The Neandertal vertebral column 1: The cervical spine

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Journal of Human Evolution 64 (2013) 608e630

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Journal of Human Evolution

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The Neandertal vertebral column 1: The cervical spine

Asier Gómez-Olivencia a,b,*, Ella Been c,d, Juan Luis Arsuaga b,e, Jay T. Stock a

a PAVE Research Group, Division of Biological Anthropology, Department of Archaeology and Anthropology, University of Cambridge, Pembroke Street, Cambridge CB2 3DZ, UKbCentro UCM-ISCIII de Investigación sobre Evolución y Comportamiento Humanos, Avda. Monforte de Lemos 5 (Pabellón 14), 28029 Madrid, SpaincDepartment of Anatomy and Anthropology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv 69978, IsraeldDepartment of Physical Therapy, Zefat Academic College, Safed, IsraeleDepartamento de Paleontología, Facultad de Ciencias Geológicas, Universidad Complutense de Madrid, Ciudad Universitaria s/n, 28040 Madrid, Spain

a r t i c l e i n f o

Article history:Received 1 June 2012Accepted 13 February 2013Available online 29 March 2013

Keywords:VertebraeHomo neanderthalensisLate Pleistocene

* Corresponding author.E-mail addresses: [email protected], ag665@cam

0047-2484/$ e see front matter � 2013 Elsevier Ltd.http://dx.doi.org/10.1016/j.jhevol.2013.02.008

a b s t r a c t

This paper provides a metric analysis of the Neandertal cervical spine in relation to modern humanvariation. All seven cervical vertebrae have been analysed. Metric data from eight Neandertal individualsare compared with a large sample of modern humans. The significance of morphometric differences istested using both z-scores and two-tailed Wilcoxon signed rank tests. The results identify significantmetric and morphological differences between Neandertals and modern humans in all seven cervicalvertebrae. Neandertal vertebrae are mediolaterally wider and dorsoventrally longer than modernhumans, due in part to longer and more horizontally oriented spinous processes. This suggests thatNeandertal cervical morphology was more stable in both mid-sagittal and coronal planes. It is hypoth-esized that the differences in cranial size and shape in the Neandertal and modern human lineages fromtheir Middle Pleistocene ancestors could account for some of the differences in the neck anatomy be-tween these species.

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r e s u m e n

Este artículo proporciona un análisis métrico de la columna cervical de los Neandertales, comparándola ala variación presente en los humanos modernos. Las siete vértebras cervicales han sido analizadas: datosmétricos de siete Neandertales son comparados a una gran muestra de humanos modernos. El grado designificación de las diferencias morfométricas es testado usando z-scores y la prueba de signos deWilcoxon con dos colas. Los resultados de este estudio indican que hay diferencias métricas y morfo-lógicas significativas entre los Neandertales y los humanos modernos en todas las vértebras cervicales.Las vértebras cervicales de los Neandertales son más anchas mediolateralmente y más largas dorso-ventralmente, en parte debido a apófisis espinosas más largas y orientadas más horizontalmente. Estosugiere que el cuello de los Neandertales era más estable tanto en el plano medio-sagital como en elplano coronal. Hipotetizamos que las diferencias en el tamaño y forma del cráneo acontecidas desde elPleistoceno Medio tanto en el linaje Neandertal como en nuestro propio linaje podrían explicar algunasde las diferencias entre las dos especies.

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Introduction

When compared with modern humans, Neandertals displaysignificant morphological differences in the cranial, dental andpostcranial skeleton (Boule, 1911e1913; Heim, 1976, 1982a;Trinkaus, 1983, 2003; Rak, 1990; Franciscus and Churchill, 2002;

.ac.uk (A. Gómez-Olivencia).

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Rak et al., 2002; Harvati, 2003; Bailey, 2006; Bonmatí and Arsuaga,2007; Balzeau and Radov�ci�c, 2008; Quam and Rak, 2008; Gómez-Olivencia et al., 2009, 2012; Balzeau and Rougier, 2010; DeGroote, 2011a, b; Pablos et al., 2012; references therein; but see;Wolpoff and Frayer, 2005). Some of these differences are present atbirth (Heim, 1982b; Rak et al., 1994; Maureille, 2002), while othersmay be due to ontogenic differences in the timing and the patternof the growth trajectories between Neandertals and modernhumans (Ramirez Rozzi and Bermúdez de Castro, 2004; Gunz et al.,2010; Smith et al., 2010). In general, morphological differences may

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Table 1List of features highlighted in the literature for the Neandertal cervical spine.

Anatomicalregion/Vertebra

Feature Referring to (Specimen/sample) Advocated Against

Overall necklength

Short La Chapelle-aux-Saints Boule, 1911e1913; Schwalbe, 1914 Heim, 1976; Stewart, 1962Massive Neandertals Boule, 1911e1913; Schwalbe, 1914;

Heim, 1976Stewart, 1962

Less curved neck La Chapelle-aux-Saints Boule, 1911e1913 Schwalbe, 1914; Arambourg, 1955;Toerien, 1957; Heim, 1976

C1 Small size of the tubercle forthe transverse ligament

Neandertals Boule, 1911e1913; Gómez-Olivenciaet al., 2007

Caudally projecting anteriortubercle of the anterior arc

Neandertals Gorjanovic-Kramberger, 1906;Boule, 1911e1913; Martin, 1923;Gómez-Olivencia et al., 2007

Wide facet for the articulationwith the axis

La Quina H5 Martin, 1923

C2 Large morphological variability Neandertals Piveteau, 1966Lesser inclination of the inferiorarticular facets of the axis

Neandertals Stewart, 1962 Trinkaus, 1983

Craniocaudally low andmediolaterally wide axes

Neandertals Gómez-Olivencia et al., 2007

C4, C5 Presence of bituberculosity ofthe tip of the spinous process

Regourdou 1 Piveteau, 1966 Trinkaus, 1983

C5 Long spinous process Neandertals Stewart, 1962C5-C7 Long spinous processes Neandertals Heim, 1976; Trinkaus, 1983

Lesser inclination of thespinous processesa

Neandertals Boule, 1911e1913; Stewart, 1962;Piveteau, 1966; Trinkaus, 1983;Arensburg, 1991 (for C6-C7)

Small craniocaudal height ofthe vertebral bodies

La Chapelle-aux-Saints Boule, 1911e1913

Absence of bituberculosity of thetip of the spinous process

Neandertals Trinkaus, 1983

a This is the only feature concerning the vertebral column that was included in a table of ‘Selected Neandertal postcranial features’ by Weaver (2009: Table 2).

A. Gómez-Olivencia et al. / Journal of Human Evolution 64 (2013) 608e630 609

reflect, either a) retention of primitive features already present inHomo from the Lower Pleistocene, or b) derived characteristics,either exclusive to Neandertals, or already present in their MiddlePleistocene European ancestors. In fact, some characteristics oftencited as Neandertal apomorphies are found among earlier Euro-pean Middle Pleistocene hominins, linking these populations toNeandertals (Arsuaga et al., 1997; Carretero et al., 1997; Martínezand Arsuaga, 1997; Gómez-Olivencia et al., 2007; Gómez-Robleset al., 2007; see; Hublin, 2009 for a review; Harvati et al., 2010).For some authors, due to the evidence for reproductive continuitybetween the Middle Pleistocene Europeans and Neandertals, thesepopulations represent the same species in evolutionary terms,although could be named differently for practical reasons due totheir morphological differences (Arsuaga et al., 1997).

While morphological differences between Homo sapiens andHomo neanderthalensis have been clearly identified for the majorityof anatomical regions (see Churchill, 1998; Weaver, 2009 for a re-view), for many years the Neandertal spine has been viewed assimilar to modern humans. Neandertal vertebrae have beendescribed as falling within the range of variation found amongmodern humans, but with a tendency towards greater robusticity(e.g., Trinkaus, 1983; see also; Stewart, 1962; Arensburg, 1991).Recent studies point towards morphological differences betweenNeandertals and modern humans in the lumbar spine (i.e., Beenet al., 2010, 2012), which suggest that reevaluation of themorphology of the entire spinal column is warranted.

1 Dawson and Trinkaus (1997) attribute this degeneration more likely to alocalized trauma, although they also speculate that some form of burden carryinginvolving the neck and shoulders could have been the origin of this pathology.

The Neandertal spine

The first Neandertal vertebrae were found in Spy in 1885(Fraipoint and Lohest, 1887; Toussaint et al., submitted forpublication). This site yielded a partial sacrum and seven verte-bral remains representing the cervical, thoracic and likely lumbarregions as well. Except for the sacrum, these fossils are currentlylost, although a new lumbar vertebra has recently been discovered

(Toussaint et al., submitted for publication). The excavations atKrapina also yielded a collection of vertebral remains (Gorjanovic-Kramberger, 1906) but it was not until the discovery of the Nean-dertal of La Chapelle-aux-Saints (LC) in 1908 and its subsequentstudy (Boule, 1911e1913), that vertebrae acquired importance inthe reconstruction of Neandertal posture. Boule acknowledged thepresence of pathology in the vertebrae of this specimen and relatedit to arthritis rather reflective of the age of the individual (“attrib-uées à une cause arthritique plutôt qu’a la vieillesse du sujet”;Boule, 1911e19131: 107). Boule did not provide measurements ofthe vertebrae and his posture reconstruction for the spine appearsto be based on “subjective assessments” (Trinkaus 1985:34).Indeed, the horizontal orientation of both the spinous processesand the articular facets led Boule to propose a less curved (or notcurved at all) cervical lordosis. Regarding the lumbar region, LCwould show a less lordotic lumbar region compared with modernhumans, but still would be lordotic, in comparison with apes(Boule, 1911e1913), in which the kyphotic thoracic curvature ex-tends into the lower back.

Boule’s interpretation received criticism shortly after publica-tion (e.g., Schwalbe, 1914) and especially in the mid 1950s. Strausand Cave (1957) comment that Boule did not take into consider-ation the pathology present in the cervical spine. This view iscontested by Trinkaus (1985), who considers that the pathology didnot affect Boule’s postural reconstruction of Neandertals, whichwas rather more influenced by his evolutionary preconceptions.Toerien (1957: 447) provided additional metric informationregarding the variation in the orientation of the spinous process inmodern human and apes and concludes that “there is no reason toassume a forward curve of this [cervical] region as in the anthro-poids” (see also Arambourg, 1955).

Table 2Comparative specimens and samples.

Specimen/sample Sex n Original/Cast/Bibliography

Cervicals present (used inthe metrical study)

Humerus length(in mm) mean � SD

(minimumemaximum)

Femur bicondylarlength (in mm)mean � SD

(minimumemaximum)

Cranial capacity (cc) Chronologicalattribution (kyr)

Additional references

H. neanderthalensisa

Kebara 2 M 1 Originalb C1-C7 (C1-C7) -/324 e e 60 � 3.5 ka Arensburg, 1991; Valladasand Valladas, 1991

La Chapelle-aux-Saints 1 M 1 Originalc C1-C2, C4-C7 (C1-C2, C4-C7) 312 (Right) (430e440) (Right) 1593 56 � 4 and47 � 3 ka

Boule, 1911e1913;Trinkaus, 1985; Heim,1989; Raynal, 1990;Trinkaus, 2011;Gómez-Olivencia, 2013a

La Ferrassie 1 M 1 Originalc C1-C7 (C1-C7) 339/335 -/(458) 1626 72 ka Heim, 1976, 1982a;Ruff et al., 1997;Gómez-Olivencia, 2013b

La Quina H5 F 1 Bibliography Remains lost (C. Verna,Personal communication) (C1)

e e 1350 50 ka Martin, 1923; Ruff et al., 1997

Regourdou 1 1 Originald,Bibliography

C1-C7 (C1-C7) 310 (Right) e e MIS5? Piveteau, 1966;Vandermeersch and Trinkaus,1995; Delpech, 1996;Gómez-Olivencia et al., in pressMaureille et al., submitted forpublication

Shanidar 1 M 1 Bibliography C1, C5-C7 (C5-C7) e (458)/- 1600 50 ka Stewart, 1962; Trinkaus, 1983Shanidar 2 M 1 Castc C1-C7 (C1-C7) e e e 100 ka Stewart, 1962; Trinkaus, 1983Shanidar 3 M 1 Originale C2, C6-C7 (C6-C7) (319)/- e e 50 ka Trinkaus, 1983; Ogilvie et al.,

1998; Supplementary OnlineInformation

Shanidar 4 M 1 Bibliography C2, C3?-C6?,C6/C7(C4-C6) (305)/- e e 100 ka Trinkaus, 1983Krapina ? e Originalf C1(n ¼ 3), C2(n ¼ 3) e e e e

H. sapiensEuroamerican M 26 Originalg C1-C7 326.74 � 16.45

(288.5e357.1)450.11 � 23.58

(387.6e485.1)1489.40 � 112.08

(1278.8e1693.8) n ¼ 25Recent

Euroamerican M 6 Originalh C1-C7 326.08 � 20.30(301.5e356.0)

442.83 � 35.18(386.5e477.5)

e Recent

European M 41 Originali C1-C7 314.80 � 9.38(302.0e330.0)

428.71 � 19.36(388.0e475.0)

e Recent

Euroamerican F e Originalh C1 (n ¼ 41), C2 (n ¼ 32) 300.28 � 12.67(276.5e332.3)

415.05 � 20.42(373.8e462.3)

1275.04 � 106.37(1070.0e1496.4) n ¼ 33

Recent

Afalou ? e Originalj C1 (n ¼ 12), C2 (n ¼ 10) e Late PleistoceneArcy-sur-Cure 1 Originalc C1 e e

Cro-Magnon 4271(Cro-Magnon 1)

M 1 Originalc C1, C7 (C1) e 27680 þ/� 270 yearsBP

Vallois and Billy,1965a, b; Henry-Gambier,2002

Ohalo 2H2 M 1 Originala C1 344 ca. 19000 years BP Hershkovitz et al., 1995Taforalt ? e Originalj C2 (n ¼ 8) e Late Pleistocene

kyr ¼ thousand years; BP ¼ years before present.a The Neandertal individuals that constitute the core sample used in this study are Kebara 2, La Chapelle-aux-Saints, La Ferrassie 1, Regourdou 1, Shanidar 1, Shanidar 2, Shanidar 3 and Shanidar 4.b Department of Anatomy and Anthropology, Tel Aviv University, Tel Aviv (Israel).c Musée de l’Homme, Paris (France).d Musée d’art et d’archéologie du Périgord, Perigueux (France).e Smithsonian Institution-National Museum of Natural History, Washington (DC, USA).f Croatian Natural History Museum, Zagreb (Croatia).g Cleveland Museum of Natural History (Hamann-Todd Collection), Cleveland (Ohio, USA).h Department of Anthropology, University of Iowa, Iowa City (Iowa, USA).i Laboratorio de Evolución Humana, Universidad de Burgos, Burgos (Spain).j Institut de Paléontologie Humaine, Paris (France).

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Table 3Measurement definition including three non-metrical traits.

Anatomical region Variable Abbreviationa Vertebra inwhich it ismeasured

Unilateral/bilateral(right/left)/non

metric

Description

General Maximum dorsoventral diameter MaxDVDi C1-C7 U Measured in the mid-sagittal plane.Maximum measurement from themost ventral point to the mostdistal point of the vertebra.

Maximum transverse diameter MaxTrDi C1 U Maximum transverse diameterbetween the most lateral pointsof the transverse processes. Onlymeasured in the atlas due to thepoor preservation of the transverseprocesses in the remaining vertebrae.

Superior transverse diameter SupTrDi C1-C7 U Maximum transverse diameterbetween the most lateral points ofthe cranial (upper) articular facets.

Inferior transverse diameter ITrD C1-C7 U Maximum transverse diameterbetween the most lateral pointsof the caudal (lower) articular facets.

Vertebral foramen Canal dorsoventral diameter M10 C1-C7 U Measured in the mid-sagittal plane.Maximum distance from thedorsalmost point of the vertebralbody (anterior arch in C1) to theventralmost point of the neuralarch (posterior arch in C1).Measured in the caudal aspectin the C2, to avoid problems withthe dens.

Canal transverse diameter M11 C1-C7 U Maximum transverse diameterof the vertebral foramen.

Distance between the tuberosities forattachment of transverse ligament

DtTubTrLg C1 U Minimum transverse distancebetween the tuberosities forattachment of transverse ligament.

Anterior arch Maximum craniocaudal diameter ofthe anterior tubercle

MaxCrCdDiAntA C1 U Measured in the mid-sagittal plane.Maximum craniocaudal diameterfrom the caudalmost point to thecranialmost point of the anteriortubercle of the anterior arch.

Maximum dorsoventral diameter(thickness) of the anterior tubercleof the atlas

MaxDVDiAntTub C1 U Measured in the mid-sagittal plane.Maximum dorsoventral diameterfrom the ventralmost point to thedorsalmost point of the anteriortubercle of the anterior arch.

Maximum transverse diameterfor the facet for the dens

MaxTrDiFaDn C1 U Measured on the dorsal surfaceof the anterior arch. Maximumtransverse diameter between themost lateral points of the facetfor the dens.

Projection of the anterior tubercle e C1 NM Following Gómez-Olivenciaet al. (2007).

Vertebral bodyand dens

Body ventral craniocaudaldiameter (height)

M1 C3-C7 U Measured in the mid-sagittal plane.Maximum craniocaudal diameterbetween the ventralmost pointsof the cranial and caudal surfaces,parallel to the ventral surface of thevertebral body.

Total vertebral ventral craniocaudaldiameter (height)

M1a C2 U Measured in the mid-sagittal plane.Maximum craniocaudal diameterbetween the caudo-ventralmostpoint of the vertebral body to thecranialmost point of the dens.

Axis dorsal craniocaudaldiameter (height)

AxDCrCdDi C2 U Measured in the mid-sagittal plane.Maximum craniocaudal diameterbetween the caudo-dorsalmostpoint of the vertebral body to thecranialmost point of the dens.

Body dorsal craniocaudaldiameter (height)

M2 C2-C7 U Measured in the mid-sagittal plane.Maximum craniocaudal diameterbetween the dorsalmost points ofthe cranial and caudal surfaces,parallel to the dorsal surface of thevertebral body. In the axis, it ismeasured from the limit betweenthe dens and the upper right

(continued on next page)


Table 3 (continued )



metric

Description

articular facet to the centre of thedorsalmost edge of the caudalsurface of the vertebral body.

Body median craniocaudal diameter(height)

M3 C3-C7 U Measured in the mid-sagittal plane.Maximum craniocaudal diameterbetween the central points of thecranial and caudal surfaces of thevertebral body.

Body superior dorsoventral diameter M4 C3-C7 U Measured in the mid-sagittalplane. Maximum dorsoventraldistance between the ventralmostand caudalmost edges of thesuperior (cranial) surface of thevertebral body.

Body inferior dorsoventral diameter M5 C2-C7 U Measured in the mid-sagittalplane. Maximum dorsoventraldistance between the ventralmostand caudalmost edges of the inferior(caudal) surface of the vertebral body.

Body superior transverse diameter M7 C3-C7 U Maximum transverse distancebetween the most lateral points ofsuperior (cranial) surface of thevertebral body.

Body inferior transverse diameter M8 C2-C7 U Maximum transverse distancebetween the most lateral points ofinferior (caudal) surface of thevertebral body.

Uncinate projection UncPrj C3-C7 U Distance between the superior(cranial) surface of the vertebral bodyand a line beween the uncinate processes.Measured using a caliper depthmeasuring bridge.

Pedicles Pedicles: craniocaudal diameter PedCrCdDi C3-C7 B Measured in the centre of the pedicle,craniocaudal diameter.

Pedicles: transverse diameter PedTrDi C3-C7 B Measured in the centre of the pedicle,external-neural diameter.

Lateral mass/articularpillar

Maximum craniocaudal diameter(height) oflateral mass of the atlas

MaxCrCdDiLMa C1 B Measured in the lateral aspect of thearticular mass, maximum craniocaudaldiameter from the caudalmost point tothe cranialmost point of the lateral mass.

Bi-articular diameter BiArtDi C3-C7 B Measured in a para-sagittal plane.Maximum diameter from the ventraland cranialmost point of the upperarticular facet and the dorsal andcaudalmost point of the lower articularfacet.

Size of the tubercle for theattachment of the transverseligament

e C1 NM Following Gómez-Olivencia et al.(2007), two morphologies are proposed:large (L) or small (S).

Posterior arch Maximum craniocaudal diameterof posterior tubercle of the atlas

MaxCrCdDiPTub C1 U Measured in the mid-sagittal plane.Maximum craniocaudal diameter fromthe caudalmost point to the cranialmostpoint of the anterior tubercle of theanterior arch.

Maximum dorsoventral diameterof the posterior tubercle of theatlas

MaxDVDiPTub C1 U Measured in the mid-sagittal plane.Maximum dorsoventral diameter fromthe ventralmost point to the dorsalmostpoint of the posterior tubercle of theposterior arch.

Craniocaudal diameter of thegroove for the vertebral artery

CrCdDiGr C1 B Craniocaudal diameter of the groovefor the vertebral artery.

Articular facets Diameters in major axis of upperarticular facets

UAFMAD C1 B Diameters in major axis of upperarticular facets.

Diameters in right angle to majoraxis of upper articular facets

UAFTrD C1 B Diameters in right angle to majoraxis of upper articular facets.

Upper articular facet: sagittal diameter UFaSgDi C2-C7 B Measured in a para-sagittal plane.Maximum diameter from theventralmost point and the dorsalmostpoint of the upper articular facet.

Upper articular facet: transversediameter

UFaTrDi C2-C7 B Maximum transverse diameter fromthe medialmost point to thelateralmost point of the upperarticular facet.

A. Gómez-Olivencia et al. / Journal of Human Evolution 64 (2013) 608e630612

Table 3 (continued )



metric

Description

Lower articular facet:sagittal diameter

LwFaSgDi C1-C7 B Measured in a para-sagittal plane.Maximum diameter from theventralmost point and thedorsalmost point of the lowerarticular facet.

Lower articular facet:transverse diameter

LwFaTrDi C1-C7 B Maximum transverse diameterfrom the medialmost point tothe lateralmost point of thelower articular facet.

Laminae Laminae: craniocaudal diameter LamCrCdDi C2-C7 B Measured at the centre of thelamina. Maximum craniocaudaldiameter parallel to the dorsalsurface of the lamina.

Laminae: thickness LamTh C2-C7 B Measured at the centre of thelamina. Thickness of the laminaperpendicular to the dorsalsurface of the lamina.

Spinous process Spinous process:maximum length

M13 C2-C7 U Maximum length of the spinousprocess, locating one of the armsof the caliper in the cranial union ofthe laminae to the furthest point ofthe spinous process.

Spinous process: angle M12 C6-C7 U Angle between the superior (cranial)surfaces of the vertebral body andthe spinous process. Measured usinga goniometer.

Spinous process: minimumtransverse diameter

SpPrMinTrDi C6-C7 U Minimum transverse diameter ofthe spinous process measured at thenarrowest point before themediolateral expansion of the tip.

Spinous process: transversediameter of the tip

SpPrTrDiTp C2, C5-C7 U Transverse diameter between thelateralmost points of the tip ofthe spine.

Bituberculosity of the tip ofthe spinous process

e C3-C7 NM We consider that there isbituberculosity in the tip of thespinous process when the tip isforked for at least 1 mm.Intermediate morphologies arepossible if the spinous process isslightly bifid, albeit it does notarrive to 1 mm.

U ¼ unilateral; B ¼ bilateral; NM ¼ non metric.a Whenever possible we have used Martin’s number (Bräuer, 1988).


During the second half of the twentieth century, new Nean-dertal vertebral remains were discovered (i.e., Shanidar 1, 2, 3 and4; Regourdou 1; Kebara 2). Kebara 2 preserves the most completevertebral column of H. neanderthalensis found to date, with the 24presacral elements present as well as the sacrum and the firstcoccygeal vertebra. Despite these new findings, the morphology ofthe Neandertal spine has generally been interpreted as “withinrecent human ranges of variation but relatively robust” (Trinkaus,1983:186e187).

More recently, reassessments of the Neandertal lumbar regionsuggest that extremely kyphotic vertebral bodies together with theorientation of the inferior articular processes lead to less lordoticcurvaturewithin the Neandertal spine than amongmodern humans(Been et al., 2010, 2012), similar to Boule’s original interpretation.Additionally, the laterally projecting and cranially oriented trans-verse processes of Neandertals indicate an advantage for lateralflexion of the lumbar spine compared with modern humans (Beenet al., 2010). Within the lower lumbar spine (L5-S1), Neandertallaminae were found to be significantly longer and more sagitallyoriented than the shorter and more coronally oriented laminae ofmodernhumans (Beenet al., 2010, 2012).Moreover, this less lordoticlumbar spine was likely present in the Middle Pleistocene popula-tion of Sima de los Huesos (Gómez-Olivencia, 2009; Bonmatí et al.,

2010) and thus, could be a derived feature in the Neandertal line-age (Homo heidelbergensis-H. neanderthalensis) (Been et al., 2012).

The cervical spine of Neandertals

Despite differing interpretations of Neandertal posture, scholarshave highlighted specific metric or morphological characteristics ofthe individual cervical vertebrae of Neandertals compared withmodern humans (see Table 1). While there is agreement in thepresence of some features (e.g., weakly developed tubercles for theattachment of the transverse ligament in the atlas), others aremorecontroversial (e.g., inclination of the lower articular facets of theaxis) (see Table 1). Finally, some of the general features of cervicalvertebrae highlighted by different authors (Table 1) have not beenstudiedwith clear metric and/or statistical analyses. In fact, some ofthe Neandertal individuals that preserve most of the cervical spinehave not been described metrically (e.g., La Chapelle-aux-Saints) orthe metric analyses were limited to only selected features (e.g., LaFerrassie 1; Heim, 1976).

The length of the cervical spine of Neandertals has been asubject of interest due to its proposed relationship with speechcapabilities. Lieberman (2007a) suggested that a vocal tract musthave a 1:1 proportion between the horizontal and the vertical

Figure 1. Some of the dimensions used in the osteometric analysis, as defined inTable 3. a) C1 in cranial view; b) Axis in left lateral view; c) C7 in cranial view.


segment of the supralaryngeal vocal tract to produce the full rangeof human speech, i.e., a similar length of the horizontal oral cavityand the vertical pharyngeal cavity, positioned at a right angle.Lieberman (2007a) cites McCarthy et al. (in prep.), in which theyestimate a neck length of 120 mm for Neandertals compared with127e134 mm of two modern populations. Thus, for Lieberman(2007a:47), McCarthy and colleagues’ data show that “Neander-thal necks were too short to accommodate human vocal tracts”. Incontrast, Boë et al. (2007:577) state that Neandertals “possessed avocal tract with a longer palatal section and likely a similarpharyngeal section” when compared with modern humans. How-ever, they consider the control of the tongue, jaw and the lips to bemore important than the relationship between the palatal/hori-zontal and pharyngeal/vertical sections, as they are important inthe production of the three vowels (i, a, u) that are found in all thespoken languages around the world (Boë et al., 2007).

Another aspect of the Neandertal morphology that could berelated to the length of the neck is the shape of the bony labyrinthof the temporal bone. Spoor et al. (2003) discussed the possiblerelationship between the characteristic morphology of the Nean-dertal bony labyrinth to the kinematic characteristics of the headand neck. For these authors, Neandertals’ “bulkier neck proportions(...) could have affected passive head-on-trunk motion” (Spooret al., 2003: 161).

Finally, the cervical vertebrae also suffer from a problem com-mon to the rest of the elements of the vertebral column and thethorax: they are metameric elements, i.e., repeated and morpho-logically similar, which means that their anatomical identificationcan be difficult. In this context, the reanalysis of some Neandertalvertebrae has yielded different results from those previously pub-lished (see Supplementary information; Gómez-Olivencia, 2013a,2013b; Gómez-Olivencia et al., in press).

Objectives

The number of Neandertal vertebrae found in the last decadehas increased thanks to new discoveries in the Iberian Peninsula(e.g., Sima de las Palomas, El Sidrón) or the re-excavation of sites(e.g., Feldhofer) (Schmitz et al., 2002; Smith et al., 2006; Walkeret al., 2011a, b; Rosas et al., 2012). In this context, it is necessaryto provide working hypotheses against which the newmaterial canbe tested. The dearth of metric data from ‘classical’ Neandertal in-dividuals (La Chapelle-aux-Saints [LC], La Ferrassie 1 [LF1]),together with the reevaluation of the anatomical position of someof the vertebrae in some individuals (LC, LF1, Regourdou 1, Shanidar3) and the detection of errors in previous reconstructions of ele-ments (Kebara 2; Gómez-Olivencia, Personal observation, seebelow) warrant an indepth study of the Neandertal vertebral col-umn from an analytical point of view (i.e., vertebra by vertebra). Inthis paper, detailed metric analysis of the cervical remains is per-formed, and comparisons are made between Neandertals and alarge sample of modern humans. The null hypothesis of morpho-logical similarity between Neandertals and modern humans, asproposed by Trinkaus (1983) and Arensburg (1991), is tested.

Materials

The Neandertal individuals that constitute the core sample usedin this study (n ¼ 8) are listed in Table 2 together with details ofcomparative fossil and modern collections. The recently revisedanatomical determinations for the cervical vertebrae of La Chapelle-aux-Saints and Regourdou 1 are followed (Gómez-Olivencia, 2013a;Gómez-Olivencia et al., in press.) Additionally, evidence for thepresence of cervical vertebrae belonging to Shanidar 3 is presentedfor the first time (see Supplementary Online Information).

This study focuses on Neandertal individuals that are: a) adult,to avoid morphological changes due to ontogeny; and b) male or ofuncertain sex but with a size similar to males, to avoid confoundingissues of sexual dimorphism and general size. In fact, there is alimitation imposed by the fossil record, as many of the most com-plete Neandertal individuals that preserve cervicals are male in-dividuals and the present available sample of Neandertal femalevertebral remains is very scarce. Thus, statistical analyses (z-scoreand ManneWhitney analyses) have been limited to the core eightmale individuals. Additional Neandertal individuals are included inthe bivariate plots of the upper cervical spine (C1 and C2) in orderto illustrate shape differences (see Table 2). In cases where addi-tional data is illustrated, we identify which individuals belong toour core sample and which correspond to additional individuals.

The modern comparative sample for the main metric analysis iscomposed of adult European (n ¼ 41) and Euroamerican males(n ¼ 32). Individuals older than 45 years have been avoided to

Table 4Raw dimensions (in mm) of the Neandertal atlases (C1), summary statistics of the modern human sample and results of the z-score and the two-tailed Wilcoxon signed rank test between Neandertals and recent humansa.

Variable Neandertals Modern human male sample WKebara 2 La Chapelle-aux-Saints

(#r, #t, #u, #v)La Ferrassie

1 (#a)Regourdou1 (V#ai)

Shanidar 2 Mean SD Min Max n

Maximum dorsoventral diameter (MaxDVDi) 48.6 43.4 45.46 2.71 40.1 50.9 64 NSMaximum transverse diameter (MaxTrDi) (80.0) (81.5) 79.10 4.27 68.4 89.6 61 NSSuperior transverse diameter (SupTrDi) 50.3 44.9 (50.1) 48.96 2.65 42.0 54.6 64 NSInferior transverse diameter (ITrDi) 47.7 (49.0) (49.5) 46.40 2.94 37.6 53.0 65 MargCanal dorsoventral diameter (M10) 36.7** 31.6 (35.5)* 30.93 2.07 27.2 36.3 64 *Canal transverse diameter (M11) 27.7 28.8 (33.5) 29.29 2.38 23.7 35.7 65 NSDistance between the tuberosities for attachment

of transverse ligament (DtTubTrLg)18.5 16.2 (18.3) 16.15 2.23 9.1 22.1 64 NS

Maximum craniocaudal diameter of the anteriortubercle (MaxCrCdDiAntA)

10.0 12.9 11.3 (12.0) 11.09 1.11 9.0 14.5 64 NS

Maximum dorsoventral diameter (thickness)of the anterior tubercle of the atlas(MaxDVDiAntTub)

4.6* 7.3 6.0 (7.0) 6.50 0.87 5.1 9.0 67 NS

Maximum transverse diameter for the facet forthe dens (MaxTrDiFaDn)

11.0 12.1 (13.2)* 9.98 1.49 6.7 13.2 66 *

Maximum craniocaudal diameter (height) oflateral mass of the atlas (MaxCrCdDiLMa)

e/20.4 20.2/(19.3) e/22.2 18.7/- 19.3/19.4 21.30 1.99 16.1 25.2 67 Marg/NS

Maximum craniocaudal diameter of posteriortubercle of the atlas (MaxCrCdDiPTub)

5.1** 9.95 1.82 5.6 13.9 63 e

Maximum dorsoventral diameter of the posteriortubercle of the atlas (MaxDVDiPTub)

(3.2)* 7.58 1.98 4.0 13.3 62 e

Craniocaudal diameter of the groove for thevertebral artery (CrCdDiGr)

e/3.5 3.6/- 3.4/4.7 4.12 0.91 2.6 8.4 62 NS/NS

Diameters in major axis of upper articularfacets (UFaSgDi)

26.7/e 27.1/27.5 21.0/23.2 22.2/22.1 23.49 2.09 17.4 27.7 66 NS/NS

Diameters in right angle to major axis of upperarticular facets (UFaTrDi)

10.6/10.6 10.6/12.3 11.4/- 11.2/10.8 10.27 1.30 7.0 13.7 67 Marg/NS

Lower articular facet: sagittal diameter (LwFaSgDi) 16.8/16.9 17.5/e 18.2/16.9 19.1/- 17.5/18.8 16.57 1.52 13.9 22.0 66 */NSLower articular facet: transverse diameter (LwFaTrDi) 15.2/15.3 17.5y (15.8)/15.8 e/16.9 14.8/- 15.5/(14.7) 15.78 1.09 13.5 18.2 65 NS/NS

a Values in parentheses are estimated. Values underlined are outside the range of the modern human comparative sample. Values with a y are affected by pathology. The z-score and ManneWhitney analyses values with an *or two ** are significantly different from the modern male comparative sample (* ¼ p < 0.05; ** ¼ p < 0.01). Cells that contain two entries are for the right and left sides (right/left) unless in modern humans in which only rightside has been taken. In the ManneWhitney, analysis a ‘e’ means that the analysis was not performed because the Neandertal sample n < 2. NS ¼ non significant (p > 0.1). Marg ¼ Marginally significant (0.1 > p > 0.05).

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Figure 2. Craniocaudal (y) and dorsoventral (x) dimensions (in mm) of the posteriorarch of the atlas (C1). Black squares represent Neandertals. Note that La Ferrassie 1(LF1) is outside the 95% of the equiprobability ellipses of the modern samples. Notethat the Krapina atlas 100e101 does not belong to our Neandertal core sample and itssex is unknown. Black dots represent Upper Pleistocene H. sapiens from Afalou andTaforalt of unknown sex, and the individuals from Arcy-sur-Cure, Ohalo 2 and Cro-Magnon 1. Black triangles represent the sample from Sima de los Huesos (Gómez-Olivencia et al., 2007).


minimize the presence of degenerative changes. Additional modernhumans have been used in some bivariate representations (seeTable 2).

Methods

Metric variables and non-metric traits

Standard anthropometric techniques and instruments wereused to collect all measurements. The metric variables are defined

Table 5Comparison of the percentages of small tubercles in Neandertals, compared with other f

Species Sample (n) Sex

H. neanderthalensis n ¼ 8 Pooled sexH. heidelbergensis Sima de los Huesos (n ¼ 6) Males (n ¼ 3), indetermH. sapiens European (n ¼ 39) MalesH. sapiens Afaolou (n ¼ 12) Pooled sexH. sapiens Euroamerican (n ¼ 29) MalesH. sapiens Euroamerican (n ¼ 33) Females

a For a complete list of the individuals see Supplementary Online Information (Table Sb Asymmetry refers to the presence of a large tubercles in one of the masses and a sm

Table 6Comparison of the percentages of presence of caudal projection of the anterior tubercle osamples.

Species Individual/sample Projectiona n

Homo antecessor ATD6-90 100% 1Homo heidelbergensis Sima de los Huesos 100% 6Homo neanderthalensis e 100% 5Fossil Homo sapiens e 25% 4Recent Homo sapiens European males 48.6% 37

Euroamerican females 36.3% 33Euroamerican males 25% 28

a For a complete list of the individuals see Supplementary Online Information (Table S

in Table 3 and most are depicted in Fig. 1. The existence of patho-logical lesions in some of the Neandertals studied here is well-documented (e.g., La Chapelle-aux-Saints; see Boule, 1911e1913;Trinkaus, 1985; Dawson and Trinkaus, 1997). The measurementsaffected by pathology have been reported, and if possible ‘non-pathological’ values have been estimated, which are used in thesubsequent analyses. All of the measurements and estimationswere taken by one of us (AGO). The estimated value was reportedwhen the original morphology was discernible. When this was notpossible, the value affected by pathology is reported, noted aspathological but excluded from subsequent analyses. Additionally,three non-metric traits were recorded: 1) the size (large/small) ofthe tubercle for the insertion of the transverse ligament in the atlas(C1) (Gómez-Olivencia et al., 2007); 2) the presence of a caudalprojection in the C1 (Gómez-Olivencia et al., 2007); and 3) thepresence of bituberculosity of the tip of the spinous process in thelower cervical spine (C3-C7).

Statistical analysis

Univariate analyses were performed in two steps. First, each ofthe Neandertal individuals was compared with our modern malecomparison sample using z-scores. Significant values, i.e., z-scorevalues beyond 1.96 (p < 0.05) and 2.576 SD (p < 0.01) (Sokal andRohlf, 1981) and/or beyond the range of our modern comparativesample were highlighted. Second, the male Neandertal sample(when this sample’s n > 1) was compared as a whole with themodern male comparative sample using the two-tailed Wilcoxonsigned rank test, which in this case is equivalent to ManneWhitney’s U-test (Wilcoxon, 1945; Mann and Whitney, 1947).We have chosen a non-parametric statistical analysis to providemore conservative tests, due to the small sample size of Nean-dertals, although this makes it more difficult to reject the nullhypothesis of equality between the median of the samples. Uni-variate and bivariate plots were used to illustrate and characterizevertebral size and shape. Statistical analyses and graphics wereperformed in the R statistical environment (R Development CoreTeam, 2011).

ossil and modern samplesa.

Large tubercle Asymmetryb Small tubercle

0.0 12.5 87.5inate (n ¼ 3) 33.3 0.0 66.7

74.4 10.2 15.483.3 0.0 16.796.6 0.0 3.475.8 15.2 9.1

2).all tublercle in the other mass, within the same atlas.

f the anterior arc of the atlas in Neandertals, compared with other fossil and modern

References

Carretero et al., 1999; Gómez-Olivencia et al., 2007Gómez-Olivencia et al., 2007Boule, 1911e1913; Martin, 1923; Heim, 1976; Arensburg, 1991; this studyMcCown and Keith, 1939; Grine et al., 1998; this studyGómez-Olivencia, 2009Gómez-Olivencia, 2009Gómez-Olivencia, 2009

3).

Morphom

etricresult

Significan

tmetri

Nean

dertalsam

ple

aallcervicalvertebra

Thefirst

cervicalver

Metric

dim

ension

tisticsof

themod

ernW

ilcoxontest

arepr

ventrally

elongateddorsoventrally

elonget

al.,2007).N

eande

atlanto-axial

joint(a

Table 7Raw dimensions (in mm) of the Neandertal axes (C2), summary statistics of the modern human sample and results of the z-score and the two-tailed Wilcoxon signed rank test between Neandertals and recent humansa.

Variable Modern humans WKebara 2 La C Mean SD Min Max n

Maximum dorsoventral diameter (MaxDVDi) 50.1 2.3 44.5 57.0 65 NSSuperior transverse diameter (SupTrDi) 50.0 45.8 2.6 38.5 50.9 69 **Inferior transverse diameter (ITrDi) 47.9 2.6 42.7 55.1 68 e

Canal dorsoventral diameter (M10) 16.8 1.4 14.3 20.1 69 NSCanal transverse diameter (M11) 25.0 23.4 1.4 18.6 27.0 69 **Total vertebral ventral craniocaudal diameter (height) (M1a) (35.0) 38.4 2.3 33.0 44.9 68 *Axis dorsal craniocaudal diameter (height) (AxDCrCdDi) 34.3 2.3 28.3 40.6 68 *Body dorsal craniocaudal diameter (height) (M2) 19.2 1.5 13.5 24.1 67 NSBody inferior dorsoventral diameter (M5) 16.5 15.2 1.1 13.1 18.4 68 **Body inferior transverse diameter (M8) 17.4 18.3 1.4 15.7 21.7 65 *Upper articular facet: sagittal diameter (UFaSgDi) 18.1 1.5 15.4 23.0 67 NS/eUpper articular facet: transverse diameter (UFaTrD) 16.7 1.5 13.6 19.5 66 NS/NSLower articular facet: sagittal diameter (LwFaSgDi) 10.3 1.4 6.8 13.3 65 */eLower articular facet: transverse diameter (LwFaTrDi) 11.4 1.2 8.7 15.5 64 NS/eLaminae: craniocaudal diameter (LamCrCdDi) 12.0 1.2 8.9 14.9 69 NS/eLaminae: thickness (LamTh) 5.7 1.2 3.4 8.6 69 NS/eSpinous process: maximum length (M13) 19.2 2.5 12.8 23.8 66 NSSpinous process: transverse diameter of the tip (SpPrTrDiTp) 14.3 3.4 6.9 21.8 62 e

a Values in parentheses are estimated. Values underlined are outside the range of the -score andManneWhitney analyses values with a * ortwo ** are significantly different from the modern male comparative sample (* ¼ p< 0 eft) unless in modern humans in which only right sidehas been taken. In the ManneWhitney analysis a ‘e’ means that the analysis was not arg ¼ Marginally significant (0.1 > p > 0.05).

b In the Regourdou 1 individual, the values of MaxDVDi, SupTrDi, M10, M11, right

Figure

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6

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56.5** 50.0 51.250.8* (47.0) (46.5) (51.5)*

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(25.0) 24.5 25.3 (27.0)*(34.5)* (37.0) 36.8 37.7(33.0) (34.5) 33.0 33.720.0 20.0 16.9 16.4

19.7** 17.5* 16.020.4 21.8* 19.6 19.717.6/e 18.0/e 17.1/16.7 18.7/e20.8**/(16.7) e/(19.0) 17.4/16.8 15.7/e

11.4/21.9y 13.0/13.5* 12.6/e12.2/15.6y 12.0/11.8 12.4/e10.4/9.9 12.5/13.2 10.0/e5.2/6.0 5.5/5.7 5.0/e19.8 (18.0)14.1

modern human comparative sample. Values with a y are affected by pathology. The z.05; **¼ p< 0.01). Cells that contain two entries are for the right and left sides (right/lperformed because the Neandertal sample n < 2. NS ¼ non significant (p > 0.1). MLamCrCdDi and right LamTh have been taken from Piveteau (1966).

scan

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and Wilcoxon test are presented in Table 7. When compared withmodern humans, Neandertals display a mediolaterally largeatlanto-axial joint, which is reflected by large values of SupTrD ofthe axis. Neandertal axes also display wider vertebral canals (M11)and are ‘low’ craniocaudally (see M1a and AxDCrCdDi) (see Fig. 3).The smaller dimensions in M1a and AxDCrCdDi are due to a smallersize of the dens, as the height of the vertebral body (M2) remainssimilar to the modern human mean. This ‘low’ and ‘wide’morphology of the axis in ventral view has previously been noted(Gómez-Olivencia et al., 2007). Finally, Neandertals display a largecaudal aspect of the vertebral body (M5, M8).

The lower cervical spine (C3-C7)

Metric dimensions of the Neandertal C3-C7, summary statisticsof the modern human sample and results of the z-score and Wil-coxon test are presented in Tables 8e12. These results are sum-marized in Table 13 and allow a more synthetic view of thedifferences between the Neandertal cervical spine and the modernmale sample. The lower cervicals of Neandertals are wider in bothabsolute terms and relative to the canal width (C3-C7) and dorso-ventrally longer (C4-C7). Their vertebral bodies are craniocaudallyshorter in C3-C7 and dorsoventrally larger in C3-C4. Their laminaeare craniocaudally shorter in C3 and thicker in C5-C7. The spinousprocesses are longer in C5-C7 andmore horizontal, at least in C6-C7(see Figs. 4e6).

The record of the presence/absence of bituberculosity of thespinous process (see Fig. 7) is presented in Table 14. Modernhumans display different percentages of bituberculosity of thespinous process throughout C3-C7 but they do not show thisfeature on the C7. Neandertals exhibit bituberculosity of certaincervicals (Piveteau, 1966; contra Trinkaus, 1983; see Fig. 6), how-ever, with the present fossil record these percentages are lowerthan in our modern comparative sample. The most noticeable dif-ference refers to C6, where none of the Neandertal vertebrae (n¼ 5)

Table 8Raw dimensions (in mm) of the Neandertal third cervical vertebrae (C3), summary staWilcoxon signed rank test between Neandertals and recent humansa.

Variable NeanKebara 2 La Ferrassie 1

(#d)

Maximum dorsoventral diameter (MaxDVDi) (47.5)Superior transverse diameter (SupTrDi) 57.0y (52.0)Inferior transverse diameter (ITrDi) 60.0yCanal dorsoventral diameter (M10) 14.3Canal transverse diameter (M11) 27.7**Body ventral craniocaudal diameter (height) (M1) 12.1Body dorsal craniocaudal diameter (height) (M2) 10.6** 12.8Body median craniocaudal diameter (height) (M3) 8.8**Body superior dorsoventral diameter (M4) 18.3y (17.3)**Body inferior dorsoventral diameter (M5) 16.9 18.6**Body superior transverse diameter (M7) 24.8yBody inferior transverse diameter (M8) 18.5 20.1Uncinate projection (UncPrj) 4.4yPedicles: craniocaudal diameter (PedCrCdDi) 6.5/7.6 5.9/ePedicles: transverse diameter (PedTrDi) 4.1/5.6 �/�Bi-articular diameter (BiArtDi) 21.7y/21.6yUpper articular facet: sagittal diameter (UFaSgDi) 15.1y/18.6yUpper articular facet: transverse diameter (UFaTrD) 13.5y/17.3yLower articular facet: sagittal diameter (LwFaSgDi) 13.6y/14.8yLower articular facet: transverse diameter (LwFaTrDi) 15.2y/16.0yLaminae: craniocaudal diameter (LamCrCdDi) 9.8/9.4Laminae: thickness (LamTh) 3.2/2.9Spinous process: maximum length (M13) 20.5

a Values in parentheses are estimated. Values underlined are outside the range of the mscore and ManneWhitney analyses values with a * or two ** are significantly different fcontain two entries are for the right and left sides (right/left) unless inmodern humans inthe analysis was not performed because the Neandertal sample n < 2. NS ¼ non signific

display a clear bituberculosity despite being present in nearly 60%of our modern comparative sample.

The length of the neck

Neandertals exhibit marginally significant or significantly(p< 0.05) lower dorsal craniocaudal dimensions (height) of the C2-C7 vertebral bodies (see Table 15). The sum of the length of the C2-C7 segments and C2þC4-C7 segments have yielded marginally(p ¼ 0.071) significant results, probably due to the small subsamplein which it has been possible to perform the analysis. In C2-C7, theinclusion of the estimation of the neck length (98.5 mm) of LaFerrassie 1 done by Heim (1976) still yields marginally significantresults with a lower p-value (p ¼ 0.063). The individual values are,however, well within our modern comparative sample and a z-score analysis does not differentiate any of them from our modernsample. However, an increase in the Neandertal sample size mayresult in significant differences from modern humans if furtherNeandertal vertebral fossils show similar morphological patterns tothose observed here.

Discussion

There are significant metric and morphological differences be-tween the Neandertal sample and modern human samples for allcervical vertebrae. When compared with modern humans, Nean-dertals are significantly larger in some dimensions, while smaller inothers. This suggests that there may be shape differences betweenNeandertals and our modern comparative sample (see above). Inorder to investigate shape variation, we performed a preliminaryprincipal components analysis (PCA) using those variables thatshow significant differences in Neandertals (Table 13) in thevertebrae that have the largest number of Neandertal individuals,i.e., C5, C6 and C7 (see Fig. 8 and Table 16). When we plot PC1against PC2, Neandertals are clustered, occupying only a fraction of

tistics of the modern human sample and results of the z-score and the two-tailed

dertals Modern humans WRegourdou 1

(V#d)Shanidar 2 Mean SD Min Max n

43.9 2.3 38.6 47.9 68 e

52.7* 47.6 2.6 42.4 54.9 70 *51.8 50.4 3.0 44.4 57.9 68 e

15.8 14.2 14.9 1.4 12.9 17.8 70 NS26.1* 22.8 1.6 15.1 26.8 70 *12.2 11.9* 14.1 1.1 11.3 16.7 70 **11.8 12.0 13.6 1.0 10.6 15.3 70 **9.4* 10.3 11.3 1.0 9.0 13.3 69 *16.0 14.5 14.4 1.0 12.2 16.8 70 Marg16.6 15.6 15.3 1.0 13.1 18.1 70 *23.8y 20.4 1.5 17.0 26.3 67 e

19.9y (19.2) 20.0 19.4 1.4 16.5 22.6 66 NS4.5 5.1 0.8 3.1 7.0 62 e

6.4/6.6 7.2/e 6.8 0.8 5.2 9.0 69 NS/NS6.1*/5.9* 8.3**/e 4.6 0.7 3.3 6.2 68 NS/*e/18.4 e/19.6 21.6 1.9 17.8 26.2 68 e/Marg9.8/9.0 12.2/e 10.6 1.2 8.0 13.3 67 �/�12.3/12.2 12.0/e 11.6 1.3 7.3 16.3 67 �/�12.3/12.4 13.9*/e 10.4 1.8 7.6 15.2 39 */e11.3/11.5 13.9/e 11.4 1.3 9.0 13.6 39 �/�9.2/9.5 9.6/e 10.7 1.2 7.7 13.9 69 */Marg2.6/2.7 3.7/e 3.2 0.9 1.2 5.2 70 NS/e

19.3 3.2 12.3 27.4 69 e

odern human comparative sample. Values with a y are affected by pathology. The z-rom the modern male comparative sample (* ¼ p < 0.05; ** ¼ p < 0.01). Cells thatwhich only right side has been taken. In theManneWhitney analysis a ‘e’means thatant (p > 0.1). Marg ¼ Marginally significant (0.1 > p > 0.05).

Table 9Raw dimensions (inmm) of the Neandertal fourth cervical vertebrae (C4), summary statistics of themodern human sample and results of the z-score and the two-tailedWilcoxon signed rank test between Neandertals and recenthumansa.

Variable Neandertals Modern humans WKebara 2 La Chapelle-aux-Saints

(#q)La Ferrassie 1

(#c)Regourdou 1b

(V#e þ V#f, V#g)Shanidar 2 Shanidar 4 Mean SD Min Max n

Maximum dorsoventral diameter (MaxDVDi) 51.4y (49.7)** 49.7** (45.0) 43.5 2.2 37.5 48.6 68 *Superior transverse diameter (SupTrDi) 57.0* 58.5y (57.1)* 55.2y (51.0) (52.0) 50.1 2.9 43.2 56.8 70 *Inferior transverse diameter (ITrDi) 60.5** (57.0) 60.0y (57.0) (53.0) 51.7 3.0 45.5 58.3 68 **Canal dorsoventral diameter (M10) 13.3 14.2 (14.5) 14.2 1.2 11.5 16.7 70 NSCanal transverse diameter (M11) 27.0* 26.2 23.3 (26.0) 24.0 1.4 19.9 28.3 70 *Body ventral craniocaudal diameter (height) (M1) 12.5 12.3 11.7 12.1 10.0** 13.4 1.0 10.0 16.1 70 **c

Body dorsal craniocaudal diameter (height) (M2) 11.7 13.2 10.4** 12.5 12.5 13.1 1.0 10.5 15.0 70 MargBody median craniocaudal diameter (height) (M3) 8.8* 10.7 11.0 9.6 9.7 10.3 10.9 0.9 8.7 13.2 69 *Body superior dorsoventral diameter (M4) 19.3y (17.0)* (16.6) (15.0) 14.6 17.3* 14.6 1.1 12.2 17.4 69 *Body inferior dorsoventral diameter (M5) 16.3 20.3y (18.6)** 16.9 16.1 15.4 15.4 15.3 1.1 13.1 18.2 70 *Body superior transverse diameter (M7) 30.9y 20.8 22.8 21.5 1.4 19.0 26.6 69 NSBody inferior transverse diameter (M8) 18.9 28.3y 20.5 20.4y (19.0) 20.0 20.2 1.4 17.0 23.3 70 NSUncinate projection (UncPrj) 4.5y 5.4 5.5 0.9 3.4 7.2 64 e

Pedicles: craniocaudal diameter (PedCrCdDi) 6.5/6.5 e/6.6 7.2 0.7 5.7 9.1 68 �/�Pedicles: transverse diameter (PedTrDi) 6.3*/5.6 4.1/4.0 4.7 0.8 3.1 7.7 68 �/�Bi-articular diameter (BiArtDi) 20.9/21.4 18.1y/20.1y (18.3) 22.3/19.9y e/19.1 21.9 1.9 16.4 27.1 69 NS/MargUpper articular facet: sagittal diameter (UFaSgDi) 13.9y(11.7)/11.9 13.4y/12.2y 11.9/14.6y 12.5/e 10.8 1.1 8.3 13.6 68 */eUpper articular facet: transverse diameter

(UFaTrD)14.3/15.4* 15.5y(14.0)/

15.4y (13.7)16.5y/16.2y 11.3/e 12.0 1.3 8.8 16.0 68 NS/*

Lower articular facet: sagittal diameter (LwFaSgDi) 15.0**/e 15.8y/12.8y (9.8) 17.9y/10.6 9.1/e 9.8 1.3 7.2 12.9 38 NS/NSLower articular facet: transverse diameter

(LwFaTrDi)16.2**/16.4** 14.6y/15.1 15.5y(13.8)/

17.2y10.7/e 11.9 1.3 8.9 16.3 37 NS/*

Laminae: craniocaudal diameter (LamCrCdDi) 10.6/10.4 e/10.2 10.9/11.6 10.8 1.2 8.4 14.2 68 NS/NSLaminae: thickness (LamTh) 2.5/3.2 e/2.7 2.4/3.2 2.6 0.7 1.2 4.5 68 NS/NSSpinous process: maximum length (M13) (20.0) 25.3 20.0 20.2 3.2 12.7 27.6 69 NS

a Values in parentheses are estimated. Values underlined are outside the range of themodern human comparative sample. Values with a y are affected by pathology. The z-score andManneWhitney analyses values with a * ortwo ** are significantly different from the modern male comparative sample (*¼ p< 0.05; **¼ p< 0.01). Cells that contain two entries are for the right and left sides (right/left) unless in modern humans in which only right sidehas been taken. In the ManneWhitney analysis a ‘e’ means that the analysis was not performed because the Neandertal sample n < 2. NS ¼ non significant (p > 0.1). Marg ¼ Marginally significant (0.1 > p > 0.05).

b In the Regourdou 1 individual, the values of MaxDVDi, SupTrDi, ITrDi and M10 have been calculated on a photograph of the vertebra published at Piveteau (1966).c This variable in Neandertals is still significantly different from our modern comparison sample even if we remove the extremely low value of Shanidar 4.

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Table 10Raw dimensions (in mm) of the Neandertal fifth cervical vertebrae (C5), summary statistics of the modern human sample and results of the z-score and the two-tailed Wilcoxon signed rank test between Neandertals and recenthumansa.

Variable Neandertals Modern humans WKebara 2b La Chapelle-aux-Saints

(#o)La Ferrassie 1

(#e)Regourdou 1c

(V#h, V#i)Shanidar 1 Shanidar 2 Shanidar 4 Mean SD Min Max n

Maximum dorsoventral diameter (MaxDVDi) 61.1y (59.5)** 58.8** (55.0)** 60.0** 55.0** 45.9 2.4 40.2 53.5 67 **Superior transverse diameter (SupTrDi) 58.7* 56.9y 57.4y (55.5) 53.0 54.0 (49.0) 51.1 3.0 44.6 57.4 70 MargInferior transverse diameter (ITrDi) 59.1* 55.9 61.4y (60.5)** 52.0 (56.5) 53.1 2.9 47.1 59.7 70 *Canal dorsoventral diameter (M10) 15.3 12.7 14.7 14.4 15.5 13.4 14.3 1.2 12.0 17.3 70 NSCanal transverse diameter (M11) 26.8 27.3 25.4 27.8 27.3 25.4 24.7 1.8 15.7 29.8 70 **Body ventral craniocaudal diameter (height) (M1) 11.1 9.4y 11.9 9.5** 10.4* 10.1* 13.1 1.3 10.6 20.0 69 **Body dorsal craniocaudal diameter (height) (M2) (11.0)* 12.9 11.4 11.9 12.5 12.5 13.0 1.0 10.4 15.2 70 *Body median craniocaudal diameter (height) (M3) 9.3 10.5 9.7 9.5 10.1 9.8 10.8 1.0 8.4 13.0 69 **Body superior dorsoventral diameter (M4) 12.7 16.2 14.2 13.0 13.8 14.5 1.2 12.3 17.8 70 NSBody inferior dorsoventral diameter (M5) (14.5) 20.4y 16.3 15.4 13.8 14.5 15.9 1.2 13.4 19.7 70 MargBody superior transverse diameter (M7) 30.8y 22.4 24.7 (22.3) 22.8 1.5 19.8 27.5 70 NSBody inferior transverse diameter (M8) 19.7 32.5y 20.9 18.8 (21.0) 20.3 20.2 21.2 1.6 18.1 26.3 70 MargUncinate projection (UncPrj) 3.3y 5.6 5.8 0.8 4.2 8.5 67 e

Pedicles: craniocaudal diameter (PedCrCdDi) e/7.3 6.3/6.3 e/7.9 (7.4)/7.4 8.0/e 7.0 0.9 5.2 9.6 69 NS/NSPedicles: transverse diameter (PedTrDi) e/4.2 3.9/3.9 e/4.9 e/4.6 4.8/5.7 5.2 0.7 3.6 6.5 68 NS/MargBi-articular diameter (BiArtDi) 21.1/e 21.5y/21.1 21.5y/20.6 e/18.4* 21.8 1.6 18.2 25.1 70 e/MargUpper articular facet: sagittal diameter (UFaSgDi) 11.9/10.9 14.3y/11.6 12.1/11.9 e/9.8 10.3 1.2 8.0 13.8 70 */NSUpper articular facet: transverse diameter (UFaTrD) 15.5**/15.4** 14.7y/14.6* e/18.2y e/12.5 12.2 1.2 9.3 15.8 70 e/*Lower articular facet: sagittal diameter (LwFaSgDi) (9.6)/e 12.9*/12.1 e/13.2** 9.4 1.4 7.1 13.8 39 NS/*Lower articular facet: transverse diameter (LwFaTrDi) 12.6/e 13.2/13.0 13.4y/15.3y e/10.0 12.0 1.4 9.4 14.9 39 NS/NSLaminae: craniocaudal diameter (LamCrCdDi) 10.4/10.4 (10.0)/11.3 11.8/12.3 11.0/10.0 10.4/12.3 11.1 1.2 8.9 15.6 70 NS/NSLaminae: thickness (LamTh) 3.0/3.1 3.2/2.2 3.6*/3.7* 3.0/3.1 3.6*/3.9* 2.3 0.6 1.4 4.1 70 **/*Spinous process: maximum length (M13) 27.4 32.1** 26.4 30.0** 28.1 22.4 2.9 15.9 28.4 67 **Spinous process: maximum transverse diameter

of the tip (SpPrTrDiTp)9.1 (13.5) 11.0 13.3 2.6 7.5 18.7 34 NS

a Values in parentheses are estimated. Values underlined are outside the range of the modern human comparative sample. Values with a y are affected by pathology. The z-score andManneWhitney analyses values with a * ortwo ** are significantly different from the modern male comparative sample (*¼ p< 0.05; **¼ p< 0.01). Cells that contain two entries are for the right and left sides (right/left) unless in modern humans in which only right sidehas been taken. In the ManneWhitney analysis a ‘e’ means that the analysis was not performed because the Neandertal sample n < 2. NS ¼ non significant (p > 0.1). Marg ¼ Marginally significant (0.1 > p > 0.05).

b The spinous process of the C5 of Kebara 2 is wrongly reconstructed. There is part of the spinous process missing between its tip and its base. Thus, the spinous process is longer, and thus the MaxDVDi longer than thereconstruction described at Arensburg (1991).

c In the Regourdou 1 individual, the values of right LamCrCdDi and right LamTh have been taken from Piveteau (1966).

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Table 11Raw dimensions (in mm) of the Neandertal sixth cervical vertebrae (C6), summary statistics of the modern human sample and results of the z-score and the two-tailedWilcoxon signed rank test between Neandertals and recenthumansa.


(#p)La Ferrassie 1

(#f)Regourdou 1(V#j, V#ah)

Shanidar 1 Shanidar 2b Shanidar 3 Shanidar 4 Mean SD Min Max n

Preserved maximum dorsoventral diameter 61.8 51.5Maximum dorsoventral diameter (MaxDVDi) 64.3** (64.0)** (64.0)** 58.8 52.1 3.6 43.0 59.6 68 **Superior transverse diameter (SupTrDi) 57.6 56.1 (53.0) (57.0) 52.4 3.0 45.7 59.3 69 *Inferior transverse diameter (ITrDi) 56.6 56.1 (55.3) (56.5) 51.9 3.1 46.0 60.7 70 **Canal dorsoventral diameter (M10) (15.3) 13.0 (16.8)* 15.8 14.2 1.2 11.9 17.6 70 NSCanal transverse diameter (M11) 27.1 27.6 28.0* 28.0* 24.7 25.0 1.5 21.7 29.7 70 **Body ventral craniocaudal diameter (height) (M1) (11.5) 11.4y 12.2 10.4* 11.9 9.7** 12.6 1.0 9.7 15.2 69 **c

Body dorsal craniocaudal diameter (height) (M2) 12.1 12.7 12.7 12.9 12.3 12.5 12.4 13.1 1.0 10.5 15.0 70 MargBody median craniocaudal diameter (height) (M3) 9.8 (10.5) 10.1 10.2 10.0 10.0 10.0 10.6 1.1 8.6 13.2 69 NSBody superior dorsoventral diameter (M4) 14.0 16.9 (14.0) 13.4 14.2 15.3 15.3 1.1 12.8 18.7 70 NSBody inferior dorsoventral diameter (M5) 15.6 17.1 (16.0) 15.2 15.5 15.3 17.3 16.2 1.1 13.9 19.1 70 NSBody superior transverse diameter (M7) 31.3y 21.5 (28.0)* 22.5 22.7 24.5 1.6 20.9 29.8 69 NSBody inferior transverse diameter (M8) (22.8) 28.7** 22.6 21.2 25.2 23.6 23.8 1.6 20.3 28.5 70 NSUncinate projection (UncPrj) (4.5)* 5.5 5.4 6.3 0.8 4.6 8.0 65 *Pedicles: craniocaudal diameter (PedCrCdDi) e/7.3 6.3/5.9 e/(7.7) 7.9/7.6 e/7.5 6.7 0.9 4.5 8.9 66 NS/NSPedicles: transverse diameter (PedTrDi) e/5.9 4.1*/5.3 5.1/e 5.4/5.2 e/6.0 5.5 0.7 4.2 7.2 65 NS/NSBi-articular diameter (BiArtDi) (right-left) 22.5/23.4 22.7y(19.9)/25.1y 24.7y/22.9 e/23.9 23.1 1.7 20.1 27.3 68 NS/NSUpper articular facet: sagittal diameter (UFaSgDi) 9.7/e 10.2/11.6 9.9/10.4 e/9.5 e/9.4 9.5 1.3 5.9 13.2 69 NS/NSUpper articular facet: transverse diameter (UFaTrD) e/12.8 13.3/12.9 16.7y/15.5 e/12.1 12.4 1.6 8.5 16.2 69 e/NSLower articular facet: sagittal diameter (LwFaSgDi) 10.3/10.0 (10.2)/11.0 e/14.0** e/12.3** 9.3 1.1 6.6 11.4 40 NS/**Lower articular facet: transverse diameter (LwFaTrDi) 14.1/14.5 14.0/13.5 18.7y/17.2y e/13.9 12.1 1.5 9.1 14.8 40 Marg/*Laminae: craniocaudal diameter (LamCrCdDi) 13.7/12.6 12.2/12.3 12.3/12.0 11.4/11.7 12.8/13.0 12.6/11.6 12.3 1.5 9.5 16.9 70 NS/NSLaminae: thickness (LamTh) 4.5*/4.3 4.6*/3.6 e/4.6* 4.0/4.5* 4.0/4.0 3.7/4.1 3.0 0.7 1.7 4.7 70 **/**Spinous process: maximum length (M13) 33.0 37.4** 35.0* 28.7 36.4** 26.6 3.5 18.1 34.7 68 **Spinous process: angle (M12) (5�)** (19�)** (14�)** 38.3 8.8 26.0 59.5 19 **Spinous process: minimum transverse diameter

(SpPrMinTrDi)4.1 6.3 5.0 5.4 5.9 5.2 1.3 2.7 9.2 69 NS

Spinous process: maximum transverse diameterof the tip (SpPrTrDiTp)

8.2 (11.0) 13.7 (10.6) 11.0 10.0 2.0 5.2 15.3 63 NS

a Values in parentheses are estimated. Values underlined are outside the range of the modern human comparative sample. Values with a y are affected by pathology. The z-score andManneWhitney analyses values with a * ortwo ** are significantly different from the modern male comparative sample (*¼ p< 0.05; **¼ p< 0.01). Cells that contain two entries are for the right and left sides (right/left) unless in modern humans in which only right sidehas been taken. In the ManneWhitney analysis a ‘e’ means that the analysis was not performed because the Neandertal sample n < 2. NS ¼ non significant (p > 0.1). Marg ¼ Marginally significant (0.1 > p > 0.05).

b The M12 value of Shanidar 2 has been taken from Trinkaus (1983).c This variable in Neandertals is still significantly different from our modern comparison sample even if we remove the extremely low value of Shanidar 4.

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Table 12Raw dimensions (in mm) of the Neandertal seventh cervical vertebrae (C7), summary statistics of the modern human sample and results of the z-score and the two-tailed Wilcoxon signed rank test between Neandertals andrecent humansa.


(#n)La Ferrassie 1

(#g)Regourdou 1(V#k, V#al)

Shanidar 1 Shanidar 2 Shanidar 3 Mean SD Min Max n

Maximum dorsoventral diameter (MaxDVDi) 62.0 65.8* >63.1# (62.0) (60.9) 59.0 2.7 52.6 69.4 68 **Superior transverse diameter (SupTrDi) 55.3 (54.0) 52.1 3.2 44.4 59.5 67 NSInferior transverse diameter (ITrDi) 52.6 59.5y 53.2 55.4* (54.0) (53.2) 49.4 3.0 41.0 57.4 68 **Canal dorsoventral diameter (M10) 13.4 15.7 16.0 14.4 1.1 12.2 18.2 69 NSCanal transverse diameter (M11) 25.3 (25.0) 26.0 25.0 26.5 24.3 1.5 21.7 30.3 69 *Body ventral craniocaudal diameter (height) (M1) 11.9* 13.4 (13.5) 13.0 (13.0) 12.1* 14.1 1.0 11.4 16.2 70 **Body dorsal craniocaudal diameter (height) (M2) 14.3 14.1 14.0 12.9 14.2 14.4 1.1 11.8 16.7 69 NSBody median craniocaudal diameter (height) (M3) 10.9 11.9 11.4 12.5 11.4 11.5 12.2 1.1 10.2 14.9 69 NSBody superior dorsoventral diameter (M4) (17.0) 15.7 14.0 (16.0) 18.0* 15.8 1.1 13.7 18.6 70 NSBody inferior dorsoventral diameter (M5) 16.1 (16.2) 16.2 15.8 17.6 15.4 1.2 13.3 18.0 70 MargBody superior transverse diameter (M7) (30.8) (27.5) 26.8 1.8 23.2 31.2 69 NSBody inferior transverse diameter (M8) 28.1 (27.0) 26.2 32.0* 27.8 2.1 23.1 34.2 69 NSUncinate projection (UncPrj) 5.0 5.6 1.1 3.3 8.1 66 e

Pedicles: craniocaudal diameter (PedCrCdDi) e/9.4** 6.0/7.6 9.6**/9.6** 8.1/e 7.2 0.8 5.1 9.3 67 NS/*Pedicles: transverse diameter (PedTrDi) e/7.4 4.5*/7.0 6.3/7.7 5.6/e 6.2 0.8 4.4 8.3 68 NS/*Bi-articular diameter (BiArtDi) (23.8)/e 24.4y/22.2y e/26.4y(25.5) 27.0 2.0 21.3 30.8 68 �/�Upper articular facet: sagittal diameter (UFaSgDi) e/8.9 8.7/8.4 e/10.7 8.9 1.1 6.0 12.0 69 e/NSUpper articular facet: transverse diameter (UFaTrD) 15.5/11.9 e/18.0 13.2 2.0 9.2 18.2 69 e/NSLower articular facet: sagittal diameter (LwFaSgDi) e/10.0 18.8y/15.3y 14.9**/13.7* e/11.7 e/13.0 10.6 1.6 7.7 14.2 36 e/MargLower articular facet: transverse diameter (LwFaTrDi) e/15.2 20.1y/16.7y 16.4/16.5 e/17.1 13.6 2.2 9.1 16.9 36 e/*Laminae: craniocaudal diameter (LamCrCdDi) e/14.5 13.4/13.9 e/14.3 13.3/13.8 13.2/14.8 15.5/e 14.9 1.3 11.6 17.7 69 Marg/NSLaminae: thickness (LamTh) e/5.5 6.0/5.1 5.5/5.5 5.0/5.5 5.3/6.0 4.8/5.2 4.7 1.0 2.6 7.2 69 NS/*Spinous process: maximum length (M13) 36.0 36.5 41.3** 33.2 (36.0) (34.8) 41.8** 34.1 2.4 28.0 41.7 69 **Spinous process: angle (M12) 20.5� 15�* 26� 17 �* 34.5 8.5 21.0 53.0 27 **Spinous process: minimum transverse diameter

(SpPrMinTrDi)4.4 6.8 4.9 4.3 5.2 (6.2)## 6.4 1.3 3.6 11.6 69 *

Spinous process: maximum transverse diameterof the tip (SpPrTrDiTp)

6.6* 12.5* (9.5) 9.5 (9.3) (10.8)## 9.6 1.3 6.7 12.7 66 NS

# ¼ Preserved value; ## ¼ Measured on CT scans.a Values in parentheses are estimated. Values underlined are outside the range of themodern human comparative sample. Values with a y are affected by pathology. The z-score andManneWhitney analyses values with a * or

two ** are significantly different from the modern male comparative sample (*¼ p< 0.05; **¼ p< 0.01). Cells that contain two entries are for the right and left sides (right/left) unless in modern humans in which only right sidehas been taken. In the ManneWhitney analysis a ‘e’ means that the analysis was not performed because the Neandertal sample n < 2. NS ¼ non significant (p > 0.1). Marg ¼ Marginally significant (0.1 > p > 0.05).

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Table 13Synthetic summary table of the significantly different metrical features for the lower cervical spine of Neandertals.

Trait Variable(s) used to assess this trait C3 C4 C5 C6 C7

Dorsoventrally longer vertebrae MaxDVDi X X X XWider distance between upper articular facets SupTrDi, ITrDi X X X X XWider vertebral canal M11 X X X X XCraniocaudally smaller vertebral bodies M1, M2, M3 X X X X XAnteroposteriorly larger vertebral bodies M4, M5 X X X? X?Craniocaudally shorter laminae LamCrCdDi XThicker laminae LamTh X X X?Longer spinous processes M13 X X XMore horizontal spinous processes M12 e e e X X

Figure 4. Length of the spinous processes (in mm) of C5-C7 in Neandertals. Nean-dertals show longer spinous processes in each of these vertebrae (see Tables 10e12and text) but there is an increasing overlapping distribution as we move cranial tocaudal elements.


the morphospace. When PC3 is considered, we note that Nean-dertals cluster as a completely separate group. Principal component3 is influenced by the length of the spinous process (M13), theoverall maximum dorsoventral diameter, and the thickness of thelamina. As we consider more caudal cervical vertebrae, there ap-pears to be morphological convergence with the range of variationfound in the modern human sample, as happens with M13 (seeFig. 4). In summary, these results reinforce our view that Nean-dertal cervical vertebrae are morphologically different from thoseof modern humans. We do however recognize that more fossils areneeded in order to fully understand the Neandertal cervical anat-omy and variation.

Some of the metric differences detected are tightly interrelatedbetween the different vertebrae that compose the cervical spine.Longer and/or more horizontal spinous processes (at least in C6-C72) together with dorsoventrally larger vertebral bodies (C3-C4)result in dorsoventrally longer vertebrae (C3-C7). In the case of thehorizontality of the spinous process, it has been quantified only in

2 We have not quantified the horizontality of the spinous processes in the C3-C5segment. In modern humans, due to the short length of the spinous processes atthis level, rather than the inclination of this process per se, we would be mostlymeasuring the inclination of the laminae.

the lowermost two vertebrae (C6-C7) but more horizontal spinousprocesses may be present in more cranially placed vertebrae. It canbe hypothesized that the Neandertal C2-C7 vertebrae are wider asthe result of a more lateral position of the articular pillars, whichcould be due to a slight change of orientation of the pediclesresulting in wider vertebral canals. In certain cases, facets are also

Figure 5. Length (in mm) (x) and orientation (in degrees) (y) of the spinous process inC6 and C7. Neandertals show longer and more horizontal spinous processes. Note thatwhile in the C6 there is no overlapping. Also note that the cervical depicted to illustratethe variables is a modern C7 in left lateral view, with the cranial surface of thevertebral body horizontally oriented.

Figure 6. Comparison of the fifth (C5), sixth (C6) and seventh (C7) cervicals of La Chapelle-aux-Saints (LC) Neandertal with a modern human from our European sample withmeasurements close to the modern mean. Note the longer and more horizontally oriented spinous processes of LC and the larger superior transverse diameter (SupTrDi), which isrelated to a mediolaterally wider vertebral canal (M11).

Table 14Bituberculosity of the spinous process in the lower cervical spine (C3-C7).

Species/individual C3 C4 C5 C6 C7 References

Homo neanderthalensisKebara 2 N NLa Chapelle-aux-Saints 1 N Y N N This studyLa Ferrassie 1 Y?* N N N N This studyRegourdou 1 Y Y N Piveteau, 1966; Gómez-Olivencia

et al., in pressShanidar 1 Partially? N Based on Stewart, 1962Shanidar 2 N Partially? N Stewart, 1962; Trinkaus, 1983Shanidar 3 N This studyShanidar 4 N NTotal Neandertals% Presence (Y) 50.00 25.00 40.00 0.00 0.00% Absence (N) 50.00 75.00 40.00 80.00 100.00% Partial 0.00 0.00 20.00 20.00 0.00n 2 4 5 5 5

Homo sapiensModern comparative sample% Presence (Y) 73.91 91.18 92.65 58.82 0.00 This study% Absence (N) 21.74 7.35 5.88 41.18 95.65% Partial 4.35 1.47 1.47 0.00 4.35n 69 68 68 68 69

Y ¼ presence of bituberculosity; N ¼ absence of bituberculosity; Partially ¼ the bituberculosity present in the spinous process is not clearly displayed (less than 1 mm ofdifference). Spaces in blank represent absent vertebrae or spinous processes. * ¼ partially broken. See also Fig. 7.


Table 15Comparative analysis of the length of the neck: Individual and dorsal craniocaudal dimension (AxDCrCdDi and M2) of the C2-C7 segment.

Dorsal height C2 C3 C4 C5 C6 C7 C2-C7 C2, C4-C7

Kebara 2 10.6 (11.0) 12.1La Chapelle (33.0) 11.7 12.9 12.7 14.3 84.6La Ferrassie 1 (34.5) 12.8 13.2 11.4 12.7Regourdou 1 33.0 11.8 10.4 11.9 12.9 14.1 94.1 82.3Shanidar 1 12.5 12.3 14.0Shanidar 2 33.7 12.0 12.5 12.5 12.5 12.9 96.1 84.1Shanidar 3 14.2Shanidar 4 12.4Neandertals 33.6 � 0.7

(n ¼ 4)11.8 � 0.9(n ¼ 4)

12.1 � 1.1(n ¼ 5)

12.0 � 0.7(n ¼ 6)

12.5 � 0.3(n ¼ 7)

13.9 � 0.6(n ¼ 5)

95.1 � 1.4(n ¼ 2)

83.7 � 1.2(n ¼ 3)

Modern males 34.3 � 2.3(n ¼ 68)

13.6 � 1.0(n ¼ 70)

13.1 � 1.0(n ¼ 70)

13.0 � 1.0(n ¼ 70)

13.1 � 1.0(n ¼ 70)

14.4 � 1.1(n ¼ 70)

101.0 � 6.0(n ¼ 67)(80.0e112.0)

87.4 � 4.7(n ¼ 66)

Results of theManneWhitney

Marg(0.05 < p < 0.1)

**(p < 0.01)

Marg(0.05 < p < 0.1)

*(p < 0.05)

Marg(0.05 < p < 0.1)

NS(p > 0.1)

Marg(0.05 < p < 0.1)

Marg(0.05 < p < 0.1)

* ¼ p < 0.05; ** ¼ p < 0.01; Marg ¼ Marginally significant (0.1 > p > 0.05); NS ¼ non significant.Note that there are differences in the modern male subsamples: the overall smaller European sample has a C2-C7 segment length of 98.9 � 6.1 while in the slightly largerEuroamerican sample it is 103.5 � 5.0.


significantly larger in the mediolateral dimension. The thickness ofthe lamina is related to the loads applied to it (Pal and Routal,1996).Thus, it is possible that the thick laminae of C5-C7 are related to thelong and horizontal spinous process and to a change of the weighttransmission in the lower cervical spine. However more research isrequired to clarify this variation.

Some of the differences that characterize the Neandertal cervicalspine observed above are present in more than one vertebra (e.g., awider canal due to a more lateral position of the articular pillars),which is a reflectionof the integrationnecessarywithin the vertebralcolumn in order for elements to properly articulate. Some of thesedifferences present in the cervical spine of Neandertals can also benoted in the upper thoracic spine (Gómez-Olivencia et al., in press).

Some of the differences in the Neandertal cervical spinedescribed in this study have been identified previously (see Table 1and references therein). However, in most cases, it was concludedthat Neandertal vertebrae were more robust but otherwise similarto our own species. This study has identified a number of differencesin the size and shape of the cervical vertebrae of Neandertals andmodern humans. The different results could stem from methodo-logical differences, variation in the anatomical determination ofcertain vertebrae of key specimens, underlying morphologicalvariation that can only be detected with the expanded Neandertalsample used here or a different approach in thewayNeandertals are

Figure 7. Three examples of the presence of a bituberculous tip of the spinous process in Ne

now perceived. Our analysis incorporates the largest Neandertalsample to date and provided the first statistical analyses of Nean-dertal cervical variation, however the attribution of specific verte-brae to their anatomical position (especially in the case of thecervical spine of La Chapelle or Shanidar 3) has changed, whichmayaffect the perceived differences (see Figure S2 in the SupplementaryOnline Information).

Limitations of the present study

There are several methodological limitations to this study. First,themodern comparative sample for themetric analysis is a modernindustrial population. For certain traits of the atlas and axis, someUpper Pleistocene H. sapiens from Europe, the MediterraneanLevant and North Africa have been included. In all of these features,the Upper Pleistocene sample follows the modern industrialpattern, which provides preliminary support for the interpretationthat Neandertals display a distinct morphological pattern in thecervical spine, and that the differences found are not an artefact ofusing modern industrial comparative samples. There is, however, aneed to study the patterns of variation of the modern human spinerelated to different activity patterns in order to fully understand theplasticity of this anatomical region. Thus, integrative approaches tothe study of the spine morphology of the Upper Paleolithic and

andertals: (a) C4 of Regoudou 1, (b) C5 of La Chapelle-aux-Saints, (c) C5 of Regoudou 1.

Figure 8. Scatterplot of the PCA for C5, C6, C7. Modern humans are represented by black circles while Neandertals are represented by triangles and a shaded poligon. The PCA wasrun without the fossils and then PC scores were generated for them. The Neandertals represented in the C5 scatterplots are Kebara 2 (K2), La Chapelle-aux-Saints (LC), La Ferrassie 1(LF1), Shanidar 1 (Sh1), Shanidar 2 (Sh2) and Regourdou 1 (R1). The Neandertals represented in the C6 scatterplots are K2, LF1, Sh1, Sh2 and R1. The Neandertals represented in theC7 scatterplots are K2, LC, Sh1, Sh2 and R1. Missing values were substituted by the mean value of the corresponding sample.


modern hunter gatherers are necessary to fully understand po-tential differences in the spine due to differences in the activitypattern.

Significance of the morphology of the Neandertal neck:biomechanical and postural implications

From a biomechanical point of view, the length and angle of thespinous processes directly influences the lever arm for all of themuscles and ligaments that attach to it: the neck and head

extensors and rotators. Thus, longer andmore horizontally orientedspinous processes increase the lever arm for these muscles(Shapiro, 2007). Additionally, the more lateral position of thearticular pillars in the cervicals indicated by wider vertebrae wouldincrease the mediolateral stabilization of the cervical spine. Thus,when compared with modern humans Neandertals show a cervicalmorphology that seems to be more stable in both mid-sagittal andtransverse planes. This could parallel differences in the neckbiomechanics due to differences in skull shape between the Ne-andertals and modern humans.

Table 16Percentage of the variance explained and factorevariable correlations (factor-loadings) for C5, C6 and C7a.

C5 C6 C7Factor 1 Factor 2 Factor 3 Factor 4 Factor 1 Factor 2 Factor 3 Factor 4 Factor 1 Factor 2 Factor 3 Factor 4

Explained variance 32.4% 18.6% 14.0% 10.7% 32.5% 19.3% 15.8% 11.8% 30.6% 19.4% 16.6% 11.4%Cumulative variance 32.4% 51.0% 65.0% 75.7% 32.5% 51.8% 67.6% 79.4% 30.6% 50.0% 66.6% 78.0%

MaxDVDi �0.30 �0.06 �0.43 �0.25 �0.36 �0.06 0.51 �0.05 �0.29 �0.20 0.45 0.29ITrDi �0.33 0.14 �0.20 0.50 �0.21 �0.05 0.01 0.71 �0.13 �0.34 0.29 �0.45M11 �0.28 �0.08 �0.18 0.66 �0.16 �0.21 �0.07 0.62 �0.16 �0.19 0.10 �0.70M1 �0.44 0.11 0.20 �0.19 �0.46 0.06 �0.25 �0.05 �0.47 0.11 �0.25 0.01M2 �0.43 0.14 0.38 �0.03 �0.46 �0.05 �0.34 �0.16 �0.50 0.09 �0.25 0.09M3 �0.41 0.06 0.43 �0.17 �0.41 �0.05 �0.42 �0.20 �0.47 0.17 �0.31 �0.09M4 �0.12 �0.68 �0.06 �0.04 0.06 �0.68 0.10 �0.14 �0.03 �0.63 �0.19 0.19M5 �0.18 �0.65 0.04 �0.09 0.01 �0.69 �0.03 �0.07 �0.04 �0.60 �0.28 0.22M13 �0.33 0.10 �0.34 �0.10 �0.37 0.00 0.43 �0.16 �0.38 �0.07 0.34 0.29LamTh (Right side) �0.14 0.19 �0.50 �0.40 �0.26 0.10 0.41 �0.02 �0.18 0.10 0.51 0.35

a These values have been calculated on the modern human comparative sample. The PCA was based on the correlation matrix and missing values were substituted by thesample mean.


When compared with Middle Pleistocene humans, both Nean-dertals and modern humans are more encephalized (Arsuaga et al.,1997). Neandertals have longer skulls than their ancestors due toincreased brain size within an ‘archaic’ endocranial model, whilethey maintain the primitive pattern of having a large degree ofprognathism (Arsuaga et al., 1997; Bruner et al., 2003). Modernhumans are more encephalized than their Middle Pleistocene an-cestors, but the shape of their skull is less elongated than that ofNeandertals due to an early postnatal globularization phase in thebrain ontogeny (Gunz et al., 2010). In addition, modern humansdisplay reduced prognathism relative to both their Middle Pleis-tocene ancestors and Neandertals (Trinkaus, 2003). Thus, it can behypothesized that the motion of Neandertal heads would havelarger inertial moments than modern humans in the mid-sagittalplane. This could account for the presence of a more stable neckshape in the mid-sagittal plane among Neandertals. In fact, longerand more horizontally oriented processes would locate the liga-mentum nuchae into a more favourable position relative to the axisaround which head flexion occurs. This would result in greaterpassive mechanism for resisting the flexion of the head.

Neandertals, however, seem to also show a more stable neck inthe coronal plane. This fact still requires further research and futurestudies on allometry and head-neck anatomical integration shouldtest whether this anatomical feature is simply a byproduct of amore stable neck in flexion-extension or if it is related to otheranatomical features.

Regarding the cervical posture and degree of lordosis in Nean-dertals, longer spinous processes, especially in C5-C6, may makethe neck extension more difficult, and it would require a lesslordotic cervical spine to maintain a similar range of movementcompared with modern humans. On the other hand, the morehorizontal orientation of the spinous processes is alreadycompensating to allow a larger degree of extension movements.Additionally, the anteroposteriorly larger vertebral bodies might berelated to larger surface area or/and may hint that there was areduced range of motion in the sagittal plane (i.e., less flexion-extension), which could be compensated by the craniocaudallyshort vertebral body.

Neandertals show a less lordotic lumbar spine, which wasalready present in their Middle Pleistocene ancestors of Sima de losHuesos (SH) and that is likely derived in this lineage (Been, 2005;Gómez-Olivencia, 2009; Bonmatí et al., 2010; Been et al., 2012). Thechain of correlations between the pelvic incidence, sacral slope,lumbar lordosis and thoracic kyphosis (Boulay et al., 2006) ledBonmatí et al. (2010) to suggest the presence of an overall lesscurved spine in both Neandertals and their Middle Pleistocene

ancestors from Sima de los Huesos. Thus, it is reasonable to hy-pothesize that Neandertals also possessed a less lordotic cervicalspine, but needs further testing and should be the subject of futurestudies. It is interesting though to explore some of the implicationsof Neandertals having a less lordotic cervical spine. A less lordoticcervical spine would increase the stress on the ventral part of thevertebral bodies. In the elderly individuals, this could lead todegenerative processes such as those seen in the individual of LaChapelle or in Krapina, which would better explain the unusualpattern on these individuals that was attributed to trauma byDawson and Trinkaus (1997) and Gardner and Smith (2006).

Origin of the morphological differences in the Neandertal cervicalspine

Our understanding of the polarity (primitive versus derived) ofthe differences detected in the Neandertal cervical spine remainsuncertain, due to the paucity of cervical remains from the Middleand Lower Pleistocene. Based on published results from Sima de losHuesos (Middle Pleistocene) and other Lower Pleistocene sites suchas Gran Dolina-TD6 (Carretero et al., 1999; Gómez-Olivencia et al.,2007), we can make some preliminary observations. First,regarding the atlas, there is an increase of small tubercles for theattachment of the transverse ligament for the axis and a gracili-zation of the posterior tubercle of the posterior arch in the Nean-dertal lineage. The significance of the small tubercles for theattachment of the transverse ligament for the axis is difficult toexplain. The gracilization of the posterior tubercle of the posteriorarch, which is the insertion point for rectus capitis posterior minorcould be due to a change in the biomechanical loading of this regionas a result of an increase in encephalization of Neandertals andrelated changes in the lower cervical spine. The dorsoventrallylonger canal of the C1 seems to be related to a dorsoventrally longerforamen magnum in both SH and Neandertals (Gómez-Olivenciaet al., 2007). Second, the axis is craniocaudally low and medi-olaterally wide among both SH and Neandertals, and thus, it is not amorphological novelty of the latter. However, Neandertals hadlonger spinous processes in C6 and C7 when compared with theirMiddle Pleistocene ancestors (Gómez-Olivencia et al., 2007).Finally, a lower inclination of the spinous process of the lowermostcervicals has been reported in Lower (WT-15000, TD6) and MiddlePleistocene (SH) hominins (Carretero et al., 1999), Thus, this aspectwould be a retention of a primitive character and more inclinedspinous process of the lower cervicals would be derived for modernhumans (Trinkaus, 2006). In summary, the ongoing study of theSima de los Huesos material will provide the key to better


understand the evolution of the spine in both the Neandertal andmodern human lineages as it will clarify the phylogenetic polarityof the detected differences in the neck of Neandertals and modernhumans. Additional studies on the ontogeny of this anatomicalregion will provide additional clues in this particular area.

Length of the neck and Neandertal speech capabilities

The metric analyses performed in this study indicate that theheight of the cervical vertebrae of Neandertals is slightly lower thanin our modern comparative sample. However, it should be notedthat: a) the length of the Neandertal neck is well within themodernrange of variation and close to their mean; b) if Neandertals had aless lordotic neck, then the perceived differences between Nean-dertals and modern humans would diminish; and c) the length ofthe vertebral column covaries with the overall stature of the in-dividuals. In fact, the shorter neck length in our modern Europeansubsample parallels their shorter stature when compared with ourEuroamerican sample. Thus, we hypothesize that part of theslightly shorter Neandertal neck could derive from stature differ-ences between Neandertals and our modern sample (see alsoCarretero et al., 2012 and references therein). Indeed, in light of thenew anatomical positions proposed for certain Neandertal verte-brae (see Gómez-Olivencia, 2013a; Gómez-Olivencia et al., in press)a reassessment of the knowledge of trunk versus lower limb pro-portion in Neandertals is warranted, and thus a proper context inwhich to compare the absolute length of its neck.

The differences in the proportion between the horizontal andvertical segment of the supralaryngeal vocal tract (SVT) in Nean-dertals stem from the long horizontal segment (i.e., the basioneprosthion length), rather than from the vertical segment.Lieberman’s (2007a) suggestion that the vocal tract must have a 1:1proportion between the horizontal and the vertical segment toproduce the full range of human speech can be considered. Due tothe relative short neck compared to their long horizontal segment(with a ratio of 0.79), in order for Neandertals to possess a modernvocal tract, their larynx would be in their chest (Lieberman, 2007b),something anatomically not seen in any primate species, ergo Ne-andertals did not have a modern vocal tract and thus were not ableto produce the full range of human speech. There are, however,different lines of evidence that go against the necessity of having a1:1 proportion between the vertical and the horizontal segments ofthe SVT. Simulations have shown that a 1:1 ratio between thehorizontal and vertical segments is not necessary for the produc-tion of the point vowels (i, a, u) (Boë et al., 2002). In modern humanontogeny, the ratio between the vertical and the horizontal seg-ments increases until attaining a proportion of 1:1 in adulthood(Lieberman et al., 2001), but children have the potential to producethe full range of human speech before the different segments of theSVT reach 1:1 (Boë et al., 2007).

From an evolutionary point of view, neck length has changedlittle since the Middle Pleistocene (Gómez-Olivencia, 2009;Martínez et al., in press), while in our species there has been adecrease in the horizontal segment of the SVT. In short, our resultssuggest that the Neandertal SVT is “compatible with the full rangeof speech sounds exhibited in modern human spoken language”,something that was already present in their Middle Pleistoceneancestors (see Martínez et al., in press, and references therein).

Summary and conclusions

This study has found significant metric and/or morphologicaldifferences in all seven cervical vertebrae of Neandertals comparedwith a modern comparative sample. Some of these differences maybe integrated with differences in other anatomical regions, such as

the vertebral foramen of the atlas, which is dorsoventrally large andpossibly related to a dorsoventrally long foramenmagnum. Some ofthe differences identified in the Neandertal cervical spine could beretentions of the primitive condition present on their Middle orLower Pleistocene ancestors like the shape of the axis, or the hor-izontal spinous processes of the C6 and C7. Other features, such as agracile posterior arch, would be derived. Overall, the Neandertalneck can be described as slightly shorter but well within themodern human range of variation for length and fully capable ofaccommodating a human vocal tract. Neandertals have medi-olaterally and dorsoventrally longer vertebrae, the latter related tolonger and more horizontally oriented spinous processes. Thus,when compared with modern humans Neandertals show a cervicalmorphology that seems to be more stable in both mid-sagittal andcoronal planes. Differences in the cranial size and shape in theNeandertal and modern human lineages from their Middle Pleis-tocene ancestors could account for some of the differencesperceived in the neck anatomy between these species.

Acknowledgements

This work is built upon the research of many scholars that havepreviously excavated, reconstructed, analysed and curated theprecious fossil remains of Neandertals. This work would have notbeen possible without their efforts and dedication.

We would like to thank the following individuals and in-stitutions for their permission to access the important materialsunder their care: José Miguel Carretero (Universidad de Burgos,Spain), Philip Mennecier (MNHN, Paris), Dominique Grimaud-Hervé (Département de Préhistoire, MNHN), Christine Couture-Veschambre, Bruno Maureille, Bernard Vandermeersch (PACEA-Université de Bordeaux, France), VéroniqueMerlin-Anglade (Muséed’Art e d’Archéologie du Périgord, Perigueux, France), YohannesHaile-Selassie (Cleveland Natural History Museum, Cleveland),Robert G. Franciscus (University of Iowa, Iowa City), Yoel Rak andIsrael Hershkowitz (Department of Anatomy, Sackler School ofMedicine, Tel Aviv University, Israel), Richard Potts (SmithsonianInstitution-National Museum of Natural History, Washington, D.C.).We are also indebted to Aurélie Fort, Véronique Laborde, LilianaHuet, Stéphanie Renault, Guy Marchesseau, Francis Couturas,Lyman Jellema, Jennifer Clark and Matthew Tocheri for curatorialassistance. We are indebted to C. Shaw, A. Mounier, I. Martínez, J.M.Carretero, C. Verna, G.A. Tuin, A. García-Pérez and our colleaguesfrom PAVE, Bioanth-Cambridge, BBP and UCM-ISCIII for stimulatingdiscussions. Thanks to the editor, the associate editor and the re-viewers for their helpful comments that have improved this paper.

AGO has received support from a postdoctoral fellowship of theMinisterio de Educación (Programa Nacional de Movilidad deRecursos Humanos del Plan Nacional de IþDþI 2008e2011). AGOhas also received support from European Community ResearchInfrastructure Action (SYNTHESYS Project; http://www.synthesys.info/; FP6 ‘Structuring the European Research Area’ Programme).AGO and JLA receive support from the Ministerio de Ciencia eInnovación (Proyecto CGL2009-12703-C03-03) and from the Min-isterio de Economía y Competitividad (CGL2012-38434-C03-01).

Appendix A. Supplementary data

Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.jhevol.2013.02.008.

References

Arambourg, C., 1955. Sur l’attitude, en station verticale, des Néanderthaliens. C.R.Acad. Sci., Paris 240, 804e806.

http://www.synthesys.info/

http://www.synthesys.info/




Arensburg, B., 1991. The vertebral column, thoracic cage and hyoid bone. In: Bar-Yosef, O., Vandermeersch, B. (Eds.), Le Squelette Moustérien de Kébara 2. Édi-tions du CNRS, Paris, pp. 113e147.

Arsuaga, J.L., Martínez, I., Gracia, A., Lorenzo, C., 1997. The Sima de los Huesos crania(Sierra de Atapuerca, Spain). A comparative study. J. Hum. Evol. 33, 219e281.

Bailey, S., 2006. Beyond shovel-shaped incisors: Neandertal dental morphology in acomparative context. Period. Biol. 108, 253e267.

Balzeau, A., Radov�ci�c, J., 2008. Variation and modalities of growth and devel-opment of the temporal bone pneumatization in Neandertals. J. Hum. Evol.54, 546e567.

Balzeau, A., Rougier, H., 2010. Is the suprainiac fossa a Neandertal autapomorphy? Acomplementary external and internal investigation. J. Hum. Evol. 58, 1e22.

Been, E., 2005. The anatomy of the lumbar spine of Homo neanderthalensis and itsphylogenetic and functional implications. Ph.D. Dissertation, Tel AvivUniversity.

Been, E., Peleg, S., Marom, A., Barash, A., 2010. Morphology and function of thelumbar spine of the Kebara 2 Neandertal. Am. J. Phys. Anthropol. 142, 549e557.

Been, E., Gómez-Olivencia, A., Kramer, P.A., 2012. Lumbar lordosis of extinct hom-inins. Am. J. Phys. Anthropol. 147, 64e77.

Boë, L.-J., Heim, J.-L., Honda, K., Maeda, S., 2002. The potential of Neanderthal vowelspace was as large as that of modern humans. J. Phonetics 30, 465e484.

Boë, L.-J., Heim, J.-L., Honda, K., Maeda, S., Badin, P., Abry, C., 2007. The vocal tract ofnewborn humans and Neanderthals: acoustic capabilities and consequences forthe debate on the origin of language. A reply to Lieberman (2007a). J. Phonetics35, 564e581.

Bonmatí, A., Arsuaga, J.L., 2007. The innominate bone sample from Krapina. Period.Biol. 109, 335e361.

Bonmatí, A., Gómez-Olivencia, A., Arsuaga, J.L., Carretero, J.M., Gracia, A.,Martínez, I., Lorenzo, C., Bermúdez de Castro, J.M., Carbonell, E., 2010. MiddlePleistocene lower back and pelvis from an aged human individual from theSima de los Huesos site. Spain. Proc. Natl. Acad. Sci. 107, 18386e18391.

Boulay, C., Tardieu, C., Hecquet, J., Benaim, C., Mouilleseaux, B., Marty, C., Prat-Pradal, D., Legaye, J., Duval-Beaupere, G., Pélissier, J., 2006. Sagittal alignment ofspine and pelvis regulated by pelvic incidence: standard values and predictionof lordosis. Eur. Spine J. 15, 415e422.

Boule, M., 1911e1913. L’homme fossile de la Chapelle aux Saints. Annls. Paléont.(Vert.) 6, 111e172, 7, 21e56, 85e192; 8, 1e70.

Bräuer, G., 1988. Osteometrie. In: Knussmann, R. (Ed.), Anthropologie. Handbuchder vergleichenden Biologie des Menschen. Gustav Fischer, Stuttgart,pp. 160e232.

Bruner, E., Manzi, G., Arsuaga, J.L., 2003. Encephalization and allometric trajectoriesin the genus Homo: evidence from the Neandertal and modern lineages. Proc.Natl. Acad. Sci. 100, 15335e15340.

Carretero, J.M., Arsuaga, J.L., Lorenzo, C., 1997. Clavicles, scapulae and humerifrom the Sima de los Huesos Site (Sierra de Atapuerca, Spain). J. Hum. Evol.33, 357e408.

Carretero, J.M., Lorenzo, C., Arsuaga, J.L., 1999. Axial and appendicular skeleton ofHomo antecessor. J. Hum. Evol. 37, 459e499.

Carretero, J.M., Rodríguez, L., García-González, R., Arsuaga, J.L., Gómez-Olivencia, A.,Lorenzo, C., Bonmatí, A., Gracia, A., Martínez, I., Quam, R., 2012. Stature esti-mation from complete long bones in the Middle Pleistocene humans from theSima de los Huesos, Sierra de Atapuerca (Spain). J. Hum. Evol. 62, 242e255.

Churchill, S.E., 1998. Cold adaptation, heterochrony, and Neandertals. Evol.Anthropol. 7, 46e60.

Dawson, J.E., Trinkaus, E., 1997. Vertebral osteoarthritis of the La Chapelle-aux-Saints 1 Neanderthal. J. Archaeol. Sci. 24, 1015e1021.

De Groote, I., 2011a. Femoral curvature in Neanderthals and modern humans: a 3Dgeometric morphometric analysis. J. Hum. Evol. 60, 540e548.

De Groote, I., 2011b. The Neanderthal lower arm. J. Hum. Evol. 61, 396e410.Delpech, F., 1996. L’environnement animal des Moustériens Quina du Périgord.

Paléo 8, 31e46.Fraipoint, J., Lohest, M., 1887. La race humaine de Néanderthal ou de Canstadt en

Belgique. Arch. Biol. 7, 587e757.Franciscus, R.G., Churchill, S.E., 2002. The costal skeleton of Shanidar 3 and a

reappraisal of Neandertal thoracic morphology. J. Hum. Evol. 42, 303e356.Gardner, J.C., Smith, F.H., 2006. The paleopathology of the Krapina Neandertals.

Period. Biol. 108, 471e484.Gómez-Olivencia, A., 2009. Estudios paleobiológicos sobre la columna vertebral y la

caja torácica de los humanos fósiles del Pleistoceno, con especial referencia alos fósiles de la Sierra de Atapuerca. Ph.D. Dissertation, Universidad de Burgos.

Gómez-Olivencia, A., 2013a. Back to the old man’s back: reassessment of theanatomical determination of the vertebrae of the Neandertal individual of LaChapelle-aux-Saints. Annls. Paléont. (Vert.) 99, 43e65.

Gómez-Olivencia, A., 2013b. The presacral spine of the La Ferrassie 1 Neandertal: arevised inventory. Bull. Mém. Soc. Anthropol. Paris, in press

Gómez-Olivencia, A., Carretero, J.M., Arsuaga, J.L., Rodríguez-García, L., García-González, R., Martínez, I., 2007. Metric and morphological study of the uppercervical spine from the Sima de los Huesos site (Sierra de Atapuerca, Burgos,Spain). J. Hum. Evol. 53, 6e25.

Gómez-Olivencia, A., Eaves-Johnson, K.L., Franciscus, R.G., Carretero, J.M.,Arsuaga, J.L., 2009. Kebara 2: new insights regarding the most completeNeandertal thorax. J. Hum. Evol. 57, 75e90.

Gómez-Olivencia, A., Franciscus, R.G., Couture-Veschambre, C., Maureille, B.,Arsuaga, J.L., 2012. The mesosternum of the Regourdou 1 Neandertal revisited.J. Hum. Evol. 62, 511e519.

Gómez-Olivencia, A., Couture-Veschambre, C., Madelaine, S., Maureille, B. Thevertebral column of the Regourdou 1 Neandertal. J. Hum. Evol. in press.

Gómez-Robles, A., Martinón-Torres, M., Bermúdez de Castro, J.M., Margvelashvili, A.,Bastir, M., Arsuaga, J.L., Pérez-Pérez, A., Estebaranz, F., Martínez, L.M., 2007.A geometric morphometric analysis of hominin upper first molar shape. J. Hum.Evol. 53, 272e285.

Gorjanovic-Kramberger, K., 1906. Der diluviale Mensch von Krapina. C.W. Kreidel’sVerlag, Wiesbaden.

Grine, F.E., Pearson, O.M., Klein, R.G., Rightmire, G.P., 1998. Additional human fossilsfrom Klasies River Mouth, South Africa. J. Hum. Evol. 35, 95e107.

Gunz, P., Neubauer, S., Maureille, B., Hublin, J.J., 2010. Brain development afterbirth differs between Neanderthals and modern humans. Curr. Biol. 20,R921eR922.

Harvati, K., 2003. The Neanderthal taxonomic position: models of intra- and inter-specific craniofacial variation. J. Hum. Evol. 44, 107e132.

Harvati, K., Hublin, J.J., Gunz, P., 2010. Evolution of middle-late Pleistocene humancranio-facial form: a 3-D approach. J. Hum. Evol. 57, 75e90.

Heim, J.-L., 1976. Les Hommes Fossiles de la Ferrassie. I. Le Gisement. Les SquelettesAdultes (Crâne et Squelette du Tronc). Masson, Paris.

Heim, J.-L., 1982a. Les Hommes Fossiles de La Ferrassie. II. Les Squelettes d’Adultes:Squelettes des Membres. Masson, Paris.

Heim, J.-L., 1982b. Les Enfants Néandertaliens de la Ferrassie. Étude Anthro-pologique et Analyse Ontogénique des Hommes de Néandertal. Masson,Paris.

Heim, J.-L., 1989. La nouvelle reconstitution du crâne Néandertalien de LaChapelle-aux-Saints: méthode et résultats. Bull. Mém. Soc. Anthropol. Paris1e2, 95e118.

Henry-Gambier, D., 2002. Les fossiles de Cro-Magnon (Les Eyzies-de-Tayac, Dor-dogne). Bull. Mém. Soc. Anthropol. Paris 14, 89e112.

Hershkovitz, I., Speirs, M.S., Frayer, D.W., Nadel, D., Wish-Baratz, S., Arensburg, B.,1995. Ohalo II H2: a 19,000-year-old skeleton from a water-logged site at theSea of Galilee. Israel. Am. J. Phys. Anthropol. 96, 215e234.

Hublin, J.J., 2009. The origin of Neandertals. Proc. Natl. Acad. Sci. 106, 16022e16027.Lieberman, D.E., McCarthy, R.C., Hiiemae, K.M., Palmer, J.B., 2001. Ontogeny and

postnatal hyoid and larynx descent in humans. Arch. Oral Biol. 46, 117e128.Lieberman, P., 2007a. The evolution of human speech. Its anatomical and neural

bases. Curr. Anthropol. 48, 31e65.Lieberman, P., 2007b. Current views on Neanderthal speech capabilities: a reply to

Boë et al. (2002). Letter to the editor. J. Phonetics 35, 552e563.Mann, H.B., Whitney, D.R., 1947. On a test of whether one of two random variables is

stochastically larger than the other. Ann. Math. Stat. 18, 50e60.Martin, H., 1923. L’Homme Fossile de la Quina. Librairie Octave Doin, Paris.Martínez, I., Arsuaga, J.L., 1997. The temporal bones from Sima de los Huesos Middle

Pleistocene site (Sierra de Atapuerca, Spain). A phylogenetic approach. J. Hum.Evol. 33, 283e318.

Martínez, I., Rosa, M., Quam, R., Jarabo, P., Lorenzo, C., Bonmatí, A., Gómez-Olivencia,A., Gracia, A., Arsuaga, J.L. Communicative capacities in Middle Pleistocenehumans from the Sierra de Atapuerca in Spain. Quatern. Int.. DOI:dx.doi.org/10.1016/j.quaint.2012.07.001, in press.

Maureille, B., 2002. A lost Neanderthal neonate found. Nature 419, 33e34.Maureille, B., Madelaine, S., Couture-Veschambre, C., Gómez-Olivencia, A., Meyer, V.,

Bonifay, E., Bonifay, M.-F., Vandermeersch, B., submitted for publication.Regourdou-suite. Sur de nouveaux restes humains rapportés au gisement(Commune de Montignac, Dordogne, France). Paleo.

McCarthy, R.C., Strait, D.S., Yates, F., Lieberman, P., in prep. The origin of humanspeech.

McCown, T.D., Keith, A., 1939. The Stone Age of Mount Carmel. The Fossil HumanRemains from the Levalloiso-Mousterian. Clarendon press, Oxford.

Ogilvie, M.D., Hilton, C.E., Ogilvie, C.D., 1998. Lumbar anomalies in the Shanidar 3Neandertal. J. Hum. Evol. 35, 597e610.

Pablos, A., Lorenzo, C., Martínez, I., Bermúdez de Castro, J.M., Martinón-Torres, M.,Carbonell, E., Arsuaga, J.L., 2012. New foot remains from the Gran Dolina-TD6Early Pleistocene site (Sierra de Atapuerca, Burgos, Spain). J. Hum. Evol. 63,610e623.

Pal, G.P., Routal, R.V., 1996. The role of the vertebral laminae in the stability of thecervical spine. J. Anat. 188, 485e489.

Piveteau, J., 1966. La grotte de Regourdou (Dordogne). Paléontologie humaine.Annls. Paléont. (Vert.) 52, 163e194.

Quam, R., Rak, Y., 2008. Auditory ossicles from southwest Asian Mousterian sites.J. Hum. Evol. 54, 414e433.

Rak, Y., 1990. On the differences between two pelvises of Mousterian context fromthe Qafzeh and Kebara caves. Israel. Am. J. Phys. Anthropol. 81, 323e332.

Rak, Y., Ginzburg, A., Geffen, E., 2002. Does Homo neanderthalensis play a role inmodern human ancestry? The mandibular evidence. Am. J. Phys. Anthropol. 119,199e204.

Rak, Y., Kimbel, W.H., Hovers, E., 1994. A Neandertal infant from Amud Cave, Israel.J. Hum. Evol. 26, 313e324.

Ramirez Rozzi, F.V., Bermúdez de Castro, J.M., 2004. Surprisingly rapid growth inNeanderthals. Nature 428, 936e939.

Raynal, J.-P., 1990. Essai de datation directe. In: Raynal, J.-P., Pautrat, Y. (Eds.), LaChapelle-aux-Saints et la Préhistoire en Corrèze. Associaion pour la RechercheArchéologique en Limousin, Limousin, pp. 43e46.

Rosas, A., Estalrrich, A., García-Tabernero, A., Bastir, M., García-Vargas, S., Sánchez-Meseguer, A., Huguet, R., Lalueza-Fox, C., Peña-Melián, Å., Kranioti, E.F.,Santamaría, D., de la Rasilla, M., Fortea, J., 2012. Les Néandertaliens d’El Sidrón

http://dx.doi.org/10.1007/s13219-012-0064-4


(Asturies, Espagne). Actualisation d’un nouvel échantillon. L’Anthropologie 116,57e76.

Ruff, C.B., Trinkaus, E., Holliday, T.W., 1997. Body mass and encephalization inPleistocene Homo. Nature 387, 173e176.

Schmitz, R.W., Serre, D., Bonani, G., Feine, S., Hillgruber, F., Krainitzki, H., Pääbo, S.,Smith, F.H., 2002. The Neandertal type site revisited: Interdisciplinary in-vestigations of skeletal remains from the Neander Valley,. Germany. Proc. Natl.Acad. Sci. 99, 13342e13347.

Schwalbe, G., 1914. Kritische Besprechung von Boule’s Werk: “L’homme fossile de LaChapelle-aux-Saints” mit einigen Untersuchungen. Z. Morphol. Anthropol. 16,527e610.

Shapiro, L.J., 2007. Morphological and functional differentiation in the lumbar spineof lorisids and galagids. Am. J. Primatol. 69, 86e102.

Smith, F.H., Ostendorf Smith, M., Schmitz, R.W., 2006. Human skeletal remains fromthe 1997 and 2000 excavations of cave deposits derived from Kleine FeldhoferGrotte in the Neander Valley, Germany. In: Schmitz, R.W. (Ed.), Neanderthal1856e2006. Verlag Philipp von Zabern, Mainz am Rhein, pp. 187e246.

Smith, T.M., Tafforeau, P., Reid, D.J., Pouech, J., Lazzari, V., Zermeno, J.P., Guatelli-Steinberg, D., Olejniczak, A.J., Hoffman, A., Radov�ci�c, J., Makaremi, M.,Toussaint, M., Stringer, C., Hublin, J.J., 2010. Dental evidence for ontogeneticdifferences between modern humans and Neanderthals. Proc. Natl. Acad. Sci.107, 20923e20928.

Sokal, R.R., Rohlf, F.J., 1981. Biometry. W.H. Freeman and Company, New York.Spoor, F., Hublin, J.-J., Braun, M., Zonneveld, F., 2003. The bony labyrinth of Nean-

derthals. J. Hum. Evol. 44, 141e165.Stewart, T.D., 1962. Neanderthal cervical vertebrae with special attention to the

Shanidar Neanderthals from Iraq. Bibl. Primatol. 1, 130e154.Straus, W.L.J., Cave, A.J.E., 1957. Pathology and the posture of Neanderthal man.

Q. Rev. Biol. 32, 248e263.Toerien, M.J., 1957. Note on the cervical vertebrae of the La Chapelle man. S. Afr. J.

Sci. 53, 447e449.Toussaint, M., Gómez-Olivencia, A., Been, E., submitted for publication. The Spy

Neandertals spine remains (the sacrum and one lumbar vertebra). In: Rougier,

H., Semal, P. (Eds.), Spy Cave. State of 120 Years of Pluridisciplinary Research onthe Betche-aux-Rotches from Spy (Jemeppe-sur-Sambre, Province of Namur,Belgium).

Trinkaus, E., 1983. The Shanidar Neandertals. Academic Press, New York.Trinkaus, E., 1985. Pathology and the posture of the La Chapelle-aux-Saints Nean-

dertal. Am. J. Phys. Anthropol. 67, 19e41.Trinkaus, E., 2003. Neandertal faces were not long; modern human faces are short.

Proc. Natl. Acad. Sci. 100, 8142e8145.Trinkaus, E., 2006. Modern human versus Neandertal evolutionary distinctiveness.

Curr. Anthropol. 47, 597e620.Trinkaus, E., 2011. The postcranial dimensions of the La Chapelle-aux-Saints 1

Neandertal. Am. J. Phys. Anthropol. 145, 461e468.Valladas, H., Valladas, G., 1991. Datation par la thermoluminescence de silex

chauffés des grottes de Kébara et de Qafzeh. In: Bar-Yosef, O., Vandermeersch, B.(Eds.), Le Squelette Moustérien de Kébara 2. Éditions du CNRS, Paris, pp. 43e47.

Vallois, H.V., Billy, G., 1965a. Nouvelles recherches sur les hommes fossiles de l’abride Cro-Magnon. L’Anthropologie 69, 47e74.

Vallois, H.V., Billy, G., 1965b. Nouvelles recherches sur les hommes fossiles de l’Abride Cro-Magnon. L’Anthropologie 69, 249e272.

Vandermeersch, B., Trinkaus, E., 1995. The postcranial remains of the Régourdou 1Neandertal: the shoulder and arm remains. J. Hum. Evol. 28, 439e476.

Walker, M.J., Ortega, J., López, M.V., Parmová, K., Trinkaus, E., 2011a. Neandertalpostcranial remains from the Sima de las Palomas del Cabezo Gordo, Murcia,southeastern Spain. Am. J. Phys. Anthropol. 144, 505e515.

Walker, M.J., Ortega, J., Parmová, K., López, M.V., Trinkaus, E., 2011b. Morphology,body proportions, and postcranial hypertrophy of a female Neandertal from theSima de las Palomas, southeastern Spain. Proc. Natl. Acad. Sci. 108,10087e10091.

Weaver, T.D., 2009. The meaning of Neandertal skeletal morphology. Proc. Natl.Acad. Sci. 106, 16028e16033.

Wilcoxon, F., 1945. Individual comparisons by ranking methods. Biometrics Bull. 1,80e83.

Wolpoff, M.H., Frayer, D.W., 2005. Unique ramus anatomy for Neandertals? Am. J.Phys. Anthropol. 128, 245e251.

The Neandertal vertebral column 1: The cervical spine

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