Significance of some previously unrecognized apomorphies in the nasal region ofHomo neanderthalensis (Neanderthals/human evolution/nasal morphology)

For many years, the Neanderthals have been recognized as a distinctive extinct hominid group that occupied Europe and western Asia between about 200,000 and 30,000 years ago. It is still debated, however, whether these hominids belong in their own species, Homo neanderthalensis, or represent an extinct variant ofHomo sapiens. Our ongoing studies indicate that the Neanderthals differ from modern humans in their skeletal anatomy in more ways than have been recognized up to now. The purpose of this contribution is to describe specializations of the Neanderthal internal nasal region that make them unique not only among hominids but possibly among terrestrial mammals in general as well. These features lend additional weight to the suggestion that Neanderthals are specifically distinct from Homo sapiens. Over the past century and a half, paleoanthropologists have come to recognize the Neanderthals as a highly distinctive extinct hominid group that inhabited a wide swath of Europe and western Asia (east from the Atlantic to Uzbekistan, and south from Wales to Gibraltar and the Levant) in the period from about 200,000 to 30,000 years ago (1). Nonetheless, possibly because of their large brain volumes, paleoanthropologists have in recent years been reluctant to recognize the Neanderthals as a distinct species of the genus Homo (e.g., ref. 2). Our recent studies of Neanderthal crania have, however, indicated that these hominids are autapomorphic (uniquely derived) in several respects that have previously gone unremarked, and our purpose here is to draw attention to some characteristics of the Neanderthal nasal region that not only distinguish these extinct human relatives from Homo sapiens, but also make them unique among hominids-and primates-in general. These previously undescribed features are particularly well illustrated in the Gibraltar 1 (Forbes' Quarry) skull, the first adult Neanderthal to be discovered (ref. 3; Fig. 1). Most striking is the presence of a rim of raised bone that projects from either side of the rim of the anterior nasal aperture just within its anterior edge, forming a secondary "internal margin." This rim runs one-third to halfway up the inner nasal wall on both sides and then expands to become a wide, broad-based and bluntly pointed mass that protrudes medially into the nasal cavity. This medial projection fades superiorly into a low ridge that continues to frame the nasal cavity within its external margin. On its posterior side, the horizontal inferior margin of the rim may be rounded, and the vertical portion is bounded by an open lacrimal groove (Fig. 2a). Varying only in relative size, the vertical medial projection is present (if usually damaged) in all the adult Neanderthal specimens we have examined in which this region is preserved (i. e., Gibraltar 1, Spy 1, La Ferrassie 1, La Chapelle-aux-Saints, and St-Cesaire) and is also clearly visible in published photographs of other Neanderthals (e.g., Shanidar 1; see Figure 76 in ref. 4). Although the conchal crest of extant mammals (5, 6), including Homo sapiens (ref. 6; Fig. 2b), occurs in the same general area within the nasal cavity as the medial prominence does in these Neanderthals, it arises farther back and is horizontal rather than vertical in orientation. It also differs morphologically from the raised and bulky Neanderthal medial eminence in being low and relatively poorly defined. The human conchal crest is the anterior line of contact with the nasal wall of the paper-thin inferior nasal concha, which arises from its own center of ossification (7). The inferior concha also contacts the thin sheet of bone that covers the lacrimal groove in modern humans. Given the unique conformation of both of these areas in Neanderthals, it is evident that the inferior nasal concha of these extinct hominids must have differed fundamentally in structure from that of modem humans (and of primates in general; ref 6)-if, indeed, one was present at all, which is not demonstrable with the current evidence. Among the other fossil hominids in our sample (Table 1), only the Steinheim cranium, taxonomically equivocal but often viewed as a Neanderthal precursor (8), shows any sign of a medial projection. In this fossil, the structure is, however, less bulky and less intrusive into the cavity than in the Neanderthals. Like Homo sapiens, other non-Neanderthal middle Pleistocene hominids we have examined (e.g., Kabwe; ref. 9) retain the conchal crest, which we take to be the primitive configuration. This also appears to be the case for the 300,000-year-old Sima de los Huesos (Atapuerca) cranium 4, which was recently figured by Arsuaga et al. (ref 10; Fig. 1) and suggested by them to belong to a potentially proto-Neanderthal group. Further, our review of the literature has revealed no mention of the specialized "Neanderthal-like" medial projection either in the Steinheim cranium or anywhere else among hominids. The "internal nasal margin," with its remarkable medial projection, does not, however, appear to be the only peculiarity of the Neanderthal nasal region. In the Gibraltar 1 specimen (Fig. 1), the enlarged posterior portion of the nasal cavity shows evidence of another unusual structure: a distinct swelling of the lateral nasal wall. From surface breaks, as well as from comparisons with the Spy 1 specimen (Fig. 2a), it appears that this swelling houses a medially expanded maxillary sinus. This area is not preserved in any other specimens we have examined, but this observation suggests that the Neanderthals were specialized in the posterior as well as the anterior nasal region relative to other terrestrial mammals (5, 6), including Homo sapiens (ref. 11; Fig. 2b). In the more general (and almost certainly primitive) configuration exemplified by the latter, there is no medial swelling of the posterolateral wall of the nasal cavity. The nasal cavity of extant terrestrial mammals is normally filled to varying degrees (5) with two, three, or even tTo whom reprint requests should be addressed at: Department of Anthropology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024. e-mail: [email protected]. 10852 The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact. Proc. Natl. Acad. Sci. USA 93 (1996) 10853 f~~~~~~~~~~~~~~~~~~~. ... .. ||... .. .:.. FIG. 1. Frontal view of the nasal cavity of the Gibraltar 1 cranium, illustrating the internal margin bearing a large internal projection (mp), behind which is the large swelling (pcs) within the posterior component of the nasal cavity, partly obscured in this view by matrix. The arrow indicates the hole in the wall of the swelling that reveals the enlarged maxillary sinus. four pairs of turbinates that derive and swell laterally from the ethmoid bone that lies in the midsection of the cavity wall, and given the peculiar nasal morphology in Neanderthals, it appears likely that the turbinates of these extinct hominids, and possibly also the ethmoid, were configured in an unusual manner. Whether the medial swelling in the Gibraltar Neanderthal is functionally a specialized nasal structure, as the medial projection appears to be, or whether it is merely a passive result of maxillary sinus expansion remains to be determined. Two of the three immature Neanderthals we studied (Engis and Roc de Marsal; Fig. 2c) are sufficiently well preserved to demonstrate that the medial projection has already begun to develop by the age of 3-4 years. However, at this age the wall of the nasal cavity has not expanded medially, nor has the maxillary sinus encroached anteriorly as far as in the adult (i.e., into the maxillary frontal processes), although as among adults the lacrimal groove is exposed. By comparison, in newborn Homo sapiens, the lacrimal groove is already partially roofed over, but the conchal crest, which arises as a series of irregularities during the second postnatal year, is not yet discernible. The maxillary sinus itself is not readily apparent in our species until the third or fourth year of life (12). Development of the features of the nasal fossa thus proceeded very differently in Neanderthals than in Homo sapiens, and the most striking characteristic of this region-the medial projection-became established very early in postnatal life. It thus appears that at least three notable apomorphies (derived characters) distinguish the structure of the Neanderthal internal nasal cavity not only from that of other hominids but also from primates in general (6). Indeed, it is quite FIG. 2. (a) Medial view of right maxilla of Spy 1, illustrating the medial projection of the internal margin of the nasal cavity (mp), the edge along its base (e), the vertical furrow that continues the lacrimal groove (g), and the expansive maxillary sinus (ms). (b) Adult Homo sapiens (AMNH VL 4578), showing the relations of the superior nasal concha (snc) to the middle nasal concha (inc) and to the conchal crest (cc), with the inferior concha also covering the lacrimal groove. (c) Posterior view of the palate and maxilla of the Engis child, illustrating the extent of expansion of the maxillary sinus (ms), the vertical furrow that continues the lacrimal groove (g), and the medial projection of the internal margin of the nasal aperture (mp). possible that they find no parallel among other terrestrial mammals (5). The apomorphies are the development of an internal nasal margin bearing a well-developed and vertically oriented medial projection, the swelling of the lateral nasal cavity wall into the capacious posterior nasal cavity, and the lack of an ossified roof over the lacrimal groove. Finally, the extraordinary architecture of the internal nasal area of Neanderthals is of particular interest, given the frequently quoted suggestion that both the unusual appearance of the external nasal region and the large size of the nasal fossa in Neanderthals represent anatomical accommodations to cold environmental conditions and/or low humidities (1, 13-16). Future hypotheses of this kind will also have to include Evolution: Schwartz and Tattersall 10854 Evolution: Schwartz and Tattersall Table 1. Middle/late Pleistocene hominids examined for this study in which internal nasal regions are adequately preserved Locality/specimen(s) Group Age, years Cro-Magnon 1 Homo sapiens 26,000 Engis 2* Neanderthal Unknown Gibraltar 1 and 2* Neanderthal Unknown Kabwe Homo heidelbergensis 400,000**