Available online at www.sciencedirect.com

Journal of Human Evolution 54 (2008) 414e433

Auditory ossicles from southwest Asian Mousterian sites

Rolf Quam a,b,*, Yoel Rak c

a Division of Anthropology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, USAb Centro UCM-ISCIII de Investigacion sobre la Evolucion y Comportamiento Humanos, c/Sinesio Delgado, 4, 28029 Madrid, Spain

c Department of Anatomy and Anthropology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv 69978, Israel

Received 25 May 2007; accepted 1 October 2007

Abstract

The present study describes and analyzes new Neandertal and early modern human auditory ossicles from the sites of Qafzeh and Amud insouthwest Asia. Some methodological issues in the measurement of these bones are considered, and a set of standardized measurement protocolsis proposed. Evidence of erosive pathological processes, most likely attributed to otitis media, is present on the ossicles of Qafzeh 12 and Amud7 but none can be detected in the other Qafzeh specimens. Qafzeh 12 and 15 extend the known range of variation in the fossil H. sapiens samplein some metric variables, but morphologically, the new specimens do not differ in any meaningful way from living humans. In most metricdimensions, the Amud 7 incus falls within our modern human range of variation, but the more closed angle between the short and long processesstands out. Morphologically, all the Neandertal incudi described to date show a very straight long process. Several tentative hypotheses can besuggested regarding the evolution of the ear ossicles in the genus Homo. First, the degree of metric and morphological variation seems greateramong the fossil H. sapiens sample than in Neandertals. Second, there is a real difference in the size of the malleus between Neandertals andfossil H. sapiens, with Neandertals showing larger values in most dimensions. Third, the wider malleus head implies a larger articular facet in theNeandertals, and this also appears to be reflected in the larger (taller) incus articular facet. Fourth, there is limited evidence for a potential tem-poral trend toward reduction of the long process within the Neandertal lineage. Fifth, a combination of features in the malleus, incus, and stapesmay indicate a slightly different relative positioning of either the tip of the incus long process or stapes footplate within the tympanic cavity inthe Neandertal lineage.� 2007 Elsevier Ltd. All rights reserved.

Keywords: Ossicle; Malleus; Incus; Neandertal; Qafzeh; Amud

Introduction

Studies of the auditory ossicles in living humans have focusedon anatomical, clinical, and auditory aspects (Helmholtz, 1873;Heron, 1923; Dahmann, 1929, 1930; Stuhlmann, 1937; Weverand Lawrence, 1954; Kirikae, 1960; Masali, 1964; Bouchetand Giraud, 1968; Arensburg and Nathan, 1971; Arensburget al., 1981; Blumer et al., 1982; Mutaw, 1986, 1988; Sarrat

* Corresponding author. Division of Anthropology, American Museum of

Natural History, Central Park West at 79th Street, New York, NY 10024,

USA. Tel.: þ1 212 496 3519; fax: þ1 212 769 5334.

E-mail addresses: rquam@amnh.org (R. Quam), yoelrak@post.tau.ac.il

(Y. Rak).

0047-2484/$ - see front matter � 2007 Elsevier Ltd. All rights reserved.

doi:10.1016/j.jhevol.2007.10.005

et al., 1988, 1992; Ferrino et al., 1994; Siori et al., 1995; Masaliand Cremasco, 2006). In addition, the ossicles have proven to beuseful phylogenetic indicators in other groups of primates(Masali and Chiarelli, 1965a,b; Hershkovitz, 1977) and othermammals (Segall, 1943, 1969, 1970). Fewer studies have beencarried out on fossil human auditory ossicles, primarily due totheir scarcity (Angel, 1972; Arensburg and Nathan, 1972; Rakand Clarke, 1979; Heim, 1982; Arensburg and Tillier, 1983), al-though the global sample size is increasing (Arensburg et al.,1996; Moggi-Cecchi and Collard, 2002; Spoor, 2002; de Ruiteret al., 2002; Lisonek and Trinkaus, 2006; Quam et al., 2006;Crevecoeur, 2007). Previous studies of late Pleistocene fossil hu-man ear ossicles have led to conflicting interpretations of theirevolutionary significance.

415R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

Arensburg et al. (1981) have argued that the middle earbones are taxonomically uninformative within the genusHomo, based on the strong similarity in metric dimensionsof the ear ossicles across a wide range of modern human pop-ulations (Heron, 1923; Kirikae, 1960; Blumer et al., 1982; Mu-taw, 1986) and their tight genetic control, being fully formedand adult-sized at birth (Scheuer and Black, 2000). Indeed,there appears to be little to differentiate the known late Pleis-tocene fossil H. sapiens specimens from their living coun-terparts (Arensburg and Nathan, 1972; Tillier, 1999; Spoor,2002; Lisonek and Trinkaus, 2006; Crevecoeur, 2007).

In contrast, Heim (1982) suggested that all three ear ossi-cles from the Neandertal infant La Ferrassie 3 showed subtledifferences from those of living humans. The malleus was ar-gued to show generally larger dimensions in total length andhead size, as well as showing a somewhat more open angle be-tween the head/neck and the manubrium. In addition, the ma-nubrium was said to be straighter, lacking the curvature thatgenerally characterizes H. sapiens. The incus was also saidto be generally larger, showing a long process that is both lon-ger and straighter than in living humans and an expanded ar-ticular facet. In contrast, the short process of the incus wassaid to be shorter, and the notch along the inferior margin ofthe short process, a feature that is variably present in living hu-mans (Arensburg and Nathan, 1971; Mutaw, 1988), is absentin La Ferrassie 3. In addition, the long and short processeswere said to form a more closed angle than is the case in mod-ern humans. The stapes was said to be smaller and to showa marked asymmetry, with the anterior crus being shorterand straighter and the posterior crus longer and more curved.Given the subtle nature of these differences and the lack ofadditional Neandertal specimens at the time, it was unclearwhether these anatomical variations identified in La Ferrassie3 were simply a manifestation of normal biological variationor whether they represented derived traits within the Neander-tal lineage.

The subsequent discovery of several new Neandertal spec-imens has made it possible to assess these initial suggestionsbased solely on La Ferrassie 3. The incus is present withinthe temporal bone in the Le Moustier 1 adolescent Neandertal,and a 3D CT reconstruction of the specimen shows a verystraight long process and a more closed angle between thelong and short crurae (Ponce de Leon and Zollikofer, 1999;Spoor, 2002). The asymmetrical configuration of the Neander-tal stapes has recently been identified in both the Subalyuk 2and Le Moustier 2 specimens (Arensburg et al., 1996; Maur-eille, 2002). These recent discoveries have raised the possibil-ity that, far from being taxonomically uninformative, the earossicles may be an underappreciated source of phylogeneticinformation within the genus Homo.

The new specimens from Qafzeh and Amud reported hereconsiderably augment the sample of these tiny bones knownfrom southwestern Asia and include the first Neandertal spec-imen recovered from this region. This enlarged sample fromQafzeh (n¼ 7) makes it possible to begin to assess the degreeof intraspecific metrical and morphological variation at a singlesite and provides a useful comparison with the geologically

younger late Pleistocene specimens from Europe and NorthAfrica. In addition, comparison of the Amud 7 incus withthe previously known European Neandertal specimens hasthe potential to provide further evidence for a Neandertal pat-tern of anatomical variation in the ear ossicles.

Materials and methods

The extremely small dimensions and peculiar morphology ofthe auditory ossicles complicates the collection and reliabilityof metrical data. Prior investigations into the dimensions ofthese bones have relied on a variety of techniques and measure-ment definitions (Heron, 1923; Kirikae, 1960; Bouchet and Gir-aud, 1968; Blumer et al., 1982; Mutaw, 1986; Siori et al., 1995).However, the two most influential studies that introduced stan-dardized techniques and measurements for the ossicles are thoseof Masali (1964) and Arensburg et al. (1981). While both sets ofmeasurements (Masali, 1964; Arensburg et al., 1981) are ade-quate for capturing the main ossicular dimensions, the defini-tions provided by Masali (1964) have been preferred in thepresent study for their more precise identification of the bonyanatomical landmarks. Some of the measurements in the twostudies are sufficiently similar, despite differences in orientationof the bone, to make them directly comparable. Nevertheless,a certain amount of confusion in the literature surroundingsome of the measurement definitions necessitates a more de-tailed discussion of the consistency between studies, and theprecise definitions used in the present work are detailed below.It is hoped that clarification of these methodological issues willprove useful for future studies of the auditory ossicles and avoidthe inconsistencies in data collection and reporting that havecharacterized previous studies.

Measurement definitions of Masali (1964)

Masali (1964) was the first to suggest a series of standard-ized measurements and orientations of the ossicles, and thesetechniques have been adopted by subsequent researchers (e.g.,Mutaw, 1986; Siori et al., 1995). He studied 40 mallei, 38 in-cudi, and 16 stapes using a projecting microscope at 10� mag-nification. For each ossicle, a series of axes were defined (twoeach for the malleus and incus and three for the stapes), withthe majority of the measurements taken either perpendicular orparallel to the axes. While the orientations and measurementdefinitions are generally clearly understandable and reproduc-ible, there are a few aspects in Masali’s (1964) original articlethat must be addressed.

The base of the gracile (anterior) process is one of the an-atomical points on the malleus used to define the X-axis (head/neck axis). However, the variable presence and preservation ofthe gracile process in both the living hominoids, as well as thefossil specimens, makes this landmark difficult to use in prac-tice. Thus, the present study has relied on the midpoint of theneck width (Fig. 1). Nevertheless, since the base of the gracileprocess (when present) is near the center of the neck width,these two landmarks are sufficiently similar to make the re-sults directly comparable.

416 R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

The orientation of the incus is reported by Masali (1964) tobe in ‘‘norma mediale,’’ with the medial face toward theobserver. However, in the drawing of the incus demonstratingthe orientation and measurement definitions, the bone isclearly oriented in ‘‘norma laterale,’’ with the lateral face to-ward the observer. In subsequent publications, the orientationof this bone has varied between medial (Masali et al., 1991,1992) and lateral (Masali and Chiarelli, 1965b; Siori et al.,1995; Masali and Cremasco, 2006). Thus, we have relied onthe drawing of the incus in the original Masali (1964) paperto establish that the measurements should indeed be taken inlateral orientation.

The stated measurement definitions of length (X-axis) andbreadth (Y-axis) of the incus (Masali, 1964) do not coincidewith the axes labeled on the figure illustrating the measure-ments. Rather, the X- and Y-axes appear to be reversed inFig. 1 of Masali (1964). The most recent article by Masali(Masali and Cremasco, 2006) has apparently corrected thisearlier error, and the X- and Y-axes in the figure defining themeasurements now coincide with the length (long process)and breadth (short process) of the incus. The present studyhas referred to the length of the long process as the X-axisand the short process as the Y-axis, following Masali andCremasco (2006).

The determination of the ‘‘functional length’’ in the incusrequires further clarification. The functional length is impor-tant in assessing the physiological role of the incus in soundtransmission from the environment to the inner ear, but hasnot been measured consistently in previous works and is par-ticularly dependent on the orientation of the bone. Given theasymmetrical morphology of the articular facet, measurementstaken in lateral view by Masali (1964; Masali and Chiarelli,1965b) are significantly smaller than those taken in medialview (Masali et al., 1991, 1992). Related to this problem oforientation, the definition of one of the measurement pointshas varied between the lowermost point along the margin ofthe articular facet and the lateralmost (most anterior in ana-tomical position) point on the articular facet. This has the

Fig. 1. Measurements of the malleus in the present study. The measurement

numbers correspond with those listed in Table 1. Modified after Masali (1964).

effect of making measurements of the functional length takenin different studies incompatible. Due to these inconsistencies,the functional length of the incus has been measured differ-ently in the present study (see below).

Compatibility of measurements between studies

For the malleus, measurements of the total length, manu-brium length, and head width are directly comparable betweenthe studies of Masali (1964) and Arensburg et al. (1981). Incontrast, the method of measuring the angle of the malleusis clearly different and produces values that cannot be com-pared. In addition, Masali (1964) defined a few additionalmeasurements for the malleus (manubrium arc depth and cor-pus length) that are not considered by Arensburg et al. (1981).

For the incus, measurement of the long process length is di-rectly comparable between the studies of Masali (1964) andArensburg et al. (1981). However, as with the Masali (1964)article, there is an inconsistency between the definition ofthe breadth of the incus and the drawing presented in theArensburg et al. (1981) paper. According to Arensburg et al.(1981), the total breadth of the incus is the same as the shortprocess length. This is defined as the ‘‘maximum distance be-tween the tip of the short process to the most protruding (in-ferior) border of the articular facet’’ (Arensburg et al., 1981:203). However, the drawing of the incus indicates that thismeasurement is taken between the tip and the superior borderof the incus. This has been a source of confusion for subse-quent authors, as Blumer et al. (1982) used the inferior borderas the proper landmark and Spoor (2002) used the superior bor-der. Given this confusion, it is not clear that the measurement ofshort process length is comparable between the studies of Ma-sali (1964) and Arensburg et al. (1981).

The angle of the axes defined by Masali (1964) is not thesame measurement as the angle of the incus defined by Are-nsburg et al. (1981), and the values from these two measure-ments cannot be directly compared. The angle of the incus(Arensburg et al., 1981) is one of the few metric variablesthat has been said to differ between Neandertals and living hu-mans, with the former showing much more closed angles(Heim, 1982; Tillier, 1999; Spoor, 2002). The angle describedis formed by the inferior edge of the short process and the pos-terior edge of the long process (Arensburg et al., 1981). How-ever, in practice, these edges are rarely straight, but rather gentlycurve into one another, making the precise determination of theangle problematic. The angle between the axes (Masali, 1964)used in the present study is a different measurement, but isboth clearly defined and can be measured consistently.

In addition, Masali (1964) defined several additional mea-surements for the incus (arc depth of the long process, inter-crural length, intercrural arc depth) that were not consideredby Arensburg et al. (1981).

Malleus measurements used in the present study

The measurements taken in the present study (Table 1;Fig. 1) follow as closely as possible the protocols established

417R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

by Masali (1964). Nevertheless, some of the original measure-ment definitions have proven problematic in their application(see above), and additional measurements not defined in theoriginal study have also been developed. Seven linear mea-surements, one angular measurement, and four indices werecollected for the malleus. In addition, two axes were definedfor the head/neck and the manubrium, respectively. Finally,the present study has measured the thickness of the manu-brium at its midpoint (to establish a manubrium robusticity in-dex) and the minimum width of the neck (to establish thehead/neck axis for measuring the angle of the axes).

The functional length of the malleus should be measuredfrom the axis of rotation, experimentally determined inhumans to pass through the base of the gracile process(Dahmann, 1929, 1930) to the tip of the manubrium. Whenin anatomical position, the length of the manubrium appearsto approximately correspond to the functional length. Theuse of the malleus manubrium length, then, seems to be a rea-sonable estimate of the malleus functional length (lever armlength), particularly in isolated bones whose original positionwithin the tympanic cavity is very difficult to establish. Thus,in the present study, the functional length of the malleus wastaken as being equivalent to the manubrium length (Masaliet al., 1991).

Incus measurements used in the present study

The measurement definitions for the incus have followed asclosely as possible those of Masali (1964). Given the confu-sion surrounding the correct orientation of the incus, the lateralorientation was used systematically when measuring this bone.However, with the exception of the functional length, the ori-entation does not have a considerable influence on the valuesfor any of the measurements. Seven linear measurements, oneangular measurement, and one index were calculated for the

Table 1

Measurement protocol for the malleus1

No. Definition Description

Orientation Bone is lying on its posterior aspect

parallel to the plane of projection (i.

X-axis (head/neck axis) Defined by a line connecting the mi

of the head. This is a slightly differe

Y-axis (manubrium axis) Defined by a line connecting the inf

1 Total length Maximum distance from the tip of t

2 Manubrium length Distance from the tip of the short pr

3 Manubrium M-L thickness Mediolateral (M-L) thickness of the

4 Arc depth of the manubrium Maximum depth of the curvature of

to the Y-axis.

5 Corpus length Distance from the tip of the head to

6 S-I head width Maximum superoinferior (S-I) distan

head, taken perpendicular to the X-a

7 Neck width Minimum distance between the ante

8 Angle between the axes (M) Angle formed between the X- and Y

Manubrium/length index (Manubrium length/total length)� 1

Manubrium robusticity index (Manubrium M-L thickness/manubri

Manubrium/corpus index (Manubrium length/corpus length)�Corpus/length index (Corpus length/total length)� 100

1 Measurement numbers correspond to those shown in Fig. 1.

incus (Table 2; Fig. 2). In addition, the inconsistent measure-ment of the functional length in previous studies has lead toa different measurement definition in the present study.

The most accurate measurement of the functional length isone that most closely approximates the distance between thetip of the long process and the axis of rotation of the mal-leus/incus complex in anatomical position within the tympaniccavity. This rotational axis has been the object of study sincethe nineteenth century (Helmholtz, 1873). The best estimate offunctional length seems to be using Dahmann’s (1929, 1930)estimation of the axis of rotation for the ossicular system(Z-axis in Fig. 2). In the incus, the lever arm is defined asthe perpendicular distance to the tip of the long processfrom a line joining the tip of the short process and the mostsalient (i.e., anterior when in anatomical position) point alongthe articular facet. This measurement is similar, but not iden-tical, to that of Masali (Masali et al., 1991, 1992) when takenwith the incus oriented in medial view.

Measurement technique

Digital photographs were taken of the specimens and mea-sured on a computer using the Photoshop� software program.This technique is similar to that used by both Masali (1964)and Arensburg et al. (1981), and has the advantages of beingportable, reproducible, relatively affordable, and compatiblewith previous studies. The ossicles were oriented accordingto the techniques of Masali (1964) (see above) and a 10-mmscale was placed next to the bone on the surface of the table.The malleus was positioned so that the manubrium was placedflat on the surface, while the incus was placed so that the longand short crurae were flat on the surface. Once the pictureswere transferred to the computer, the images were calibrated,using the scale included in the photo, so that the measurementscould be taken.

(with the articular facet away from the observer) and with the manubrium

e. flat on the surface).

dpoint of the minimum neck width and the most salient point along the top

nt definition than that of Masali (see text).

eriormost points of the short process and the manubrium tip.

he manubrium to the top of the head.

ocess to the manubrium tip, following the Y-axis.

manubrium at mid manubrium length, taken perpendicular to the Y-axis.

the arc of the manubrium, measured from the point of maximum depth

the lower border of the manubrium, taken following the X-axis.

ce between two parallel lines marking the widest points of the margin of the

xis.

rior and posterior borders of the neck.

-axes.

00

um length)� 100

100

Table 2

Measurement protocol for the incus1

No. Definition Description

Orientation Bone is lying on its medial aspect. In this orientation, more of the articular facet is visible and the lowest

point of the articular facet is marked by a ‘‘lip’’

X-axis (long process axis) Defined by a line joining the tip of the long process to the most salient point along the superior

border of the body.

Y-axis (short process axis) Defined by a line joining the tip of the short process to the most salient point along the anterior portion

of the superior border of the body.

Z-axis (rotational axis) Defined by a line joining the tip of the short process to the most external point along the margin of the

articular facet. This axis approximates the rotational axis of the incus within the tympanic cavity.

9 Short process length Maximum distance from the tip of the short process to the most salient point along the anterior portion of

the superior border of the body, following the Y-axis.

10 Long process length Maximum distance from the tip of the long process to the most salient point along the superior border of the body,

following the X-axis.

11 Articular facet height Maximum height of the articular facet taken perpendicular to the Z-axis.

12 Functional length Maximum distance from the tip of the long process to the Z-axis, taken perpendicular to the Z-axis.

13 Arc depth of the long process Maximum depth of the arc along the long process, measured from the plane defined by the lateralmost edge

of the articular facet and the lateralmost point along the tip of the long process.

14 Intercrural length Maximum distance between the most salient points along the superior margin of the short process and the tip

of the long process. The lateralmost points of the short and long process tips define the measurement plane.

15 Intercrural arc depth Maximum depth of the curvature between the short and long crurae tips. The depth is taken perpendicular to the

axis defined above for the intercrural length (No. 14).

16 Angle between the axes Angle formed between the X- and Y-axes.

Crural index (Short process length/long process length)� 100

1 Measurement numbers correspond to those shown in Fig. 2.

418 R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

The use of photographs to measure the ossicles results ina three-dimensional object being reduced to two dimensions,and introduces a potential source of measurement error. Ingeneral, this is not a significant problem in the case of the os-sicles since they are parallel to the surface of the table and do

Fig. 2. Measurements of the incus in the present study. The measurement num-

bers correspond with those listed in Table 2. Modified after Masali (1964).

not project markedly off the table’s surface. Indeed, despitethe wide variety of methods used in the past to measure thesetiny anatomical structures, Arensburg et al. (1981) point outthat the mean sizes of the ossicles among many previousstudies are remarkably similar (Heron, 1923; Kirikae, 1960;Bouchet and Giraud, 1968; Blumer et al., 1982; Mutaw,1986; Siori et al., 1995).

A recent study (Bailey et al., 2004) analyzed the intraob-server error in the measurement of molar tooth cusp base areasusing calibrated digital photographs. That study followed sim-ilar procedures and was subject to similar sources of error as inthe present work, and found a maximum intraobserver error of2.6% for any particular measurement. In the present study, in-traobserver error in measuring the auditory ossicles from pho-tographs was experimentally determined to be 2.5%, in closeagreement with the results for measures of molar tooth cuspbase areas (Bailey et al., 2004).

Morphological features

The variation in a number of anatomical features was as-sessed in the fossil specimens and our modern human re-ference sample. Some of these features were mentionedpreviously as potentially showing interspecific patterns of var-iation reflecting taxonomic differences between Neandertalsand modern humans. These include: the inflection of the tipof the malleus’ manubrium, the development of the short pro-cess of the manubrium, the presence of a groove on the ante-rior neck of the malleus, and a relatively straight long processin the incus (Arensburg and Nathan, 1972; Heim, 1982). Otherfeatures were seen to vary within modern humans, including:the presence of the gracile process in the malleus, the

419R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

development of a depressed area on the medial aspect of thebody of the incus, the contour of the superior border ofthe short process of the incus, and the presence of a notch inthe inferior border of the incus’ short process (Arensburgand Nathan, 1971; Mutaw, 1988). Finally, one feature showedvariation within the Qafzeh sample: morphology of the tip ofthe short process of the incus.

Although the functional significance, if any, of many ofthese anatomical variants is not clear, the strong genetic com-ponent to the development of the ear ossicles, being fullyformed and adult-sized at birth (Scheuer and Black, 2000),means that any consistent anatomical differences can be takento largely reflect genetic differentiation between populations.

Fossil specimens and comparative sample

The new Qafzeh specimens were removed from the tym-panic cavity and external auditory canal of Qafzeh 12 (rightmalleus and incus) and 15 (right malleus and incus) duringstudy of the collection in 2005. Qafzeh 12 is a partial skeletonof a 3e4-year-old child, while Qafzeh 15 represents an olderindividual, between 8 and 10 years old at death. Both these in-dividuals were found in a Mousterian context and representearly modern humans (Tillier, 1999). The fossils from thissite have been dated to 90e100 ka (Valladas et al., 1988;Grun and Stringer, 1991). The left incus was removed previ-ously from the tympanic cavity of the Amud 7 specimen dur-ing cleaning of the adhering sediments. This is a partialskeleton of a 10-month-old infant recovered from a Mousteriancontext and attributed to a Neandertal (Rak et al., 1994;Hovers et al., 1995). This specimen dates to 53.0� 7 ka(Rink et al., 2001).

For comparative purposes, the previously known ear ossi-cles from Qafzeh (Qafzeh 11 and 21) were also studied, aswere the original fossil specimens from the site of LagarVelho. In the case of both Qafzeh 12 and Qafzeh 15,0.2 mm was added to the incomplete long process to estimatethe original length. Regarding Qafzeh 21, damage to the spec-imen subsequent to its publication (Tillier, 1999), but prior tothe present study, led to the loss of the lower half of the longprocess. Thus, measurements that rely on the long process be-ing complete were taken on the published photograph of thespecimen (Tillier, 1999). No attempt was made to estimatethe missing portion of the incus’ long process in Lagar Velho.

In addition, measurements were taken from the literature andon published scaled photographs for a number of Pleistocenespecimens, including Darra-i-Kur (Angel, 1972), Nazlet Khater(Crevecoeur, 2007), Dolni Vestonice (Lisonek and Trinkaus,2006), Le Moustier 1 (Ponce de Leon and Zollikofer, 1999),La Ferrassie 3 (Heim, 1982), and Biache-Saint-Vaast 1 (Creve-coeur, 2007). Nevertheless, given the inconsistencies in mea-surement definitions discussed above and the preservationcharacteristics of fossil specimens, a few comments are war-ranted. To ensure the reliability of the comparative analysis,careful consideration was given to the selection of the measure-ments from the literature to assure their compatibility with thosedefined in the present study.

A few measurements have been reported for the late middlePleistocene specimen Biache-Saint-Vaast 1 (Rougier, 2003;Lisonek and Trinkaus, 2006; Crevecoeur, 2007). The remainsfrom this site show clear affinities with late Pleistocene Nean-dertals (Rougier, 2003), and they form part of the Neandertalevolutionary lineage. For the malleus, the present study reliedon the published measurements of total length, manubriumlength, head width, corpus length, and angle between theaxes while for the incus, only long process length and intercru-ral length are available (Lisonek and Trinkaus, 2006; Creve-coeur, 2007). The manubrium of the malleus is incomplete,and its length has been estimated (Rougier, 2003; Crevecoeur,2007); therefore, the values that depend on this measurementshould be considered tentative in this specimen.

The maximum length of the malleus in the La Ferrassie 3Neandertal specimen was reported as 8.3 mm by Heim(1982). However, several recent studies have suggested thatthis is an underestimate (Masali et al., 1991; Spoor, 2002;Crevecoeur, 2007). Spoor (2002) measured the total length,manubrium length, and head width in the published scaledphoto (Heim, 1982), and these values were used in the presentstudy. In addition, both Masali et al. (1991) and Crevecoeur(2007) reported an identical value (6.0 mm) for the corpuslength. Finally, the angle of the axes of the malleus was mea-sured on the scaled published photo (Heim, 1982). For the LaFerrassie 3 incus, the published value for long process length(7.2 mm) was used (Heim, 1982). The remaining variableswere measured on the published scaled photograph.

The only measurement available for the Le Moustier 1incus that is compatible with the measurements in the presentstudy is the long process length (Ponce de Leon andZollikofer, 1999). No attempt was made to measure other vari-ables on the published image of the specimen since it is notclear that the orientation of the specimen allows for reliabledata collection.

The ear ossicles from the Darra-i-Kur specimen are of par-ticular relevance for comparative purposes in the present studysince they were also found in a southwest Asian Mousteriancontext and were recovered from a temporal bone that report-edly shows modern human affinities (Angel, 1972). Only a fewpreliminary measurements were published for these speci-mens, and the measurement definitions were not specified.Nevertheless, the values for total length, manubrium length,and head width of the malleus seem reliable, since all threeof these measurements are compatible between the studiesof Masali (1964) and Arensburg et al. (1981). For the incus,the intercrural length and articular facet height in Darra-i-Kur can be compared with the values in the present study.

Some data are available on Upper Paleolithic modern hu-mans. For the Nazlet Khater 2 specimen, in addition to thepublished values (Crevecoeur, 2007), the manubrium thicknessand arc depth, neck width, and angle between the axes weremeasured in the scaled published photograph in lateral view.Measurements and photos of the Dolni Vestonice ear ossicleswere also published recently (Lisonek, 1992; Lisonek andTrinkaus, 2006). For the malleus, the published values wereused for the total length, manubrium length, and head width,

420 R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

while for the incus the long process length and intercrurallength were used. The remaining measurements in these boneswere measured on the published photos in lateral orientation(Lisonek and Trinkaus, 2006).

In order to estimate the normal range of biological variationthat can be expected to characterize any living population,a modern human sample (n¼ 43) of ear ossicles was drawnfrom a large collection removed during cadaver dissection ingross anatomy instruction at the New York Chiropractic Col-lege in Seneca Falls, New York (USA). This sample comprisesindividuals of known sex and race ranging in age from 51 to100 years old. The individuals included in the present studywere selected based on preservation criteria, the absence ofany obvious pathological conditions, and the presence ofmore than one ossicle in order to facilitate comparison be-tween ossicles in the same individual.

Anatomical descriptions

The new specimens reported here consist of the right malleiand incudi from the early modern human specimens Qafzeh 12and Qafzeh 15 and the left incus from the Amud 7 Neandertalinfant. These specimens considerably augment the sample ofthese tiny bones known from southwestern Asia and includethe first Neandertal specimen recovered from this region.

Qafzeh 12 (right malleus) (Fig. 3)

This specimen, along with the incus, was recovered fromthe matrix filling the mastoid antrum of Qafzeh 12. The spec-imen is dark brown in color and has concretions adhering tomost of it, including the top of the head, the articular facet,and tip of the manubrium. After cleaning, the specimen stillretains some concretion on the anterior side of the manu-brium’s tip, but this does not affect the reliability of measure-ments. There is a pronounced crack present along the base ofthe manubrium just posterior to the mid manubrium point, butmeasurements of this specimen are unaffected.

The specimen appears quite small overall but is complete,and the basal portion of an ossified gracile process projects an-teriorly. The superior border of the articular facet is separated

Fig. 3. The Qafzeh 12 right m

from the head of the malleus by a shallow groove. Viewedfrom above, the head shows a flattening in the anteroposteriordirection, as in living humans, such that the maximum antero-posterior width (1.74 mm) is considerably smaller than themaximum inferosuperior width (2.70 mm). A pronouncedcrest extends from the superior border of the neck and wrapsaround the anterior aspect. The manubrium of the malleus isgently concave, with a well-developed short process. Thereis no tubercle marking the insertion of the tensor tympanimuscle.

Qafzeh 12 (right incus) (Fig. 4)

This specimen shows the same coloring as the associatedmalleus. The specimen is nearly complete, missing onlya small portion of the tip of the long process. To estimatethe original length, 0.2 mm has been added to the measure-ments of the preserved long process. The tip appears to havebeen broken off, rather than eroded by any pathological pro-cess, such as otitis media, during the lifetime of the individual.The margins of the break are relatively smooth, but this couldeasily be a product of taphonomic factors. A deep crack is alsopresent along the entire length of the anterior border of thelong process. Like the associated malleus, the Qafzeh 12 incusalso shows small overall dimensions. Both the superior borderof the short process and the anterior border of the long processare gently concave. A clear notch is present along the lowermargin of the short process, which terminates in a bulboustip. The medial aspect of the body shows a deeply excavatedarea, and the medial margin of the articular facet is damaged.

Qafzeh 15 (right malleus) (Fig. 5)

This specimen was recovered from the matrix filling the ex-ternal auditory canal of Qafzeh 15. During the removal pro-cess, the tip of the manubrium was broken. However, theclean nature of the break allowed for the reliable reattachmentof the tip, and measurements are unaffected. After cleaningand restoration of the specimen, a heavy sandy/salty concre-tion remains on the distal portion of the manubrium, towardthe tip. Further preparation of the specimen runs the risk of

alleus. Scale bar¼ 1 cm.

Fig. 4. The Qafzeh 12 right incus. Scale bar¼ 1 cm.

421R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

damage, given the fragility of the bone, but the measurementsare unaffected. This specimen shows the same brown/caramelcoloring as the Qafzeh 15 incus, but the head and neck are alsocovered by numerous black stains. There is no evidence of anypathology in the form of pockmarks or pitting on the surfaceof the bone.

The specimen is complete, and the base of a gracile processprojects anteriorly. There is a well-developed crest on the su-perior aspect of the neck that extends onto the anterior aspectas well. The superior border of the articular facet is separatedfrom the head of the malleus by a deep groove. The head againshows a smaller anteroposterior width (1.47 mm) than the in-ferosuperior width (2.58 mm). The manubrium is gently con-cave and shows a well-developed short process, but notubercle for the tensor tympani muscular insertion is present.

Qafzeh 15 (right incus) (Fig. 6)

This specimen was recovered from the aditus to the mastoidantrum, just superior to the tympanic cavity in Qafzeh 15. Thespecimen was coated with a patchy, black concretion of saltand sand, especially on the lateral surface, while the medialsurface showed an ashy white color. After cleaning and resto-ration, the concretions were removed and the specimen is

Fig. 5. The Qafzeh 15 right m

brown/carmel in color with numerous black stains over thesurface area.

The specimen is nearly complete. The long process is miss-ing the lenticular process, but on the lateral aspect, the tip be-gins to curve medially, indicating that it is very nearlycomplete. Thus, as with the Qafzeh 12 incus, 0.2 mm wasadded to the measurements of the preserved long process toapproximate the original length. Slight abrasion/erosion is vis-ible on the anterior aspect of the lower border of the articularfacet. Some small pockmarks (pits) are present on the shortprocess and body, but it is not clear that these representbony lesions due to otitis media.

A very deeply excavated area on the medial aspect of thebody combined with the medial projection of the articularfacet produces a very thin, projecting medial border for the ar-ticular facet. A notch is present along the lower margin of therather pointed short process of this specimen and the bodyseems considerably narrower. The superior margin of the shortprocess is mainly straight, but shows a concave bulge towardthe tip. In contrast, the anterior margin of the long processis gently concave.

Amud 7 (left incus) (Fig. 7)

This specimen was removed from the tympanic cavity dur-ing cleaning of the specimen and is brown/tan in color. Thespecimen is missing the lenticular process but is otherwisecomplete and the measurements of the long process are accu-rate. The excavated area on the medial aspect of body is ex-tremely deep and takes the form of a well-defined trianglewith its sides represented by the articular facet, the short pro-cess, and the intercrural arc. A well-defined notch is also vis-ible along the lower border of the short process, whichterminates in a bulbous tip. The superior border of the shortprocess is gently concave, while the anterior border of thelong process is markedly straight.

Paleopathology

Middle ear pathology, frequently involving the ear ossicles,has been reported previously in archaeological skeletal

alleus. Scale bar¼ 1 cm.

Fig. 6. The Qafzeh 15 right incus. Scale bar¼ 1 cm.

422 R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

material (Arensburg et al., 2005). Ossification of the head ofthe malleus with the roof of the tympanic cavity (Arensburget al., 1977) and fixation of the stapedial footplate within theoval window (Birkby and Gregg, 1975) are complicationsthat can arise from otosclerosis (Davis, 1987). This diseaseprocess is rare in individuals younger than about ten yearsof age (Linthicum, 1993), and the individuals in both the stud-ies cited above were between 40 and 50 years old at death. Asecond class of pathology is manifested by bony lesions on thesurface of the ossicles and/or erosion of the tips of themalleus’ manubrium, the long process of the incus, or the sta-pedial head (Lisonek et al., 1986; Bruintjes, 1990). Theselesions are generally attributed to inflammatory processes, in-clulding otitis media, and can also involve the walls of thetympanic cavity and the mastoid process (Schultz, 1979). Inliving humans, chronic otitis media is most prevalent amongchildren (Daniel et al., 1988) and is reflected in bony lesions

Fig. 7. The Amud 7 left in

of the ossicles in approximately 25% of clinical cases (Sadeet al., 1981).

Among fossil H. sapiens, the tip of the long process in theDolni Vestonice 14 incus is said to show damage due to aninflammatory condition during the lifetime of the individual(Lisonek and Trinkaus, 2006). In addition, the Dolni Vestonice15 incus also shows conspicuous pitting of the surface on thelateral aspect of the body, and the malleus from this side ap-pears severely deformed. In contrast, there is no evidence ofpathology in the ossicles of Qafzeh 21, Lagar Velho, or NazletKhater 2 (Crevecoeur, 2007).

The Qafzeh 11 malleus and incus were also previously re-ported to have been affected by otitis media, causing the ero-sion of the tips of the manubrium in the malleus and thelong process in the incus (Arensburg and Nathan, 1972). How-ever, our examination of the original fossil specimens does notsupport this contention. There is no sign of porosity anywhere

cus. Scale bar¼ 1 cm.

423R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

on the bony surface of either specimen, including near the pre-served distal ends of either the manubrium of the malleus orthe long process of the incus. In addition, the transverse natureof the breaks on both bones, being both clean and perpendic-ular to the long axes of the manubrium of the malleus and thelong process of the incus, suggest that the bone was not eatenaway by a pathological process. Rather, it is more reasonableto invoke taphonomic factors to explain the damage to bothspecimens.

Among the new Qafzeh specimens, the malleus of Qafzeh15 shows no signs of pathology, while some small pockmarks(pits) are present on the short process and body of the Qafzeh15 incus. It is often difficult to distinguish between lesions thathave a pathological origin and those caused by post mortemtaphonomic factors, and it is not clear whether the pockmarkspresent in Qafzeh 15 represent bony lesions due to otitis mediaor may simply be due to taphonomic factors.

In contrast, the posterior aspect of the manubrium of Qaf-zeh 12 shows several deep pits that do seem consistent withotitis media, but the manubrium’s tip is complete and unaf-fected. In addition, the short process of the incus also showssome pockmarks/pits that are consistent with otitis media, al-though the anatomical details of the specimen are not affected.While the tip of the long process of the incus is missing, it ap-pears to have been broken off rather than eroded. Thus, thiscase of otitis media was severe enough to affect the bony sur-face of the ossicles, but not so severe that it significantlyaltered the morphology of the ossicles.

Although the presence of a depressed area on the medialaspect of the body of the incus is normal in modern humans,the marked degree of expression in Amud 7 suggests that itmay be pathological in this individual. Pitting is also visiblein this area, as well as just inferiorly toward the long process.Pock-marks are present along the superior aspect of the bodyand short process. Those toward the tip of the short processare larger and the surrounding bone appears to be damagedhere. Those on the body are smaller and more well defined.The presence of these pockmarks in Amud 7 appears to bedue to an erosive pathological process, such as otitis media.

Amud 7 would not be the only Neandertal specimen toshow middle ear pathology. Although none was reported forLa Ferrassie 3 (Heim, 1982), the stapes of the Subalyuk 2 Ne-andertal shows the presence of a large tubercle just posterior tothe head, and this has been interpreted as evidence of the os-sification of the articular capsule surrounding the incudostape-dial joint (Arensburg et al., 1996). The presence of bonylesions on the external surface of the mastoid process and tem-poral squama in the Krapina 1 juvenile Neandertal craniumhas also been interpreted as evidence of otitis media(Minugh-Purvis et al., 2000). Thus, pathological processesaffecting the middle ear structures have been reported inboth modern human and Neandertal specimens and seem tobe more common than those afflicting the inner ear (Spooret al., 1998). Interestingly, the young ages at death for boththe Amud 7 Neandertal (10 months; Rak et al., 1994) andthe Qafzeh 12 early modern human (3e4 years; Tillier,1999) indicate that otitis media was present in very young

infants and children in both of these Pleistocene populations,a situation that parallels that documented in living humans(Daniel et al., 1988).

Comparative morphology of the malleus

All of the Qafzeh mallei show clear resemblances to thoseof living humans in their anatomical details. Specifically, theyshow a flattening of the head in the anteroposterior direction,a curved aspect to the manubrium, and a well-developed shortprocess. In contrast, some variation can be seen in the presenceof both the gracile process and a groove on the anterior neck.The taxonomic utility of variation in several of these anatom-ical discrete traits was further analyzed in a sample of middleand late Pleistocene specimens and within Holocene humans.

Development of the short (lateral) process

The short process of the malleus is a projection of the su-perior portion of the manubrium and marks the limit betweenthe pars tensa and the pars flaccida within the tympanic mem-brane (Gray, 1977). All three Qafzeh mallei show a clear, pro-jecting short process, as do the Nazlet Khater 2 and DolniVestonice 14 specimens (Table 3). In contrast, a projectingshort process is missing from both the right and left malleiof Lagar Velho. Although the variation in this structure in liv-ing humans is considerable, with some specimens showingwell-developed, projecting short processes and other speci-mens lacking them, most modern human specimens showsome degree of development of the short process. Thus, thevariation in the fossil H. sapiens sample is clearly encom-passed by that seen in living humans. The short process inthe Neandertal specimen La Ferrassie 3 is said to be largerand to imply a greater projection of this structure on the exter-nal face of the tympanic membrane (Heim, 1982). However,this tentative hypothesis can only be confirmed by the discov-ery of additional Neandertal mallei.

Development of the gracile process

The anterior ligament of the malleus inserts on the anteriorsurface of the neck, connecting the malleus with the anteriorwall of the tympanic cavity. At the site of attachment of thisligament on the malleus, a slender bony projection, the gracileprocess, is often present. In our modern human reference sam-ple, a gracile process is present in 64.0% of the individuals(Table 3). Among the fossil human specimens, this structureis commonly broken off at its base. Nevertheless, in mostcases a small projection of bone is still preserved, indicatingthe presence of a gracile process and making it possible toscore this anatomical trait. This structure has been identifiedin Lagar Velho, Nazlet Khater 2 (Crevecoeur, 2007), andQafzeh 11 and 12. However, it is absent in Qafzeh 15. Thus,it is present in 80% of late Pleistocene H. sapiens individuals.The presence or absence of this structure in Neandertals is cur-rently unknown.

Table 3

Morphological observations of the malleus in fossil and living humans

Specimen/sample Side Short process Gracile process Groove on anterior neck Inflection of manubrium tip Reference

La Ferrassie 3 R Present ? Absent Straight Heim (1982)

Qafzeh 11 L Present Present Present - Original specimen

Qafzeh 12 R Present Present Absent Lateral Original specimen

Qafzeh 15 R Present Absent Present? Lateral Original specimen

Nazlet Khater 2 R Present Present Present? Straight Crevecoeur (2007)

Dolni Vestonice 14 L Present ? ? Lateral Lisonek and Trinkaus (2006)

Lagar Velho 1 R Absent Present Present Lateral Original specimen

Lagar Velho 1 L Absent Present Present Lateral Original specimen

Modern humans Present Absent¼ 36%

(n¼ 27)

Absent¼ 53.5%

(n¼ 23)

Straight¼ 33.8%

(n¼ 25)

Present study

Present¼ 58.7%

(n¼ 44)

Present¼ 46.5%

(n¼ 20)

Lateral¼ 66.2%

(n¼ 49)

Developed¼ 5.3%

(n¼ 4)

424 R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

Groove on the anterior neck

Arensburg and Nathan (1972) reported the presence of anarrow and deep groove on the anterior aspect of the neck,between the head and the gracile process, on the malleus ofQafzeh 11. A similar groove was said to occur in a less markedfashion on both Epipaleolithic and recent human mallei. Thisgroove is absent on Qafzeh 12, but a slight manifestation of itdoes appear on Qafzeh 15 (Table 3). In addition, it is presenton both right and left mallei from Lagar Velho and seems tobe present in the Nazlet Khater specimen as well (Crevecoeur,2007). Among our modern human comparative sample, a similargroove appears to be present in just under half of the sample(46.5%). Thus, this appears to be a common feature in H. sapiensindividuals, both living and fossil. In contrast, it is absent in theNeandertal specimen La Ferrassie 3 (Heim, 1982).

Inflection of the manubrium tip

The tip (spatula) of the manubrium generally points later-ally when in anatomical position in living humans. A laterallypointing manubrium tip is found in 66.2% of the recent humanreference sample, while the remaining specimens (33.8%)were judged to show a straight manubrium with no inflectionof the tip (Table 3). Among the fossil H. sapiens individuals,80.0% show a lateral inflection to the tip of the manubrium,including both Qafzeh 12 and 15. The only exception appearsto be the Nazlet Khater 2 specimen, whose manubrium is saidto be straight (Crevecoeur, 2007). The only data available forthe Neandertals are from La Ferrassie 3, which also showsa straight manubrium (Heim, 1982).

Since the manubrium is embedded in the fibers of the tym-panic membrane and the tip of the manubrium marks the deep-est point of curvature of the membrane, variation in theinflection of the manubrium’s tip may be related to the curva-ture of the membrane. However, both straight and inflectedmanubria are found in normal living human individuals, andthis feature does not appear to have much functional

significance. Heim (1982) suggested that the lack of an infe-rior inflection of the manubrium tip in the La Ferrassie 3 Ne-andertal infant may be taxonomically relevant. However, thepresence of a straight manubrium in the Nazlet Khater 2 indi-vidual and about one third of our modern human referencesample suggests that this anatomical variant does not followtaxonomic boundaries.

Comparative morphology of the incus

The morphological variation in the incus within the Qafzehsample is somewhat greater than that of the malleus. This isparticularly evident in the anatomical details of the short pro-cess, the curvature of the long process, and the depth of theexcavated area on the medial aspect of the body. In contrast,the Neandertals seem to show less variation in their incusmorphology.

Short process tip

The short process in Qafzeh 21 is slender and gradually ta-pers to a well-defined point, differing from the other Qafzeh in-cudi. The short process in Qafzeh 15 is also pointed, butconsiderably larger, while Qafzeh 12 shows a small, bulboustip and Qafzeh 11 shows a large and bulbous tip. Variation isalso apparent between the two Dolni Vestonice incudi, withDV 14 showing a more extended short process, while that ofDV 15 appears more truncated (Lisonek and Trinkaus, 2006).The short process in Lagar Velho is perhaps most similar tothat in Qafzeh 15. The short process in Amud 7 shows a large,bulbous tip and, compared to the Qafzeh sample, is most similarto Qafzeh 11. Both the Le Moustier 1 (Ponce de Leon and Zol-likofer, 1999) and La Ferrassie 3 (Heim, 1982) Neandertal spec-imens also show a bulbous tip, and, based on this small sample,this morphology appears to be more frequent in this group ofhominins. Nevertheless, the range of variation in modernhumans is, again, quite large and easily encompasses thatexpressed by the fossil specimens.

425R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

Contour of the superior border of the short process

The superior border of the short process is normally straightor concave in living humans. Among our recent human com-parative sample, 48 of 75 individuals (64.0%) were judgedas showing a straight contour to the superior border of theshort process, while a concave contour is seen in 26 individ-uals (34.7%) and a convex curvature was recorded in onlyone (1.3%) specimen (Table 4).

Within the Qafzeh sample, a concave curvature is seen inboth Qafzeh 11 and 12, while both Qafzeh 15 and 21 showa straight contour. The two Dolni Vestonice specimens alsoshow variation in this feature, with DV 14 having a concavecontour and that of DV 15 being convex. Finally, Lagar Velhois straight. Thus, the straight and concave contours occur inequal frequencies within the fossil H. sapiens sample, withone individual showing a convex curvature, the least commonanatomical variant in living humans. In contrast to this varia-tion, a concave curvature is seen in all three Neandertal spec-imens (Amud 7, La Ferrassie 3 [Heim, 1982], and Le Moustier1 [Ponce de Leon and Zollikofer, 1999]).

Presence of a notch in the short process

The development of a notch along the inferior margin of theshort process is the most well-known anatomical variant in theear ossicles, and its expression has been the object of study inboth living populations and fossil specimens (Heron, 1923;Bouchet and Giraud, 1968; Arensburg and Nathan, 1971,1972; Mutaw, 1986, 1988; Tillier, 1999). The notch is locatedat the insertion point of the posterior incudal ligament, and itspresence has been linked with this anatomical structure. Thefrequency of this feature in living humans has been reportedto range from 30.4 to 100% in diverse populations (Mutaw,1988). In the present study, this notch was observed in only

Table 4

Morphological observations of the incus in fossil and living humans

Specimen/sample Side Contour of superior

border of short process

Notch in short

process

Dep

med

La Ferrassie 3 R Concave Absent ?

Le Moustier 1 L Concave Present ?

Amud 7 L Concave Present Dee

Darra-i-Kur R Absent

Qafzeh 11 L Concave Present Pres

Qafzeh 12 R Concave Present Dee

Qafzeh 15 R Straight Present Dee

Qafzeh 21 R Straight Present Pres

Dolni Vestonice 14 L Concave Present ?

Dolni Vestonice 15 R Convex ? Pres

Lagar Velho 1 R Straight Absent Pres

Modern humans Straight¼ 64.0%

(n¼ 48)

Absent¼ 89.2%

(n¼ 66)

Abs

(n¼Concave¼ 34.7%

(n¼ 26)

Present¼ 10.8%

(n¼ 8)

Pres

(n¼Convex¼ 1.3%

(n¼ 1)

Dee

(n¼

10.8% of our modern human comparative sample (Table 4),a relatively low frequency of occurrence.

Among the Neandertals, a pronounced notch is present inboth Le Moustier 1 (Ponce de Leon and Zollikofer, 1999)and Amud 7, but is absent in La Ferrassie 3 (Heim, 1982).A notch is also present in all four fossil H. sapiens individualsfrom Qafzeh. Again, some variation is present, with bothQafzeh 11 and 12 showing well-developed notches, followedby Qafzeh 15 and Qafzeh 21, which shows the weakest expres-sion. In contrast, no trace of a notch is present in eitherDarra-i-Kur or the Upper Paleolithic specimen from LagarVelho. Although no notch is mentioned in the description ofthe Dolni Vestonice specimens (Lisonek and Trinkaus,2006), DV 14 does appear to show a notch in the lower borderof the short process.

Thus, there is variation in this feature in Neandertals wellas modern humans. Nevertheless, both the developmentalcomponent of this trait (related to the posterior incudal liga-ment) and the significant variation in its expression in thosetaxa that exhibit a notch suggest caution in attributing an evo-lutionary interpretation to this anatomical variant.

Depressed area on the medial body

The medial aspect of the body of the incus commonly showsa depressed area just posterior to the articular facet. The degreeof expression of this feature varies in our modern human com-parative sample from absent (13.3%) to present (70.7%) todeep (16.0%) (Table 4). All four of the Qafzeh specimensshow this depressed area, although, again, there is some varia-tion. Qafzeh 15 shows the deepest depression, followed by Qaf-zeh 12, while Qafzeh 11 and 21 are somewhat shallower andabout the same. This depressed area is also clearly present in La-gar Velho and Dolni Vestonice 15 (Lisonek and Trinkaus, 2006).Thus, it is a ubiquitous feature within the fossil H. sapiens

ressed area on

ial aspect of body

Curvature of anterior

border of long process

Reference

Straight Heim (1982)

Straight Ponce de Leon and

Zollikofer (1999)

p Straight Original specimen

Angel (1972)

ent Straight Original specimen

p Curved Original specimen

p Curved Original specimen

ent Curved Original specimen

Curved Lisonek and Trinkaus (2006)

ent Straight Lisonek and Trinkaus (2006)

ent Curved Original specimen

ent¼ 13.3%

10)

Straight¼ 23.3%

(n¼ 10)

Present study

ent¼ 70.7%

53)

Concave¼ 76.7%

(n¼ 33)

p¼ 16.0%

12)

426 R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

sample. It is also present in Amud 7, where it is very deep andpossibly pathological. Unfortunately, it is currently not clearwhether La Ferrassie 3 or Le Moustier 1 show this depressedarea.

Curvature of the long process

In lateral view, the anterior surface of the long process inliving humans normally shows a gently or markedly concavecurvature (Fig. 8). This curvature is accentuated distally bythe lenticular process, which joins the tip of the long processwith the head of the stapes. However, the body of the long pro-cess itself also generally shows this curvature. Among ourmodern human comparative sample, 23.3% of the individualsshowed what was judged to be a relatively straight longprocess, while the remainder showed a concave curvature(Table 4).

The incus in Neandertals has been said to be characterizedby a relatively straight long process, which differs from themore curved long process in modern humans (Heim, 1982).Indeed, all three known Neandertal incudi (La Ferrassie 3,Le Moustier 1 and Amud 7) show a very straight long processwith very little anterior curvature (Heim, 1982; Ponce de Leonand Zollikofer, 1999). Among our modern human comparativesample, 16.3% of the individuals (7 of 43 specimens) showa long process as straight as that seen in Amud 7.

Within the Qafzeh sample, Qafzeh 11 shows a straight longprocess (Fig. 8), almost as straight as in Amud 7. The curvature

Fig. 8. Variation in the long process of the incus among Pleistocene and recent hu

border of the long process is the normal condition in both living and fossil H. sapi

straight long process. Note also the more closed angle between the long and shor

human, straight (NYC 061948; reversed); (B) modern human, concave (SF 4610);

15. Scale bar¼ 1 cm.

is more pronounced in Qafzeh 21, while both Qafzeh 12 andQafzeh 15 (Fig. 8) show the clearest curvatures. The incus inthe Lager Velho 1 individual is missing the tip of the long pro-cess. Nevertheless, it is clear that this specimen shows a curva-ture similar to that in the majority of living humans. Among theDolni Vestonice specimens, DV 14 shows a clearly curved longprocess, while that of DV 15 is somewhat straighter (Lisonekand Trinkaus, 2006).

Thus, the straight long process of Neandertals is a featurethat can be found among both living and fossil H. sapiens,but it is present in 100% of the, admittedly small, Neandertalsample. The functional implications of the straight long pro-cess in Neandertals are not currently clear, but it may be re-lated to a different placement of either the tip of the longprocess of the incus or the footplate of the stapes within thetympanic cavity. Additional support for this hypothesis isfound in the highly asymmetrical crurae (Heim, 1982;Arensburg et al., 1996) and anteriorly skewed head of thestapes in the Neandertals.

Metric variation in the malleus

The metrical assessment of the malleus includes seven lin-ear variables and one angular variable. In our modern humanreference sample, the total length of the malleus was moder-ately correlated with both corpus length (r¼ 0.75) and manu-brium length (r¼ 0.68), suggesting that the variation in thetotal length of the malleus depends primarily on the lengths

mans. Although some variation is present, a concave curvature to the anterior

ens. In contrast, all known Neandertal incudi, including Amud 7, show a very

t processes in Amud 7 compared with the H. sapiens specimens. (A) Modern

(C) Amud 7 (reversed); (D) Qafzeh 11 (reversed); (E) Qafzeh 12; (F) Qafzeh

Tab

le5

Mal

leu

sm

easu

rem

ents

1(m

m)

info

ssil

and

liv

ing

hu

man

s

Sp

ecim

en/s

amp

leS

ide

To

tal

len

gth

Man

ubri

um

Co

rpu

s

len

gth

Hea

d

wid

th

Nec

k

wid

th

An

gle

bet

wee

n

the

axes

(deg

.)

Man

ubri

um

/

len

gth

inde

x

Man

ubri

um

/

corp

us

inde

x

Co

rpu

s/

len

gth

ind

ex

Man

ubri

um

robu

stic

ity

ind

exL

eng

thT

hic

kn

ess

Arc

dep

th

Bia

che-

Sai

nt-

Vaa

st1

Lw

8.8

w4

.16

.40

2.7

0w

46

.59

w6

4.0

6w

77

.27

La

Fer

rass

ie3

R9

.00

4.8

06

.00

2.7

01

47

.05

3.3

38

0.0

06

6.6

7

Dar

ra-i

-Ku

rR

8.3

05

.00

2.5

06

0.2

4

Qaf

zeh

11

L>

7.1

45

.39

2.4

10

.82

w1

40

.0

Qaf

zeh

12

R7

.37

4.0

21

.10

0.3

35

.21

2.6

20

.92

13

8.0

54

.55

77

.16

70

.69

27

.36

Qaf

zeh

15

R7

.72

4.4

81

.00

0.2

85

.30

2.4

40

.84

13

7.0

58

.03

84

.53

68

.65

22

.32

Naz

let

Kh

ater

2R

8.0

14

.67

0.9

00

.27

5.4

32

.55

0.8

61

36

.45

8.3

08

6.0

06

7.7

91

9.2

7

Do

lni

Ves

ton

ice

14

L7

.90

4.6

02

.50

58

.23

Lag

arV

elh

o1

R7

.99

4.3

60

.81

0.2

55

.50

2.2

60

.86

13

7.4

54

.57

79

.27

68

.84

18

.58

Lag

arV

elh

o1

L8

.00

4.3

80

.81

0.1

95

.67

2.3

30

.88

13

9.9

54

.75

77

.25

70

.88

18

.49

Fo

ssil

H.

sapi

ens

mea

n7

.90

4.5

00

.92

0.2

65

.42

2.4

50

.86

13

8.1

56

.95

80

.84

69

.37

21

.21

Liv

ing

hu

man

s

Mea

n�

s.d

.

8.2

5�

0.4

14

.94�

0.3

11

.00�

0.0

90

.33�

0.1

55

.83�

0.3

52

.43�

0.1

70

.99�

0.1

31

32

.1�

6.2

59

.97�

2.8

18

5.0

1�

5.1

57

0.6

6�

2.8

02

0.2

8�

1.9

4

Liv

ing

hu

man

s

Ran

ge

(n)

7.4

3e

9.3

1

(43

)

4.2

2e5

.59

(43

)

0.8

1e1

.19

(43

)

0.0

5e

0.6

4

(43

)

4.9

6e6

.69

(43

)

2.0

3e2

.79

(43

)

0.8

0e1

.36

(43

)

11

6.5

e1

45

.7

(43

)

53

.13e

65

.69

(43

)

74

.12e

93

.48

(43

)

65

.18e

76

.35

(43

)

16

.57e

25

.62

(43

)

1S

eete

xt

for

mea

sure

men

tso

urc

es.

427R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

of these two structures. A similar correlation (r¼ 0.67) wasfound between head width and total malleus length. The corre-lations were much lower between all other malleus variables.

The total length of the malleus in all of the fossil H. sapiensspecimens falls below the mean value for our modern humansample (except for Darra-i-Kur), and the two Qafzeh specimensrepresent the smallest individuals in the sample (Table 5). Al-though Qafzeh 12 (7.37 mm) falls below the lower limit of themodern human range in the present study, it is within the vari-ation observed in other studies of living humans (Arensburget al., 1981). The manubrium length, both absolute and relativeto total malleus length, is similarly short and the mean values inthe fossil H. sapiens sample are more than 1.0 s.d. below thoseof our sample of living humans. Among the Qafzeh specimens,Qafzeh 12 shows the shortest absolute length of the manubrium(4.02 mm), but its relative length is nearly identical to that ofLagar Velho.

In contrast, the total length in the two Neandertal lineagespecimens, Biache (w8.8 mm) and La Ferrassie 3 (9.0 mm),is very long, falling, respectively, 1.3 and 1.8 s.d. above themean of our modern human sample (8.25 mm). The manu-brium length shows a degree of variation, with Biache(w4.1 mm) being very short and that of La Ferrassie 3(4.80 mm) being very similar to our modern human mean.When manubrium length is compared with the total length,Biache falls outside our modern human range of variation,while La Ferrassie 3 is toward the lower limit. Nevertheless,the incomplete nature of the manubrium in Biache (Crevecoeur,2007) urges caution when interpreting this specimen. Indeed,the manubrium length is very short, similar to the very shortvalue in Qafzeh 12. If a longer manubrium is estimated, itwould also have the effect of increasing the total lengthsomewhat. Thus, both the manubrium length and total lengthin Biache may represent minimum values.

The mean corpus length within the fossil H. sapiens spec-imens (5.42 mm) falls just over 1.0 s.d. below the mean forour extant human sample (5.83 mm), and the Qafzeh speci-mens are again the smallest individuals. The corpus lengthsin the two Neandertal lineage specimens (6.00 and 6.40 mm)are considerably longer, although within our modern humanrange of variation. This is not surprising, given the correlationwith total length mentioned above. Within living humans, in-creases in total malleus length are primarily a result of in-creases in the corpus length, and in our modern humancomparative sample, the specimen with the longest corpuslength also showed the longest total length. Nevertheless,when corpus length is compared with the total length, the re-sulting index in both Qafzeh specimens is within 1.0 s.d. of themean value in our modern human comparative sample. Varia-tion in this index in the two Neandertals brackets that of thefossil H. sapiens specimens. When the corpus length is com-pared with the manubrium length, all of the fossil specimens(except Nazlet Khater 2) fall below our modern humanmean, but only Biache falls outside the range of variation.However, this may be an artifact of the short estimated lengthreconstructed for the incomplete manubrium in the Biachespecimen.

428 R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

The angle between the axes of the malleus in all of the fos-sil specimens is above the mean of our modern human com-parative sample (132.1�). This angle is quite similar in allthe fossil H. sapiens specimens, and the Qafzeh individualsdo not stand out within the sample. In contrast, the angle inboth Biache (154�) and the La Ferrassie 3 Neandertal (147�)is considerably higher, falling above our modern human rangeof variation. Thus, there is evidence for a wider angle in the Ne-andertal lineage specimens.

The mean head width among the fossil H. sapiens(2.45 mm) is nearly identical to our modern human meanvalue (2.43 mm), and Qafzeh 12 (2.62 mm) shows the largesthead within the sample. Both Neandertal specimens showidentical larger values (2.70 mm), suggesting a wider headcharacterized the malleus in the Neandertal lineage.

In the remaining malleus variables (manubrium thickness,robusticity index, arc depth, and the width of the neck), thevalues in the fossil H. sapiens specimens are quite similar tothose in living humans (Table 5). The one exception seemsto be the high robusticity index of the manubrium in Qafzeh12 (27.36), which falls well above our modern human rangeof variation (16.57e25.62) and suggests a short but thick ma-nubrium in this specimen. Interestingly, the values for headwidth and neck width in Qafzeh 12 are also the largest withinthe fossil H. sapiens sample. These three dimensions suggestthat Qafzeh 12, while showing small metric dimensions over-all, is a robust ossicle. In contrast, Qafzeh 15 is slightly larger,but appears less robust.

The comparative metric analysis of the malleus has re-vealed that the fossil H. sapiens sample is generally smallerthan in living humans. Within the fossil H. sapiens sample,Qafzeh 12 and 15 represent the smallest individuals, extendingthe known range of variation for this sample. In contrast, thetwo Neandertal lineage specimens show larger dimensions inboth total length and corpus length but not manubrium length.The results of the present study, then, support previous sugges-tions for a clear and consistent size difference between Nean-dertals and fossil H. sapiens individuals (Heim, 1982;Crevecoeur, 2007).

In addition, a higher angle in the malleus has been previ-ously suggested to represent a shared feature between the Ne-andertals and fossil H. sapiens (Spoor, 2002; Crevecoeur,2007). However, the present study, using a different definitionof the malleus angle, found a more modest difference betweenthe fossil H. sapiens and living humans. In contrast, the Nean-dertal specimens continue to fall outside the range of variationin our extant human sample. Thus, rather than representinga shared feature between Neandertals and fossil H. sapiens in-dividuals, the results of the present study suggest that a moreopen angle of the malleus characterizes only the Neandertalevolutionary lineage.

Metric variation in the incus

The metric assessment of the incus includes seven linear var-iables and one angular variable. In our modern human referencesample, the long process length is moderately correlated with

both intercrural length (r¼ 0.80) and the functional length(r¼ 0.78). The correlations were much lower between all otherincus variables.

The length of the short process in most of the fossil H. sa-piens specimens falls below our modern human mean value(5.07 mm), but the range of variation in the fossil sample isvery similar to that in living humans (Table 6). The two newQafzeh specimens fall between the previously known individ-uals. Similarly, the two Neandertal specimens are unremark-able in their short process lengths, with La Ferrassie 3(4.86 mm) being somewhat shorter, and Amud 7 (5.07 mm)being identical to the values of both Qafzeh 11 and our modernhuman sample.

Although the mean length of the long process in the fossilH. sapiens sample is below our modern human sample mean,the range of variation in the fossil sample (6.34e7.10 mm) islarge. The Neandertal lineage specimens do seem to show lon-ger long processes, with the value in Biache (7.50 mm) fallingtoward the upper limit of our modern human range.

The crural index compares the short process (crus) with thelong process (crus), and the values in all of the fossil speci-mens (except Dolni Vestonice 14) fall below our modern hu-man mean (74.28). Contrary to previous suggestions (Poncede Leon and Zollikofer, 1999), it is difficult to identify anyconsistent difference between the fossil H. sapiens and Nean-dertal specimens.

The angle formed between the long and short processes is quitestable within the fossil H. sapiens specimens and similar to themean value for our extant human sample (64.0�) (Table 6).The notable exception to this is Qafzeh 11, whose angle (52.4�)is below the lower limit of our modern human range and moresimilar to the low angles found in both La Ferrassie 3 (52.1�)and Amud 7 (48.3�).

The articular facet height in nearly all of the fossil speci-mens (except Qafzeh 21) is larger than the mean value inour modern human comparative sample in the present study.Nevertheless, Kirikae (1960) reported a somewhat taller artic-ular facet (3.26� 0.05 mm) in his modern human sample. Thisis nearly identical to the fossil H. sapiens mean value, al-though the values in Darra-i-Kur (3.70 mm) and Qafzeh 11(3.45 mm) continue to stand out. Both the Neandertal speci-mens are also fairly large (3.37e3.40 mm), suggesting thata slightly expanded incus articular facet characterizes thisgroup of hominins.

The functional length of the long process is a physiologicallyrelevant variable for evaluating the contribution of the incus tothe transmission of sound energy through the middle ear (Ro-sowski and Relkin, 2001). The functional lengths in the fossilH. sapiens individuals are all quite similar to the living humanmean value, with the sole exception of Qafzeh 15, which fallsjust below the lower limit of our modern human range of vari-ation (Table 6). The value in Amud 7 (4.08 mm) falls just aboveour modern human mean (4.01 mm), while that in La Ferrassie3 (4.41 mm) is close to the upper limit of our modern humanrange of variation. Based on its correlation with the long cruslength, variation in the functional length appears to explainabout 60% of the variation in long crus length in living humans.

Tab

le6

Incu

sm

easu

rem

ents

1(m

m)

info

ssil

and

liv

ing

hu

man

s

Sp

ecim

en/s

amp

leS

ide

Sh

ort

pro

cess

len

gth

Lo

ng

pro

cess

Art

icul

arfa

cet

hei

ght

Fu

nct

ion

al

len

gth

Inte

rcru

ral

An

gle

of

the

axes

(deg

.)

Cru

ral

ind

ex

Len

gth

Arc

dep

thL

eng

thA

rcd

epth

Bia

che-

Sai

nt-

Vaa

st1

7.5

05

.90

La

Fer

rass

ie3

R4.8

67.2

00.3

63.4

04.4

15.8

41.4

652.1

67.5

Le

Mo

ust

ier

1L

6.8

0

Am

ud

7L

5.0

76

.98

0.2

83

.37

4.0

85

.38

2.1

34

8.3

72

.6

Dar

ra-i

-Ku

rR

4.8

03

.70

6.0

0

Qaf

zeh

11

L5

.07

6.9

40

.30

3.4

54

.05

5.9

52

.00

52

.47

3.1

Qaf

zeh

12

2R

4.7

06

.73

0.4

33

.30

3.8

45

.85

1.3

06

2.0

69

.8

Qaf

zeh

15

2R

4.6

46

.34

0.3

53

.20

3.5

75

.29

1.6

06

1.7

73

.2

Qaf

zeh

21

R4

.55

6.4

70

.44

2.9

93

.93

5.5

21

.46

61

.77

0.3

Do

lni

Ves

ton

ice

14

L5

.50

7.1

00

.56

3.3

54

.11

6.6

01

.75

67

.37

7.5

Do

lni

Ves

ton

ice

15

R4

.10

6.4

00

.35

3.1

53

.89

5.5

01

.35

62

.66

4.1

Lag

arV

elh

o1

R4

.76

0.2

63

.14

>3

.23

w6

1.5

Fo

ssil

H.

sapi

ens

mea

n4

.77

6.6

60

.38

3.2

93

.90

5.8

21

.58

61

.37

1.3

2

Liv

ing

hu

man

s

Mea

n�

s.d

.

5.0

7�

0.3

76

.83�

0.3

20

.56�

0.1

43

.00�

0.1

94

.01�

0.2

26

.18�

0.3

41

.66�

0.2

16

4.0�

4.7

74

.28�

4.9

0

Liv

ing

hu

man

s

Ran

ge

(n)

4.0

2e5

.86

(41

)

6.1

7e7

.59

(43

)

0.2

5e0

.80

(43

)

2.6

0e3

.41

(42

)

3.6

1e

4.4

6

(42

)

5.6

1e

7.4

4

(41

)

1.1

8e

1.9

5

(41

)

56

.6e

75

.6

(41

)

59

.20e

84

.78

(41

)

1S

eete

xt

for

mea

sure

men

tso

urc

es.

20

.2m

mw

asad

ded

toth

ep

rese

rved

lon

gp

roce

ssle

ngt

han

dre

late

dm

easu

res.

429R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

Thus, the long functional length in the Neandertals appearsto explain the longer long process lengths in these twospecimens.

The values for the curvature (arc depth) of the long processare generally lower in both the fossil H. sapiens and Neander-tals than in living humans, with only Dolni Vestonice 14matching our modern human mean (0.56 mm). This meansthat the long process is generally straighter in the fossil spec-imens. The low values in the Neandertals are compatible withthe suggestion that they show very straight long crurae. Nev-ertheless, the value in Qafzeh 11 (0.30 mm) is nearly identicalto that in Amud 7 (0.28 mm), and there is some overlap in thismeasure between Neandertals and fossil H. sapiens.

The intercrural length in the fossil H. sapiens sample is againsmall, with the exception of Dolni Vestonice 14, which falls be-low our modern human mean value (6.18 mm). Interestingly, allthree of the Neandertal lineage specimens also show small inter-crural lengths, with the value in Amud 7 (5.38 mm) beingvery similar to that in Qafzeh 15 (5.29 mm), the smallest fossilH. sapiens individual. Given the correlation between intercrurallength and long process length mentioned above, the Neander-tals might be expected to show wider intercrural lengths. How-ever, the lower angle between the long and short processes in theNeandertals results in an absolutely short intercrural length.

The intercrural arc depth does not seem to follow any con-sistent pattern. Large and small values are found in both thefossil H. sapiens and Neandertal specimens, and the valuesin Qafzeh 11 (2.00 mm) and Amud 7 (2.13 mm) fall abovethe upper limits of the range of variation in our modern humansample.

The analysis of metric variation in the incus has shown thefossil H. sapiens specimens to be generally smaller than theirliving counterparts. Both Qafzeh 12 and 15 conform to thispattern, and in several dimensions, Qafzeh 15 extends theknown range of variation within the fossil H. sapiens sample.

The Amud 7 Neandertal incus shows a very low anglebetween the short and long processes, resembling the La Fer-rassie 3 Neandertal specimen. These results confirm that Ne-andertals do indeed have lower angles, while the angle inmodern humans is more open, although the differences arenot as marked as suggested previously (Heim, 1982; Spoor,2002; Tillier, 1999). In addition, the curvature (arc depth) ofthe long process in Amud 7 and La Ferrassie 3 is very low,confirming that Neandertals are characterized by very straightlong processes (Heim, 1982). Interestingly, both the lower an-gle and the straighter long process in Neandertals may indicatea slightly different placement of either the oval window or tipof the long process within the tympanic cavity. However,Amud 7 is also metrically very close to Qafzeh 11 in nearlyall dimensions, including the angle between the axes and thearc depth of the long crus. Thus, these are not uniquely derivedfeatures in Neandertals, although they do occur at a higher fre-quency among them.

Two additional inferences can be drawn regarding the Ne-andertal incus from the available data. First, the Neandertalsappear to show an expanded articular facet compared with liv-ing humans, a finding that parallels the larger head widths in

430 R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

the malleus. Second, there is a suggestion of a temporal trendwithin the Neandertal lineage toward reduction of the longprocess. The oldest specimen (Biache) has the longest longprocess, while the youngest (Le Moustier 1) has the shortest.Nevertheless, a larger sample size of both Neandertals andtheir middle Pleistocene precursors is clearly needed to con-firm this.

Metric variation in the malleus/incus complex

The presence of both the malleus and incus in Qafzeh 12and 15 makes it possible to investigate relationships betweenthese bones within the same individual. Comparison of the to-tal malleus length with the long process length of the incus isa good measure of the relative size of both bones. The result-ing index in Qafzeh 12 (109.5) falls just outside the lower limitof our modern human range of variation and is very similar tothe value in Dolni Vestonice 14 (111.3) (Table 7). The lowvalues in these two specimens are a product mainly of a shortmalleus in Qafzeh 12 and a long long process in the Dolni Ves-tonice 14 incus. In contrast, the value in Qafzeh 15 (121.8) isnearly identical to our modern human mean value. Similarly,despite their absolutely long mallei, the two Neandertal line-age specimens fall easily within 1.0 s.d. of the mean valuefor our sample of modern humans (Table 7).

When the malleus’ manubrium length is compared with theincus’ functional length, the resulting index is known as thelever ratio of the middle ear. This is an important variable indetermining the physiological role of the ear ossicles in audi-tion (Rosowski and Relkin, 2001). The precise measurementof the malleus and incus levers (i.e., functional lengths) hasbeen a topic of research for over a century and a number ofstudies have reached different conclusions regarding the valueof this anatomical transformer in the middle ear. Estimates ofthe lever ratio have ranged from 150 (Helmholtz, 1873) to 100(i.e., no mechanical advantage) (Kirikae, 1960). Nevertheless,most studies seem to suggest a value of 125e130 for living hu-mans (Dahmann, 1929, 1930; Stuhlmann, 1937; Rosowski,1994). The modern human lever ratio in the present studyyields values (mean¼ 123.4) that are similar to those reported

Table 7

Measurements1 of the malleus/incus complex in fossil and living humans

Specimen/sample Malleus total length/

Incus long process length

Biache-Saint-Vaast 1 w117.3

La Ferrassie 3 125.0

Darra-i-Kur

Qafzeh 11

Qafzeh 122 109.5

Qafzeh 152 121.8

Dolni Vestonice 14 111.3

Lagar Velho 1

Living human mean � s.d. 120.83� 5.56

Living human range (n) 111.24e130.95 (43)

1 See text for measurement sources.2 0.2 mm was added to the preserved incus long process length and related mea3 Lever ratio¼ (manubrium length/incus functional length)� 100.

in other studies, notably Rosowski (1994) (mean¼130), Stuhlmann (1937) (mean¼ 127) and Dahmann (1929,1930) (mean¼ 131).

The lever ratios in the fossil H. sapiens specimens showa wide range of variation (Table 7). The value in Qafzeh 12(104.7) falls toward the lower limit of our modern humanrange, indicating that the malleus’ manubrium is only slightlylonger than the functional length of the incus. In contrast, thatof Qafzeh 15 (125.5) is slightly above our modern humanmean value. Both the Dolni Vestonice 14 (111.9) and the LaFerrassie 3 Neandertal (108.8) fall in between the two Qafzehindividuals but are still low compared with modern humans.

The combination of a longer manubrium of the malleus andshorter functional length of the incus results in a higher leverratio, which is theoretically more efficient at transmittingsound energy through the middle ear (Coleman and Ross,2004). However, other physical properties of the ossicles,such as their mass, density, and ligamentous attachments alsoinfluence sound transmission through the middle ear, makingit difficult to quantify the effects of a single structural change(i.e., the lever ratio) on auditory performance (Rosowski,1994, 1996). Thus, inferences on the auditory capacities in fos-sil humans should not be based primarily on the lever ratio ora simple model incorporating a limited number of anatomicalmeasurements (Masali et al., 1991; Masali and Cremasco,2006), as these have been shown to generate unreliable resultsin living humans (Rosowski and Relkin, 2001). Rather, a moreprecise approach to estimating the auditory capacities in fossilspecimens requires a comprehensive model that takes intoaccount the physical properties of the ear ossicles and the struc-tures of the outer, middle, and inner ear (Ruggero and Temchin,2002; Martınez et al., 2004).

The articulation of the malleus and incus at the incudomal-leolar joint implies a close functional relationship between thehead of the malleus and the articular facet of the incus. Thehead width measured in the present study corresponds approx-imately to the size of the articular facet on the malleus, andthis, in turn, is related to the height of the articular facet onthe incus. However, the correlation between the malleus’head width and articular facet height of the incus in our

Malleus/Incus

lever ratio3Malleus head width/

Incus articular facet height

108.8 79.4

67.6

69.9

104.7 79.4

125.5 76.3

111.9 74.6

72.0

123.4� 8.5 81.0� 6.1

101.9e138.9 (42) 69.4e97.4 (42)

sures.

431R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

modern human comparative sample is low (r¼ 0.40). The Ne-andertal lineage specimens showed evidence for both a tallerarticular facet height on the incus and an expanded malleus’head width. Comparison of these two dimensions suggeststhat living humans have a head width of the malleus that is ap-proximately 80% of the height of the articular facet of the in-cus. Among the fossil specimens, the identical value (79.4%)in both Qafzeh 12 and La Ferrassie 3 is closest to our modernhuman mean, while the remaining fossil H. sapiens specimenshave a lower index. The two fossil H. sapiens specimens withthe tallest incus articular facets, Qafzeh 11 (3.45 mm) andDarra-i-Kur (3.70 mm), fall toward the very lower limit andoutside of the living human range of variation, respectively.

The comparison of selected variables between the malleusand incus in several fossil human specimens has revealed theirfundamentally human pattern. The short malleus in Qafzeh 12produces very low index values for both of the length ratiosbetween the malleus and incus in this individual, but the artic-ular facet index is very close to our modern human mean. Thiswould suggest that the size of the articular facet is largelyindependent of malleus length. The Neandertal lineage speci-mens do not differ from living humans in any of the indices.

Discussion and conclusion

There are clear anatomical differences between the ear ossi-cles in the Neandertal and H. sapiens evolutionary lineages, and,contrary to previous assertions (Arensburg et al., 1981), thesebones contain taxonomic information useful for separating spe-cies of the genus Homo. The Neandertal malleus can be said todiffer from that of living humans in its larger dimensions, moreopen angle between the head/neck and the manubrium, andlarger head size. Likewise, the Neandertal incus (includingthat of Amud 7) shows a straighter long process, a taller articularfacet, and a more closed angle between the long and short pro-cesses. Although all of the anatomical variants considered in thepresent study can also be found in living humans, they occur ata higher frequency among Neandertals, sometimes reaching100% frequency (e.g., the straight long process of the incus).These bones show a consistent anatomical pattern within theNeandertal lineage that sets them apart, both morphologicallyand metrically, from the majority of living humans.

Neandertals, then, can be said to consistently express onlya portion of the modern human range of variation. Given thislimited degree of metrical and morphological overlap betweenNeandertals and modern humans, it is important to understandthe range of variation expressed in the fossil H. sapiens sam-ple. The new specimens from Qafzeh are particularly im-portant in this regard since they considerably augment thecurrent sample of fossil H. sapiens and predate the latePleistocene specimens from Europe and North Africa.

The fossil H. sapiens sample generally shows smaller di-mensions in both the malleus and incus than their living coun-terparts in most metric variables, and the Qafzeh specimensare no exception. Within the Qafzeh sample, the malleus ofQafzeh 12 shows much smaller dimensions than either Qafzeh15 or (where they can be compared) Qafzeh 11. The

exceptions include manubrium thickness, neck width, andhead width. These three thickness dimensions suggest thatthe Qafzeh 12 malleus is a more ‘‘robust’’ ossicle than is Qaf-zeh 15. In contrast, the incus of Qafzeh 15 is generally smallerthan that of Qafzeh 12, while Qafzeh 11 is the largest in mostdimensions. Nevertheless, the metric variation within the Qaf-zeh sample is similar in degree to the differences observed be-tween Dolni Vestonice 14 and 15. The new Qafzeh specimensdo extend the known range of variation in the fossil H. sapienssample in a number of metric dimensions in both the malleusand incus, and some measurements in the Qafzeh specimensfall outside the range of variation in our modern human compar-ative sample in the present study. However, it is not possible toidentify any consistent metric or morphological differences be-tween the Qafzeh sample and the geologically younger UpperPaleolithic specimens from Europe or North Africa.

In both the malleus and incus, the variation within the tem-porally and geographically restricted Qafzeh sample is gener-ally greater than that observed among the temporally andgeographically diverse sample of Neandertal lineage speci-mens. The Qafzeh 11 incus stands out within the sample forhaving both a more closed angle between the long and shortprocesses and a very straight long process; it resembles Nean-dertals in both these aspects. Indeed, the Qafzeh 11 incus isboth metrically and morphologically very similar to that ofAmud 7. However, the malleus in Qafzeh 11 lacks the elon-gated corpus length that is characteristic of Neandertals, andthe cranial anatomy in this specimen is consistent with its at-tribution to H. sapiens (Tillier, 1999; Schwartz and Tattersall,2003). Thus, despite the metric and morphological similaritybetween the Qafzeh 11 and Amud 7 incudi, there is no evi-dence among the auditory ossicles from Qafzeh for morethan one species at this site.

From the metric data, three tentative hypotheses regardingevolution of the ear ossicles in the genus Homo can be ad-vanced. First, there appears to have been a real difference inthe overall dimensions of the malleus between Neandertalsand fossil H. sapiens individuals. In their total malleus length,corpus length, and head width, Neandertals are clearly larger.This size difference may be partly related to the generallylarger body mass in Neandertals (Ruff et al., 1997), sinceacross mammals, the size of the ossicles is generally correlatedwith body size (Rosowski, 1994). The larger malleus headwidth suggests a larger incudomalleolar joint, and this also ap-pears to be reflected in the taller incus articular facet amongthe Neandertals.

Second, contrary to previous suggestions (Lisonek andTrinkaus, 2006), there does appear to be limited evidencefor a temporal trend among Neandertals in the reduction ofthe long process in the incus. The earliest specimen (Biache)shows the longest long process, while successively youngerspecimens show decreasing lengths of the long process.Clearly, a larger sample of Neandertal lineage specimens isneeded to confirm this tentative suggestion.

Third, there is evidence for a slightly different placement ofeither the tip of the incus long process or the oval window, forthe insertion of the stapes footplate, within the tympanic cavity

432 R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

in the Neandertals. This suggestion is based on the higher an-gle between the head/neck and manubrium in the malleus, thelower angle between the long and short processes in the incus,and the straighter long process of the incus in Neandertals. Inaddition, the few Neandertal stapes that are known all show ananteriorly skewed stapedial head (Heim, 1982; Arensburget al., 1996; Maureille, 2002).

Interestingly, many of these features were mentioned byHeim (1982) as possible Neandertal distinctions present inthe La Ferrassie 3 ear ossicles. Thus, Heim’s (1982) early sug-gestions of consistent differences between Neandertal andmodern human auditory ossicles are largely borne out by sub-sequent discoveries. What is less clear is whether these ana-tomical differences represent derived features within theNeandertal lineage or primitive retentions common to archaicmembers of the genus Homo.

The consistent differences identified between the malleusand incus in the Neandertal and H. sapiens lineages indicatethat the auditory ossicles are an important source of phyloge-netic information. Future discoveries of auditory ossicles fromNeandertals, as well as geologically older and taxonomicallydiverse specimens, should aide in resolving some of the tenta-tive hypotheses outlined in the present study. Given the stronggenetic control that governs the development of the ear ossi-cles, analysis of the morphological and metric variation inthese tiny anatomical structures promises to provide newinsights into evolutionary processes in the genus Homo.

Acknowledgements

E. Trinkaus and C. Duarte kindly provided access to the La-gar Velho specimens. T. Greiner allowed for data collection onthe sample of ear ossicles from the New York ChiropracticCollege in Seneca Falls, New York. B. Arensburg kindly pro-vided access to the Subalyuk 2 stapes in his care. A.M. Tillierprovided helpful comments on the final version of the manu-script. M.C. Ortega cleaned and prepared the new Qafzeh spec-imens. R. Quam was supported by a grant from the FundacionDuques de Soria/Fundacion Atapuerca. This research wassupported by the Ministerio de Ciencia y Tecnologıa of theGovernment of Spain, Project No. CGL2006-13532-C03-02.

References

Angel, J.L., 1972. A Middle Paleolithic temporal bone from Darra-i-Kur,

Afghanistan. Trans. Am. Phil. Soc. 62, 54e56.

Arensburg, B., Belkin, V., Wolf, M., 2005. Middle ear pathology in ancient

and modern populations: incudal osteoma. Acta Otolaryngol. 125,

1164e1167.

Arensburg, B., Harrell, M., Nathan, H., 1981. The human middle ear ossicles:

morphometry, and taxonomic implications. J. Hum. Evol. 10, 199e205.

Arensburg, B., Nathan, H., 1971. Observations on a notch in the short

(superior or posterior) process of the incus. Acta Anat. 78, 84e90.

Arensburg, B., Nathan, H., 1972. A propos de deux osselets de l’oreille moy-

enne d’un neandertalo€ıde trouves a Qafzeh (Israel). L’Anthropologie

(Paris) 76, 301e308.

Arensburg, B., Nathan, H., Ziv, M., 1977. Malleus fixed (ossified) to the

tegmen tympani in an ancient skeleton in Israel. Ann. Otol. 86, 75e79.

Arensburg, B., Pap, I., Tillier, A.M., Chech, M., 1996. The Subalyuk 2 middle

ear stapes. Int. J. Osteoarcheol. 6, 185e188.

Arensburg, B., Tillier, A.M., 1983. A new Mousterian child from Qafzeh

(Israel). Bull. Mem. Soc. Anthropol. Paris 10, 61e69.

Bailey, S., Pilbrow, V., Wood, B., 2004. Interobserver error involved in inde-

pendent attempts to measure cusp base areas of Pan M1s. J. Anat. 205,

323e331.

Birkby, W., Gregg, J., 1975. Otosclerotic stapedial footplate fixation in an 18th

century burial. Am. J. Phys. Anthropol. 42, 81e84.

Blumer, W., Freedman, L., Lofgren, M., 1982. Middle ear ossicles of Australian

aborigines. Archaeol. Oceania 17, 127e131.

Bouchet, A., Giraud, M., 1968. Contribution a l’etude morphologique et radi-

ologique des osselets de l’ouie. C.R. Assoc. Anat. 53, 588e600.

Bruintjes, T., 1990. The auditory ossicles in human skeletal remains from

a leper cemetery in Chichester, England. J. Archaeol. Sci. 17, 627e633.

Coleman, M., Ross, C., 2004. Primate auditory diversity and its influence on

hearing performance. Anat. Rec. 281A, 1123e1137.

Crevecoeur, I., 2007. New discovery of an Upper Paleolithic auditory ossicle:

The right malleus of Nazlet Khater 2. J. Hum. Evol. 52, 341e345.

Dahmann, H., 1929. Zur physiologie der horens; experimentelle untersuchun-

gen uber die mechanik der Gehorknochelchenkette, sowie uber deren ver-

halten auf ton und luftdruck. Z. Hals-Nasen-Ohrenheilk 24, 462e497.

Dahmann, H., 1930. Zur physiologie der horens; experimentelle untersuchun-

gen uber die mechanik der Gehorknochelchenkette, sowie uber deren

verhalten auf ton und luftdruck. Z. Hals-Nasen-Ohrenheilk 27, 329e368.

Daniel, H., Schmidt, R., Fulghum, R., Ruckriegal, L., 1988. Otitis media:

a problem for the physical anthropologist. Yearb. Phys. Anthropol. 31,

143e167.

Davis, G., 1987. Pathology of otosclerosis. Am. J. Otolaryngol. 8, 273e281.

de Ruiter, D., Moggi-Cecchi, J., Magali, M., 2002. Auditory ossicles of Paran-thropus robustus from Swartkrans, South Africa. Am. J. Phys. Anthropol.

34 (Suppl.), 60.

Ferrino, M., Magali, M., Masiero, C., 1994. Primi tentativi di fotogrammetria

degli ossicini dell’orecchio medio: esperienze metodologiche. Antropol.

Contemp. 17, 167e175.

Gray, H., 1977. Anatomy, Descriptive and Surgical. Bounty Books, New York.

Grun, R., Stringer, C., 1991. ESR dating and the evolution of modern humans.

Archaeometry 33, 153e199.

Heim, J.L., 1982. Les Enfants Neandertaliens de La Ferrassie. Masson, Paris.

Helmholtz, H., 1873. The Mechanism of the Ossicles of the Ear and

Membrana Tympani. William Wood & Co, New York.

Heron, I., 1923. Measurements and observations upon the human auditory

ossicles. Am. J. Phys. Anthropol. 6, 11e26.

Hershkovitz, I., 1977. Living New World Monkeys (Platyrrhini) with an Intro-

duction to Primates. Vol. 1. University of Chicago Press, Chicago.

Hovers, E., Rak, Y., Lavi, R., Kimbel, W., 1995. Hominid remains from Amud

cave in the context of the Levantine Middle Paleolithic. Paleorient 21,

47e61.

Kirikae, I., 1960. The Structure and Function of the Middle Ear. University of

Tokyo Press, Tokyo.

Linthicum, T., 1993. Histopathology of otosclerosis. Otolaryngol. Clin. North

Am. 26, 335e352.

Lisonek, P., 1992. Ossicula auditus mladopaleolitickych lovcu mamutu z

Dolnıch Vestonic. Acta Musei Nationalis Pragae XLVIII, 65e68.

Lisonek, P., Kutal, M., Peske, L., Kubınek, R., 1986. Auditory ossicles from

archaeological finds. L’Anthropologie (Brno) 24, 185e188.

Lisonek, P., Trinkaus, E., 2006. The auditory ossicles. In: Trinkaus, E.,

Svoboda, J. (Eds.), Early Modern Human Evolution in Central Europe:

The People of Dolni Vestonice and Pavlov. Oxford University Press,

Oxford, pp. 153e155.

Martınez, I., Rosa, M., Arsuaga, J.L., Jarabo, P., Quam, R., Lorenzo, C.,

Gracia, A., Carretero, J.M., Bermudez de Castro, J., Carbonell, E., 2004.

Auditory capacities in middle Pleistocene humans from the Sierra de

Atapuerca in Spain. Proc. Nat. Acad. Sci. U.S.A. 101, 9976e9981.

Masali, M., 1964. Dati sulla variabilita morfometrica e ponderale degli ossicini

dell’udito nell’Uomo. Arch. Ital. Anat. Embriol. 69, 435e446.

Masali, M., Borgognini Tarli, S.M., Maffei, M., 1992. Auditory ossicles and

the evolution of the primate ear: a biomechanical approach. In: Wind, J.

433R. Quam, Y. Rak / Journal of Human Evolution 54 (2008) 414e433

(Ed.), Language Origin: A Multidisciplinary Approach. Kluwer Academic

Publishers, Amsterdam, pp. 67e86.

Masali, M., Chiarelli, B., 1965a. Analisi morfometrica comparata degli ossi-

cini dell’udito dei primati I. Il martello nelle scimmie del Vecchio Mondo

e nell’uomo. Riv. Antropol. 52, 137e146.

Masali, M., Chiarelli, B., 1965b. Analisi morfometrica comparata degli ossi-

cini dell’udito dei Primati II. L’incudine nelle scimmie del Vecchio Mondo

e nell’uomo. Riv. Antropol. 52, 147e157.

Masali, M., Cremasco, M., 2006. Hoc alterum auditus organi ossiculum est:

ear ossicles in physical anthropology. Hum. Evol. 21, 1e17.

Masali, M., Maffei, M., Borgognini Tarli, S.M., 1991. Application of a mor-

phometric model for the reconstruction of some functional characteristics

of the external and middle ear in Circeo 1. In: Piperno, M., Scichilone, G.

(Eds.), The Circeo 1 Neandertal Skull: Studies and Documentation. Insti-

tuto Poligrafico e Zecca Dello Stato, Rome, pp. 321e338.

Maureille, B., 2002. A lost Neanderthal neonate found. Nature 419, 33e34.

Minugh-Purvis, N., Radovcic, J., Smith, F., 2000. Krapina 1: a juvenile Nean-

dertal from the early late Pleistocene of Croatia. Am. J. Phys. Anthropol.

111, 393e424.

Moggi-Cecchi, J., Collard, M., 2002. A fossil stapes from Sterkfontein, South

Africa, and the hearing capabilities of early hominids. J. Hum. Evol. 42,

259e265.

Mutaw, R., 1986. Human Auditory Ossicle Variation and Function. Depart-

ment of Anthropology, University of Colorado, Boulder, CO.

Mutaw, R., 1988. Variation in the frequency of a notch in the short process of

the incus in six different human skeletal populations. Int. J. Anthropol. 3,

199e205.

Ponce de Leon, M.S., Zollikofer, C., 1999. New evidence from Le Moustier 1:

computer-assisted reconstruction and morphometry of the skull. Anat. Rec.

254, 474e489.

Quam, R., Martınez, I., Arsuaga, J.L., 2006. Middle Pleistocene auditory

ossicles from the Sierra de Atapuerca (Spain). Am. J. Phys. Anthropol.

42 (Suppl.), 149.

Rak, Y., Clarke, R., 1979. Ear ossicle of Australopithecus robustus. Nature

279, 62e63.

Rak, Y., Kimbel, W., Hovers, E., 1994. A Neandertal infant from Amud cave,

Israel. J. Hum. Evol. 26, 313e324.

Rink, W., Schwarcz, H., Lee, H., Rees-Jones, J., Rabinovich, R., Hovers, E.,

2001. Electron spin resonance (ESR) and thermal ionization mass spectro-

metric (TIMS) 230Th/234U dating of teeth in Middle Paleolithic layers at

Amud Cave, Israel. Geoarchaeology 16, 701e717.

Rosowski, J., 1994. Outer and middle ears. In: Fay, R., Popper, A. (Eds.),

Comparative Hearing: Mammals. Springer-Verlag, New York, pp. 172e

247.

Rosowski, J., 1996. Models of external- and middle-ear function. In:

Hawkins, H., McMullen, T., Popper, A., Fay, R. (Eds.), Auditory Compu-

tation. Springer, New York, pp. 15e61.

Rosowski, J., Relkin, E., 2001. Introduction to the analysis of middle-ear func-

tion. In: Jahn, A., Santos-Sacchi, J. (Eds.), Physiology of the Ear, second

ed. Singular, San Diego, pp. 161e190.

Rougier, H., 2003. Etude descriptive et comparative de Biache-Saint-Vaast 1

(Biache-Saint-Vaast, Pas-de-Calais, France). These de Doctorate. Univer-

site Bordeaux 1.

Ruff, C., Trinkaus, E., Holliday, T., 1997. Body mass and encephalization in

Pleistocene Homo. Nature 387, 173e176.

Ruggero, M., Temchin, A., 2002. The roles of the external, middle and inner

ears in determining the bandwidth of hearing. Proc. Nat. Acad. Sci. U.S.A.

99, 13206e13210.

Sade, J., Berco, E., Buyanover, D., Brown, M., 1981. Ossicular damage in

chronic middle ear inflammation. Acta Otolaryngol. 92, 273e283.

Sarrat, R., Garcıa, A., Torres, A., 1988. Morphological variations of human

ossicula tympani. Acta Anat. 131, 146e149.

Sarrat, R., Torres, A., Guzman, A., Lostale, F., Whyte, J., 1992. Functional

structure of human auditory ossicles. Acta Anat. 144, 189e195.

Scheuer, L., Black, S., 2000. Developmental Juvenile Osteology. Academic

Press, San Diego.

Schultz, M., 1979. Diseases in the ear region in early and prehistoric popula-

tions. J. Hum. Evol. 8, 575e580.

Schwartz, J., Tattersall, I., 2003. The Human Fossil Record, Vol. 2. Craniodental

Morphology of Genus Homo (Africa and Asia). Wiley-Liss, New York.

Segall, W., 1943. The auditory region of arctoid carnivores. Field Mus. Nat.

Hist. Zoology Series 29, 33e59.

Segall, W., 1969. The auditory ossicles (malleus, incus) and their relationships

to the tympanic: in marsupials. Acta Anat. 73, 176e191.

Segall, W., 1970. Morphological parallelisms of the bulla and auditory ossicles

in some insectivores and marsupials. Fieldiana Zool. 51, 169e205.

Siori, M., Monchietto, M., Masali, M., 1995. Morphometrics of human auditory

ossicles from Antinoe Necropolis (Egypt). Int. J. Anthropol. 10, 29e36.

Spoor, F., 2002. The auditory ossicles. In: Zilh~ao, J., Trinkaus, E. (Eds.), Por-

trait of the Artist as a Child The Gravettian Human Skeleton from the

Abrigo do Lagar Velho and Its Archeological Context. Instituto Portugues

de Arqueologia, Lisbon, pp. 293e296.

Spoor, F., Stringer, C., Zonneveld, F., 1998. Rare temporal bone pathology of

the Singa calvaria from Sudan. Am. J. Phys. Anthropol. 107, 41e50.

Stuhlmann, O., 1937. The nonlinear transmission characteristics of the audi-

tory ossicles. J. Acoust. Soc. Am. 9, 119e128.

Tillier, A.M., 1999. Les Enfants Mousteriens de Qafzeh: Interpretation Phylo-

genetique et Paleoauxologique. CNRS Editions, Paris.

Valladas, H., Reyss, J.L., Joron, J., Valladas, G., Bar-Yosef, O.,

Vandermeersch, B., 1988. Thermoluminescence dating of Mousterian

‘‘Proto-Cro-Magnon’’ remains from Israel and the origin of modern

man. Nature 331, 614e616.

Wever, E., Lawrence, M., 1954. Physiological Acoustics. Princeton University

Press, Princeton, NJ.