The bony labyrinth of the middle Pleistocene Sima de los Huesos hominins (Sierra de Atapuerca, Spain)

Journal of Human Evolution 90 (2016) 1e15

Contents lists available at ScienceDirect

Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol

The bony labyrinth of the middle Pleistocene Sima de los Huesos hominins (Sierra de Atapuerca, Spain)
llez b, g, Rolf Quam a, b, c, *, Carlos Lorenzo d, e, b, Ignacio Martínez b, f, Ana Gracia-Te Juan Luis Arsuaga b, h a

Department of Anthropology, Binghamton University (SUNY), Binghamton, NY 13902-6000, USA
n (UCM-ISCIII) sobre la Evolucio
n y Comportamiento Humanos, Avda. Monforte de Lemos 5, 28029 Madrid, Spain Centro de Investigacio Division of Anthropology, American Museum of Natural History, Central Park West at 79th St., New York, NY 10024, USA d ria, Facultat de Lletres, Universitat Rovira i Virgili, Avda. Catalunya 35, 43002 Tarragona, Spain Area de Prehisto e  de Paleoecologia Humana i Evolucio
Social, Campus Sescelades URV (Edifici W3), 43007, Spain IPHES, Institut Catala f

Campus Universitario, 28871 Alcala
de Henares, Spain Area de Antropología Física, Departamento de Ciencias de la Vida, Universidad de Alcala g

, Campus Universitario, 28871 Alcala
de Henares, Area de Paleontología, Departamento de Geología, Geografía y Medio Ambiente, Universidad de Alcala Spain h
gicas, Ciudad Universitaria s/n, 28040 Madrid, Spain Departamento de Paleontología, Universidad Complutense de Madrid, Facultad de Ciencias Geolo b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 4 April 2015 Accepted 10 September 2015 Available online xxx

We performed 3D virtual reconstructions based on CT scans to study the bony labyrinth morphology in 14 individuals from the large middle Pleistocene hominin sample from the site of the Sima de los Huesos (SH) in the Sierra de Atapuerca in northern Spain. The Atapuerca (SH) hominins represent early members of the Neandertal clade and provide an opportunity to compare the data with the later in time Neandertals, as well as Pleistocene and recent humans more broadly. The Atapuerca (SH) hominins do not differ from the Neandertals in any of the variables related to the absolute and relative sizes and shape of the semicircular canals. Indeed, the entire Neandertal clade seems to be characterized by a derived pattern of canal proportions, including a relatively small posterior canal and a relatively large lateral canal. In contrast, one of the most distinctive features observed in Neandertals, the low placement of the posterior canal (i.e., high sagittal labyrinthine index), is generally not present in the Atapuerca (SH) hominins. This low placement is considered a derived feature in Neandertals and is correlated with a more vertical orientation of the ampullar line (LSCm < APA), posterior surface of the petrous pyramid (LSCm > PPp), and third part of the facial canal (LSCm < FC3). Some variation is present within the Atapuerca (SH) sample, however, with a few individuals approaching the Neandertal condition more closely. In addition, the cochlear shape index in the Atapuerca (SH) hominins is low, indicating a reduction in the height of the cochlea. Although the phylogenetic polarity of this feature is less clear, the low shape index in the Atapuerca (SH) hominins may be a derived feature. Regardless, cochlear height subsequently increased in Neandertals. In contrast to previous suggestions, the expanded data in the present study indicate no difference across the genus Homo in the angle of inclination of the cochlear basal turn (COs < LSCm). Principal components analysis largely confirms these observations. While not fully resolved, the low placement of the posterior canal in Neandertals may be related to some combination of absolutely large brain size, a wide cranial base, and an archaic pattern of brain allometry. This more general explanation would not necessarily follow taxonomic lines, even though this morphology of the bony labyrinth occurs at high frequencies among Neandertals. While a functional interpretation of the relatively small vertical canals in the Neandertal clade remains elusive, the relative proportions of the semicircular canals is one of several derived Neandertal features in the Atapuerca (SH) crania. Examination of additional European middle Pleistocene specimens suggests that the full suite of Neandertal features in the bony labyrinth did not emerge in Europe until perhaps <200 kya. © 2015 Elsevier Ltd. All rights reserved.

Keywords: Semicircular canal Cochlea Neandertal Inner ear

* Corresponding author. E-mail address: [email protected] (R. Quam). http://dx.doi.org/10.1016/j.jhevol.2015.09.007 0047-2484/© 2015 Elsevier Ltd. All rights reserved.

2

R. Quam et al. / Journal of Human Evolution 90 (2016) 1e15

1. Introduction The inner ear serves dual physiological roles in sensory perception. The cochlea houses the organ of Corti, which is responsible for transforming the mechanical energy of sound waves into electrical signals that are sent via the auditory nerve to the brain, where they are perceived as sound (Robles and Ruggero, 2001). The semicircular canal system is responsible for the sense of balance and equilibrium during locomotion, and differences in the relative sizes of the canals have been linked with distinct locomotor repertoires across primates (Spoor and Zonneveld, 1998; Spoor et al., 2007; Silcox et al., 2009). Anthropological study of the primate bony labyrinth has become feasible within the last 30 years due to the advent and widespread application of medical imaging technology to the study of human fossils (Zonneveld and Wind, 1985). Indeed, the study of the bony labyrinth in fossil hominins was one of the first systematic approaches to addressing evolutionary questions relying on CT scans (Spoor, 1993), an analytical tool that has become commonplace in paleoanthropological studies today. The primate bony labyrinth has been studied across a wide range of fossil and extant taxa to provide insight into locomotor behavior and to assess the phylogenetic affinities in fossil hominin temporal bones (Spoor et al., 1994, 2007; Spoor and Zonneveld, 1998; Rook et al., 2004; Lebrun et al., 2010; Braga et al., 2013). Among fossil hominins, the bony labyrinth has been studied in the early hominin taxa Australopithecus and Paranthropus, and the anatomical features have been related to the emergence of bipedalism in the human lineage (Spoor et al., 1994; Spoor, 2003; Braga et al., 2013). The bony labyrinth has also been studied in diverse species of the genus Homo (Spoor, 1993; Hublin et al., 1996; Gilbert et al., 2008; Glantz et al., 2008; Bouchneb and
n and Crevecoeur, 2009; Gunz et al., 2009, 2013; Ponce De Leo
n and Zollikofer, 2010; Guipert et al., 2011; Ponce De Leo
mezZollikofer, 2013; Hill et al., 2014; Wu et al., 2014; Go Olivencia et al., 2015). These studies have revealed that the labyrinth in lower Pleistocene specimens from Africa and Asia is similar to recent Homo sapiens in absolute and relative dimensions, suggesting that modern humans show the primitive condition. In contrast, several morphological differences from H. sapiens have been identified in the Neandertal bony labyrinth (Hublin et al., 1996; Spoor et al., 2003) and appear to be derived features. Among these derived Neandertal features are absolutely and relatively smaller anterior and posterior canals. Larger dimensions in these vertical canals have been associated with an increased agility across primates (Spoor et al., 2007), and the smaller size of the canals in Neandertals have been hypothesized to indicate a decreased agility or differences in their angular head motions (Spoor et al., 2003). In contrast, the lateral (horizontal) canal is larger in Neandertals, and this may be related with their larger body mass. In addition to the sizes of the canals, the posterior canal in Neandertals is located in a relatively inferior position, particularly when compared to the plane of the lateral canal. This has been argued to be a consequence of a rotation of the cerebellum within the posterior cranial fossa associated with increased encephalization, and Neandertals have been characterized as “hyper-rotated.” The few European middle Pleistocene specimens studied to date share some features with Neandertals (Spoor et al., 2003). Given their earlier geological age, the large number of individuals represented, and their close evolutionary relationship with the Neandertals, an analysis of the bony labyrinth in the Atapuerca Sima de los Huesos (SH) hominins may help elucidate the pattern of emergence of these derived traits within the Neandertal clade (Lorenzo et al., 2011).

The human fossils recovered at the SH site are dated to c. 430 kya (Arsuaga et al., 2014) and represent some of the earliest specimens in the fossil record to show derived Neandertal features and are members of the Neandertal clade (Arsuaga et al., 1993, 1997, 2014; Martínez and Arsuaga, 1997). The SH human fossil sample includes a minimum of 17 crania in variable states of preservation (Arsuaga et al., 2014). Phylogenetic analysis of the temporal bones has indicated Neandertal affinities in the presence of a shallow glenoid fossa, as well as retention of some primitive features such as a large and projecting mastoid process (Martínez and Arsuaga, 1997; Martínez et al., 2008). A large sample of middle ear ossicles has also been recovered, and these show some features also seen in Neandertal specimens (Quam et al., 2006, 2013b). In addition, the auditory capacities of the Atapuerca (SH) hominins have been reconstructed as showing a modern-human-like auditory pattern (Martínez et al., 2004, 2013; Quam et al., 2012). Study of the ear structures then clearly has the potential to offer new insights into the phylogenetic relationships and paleobiology of fossil human taxa. 2. Materials and methods We studied the bony labyrinth in 14 individuals in the SH sample (Fig. 1). Given the early ontogenetic development of the inner ear, which is fully formed and has reached adult dimensions at birth (Scheuer and Black, 2000), both juvenile and adult specimens were included. The SH measurements were compared with published data on a taxonomically diverse array of fossil hominin specimens attributed to the genus Homo (Table 1). In addition, we collected data on 26 recent H. sapiens individuals. This sample is
(Burgos, Spain; composed of crania from the Cementerio San Jose n ¼ 7), the Sepúlveda medieval site (Segovia, Spain; n ¼ 8), the American Museum of Natural History (New York, USA; n ¼ 4), and the NESPOS internet platform (www.nespos.org; n ¼ 7). Although different CT scanners have been used for this comparative data, all the images were obtained with a slice increment between 0.2 and 0.5 mm and pixel size ranging from 0.109 to 0.220 mm (see Supplementary Online Material [SOM] Appendix A). Most of the SH individuals were scanned at the Universidad de Burgos (Spain) using a YXLON Compact (YXLON International XRay) industrial multislice computed tomography (CT) scanner. Slices were obtained as a 1024  1024 matrix of 32-bit Float format and with a pixel size ranging from 0.161 to 0.217 mm (SOM Appendix A). This is approximately double the resolution of standard medical CT scanners. Virtual 3D reconstructions and measurements of the bony labyrinth were made using the Mimics™ software program. We relied on the half maximum height (HMH) thresholding protocol to delimit the bone/air interface. Thresholding was based on the Hounsfield units (gray values), and the boundary of bone and air was determined as the mean of the first maximum and minimum gray scale values along a profile line crossing the bone/air boundary. Within the SH sample, most individuals preserved all of the relevant measurements. However, it was not possible to measure some of the cochlear variables in Cr. 5 and Cr. 17. In addition, Cr. 14 shows pathological deformities (Gracia et al., 2009), which have resulted in pronounced asymmetry of the cranial base. The left glenoid fossa is displaced 4.4 mm inferior to and 10.1 mm anterior to the right side. Nevertheless, the brain size (1224 cm3; Arsuaga et al., 2014) is very close to the sample mean, and most of the dimensions of the bony labyrinth appear unaffected since they fall within the range of variation of other individuals in the Atapuerca (SH) sample. Only the value for the inclination of the cochlea (COs < LSCm; 36.6) represents the extreme of the Atapuerca (SH) sample variation. Indeed, this represents the lowest value of any

R. Quam et al. / Journal of Human Evolution 90 (2016) 1e15

3

Figure 1. Virtual reconstructions of the Atapuerca (SH) bony labyrinths in (from left to right) superior, anterolateral, lateral, and posteromedial views.

individual included in our study. Nevertheless, inclusion of this measurement does not alter our conclusions regarding this variable in the Atapuerca (SH) sample. 2.1. Measurement definitions and protocol The measurement definitions and protocol followed those outlined in previous studies (Spoor, 1993; Spoor and Zonneveld, 1995, 1998) and consist mainly of linear and angular measures of the

semicircular canals and cochlea and their relationship to one another, the sagittal plane, the posterior petrosal surface, and the facial canal (Fig. 2). Linear measurements of the canals and basal turn of the cochlea mainly related to their diameters, from which the shape index and radius of curvature was calculated. The relative size of each canal was determined by summing the radii of all three canals and dividing by the radius of the individual canals. For the angular relationships, the labyrinths were oriented so that the plane of the lateral canal was horizontal. The angles of the cochlear

Table 1 Fossil and recent hominin samples used in the present study. Taxon/Group

n

Lower/Middle Pleistocene Africa þ Asia Atapuerca (SH)a Non-SH Middle Pleistocene Europe Neandertals

7

Specimens

Source

SK 847, OH 9, Daka, Sangiran 2, 4, Lantian 1, Hexian 1

Spoor (1993), Gilbert et al. (2008), Wu et al. (2014)

14 4

Cranium 3, 4, 5, 6, 7, 8, 9, 11, 12, 13, 14, 15, 17, AT-1907 Abri Suard, Reilingen, Steinheim, Biache-Saint-Vaast 2

Present Study Spoor et al. (2003), Guipert et al. (2011)

27

Arcy-sur-Cure, Dederiyeh 93002, Gibraltar 1, 2,

Xujiayao Fossil H. sapiens

1 11

La Chapelle-aux-Saints, La Ferrassie 1, 2, 3, 8,
, La Quina H5, H27, Le Moustier 1, Pech de l'Aze Petit Puymoyen 5, Spy 1, 2, Tabun 1, Obi-Rakhmat 1, Krapina 38.1, 38.12, 38.13, 39.1, 39.4, 39.8, 39.13, 39.18, 39.20 Xujiayao 15 Oase 2, Muierii 2, Abri Pataud 1, 3, Cro-Magnon 1, Laugerie Basse 1,

Hublin et al. (1996), Spoor et al. (2003), Glantz et al. (2008), Hill et al. (2014)
mez-Olivencia et al. (2015) Go

Recent H. sapiens

26

Lagar Velho, Nazlet Khater 2, Qafzeh 6, Skhul 5, Liujiang 1
(7), Sepúlveda (8), AMNH (4), NESPOS (7) Cementerio San Jose

a

Wu et al. (2014) Spoor et al. (2002, 2003), Bouchneb and Crevecoeur (2009), Wu et al. (2014)
n and Zollikofer (2010, 2013) Ponce De Leo Present Study

Details of specimen numbers of the temporal bones associated with the SH crania, as well as their corresponding dental individuals, are provided in Arsuaga et al. (2014).

4

R. Quam et al. / Journal of Human Evolution 90 (2016) 1e15

Figure 2. Superior (a) and lateral (b) aspects of a left human labyrinth, and lateral aspect (c) with the petrosal contour included showing the measurements and orientations used in the study. Abbreviations: ASCh ¼ height of the anterior semicircular canal; ASCw ¼ width of the anterior semicircular canal; LSCh ¼ height of the lateral semicircular canal; LSCw ¼ width of the lateral semicircular canal; PSCh ¼ height of the posterior semicircular canal; PSCw ¼ width of the posterior semicircular canal; COh ¼ height of the basal turn of the cochlea; COw ¼ width of the basal turn of the cochlea; SLI ¼ Sagittal Labyrinthine Index, calculated from the width of the posterior canal above (SLIs) and below (SLIi) the plane of the lateral canal; LSCm ¼ arc of the lateral semicircular canal at its greatest width in the sagittal plane; PPp ¼ posterior petrosal surface in the sagittal plane at the level of the common crus; APA ¼ ampullar line; COs ¼ basal turn of the cochlea in the sagittal plane; FC3 ¼ third part of the facial canal in the sagittal plane. Definitions of the measurements and orientations are in Spoor et al. (2003). Figure modified from Spoor et al. (2003).

basal turn, ampullar line, posterior petrosal surface, and third part of the facial canal were then measured as projected onto the sagittal plane, with the angular value reflecting the inclination relative to the plane of the lateral canal. The diameters of the semicircular canals and cochlear basal turn were taken from the midpoint of the canal lumen and cochlear basal turn. The Mimics™ software program we used to create the virtual reconstructions allows the researcher to view simultaneously the individual 2D slices in the transverse, sagittal, and coronal planes, as well as the resulting 3D virtual reconstruction of the labyrinth. Measurement points were placed at the midpoint of the canal lumen and the cochlear basal turn in the individual 2D slices, relying on visualizing the placement in all three of the anatomical planes, and measurements were calculated directly from these points in the 3D virtual reconstruction. These same measurement points were also used to establish the planes of each of the canals and the inclination of the cochlear basal turn. Measurements in the present study were meant to capture the main characteristics of the semicircular canals and cochlea. However, given the close evolutionary relationship between the SH hominins and Neandertals, we have focused our analysis mainly on those variables which revealed distinctions between Neandertals and other Pleistocene human taxa (Spoor et al., 2003). Linear measurements were taken to the nearest 0.1 mm and angles were measured to the nearest degree. Given the resolution of the CT scans in the present study, measurement error has been estimated

as ±0.1 mm and ±4 based on the results of previous studies (Spoor and Zonneveld, 1995). 2.2. Statistical analysis Statistical analysis of the metric data was carried out using the Statistica™ software program and was oriented toward elucidating taxonomic differences between the groups under consideration. In addition, published regression formulae relating labyrinth variables and body mass were used to determine how well they predict certain labyrinth dimensions in the SH sample (Spoor et al., 2003, 2007). Although these regressions do not rely on phylogenetically sensitive methods, they have been applied to a large number of fossil specimens and we provide them here for comparative purposes. To examine the presence of differences between the groups of hominins (Table 1), analysis of variance (ANOVA) was performed comparing the means between the SH hominins, Neandertals, and recent H. sapiens samples. These are the only groups with sufficient sample size to allow for a statistical comparison. The present study relied on a p < 0.05 significance level to reject the null hypothesis (Ho) of no difference between sample means. When analyzing several samples, ANOVA is preferred over multiple t-tests since it lowers the chance of a type I error (Levin et al., 2010). A post-hoc variant of Tukey's Honestly Significant Difference (HSD) test (unequal N HSD) was subsequently performed on those variables that yielded a significant result to examine specific group differences in

R. Quam et al. / Journal of Human Evolution 90 (2016) 1e15

the metric variable. The Tukey unequal N HSD does not require equal sample sizes between the groups being compared. Principal components analysis (PCA) was carried out on the correlation matrix of the metric data. To avoid using combinations of variables in the PCA, the variables were limited to the radii of the canals and cochlea, the sagittal labyrinthine index (SLI), and the angular measures. The variables were first transformed (by dividing by the geometric mean) to control for the effects of overall size. PCA reduces the number of variables to a smaller number of components whose constituent variables can then be analyzed. By default, PCA generates the same number of components as variables in the analysis, but only those components that yield eigenvalues >1.0 can be considered to explain more variation than the individual variables in isolation. Factor loadings of >0.7 for the individual variables, indicating their correlation with the principal component, were generally considered high. 3. Results 3.1. Size and shape of the semicircular canals Data for the absolute and relative sizes and the shape of each of the three semicircular canals are provided in Table 2 (Raw data for all the Atapuerca [SH] individuals are provided in SOM Appendix B). The absolute and relative size of the anterior canal has remained fairly stable across Pleistocene Homo samples and does not differ statistically between any of the groups compared. However, the shape of the anterior canal in the SH sample is narrower than in the lower/middle Pleistocene African þ Asian sample and recent H. sapiens. In contrast, the absolute and relative sizes of the posterior canal in the SH hominins and Neandertals are small compared with recent humans. The shape index of the posterior canal, however, does not differ across Pleistocene Homo. While the non-SH middle Pleistocene European sample does appear to show a slightly narrower canal, this is largely due to the very high value in a single individual (Reilingen ¼ 132.0). The lateral canal is relatively larger in the SH hominins and Neandertals, and this appears to be a derived feature, one that is also present in the non-SH middle Pleistocene European sample. The shape of the lateral canal is narrower in the SH hominins than in the lower/middle Pleistocene African þ Asian sample, and a wider lateral canal may be a primitive feature within the genus Homo. The SH hominins do not differ from the Neandertals in any of the canal variables. In both absolute and relative canal sizes, the lower Pleistocene African and Asian specimens and fossil H. sapiens samples resemble recent humans, while the small non-SH middle Pleistocene sample seems most similar to both the SH hominins and Neandertals. When the relative sizes of the lateral and posterior canals are plotted against one another (Fig. 3), the SH hominins fall outside of the recent H. sapiens 95% equiprobability ellipse. In contrast, the SH ellipse essentially overlaps and largely falls within that of Neandertals. The small non-SH middle Pleistocene sample is also contained within the Neandertal ellipse. Three of the lower/middle Pleistocene African þ Asian hominins, as well as the Xujiayao 15 specimen also fall within the Neandertal ellipse and outside of the recent human range of variation. 3.2. Relative position of the posterior canal The sagittal labyrinthine index (SLI) compares the position of the posterior canal relative to the horizontal plane of the lateral canal. In lower and middle Pleistocene specimens from Africa and Asia, as well as H. sapiens, the vertical posterior canal is approximately bisected by the plane of the horizontal lateral canal. In contrast, Neandertals have been shown to have a low placement of

5

the posterior canal (resulting in a high value for the SLI), with more than half of the posterior canal located below the plane of the lateral canal (Table 3), and an absolutely short common crus between the anterior and posterior canals. This low placement is generally considered a derived feature in Neandertals. The mean SLI in the SH sample (49.2) indicates that the posterior canal is not positioned low relative to the lateral canal. Although we have not quantified the length of the common crus, this does not appear to be shortened in the Atapuerca (SH) hominins. The SLI in the SH hominins can also be predicted based on its relationship with the size of the posterior canal (PSC-R; Spoor et al., 2003), according to the following regression equation: SLI ¼ 23.59(PSC-R) e 22.91 Based on a mean posterior canal radius of 2.6 mm, a value of 38.4 is predicted for the SLI in the SH hominins. The predicted value is approximately 1.5 s.d. below the mean observed SLI (49.5), and only two SH individuals (Cr. 9 and 15) fall close to this value (Table 3). Neandertals and non-SH European middle Pleistocene individuals, like the SH hominins, were considerably underestimated by the regression formula. When the SLI is compared with the PSC-R (Fig. 4), the SH specimens generally fall separately from the Neandertals. Four SH individuals do fall within the Neandertal 95% equiprobability ellipse, with Cr. 4 and Cr. 7 showing the highest values for the SLI. Two additional individuals (Cr. 3 and Cr. 12) fall within the Neandertal range of variation in the SLI, but the remaining ten individuals (71.4% of the sample) fall below the Neandertal range (Table 4; Fig. 4). All three non-SH European middle Pleistocene specimens fall within the SH 95% equiprobability ellipse, but Reilingen does show a low placement of the posterior canal (i.e., high SLI) like in Neandertals. The lower/middle Pleistocene African þ Asian hominins generally fall within the recent H. sapiens and SH equiprobability ellipses, but Sangiran 4 does fall with the Neandertals. The Xujiayao 15 individual is most similar to Neandertals in both dimensions. 3.3. Angular measures of the lateral canal Several angular measures of the bony labyrinth and some surrounding structures relative to the plane of the lateral canal were also measured (Table 5). The inclination of the ampullar line (LSCm < APA) in the SH hominins, connecting the ampullae of the anterior and posterior canals, does not differ from either the lower/ middle Pleistocene African þ Asian hominins or recent humans. In contrast, the ampullar line is more vertically inclined in Neandertals than in any of the other groups and appears to be a derived feature. The angulation of the third part of the facial canal (LSCm < FC3) shows a similar pattern, and the more vertical orientation in Neandertals is apparently derived. The posterior petrosal surface (LSCm < PPp) is more inclined in Neandertals compared with recent H. sapiens, but none of the other comparisons were significant. The SH hominin mean value falls closest to that in the lower/middle Pleistocene African þ Asian hominins. Finally, the angle of the basal turn of the cochlea (COs < LSCm) does not differ statistically between any of the groups compared. Thus, the lower/middle Pleistocene African þ Asian sample, the SH hominins, and recent H. sapiens do not differ statistically in any of these angular measures. In the two most diagnostic measures, where Neandertals differ from the other three groups, only minimal overlap is present between the SH hominins and Neandertals (Fig. 5; Table 5). Of the SH hominins, only Cr. 12 falls within the Neandertal 95% equiprobability ellipse, although Cr. 4 and 7 are very close. Among the non-SH European middle Pleistocene

6

Table 2 Size and shape of the semicircular canals in Pleistocene and recent humans. Specimen/Sample

Radii of curvature (mm) ASC-R

PSC%R

LSC%R

ASCh/w

PSCh/w

LSCh/w

2.5 2.8 2.4 2.7 2.6 2.9 2.6 2.6 2.6 2.6 2.5 2.6 2.6 2.8 2.6 ± 0.1 2.4e2.9 (14)

2.3 2.7 2.3 2.7 2.5 2.7 2.4 2.6 2.4 2.4 2.4 2.3 2.3 2.5 2.5 ± 0.2 2.3e2.7 (14)

35.9 35.4 37.8 36.5 37.6 35.9 36.5 34.3 37.0 36.0 35.6 38.0 35.8 37.9 36.4 ± 1.1 34.3e38.0 (14)

33.5 32.9 31.5 31.5 32.0 33.2 33.2 32.9 33.2 33.5 33.0 33.1 34.3 32.8 32.9 ± 0.8 31.5e34.3 (14)

30.6 31.7 30.7 32.0 30.3 30.9 30.3 32.8 29.8 30.5 31.4 28.9 29.9 29.3 30.7 ± 1.1 28.9e32.8 (14)

103.9 93.5 89.2 94.8 100.5 98.7 107.2 94.5 100.5 89.9 95.4 93.3 87.3 96.1 96.1 ± 5.6 87.2e107.2 (14)

88.4 105.1 102.7 111.0 105.1 96.6 100.2 108.1 99.2 101.0 93.9 95.5 104.2 102.1 100.9 ± 6.0 88.4e111.0 (14)

99.1 93.6 96.2 90.7 104.9 98.0 98.8 88.7 93.0 103.8 89.1 105.7 85.0 95.9 95.9 ± 6.3 85.0e105.7 (14)

L./M. Pleist. Africa þ Asia Mean ± s.d. L./M. Pleist. Africa þ Asia Range (n) M. Pleist. Europe Mean ± s.d. M. Pleist. Europe Range (n) Neandertals Mean ± s.d. Neandertals Range (n) Fossil H. sapiens Mean ± s.d. Fossil H. sapiens Range (n) Recent H. sapiens Mean ± s.d. Recent H. sapiens Range (n)

3.1 ± 0.2 2.8e3.5 (7) 3.0 ± 0.1 2.8e3.1 (4) 3.0 ± 0.2 2.7e3.4 (26) 3.3 ± 0.2 3.0e3.6 (11) 3.1 ± 0.2 2.5e3.6 (26)

2.9 ± 0.3 2.5e3.3 (7) 2.7 ± 0.0 2.7e2.7 (4) 2.8 ± 0.2 2.2e3.4 (25) 3.0 ± 0.3 2.5e3.3 (10) 3.1 ± 0.3 2.4e3.6 (26)

2.3 ± 0.3 2.0e2.9 (7) 2.5 ± 0.1 2.3e2.6 (4) 2.6 ± 0.2 2.3e2.9 (26) 2.5 ± 0.2 2.2e2.8 (11) 2.3 ± 0.2 1.9e2.7 (26)

37.4 ± 0.9 36.5e39.2 36.3 ± 0.7 35.4e36.9 35.9 ± 1.3 33.8e39.0 37.5 ± 1.2 36.0e39.5 36.5 ± 1.2 34.2e39.0

34.9 ± 2.1 32.5e38.8 33.3 ± 1.0 32.1e34.2 33.7 ± 1.6 28.6e35.8 33.7 ± 1.7 30.6e35.9 36.3 ± 1.3 33.5e38.6

27.8 ± 2.6 23.5e30.6 30.4 ± 0.9 29.1e31.0 30.4 ± 1.3 28.0e32.5 28.9 ± 1.3 27.2e31.8 27.2 ± 1.6 25.0e30.5

ANOVA L./M. Pleist. Africa þ Asia vs. SH L./M. Pleist. Africa þ Asia vs. Neandertal L./M. Pleist. Africa þ Asia vs. Recent H. sapiens SH vs. Neandertal SH vs. Recent H. sapiens Neandertal vs. Recent H. sapiens

0.027 0.188 0.691 0.991 0.559 0.076 0.409

<0.001 0.666 0.180 0.998 0.574 0.259 <0.001

0.040 0.454 0.120 0.535 0.698 0.998 0.312

(7) (4) (25) (10) (26)

<0.001 0.074 0.393 0.308 0.598 <0.001 <0.001

(7) (4) (25) (10) (26)

<0.001 0.004 0.008 0.915 0.978 <0.001 <0.001

(7) (4) (25) (10) (26)

85.3 ± 11.5 69.7e104.9 (7) 94.3 ± 3.3 90.0e98.0 (4) 92.7 ± 5.6 84.0e103.0 (25) 86.3 ± 8.8 72.0e98.4 (9) 89.2 ± 5.0 80.3e97.3 (26) <0.001 0.010 0.096 0.645 0.588 0.023 0.114

104.9 ± 7.6 95.4e114.6 110.9 ± 15.2 96.0e132.0 101.9 ± 7.8 87.0e115.0 103.4 ± 10.9 88.0e118.0 103.2 ± 5.9 92.4e116.3 0.561 0.687 0.854 0.965 0.973 0.807 0.926

(7) (4) (24) (9) (26)

83.1 ± 10.6 62.5e92.6 (7) 89.8 ± 5.7 84.0e97.1 (4) 92.0 ± 5.8 83.0e105.0 (25) 91.7 ± 6.1 82.0e104.3 (10) 93.8 ± 8.0 78.1e108.0 (26) 0.002 0.007 0.102 0.034 0.482 0.858 0.816

R. Quam et al. / Journal of Human Evolution 90 (2016) 1e15

ASC%R

2.7 3.0 2.9 3.1 3.1 3.1 2.9 2.7 2.9 2.8 2.7 3.0 2.8 3.3 2.9 ± 0.2 2.7e3.3 (14)

<0.001 0.109 0.841 0.610 0.172 <0.001 0.001

LSC-R

Shape indices

SH Cranium 3 (L) SH Cranium 4 (R) SH Cranium 5 (L) SH Cranium 6 (R) SH Cranium 7 (R) SH Cranium 8 (R) SH Cranium 9 (R) SH Cranium 11 (L) SH Cranium 12 (R) SH Cranium 13 (R) SH Cranium 14 (R) SH Cranium 15 (R) SH Cranium 17 (L) AT-1907 (R) Atapuerca SH Mean ± s.d. Atapuerca SH Range (n)

Mean values in hominin samples in bold. Significant differences in ANOVA results in bold and italicized.

PSC-R

Relative size (%)

R. Quam et al. / Journal of Human Evolution 90 (2016) 1e15

7

Figure 3. Scatterplot of the relative sizes of the lateral (LSC) and posterior (PSC) canals. The 95% equiprobability ellipses for the SH sample, Neandertals, and recent H. sapiens based on the range of values are also presented. The Atapuerca (SH) individuals are indicated.

Figure 4. Scatterplot of the radius of the posterior canal (PSC) and the sagittal labyrinthine index (SLI). The 95% equiprobability ellipses for the SH sample, Neandertals, and recent H. sapiens based on the range of values are also presented. The Atapuerca (SH) individuals are indicated.

hominins, both Abri Suard and Reilingen resemble the Neandertals more closely in their angular relationships, while Steinheim falls outside the Neandertal range of variation, resembling the SH hominins more closely. The fossil H. sapiens individuals fall outside

of the Neandertal 95% equiprobability ellipse and resemble the SH hominins and recent humans more closely.

Table 3 The sagittal labyrinthine index in Pleistocene and recent humans. Specimen/Sample

Sagittal Labyrinthine Index (%)

SH Cranium 3 (L) SH Cranium 4 (R) SH Cranium 5 (L) SH Cranium 6 (R) SH Cranium 7 (R) SH Cranium 8 (R) SH Cranium 9 (R) SH Cranium 11 (L) SH Cranium 12 (R) SH Cranium 13 (R) SH Cranium 14 (R) SH Cranium 15 (R) SH Cranium 17 (L) AT-1907 (R) Atapuerca SH Mean ± s.d. Atapuerca SH Range (n)

56.4 60.9 50.4 48.2 58.2 47.3 38.6 42.7 54.3 47.9 51.7 36.1 45.0 51.0 49.2 ± 7.1 36.1e60.9 (14)

L./M. Pleist. Africa þ Asia Mean ± s.d. L./M. Pleist. Africa þ Asia Range (n) M. Pleist. Europe Mean ± s.d. M. Pleist. Europe Range (n) Neandertals Mean ± s.d. Neandertals Range (n) Fossil H. sapiens Mean ± s.d. Fossil H. sapiens Range (n) Recent H. sapiens Mean ± s.d. Recent H. sapiens Range (n)

49.2 ± 6.7 41.4e61.0 (7) 50.3 ± 10.0 40.0e60.0 (3) 63.4 ± 5.7 53.0e76.0 (25) 45.7 ± 7.5 33.0e55.1 (11) 50.6 ± 5.4 38.9e61.1 (26)

ANOVA L./M. Pleist. Africa þ Asia vs. SH L./M. Pleist. Africa þ Asia vs. Neandertal L./M. Pleist. Africa þ Asia vs. Recent H. sapiens SH vs. Neandertal SH vs. Recent H. sapiens Neandertal vs. Recent H. sapiens

<0.001 1.000 <0.001 0.980 <0.001 0.937 <0.001

Mean values in hominin samples in bold. Significant differences in ANOVA results in bold and italicized.

3.4. Size and shape of the basal turn of the cochlea The radius of the basal turn of the cochlea (CO-R) does not differ between any of the groups compared in the present study (Table 4; Raw data for all the Atapuerca-SH individuals are provided in SOM Appendix B). Indeed, the values for this variable do not differ much between most hominin groups, although the fossil H. sapiens show the largest mean value. The size of the basal turn of the cochlea (CO-R) can also be predicted in the SH hominins based on its relationship with body mass (Spoor et al., 2003), relying on the following regression formula: Log10CO-R ¼ 0.139(Log10Body Mass) e 0.335 Based on a mean body mass of 95 kg in the SH hominins (Arsuaga et al., 1999), a value of 2.27 mm is predicted for the CO-R. This is very close to the observed value of 2.2 mm for CO-R in the SH sample (Table 4). The shape index of the basal turn in the SH hominins (120.3) is unusually low (Fig. 6), and the SH mean is significantly different from Neandertals (Table 4). Although there is overlap between most of the samples, the upper limit of the SH range of variation falls near the mean of the lower/middle Pleistocene African þ Asian hominins, and only three individuals fall within the SH range of variation. Among the non-SH European middle Pleistocene specimens, Reilingen falls within the SH 95% equiprobability ellipse close to the SH mean, but both Steinheim and La Chaise-Suard fall outside the SH range of variation. Based on the values for the height and width of the basal turn in the SH sample and recent H. sapiens, the low index in the SH sample mainly reflects a reduction in the height of the basal turn. 3.5. Principal components analysis The PCA based on nine transformed variables yielded only two principal components with eigenvalues >1.0 and which explain a total of 60.4% of the variance (Table 6; Fig. 7). The sizes of the anterior and posterior canals and the cochlea showed high positive

8

R. Quam et al. / Journal of Human Evolution 90 (2016) 1e15 Table 4 Size and shape of the cochlear basal turn in Pleistocene and recent humans. Specimen/Sample

CO-R (mm)

COh/w

SH Cranium 3 (L) SH Cranium 4 (R) SH Cranium 5 (L) SH Cranium 6 (R) SH Cranium 7 (R) SH Cranium 8 (R) SH Cranium 9 (R) SH Cranium 11 (L) SH Cranium 12 (R) SH Cranium 13 (R) SH Cranium 14 (R) SH Cranium 15 (R) SH Cranium 17 (L) AT-1907 (R) Atapuerca SH Mean ± s.d. Atapuerca SH Range (n)

2.1 2.3 e 2.5 2.2 2.3 2.3 2.1 2.3 2.3 2.1 2.1 e 2.1 2.2 ± 0.1 2.1e2.5 (12)

116.0 116.6 e 119.4 121.2 113.3 132.6 119.5 131.7 125.6 113.7 115.7 e 118.6 120.3 ± 6.5 113.3e132.6 (12)

L./M. Pleist. Africa þ Asia Mean ± s.d. L./M. Pleist. Africa þ Asia Range (n) M. Pleist. Europe Mean ± s.d. M. Pleist. Europe Range (n) Neandertals Mean ± s.d. Neandertals Range (n) Fossil H. sapiens Mean ± s.d. Fossil H. sapiens Range (n) Recent H. sapiens Mean ± s.d. Recent H. sapiens Range (n)

2.3 ± 0.3 1.8e2.6 (7) 2.2 ± 0.1 2.1e2.3 (3) 2.3 ± 0.2 2.0e2.5 (15) 2.4 ± 0.2 2.2e2.7 (8) 2.3 ± 0.2 2.0e2.6 (26)

131.8 ± 10.6 118.2e147.4 137.3 ± 13.3 122.0e145.0 134.7 ± 11.2 122.0e154.0 136.4 ± 11.8 120.0e155.0 128.4 ± 7.0 114.5e144.8

ANOVA L./M. Pleist. Africa þ Asia vs. SH L./M. Pleist. Africa þ Asia vs. Neandertal L./M. Pleist. Africa þ Asia vs. Recent H. sapiens SH vs. Neandertal SH vs. Recent H. sapiens Neandertal vs. Recent H. sapiens

0.141 0.389 0.868 0.999 0.702 0.249 0.795

(7) (3) (15) (8) (26)

0.001 0.073 0.959 0.882 0.001 0.112 0.253

Mean values in hominin samples in bold. Significant differences in ANOVA results in bold and italicized.

loadings with PC1, while the SLI and the angle of the ampullar line (LSCm < APA) showed strong negative loadings. Some separation of groups is apparent along PC1. Neandertals show negative values on PC1, reflecting smaller anterior and posterior canals, a more inferior position of the posterior canal, and a more inclined ampullar line. In contrast, while some overlap is present, fossil and recent H. sapiens generally show positive values along PC1, reflecting larger anterior and posterior canals, a more superior position of the posterior canal, and a less inclined ampullar line. The majority of the Atapuerca (SH) specimens and the non-SH European middle Pleistocene hominins group with Neandertals. Nevertheless, Atapuerca (SH) Cr. 6, 13, and 15 and Steinheim show positive values along PC1, generally falling with the modern humans, while Sangiran 2 and Abri Pataud show negative values falling with the Neandertals. The Xujiayao 15 individual also shows negative values along PC1. The angle of the cochlear basal turn showed a strong positive loading with PC2, while the angles of the facial canal and (less-so) the posterior petrosal surface showed strong negative loadings with PC2. Less separation between groups is evident along PC2, but Neandertals generally show negative values, reflecting a more inclined facial canal. All of the Atapuerca (SH) and non-SH European middle Pleistocene individuals also show negative values. Here, the Xujiayao 15 shows positive values, falling outside the Neandertal 95% equiprobability ellipse. All of the lower/middle Pleistocene African þ Asian specimens fall within the recent H. sapiens 95% equiprobability ellipse on both PC1 and PC2, reflecting the broad similarity between these two groups of hominins in most of the bony labyrinth dimensions.

4. Discussion It is now possible to outline a more complete picture of the evolutionary pattern of bony labyrinth variation during the Pleistocene and to propose the phylogenetic polarity within the genus Homo for several features (Table 7). Compared with the early hominin taxa Australopithecus africanus and Paranthropus robustus, the genus Homo saw an increase in body size and concomitant increase in the absolute sizes of the three semicircular canals (Spoor, 1993; Spoor et al., 1994). Nevertheless, when canal size is predicted from body mass and agility across primates (Spoor et al., 2007), the absolute size of all three semicircular canals in the genus Homo appears small (Table 8). The anterior and posterior canals are somewhat better predicted in the lower/middle Pleistocene African þ Asian hominins and recent H. sapiens, with the predicted posterior canal size in H. sapiens nearly matching the observed value in our sample. In contrast, the lateral canal size is better predicted in the Atapuerca (SH) hominins and Neandertals. The lower/middle Pleistocene Africa þ Asia sample differs from recent H. sapiens in only a single variable, the shape of the lateral canal. This strong similarity suggests that the H. sapiens bony labyrinth morphology is largely primitive for the genus Homo, corroborating previous suggestions. The absolute and relative sizes of the anterior canal (ASC-R and ASC%R) seem to have changed little during the course of evolution of Pleistocene Homo. In contrast, the absolute and relative posterior canal sizes (PSC-R and PSC%R) are smaller in the Atapuerca (SH) hominins and Neandertals compared with recent H. sapiens, who

R. Quam et al. / Journal of Human Evolution 90 (2016) 1e15

9

Table 5 Angular measures of the lateral canal in Pleistocene and recent humans. Specimen/Sample

Angles (deg.) LSCm < APA

LSCm < FC3

LSCm < PPp

COs < LSCm

SH Cranium 3 (L) SH Cranium 4 (R) SH Cranium 5 (L) SH Cranium 6 (R) SH Cranium 7 (R) SH Cranium 8 (R) SH Cranium 9 (R) SH Cranium 11 (L) SH Cranium 12 (R) SH Cranium 13 (R) SH Cranium 14 (R) SH Cranium 15 (R) SH Cranium 17 (L) AT-1907 (R) Atapuerca SH Mean ± s.d. Atapuerca SH Range (n)

33.3 38.9 34.5 37.2 39.1 e 32.8 42.0 41.7 33.6 28.4 28.2 e 35.4 35.4 ± 4.6 28.2e42.0 (12)

82.0 87.0 69.0 79.0 90.0 73.0 78.0 76.0 83.0 68.0 75.0 72.0 e 71.0 77.2 ± 6.8 68.0e90.0 (13)

69.0 71.0 68.0 59.0 63.0 65.0 e 61.0 62.0 59.0 e 60.0 e e 63.7 ± 4.3 59.0e71.0 (10)

60.1 61.4 55.8 56.4 58.4 e 43.2 55.1 52.7 51.9 36.6 47.8 e 61.2 53.4 ± 7.6 36.6e61.4 (12)

L./M. Pleist. Africa þ Asia Mean ± s.d. L./M. Pleist. Africa þ Asia Range (n) M. Pleist. Europe Mean ± s.d. M. Pleist. Europe Range (n) Neandertals Mean ± s.d. Neandertals Range (n) Fossil H. sapiens Mean ± s.d. Fossil H. sapiens Range (n) Recent H. sapiens Mean ± s.d. Recent H. sapiens Range (n)

36.7 ± 5.1 32.1e45.0 37.1 ± 3.9 33.0e40.0 46.7 ± 4.7 40.0e53.0 34.5 ± 4.3 29.0e42.0 36.3 ± 4.0 29.1e42.6

74.7 ± 3.1 71.0e78.0 (6) 83.7 ± 9.1 74.0e92.0 (3) 91.1 ± 8.4 81.0e104.0 (9) 77.1 ± 8.4 63.5e86.0 (6) 70.7 ± 6.7 58.7e83.3 (26)

64.7 ± 7.3 56.0e73.0 (6) 61.7 ± 6.8 54.0e67.0 (3) 69.0 ± 6.7 61.0e82.0 (10) 60.3 ± 10.5 51.0e80.0 (7) 59.4 ± 6.5 44.8e69.9 (25)

57.0 ± 7.3 48.9e68.0 48.2 ± 5.6 43.0e54.0 58.7 ± 6.3 46.0e68.0 56.9 ± 2.9 52.0e60.0 55.9 ± 5.5 41.2e65.6

ANOVA L./M. Pleist. Africa þ Asia vs. SH L./M. Pleist. Africa þ Asia vs. Neandertal L./M. Pleist. Africa þ Asia vs. Recent H. sapiens SH vs. Neandertal SH vs. Recent H. sapiens Neandertal vs. Recent H. sapiens

<0.001 0.959 0.002 0.999 <0.001 0.959 <0.001

(6) (3) (15) (7) (26)

<0.001 0.914 0.001 0.785 <0.001 0.102 <0.001

0.003 0.992 0.652 0.522 0.256 0.500 0.010

(6) (3) (15) (7) (26)

0.183 0.761 0.960 0.990 0.170 0.776 0.587

Mean values in hominin samples in bold. Significant differences in ANOVA results in bold and italicized.

show the largest posterior canals. Although not tested statistically, the non-SH European middle Pleistocene specimens also seem smaller than recent humans. The lateral canal is relatively larger (LSC%R) in Neandertals and the SH hominins, as well as the non-SH

European middle Pleistocene specimens. The enlarged lateral canal has been attributed to an increase in body mass in Neandertals and middle Pleistocene specimens (Spoor et al., 2003), and the large body mass in the SH hominins (c. 95 kg; Arsuaga et al., 1999) could

Figure 5. Scatterplot of the angles of the facial canal and ampullar line. The 95% equiprobability ellipses for the SH sample, Neandertals, and recent H. sapiens based on the range of values are also presented. The Atapuerca (SH) individuals are indicated. LSCm ¼ arc of the lateral semicircular canal at its greatest width in the sagittal plane; FC3 ¼ third part of the facial canal in the sagittal plane; APA ¼ ampullar line.

Figure 6. Scatterplot of the size and shape of the basal turn of the cochlea. The 95% equiprobability ellipses for the SH sample, Neandertals, and recent H. sapiens based on the range of values are also presented. The Atapuerca (SH) individuals are indicated. COh ¼ height of the basal turn of the cochlea; COw ¼ width of the basal turn of the cochlea; CO-R ¼ radius of the basal turn of the cochlea.

10

R. Quam et al. / Journal of Human Evolution 90 (2016) 1e15

Table 6 Results of the principal components analysis for the transformed bony labyrinth variables.

Eigenvalue % Total variance Variable factor loadings ASC-R PSC-R LSC-R SLI CO-R LSCm < PPp LSCm < FC3 LSCm < APA LSCm < COs

Factor 1

Factor 2

3.71 41.25

1.73 19.19

0.897 0.816 0.531 ¡0.736 0.674 0.444 0.494 ¡0.712 0.122

0.069 0.324 0.406 0.301 0.159 0.556 0.668 0.391 0.656

Factor loadings >0.7 in bold.

also explain their relatively large lateral canals. Nevertheless, the reduced posterior canal in the Neandertal clade seems to represent a derived feature within the genus Homo. The shape of the posterior canal does not seem to have changed much during the course of the Pleistocene. The higher mean value in the non-SH European middle Pleistocene specimens is due mainly to the presence of a single individual with a very high value, but no significant differences were found in this variable between any of the groups compared (Table 2). The arc shape of the lateral canal has also been argued previously to show no differences between hominin groups (Spoor et al., 2003). However, the expanded samples in the present study have revealed that a relatively wide lateral canal characterizes the lower/middle Pleistocene African þ Asian hominins. This feature appears to be primitive for the genus Homo, with later taxa, including H. sapiens, showing a more rounded, derived canal shape. Indeed this was the only variable that differed significantly between the lower/middle Pleistocene African þ Asian hominins and recent H. sapiens, suggesting it may represent a derived feature in the modern human bony labyrinth. The shape of the anterior canal in the Atapuerca (SH) hominins is more rounded (or narrower) than in all the other fossil samples, and a statistical difference was found with both lower/ middle Pleistocene African þ Asian hominins and recent H. sapiens. Thus, the present study has confirmed the suggestion of a relatively narrow anterior canal in the Neandertal clade (Spoor et al., 2003). Compared with the lower/middle Pleistocene African þ Asian hominins and recent humans, the shape index of the Atapuerca (SH) hominins is due to a reduction of the ASCw, rather than ASCh, suggesting the anterior canal is shortened in the AP direction like in Neandertals (Spoor et al., 2003).

4.1. Position of the posterior canal and “hyper-rotation” of the cerebellum

Figure 7. Principal components analysis of the transformed bony labyrinth variables. The 95% equiprobability ellipses for the SH sample, Neandertals, and recent H. sapiens based on the range of values are also presented. Higher scores along PC1 are associated with larger anterior and posterior canals and cochlea, a more superior placement of the posterior canal, and a less inclined ampullar line. Higher scores along PC2 indicate a lower angle of the facial canal and higher angle of the cochlear basal turn. The fossil individuals are indicated.

The low placement of the posterior canal (SLI) has been proposed as a derived feature in Neandertals, and the greater inclination of the ampullar line (LSCm < APA) is correlated with the placement of the posterior canal (Hublin et al., 1996; Spoor et al., 2003). Although it has not been quantified, the common crus, joining the anterior and posterior canals, is described as absolutely short in Neandertals (Spoor et al., 2003), perhaps related to the low placement of the posterior canal. Our qualitative observation of the Atapuerca (SH) hominins indicates they do not show a particularly short common crus.

Table 7 Phylogenetic polarity of bony labyrinth traits within the genus Homo. Trait

Absolute and relative size of the anterior canal Shape of the anterior canal Absolute and relative size of the posterior canal Shape of the posterior canal Absolute and relative size of the lateral canal Shape of the lateral canal Relative position of the posterior canal Inclination of ampullar line Length of common crus Angle of posterior petrosal surface Angle of the facial canal Angle of radius of the cochlear basal turn Radius of the cochlea basal turn Shape index of the cochlea basal turn Inferred derived character states are in bold.

Lower/Middle Pleist.

Recent H. sapiens

Abbreviation

Africa þ Asia

Atapuerca (SH)

Neandertals

ASC-R, ASC%R ASCh/w PSC-R, PSC%R PSCh/w LSC-R, LSC%R LSCh/w SLI LSCm < APA CCR LSCm < PPp LSCm < FC3 COs < LSCm CO-R COh/w

Large Wider Large Circular Small Wider Mid-height Less vertical Long Less vertical Less vertical High Large High

Large Narrower Small Circular Large Narrower Mid-height Less vertical Long Less vertical Less vertical High Large Low

Large Narrower Small Circular Large Narrower Low More Vertical Short More Vertical More Vertical High Large High

Large Wider Large Circular Small Narrower Mid-height Less vertical Long Less vertical Less vertical High Large High

R. Quam et al. / Journal of Human Evolution 90 (2016) 1e15

11

Table 8 Predicted semicircular canal size from body mass and agilitya in the genus Homo. Group

Low/Mid Pleist. Africa þ Asia Atapuerca (SH) Neandertals Recent H. sapiens

Body mass (kg)b

60.7 95.0 76.0 58.3

Observed canal size

Predicted canal size

% Difference

ASC-R

PSC-R

LSC-R

ASC-R

PSC-R

LSC-R

ASC-R

PSC-R

LSC-R

3.1 2.9 3.0 3.1

2.9 2.6 2.8 3.1

2.3 2.5 2.6 2.3

3.56 3.80 3.68 3.55

3.13 3.32 3.22 3.12

2.69 2.84 2.76 2.69

15.0 31.0 22.6 14.6

7.8 27.8 15.1 0.5

17.1 13.6 6.3 16.8

SH body mass from Arsuaga et al. (1999), Neandertals from Ruff et al. (1997), Recent H. sapiens from Smith and Jungers (1997). a Based on regression equations in Spoor et al. (2007). Fossil taxa assigned an agility score of 4, as in recent H. sapiens. b Body mass for Low/Mid Pleist. Africa þ Asia sample based on eight L. Pleist. Homo individuals from Koobi Fora (Ruff et al., 1997).

The inferior placement of the posterior canal in Neandertals, as well as the more vertical orientation of the facial canal (LSCm < FC3) and posterior petrosal surface (LSCm < PPp) relative to the lateral canal, have been suggested to reflect a “hyperrotation” of the cerebellum in the posterior cranial fossa (Spoor et al., 2003). This is argued to be a consequence of distinctive brain morphology in Neandertals, particularly in the posterior cranial fossa. In fact, within H. sapiens, increases in the size of the posterior cranial fossa, coupled with a wider cranial base and more coronal orientation of the petrous pyramid, have been shown to be associated with a smaller posterior semicircular canal and a superior tilting of the lateral canal (Gunz et al., 2013). In this regard, it is noteworthy that the encephalization process in Neandertals and modern humans has been shown to follow distinct allometric trajectories (Bruner et al., 2003), resulting in similarly large brain sizes but distinctive brain shapes in both groups of hominins. In particular, increased brain size in Neandertals is associated with relative reductions in the length and width of the occipital lobes, and this pattern of allometry is argued to represent the primitive condition for the genus Homo, being present in earlier fossil taxa. Perhaps more directly relevant, increases in brain size in Neandertals mainly involved the neocortex, rather than the cerebellum, while recent H. sapiens also show a considerable increase in the size of the cerebellum (Weaver, 2005). Thus, the derived Neandertal bony labyrinth morphology may reflect the combination of an archaic pattern of brain allometry, a relatively wide cranial base, and absolutely large brain size. In this light, the distinctive labyrinth morphology found in Neandertals might be a particular expression of more general trends across the genus Homo. Although some variation is present within the sample, the Atapuerca (SH) hominins generally do not show a low placement of the posterior canal and do not resemble Neandertals in the inclination of the ampullar line and the facial canal. The inclination of the posterior petrosal surface did not differ much between groups, with a statistical difference found only between Neandertals and recent H. sapiens. Those Atapuerca (SH) individuals that did show a value for the SLI within the Neandertal range of variation (Table 3) also generally have higher angular values for the ampullar line and facial canal (Table 4). Nevertheless, most of the Atapuerca (SH) hominins do not show the “hyper-rotated” morphology seen in Neandertals. While the same archaic pattern of brain shape is present in the Atapuerca (SH) hominins and Neandertals (Bruner et al., 2003), the brain size is notably smaller in the Atapuerca (SH) sample (mean ¼ 1232 cm3; range ¼ 1057e1436 cm3; n ¼ 15; Arsuaga et al., 2014). Thus, the emergence of these derived bony labyrinth features in the Neandertal clade may have occurred only after brain size had reached a certain threshold. One of the non-SH European middle Pleistocene specimens (Reilingen) falls within the Neandertal range of variation for the SLI and shows a large brain size (c. 1430 cm3; Dean et al., 1998), while Steinheim does not show a low placement of the posterior canal

and the brain size is more modest (c. 1110e1200 cm3; Prossinger et al., 2003). However, the four Atapuerca (SH) individuals that have a value for the SLI within the Neandertal range of variation (Table 3) show considerable variation in brain size. Cr. 4 (1360 cm3) and Cr. 7 (1143 cm3) fall toward the upper and lower ends of the SH range of variation, respectively, while Cr. 3 (1230 cm3) and Cr. 12 (1227 cm3) are close to the sample mean (Arsuaga et al., 2014). In addition, within the Neandertal sample, variation in the SLI does not seem to be directly related to brain size, since high values for the SLI are found in individuals with small brain sizes (Tabun C1, Gibraltar 1) and individuals with similar-sized brains (La Chapelle and La Ferrassie 1) show different values for the SLI. Regarding the width of the cranial base, the Atapuerca (SH) specimens that show a low placed posterior canal also vary in biasterionic breadth, roughly paralleling the pattern in brain size, with Cr. 4 showing a very wide cranial base (132 mm) but Cr. 3 (113.5 mm) and Cr. 7 (112 mm) showing more modest values (Arsuaga et al., 1997). Among the non-SH European middle Pleistocene individuals, Reilingen shows a low placement of the posterior canal and a wider cranial base (120.4 mm; Dean et al., 1998), while Steinheim lacks a low placed posterior canal and shows a narrower cranial base (106 mm). Within the Neandertal sample, biasterionic breadth does not seem to vary directly with the SLI since specimens with a wider cranial base (e.g., La Ferrassie 1 ¼ 127 mm) show similar values for the SLI as specimens with narrower cranial bases (e.g., La Quina 5 ¼ 112 mm; Dean et al., 1998). The presence of a low placed posterior canal in the Sangiran 4 (SLI ¼ 61) and Xujiayao 15 (SLI ¼ 61.4) specimens from Asia (Wu et al., 2014) also suggests some degree of variation in this feature may be present in different Pleistocene Homo taxa. The brain size in Sangiran 4 is not large (908 cm3; Holloway et al., 2004). However, while the brain size of the Xujiayao 15 specimen cannot be determined, another individual from this sample has a very large cranial capacity (c. 1700 cm3; Wu et al., 2014). Thus, while it might be tempting to propose a threshold value for brain size, above which a low placed posterior canal would be present, such a “cerebral rubicon” remains elusive. In addition, the general lack of difference in the angle of the posterior petrosal surface (LSCm < PPp) between groups in the present study (Table 5) also suggests caution. Of the angular measures considered here, this would appear to be the most direct reflection of a “hyperrotated” cerebellum, yet Neandertals were only significantly different from recent H. sapiens. Nevertheless, while still not fully resolved, a large absolute brain size does generally seem to be related to the “hyper-rotated” morphology of the bony labyrinth in archaic members of the genus Homo. Thus, despite some intraspecific variation, the low placement of the posterior canal may be due to a combination of large absolute brain size, an archaic allometric trajectory of brain expansion, and a wide cranial base. This more general explanation would not necessarily follow taxonomic lines, even though this morphology of the bony labyrinth occurs at high frequencies among Neandertals.

12

R. Quam et al. / Journal of Human Evolution 90 (2016) 1e15

4.2. Cochlear size, shape, and inclination While the radius of the basal turn of the cochlea also appears to have increased in size over the early hominins, at least one early member of the genus Homo (SK 847) appears to have maintained a small cochlea (Spoor, 1993). Thus, it is possible that cochlear size increased only later in Pleistocene Homo, and the radius of the basal turn of the cochlea did not differ between any of the groups compared in the present study (Table 4). Nevertheless, the expanded fossil H. sapiens sample shows the highest mean value of all the samples, and the observed values for CO-R in fossil and recent H. sapiens fall either outside or at the very upper limit of the confidence interval for CO-R predicted from body mass (Spoor et al., 2003). Thus, the emergence of our own species appears to coincide with a relative increase in cochlear size, as suggested previously (Spoor et al., 2003), and this might be consistent with the larger stapes footplate in H. sapiens compared with previous fossil Homo taxa (Quam et al., 2013b). Nevertheless, this would imply a subsequent reduction in cochlear size within H. sapiens, and more data from early H. sapiens individuals is clearly necessary to confirm this suggestion. The shape index of the cochlear basal turn is very low in the Atapuerca (SH) hominins, reflecting mainly a reduction in the cochlear height, rather than the width. While the ranges of variation between most of the samples largely overlap, the upper limit of the Atapuerca (SH) range of variation is close to or below the mean values in the other samples. A significant difference was found only with the Neandertals. Among the non-SH European middle Pleistocene specimens, the cochlear shape index is low in Reilingen (122.0), falling very close to the Atapuerca (SH) sample mean (120.3), while both Abri Suard (145.0) and Steinheim (145.0) show higher values that fall outside the Atapuerca (SH) range of variation. While a high cochlear shape index might seem to represent a derived feature in Neandertals, the mean shape index in the fossil H. sapiens sample, while not tested statistically, is even higher than in the Neandertals. In addition, although the lower Pleistocene SK 847 individual is very small, falling outside the range of variation of the other fossil samples in both cochlear height and width, the resulting index (135.5) is not low. Thus, currently the phylogenetic polarity of cochlear shape is difficult to determine. Indeed, it is the low shape index in the Atapuerca (SH) hominins that seems to differ most from the other samples, with cochlear height increasing within the Neandertal clade. The inclination of the cochlea (COs < LSCm) does not differ between any of the hominin groups studied here. The previous suggestion of a lower value in European middle Pleistocene hominins was based on a smaller sample size (Spoor et al., 2003), but the larger dataset used here, including the Atapuerca (SH) sample, does not support this assertion. While the mean value in the nonSH European middle Pleistocene hominins is considerably lower than in the Neandertals, only Steinheim (43.0) falls outside of the Neandertal range of variation, and the values for these three individuals are encompassed by the Atapuerca (SH) range of variation. Within the Atapuerca (SH) sample, only two individuals (Cr. 9 and Cr. 14) fall outside of the Neandertal range of variation. The value in Cr. 9 is similar to that in Steinheim, while Cr. 14 suffered from pathological deformities of the skull and cranial base which may have reduced the value in this measure (Gracia et al., 2009), even though other dimensions of the cochlea appear largely unaffected. Removal of this individual raises the sample mean value slightly (54.9), making it more similar to Neandertals and most of the other comparative groups (Table 5). One other relevant observation can perhaps be drawn from the present data on the size and inclination of the cochlear basal turn. Differences from fossil and recent H. sapiens in the middle ear

ossicles of Neandertals include an anteriorly skewed stapedial head, a smaller stapes footplate, and a more closed angle between the long and short processes of the incus (Quam and Rak, 2008; Quam et al., 2013b). The latter two features likely represent primitive characteristics since they are present in the early hominin taxa A. africanus and P. robustus and also characterize the African apes (Quam et al., 2013a, 2014). These differences in the Neandertal ossicles are consistent with a slightly different articulation of the ossicular chain within the tympanic cavity compared with recent H. sapiens and imply either a change in the position of the oval window on the medial wall of the tympanic cavity (for the insertion of the stapes footplate) or the tympanic membrane (for the insertion of the manubrium of the malleus). The general stability of both the absolute size and orientation of the basal turn of the cochlea across the genus Homo suggests little change in the position of the oval window. In addition, the embryonic development of the otic capsule housing the inner ear indicates a strong genetic role in its formation and implies a strong genetic and evolutionary constraint. Thus, these results, while not definitive, would seem to be more consistent with differences in the middle ear ossicles of Neandertals reflecting a somewhat different position or orientation of the tympanic membrane.

4.3. Locomotor implications Differences in the absolute and relative sizes of the semicircular canals have been broadly linked to locomotor repertoires, head movements, and agility across primates. In particular, a larger mean canal arc size is associated with increased agility and head jerkiness during locomotion (Spoor et al., 2007). The vertical (i.e., anterior and posterior) canals are more closely related with angular movements of the head in the sagittal and coronal planes, while the horizontal (i.e., lateral) canal is most closely related with angular movement in the transverse plane. When the sizes of the canals are compared to one another, Neandertals and European middle Pleistocene specimens, including the SH sample, show relatively smaller vertical canals than do lower Pleistocene individuals from Africa and Asia or modern humans. In contrast, the size of the horizontal canal seems to largely reflect differences in body size within the genus Homo. The present study did find a statistical difference in the relative size of the anterior canal across the genus Homo, but none of the individual comparisons between groups reached significance (Table 2). Nevertheless, the mean values in the Atapuerca (SH) hominins and Neandertals are generally slightly lower than in the other comparative samples, and the posterior canal is relatively smaller in the Neandertals and the Atapuerca (SH) hominins. The relatively small dimensions of the vertical canals in Neandertals have been hypothesized to be related to greater angular movements of the head during locomotion, perhaps related with their AP-elongated cranium producing more tilting in the sagittal plane during locomotion (Spoor et al., 2003). The elongated Neandertal cranium is due to the combination of an absolutely large brain size, the protrusion of the occipital bun in the posterior of the skull, and a high degree of facial prognathism. These are classic features of Neandertals (Heim, 1976). Recent analysis of the Neandertal cervical spine has suggested that while the neck length was similar to H. sapiens, the mediolateral distance between the articular pillars (facets) and the length of the cervical spinous processes were
mez-Olivencia et al., 2013). This combigreater in Neandertals (Go nation of features implies a more stable neck in Neandertals in both the midsagittal and coronal planes and might be taken to reflect a passive resistance mechanism to greater angular movements of the head.

R. Quam et al. / Journal of Human Evolution 90 (2016) 1e15

The European middle Pleistocene specimens, including the SH sample, also show relatively small vertical canals. However, while the degree of facial prognathism in the SH population is similar to that in Neandertals, the absolute brain size is smaller, the cranial vault is not as AP-elongated, and the occipital is not as protruding (Arsuaga et al., 1997, 2014). In addition, although there is no difference from Neandertals in the neck length (Martínez et al., 2013), the cervical spinous processes are shorter in the SH sample
mez-Olivencia et al., 2013). These anatomical differences from (Go Neandertals in the cranium and neck suggest that the relatively small vertical canals found in members of the Neandertal clade may not be directly related with differences in angular head movements, and Malinzak et al. (2012) have questioned the relationship between canal radius of curvature and locomotor agility in primates. Regarding possible locomotor differences between Neandertals and recent H. sapiens, the SH hominins generally share with Neandertals the same differences from modern humans in the pelvis (Arsuaga et al., 1999), but the lower limb may have been slightly shorter (Carretero et al., 2012). Given that lower limb length makes a large contribution to bipedal mechanical efficiency (SteudelNumbers and Tilkens, 2004), the Neandertals may have been slightly more efficient than the Atapuerca (SH) hominins, but both populations would likely have been less efficient than H. sapiens. Thus, any postulated differences between modern human and Neandertal locomotor patterns would also largely apply to the SH population, suggesting that factors other than locomotor differences may be responsible for the derived canal proportions in the Neandertal clade. However, the smaller vertical canal sizes might be taken to be inconsistent with the suggestion of endurance running being an important component of the locomotor repertoire in the genus Homo since the lower Pleistocene (Bramble and Lieberman, 2004). Perhaps relevant in this regard, the calcanei in the Atapuerca (SH) hominins and Neandertals show longer body lengths, which is correlated with a longer moment arm of the Achilles tendon and less efficient endurance running (Raichlen et al., 2011; Pablos et al., 2014). Even if endurance running were a basal adaptation of the genus Homo, this behavior and the morphological correlates of it were subsequently lost in the Neandertal clade.

13

In contrast, the Atapuerca (SH) hominins are different from the Neandertals in generally lacking a low placement of the posterior canal and more inclined ampullar line and facial canal. Some variation is present within the sample, however, with a few individuals approaching the Neandertal condition more closely. In particular, Atapuerca (SH) Cr. 4, 7, and 12 do show a low posterior canal (high SLI) and more inclined facial canal and ampullar line, and these are the most Neandertal-like individuals within the sample. In addition, the cochlear shape index in the Atapuerca (SH) hominins is low, indicating a reduction in the height of the cochlea. This may represent a derived condition and, if so, cochlear height subsequently increased in Neandertals. Given these differences in the bony labyrinth within the Neandertal clade, it may be possible to identify when the full suite of Neandertal features emerged during the middle Pleistocene. The Steinheim and Reilingen specimens have been compared favorably with the Atapuerca (SH) hominins in terms of their cranial morphology (Dean et al., 1998). Nevertheless, the incipient occipital bun, bilateral occipital torus, and developed suprainiac fossa in Reilingen are more derived than the Atapuerca (SH) hominins and Steinheim. Although the dating is uncertain, both Steinheim and Reilingen probably date to between 200 and 300 kya (Dean et al., 1998; Prossinger et al., 2003). The Biache-Saint-Vaast 2 specimen is somewhat younger, dating to OIS 6 or 7 and probably around 200 kya (Guipert et al., 2011). The Abri Suard temporal bone dates to OIS stage 6 (Hublin, 1998) and probably falls between 130 and 150 kya. Both of these latter specimens have been suggested to largely show the fully developed Neandertal cranial morphology. All of these European middle Pleistocene specimens show the derived pattern of relative canal proportions, but only Reilingen showed a low placed posterior canal and inclined facial canal. Steinheim most closely resembles the Atapuerca (SH) sample in the lack of these derived features, while Abri Suard is somewhat intermediate in the inclination of the facial canal. In the cochlea, Reilingen shows a low shape index, similar to the Atapuerca (SH) mean value, while both Steinheim and Abri Suard are more similar to Neandertals. This might suggest that the full suite of Neandertal features in the bony labyrinth did not emerge in Europe until <200 kya. 5. Conclusion

4.4. Bony labyrinth morphology in the Neandertal clade The expanded samples in the present study now make it possible to propose phylogenetic polarities for a number of features of the hominin bony labyrinth. Specifically, a relatively wide shape of the lateral canal seems to represent a primitive feature within the genus Homo. Related to this, a narrower lateral canal would be a shared derived feature in the Neandertal clade and fossil and recent H. sapiens. No significant differences were found between the Atapuerca (SH) hominins and Neandertals in any of the canal variables, suggesting they share a similar pattern of size and shape, including a relatively small posterior canal and a relatively large lateral canal. Since the non-SH European middle Pleistocene specimens also show this morphology, the entire Neandertal clade seems to be characterized by a derived pattern of semicircular canal proportions within the genus Homo. The relative proportions of the semicircular canals are one of the few derived Neandertal features in the Atapuerca (SH) crania. This feature joins the shallow glenoid fossa and a suite of features in the face, mandible, and dentition that are Neandertal-like, while other cranial features show an incipient state of formation (e.g., suprainiac fossa) or remain primitive (e.g., projecting mastoid processes; Martínez and Arsuaga, 1997; Arsuaga et al., 2014).

The present study has benefitted from the largest dataset of Pleistocene Homo specimens to date to study the evolution of the bony labyrinth in the genus Homo. The results have confirmed the presence of a derived pattern of semicircular canal proportions that characterized the entire Neandertal clade, including the Atapuerca (SH) hominins. However, a functional interpretation of this derived pattern of canal proportions remains elusive. Differences within the Neandertal clade include the emergence of some potentially derived features in the bony labyrinth in Neandertals, including a low placement of the posterior canal and more vertical inclination of the ampullar line and facial canal. Although not fully resolved, the emergence of these features may be due to some combination of a large brain size, an archaic pattern of brain allometry, and a wide cranial base. The phylogenetic polarity of the cochlear shape index in the Atapuerca (SH) hominins is currently less clear, but the low shape index, reflecting a reduction in cochlear height, may be a derived feature. Regardless, the height of the cochlear basal turn increased within the Neandertal clade. Additional findings include a possibly shared derived feature, a relatively narrow lateral canal, in modern humans and the Neandertal clade. Nevertheless, additional data on lower and middle Pleistocene specimens from Africa and Asia are necessary to more firmly establish the phylogenetic

14

R. Quam et al. / Journal of Human Evolution 90 (2016) 1e15

polarities of some bony labyrinth features proposed in the present study. Acknowledgments We wish to thank the Atapuerca excavation team, especially that of the Sima de los Huesos (A. Aramburu, A. Esquivel, N. García, N. Sala, and J. Trueba), for their work in the field. Thanks also to L.
lez, E. Santos, and J.M. Carretero in the Rodríguez, R. García Gonza
n Humana at the Universidad de Burgos for Laboratorio de Evolucio their help with the CT scanning. We thank I. Tattersall and G. García for access to the collections at the American Museum of Natural History and to J. Laitman for help with the CT scanning of these
gico individuals at the Mt. Sinai Hospital. The Grupo Espeleolo Edelweiss also provided essential assistance in the field. Access to several Homo sapiens specimens was made possible by EVAN, €t Leipzig, through the NESPOS Anatomisches Institut, Universita
llez has a Contract-Grant platform (www.nespos.org). A. Gracia-Te
n y Cajal Program, RYC-2010-408 06152. Portions from the Ramo
n of this work were funded by the Ministerio de Ciencia e Innovacio of the Government of Spain (Project No. GL2012-38434-C03-01/
n (Project No. BU005A09), the AGAUR 03), the Junta de Castilla y Leo Project (2014-SGR-899), and Binghamton University (SUNY). Appendix A. Supplementary Online Material Supplementary online material related to this article can be found at http://dx.doi.org/10.1016/j.jhevol.2015.09.007. References Arsuaga, J.L., Martínez, I., Gracia, A., Carretero, J.M., Carbonell, E., 1993. Three new human skulls from the Sima de los Huesos site in Sierra de Atapuerca, Spain. Nature 362, 534e537. Arsuaga, J.L., Martínez, I., Gracia, A., Lorenzo, C., 1997. The Sima de los Huesos crania (Sierra de Atapuerca, Spain). A comparative study. J. Hum. Evol. 33, 219e282. Arsuaga, J.L., Lorenzo, C., Carretero, J.M., Gracia, A., Martínez, I., García, N., Bermúdez de Castro, J., Carbonell, E., 1999. A complete human pelvis from the Middle Pleistocene of Spain. Nature 399, 255e258.
llez, A., Sharp, W., Arsuaga, J.L., Martínez, I., Arnold, L., Aranburu, A., Gracia-Te res, C., Pantoja-Pe
rez, A., Bischoff, J., Poza-Rey, E., Pare
s, J., Quam, R., Falgue
n-Torres, M., García, N., Carretero, J., Demuro, M., Lorenzo, C., Sala, N., Martino
zar de Velasco, A., Cuenca-Besco
s, G., Go
mez-Olivencia, A., Moreno, D., Alca Pablos, A., Shen, C., Rodríguez, L., Ortega, A., García, R., Bonmatí, A., Bermúdez de Castro, J., Carbonell, E., 2014. Neandertal roots: Cranial and chronological evidence from Sima de los Huesos. Science 344, 1358e1363. Bouchneb, L., Crevecoeur, I., 2009. The inner ear of Nazlet Khater 2 (Upper Paleolithic, Egypt). J. Hum. Evol. 56, 257e262. Braga, J., Thackeray, J.F., Dumoncel, J., Descouens, D., Bruxelles, L., Loubes, J.-M., Kahn, J.-L., Stampanoni, M., Bam, L., Hoffman, J., de Beer, F., Spoor, F., 2013. A new partial temporal bone of a juvenile hominin from the site of Kromdraai B (South Africa). J. Hum. Evol. 65, 447e456. Bramble, D.M., Lieberman, D.E., 2004. Endurance running and the evolution of Homo. Nature 432, 345e352. Bruner, E., Manzi, G., Arsuaga, J., 2003. Encephalization and allometric trajectories in the genus Homo: Evidence from the Neandertal and modern lineages. Proc. Nat. Acad. Sci. 100, 15335e15340.
mezCarretero, J.-M., Rodríguez, L., García-Gonz
alez, R., Arsuaga, J.-L., Go Olivencia, A., Lorenzo, C., Bonmatí, A., Gracia, A., Martínez, I., Quam, R., 2012. Stature estimation from complete long bones in the Middle Pleistocene humans from the Sima de los Huesos, Sierra de Atapuerca (Spain). J. Hum. Evol. 62, 242e255. Dean, D., Hublin, J., Holloway, R., Ziegler, R., 1998. On the phylogenetic position of the pre-Neandertal specimen from Reilingen, Germany. J. Hum. Evol. 34, 485e508. Gilbert, W., Holloway, R., Kubo, D., Kono, R., Suwa, G., 2008. Tomographic analysis of the Daka calvaria. In: Gilbert, W., Asfaw, B. (Eds.), Homo erectus. Pleistocene evidence from the Middle Awash, Ethiopia. University of California Press, Berkeley, pp. 329e348. Glantz, M., Viola, B., Wrinn, P., Chikisheva, T., Derevianko, A., Krivoshapkin, A., Islamov, U., Suleimanov, R., Ritzmann, T., 2008. New hominin remains from Uzbekistan. J. Hum. Evol. 55, 223e237.
mez-Olivencia, A., Been, E., Arsuaga, J.L., Stock, J.T., 2013. The Neandertal verteGo bral column 1: The cervical spine. J. Hum. Evol. 64, 608e630.


mez-Olivencia, A., Crevecoeur, I., Balzeau, A., 2015. La Ferrassie 8 Neandertal Go child reloaded: New remains and re-assessment of the original collection. J. Hum. Evol. 82, 107e126. Gracia, A., Arsuaga, J., Martínez, I., Lorenzo, C., Carretero, J., Bermúdez de Castro, J., Carbonell, E., 2009. Craniosynostosis in the Middle Pleistocene human Cranium 14 from the Sima de los Huesos, Atapuerca, Spain. Proc. Nat. Acad. Sci. 106, 6573e6578. Guipert, G., de Lumley, M.-A., Tuffreau, A., Mafart, B., 2011. A late Middle Pleistocene hominid: Biache-Saint-Vaast 2, north France. C. R. Palevol. 10 (1), 21e33. Gunz, P., Spoor, F., Tilgner, R., Hublin, J.-J., 2009. The Neanderthal bony labyrinth reconsidered, introducing a new geometric morphometric approach (abstract). Am. J. Phys. Anthropol. 138 (S48), 142. Gunz, P., Stoessel, A., Neubauer, S., Kuhrig, M., Hoyka, M., Hublin, J.-J., Spoor, F., 2013. Morphological integration of the bony labyrinth and the cranial base in modern humans and Neandertals (abstract). Europ. Soc. Hum. Evol. 2013, 104. Heim, J.L., 1976. Les Hommes Fossiles de La Ferrassie. Tome I. Masson, Paris. Hill, C.A., Radov ci
c, J., Frayer, D.W., 2014. Brief communication: Investigation of the semicircular canal variation in the Krapina Neandertals. Am. J. Phys. Anthropol. 154, 302e306. Holloway, R., Broadfield, D., Yuan, M., 2004. The Human Fossil Record. Volume 3. Brain Endocasts. The Paleoneurological Evidence. Wiley-Liss, New York. Hublin, J.J., 1998. Climatic changes, paleogeography, and the evolution of the Neandertals. In: Akazawa, T., Aoki, K., Bar-Yosef, O. (Eds.), Neandertals and Modern Humans in Western Asia. Plenum Press, New York, pp. 295e310. Hublin, J.J., Spoor, F., Braun, M., Zonneveld, F., Condemi, S., 1996. A late Neanderthal associated with Upper Paleolithic artefacts. Nature 381, 224e226.
n, M.P., Tafforeau, P., Zollikofer, C., 2010. Deep evolutionary roots Lebrun, R., De Leo of strepsirrhine primate labyrinthine morphology. J. Anat. 216, 368e380. Levin, J., Fox, J., Forde, D., 2010. Elementary Statistics in Social Research, Eleventh Edition. Pearson Education, Boston. Lorenzo, C., Quam, R., Martinez, I., Gracia, A., Arsuaga, J., 2011. The bony labyrinth of the Middle Pleistocene Sima de los Huesos hominids (Sierra de Atapuerca, Spain). Paleoanthropol. 2011, 22 (Abstract). Malinzak, M.D., Kay, R.F., Hullar, T.E., 2012. Locomotor head movements and semicircular canal morphology in primates. Proc. Nat. Acad. Sci. 109, 17914e17919. Martínez, I., Arsuaga, J.L., 1997. The temporal bones from Sima de los Huesos Middle Pleistocene site (Sierra de Atapuerca, Spain). A phylogenetic approach. J. Hum. Evol. 33, 283e318. Martínez, I., Rosa, M., Arsuaga, J., Jarabo, P., Quam, R., Lorenzo, C., Gracia, A., Carretero, J., Bermúdez de Castro, J., Carbonell, E., 2004. Auditory capacities in Middle Pleistocene humans from the Sierra de Atapuerca in Spain. Proc. Nat. Acad. Sci. 101, 9976e9981. Martínez, I., Quam, R., Arsuaga, J., 2008. Evolutionary trends in the temporal bone in the Neandertal lineage: a comparative study between the Sima de los Huesos (Sierra de Atapuerca) and Krapina samples. In: Monge, J., Mann, A., Frayer, D., Radov ci
c, J. (Eds.), New Insights on the Krapina Neandertals: 100 years after Gorjanovi
c-Kramberger. Croatian Natural History Museum, Zagreb, pp. 75e80.
mez-Olivencia, A., Martínez, I., Rosa, M., Quam, R., Jarabo, P., Lorenzo, C., Bonmatí, A., Go Gracia, A., Arsuaga, J., 2013. Communicative capacities in Middle Pleistocene humans from the Sierra de Atapuerca in Spain. Quat. Int. 295, 94e101.
llez, A., Arsuaga, J.L., 2014. Pablos, A., Martínez, I., Lorenzo, C., Sala, N., Gracia-Te Human calcanei from the Middle Pleistocene site of Sima de los Huesos (Sierra de Atapuerca, Burgos, Spain). J. Hum. Evol. 76, 63e76.
n, M., Zollikofer, C., 2010. The labyrinthine morphology. In: Dobos¸, A., Ponce De Leo Soficaru, A., Trinkaus, E. (Eds.), The Prehistory and Paleontology of the Pes¸tera ge, Lie ge, pp. 96e97. Muierii, Romania. Etud Rech Archeol Univ Lie
n, M., Zollikofer, C., 2013. The internal cranial morphology of Oase 2. Ponce De Leo ~o, J. (Eds.), Life and Death at the Pes¸tera cu In: Trinkaus, E., Constantin, S., Zilha Oase. A Setting for Modern Human Emergence in Europe. Oxford University Press, New York, pp. 332e347. Prossinger, H., Seidler, H., Wicke, L., Weaver, D., Recheis, W., Stringer, C., Müller, G.B., 2003. Electronic removal of encrustations inside the Steinheim cranium reveals paranasal sinus features and deformations, and provides a revised endocranial volume estimate. Anat. Rec. Part B 273, 132e142. Quam, R., Rak, Y., 2008. Auditory ossicles from southwest Asian Mousterian sites. J. Hum. Evol. 54, 414e433. Quam, R., Martinez, I., Arsuaga, J.L., 2006. Middle Pleistocene auditory ossicles from the Sierra de Atapuerca (Spain). Am. J. Phys. Anthropol. 42 (Supp.), 149 (abstract). Quam, R., Martínez, I., Lorenzo, C., Bonmatí, A., Rosa, M., Jarabo, P., Arsuaga, J., 2012. Studying audition in fossil hominins: A new approach to the evolution of language? In: Jackson, M. (Ed.), Psychology of Language. Nova Science Publishers, Inc., Hauppage, pp. 47e95. Quam, R., De Ruiter, D., Masali, M., Arsuaga, J., Martínez, I., Moggi-Cecchi, J., 2013a. Early hominin auditory ossicles from South Africa. Proc. Nat. Acad. Sci. 110, 8847e8851. Quam, R., Martínez, I., Arsuaga, J.L., 2013b. Reassessment of the La Ferrassie 3 Neandertal ossicular chain. J. Hum. Evol. 64, 250e262. Quam, R.M., Coleman, M.N., Martínez, I., 2014. Evolution of the auditory ossicles in extant hominids: metric variation in African apes and humans. J. Anat. 225, 167e196. Raichlen, D.A., Armstrong, H., Lieberman, D.E., 2011. Calcaneus length determines running economy: implications for endurance running performance in modern humans and Neandertals. J. Hum. Evol. 60 (3), 299e308.

R. Quam et al. / Journal of Human Evolution 90 (2016) 1e15 Robles, L., Ruggero, M., 2001. Mechanics of the mammalian cochlea. Physiol. Rev. 81 (3), 1305e1352. € hler, M., Moy
Rook, L., Bondioli, L., Casali, F., Rossi, M., Ko a-Sol
a, S., Macchiarelli, R., 2004. The bony labyrinth of Oreopithecus bambolii. J. Hum. Evol. 46, 347e354. Ruff, C.B., Trinkaus, E., Holliday, T.W., 1997. Body mass and encephalization in Pleistocene Homo. Nature 387, 173e176. Scheuer, L., Black, S., 2000. Developmental Juvenile Osteology. Academic Press, San Diego. Silcox, M.T., Bloch, J.I., Boyer, D.M., Godinot, M., Ryan, T.M., Spoor, F., Walker, A., 2009. Semicircular canal system in early primates. J. Hum. Evol. 56, 315e327. Smith, R.J., Jungers, W.L., 1997. Body mass in comparative primatology. J. Hum. Evol. 32 (6), 523e559. Spoor, F., 1993. The comparative morphology and phylogeny of the human bony labyrinth. Utrecht University, Utrecht. Spoor, F., 2003. The semicircular canal system and locomotor behaviour, with special reference to hominin evolution. Courier-Forschunginstitut Senckenberg 243, 93e104. ~o Silva, F., Pacheco Dias, R., 2002. The bony labyrinth of Spoor, F., Esteves, F., Tecela Lagar Velho 1. In: Portrait of the Artist as a Child. The Gravettian human skeleton from the Abrigo do Lagar Velho and its archaeological context, pp. 287e292.

15

Spoor, F., Zonneveld, F., 1995. Morphometry of the primate bony labyrinth: a new method based on high-resolution computed tomography. J. Anat. 186, 271e286. Spoor, F., Zonneveld, F., 1998. Comparative review of the human bony labyrinth. Yrbk. Phys. Anthropol. 41, 211e252. Spoor, F., Wood, B., Zonneveld, F., 1994. Implications of early hominid labyrinthine morphology for the evolution of human bipedal locomotion. Nature 369, 645e648. Spoor, F., Hublin, J., Braun, M., Zonneveld, F., 2003. The bony labyrinth of Neanderthals. J. Hum. Evol. 44, 141e165. Spoor, F., Garland Jr., T., Krovitz, G., Ryan, T., Silcox, M., Walker, A., 2007. The primate semicircular canal system and locomotion. Proc. Nat. Acad. Sci. 104, 10808e10812. Steudel-Numbers, K.L., Tilkens, M.J., 2004. The effect of lower limb length on the energetic cost of locomotion: implications for fossil hominins. J. Hum. Evol. 47, 95e109. Weaver, A.H., 2005. Reciprocal evolution of the cerebellum and neocortex in fossil humans. Proc. Nat. Acad. Sci. 102, 3576e3580. Wu, X.-J., Crevecoeur, I., Liu, W., Xing, S., Trinkaus, E., 2014. Temporal labyrinths of eastern Eurasian Pleistocene humans. Proc. Nat. Acad. Sci. 111, 10509e10513. Zonneveld, F., Wind, J., 1985. High resolution computed tomography of fossil hominid skulls: a new method and some results. In: Tobias, P. (Ed.), Hominid Evolution: Past, Present and Future. Alan R. Liss, Inc., New York, pp. 427e436.