Auditory ossicles from southwest Asian Mousterian sites

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Journal of Human Evolution 54 (2008) 414e433

Auditory ossicles from southwest Asian Mousterian sites Rolf Quam a,b,*, Yoel Rak c b

a Division of Anthropology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, USA Centro UCM-ISCIII de Investigacio´n sobre la Evolucio´n 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 in southwest Asia. Some methodological issues in the measurement of these bones are considered, and a set of standardized measurement protocols is proposed. Evidence of erosive pathological processes, most likely attributed to otitis media, is present on the ossicles of Qafzeh 12 and Amud 7 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 sample in some metric variables, but morphologically, the new specimens do not differ in any meaningful way from living humans. In most metric dimensions, the Amud 7 incus falls within our modern human range of variation, but the more closed angle between the short and long processes stands out. Morphologically, all the Neandertal incudi described to date show a very straight long process. Several tentative hypotheses can be suggested regarding the evolution of the ear ossicles in the genus Homo. First, the degree of metric and morphological variation seems greater among the fossil H. sapiens sample than in Neandertals. Second, there is a real difference in the size of the malleus between Neandertals and fossil H. sapiens, with Neandertals showing larger values in most dimensions. Third, the wider malleus head implies a larger articular facet in the Neandertals, and this also appears to be reflected in the larger (taller) incus articular facet. Fourth, there is limited evidence for a potential temporal trend toward reduction of the long process within the Neandertal lineage. Fifth, a combination of features in the malleus, incus, and stapes may indicate a slightly different relative positioning of either the tip of the incus long process or stapes footplate within the tympanic cavity in the Neandertal lineage. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Ossicle; Malleus; Incus; Neandertal; Qafzeh; Amud

Introduction Studies of the auditory ossicles in living humans have focused on anatomical, clinical, and auditory aspects (Helmholtz, 1873; Heron, 1923; Dahmann, 1929, 1930; Stuhlmann, 1937; Wever and Lawrence, 1954; Kirikae, 1960; Masali, 1964; Bouchet and Giraud, 1968; Arensburg and Nathan, 1971; Arensburg et 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: [email protected] (R. Quam), [email protected] (Y. Rak). 0047-2484/$ - see front matter Ó 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; Masali and Cremasco, 2006). In addition, the ossicles have proven to be useful phylogenetic indicators in other groups of primates (Masali and Chiarelli, 1965a,b; Hershkovitz, 1977) and other mammals (Segall, 1943, 1969, 1970). Fewer studies have been carried out on fossil human auditory ossicles, primarily due to their scarcity (Angel, 1972; Arensburg and Nathan, 1972; Rak and Clarke, 1979; Heim, 1982; Arensburg and Tillier, 1983), although the global sample size is increasing (Arensburg et al., 1996; Moggi-Cecchi and Collard, 2002; Spoor, 2002; de Ruiter et al., 2002; Lisonek and Trinkaus, 2006; Quam et al., 2006; Crevecoeur, 2007). Previous studies of late Pleistocene fossil human ear ossicles have led to conflicting interpretations of their evolutionary significance.

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Arensburg et al. (1981) have argued that the middle ear bones are taxonomically uninformative within the genus Homo, based on the strong similarity in metric dimensions of the ear ossicles across a wide range of modern human populations (Heron, 1923; Kirikae, 1960; Blumer et al., 1982; Mutaw, 1986) and their tight genetic control, being fully formed and adult-sized at birth (Scheuer and Black, 2000). Indeed, there appears to be little to differentiate the known late Pleistocene fossil H. sapiens specimens from their living counterparts (Arensburg and Nathan, 1972; Tillier, 1999; Spoor, 2002; Lisonek and Trinkaus, 2006; Crevecoeur, 2007). In contrast, Heim (1982) suggested that all three ear ossicles from the Neandertal infant La Ferrassie 3 showed subtle differences from those of living humans. The malleus was argued to show generally larger dimensions in total length and head size, as well as showing a somewhat more open angle between the head/neck and the manubrium. In addition, the manubrium was said to be straighter, lacking the curvature that generally characterizes H. sapiens. The incus was also said to be generally larger, showing a long process that is both longer and straighter than in living humans and an expanded articular facet. In contrast, the short process of the incus was said to be shorter, and the notch along the inferior margin of the short process, a feature that is variably present in living humans (Arensburg and Nathan, 1971; Mutaw, 1988), is absent in La Ferrassie 3. In addition, the long and short processes were said to form a more closed angle than is the case in modern humans. The stapes was said to be smaller and to show a marked asymmetry, with the anterior crus being shorter and straighter and the posterior crus longer and more curved. Given the subtle nature of these differences and the lack of additional Neandertal specimens at the time, it was unclear whether these anatomical variations identified in La Ferrassie 3 were simply a manifestation of normal biological variation or whether they represented derived traits within the Neandertal lineage. The subsequent discovery of several new Neandertal specimens has made it possible to assess these initial suggestions based solely on La Ferrassie 3. The incus is present within the temporal bone in the Le Moustier 1 adolescent Neandertal, and a 3D CT reconstruction of the specimen shows a very straight long process and a more closed angle between the long and short crurae (Ponce de Leo´n and Zollikofer, 1999; Spoor, 2002). The asymmetrical configuration of the Neandertal stapes has recently been identified in both the Subalyuk 2 and Le Moustier 2 specimens (Arensburg et al., 1996; Maureille, 2002). These recent discoveries have raised the possibility that, far from being taxonomically uninformative, the ear ossicles may be an underappreciated source of phylogenetic information within the genus Homo. The new specimens from Qafzeh and Amud reported here considerably augment the sample of these tiny bones known from southwestern Asia and include the first Neandertal specimen recovered from this region. This enlarged sample from Qafzeh (n ¼ 7) makes it possible to begin to assess the degree of intraspecific metrical and morphological variation at a single site and provides a useful comparison with the geologically

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younger late Pleistocene specimens from Europe and North Africa. In addition, comparison of the Amud 7 incus with the previously known European Neandertal specimens has the potential to provide further evidence for a Neandertal pattern of anatomical variation in the ear ossicles. Materials and methods The extremely small dimensions and peculiar morphology of the auditory ossicles complicates the collection and reliability of metrical data. Prior investigations into the dimensions of these bones have relied on a variety of techniques and measurement definitions (Heron, 1923; Kirikae, 1960; Bouchet and Giraud, 1968; Blumer et al., 1982; Mutaw, 1986; Siori et al., 1995). However, the two most influential studies that introduced standardized techniques and measurements for the ossicles are those of Masali (1964) and Arensburg et al. (1981). While both sets of measurements (Masali, 1964; Arensburg et al., 1981) are adequate for capturing the main ossicular dimensions, the definitions provided by Masali (1964) have been preferred in the present study for their more precise identification of the bony anatomical landmarks. Some of the measurements in the two studies are sufficiently similar, despite differences in orientation of the bone, to make them directly comparable. Nevertheless, a certain amount of confusion in the literature surrounding some of the measurement definitions necessitates a more detailed discussion of the consistency between studies, and the precise definitions used in the present work are detailed below. It is hoped that clarification of these methodological issues will prove useful for future studies of the auditory ossicles and avoid the inconsistencies in data collection and reporting that have characterized previous studies. Measurement definitions of Masali (1964) Masali (1964) was the first to suggest a series of standardized measurements and orientations of the ossicles, and these techniques have been adopted by subsequent researchers (e.g., Mutaw, 1986; Siori et al., 1995). He studied 40 mallei, 38 incudi, and 16 stapes using a projecting microscope at 10 magnification. For each ossicle, a series of axes were defined (two each for the malleus and incus and three for the stapes), with the majority of the measurements taken either perpendicular or parallel to the axes. While the orientations and measurement definitions are generally clearly understandable and reproducible, there are a few aspects in Masali’s (1964) original article that must be addressed. The base of the gracile (anterior) process is one of the anatomical points on the malleus used to define the X-axis (head/ neck axis). However, the variable presence and preservation of the gracile process in both the living hominoids, as well as the fossil specimens, makes this landmark difficult to use in practice. Thus, the present study has relied on the midpoint of the neck width (Fig. 1). Nevertheless, since the base of the gracile process (when present) is near the center of the neck width, these two landmarks are sufficiently similar to make the results directly comparable.

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The orientation of the incus is reported by Masali (1964) to be in ‘‘norma mediale,’’ with the medial face toward the observer. However, in the drawing of the incus demonstrating the orientation and measurement definitions, the bone is clearly oriented in ‘‘norma laterale,’’ with the lateral face toward the observer. In subsequent publications, the orientation of 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 on the drawing of the incus in the original Masali (1964) paper to establish that the measurements should indeed be taken in lateral orientation. The stated measurement definitions of length (X-axis) and breadth (Y-axis) of the incus (Masali, 1964) do not coincide with the axes labeled on the figure illustrating the measurements. Rather, the X- and Y-axes appear to be reversed in Fig. 1 of Masali (1964). The most recent article by Masali (Masali and Cremasco, 2006) has apparently corrected this earlier error, and the X- and Y-axes in the figure defining the measurements now coincide with the length (long process) and breadth (short process) of the incus. The present study has referred to the length of the long process as the X-axis and the short process as the Y-axis, following Masali and Cremasco (2006). The determination of the ‘‘functional length’’ in the incus requires further clarification. The functional length is important in assessing the physiological role of the incus in sound transmission from the environment to the inner ear, but has not been measured consistently in previous works and is particularly dependent on the orientation of the bone. Given the asymmetrical morphology of the articular facet, measurements taken in lateral view by Masali (1964; Masali and Chiarelli, 1965b) are significantly smaller than those taken in medial view (Masali et al., 1991, 1992). Related to this problem of orientation, the definition of one of the measurement points has varied between the lowermost point along the margin of the articular facet and the lateralmost (most anterior in anatomical position) point on the articular facet. This has the

effect of making measurements of the functional length taken in different studies incompatible. Due to these inconsistencies, the functional length of the incus has been measured differently in the present study (see below). Compatibility of measurements between studies For the malleus, measurements of the total length, manubrium length, and head width are directly comparable between the studies of Masali (1964) and Arensburg et al. (1981). In contrast, the method of measuring the angle of the malleus is clearly different and produces values that cannot be compared. In addition, Masali (1964) defined a few additional measurements for the malleus (manubrium arc depth and corpus length) that are not considered by Arensburg et al. (1981). For the incus, measurement of the long process length is directly comparable between the studies of Masali (1964) and Arensburg et al. (1981). However, as with the Masali (1964) article, there is an inconsistency between the definition of the breadth of the incus and the drawing presented in the Arensburg et al. (1981) paper. According to Arensburg et al. (1981), the total breadth of the incus is the same as the short process length. This is defined as the ‘‘maximum distance between the tip of the short process to the most protruding (inferior) border of the articular facet’’ (Arensburg et al., 1981: 203). However, the drawing of the incus indicates that this measurement is taken between the tip and the superior border of the incus. This has been a source of confusion for subsequent authors, as Blumer et al. (1982) used the inferior border as the proper landmark and Spoor (2002) used the superior border. Given this confusion, it is not clear that the measurement of short process length is comparable between the studies of Masali (1964) and Arensburg et al. (1981). The angle of the axes defined by Masali (1964) is not the same measurement as the angle of the incus defined by Arensburg et al. (1981), and the values from these two measurements cannot be directly compared. The angle of the incus (Arensburg et al., 1981) is one of the few metric variables that has been said to differ between Neandertals and living humans, with the former showing much more closed angles (Heim, 1982; Tillier, 1999; Spoor, 2002). The angle described is formed by the inferior edge of the short process and the posterior edge of the long process (Arensburg et al., 1981). However, in practice, these edges are rarely straight, but rather gently curve into one another, making the precise determination of the angle problematic. The angle between the axes (Masali, 1964) used in the present study is a different measurement, but is both clearly defined and can be measured consistently. In addition, Masali (1964) defined several additional measurements for the incus (arc depth of the long process, intercrural length, intercrural arc depth) that were not considered by Arensburg et al. (1981). Malleus measurements used in the present study

Fig. 1. Measurements of the malleus in the present study. The measurement numbers correspond with those listed in Table 1. Modified after Masali (1964).

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

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by Masali (1964). Nevertheless, some of the original measurement definitions have proven problematic in their application (see above), and additional measurements not defined in the original study have also been developed. Seven linear measurements, one angular measurement, and four indices were collected for the malleus. In addition, two axes were defined for the head/neck and the manubrium, respectively. Finally, the present study has measured the thickness of the manubrium at its midpoint (to establish a manubrium robusticity index) and the minimum width of the neck (to establish the head/neck axis for measuring the angle of the axes). The functional length of the malleus should be measured from the axis of rotation, experimentally determined in humans to pass through the base of the gracile process (Dahmann, 1929, 1930) to the tip of the manubrium. When in anatomical position, the length of the manubrium appears to approximately correspond to the functional length. The use of the malleus manubrium length, then, seems to be a reasonable estimate of the malleus functional length (lever arm length), particularly in isolated bones whose original position within the tympanic cavity is very difficult to establish. Thus, in the present study, the functional length of the malleus was taken as being equivalent to the manubrium length (Masali et al., 1991). Incus measurements used in the present study The measurement definitions for the incus have followed as closely as possible those of Masali (1964). Given the confusion surrounding the correct orientation of the incus, the lateral orientation was used systematically when measuring this bone. However, with the exception of the functional length, the orientation does not have a considerable influence on the values for any of the measurements. Seven linear measurements, one angular measurement, and one index were calculated for the

417

incus (Table 2; Fig. 2). In addition, the inconsistent measurement of the functional length in previous studies has lead to a different measurement definition in the present study. The most accurate measurement of the functional length is one that most closely approximates the distance between the tip of the long process and the axis of rotation of the malleus/incus complex in anatomical position within the tympanic cavity. This rotational axis has been the object of study since the nineteenth century (Helmholtz, 1873). The best estimate of functional 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 as the perpendicular distance to the tip of the long process from a line joining the tip of the short process and the most salient (i.e., anterior when in anatomical position) point along the articular facet. This measurement is similar, but not identical, to that of Masali (Masali et al., 1991, 1992) when taken with the incus oriented in medial view. Measurement technique Digital photographs were taken of the specimens and measured on a computer using the PhotoshopÔ software program. This technique is similar to that used by both Masali (1964) and Arensburg et al. (1981), and has the advantages of being portable, reproducible, relatively affordable, and compatible with previous studies. The ossicles were oriented according to the techniques of Masali (1964) (see above) and a 10-mm scale was placed next to the bone on the surface of the table. The malleus was positioned so that the manubrium was placed flat on the surface, while the incus was placed so that the long and short crurae were flat on the surface. Once the pictures were transferred to the computer, the images were calibrated, using the scale included in the photo, so that the measurements could be taken.

Table 1 Measurement protocol for the malleus1 No.

Definition

Description

Orientation

Bone is lying on its posterior aspect (with the articular facet away from the observer) and with the manubrium parallel to the plane of projection (i.e. flat on the surface). Defined by a line connecting the midpoint of the minimum neck width and the most salient point along the top of the head. This is a slightly different definition than that of Masali (see text). Defined by a line connecting the inferiormost points of the short process and the manubrium tip. Maximum distance from the tip of the manubrium to the top of the head. Distance from the tip of the short process to the manubrium tip, following the Y-axis. Mediolateral (M-L) thickness of the manubrium at mid manubrium length, taken perpendicular to the Y-axis. Maximum depth of the curvature of the arc of the manubrium, measured from the point of maximum depth to the Y-axis. Distance from the tip of the head to the lower border of the manubrium, taken following the X-axis. Maximum superoinferior (S-I) distance between two parallel lines marking the widest points of the margin of the head, taken perpendicular to the X-axis. Minimum distance between the anterior and posterior borders of the neck. Angle formed between the X- and Y-axes. (Manubrium length/total length)  100 (Manubrium M-L thickness/manubrium length)  100 (Manubrium length/corpus length)  100 (Corpus length/total length)  100

X-axis (head/neck axis)

1 2 3 4

Y-axis (manubrium axis) Total length Manubrium length Manubrium M-L thickness Arc depth of the manubrium

5 6

Corpus length S-I head width

7 8

Neck width Angle between the axes (M) Manubrium/length index Manubrium robusticity index Manubrium/corpus index Corpus/length index 1

Measurement numbers correspond to those shown in Fig. 1.

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418 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’’ Defined by a line joining the tip of the long process to the most salient point along the superior border of the body. 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. 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. 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. 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. Maximum height of the articular facet taken perpendicular to the Z-axis. Maximum distance from the tip of the long process to the Z-axis, taken perpendicular to the Z-axis. 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. 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. 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). Angle formed between the X- and Y-axes. (Short process length/long process length)  100

X-axis (long process axis) Y-axis (short process axis) Z-axis (rotational axis) 9

Short process length

10

Long process length

11 12 13

Articular facet height Functional length Arc depth of the long process

14

Intercrural length

15

Intercrural arc depth

16

Angle between the axes Crural index

1

Measurement numbers correspond to those shown in Fig. 2.

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

not project markedly off the table’s surface. Indeed, despite the wide variety of methods used in the past to measure these tiny anatomical structures, Arensburg et al. (1981) point out that the mean sizes of the ossicles among many previous studies 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 intraobserver error in the measurement of molar tooth cusp base areas using calibrated digital photographs. That study followed similar procedures and was subject to similar sources of error as in the present work, and found a maximum intraobserver error of 2.6% for any particular measurement. In the present study, intraobserver error in measuring the auditory ossicles from photographs was experimentally determined to be 2.5%, in close agreement with the results for measures of molar tooth cusp base areas (Bailey et al., 2004). Morphological features

Fig. 2. Measurements of the incus in the present study. The measurement numbers correspond with those listed in Table 2. Modified after Masali (1964).

The variation in a number of anatomical features was assessed in the fossil specimens and our modern human reference sample. Some of these features were mentioned previously as potentially showing interspecific patterns of variation reflecting taxonomic differences between Neandertals and modern humans. These include: the inflection of the tip of the malleus’ manubrium, the development of the short process of the manubrium, the presence of a groove on the anterior neck of the malleus, and a relatively straight long process in the incus (Arensburg and Nathan, 1972; Heim, 1982). Other features were seen to vary within modern humans, including: the presence of the gracile process in the malleus, the

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development of a depressed area on the medial aspect of the body of the incus, the contour of the superior border of the short process of the incus, and the presence of a notch in the inferior border of the incus’ short process (Arensburg and Nathan, 1971; Mutaw, 1988). Finally, one feature showed variation within the Qafzeh sample: morphology of the tip of the short process of the incus. Although the functional significance, if any, of many of these anatomical variants is not clear, the strong genetic component to the development of the ear ossicles, being fully formed and adult-sized at birth (Scheuer and Black, 2000), means that any consistent anatomical differences can be taken to largely reflect genetic differentiation between populations. Fossil specimens and comparative sample The new Qafzeh specimens were removed from the tympanic cavity and external auditory canal of Qafzeh 12 (right malleus and incus) and 15 (right malleus and incus) during study of the collection in 2005. Qafzeh 12 is a partial skeleton of a 3e4-year-old child, while Qafzeh 15 represents an older individual, between 8 and 10 years old at death. Both these individuals were found in a Mousterian context and represent early modern humans (Tillier, 1999). The fossils from this site have been dated to 90e100 ka (Valladas et al., 1988; Gru¨n and Stringer, 1991). The left incus was removed previously from the tympanic cavity of the Amud 7 specimen during cleaning of the adhering sediments. This is a partial skeleton of a 10-month-old infant recovered from a Mousterian context 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 ossicles from Qafzeh (Qafzeh 11 and 21) were also studied, as were the original fossil specimens from the site of Lagar Velho. In the case of both Qafzeh 12 and Qafzeh 15, 0.2 mm was added to the incomplete long process to estimate the original length. Regarding Qafzeh 21, damage to the specimen subsequent to its publication (Tillier, 1999), but prior to the present study, led to the loss of the lower half of the long process. Thus, measurements that rely on the long process being complete were taken on the published photograph of the specimen (Tillier, 1999). No attempt was made to estimate the missing portion of the incus’ long process in Lagar Velho. In addition, measurements were taken from the literature and on published scaled photographs for a number of Pleistocene specimens, 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 (Crevecoeur, 2007). Nevertheless, given the inconsistencies in measurement definitions discussed above and the preservation characteristics of fossil specimens, a few comments are warranted. To ensure the reliability of the comparative analysis, careful consideration was given to the selection of the measurements from the literature to assure their compatibility with those defined in the present study.

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A few measurements have been reported for the late middle Pleistocene specimen Biache-Saint-Vaast 1 (Rougier, 2003; Lisonek and Trinkaus, 2006; Crevecoeur, 2007). The remains from this site show clear affinities with late Pleistocene Neandertals (Rougier, 2003), and they form part of the Neandertal evolutionary lineage. For the malleus, the present study relied on the published measurements of total length, manubrium length, head width, corpus length, and angle between the axes while for the incus, only long process length and intercrural length are available (Lisonek and Trinkaus, 2006; Crevecoeur, 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 measurement should be considered tentative in this specimen. The maximum length of the malleus in the La Ferrassie 3 Neandertal specimen was reported as 8.3 mm by Heim (1982). However, several recent studies have suggested that this 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 scaled photo (Heim, 1982), and these values were used in the present study. In addition, both Masali et al. (1991) and Crevecoeur (2007) reported an identical value (6.0 mm) for the corpus length. Finally, the angle of the axes of the malleus was measured on the scaled published photo (Heim, 1982). For the La Ferrassie 3 incus, the published value for long process length (7.2 mm) was used (Heim, 1982). The remaining variables were measured on the published scaled photograph. The only measurement available for the Le Moustier 1 incus that is compatible with the measurements in the present study is the long process length (Ponce de Leo´n and Zollikofer, 1999). No attempt was made to measure other variables on the published image of the specimen since it is not clear that the orientation of the specimen allows for reliable data collection. The ear ossicles from the Darra-i-Kur specimen are of particular relevance for comparative purposes in the present study since they were also found in a southwest Asian Mousterian context and were recovered from a temporal bone that reportedly shows modern human affinities (Angel, 1972). Only a few preliminary measurements were published for these specimens, 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 three of these measurements are compatible between the studies of Masali (1964) and Arensburg et al. (1981). For the incus, the intercrural length and articular facet height in Darra-iKur can be compared with the values in the present study. Some data are available on Upper Paleolithic modern humans. For the Nazlet Khater 2 specimen, in addition to the published values (Crevecoeur, 2007), the manubrium thickness and arc depth, neck width, and angle between the axes were measured in the scaled published photograph in lateral view. Measurements and photos of the Dolni Vestonice ear ossicles were also published recently (Lisonek, 1992; Lisonek and Trinkaus, 2006). For the malleus, the published values were used for the total length, manubrium length, and head width,

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while for the incus the long process length and intercrural length were used. The remaining measurements in these bones were measured on the published photos in lateral orientation (Lisonek and Trinkaus, 2006). In order to estimate the normal range of biological variation that can be expected to characterize any living population, a modern human sample (n ¼ 43) of ear ossicles was drawn from a large collection removed during cadaver dissection in gross anatomy instruction at the New York Chiropractic College in Seneca Falls, New York (USA). This sample comprises individuals of known sex and race ranging in age from 51 to 100 years old. The individuals included in the present study were selected based on preservation criteria, the absence of any obvious pathological conditions, and the presence of more than one ossicle in order to facilitate comparison between ossicles in the same individual. Anatomical descriptions The new specimens reported here consist of the right mallei and incudi from the early modern human specimens Qafzeh 12 and Qafzeh 15 and the left incus from the Amud 7 Neandertal infant. These specimens considerably augment the sample of these tiny bones known from southwestern Asia and include the first Neandertal specimen recovered from this region. Qafzeh 12 (right malleus) (Fig. 3) This specimen, along with the incus, was recovered from the matrix filling the mastoid antrum of Qafzeh 12. The specimen is dark brown in color and has concretions adhering to most of it, including the top of the head, the articular facet, and tip of the manubrium. After cleaning, the specimen still retains some concretion on the anterior side of the manubrium’s tip, but this does not affect the reliability of measurements. There is a pronounced crack present along the base of the manubrium just posterior to the mid manubrium point, but measurements of this specimen are unaffected. The specimen appears quite small overall but is complete, and the basal portion of an ossified gracile process projects anteriorly. The superior border of the articular facet is separated

from the head of the malleus by a shallow groove. Viewed from above, the head shows a flattening in the anteroposterior direction, as in living humans, such that the maximum anteroposterior width (1.74 mm) is considerably smaller than the maximum inferosuperior width (2.70 mm). A pronounced crest extends from the superior border of the neck and wraps around the anterior aspect. The manubrium of the malleus is gently concave, with a well-developed short process. There is no tubercle marking the insertion of the tensor tympani muscle. Qafzeh 12 (right incus) (Fig. 4) This specimen shows the same coloring as the associated malleus. The specimen is nearly complete, missing only a small portion of the tip of the long process. To estimate the original length, 0.2 mm has been added to the measurements of the preserved long process. The tip appears to have been broken off, rather than eroded by any pathological process, such as otitis media, during the lifetime of the individual. The margins of the break are relatively smooth, but this could easily be a product of taphonomic factors. A deep crack is also present along the entire length of the anterior border of the long process. Like the associated malleus, the Qafzeh 12 incus also shows small overall dimensions. Both the superior border of the short process and the anterior border of the long process are gently concave. A clear notch is present along the lower margin of the short process, which terminates in a bulbous tip. The medial aspect of the body shows a deeply excavated area, 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 external auditory canal of Qafzeh 15. During the removal process, the tip of the manubrium was broken. However, the clean nature of the break allowed for the reliable reattachment of the tip, and measurements are unaffected. After cleaning and restoration of the specimen, a heavy sandy/salty concretion remains on the distal portion of the manubrium, toward the tip. Further preparation of the specimen runs the risk of

Fig. 3. The Qafzeh 12 right malleus. Scale bar ¼ 1 cm.

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Fig. 4. The Qafzeh 12 right incus. Scale bar ¼ 1 cm.

damage, given the fragility of the bone, but the measurements are unaffected. This specimen shows the same brown/caramel coloring as the Qafzeh 15 incus, but the head and neck are also covered by numerous black stains. There is no evidence of any pathology in the form of pockmarks or pitting on the surface of the bone. The specimen is complete, and the base of a gracile process projects anteriorly. There is a well-developed crest on the superior aspect of the neck that extends onto the anterior aspect as well. The superior border of the articular facet is separated from the head of the malleus by a deep groove. The head again shows a smaller anteroposterior width (1.47 mm) than the inferosuperior width (2.58 mm). The manubrium is gently concave and shows a well-developed short process, but no tubercle for the tensor tympani muscular insertion is present. Qafzeh 15 (right incus) (Fig. 6) This specimen was recovered from the aditus to the mastoid antrum, just superior to the tympanic cavity in Qafzeh 15. The specimen was coated with a patchy, black concretion of salt and sand, especially on the lateral surface, while the medial surface showed an ashy white color. After cleaning and restoration, the concretions were removed and the specimen is

421

brown/carmel in color with numerous black stains over the surface area. The specimen is nearly complete. The long process is missing the lenticular process, but on the lateral aspect, the tip begins to curve medially, indicating that it is very nearly complete. Thus, as with the Qafzeh 12 incus, 0.2 mm was added to the measurements of the preserved long process to approximate the original length. Slight abrasion/erosion is visible on the anterior aspect of the lower border of the articular facet. Some small pockmarks (pits) are present on the short process and body, but it is not clear that these represent bony lesions due to otitis media. A very deeply excavated area on the medial aspect of the body combined with the medial projection of the articular facet produces a very thin, projecting medial border for the articular facet. A notch is present along the lower margin of the rather pointed short process of this specimen and the body seems considerably narrower. The superior margin of the short process is mainly straight, but shows a concave bulge toward the tip. In contrast, the anterior margin of the long process is gently concave. Amud 7 (left incus) (Fig. 7) This specimen was removed from the tympanic cavity during cleaning of the specimen and is brown/tan in color. The specimen is missing the lenticular process but is otherwise complete and the measurements of the long process are accurate. The excavated area on the medial aspect of body is extremely deep and takes the form of a well-defined triangle with its sides represented by the articular facet, the short process, and the intercrural arc. A well-defined notch is also visible along the lower border of the short process, which terminates in a bulbous tip. The superior border of the short process is gently concave, while the anterior border of the long process is markedly straight. Paleopathology Middle ear pathology, frequently involving the ear ossicles, has been reported previously in archaeological skeletal

Fig. 5. The Qafzeh 15 right malleus. Scale bar ¼ 1 cm.

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Fig. 6. The Qafzeh 15 right incus. Scale bar ¼ 1 cm.

material (Arensburg et al., 2005). Ossification of the head of the malleus with the roof of the tympanic cavity (Arensburg et al., 1977) and fixation of the stapedial footplate within the oval window (Birkby and Gregg, 1975) are complications that can arise from otosclerosis (Davis, 1987). This disease process is rare in individuals younger than about ten years of age (Linthicum, 1993), and the individuals in both the studies cited above were between 40 and 50 years old at death. A second class of pathology is manifested by bony lesions on the surface of the ossicles and/or erosion of the tips of the malleus’ manubrium, the long process of the incus, or the stapedial head (Lisonek et al., 1986; Bruintjes, 1990). These lesions are generally attributed to inflammatory processes, inclulding otitis media, and can also involve the walls of the tympanic cavity and the mastoid process (Schultz, 1979). In living humans, chronic otitis media is most prevalent among children (Daniel et al., 1988) and is reflected in bony lesions

of the ossicles in approximately 25% of clinical cases (Sade et al., 1981). Among fossil H. sapiens, the tip of the long process in the Dolni Vestonice 14 incus is said to show damage due to an inflammatory condition during the lifetime of the individual (Lisonek and Trinkaus, 2006). In addition, the Dolni Vestonice 15 incus also shows conspicuous pitting of the surface on the lateral aspect of the body, and the malleus from this side appears severely deformed. In contrast, there is no evidence of pathology in the ossicles of Qafzeh 21, Lagar Velho, or Nazlet Khater 2 (Crevecoeur, 2007). The Qafzeh 11 malleus and incus were also previously reported to have been affected by otitis media, causing the erosion of the tips of the manubrium in the malleus and the long process in the incus (Arensburg and Nathan, 1972). However, our examination of the original fossil specimens does not support this contention. There is no sign of porosity anywhere

Fig. 7. The Amud 7 left incus. Scale bar ¼ 1 cm.

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on the bony surface of either specimen, including near the preserved distal ends of either the manubrium of the malleus or the long process of the incus. In addition, the transverse nature of the breaks on both bones, being both clean and perpendicular to the long axes of the manubrium of the malleus and the long process of the incus, suggest that the bone was not eaten away by a pathological process. Rather, it is more reasonable to invoke taphonomic factors to explain the damage to both specimens. Among the new Qafzeh specimens, the malleus of Qafzeh 15 shows no signs of pathology, while some small pockmarks (pits) are present on the short process and body of the Qafzeh 15 incus. It is often difficult to distinguish between lesions that have a pathological origin and those caused by post mortem taphonomic factors, and it is not clear whether the pockmarks present in Qafzeh 15 represent bony lesions due to otitis media or may simply be due to taphonomic factors. In contrast, the posterior aspect of the manubrium of Qafzeh 12 shows several deep pits that do seem consistent with otitis media, but the manubrium’s tip is complete and unaffected. In addition, the short process of the incus also shows some pockmarks/pits that are consistent with otitis media, although the anatomical details of the specimen are not affected. While the tip of the long process of the incus is missing, it appears to have been broken off rather than eroded. Thus, this case of otitis media was severe enough to affect the bony surface of the ossicles, but not so severe that it significantly altered the morphology of the ossicles. Although the presence of a depressed area on the medial aspect of the body of the incus is normal in modern humans, the marked degree of expression in Amud 7 suggests that it may be pathological in this individual. Pitting is also visible in this area, as well as just inferiorly toward the long process. Pock-marks are present along the superior aspect of the body and short process. Those toward the tip of the short process are larger and the surrounding bone appears to be damaged here. Those on the body are smaller and more well defined. The presence of these pockmarks in Amud 7 appears to be due to an erosive pathological process, such as otitis media. Amud 7 would not be the only Neandertal specimen to show middle ear pathology. Although none was reported for La Ferrassie 3 (Heim, 1982), the stapes of the Subalyuk 2 Neandertal shows the presence of a large tubercle just posterior to the head, and this has been interpreted as evidence of the ossification of the articular capsule surrounding the incudostapedial joint (Arensburg et al., 1996). The presence of bony lesions on the external surface of the mastoid process and temporal squama in the Krapina 1 juvenile Neandertal cranium has also been interpreted as evidence of otitis media (Minugh-Purvis et al., 2000). Thus, pathological processes affecting the middle ear structures have been reported in both modern human and Neandertal specimens and seem to be more common than those afflicting the inner ear (Spoor et al., 1998). Interestingly, the young ages at death for both the Amud 7 Neandertal (10 months; Rak et al., 1994) and the Qafzeh 12 early modern human (3e4 years; Tillier, 1999) indicate that otitis media was present in very young

423

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 those of living humans in their anatomical details. Specifically, they show a flattening of the head in the anteroposterior direction, a curved aspect to the manubrium, and a well-developed short process. In contrast, some variation can be seen in the presence of both the gracile process and a groove on the anterior neck. The taxonomic utility of variation in several of these anatomical discrete traits was further analyzed in a sample of middle and late Pleistocene specimens and within Holocene humans. Development of the short (lateral) process The short process of the malleus is a projection of the superior portion of the manubrium and marks the limit between the pars tensa and the pars flaccida within the tympanic membrane (Gray, 1977). All three Qafzeh mallei show a clear, projecting short process, as do the Nazlet Khater 2 and Dolni Vestonice 14 specimens (Table 3). In contrast, a projecting short process is missing from both the right and left mallei of Lagar Velho. Although the variation in this structure in living humans is considerable, with some specimens showing well-developed, projecting short processes and other specimens lacking them, most modern human specimens show some degree of development of the short process. Thus, the variation in the fossil H. sapiens sample is clearly encompassed by that seen in living humans. The short process in the Neandertal specimen La Ferrassie 3 is said to be larger and to imply a greater projection of this structure on the external face of the tympanic membrane (Heim, 1982). However, this tentative hypothesis can only be confirmed by the discovery of additional Neandertal mallei. Development of the gracile process The anterior ligament of the malleus inserts on the anterior surface of the neck, connecting the malleus with the anterior wall of the tympanic cavity. At the site of attachment of this ligament on the malleus, a slender bony projection, the gracile process, is often present. In our modern human reference sample, a gracile process is present in 64.0% of the individuals (Table 3). Among the fossil human specimens, this structure is commonly broken off at its base. Nevertheless, in most cases a small projection of bone is still preserved, indicating the presence of a gracile process and making it possible to score this anatomical trait. This structure has been identified in Lagar Velho, Nazlet Khater 2 (Crevecoeur, 2007), and Qafzeh 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 currently unknown.

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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 Qafzeh 11 Qafzeh 12 Qafzeh 15 Nazlet Khater 2 Dolni Vestonice 14 Lagar Velho 1 Lagar Velho 1 Modern humans

R L R R R L R L

Present Present Present Present Present Present Absent Absent Present

? Present Present Absent Present ? Present Present Absent ¼ 36% (n ¼ 27) Present ¼ 58.7% (n ¼ 44) Developed ¼ 5.3% (n ¼ 4)

Absent Present Absent Present? Present? ? Present Present Absent ¼ 53.5% (n ¼ 23) Present ¼ 46.5% (n ¼ 20)

Straight Lateral Lateral Straight Lateral Lateral Lateral Straight ¼ 33.8% (n ¼ 25) Lateral ¼ 66.2% (n ¼ 49)

Heim (1982) Original specimen Original specimen Original specimen Crevecoeur (2007) Lisonek and Trinkaus (2006) Original specimen Original specimen Present study

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

significance. Heim (1982) suggested that the lack of an inferior inflection of the manubrium tip in the La Ferrassie 3 Neandertal infant may be taxonomically relevant. However, the presence of a straight manubrium in the Nazlet Khater 2 individual and about one third of our modern human reference sample suggests that this anatomical variant does not follow taxonomic boundaries. Comparative morphology of the incus The morphological variation in the incus within the Qafzeh sample is somewhat greater than that of the malleus. This is particularly evident in the anatomical details of the short process, the curvature of the long process, and the depth of the excavated area on the medial aspect of the body. In contrast, the Neandertals seem to show less variation in their incus morphology.

Inflection of the manubrium tip Short process tip The tip (spatula) of the manubrium generally points laterally when in anatomical position in living humans. A laterally pointing manubrium tip is found in 66.2% of the recent human reference sample, while the remaining specimens (33.8%) were judged to show a straight manubrium with no inflection of 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 appears to be the Nazlet Khater 2 specimen, whose manubrium is said to be straight (Crevecoeur, 2007). The only data available for the Neandertals are from La Ferrassie 3, which also shows a straight manubrium (Heim, 1982). Since the manubrium is embedded in the fibers of the tympanic membrane and the tip of the manubrium marks the deepest point of curvature of the membrane, variation in the inflection of the manubrium’s tip may be related to the curvature of the membrane. However, both straight and inflected manubria are found in normal living human individuals, and this feature does not appear to have much functional

The short process in Qafzeh 21 is slender and gradually tapers to a well-defined point, differing from the other Qafzeh incudi. The short process in Qafzeh 15 is also pointed, but considerably larger, while Qafzeh 12 shows a small, bulbous tip and Qafzeh 11 shows a large and bulbous tip. Variation is also apparent between the two Dolni Vestonice incudi, with DV 14 showing a more extended short process, while that of DV 15 appears more truncated (Lisonek and Trinkaus, 2006). The short process in Lagar Velho is perhaps most similar to that in Qafzeh 15. The short process in Amud 7 shows a large, bulbous tip and, compared to the Qafzeh sample, is most similar to Qafzeh 11. Both the Le Moustier 1 (Ponce de Leon and Zollikofer, 1999) and La Ferrassie 3 (Heim, 1982) Neandertal specimens also show a bulbous tip, and, based on this small sample, this morphology appears to be more frequent in this group of hominins. Nevertheless, the range of variation in modern humans is, again, quite large and easily encompasses that expressed by the fossil specimens.

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Contour of the superior border of the short process

425

The superior border of the short process is normally straight or concave in living humans. Among our recent human comparative sample, 48 of 75 individuals (64.0%) were judged as showing a straight contour to the superior border of the short process, while a concave contour is seen in 26 individuals (34.7%) and a convex curvature was recorded in only one (1.3%) specimen (Table 4). Within the Qafzeh sample, a concave curvature is seen in both Qafzeh 11 and 12, while both Qafzeh 15 and 21 show a straight contour. The two Dolni Vestonice specimens also show variation in this feature, with DV 14 having a concave contour and that of DV 15 being convex. Finally, Lagar Velho is straight. Thus, the straight and concave contours occur in equal frequencies within the fossil H. sapiens sample, with one individual showing a convex curvature, the least common anatomical variant in living humans. In contrast to this variation, a concave curvature is seen in all three Neandertal specimens (Amud 7, La Ferrassie 3 [Heim, 1982], and Le Moustier 1 [Ponce de Leo´n and Zollikofer, 1999]).

10.8% of our modern human comparative sample (Table 4), a relatively low frequency of occurrence. Among the Neandertals, a pronounced notch is present in both Le Moustier 1 (Ponce de Leo´n 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 individuals from Qafzeh. Again, some variation is present, with both Qafzeh 11 and 12 showing well-developed notches, followed by Qafzeh 15 and Qafzeh 21, which shows the weakest expression. In contrast, no trace of a notch is present in either Darra-i-Kur or the Upper Paleolithic specimen from Lagar Velho. Although no notch is mentioned in the description of the Dolni Vestonice specimens (Lisonek and Trinkaus, 2006), DV 14 does appear to show a notch in the lower border of the short process. Thus, there is variation in this feature in Neandertals well as modern humans. Nevertheless, both the developmental component of this trait (related to the posterior incudal ligament) and the significant variation in its expression in those taxa that exhibit a notch suggest caution in attributing an evolutionary interpretation to this anatomical variant.

Presence of a notch in the short process

Depressed area on the medial body

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

The medial aspect of the body of the incus commonly shows a depressed area just posterior to the articular facet. The degree of expression of this feature varies in our modern human comparative sample from absent (13.3%) to present (70.7%) to deep (16.0%) (Table 4). All four of the Qafzeh specimens show this depressed area, although, again, there is some variation. Qafzeh 15 shows the deepest depression, followed by Qafzeh 12, while Qafzeh 11 and 21 are somewhat shallower and about the same. This depressed area is also clearly present in Lagar Velho and Dolni Vestonice 15 (Lisonek and Trinkaus, 2006). Thus, it is a ubiquitous feature within the fossil H. sapiens

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

Depressed area on medial aspect of body

Curvature of anterior border of long process

Reference

La Ferrassie 3 Le Moustier 1

R L

Concave Concave

Absent Present

? ?

Straight Straight

Amud 7 Darra-i-Kur Qafzeh 11 Qafzeh 12 Qafzeh 15 Qafzeh 21 Dolni Vestonice 14 Dolni Vestonice 15 Lagar Velho 1 Modern humans

L R L R R R L R R

Concave

Present Absent Present Present Present Present Present ? Absent Absent ¼ 89.2% (n ¼ 66) Present ¼ 10.8% (n ¼ 8)

Deep

Straight

Present Deep Deep Present ? Present Present Absent ¼ 13.3% (n ¼ 10) Present ¼ 70.7% (n ¼ 53) Deep ¼ 16.0% (n ¼ 12)

Straight Curved Curved Curved Curved Straight Curved Straight ¼ 23.3% (n ¼ 10) Concave ¼ 76.7% (n ¼ 33)

Heim (1982) Ponce de Leo´n and Zollikofer (1999) Original specimen Angel (1972) Original specimen Original specimen Original specimen Original specimen Lisonek and Trinkaus (2006) Lisonek and Trinkaus (2006) Original specimen Present study

Concave Concave Straight Straight Concave Convex Straight Straight ¼ 64.0% (n ¼ 48) Concave ¼ 34.7% (n ¼ 26) Convex ¼ 1.3% (n ¼ 1)

426

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sample. It is also present in Amud 7, where it is very deep and possibly pathological. Unfortunately, it is currently not clear whether La Ferrassie 3 or Le Moustier 1 show this depressed area. Curvature of the long process In lateral view, the anterior surface of the long process in living humans normally shows a gently or markedly concave curvature (Fig. 8). This curvature is accentuated distally by the lenticular process, which joins the tip of the long process with the head of the stapes. However, the body of the long process itself also generally shows this curvature. Among our modern human comparative sample, 23.3% of the individuals showed what was judged to be a relatively straight long process, while the remainder showed a concave curvature (Table 4). The incus in Neandertals has been said to be characterized by a relatively straight long process, which differs from the more 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 process with very little anterior curvature (Heim, 1982; Ponce de Leo´n and Zollikofer, 1999). Among our modern human comparative sample, 16.3% of the individuals (7 of 43 specimens) show a long process as straight as that seen in Amud 7. Within the Qafzeh sample, Qafzeh 11 shows a straight long process (Fig. 8), almost as straight as in Amud 7. The curvature

is more pronounced in Qafzeh 21, while both Qafzeh 12 and Qafzeh 15 (Fig. 8) show the clearest curvatures. The incus in the Lager Velho 1 individual is missing the tip of the long process. Nevertheless, it is clear that this specimen shows a curvature similar to that in the majority of living humans. Among the Dolni Vestonice specimens, DV 14 shows a clearly curved long process, while that of DV 15 is somewhat straighter (Lisonek and Trinkaus, 2006). Thus, the straight long process of Neandertals is a feature that can be found among both living and fossil H. sapiens, but it is present in 100% of the, admittedly small, Neandertal sample. The functional implications of the straight long process in Neandertals are not currently clear, but it may be related to a different placement of either the tip of the long process of the incus or the footplate of the stapes within the tympanic cavity. Additional support for this hypothesis is found in the highly asymmetrical crurae (Heim, 1982; Arensburg et al., 1996) and anteriorly skewed head of the stapes in the Neandertals. Metric variation in the malleus The metrical assessment of the malleus includes seven linear variables and one angular variable. In our modern human reference sample, the total length of the malleus was moderately correlated with both corpus length (r ¼ 0.75) and manubrium length (r ¼ 0.68), suggesting that the variation in the total length of the malleus depends primarily on the lengths

Fig. 8. Variation in the long process of the incus among Pleistocene and recent humans. Although some variation is present, a concave curvature to the anterior border of the long process is the normal condition in both living and fossil H. sapiens. In contrast, all known Neandertal incudi, including Amud 7, show a very straight long process. Note also the more closed angle between the long and short processes in Amud 7 compared with the H. sapiens specimens. (A) Modern human, straight (NYC 061948; reversed); (B) modern human, concave (SF 4610); (C) Amud 7 (reversed); (D) Qafzeh 11 (reversed); (E) Qafzeh 12; (F) Qafzeh 15. Scale bar ¼ 1 cm.

16.57e25.62 (43) 65.18e76.35 (43) 74.12e93.48 (43) 53.13e65.69 (43) 116.5e145.7 (43) 0.80e1.36 (43) 2.03e2.79 (43) 4.96e6.69 (43) 0.05e0.64 (43) 4.22e5.59 (43) 7.43e9.31 (43)

See text for measurement sources. 1

137.4 139.9 138.1 132.1  6.2 0.86 0.88 0.86 0.99  0.13 0.25 0.19 0.26 0.33  0.15 0.81 0.81 0.92 1.00  0.09

5.50 5.67 5.42 5.83  0.35

0.33 0.28 0.27

4.02 4.48 4.67 4.60 4.36 4.38 4.50 4.94  0.31

1.10 1.00 0.90

5.39 5.21 5.30 5.43

2.70 2.70 2.50 2.41 2.62 2.44 2.55 2.50 2.26 2.33 2.45 2.43  0.17 6.40 6.00

L R R L R R R L R L Biache-Saint-Vaast 1 La Ferrassie 3 Darra-i-Kur Qafzeh 11 Qafzeh 12 Qafzeh 15 Nazlet Khater 2 Dolni Vestonice 14 Lagar Velho 1 Lagar Velho 1 Fossil H. sapiens mean Living humans Mean  s.d. Living humans Range (n)

w4.1 4.80 5.00

w8.8 9.00 8.30 >7.14 7.37 7.72 8.01 7.90 7.99 8.00 7.90 8.25  0.41

0.81e1.19 (43)

18.58 18.49 21.21 20.28  1.94 68.84 70.88 69.37 70.66  2.80 79.27 77.25 80.84 85.01  5.15

27.36 22.32 19.27 70.69 68.65 67.79 77.16 84.53 86.00

54.55 58.03 58.30 58.23 54.57 54.75 56.95 59.97  2.81 0.82 0.92 0.84 0.86

w140.0 138.0 137.0 136.4

w77.27 66.67 w64.06 80.00 w46.59 53.33 60.24 147.0

Corpus/ length index Manubrium/ corpus index Manubrium/ length index Angle between the axes (deg.) Neck width Head width Corpus length Arc depth Thickness

Manubrium

Length Side

Total length

427

Specimen/sample

Table 5 Malleus measurements1 (mm) in fossil and living humans

of these two structures. A similar correlation (r ¼ 0.67) was found between head width and total malleus length. The correlations were much lower between all other malleus variables. The total length of the malleus in all of the fossil H. sapiens specimens falls below the mean value for our modern human sample (except for Darra-i-Kur), and the two Qafzeh specimens represent the smallest individuals in the sample (Table 5). Although Qafzeh 12 (7.37 mm) falls below the lower limit of the modern human range in the present study, it is within the variation observed in other studies of living humans (Arensburg et al., 1981). The manubrium length, both absolute and relative to total malleus length, is similarly short and the mean values in the fossil H. sapiens sample are more than 1.0 s.d. below those of 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 of Lagar Velho. In contrast, the total length in the two Neandertal lineage specimens, Biache (w8.8 mm) and La Ferrassie 3 (9.0 mm), is very long, falling, respectively, 1.3 and 1.8 s.d. above the mean of our modern human sample (8.25 mm). The manubrium 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 short value in Qafzeh 12. If a longer manubrium is estimated, it would also have the effect of increasing the total length somewhat. Thus, both the manubrium length and total length in Biache may represent minimum values. The mean corpus length within the fossil H. sapiens specimens (5.42 mm) falls just over 1.0 s.d. below the mean for our extant human sample (5.83 mm), and the Qafzeh specimens are again the smallest individuals. The corpus lengths in the two Neandertal lineage specimens (6.00 and 6.40 mm) are considerably longer, although within our modern human range of variation. This is not surprising, given the correlation with total length mentioned above. Within living humans, increases in total malleus length are primarily a result of increases in the corpus length, and in our modern human comparative sample, the specimen with the longest corpus length also showed the longest total length. Nevertheless, when corpus length is compared with the total length, the resulting index in both Qafzeh specimens is within 1.0 s.d. of the mean value in our modern human comparative sample. Variation in this index in the two Neandertals brackets that of the fossil H. sapiens specimens. When the corpus length is compared with the manubrium length, all of the fossil specimens (except Nazlet Khater 2) fall below our modern human mean, but only Biache falls outside the range of variation. However, this may be an artifact of the short estimated length reconstructed for the incomplete manubrium in the Biache specimen.

Manubrium robusticity index

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The angle between the axes of the malleus in all of the fossil specimens is above the mean of our modern human comparative sample (132.1 ). This angle is quite similar in all the fossil H. sapiens specimens, and the Qafzeh individuals do not stand out within the sample. In contrast, the angle in both Biache (154 ) and the La Ferrassie 3 Neandertal (147 ) is considerably higher, falling above our modern human range of variation. Thus, there is evidence for a wider angle in the Neandertal lineage specimens. The mean head width among the fossil H. sapiens (2.45 mm) is nearly identical to our modern human mean value (2.43 mm), and Qafzeh 12 (2.62 mm) shows the largest head within the sample. Both Neandertal specimens show identical larger values (2.70 mm), suggesting a wider head characterized the malleus in the Neandertal lineage. In the remaining malleus variables (manubrium thickness, robusticity index, arc depth, and the width of the neck), the values in the fossil H. sapiens specimens are quite similar to those in living humans (Table 5). The one exception seems to be the high robusticity index of the manubrium in Qafzeh 12 (27.36), which falls well above our modern human range of variation (16.57e25.62) and suggests a short but thick manubrium in this specimen. Interestingly, the values for head width and neck width in Qafzeh 12 are also the largest within the fossil H. sapiens sample. These three dimensions suggest that Qafzeh 12, while showing small metric dimensions overall, is a robust ossicle. In contrast, Qafzeh 15 is slightly larger, but appears less robust. The comparative metric analysis of the malleus has revealed that the fossil H. sapiens sample is generally smaller than in living humans. Within the fossil H. sapiens sample, Qafzeh 12 and 15 represent the smallest individuals, extending the known range of variation for this sample. In contrast, the two Neandertal lineage specimens show larger dimensions in both total length and corpus length but not manubrium length. The results of the present study, then, support previous suggestions for a clear and consistent size difference between Neandertals and fossil H. sapiens individuals (Heim, 1982; Crevecoeur, 2007). In addition, a higher angle in the malleus has been previously suggested to represent a shared feature between the Neandertals and fossil H. sapiens (Spoor, 2002; Crevecoeur, 2007). However, the present study, using a different definition of the malleus angle, found a more modest difference between the fossil H. sapiens and living humans. In contrast, the Neandertal specimens continue to fall outside the range of variation in our extant human sample. Thus, rather than representing a shared feature between Neandertals and fossil H. sapiens individuals, the results of the present study suggest that a more open angle of the malleus characterizes only the Neandertal evolutionary lineage. Metric variation in the incus The metric assessment of the incus includes seven linear variables and one angular variable. In our modern human reference sample, the long process length is moderately correlated with

both intercrural length (r ¼ 0.80) and the functional length (r ¼ 0.78). The correlations were much lower between all other incus variables. The length of the short process in most of the fossil H. sapiens specimens falls below our modern human mean value (5.07 mm), but the range of variation in the fossil sample is very similar to that in living humans (Table 6). The two new Qafzeh specimens fall between the previously known individuals. Similarly, the two Neandertal specimens are unremarkable 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 modern human sample. Although the mean length of the long process in the fossil H. sapiens sample is below our modern human sample mean, the range of variation in the fossil sample (6.34e7.10 mm) is large. The Neandertal lineage specimens do seem to show longer long processes, with the value in Biache (7.50 mm) falling toward the upper limit of our modern human range. The crural index compares the short process (crus) with the long process (crus), and the values in all of the fossil specimens (except Dolni Vestonice 14) fall below our modern human mean (74.28). Contrary to previous suggestions (Ponce de Leon and Zollikofer, 1999), it is difficult to identify any consistent difference between the fossil H. sapiens and Neandertal specimens. The angle formed between the long and short processes is quite stable within the fossil H. sapiens specimens and similar to the mean 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 more similar 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 specimens (except Qafzeh 21) is larger than the mean value in our modern human comparative sample in the present study. Nevertheless, Kirikae (1960) reported a somewhat taller articular facet (3.26  0.05 mm) in his modern human sample. This is nearly identical to the fossil H. sapiens mean value, although the values in Darra-i-Kur (3.70 mm) and Qafzeh 11 (3.45 mm) continue to stand out. Both the Neandertal specimens are also fairly large (3.37e3.40 mm), suggesting that a slightly expanded incus articular facet characterizes this group of hominins. The functional length of the long process is a physiologically relevant variable for evaluating the contribution of the incus to the transmission of sound energy through the middle ear (Rosowski and Relkin, 2001). The functional lengths in the fossil H. sapiens individuals are all quite similar to the living human mean value, with the sole exception of Qafzeh 15, which falls just below the lower limit of our modern human range of variation (Table 6). The value in Amud 7 (4.08 mm) falls just above our modern human mean (4.01 mm), while that in La Ferrassie 3 (4.41 mm) is close to the upper limit of our modern human range of variation. Based on its correlation with the long crus length, variation in the functional length appears to explain about 60% of the variation in long crus length in living humans.

59.20e84.78 (41) 56.6e75.6 (41) 1.18e1.95 (41) 5.61e7.44 (41) 3.61e4.46 (42) 2

1

6.66 6.83  0.32

6.17e7.59 (43) 4.02e5.86 (41)

6.94 6.73 6.34 6.47 7.10 6.40

See text for measurement sources. 0.2 mm was added to the preserved long process length and related measures.

2.60e3.41 (42)

1.58 1.66  0.21 5.82 6.18  0.34

4.05 3.84 3.57 3.93 4.11 3.89 >3.23 3.90 4.01  0.22 0.30 0.43 0.35 0.44 0.56 0.35 0.26 0.38 0.56  0.14

0.25e0.80 (43)

71.32 74.28  4.90

73.1 69.8 73.2 70.3 77.5 64.1

52.4 62.0 61.7 61.7 67.3 62.6 w61.5 61.3 64.0  4.7 2.00 1.30 1.60 1.46 1.75 1.35

72.6 48.3 2.13

5.38 6.00 5.95 5.85 5.29 5.52 6.60 5.50 4.08

3.37 3.70 3.45 3.30 3.20 2.99 3.35 3.15 3.14 3.29 3.00  0.19 0.28

5.07 4.80 5.07 4.70 4.64 4.55 5.50 4.10 4.76 4.77 5.07  0.37

52.1 4.86

R L L R L R R R L R R

Arc depth

1.46 0.36

3.40

4.41

5.90 5.84

Length Arc depth Length

7.50 7.20 6.80 6.98

Functional length Articular facet height Long process

Short process length Side Specimen/sample

Table 6 Incus measurements1 (mm) in fossil and living humans

Biache-Saint-Vaast 1 La Ferrassie 3 Le Moustier 1 Amud 7 Darra-i-Kur Qafzeh 11 Qafzeh 122 Qafzeh 152 Qafzeh 21 Dolni Vestonice 14 Dolni Vestonice 15 Lagar Velho 1 Fossil H. sapiens mean Living humans Mean  s.d. Living humans Range (n)

Intercrural

Angle of the axes (deg.)

67.5

Crural index

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Thus, the long functional length in the Neandertals appears to explain the longer long process lengths in these two specimens. The values for the curvature (arc depth) of the long process are generally lower in both the fossil H. sapiens and Neandertals than in living humans, with only Dolni Vestonice 14 matching our modern human mean (0.56 mm). This means that the long process is generally straighter in the fossil specimens. The low values in the Neandertals are compatible with the suggestion that they show very straight long crurae. Nevertheless, the value in Qafzeh 11 (0.30 mm) is nearly identical to that in Amud 7 (0.28 mm), and there is some overlap in this measure between Neandertals and fossil H. sapiens. The intercrural length in the fossil H. sapiens sample is again small, with the exception of Dolni Vestonice 14, which falls below our modern human mean value (6.18 mm). Interestingly, all three of the Neandertal lineage specimens also show small intercrural lengths, with the value in Amud 7 (5.38 mm) being very similar to that in Qafzeh 15 (5.29 mm), the smallest fossil H. sapiens individual. Given the correlation between intercrural length and long process length mentioned above, the Neandertals might be expected to show wider intercrural lengths. However, the lower angle between the long and short processes in the Neandertals results in an absolutely short intercrural length. The intercrural arc depth does not seem to follow any consistent pattern. Large and small values are found in both the fossil H. sapiens and Neandertal specimens, and the values in Qafzeh 11 (2.00 mm) and Amud 7 (2.13 mm) fall above the upper limits of the range of variation in our modern human sample. The analysis of metric variation in the incus has shown the fossil H. sapiens specimens to be generally smaller than their living counterparts. Both Qafzeh 12 and 15 conform to this pattern, and in several dimensions, Qafzeh 15 extends the known range of variation within the fossil H. sapiens sample. The Amud 7 Neandertal incus shows a very low angle between the short and long processes, resembling the La Ferrassie 3 Neandertal specimen. These results confirm that Neandertals do indeed have lower angles, while the angle in modern humans is more open, although the differences are not as marked as suggested previously (Heim, 1982; Spoor, 2002; Tillier, 1999). In addition, the curvature (arc depth) of the long process in Amud 7 and La Ferrassie 3 is very low, confirming that Neandertals are characterized by very straight long processes (Heim, 1982). Interestingly, both the lower angle and the straighter long process in Neandertals may indicate a slightly different placement of either the oval window or tip of the long process within the tympanic cavity. However, Amud 7 is also metrically very close to Qafzeh 11 in nearly all dimensions, including the angle between the axes and the arc depth of the long crus. Thus, these are not uniquely derived features in Neandertals, although they do occur at a higher frequency among them. Two additional inferences can be drawn regarding the Neandertal incus from the available data. First, the Neandertals appear to show an expanded articular facet compared with living humans, a finding that parallels the larger head widths in

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the malleus. Second, there is a suggestion of a temporal trend within the Neandertal lineage toward reduction of the long process. The oldest specimen (Biache) has the longest long process, while the youngest (Le Moustier 1) has the shortest. Nevertheless, a larger sample size of both Neandertals and their middle Pleistocene precursors is clearly needed to confirm this. Metric variation in the malleus/incus complex The presence of both the malleus and incus in Qafzeh 12 and 15 makes it possible to investigate relationships between these bones within the same individual. Comparison of the total malleus length with the long process length of the incus is a good measure of the relative size of both bones. The resulting index in Qafzeh 12 (109.5) falls just outside the lower limit of our modern human range of variation and is very similar to the value in Dolni Vestonice 14 (111.3) (Table 7). The low values in these two specimens are a product mainly of a short malleus in Qafzeh 12 and a long long process in the Dolni Vestonice 14 incus. In contrast, the value in Qafzeh 15 (121.8) is nearly identical to our modern human mean value. Similarly, despite their absolutely long mallei, the two Neandertal lineage specimens fall easily within 1.0 s.d. of the mean value for our sample of modern humans (Table 7). When the malleus’ manubrium length is compared with the incus’ functional length, the resulting index is known as the lever ratio of the middle ear. This is an important variable in determining the physiological role of the ear ossicles in audition (Rosowski and Relkin, 2001). The precise measurement of the malleus and incus levers (i.e., functional lengths) has been a topic of research for over a century and a number of studies have reached different conclusions regarding the value of this anatomical transformer in the middle ear. Estimates of the 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 humans (Dahmann, 1929, 1930; Stuhlmann, 1937; Rosowski, 1994). The modern human lever ratio in the present study yields values (mean ¼ 123.4) that are similar to those reported

in other studies, notably Rosowski (1994) (mean ¼ 130), Stuhlmann (1937) (mean ¼ 127) and Dahmann (1929, 1930) (mean ¼ 131). The lever ratios in the fossil H. sapiens specimens show a wide range of variation (Table 7). The value in Qafzeh 12 (104.7) falls toward the lower limit of our modern human range, indicating that the malleus’ manubrium is only slightly longer than the functional length of the incus. In contrast, that of Qafzeh 15 (125.5) is slightly above our modern human mean value. Both the Dolni Vestonice 14 (111.9) and the La Ferrassie 3 Neandertal (108.8) fall in between the two Qafzeh individuals but are still low compared with modern humans. The combination of a longer manubrium of the malleus and shorter functional length of the incus results in a higher lever ratio, which is theoretically more efficient at transmitting sound energy through the middle ear (Coleman and Ross, 2004). However, other physical properties of the ossicles, such as their mass, density, and ligamentous attachments also influence sound transmission through the middle ear, making it 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 fossil humans should not be based primarily on the lever ratio or a simple model incorporating a limited number of anatomical measurements (Masali et al., 1991; Masali and Cremasco, 2006), as these have been shown to generate unreliable results in living humans (Rosowski and Relkin, 2001). Rather, a more precise approach to estimating the auditory capacities in fossil specimens requires a comprehensive model that takes into account the physical properties of the ear ossicles and the structures of the outer, middle, and inner ear (Ruggero and Temchin, 2002; Martı´nez et al., 2004). The articulation of the malleus and incus at the incudomalleolar joint implies a close functional relationship between the head of the malleus and the articular facet of the incus. The head width measured in the present study corresponds approximately to the size of the articular facet on the malleus, and this, in turn, is related to the height of the articular facet on the incus. However, the correlation between the malleus’ head width and articular facet height of the incus in our

Table 7 Measurements1 of the malleus/incus complex in fossil and living humans Specimen/sample Biache-Saint-Vaast 1 La Ferrassie 3 Darra-i-Kur Qafzeh 11 Qafzeh 122 Qafzeh 152 Dolni Vestonice 14 Lagar Velho 1 Living human mean  s.d. Living human range (n) 1 2 3

Malleus total length/ Incus long process length

Malleus/Incus lever ratio3

w117.3 125.0

108.8

109.5 121.8 111.3

104.7 125.5 111.9

120.83  5.56 111.24e130.95 (43)

See text for measurement sources. 0.2 mm was added to the preserved incus long process length and related measures. Lever ratio ¼ (manubrium length/incus functional length)  100.

123.4  8.5 101.9e138.9 (42)

Malleus head width/ Incus articular facet height 79.4 67.6 69.9 79.4 76.3 74.6 72.0 81.0  6.1 69.4e97.4 (42)

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modern human comparative sample is low (r ¼ 0.40). The Neandertal lineage specimens showed evidence for both a taller articular facet height on the incus and an expanded malleus’ head width. Comparison of these two dimensions suggests that living humans have a head width of the malleus that is approximately 80% of the height of the articular facet of the incus. Among the fossil specimens, the identical value (79.4%) in both Qafzeh 12 and La Ferrassie 3 is closest to our modern human mean, while the remaining fossil H. sapiens specimens have a lower index. The two fossil H. sapiens specimens with the tallest incus articular facets, Qafzeh 11 (3.45 mm) and Darra-i-Kur (3.70 mm), fall toward the very lower limit and outside of the living human range of variation, respectively. The comparison of selected variables between the malleus and incus in several fossil human specimens has revealed their fundamentally human pattern. The short malleus in Qafzeh 12 produces very low index values for both of the length ratios between the malleus and incus in this individual, but the articular facet index is very close to our modern human mean. This would suggest that the size of the articular facet is largely independent of malleus length. The Neandertal lineage specimens do not differ from living humans in any of the indices. Discussion and conclusion There are clear anatomical differences between the ear ossicles in the Neandertal and H. sapiens evolutionary lineages, and, contrary to previous assertions (Arensburg et al., 1981), these bones contain taxonomic information useful for separating species of the genus Homo. The Neandertal malleus can be said to differ from that of living humans in its larger dimensions, more open angle between the head/neck and the manubrium, and larger head size. Likewise, the Neandertal incus (including that of Amud 7) shows a straighter long process, a taller articular facet, and a more closed angle between the long and short processes. Although all of the anatomical variants considered in the present study can also be found in living humans, they occur at a higher frequency among Neandertals, sometimes reaching 100% frequency (e.g., the straight long process of the incus). These bones show a consistent anatomical pattern within the Neandertal lineage that sets them apart, both morphologically and metrically, from the majority of living humans. Neandertals, then, can be said to consistently express only a portion of the modern human range of variation. Given this limited degree of metrical and morphological overlap between Neandertals and modern humans, it is important to understand the range of variation expressed in the fossil H. sapiens sample. The new specimens from Qafzeh are particularly important in this regard since they considerably augment the current sample of fossil H. sapiens and predate the late Pleistocene specimens from Europe and North Africa. The fossil H. sapiens sample generally shows smaller dimensions in both the malleus and incus than their living counterparts in most metric variables, and the Qafzeh specimens are no exception. Within the Qafzeh sample, the malleus of Qafzeh 12 shows much smaller dimensions than either Qafzeh 15 or (where they can be compared) Qafzeh 11. The

431

exceptions include manubrium thickness, neck width, and head width. These three thickness dimensions suggest that the Qafzeh 12 malleus is a more ‘‘robust’’ ossicle than is Qafzeh 15. In contrast, the incus of Qafzeh 15 is generally smaller than that of Qafzeh 12, while Qafzeh 11 is the largest in most dimensions. Nevertheless, the metric variation within the Qafzeh sample is similar in degree to the differences observed between Dolni Vestonice 14 and 15. The new Qafzeh specimens do extend the known range of variation in the fossil H. sapiens sample in a number of metric dimensions in both the malleus and incus, and some measurements in the Qafzeh specimens fall outside the range of variation in our modern human comparative sample in the present study. However, it is not possible to identify any consistent metric or morphological differences between the Qafzeh sample and the geologically younger Upper Paleolithic specimens from Europe or North Africa. In both the malleus and incus, the variation within the temporally and geographically restricted Qafzeh sample is generally greater than that observed among the temporally and geographically diverse sample of Neandertal lineage specimens. The Qafzeh 11 incus stands out within the sample for having both a more closed angle between the long and short processes and a very straight long process; it resembles Neandertals in both these aspects. Indeed, the Qafzeh 11 incus is both metrically and morphologically very similar to that of Amud 7. However, the malleus in Qafzeh 11 lacks the elongated corpus length that is characteristic of Neandertals, and the cranial anatomy in this specimen is consistent with its attribution to H. sapiens (Tillier, 1999; Schwartz and Tattersall, 2003). Thus, despite the metric and morphological similarity between the Qafzeh 11 and Amud 7 incudi, there is no evidence among the auditory ossicles from Qafzeh for more than one species at this site. From the metric data, three tentative hypotheses regarding evolution of the ear ossicles in the genus Homo can be advanced. First, there appears to have been a real difference in the overall dimensions of the malleus between Neandertals and 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 generally larger body mass in Neandertals (Ruff et al., 1997), since across mammals, the size of the ossicles is generally correlated with body size (Rosowski, 1994). The larger malleus head width suggests a larger incudomalleolar joint, and this also appears to be reflected in the taller incus articular facet among the Neandertals. Second, contrary to previous suggestions (Lisonek and Trinkaus, 2006), there does appear to be limited evidence for a temporal trend among Neandertals in the reduction of the long process in the incus. The earliest specimen (Biache) shows the longest long process, while successively younger specimens show decreasing lengths of the long process. Clearly, a larger sample of Neandertal lineage specimens is needed to confirm this tentative suggestion. Third, there is evidence for a slightly different placement of either the tip of the incus long process or the oval window, for the insertion of the stapes footplate, within the tympanic cavity

432

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in the Neandertals. This suggestion is based on the higher angle between the head/neck and manubrium in the malleus, the lower angle between the long and short processes in the incus, and the straighter long process of the incus in Neandertals. In addition, the few Neandertal stapes that are known all show an anteriorly skewed stapedial head (Heim, 1982; Arensburg et al., 1996; Maureille, 2002). Interestingly, many of these features were mentioned by Heim (1982) as possible Neandertal distinctions present in the La Ferrassie 3 ear ossicles. Thus, Heim’s (1982) early suggestions of consistent differences between Neandertal and modern human auditory ossicles are largely borne out by subsequent discoveries. What is less clear is whether these anatomical differences represent derived features within the Neandertal lineage or primitive retentions common to archaic members of the genus Homo. The consistent differences identified between the malleus and incus in the Neandertal and H. sapiens lineages indicate that the auditory ossicles are an important source of phylogenetic information. Future discoveries of auditory ossicles from Neandertals, as well as geologically older and taxonomically diverse specimens, should aide in resolving some of the tentative hypotheses outlined in the present study. Given the strong genetic control that governs the development of the ear ossicles, analysis of the morphological and metric variation in these tiny anatomical structures promises to provide new insights into evolutionary processes in the genus Homo. Acknowledgements E. Trinkaus and C. Duarte kindly provided access to the Lagar Velho specimens. T. Greiner allowed for data collection on the sample of ear ossicles from the New York Chiropractic College in Seneca Falls, New York. B. Arensburg kindly provided access to the Subalyuk 2 stapes in his care. A.M. Tillier provided helpful comments on the final version of the manuscript. M.C. Ortega cleaned and prepared the new Qafzeh specimens. R. Quam was supported by a grant from the Fundacio´n Duques de Soria/Fundacio´n Atapuerca. This research was supported by the Ministerio de Ciencia y Tecnologı´a of the Government 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 moyenne d’un ne´andertalo€ıde trouve´s 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.

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