the total combined sample (i.e., all fossil and recent humans; Table 4). In both males and females, the level configuration is most frequent, followed closely by the sloped configuration; the bilevel configuration is found in only 10.7% and 14.1% of females and males respectively. There are also no sex differences in the distribution of internal nasal floor configuration when fossil and recent samples are considered separately (recent only: n = 522;
2 = 1.10; p = 0.5776, and fossils only: n = 116;
2 = 1.79; p = 0.4093). Finally, collapsing the level and sloped categories into a single category to compare with the bilevel group in the aggregate

715

sample also results in no significant sex differences (
2 = 1.66; p = 0.1978). In contrast to sex, the respective frequencies of internal nasal floor configuration, does vary by sample grouping (Table 5). On average, across all samples combined, the level internal nasal floor configuration is the most frequent (47.8%), followed by the sloped configuration (38.5%); the bilevel configuration is the least frequent (13.7%) on average. However, there are marked deviations from this average pattern in some samples. In particular, the Neandertals (combined due to nonsignificant difference between European and Near Eastern samples: n = 25;
2 = 0.33; p = 0.8483) stand out most prominently by not only reversing the expected frequency pattern (level = 4.0%; sloped = 16.0%; bilevel = 80.0%), but by exhibiting, in particular, much higher than expected frequencies for the bilevel configuration. Their contribution to the total difference among samples is unmatched by any other group. After the Neandertals, the next most prominent deviation from overall average patterns is the recent subSaharan African Bantu sample which exhibits relatively higher than expected frequencies for the sloped configuration, and especially relatively lower than expected values for the level configuration. After the Bantu sample, the European Early Upper Paleolithic sample, the North African late modern sample (Taforalt, Afalou, and Jebel Sahaba), and the recent North African samples all show higher than expected frequencies of the level configuration. Moreover, none of the samples singled out above are excessively small (range n = 17–119). Collapsing the level and sloped categories into a single category does not alter the results; significant group differences remain (
2 = 124.19; p<0.00001), and the disproportionately large percentage of the
2 total accounted for by the Neandertal sample remains unchanged. Internal nasal floor configuration and nasofacial morphometrics Means and standard deviations for all nasofacial measurements, grouped by internal nasal floor configuration for the combined recent and fossil samples, are presented in Table 6 (males) and

716

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

Table 5 Cross-tabulation summary results for internal nasal floor configuration frequencies by sample1 Sample Western Europe (recent) Central Europe (recent) Mediterranean/Near East (recent) North African (recent) sub-Saharan African Bantu (recent) sub-Saharan African Khoisan (recent) African Early Pleistocene African Middle Pleistocene European Middle Pleistocene African Late Pleistocene North African Late Pleistocene African Archaic/Early Modern Near Eastern Archaic/Early Modern Neandertals (European & Near East) Near Eastern Early Modern North African Early Modern European Early Upper Paleolithic European Late Upper Paleolithic North African Late Modern African Late Modern Total

1

Level

Sloped

Bilevel

Total
2

48.6 41.4 9.9 0.02 0.23 1.16 1.41 39.4 51.4 9.2 1.56 4.62 1.63 7.81 51.4 38.9 9.7 0.20 0.00 0.83 1.03 69.1 (+) 22.1 8.8 6.53 4.81 1.18 12.52 22.7 (
) 58.0 (+) 19.3 15.62 11.60 2.76 29.98 51.2 39.5 9.3 0.11 0.01 0.61 0.73 50.0 50.0 0.0 0.00 0.07 0.27 0.34 50.0 0.0 50.0 0.00 1.54 3.85 5.39 71.4 0.0 28.6 0.82 2.70 1.13 4.65 100.0 0.0 0.0 1.72 1.16 0.41 3.29 0.0 50.0 50.0 0.95 0.07 1.92 2.94 100.0 0.0 0.0 0.57 0.39 0.14 1.10 40.0 20.0 40.0 0.06 0.45 2.53 3.04 4.0 (
) 16.0 80.0 (+) 10.01 3.31 80.24 93.56 50.0 50.0 0.0 0.00 0.07 0.27 0.34 50.0 50.0 0.0 0.00 0.07 0.27 0.34 93.8 (+) 6.3 0.0 7.07 4.33 2.19 13.59 63.6 22.7 13.6 1.16 1.43 0.00 2.59 73.8 (+) 23.0 3.3 8.68 3.86 4.83 17.37 66.7 33.3 0.0 0.45 0.04 0.82 1.31 47.8 38.5 13.7 55.50 40.85 107.20 203.55 Total
2 = 203.55; d.f. = 38; probability level = <0.0001; Significant

For each sample, the top row is the frequency occurrence (in percent) for each internal nasal floor configuration; the bottom row is the
2 contribution for each frequency. Bold-faced values in the Total
2 column reflect relatively large contributions to the overall difference in frequencies among the samples, and bold-faced values in the other three columns indicate which specific internal nasal floor configuration accounts for that difference; (+) are higher than expected values, and (
) are lower than expected values.

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

717

Table 6 Male ANOVA results for nasofacial measurements grouped by internal nasal floor configuration1 Measurement (n)

Level range n (117–146) mm mean (sd)

Sloped range n (127–131) mm mean (sd)

Bilevel range n (38–45) mm mean (sd)

Fs

INFB (276/27) IOW (276/47) SEB (276/18) DKB (276/44) ZINMS (276/44) ISIS (276/25) NPH (276/54) INFL (276/15) IEB (276/10) ALC (276/38) MNTE (276/26) ZINMSS (276/44) CLH (276/10) MOB (276/38) NLB (276/61) NAS (276/31) BRL (276/21) IOWS (276/46) SIS (276/40) PAH (276/29) CLB (276/13) NHL (276/23) NLH (276/53) ZYB (276/42) ANSSL (276/23) NDS (276/36) GBNB (276/40) MOBSR (276/27) INBW (276/39) WNB (276/45) SNBW (276/40) BNL (276/35) BSS (276/32) NZS (276/30) BPL (276/33) NBH (276/43) ICB (276/49) BSL (276/20) BSHS (276/16)

32.6 (3.5) 99.4 (5.0) 26.0 (2.8) 23.4 (2.8) 24.4 (2.9) 10.7 (2.5) 68.5 (4.6) 76.2 (5.2) 37.3 (3.4) 31.8 (4.4) 7.3 (2.2) 4.2 (1.0) 24.0 (2.6) 56.6 (6.7) 25.4 (2.7) 19.1 (3.0) 105.8 (5.6) 18.6 (2.5) 4.4 (1.5) 34.8 (3.6) 27.3 (2.5) 71.4 (3.8) 50.2 (3.7) 132.2 (6.7) 49.6 (3.0) 10.7 (2.2) 17.2 (2.2) 21.8 (3.8) 17.0 (2.2) 9.9 (2.3) 12.7 (2.6) 102.0 (5.1) 94.6 (5.0) 20.8 (3.3) 99.0 (6.1) 25.1 (2.9) 25.1 (2.5) 47.2 (4.0) 17.5 (1.9)

< 34.7 (3.4) 99.7 (4.5) < 27.1 (2.8) 23.6 (2.4) 24.7 (2.7) > 9.5 (3.0) 68.2 (6.4) > 73.6 (5.3) < 38.5 (3.4) 32.2 (4.1) > 6.4 (2.5) 4.0 (1.1) 24.5 (2.7) 57.5 (6.0) 25.8 (2.8) > 17.9 (3.8) > 103.4 (5.7) 18.5 (2.6) 3.9 (1.6) 33.4 (4.2) 27.8 (2.4) 70.4 (4.0) 50.1 (4.5) 131.9 (6.2) 48.5 (3.8) 9.9 (2.3) 17.5 (2.3) 20.6 (4.4) 17.2 (2.2) 9.3 (2.0) 12.1 (2.6) 100.7 (4.9) 93.3 (5.6) 20.1 (3.9) 98.3 (6.6) 24.6 (3.6) 24.9 (2.5) 46.8 (3.8) 17.5 (2.3)

< 37.2 (4.5) < 104.3 (8.3) < 28.5 (3.7) < 25.4 (3.8) < 26.6 (3.9) 9.1 (2.6) < 72.3 (8.3) < 76.0 (6.5) 39.8 (4.9) < 34.8 (7.9) 6.4 (2.4) 3.6 (1.3) < 25.7 (3.6) < 60.5 (9.1) < 27.1 (4.7) 17.8 (3.7) 105.0 (6.8) 19.9 (3.3) 3.9 (1.4) 34.3 (4.8) 28.7 (2.8) 72.4 (5.5) 52.2 (5.7) 135.2 (8.3) 49.5 (3.6) 10.1 (2.1) 18.3 (3.5) 21.7 (4.8) 18.0 (3.3) 9.9 (2.4) 12.9 (2.9) 101.9 (5.9) 94.4 (8.8) 20.4 (3.9) 100.3 (9.9) 25.4 (3.7) 25.5 (3.8) 47.5 (6.6) 17.6 (2.2)

28.25*** 14.27*** 11.32*** 9.16** 8.9** 8.44** 8.44** 8** 7.99** 6.03* 5.83* 5.48* 5.44* 5.36* 5.31* 5.21* 5.15* 4.6 4.51 4.28 4.18 4.12 4.1 3.95 3.7 3.63 3.11 2.76 2.75 2.73 2.15 2.1 1.59 1.42 1.31 1.12 0.82 0.44 0.07

1 Combined fossil and recent human male means arranged in descending Fs value order; * = significant at p<0.01; ** = significant at p<0.001; *** = significant at p<0.0001; < > = indicates difference between configurations using Tukey-Kramer multiple comparison test; total sample sizes for each measurement are noted in parentheses as (recent/fossils).

Table 7 (females) in descending order of ANOVA Fs values. This initial combined grouping is intended to maximize the metric nasofacial size range across Homo in order to explore gross univariate patterns. Recent human sample sizes were uniform for all measurements, and fossil

sample sizes ranged from n = 10–61 for males and n = 9–45 for females. There is some degree of sexual dimorphism in the overall measurement order. However, the single highest resulting Fs value by an order of magnitude in both the male and female samples is for internal nasal fossa

718

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

Table 7 Female ANOVA results for nasofacial measurements grouped by internal nasal floor configuration1 Measurement (n)

Level range n (119–136) mm mean (sd)

Sloped range n (107–113) mm mean (sd)

Bilevel range n (26–29) mm mean (sd)

Fs

INFB (247/17) NDS (247/27) NLB (247/45) IEB (247/9) CLB (247/10) BPL (247/18) SEB (247/19) BSL (247/12) CLH (247/7) ALC (247/27) INBW (247/27) MOB (247/28) GBNB (247/28) ISIS (247/15) ZINMS (247/29) ICB (247/35) PAH (247/17) SNBW (247/29) MNTE (247/16) BSS (247/18) SIS (247/27) NAS (247/18) IOW (247/32) ZINMSS (247/29) DKB (247/35) BNL (247/21) INFL (247/11) NZS (247/18) MOBSR (247/16) ANSSL (247/16) NBH (247/32) NLH (247/37) NPH (247/34) BRL (247/13) BSHS (247/11) WNB (247/34) NHL (247/13) ZYB (247/24) IOWS (247/32)

31.9 (2.8) 9.6 (1.8) 24.0 (2.0) 35.2 (3.2) 26.2 (2.2) 94.0 (5.7) 24.5 (2.8) 44.7 (4.0) 22.3 (2.2) 30.4 (4.0) 16.0 (2.0) 53.6 (6.0) 16.2 (2.1) 9.2 (2.9) 22.7 (2.6) 23.5 (2.1) 32.1 (3.8) 12.1 (3.0) 6.2 (2.3) 89.7 (5.1) 3.7 (1.5) 17.0 (3.3) 94.8 (3.9) 3.7 (1.0) 22.1 (2.4) 96.6 (4.1) 70.9 (4.8) 18.9 (3.5) 19.5 (3.9) 46.9 (3.0) 23.2 (3.0) 48.0 (3.5) 64.8 (4.7) 99.4 (5.4) 16.4 (1.9) 9.3 (2.6) 67.6 (3.2) 123.9 (5.4) 17.2 (2.2)

< 34.0 (3.4) 9.2 (1.9) < 24.8 (2.4) < 36.4 (3.4) 27.0 (2.3) 95.7 (6.7) 25.2 (2.5) 45.8 (3.7) 23.0 (2.5) 31.3 (4.2) 16.6 (2.1) 55.0 (5.8) 16.8 (2.2) 8.7 (2.9) 23.2 (2.7) 23.9 (2.2) 31.4 (3.9) 12.2 (2.7) 6.1 (2.5) 90.3 (5.2) 3.6 (1.5) 17.0 (3.5) 95.1 (4.5) 3.7 (1.1) 22.1 (1.9) 97.1 (4.2) 70.5 (4.7) 19.1 (3.8) 19.5 (4.3) 46.6 (3.0) 23.5 (3.0) 47.6 (3.6) 65.2 (4.5) 99.9 (4.8) 16.4 (2.1) 9.4 (2.2) 67.5 (3.8) 124.2 (6.1) 17.2 (2.5)

< 36.8 (4.5) > 7.9 (2.0) 25.5 (3.1) 36.9 (3.9) 27.2 (2.9) 96.9 (5.2) 25.7 (3.3) 46.2 (2.7) 23.1 (2.2) 32.1 (4.5) 16.7 (2.2) 55.7 (4.5) 16.8 (2.3) 7.9 (3.0) 23.6 (2.8) 23.3 (1.9) 31.0 (3.8) 11.2 (2.7) 5.4 (2.6) 91.1 (5.1) 3.2 (1.6) 16.1 (4.0) 96.0 (4.8) 3.4 (0.8) 21.6 (2.2) 97.4 (4.8) 69.9 (6.0) 18.4 (4.5) 18.7 (4.9) 46.7 (3.6) 23.6 (3.1) 47.8 (3.9) 65.3 (5.0) 99.6 (6.0) 16.6 (1.9) 9.1 (2.1) 67.8 (4.8) 124.3 (7.2) 17.2 (2.8)

29.44*** 8.76** 6.66* 5.12* 4.44 3.69 3.29 2.97 2.79 2.61 2.59 2.32 2.23 2.06 1.76 1.69 1.45 1.41 1.14 1.03 1 0.95 0.91 0.82 0.74 0.73 0.48 0.42 0.39 0.35 0.35 0.34 0.32 0.2 0.15 0.14 0.12 0.11 0.03

1 Combined fossil and recent human female means arranged in descending Fs value order; * = significant at p<0.01; ** = significant at p<0.001; *** = significant at p<0.0001; < > = indicates difference between configurations using Tukey-Kramer multiple comparison test; total sample sizes for each measurement are noted in parentheses as (recent/fossils).

breadth, which shows a clear gradient of increasing width from level to sloped to bilevel nasal floor configuration. Note also that 3 out of the 4 significant differences in females are found in measures of nasal breadth (internal nasal fossa breadth, nasal breadth, and inferior ethmoidal breadth),

and that 2 out of the top 3 in males are also nasal breadth measures (internal nasal fossa breadth and superior ethmoidal breadth). In males, further significant Fs values are associated with measures of nasal bridge elevation, facial height, internal nasal fossa length, and to a lesser extent, choanal height

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

719

Table 8 Discriminant function analysis summary for metric variables grouped by nasal floor configuration in recent humans and fossils. Samples Recent males and females

Fossil males and females

n

Variables retained1

% Correct classification2

Canonical3 r/r2

F-value4

3 categories: level, sloped, bilevel

522

INFB**** NZS**, PAH** NDS**, NLB** IOW*, INFL*, GBNB*, CLH*

50.6

0.49/0.24

8.1****

2 categories: level+sloped, bilevel

522

INFB**** NLB*** NDS**, IOW**, NPH** NLH*

77.0

0.40/0.16

13.6****

3 categories: Level, sloped, bilevel

30

NPH**, ZINMS** MOB, INFB

85.7

0.91/0.82

9.2****

2 categories: level+sloped, bilevel

30

NPH**, ZINMS** MOB*, INFB*

100.0

0.89/0.79

24.0****

3 categories: Level, sloped, bilevel

51

NPH** ZINMS*

79.2

0.80/0.64

15.9****

2 categories: level+sloped, bilevel

51

NPH**, ZINMS**

95.8

0.77/0.60

35.0****

Nasal floor groups

Significant at * = p<.05; ** = p<.01; *** p<0.001; **** p<0.0001. 1 Variables from Table 4 selected by stepwise regression and significance level for the impact of removing this variable from the discriminant function. 2 Validated classification results: i.e., the discriminant function was generated on one half of the randomly divided sample, and the resulting discriminant function equation was then used to independently classify the other half of the sample. 3 Correlation coefficient and coefficient squared for the 1st canonical function (range of percent of total explained by 1st canonical variate = 85.7–100.0%). 4 Value for F-ratio testing the significance of Wilks’ Lambda.

(posterior nasal aperture height), and external nasal breadth. Note that variation in the one direct dentognathic measure included in this study, intercanine breadth, yields no significant differences between nasal floor groups in both males and females. These relationships are further clarified with discriminant function and canonical variate analysis. Here, the combined recent sample and combined fossil sample are analyzed separately due to variably missing metric data cells in the fossil sample. An initial discriminant function with stepwise regression on all 39 metric variables, using all three internal nasal floor configurations as the grouping variable in the sex combined recent human sample (Table 8), results in the retention of nine variables (internal nasal fossa breadth, nasozygoorbital subtense, piriform aperture height, naso-dacryal subtense, nasal breadth, interorbital

width, internal nasal fossa length, greatest breadth of nasal bones, and choanal height), most of which were found to be significant in the initial ANOVA results above. However, the initial classification (56.3%) of the individuals into correct internal nasal floor classes using this discriminant function leaves nearly half of the sample misclassified. The discriminant function was also generated on one half of the randomly divided sample, and the resulting predictive equation was then used to independently classify the other half of the sample. This validation procedure produced a similar low level of classification (52.9%). To examine whether classification is improved by collapsing the level and sloped categories into a single grouping category, the same procedure was applied to the two group comparison (level + sloped vs. bilevel). This procedure retained

720

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

Table 9 Variable loadings on the major canonical variate of nasal floor configuration.1 Sample/variables retained

3 categories: level, sloped, bilevel Canonical variate 1

2 categories: level + sloped vs. bilevel Canonical variate 1

Recent males and females (n = 522) INFB IOW NLB CLH GBNB NPH NLH NZS PAH INFL NDS


0.767625
0.280483
0.268801
0.247476
0.168799 – – 0.110452 0.201023 0.213046 0.357493


0.741472
0.318009
0.147330 – –
0.079963
0.028487 – – – 0.360453

Fossil males and females (n = 30) NPH ZINMS MOB INFB


0.688168
0.667434
0.512803
0.414174

0.666902 0.660460 0.513485 0.471966

Fossil males and females (n = 51) NPH ZINMS

0.881495 0.788177

0.868768 0.829448

1

Corresponds to summary results presented in Table 10.

six variables (internal nasal fossa breadth, nasal breadth, naso-dacryal subtense, interorbital width, nasion prosthion height, and nasal height) with a markedly improved classification result (validated percent correct classification = 77.0%). Examination of the variable loadings on the first canonical variate (Table 9) shows that in recent humans the major variable associated with nasal floor configuration is internal nasal fossa breadth, consistent with results obtained in the initial ANOVA analysis conducted on the aggregate sample. Smaller loadings are found in the contrast between interorbital width and nasal bridge projection measured as the naso-dacryal subtense, and sequentially smaller loadings are found with nasal breadth, facial height (nasion-prosthion height) and nasal height. In order to test the association of metric variables with nasal floor configuration in fossils, some a priori variable reduction is necessary because too few fossils are complete enough to conduct a

stepwise regression on the total 39 measurement variable set. Various combinations of the subset of measurements which were significant in the initial ANOVA analyses were explored to maximize both sample size and to retain the most influential measurements to predict inclusion in the nasal floor categories. Four variables preserved on 30 fossil specimens were robust to various stepwise regressions: nasion-prosthion (facial height), zygoorbitale-inferior nasomaxillary suture length (a measure of nasal bridge elevation), and, to a lesser degree, mid-orbital breadth, and internal nasal fossa breadth. A discriminant function using these measurements and all three nasal floor categories resulted in a validated classification of 85.7% (Table 8). As with the recent human sample, the fossil classification is improved by collapsing the level and sloped categories into a single grouping category, in this case to 100.0%. A discriminant function using only the two most influential measurements, nasion-prosthion and

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

721

and nasal bridge projection rather than internal nasal fossa breadth. Internal nasal floor configuration and nasal margin patterns

Fig. 5. Individual scores for the first and second canonical variates of nasofacial measurements grouped by nasal floor configuration based on the 3 category nasal floor model discriminant function in 51 mixed-sex fossil specimens (Table 8). Black circles = individuals with bilevel nasal floors; open triangles = individuals with sloped nasal floors; gray circles = individuals with level nasal floors. Note the separation of bilevel nasal floor individuals from both level and sloped nasal floor individuals on canonical variate 1 which explains 99.4% of the total variance and is accounted for largely by differences in facial height.

zygoorbitale-inferior nasomaxillary suture length enlarges the fossil sample size to 51 and produces a relatively high validated classification into both the three category scheme (79.2%) and the collapsed two category scheme (95.8%). The separation between fossils with bilevel nasal floors and those with both level and sloped configurations is rather marked along the first canonical function (Fig. 5). These results indicate that in recent humans, the major variable associated with nasal floor configuration is internal nasal fossa breadth. While multivariate classification improves when the sloped and level categories are collapsed, variation in internal nasal fossa breadth is nonetheless arrayed along all three internal nasal floor categories such that the level and sloped samples are statistically separated from each other (as well as from the bilevel sample) and cannot be collapsed into a single category (Tables 6 and 7). This provides some basis for maintaining a three category classification system in Homo. In the fossil specimens, in contrast to recent humans, nasal floor depression is most strongly associated with large facial height

Given the apparent developmental stability of internal nasal floor configuration (McCollum and Ward, 1997) and nasal margin cresting patterns (Franciscus, 1995), cross-tabulation analysis for these two traits was conducted first on the aggregate sample (i.e., all fossil adults and subadults and recent samples combined, n = 666; Table 10). This produced a significantly large global
2 result with an unusually large association in one cell only, a larger than expected frequency of nasal margin category 5 (i.e., fused lateral and spinal crests but partial fusion of spinal and turbinal crests, resulting in the formation of a triangular fossa intranasalis) with the bilevel nasal floor category. The association of both of these features is very common in Neandertals, and when the Neandertal sample is omitted from the aggregate sample, the cross-tabulation results become non-significant at p<0.05. This comparison was also employed on all fossils only (n = 144; Table 11) producing the same results; a significant association between nasal margin and nasal floor frequencies becomes nonsignificant when the Neandertals are omitted from the cross-tabulation comparison. The same test applied to the recent sample only also produces a non-significant result (n = 522;
2 = 19.03; p = 0.0878). Finally, collapsing the level and sloped categories into a single category produces the same result at p<0.05 across all of these comparisons. Therefore, with the exception of the Neandertals, nasal margin patterning appears unassociated with nasal floor configuration in both recent humans and fossil Homo.

Discussion and conclusions The predominant pattern that emerges from the comparisons of internal nasal floor configuration in Homo is the distinctive position of the Neandertals. Specifically, relative to all other groups, they possess an unusually high frequency

722

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

Table 10 Total sample cross-tabulation results for nasal floor configuration by nasal margin frequencies1

Table 11 Fossil cross-tabulation results for nasal floor configuration by nasal margin frequencies1

Total sample (n = 666) Nasal margin 1 2 3 4 5 6 7 Total

1 2 3 4 5 6 7 Total

1

Level

Sloped

Bilevel

All Fossils (n = 144) 2

Total


43.9 42.0 14.2 0.53 0.42 0.06 1.01 45.8 37.3 16.9 0.03 0.05 0.52 0.60 57.1 36.0 6.9 3.87 0.50 6.16 10.53 47.6 38.1 14.3 0.00 0.01 0.02 0.03 31.3 42.5 26.3 (+) 4.36 0.22 9.60 14.18 41.5 39.0 19.5 0.30 0.00 1.09 1.39 58.1 37.2 4.7 1.07 0.04 2.50 3.61 47.3 39.2 13.5 10.46 1.24 19.95 31.35 Total
2 = 31.35; d.f. = 12; probability level = 0.0017; Significant Total sample omitting Neandertals (n = 645) 44.5 42.6 12.9 0.81 0.39 0.47 1.67 46.6 36.2 17.2 0.06 0.19 1.80 2.05 57.4 35.6 76.9 2.85 0.83 3.22 6.90 50.0 40.0 10.0 0.01 0.00 0.06 0.07 37.9 48.5 13.6 1.62 1.24 0.31 3.17 41.5 39.0 19.5 0.46 0.01 2.43 2.90 58.1 37.2 4.7 0.76 0.07 1.69 2.52 48.8 39.8 11.3 6.57 2.73 9.98 19.28 Total
2 = 19.28; d.f. = 12; probability level = 0.0815; Not Significant

For each sample, the top row is the frequency occurrence (in percent) for each internal nasal floor configuration; the bottom row is the
2 contribution for each frequency. Bold-faced values in the Total
2 column reflect relatively large contributions to the overall difference in frequencies among the nasal margin samples, and bold-faced values in the other three columns indicate which specific internal nasal floor configuration accounts for that difference; (+) are higher than expected values. There are no significant nasal margin class differences at p<0.05 when Neandertals are omitted.

Nasal Margin 1 2 3 4 5 6 7 Total

1 2 3 4 5 6 7 Total

1

Level

Sloped

Bilevel

Total
2

68.0 16.0 16.0 0.34 0.28 0.21 0.83 50.0 30.0 20.0 0.14 0.40 0.00 0.54 64.6 25.0 10.4 0.25 0.40 2.25 2.90 53.8 15.4 30.8 0.06 0.19 0.73 0.98 26.1 17.4 56.5 (+) 4.23 0.13 15.12 19.48 100.0 0.0 0.0 0.85 0.63 0.60 2.08 72.7 22.7 4.5 0.70 0.04 2.66 3.40 59.0 20.8 20.1 6.57 2.07 21.57 30.21 Total
2 = 30.21; d.f. = 12; probability level = 0.0026; Significant Total sample omitting Neandertals (n = 123) 77.3 18.2 4.5 0.21 0.09 0.61 0.91 55.6 22.2 22.2 0.24 0.01 1.43 1.68 66.0 23.4 10.6 0.07 0.11 0.04 0.22 63.6 18.2 18.2 0.05 0.05 0.80 0.90 66.7 22.2 11.1 0.01 0.01 0.02 0.04 100.0 0.0 0.0 0.41 0.63 0.29 1.33 72.7 22.7 4.5 0.04 0.03 0.61 0.68 69.1 21.1 9.8 1.03 0.93 3.80 5.76 Total
2 = 5.76; d.f. = 12; probability level = 0.9278; Not Significant

For each sample, the top row is the frequency occurrence (in percent) for each internal nasal floor configuration; the bottom row is the
2 contribution for each frequency. Bold-faced values in the Total
2 column reflect relatively large contributions to the overall difference in frequencies among the nasal margin samples, and bold-faced values in the other three columns indicate which specific internal nasal floor configuration accounts for that difference; (+) are higher than expected values. There are no significant nasal margin class differences at p<0.05 when Neandertals are omitted.

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

of bilevel (depressed) internal nasal floors. Moreover, it appears that a level or sloped internal floor, and not the bilevel configuration, is the primitive condition for Homo (present results; McCollum, 2000). However, given the attainment of between 10%–50% of the bilevel floor configuration occurrence in some non-Neandertal groups, the Neandertal pattern of differentiation is clearly phenetically rather than cladistically patterned. There appear to be at least two different sets of metrical nasofacial relationships underlying nasal floor configuration in Homo. In a wide range of recent humans, nasal floor depression is positively tied to internal nasal fossa breadth (the single most dominating variable by an order of magnitude) and other general measures of nasal capsular and midfacial breadth, while being inversely related to measures of nasal bridge elevation. This metric pattern of association is similar in both males and females, and at least provisionally, suggests that a three category scheme for nasal floor configuration is warranted. In fossil Homo, nasal floor depression is most strongly associated with variation in nasion-prosthion height (facial height) and zygoorbitale-inferior nasomaxillary suture length (a measure of size and projection of the nasal bridge and mid-face). These results, therefore, suggest the possibility that the bilevel nasal configuration found in low frequencies in recent humans, and the bilevel nasal floors manifested in varying frequencies in mid and late Pleistocene fossil Homo are not developmentally homologous, and instead are the result of different midfacial fetal growth patterns (see below). To some degree, the association of depressed nasal floors with high values for facial height supports Stewart’s (1977) initial contention based on Shanidar 1 and 2 that facial size in modern humans had become too reduced to accommodate the characteristic Neandertal internal nasal floor depression. Especially since differential inferiorly directed drift of the internal nasal floor through resorption and deposition during oro-nasal cavity growth (Enlow, 1990; McCollum, 1999) is tied to adult differences in midfacial vertical heights. However, Neandertals cluster most closely with Petralona and Middle Pleistocene African speci-

723

mens, such as Bodo and Broken Hill 1, with large vertical facial dimensions and bilevel nasal floors (Fig. 5). Stewart’s observation, therefore, is germane not only to Neandertals, but likely to Middle and Late Pleistocene Homo in general. With the exception of the Neandertals, nasal margin cresting patterning appears unassociated with internal nasal floor configuration in Homo. The hypothesis raised earlier, that bilevel nasal floor depression might be secondarily related to a high nasal margin in the categories associated with “raised” nasal sills (Categories 1, 4 and 5), or that level nasal floors might be related to “lowered” guttered margins is strongly rejected for genus Homo generally. However, as documented here, a relationship between the two traits does exist in Neandertals. The data presented here leave open a possibility that requires further evaluation; namely, that the high frequency of bilevel nasal floors in Neandertals is due to a spatial combination of vertically high faces (a trait associated with nasal floor depression common in mid and late Pleistocene Homo) and the derived 1 and 5 nasal margin categories with high relief sills, that serves to accentuate the appearance of bilevel depression. The chronological morphocline within the Neandertals themselves, with respect to these two features, further supports this hypothesis. The Krapina Neandertal maxillae (Kr 47, 48, and 49) deriving from Oxygen Isotope Stage 5e (ca. 130 Ka) all lack the more derived bilevel nasal floors and the category 1 and 5 nasal margin patterns that reach near fixation in the later Oxygen Isotope Stage 4 and younger Neandertals (Franciscus, 1999c). Neandertal children at very young ages show the same unusually high frequencies for the bilevel nasal floor configuration evident in adults. The internal nasal floor, thus, is one of a series of nasal features (nasal margin configuration, anterior nasal spine development, and piriform aperture shape) that manifest statistically significant populational differences by the second trimester of fetal development (Schultz, 1918, 1920; Mooney and Siegel, 1986a,b, 1991; Mooney et al., 1992). There is now substantial evidence that the unique constellation of Neandertal facial features most frequently associated with adults also results

724

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

from key developmental changes very early in growth (Green and Smith, 1990; Smith, 1991; Maureille and Bar, 1999; Williams, 2000; Ponce de Leo´n and Zollikofer, 2001; Krovitz, 2001; Maureille, 2002; Williams et al., 2002). As emphasized above, the Neandertal pattern of differentiation in nasal floor topography relative to other groups subsumed in Homo is clearly phenetically rather than cladistically patterned; this now appears to be the case for most Neandertal craniofacial features on a trait by trait basis (Trinkaus, 1993; Franciscus and Trinkaus, 1995; Franciscus, 1999a). It may, therefore, be more biologically meaningful to view the clustering of Neandertal traits in combination as a highly intercorrelated “trait set” that is secondarily derived from a unique pattern of fetal development. In this case, the altered growth pattern, or a series of such growth alterations through time (perhaps governed by only a few key regulator genes), and not the individual skeletal traits themselves, may well be autapomorphic in the sense that cladistically oriented workers have traditionally viewed the individual traits (Franciscus, 1995). This distinction goes beyond mere semantics, and lies at the heart of ongoing arguments regarding trait conceptualization and the status of purported Neandertal skeletal autapomorphies (Schwartz and Tattersall, 1996; Maureille and Houe¨t, 1998; Franciscus, 1999a). An important question remains as to whether such altered fetal developmental patterns arose in Neandertals through natural selection, or were instead stochastically derived through random genetic drift in a relatively small and isolated population. Two general selective models for unique aspects of Neandertal facial form have predominated: cold-climate adaptation (Coon, 1962; Steegman, 1970; Trinkaus, 1987a; Franciscus and Trinkaus, 1988; Smith, 1991; Wolpoff, 1999), and biomechanical response to the unusual use of their anterior teeth as tools (Heim, 1976; Smith, 1983, Rak, 1986; Trinkaus, 1987b; Demes, 1987; Smith and Paquette, 1989; Spencer and Demes, 1993). Previous suggestions that the depressed nasal floor functioned as part of an unusually large internal nasal fossa in Neandertals, that had evolved for: 1) warming inspired air for cerebral

thermoregulation (Coon, 1962), or 2) shedding heat under conditions of heavy exercise in cool and moderate thermal conditions (Trinkaus, 1987a; Dean, 1988), or 3) increased rates of airflow and turbulence in the nasal cavity minimizing respiratory moisture loss in cold and arid environments (Franciscus and Trinkaus, 1988) are not supported by the present study. The fact that a greater frequency of sloped and especially bilevel depressed nasal floors in recent humans occurs among the warm adapted sub-Saharan African Bantu samples strongly undermines the notion that such a configuration is physiologically adaptive in cold environments. Additionally, bilevel nasal floors occur in African Middle Pleistocene Homo, and in specimens from Skhul and Qafzeh whose overall body proportions are essentially “tropical” (Holliday, 1997). Moreover, European Late Upper Paleolithic individuals, who arguably had adapted to extremely cold conditions by around 20 Ka show predominantly level nasal floors, not bilevel ones. Recent experimental work on nasal airflow in cadaver models has also failed to find an association between airflow patterns (i.e., laminar vs. turbulent) and internal nasal floor configuration (Churchill et al., 1999), although it is difficult to generalize these results from the relatively small and regionally restricted sample (n = 10 Euroamericans) that was used. Thus, there is currently no evidence that variation in nasal floor configuration in Neandertals, or in Homo more generally, is functionally related to climatic adaptation. It is important to stress that this result does not negate the air conditioning role of other aspects of internal nasal cavity form. This is especially true for superior ethmoidal width which does array fossil and recent human samples along climatic gradients that are consistent with empirical patterns based on external nose form and clinical experimental studies (Franciscus, 1999b, 2003). With respect to biomechanical models for Neandertal facial architecture, there is currently no evidence that variation in nasal floor configuration, or other aspects of nasal fossa anatomy are functionally tied to masticatory biomechanics in Homo. Despite a statistically significant correlation between intercanine breadth and nasal breadth

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

(Schwalbe, 1887; Glanville, 1969), that some have argued accounts for the large nasal breadths in all Middle Pleistocene Homo (Wolpoff, 1999:668), the only study to directly test this assertion, Glanville (1969) rejected the hypothesis that nasal breadth was dependent on intercanine breadth, and was unable to reject the reciprocal hypothesis that nasal breadth was the independent variable. Likewise, the only direct dentognathic measure included here (intercanine breadth) consistently yielded a non-significant association with nasal floor configuration frequencies. Furthermore, experimental studies have demonstrated that the growth mechanisms controlling the position of the lateral walls of the nasal cavity are relatively independent of the shape and position of the alveolar portion of the maxillae, and are more likely responsive to the demands of the respiratory system2 (e.g., Chierici et al., 1973). There is also substantial evidence for the functional autonomy and developmental stability of the nasal capsule relative to peripheral facial structures (LinderAronson, 1970; Koski and La¨hdema¨ki, 1975; McNamara and Ribbons, 1979; Hannuksela, 1981; Bresolin et al., 1983; Linder-Aronson et al., 1986; Kerr et al., 1989; Anton, 1989). In addition, at least three groups have rejected the mechanical arguments for Neandertal facial form on the basis of masticatory muscle attachments and mechanics (Anto´n, 1994, 1996; Fuss and Niegl, 2000; Kallfelz-Klemish et al., n.d). Taken together, these considerations support a view of Neandertal craniofacial evolution that was driven largely by stochastic processes in an “accretional” or “mosaic” fashion (Stringer et al., 1984; Hublin, 1998; Maureille and Houe¨t, 1998) with decreasing variation through time. A widely recognized process for this accretional pattern in Neandertal traits, namely random genetic drift and local selection in an increasingly glacially-isolated population, has been seen as a plausible evolutionary model for some time (Howell, 1952). Futuyma, in a recent discussion of the general relationship 2

Respiratory demand, in this case, refers specifically to growth in lung volume and related tissues tied to gaseous exchange and energy production in the growing body, and not to temperature and moisture modification of respiratory air in response to ambient climate as discussed elsewhere.

between stasis and punctuated (2002:662) re-emphasized that:

725

equilibrium

If a character has multiple equilibrial states, perhaps as adaptations to different resources or habitats, evolution from the ancestral state z0 to one such state zk, may readily occur in population k. However, the divergence will eventually be undone when the population’s geographic distribution is altered and it interbreeds with conspecific populations that have retained z0. Only reproductive isolation confers long term integrity, enabling the character change to persist long enough to be registered in the fossil record and, moreover, to be ratcheted toward a more extreme state in later evolution (emphasis added). Neandertal features clearly persisted long enough to be registered in the fossil record, appearing in incipient form as early as 450 Ka during a particularly cold phase, and Neandertals appear to become a distinctive morphotype relatively late in their evolutionary trajectory (i.e., Oxygen Isotope Stages 5e). Hawks and Wolpoff (2001) have criticized the accretional model, in part, for being merely descriptive rather than processual. However, a model of random genetic drift and local selection in isolated Neandertal populations first elaborated by Howell (1952), and modified more recently with refined environmental, ecological and paleodemographic data for the past 450 Ka in Europe (Hublin, 1998) is arguably processual as well as descriptive. In particular, the notion of complete isolation by western European Neandertals as originally argued by Howell (1952) that occurred only after Oxygen Isotope Stage 5e (Boaz et al., 1982), has given way to a more dynamic model of discontinuous occupation over space and time with isolation by distance rather than complete isolation. Nonetheless, some of the issues raised by Hawks and Wolpoff (2001) in their critique of the accretional model (e.g., actual expectations for trait variability in small isolated populations) are certainly important and will provide impetus to more thoroughly and rigorously evaluate the mosaic pattern of “Neandertalization” throughout the later Pleistocene.

726

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

At present, given current paleontological, neontological, and ecological data and theory, the proposition that the “accretional” pattern of Neandertal craniofacial evolution is due primarily to increased reproductive isolation and largely stochastic differentiation among Neandertals during a series of glacial advances over the past 450 Ka remains viable, as is the emerging view that this process resulted in population specific patterns of very early fetal growth. Clearly, directional selection on Neandertal facial form in response to both biomechanical and especially climatic factors occurred as it does to variable degrees in most populations. The salient point, however, is that these adaptive factors were likely secondary causal mechanisms overlying, accommodating, and being constrained by the more primary stochastically derived fetal developmental patterns that emerged and crystallized during the increasingly colder and more isolating phases of the last Ice Ages.

Acknowledgements I am deeply indebted to all of the individuals who made original fossils and comparative skeletal collections in Europe, Israel, Africa, and the United States available to me: B. Arensburg, G. Avery, A. Barzilay, M. Bellatti, M. Beruer, L. Bondioli, J. Brauer, J. Brink, D. Buisson, J.F. Bussire, S.G. Caldo, M.M. Calvani, N. Cameron, C. Charlier, J.J. Cleyet-Merle, S. Condemi, G. Commerford, J.M. Cordy, H. Deacon, J. Deacon, A. Del Lucchese, H. de Lumley, M. Docˇkalova´, C.M. Engelbrecht, R. Foley, M.A. Fugazzola, D. Gambier, O. Giuggiola´, D. Grimaud-Herv, M. Guerri, S. Guld, J.L. Heim, M. Henneberg, I. Hershkovitz, F.C. Howell, J.J. Hublin, J. Jelı´nek, H.E. Joachim, G. Koufos, H. Kritscher, R. Kruszynski, V. Kuzelka, E. Ladier, A. Langaney, M. Leakey, J.K. Ligunda, S. Linder-Linsley, C. Loring Brace, R. Macchiarelli, M-H. Marinot, M. Mbago, E. Mbua, A. Morris, R. Muse Wanasakaami, R. Orban, I. Pap, M. Paunovic, D. Pilbeam, J. Radovcˇic´, Y. Rak, G. Rossi, L. Salvadei, L. Seitl, S. Simone, M. and Mme. Soubeyron, M. Stloukal, C.B. Stringer, J. Svoboda, L. Tagliaferro, I. Tattersall, M.

Teschler-Nicola, A-M. Tillier, P. Tobias, B. Vandermeersch, P. Vermeersch, G. Vicino, A. Vigliardi, E. Vlcˇek, F. Wendorf, H. White, T.D. White, K. Wilschke, M. Wilson, and J. Zias. I am also grateful to C. Franciscus and K.L. Eaves-Johnson for data transcription, manuscript editing, and helpful comments and K. Mykris for helping to craft the photo and figure illustrations. R. Ciochon, S. Miller, J. Polanski, C. Toll and E. Trinkaus provided helpful comments. This work has been supported by grants from the L.S.B. Leakey Foundation, NSF (SBR-9312567), and an Old Gold Fellowship from the University of Iowa.

References Anton, S.C., 1989. Intentional cranial vault deformation and induced changes of the cranial base and face. Am. J. Phys. Anthrop. 79, 253–267. Anto´n, S.C., 1994. Mechanical and other perspectives on Neandertal craniofacial morphology. In: Corruccini, R.S., Ciochon, R.L. (Eds.), Integrative Paths to the Past. Prentice-Hall, Englewood Cliffs, pp. 677–695. Anto´n, S.C., 1996. Tendon-associated bone features of the masticatory system in Neandertals. J. Hum. Evol. 31, 391–408. Arsuaga, J.L., Martı´nez, I., Gracia, A., Lorenzo, C., 1997. The Sima de los Huesos crania (Sierra de Atapuerca, Spain). A comparative study. J. Hum. Evol. 33, 219–281. Arsuaga, J.L., Martı´nez, I., Lorenzo, C., Gracia, A., Mun˜oz, A., Alonso, O., Gallego, J., 1999. The human cranial remains from Gran Dolina Lower Pleistocene site (Sierra de Atapuerca, Spain). J. Hum. Evol. 37, 431–457. Boaz, N.T., Ninkovitch, D., Rossignol-Strick, M., 1982. Paleoclimatic setting for Homo sapiens neanderthalensis. Naturwissenschaften 69, 29–33. Brace, C.L., Hunt, K.D., 1990. A nonracial craniofacial perspective on human variation A(ustralia) to Z(uni). Am. J. Phys. Anthrop. 82, 341–360. Bra¨uer, G., 1988. Osteometrie. In: Knussmann, R. (Ed.), Anthropologie: Handbuch der vergleichenden Biologie des Menschen, Band I: Wesen und Methoden der Anthropologie. Gustav Fischer, Stuttgart, pp. 160–192. Bra¨uer, G., Singer, R., 1996. The Klasies zygomatic bone: archaic or modern? J. Hum. Evol. 30, 161–165. Bresolin, D., Shapiro, P., Shapiro, G., Chapko, M., Dassel, S., 1983. Mouth breathing in allergic children: its relationship to dentofacial development. Am. J. Orthodont. 83, 334–340. Cabanac, M., Caputa, M., 1979a. Natural selective cooling of the human brain: Evidence of its occurrence and magnitude. J. Physiol. (Lond.) 286, 255–264.

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729 Cabanac, M., Caputa, M., 1979b. Open loop increase in trunk temperature produced by face cooling in working humans. J. Physiol. (Lond.) 289, 163–174. Cameron, J., 1933. The inferior gnathic triangle: A new cranial triangle: Its significance in modern and fossil man, the anthropoids and lower mammals, Craniometric Memoirs No. 5. J. Anat. 67, 318–330. Charles, C.M., 1930. The cavum nasi of the American negro. Am. J. Phys. Anthrop. 14, 177–253. Chierici, G., Harrold, E.P., Vargervik, K., 1973. Morphogenetic experiments in facial asymmetry: the nasal cavity. Am. J. Phys. Anthrop. 38, 291–300. Churchill, S.E., Shackleford, L.L., Georgi, J.N., Black, M.T., 1999. Airflow dynamics in the Neandertal nose. J. Hum. Evol. 36(4), A5. Coon, C.S., 1962. The Origin of Races. Knopf, New York. Corruccini, R.S., 1992. Metrical reconsideration of the Skhul IV and IX and Border Cave 1 crania in the context of modern human origins. Am. J. Phys. Anthrop. 87, 433–445. Courtiss, E.H., Gargan, T.J., Courtiss, G.B., 1984. Nasal physiology. Ann. Plast. Surg. 13, 214–223. Dean, M.C., 1988. Another look at the nose and the functional significance of the face and nasal mucous membrane for cooling the brain in fossil hominids. J. Hum. Evol. 17, 715–718. Demes, B., 1987. Another look at an old face: Biomechanics of the Neandertal facial skeleton reconsidered. J. Hum. Evol. 16, 297–303. De Villiers, H., 1968. The Skull of the South African Negro: A Biometrical and Morphological Study. Witwatersrand University Press, Johannesburg. Enlow, D.H., 1990. Facial Growth, 3rd Edition. WB Saunders, Philadelphia. Franciscus, R.G., 1995. Later Pleistocene Nasofacial Variation in Western Europe and Africa and Modern Human Origins. PhD. Dissertation, University of New Mexico, Albuquerque. Franciscus, R.G., 1999a. Neandertal nasal structures and upper respiratory tract “specialization”. Proc. Natl. Acad. Sci. (USA) 96, 1805–1809. Franciscus, R.G., 1999b. Unique vs. non-unique aspects of Neandertal upper respiratory anatomy. J. Hum. Evol. 36, A7. Franciscus, R.G., 1999c. The significance of Krapina for understanding the evolution of Neandertal naso-facial morphology (abstract), Krapina 1899–1999: The Krapina Neandertals and Human Evolution in Central Europe. Franciscus, R.G., 2002. The Midfacial Morphology. In: Zilha˜o, J., Trinkaus, E. (Eds.), Portrait of the Artist as a Child: The Gravettian Human Skeleton from the Abrigo do Lagar Velho and its Archeological Context, Trabalhos de Arqueologia. Vol. 22. Lisbon, Instituto Portugueˆs de Arqueologia, pp. 297–311. Franciscus, R.G., 2003. Comparing internal nasal fossa dimensions and classical measures of the external nasal skeleton in recent humans: Inferences for respiratory airflow dynamics

727

and climatic adaptation. Am. J. Phys. Anthrop.(Suppl. 36), 96–97. Franciscus, R.G., in prep. Nasal margin variation and patterning in fossil Homo and extant humans. J. Hum. Evol. Franciscus, R.G., Long, J.C., 1991. Variation in human nasal height and breadth. Am. J. Phys. Anthrop. 85, 419–427. Franciscus, R.G., Trinkaus, E., 1988. The Neandertal nose. Am. J. Phys. Anthrop. 75, 209–210. Franciscus, R.G., Trinkaus, E., 1995. Determinants of retromolar space presence in Pleistocene Homo mandibles. J. Hum. Evol. 28, 577–595. Fuss, F.K., Niegl, G. 2000. A static model of the masticatory system and its anthropological application. 12th Conference of the European Society of Biomechanics, Dublin, p. 129. Futuyma, D., 2002. Review of The Structure of Evolutionary Theory by S.J. Gould. Science 296, 662. Gill, G.W., 1984. A forensic test case for a new method of geographical race determination. In: Rathbun, T.A., Buikstra, J.E. (Eds.), Human Identification. Charles C. Thomas, Springfield, Illinois, pp. 329–339. Gill, G.W., Hughes, S.S., Bennet, S.M., Gilbert, B.M., 1988. Racial identification from the midfacial skeleton with special reference to American Indians and Whites. J. Forens. Sci. 33, 92–99. Girgis, F.G., Turkel, S., 1984. Comment on: K.L. Beals, C.L. Smith, and S.M. Dodd: Brain size, cranial morphology, climate, and time machines. Curr. Anthrop. 25, 301–330. Glanville, E.W., 1969. Nasal shape, prognathism and adaptation in man. Am. J. Phys. Anthrop. 30, 29–38. Gower, C.G., 1923. A contribution to the morphology of the apertura piriformis. Am. J. Phys. Anthrop. 6, 27–36. Green, M., Smith, F.H., 1990. Neandertal craniofacial growth. Am. J. Phys. Anthrop. 81, 232. Hannuksela, A., 1981. The effect of moderate and severe atopy on the facial skeleton. Eur. J. Ortho. 3, 187–193. Hawks, J.D., Wolpoff, M.H., 2001. The accretion model of Neandertal evolution. Evolution 557, 1474–1485. Heim, J.L., 1976. Les hommes fossiles de La Ferrassie I. Archs. Inst. Pale´ont. Hum. 35, 1–131. Hintze, J., 2001. NCSS Statistical System for Windows. Kaysville, Utah. Holliday, T.W., 1997. Body proportions in Late Pleistocene Europe and modern human origins. J. Hum. Evol. 32, 423–447. Howell, F.C., 1952. Pleistocene glacial ecology and the evolution of “classic Neandertal” man. Southwest J. Anthrop. 8, 377–410. Howells, W.W., 1973. Cranial variation in man. Peabody Mus. Pap. 67, 1–259. Hublin, J.-J., 1991. L’e´mergence des Homo sapiens archaiques: Afrique de Nord-Ouest et Europe occidentale. The`se d’Etat, Universite´ de Bordeaux 1. Hublin, J.-J., 1998. Climatic changes, paleogeography, and the evolution of the Neandertals. In: Akazawa, T., Aoki, K., Bar-Yosef, O. (Eds.), Neandertals and Modern Humans in Western Asia. Plenum Press, New York, pp. 295–310.

728

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729

Kallfelz-Klemish, C.F., Franciscus, R.G., Holton, N. (n.d.). Bite force production capability and efficiency in Neandertals and modern humans. Am. J. Phys. Anthrop. Kerr, J.S., McWilliams, J.S., Linder-Aronson, S., 1989. Mandibular form and position related to changed mode of breathing - a five year longitudinal study. Angle Ortho. 59, 91–96. Kidder, J.H., Jantz, R.L., Smith, F.H., 1992. Defining modern humans: A multivariate approach. In: Bra¨uer, G., Smith, F.H. (Eds.), Continuity or Replacement: Controversies in Homo sapiens Evolution. A.A. Balkema, Rotterdam, pp. 157–177. Koski, K., La¨hdema¨ki, P., 1975. Adaptation of the mandible in children with adenoids. Am. J. Ortho. 68, 660–665. Krovitz, G.E., 2001. Shape and growth differences between Neandertals and modern humans: Grounds for a species level distinction?. Am. J. Phys. Anthrop. 32, A93. Lahr, M.M., 1994. The multiregional model of modern human origins: a reassessment of its morphological basis. J. Hum. Evol. 26, 23–56. Linder-Aronson, S., 1970. Adenoids: their effect on mode of breathing and nasal airflow and their relationship to characteristics of the facial skeleton and the dentition. Acta. Otolaryngol. [Supplement], 265. Linder-Aronson, S., Woodside, D.G., Lundstro¨m, A., 1986. Mandibular growth direction following adenoidectomy. Am. J. Ortho. 89, 273–284. Maron, M.B., Wagner, J.A., Horvath, S.M., 1977. Thermoregulatory responses during competitive marathon running. J. Appl. Physiol. 42, 909–914. Martin, R., 1928. Lehrbuch der Anthropologie, 2nd Edition. Gustav Fisher, Jena. Maureille, B., 2002. A lost Neanderthal neonate found. Nature 419, 33–34. Maureille, B., Bar, D., 1999. The premaxilla in Neandertal and early modern children: ontogeny and morphology. J. Hum. Evol. 37, 137–152. Maureille, B., Houe¨t, F., 1998. La variabilite´ morpho-me´trique du nez: De´rivege´nique dans la ligne´e Ne´andetalienne?. Biom. Hum. Anthrop. 16, 27–33. McCollum, M.A., 1999. The robust australopithecine face: A morphometric perspective. Science 284, 301–305. McCollum, M.A., 2000. Subnasal morphological variation in fossil hominids: A reassessment based on new observations and recent developmental findings. Am. J. Phys. Anthrop. 112, 275–283. McCollum, M.A., Ward, S.C., 1997. Subnasoalveolar anatomy and hominoid phylogeny: evidence from comparative ontogeny. Am. J. Phys. Anthrop. 102, 377–405. McCollum, M.A., Grine, F.E., Ward, S.C., Kimbel, W.H., 1993. Subnasal morphological variation in extant hominoids and fossil hominids. J. Hum. Evol. 24, 87–111. McNamara, J.A., Ribbens, K.A., 1979. Nasorespiratory Function and Craniofacial Growth. Center for Human Growth and Development, University of Michigan, Ann Arbor.

Mooney, M.P., Siegel, M.I., 1986a. Racial variation in anterior nasal spine (ANS) formation: Testing the traction hypothesis. Am. J. Phys. Anthrop. 69, 242. Mooney, M.P., Siegel, M.I., 1986b. Developmental relationship between premaxillary-maxillary suture patency and anterior nasal spine morphology. Cleft Palate J. 23, 101–107. Mooney, M.P., Siegel, M.I., 1991. Premaxillary-maxillary suture fusion and anterior nasal tubercle morphology in the chimpanzee. Am. J. Phys. Anthrop. 85, 451–456. Mooney, M.P., Siegel, M.I., Kimes, K.R., Todhunter, J., Janosky, J., 1992. Multivariate analysis of second trimester midfacial morphology in normal and cleft lip and palate human fetal specimens. Am. J. Phys. Anthrop. 88, 203–209. Ponce de Le´on, M.S., Zollikofer, C.P.E., 2001. Neanderthal cranial ontogeny and its implications for late hominid diversity. Nature 412, 534–538. Proetz, A.W., 1951. Air currents in the upper respiratory tract and their clinical importance. Ann. Otol. Rhin. Laryngol. 60, 439–467. Rak, Y., 1986. The Neanderthal: A new look at an old face. J. Hum. Evol. 15, 151–164. Rightmire, G.P., 1996. The human cranium from Bodo, Ethiopia: Evidence for speciation in the Middle Pleistocene? J. Hum. Evol. 31, 21–39. Rightmire, G.P., Deacon, H.J., 1991. Comparative studies of Late Pleistocene human remains from Klasies River Mouth, South Africa. J. Hum. Evol. 20, 131–156. Schultz, A.H., 1918. Relation of the external nose to the bony nose and nasal cartilages in Whites and Negroes. Am. J. Phys. Anthrop. 1, 329–338. Schultz, A.H., 1920. The development of the external nose in Whites and Negroes. Contrib. Embryol. 34, 175–190. Schwalbe, G., 1887. Lehrbuch der Anatomie der Sinnesorgane. Besold, Erlangen. Schwartz, J.H., Tattersall, I., 1996. Significance of some previously unrecognized apomorphies in the nasal region of Homo neanderthalensis. Proc. Natl. Acad. Sci. (USA) 93, 10852–10854. Smith, F.H., 1983. Behavioral interpretations of changes in craniofacial morphology across the archaic/modern Homo sapiens transition. In: Trinkaus, E. (Ed.), The Mousterian Legacy. BAR, Oxford, pp. 141–163. S164. Smith, F.H., 1991. The Neandertals: Evolutionary dead ends or ancestors of modern people? J. Anthrop. Res. 47, 219–238. Smith, F.H., 1993. Models and realities in modern human origins: the African fossil evidence. In: Aitken, M.J., Stringer, C.B., Mellars, P. (Eds.), The Origin of Modern Humans and the Impact of Chronometric Dating. Princeton University Press, Princeton, pp. 234–248. Smith, F.H., Paquette, S.P., 1989. The adaptive basis of Neandertal facial form, with some thoughts on the nature of modern human origins. In: Trinkaus, E. (Ed.), The Emergence of Modern Humans: Biocultural Adaptations in the Later Pleistocene. Cambridge University Press, Cambridge, pp. 181–210.

R.G. Franciscus / Journal of Human Evolution 44 (2003) 701–729 Spencer, M.A., Demes, B., 1993. Biomechanical analysis of masticatory system configuration in Neandertals and Inuits. Am. J. Phys. Anthrop. 91, 1–20. Steegmann, A.T. Jr., 1970. Cold adaptation and the human face. Am. J. Phys. Anthrop. 32, 243–250. Stewart, T.D., 1959. The restored Shanidar I skull. Smithsonian Rep. for 1958, 479. Stewart, T.D., 1961. The skull of Shanidar II. Ann. Rep. Smithsonian Inst., 521–533. Stewart, T.D., 1977. The Neanderthal skeletal remains from Shanidar Cave, Iraq: A summary of findings to date. Proc. Am. Phil. Soc. 121, 121–165. Stringer, C.B., 1983. Some further notes on the morphology and dating of the Petralona hominid. J. Hum. Evol. 12, 731–742. Stringer, C.B., Trinkaus, E., 1981. The Shanidar Neandertal crania. In: Stringer, C.B. (Ed.), Aspects of Human Evolution. Taylor & Francis, London, pp. 129–165. Stringer, C.B., Hublin, J.J., Vandermeersch, B., 1984. The origins of anatomically modern humans in Western Europe. In: Smith, F.H., Spencer, F. (Eds.), The Origins of Modern Humans: A World Survey of the Fossil Evidence. Alan R. Liss, New York, pp. 51–135. Suzuki, H., 1970. Skull of the Amud man. In: Suzuki, H., Takai, F. (Eds.), The Amud Man and his Cave Site. Academic Press, Tokyo, pp. 123–206. Trinkaus, E., 1983. The Shanidar Neandertals. Academic Press, New York. Trinkaus, E., 1987a. Bodies, brawn, brains and noses: Human ancestors and human predation. In: Nitecki, M.H., Nitecki, D.V. (Eds.), The Evolution of Human Hunting. Plenum, New York, pp. 107–145.

729

Trinkaus, E., 1987b. The Neandertal face: Evolutionary and functional perspectives on a recent hominid face. J. Hum. Evol. 16, 429–443. Trinkaus, E., 1993. Variability in the position of the mandibular mental foramen and the identification of Neandertal apomorphies. Riv. Antropol. (Roma) 74, 259–274. Walker, J.E.C., Wells, R.E., Merrill, E.W., 1961. Heat and water exchange in the respiratory tract. Am. J. Med. 30, 259–267. Webb, P., 1951. Air temperatures in respiratory tracts of resting subjects in cold. J. Appl. Physiol. 4, 378–382. Webb, P., 1955. Respiratory heat loss in cold. Fed. Proc. 14, 486–487. Wheeler, P.E., 1984. The evolution of bipedality and the loss of functional body hair in hominids. J. Hum. Evol. 13, 91–98. Williams, F.L., 2000. Heterochrony and the human fossil record: Comparing Neandertal and modern human craniofacial ontogeny. In: Stringer, C.B., Barton, R.N.E., Finlayson, J.C. (Eds.), Neanderthals on the Edge. Oxbow, Oxford, pp. 257–267. Williams, F.L., Godfrey, L.R., Sutherland, R., 2002. Heterochrony and the evolution of Neandertal and modern human craniofacial form. In: Minugh-Purvis, N., McNamara, K.J. (Eds.), Human Evolution Through Developmental Change. Johns Hopkins University Press, Baltimore, pp. 405–441. Wolpoff, M.H., 1999. Paleoanthropology, 2nd Edition. McGraw-Hill, Boston. Wolpoff, M., Caspari, R., 1996. The modernity mess. J. Hum. Evol. 30, 167–172. Woo, T.L., Morant, G.M., 1934. A biomechanical study of the “flatness” of the facial skeleton in man. Biometrika 26, 196–250.