Journal of Human Evolution 148 (2020) 102887

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Journal of Human Evolution

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Short Communications The cochlea of the Aroeira 3 Middle craniumda comparative study

* Mercedes Conde-Valverde a, , Ignacio Martínez a, Rolf Quam a, b, c, d, Juan-Luis Arsuaga a, c, e, Joan Daura f, g, Montserrat Sanz f, g,Joao~ Zilhao~ g, h, i a Catedra de Bioacústica Evolutiva y Paleoantropología (HM Hospitales e Universidad de Alcala), Area de Antropología Física, Departamento de Ciencias de la Vida, Universidad de Alcala, 28871 Alcala de Henares, Madrid, Spain b Department of Anthropology, Binghamton University (SUNY) Binghamton, NY, 13902-6000, USA c Centro Mixto (UCM-ISCIII) de Evolucion y Comportamiento Humanos, Av. Monforte de Lemos 5, 28029, Madrid, Spain d Division of Anthropology, American Museum of Natural History, Central Park West-79th St., New York, NY, 10024, USA e Departamento de Geodinamica, Estratigrafía y Paleontología, Facultad de Ciencias Geologicas, Universidad Complutense de Madrid, 28040, Madrid, Spain f Grup de Recerca del Quaternari (GRQ)-SERP, Departament d'Historia i Arqueologia, C/ Montalegre 6-8, 08001 Barcelona, Spain g UNIARQ-Centro de Arqueologia da Universidade de Lisboa, Faculdade de Letras, Universidade de Lisboa, Alameda da Universidades, 1600-214, Lisbon, Portugal h Department d’Historia i Arqueologia, Universitat de Barcelona, 08007, Barcelona, Spain i Institucio Catalana de Recerca i Estudis Avançats (ICREA), Passeig Lluís Companys 23, 08010, Barcelona, Spain article info

Article history: characteristic of the Neandertals; (2) a number of fossils dated to Received 9 April 2020 the middle portion of the Middle Pleistocene, including the Accepted 10 September 2020 Atapuerca-Sima de los Huesos (SH) fossils, Swanscombe, Stein- Available online xxx heim, and Reilingen, which show many primitive features, along with some derived Neandertal characteristics; and (3) a group of Keywords: fossils that includes those from the sites of Mauer, Arago, and Inner ear Cochlear evolution Ceprano, which are also dated to the middle portion of the Middle Homo Pleistocene, but show few, if any, clear Neandertal features. Daura Middle Pleistocene et al. (2017) included the Aroeira 3 cranium in the second group. Gruta da Aroeira In particular, the morphology of the glabellar region and the large, triangular postglenoid process were argued to be similar to those of the SH hominins, Steinheim, and Petralona. The preservation of the complete right temporal bone in Aroeira 3 has also allowed for the bony labyrinth to be virtually reconstructed and studied (Conde- Valverde et al., 2018). The bony labyrinth can be divided into three distinct regions: 1. Introduction the semicircular canals, the cochlea, and the vestibule, which joins these two regions together. The semicircular canals perceive head The partial adult cranium Aroeira 3 was discovered in 2014 in movement in three spatial directions, and the cochlea houses the the Gruta da Aroeira, in the Portuguese municipality of Torres organ of Corti, which is responsible for the perception of different Novas and has been dated by means of UeTh disequilibrium to sounds. Jeffery and Spoor (2004) studied changes in the bony lab- between 389 and 436 ka (Daura et al., 2017), making it one of the yrinth during prenatal development and found that adult size is best dated European Middle Pleistocene crania known so far. Cur- achieved during weeks 17e19 of gestation. At the same time, these rent models of Middle Pleistocene human evolution in Europe posit authors suggested the possibility of changes occurring throughout the existence of three distinct hominin groups (Arsuaga et al., 2014; ontogeny. This suggestion has been confirmed by Lyu et al. (2016), Daura et al., 2017): (1) the specimens from some late Middle who found differences in the orientation of the semicircular canals, Pleistocene sites such as Ehringsdorf, La Chaise, or Biache-Saint- and by McRackan et al. (2012), who reported changes in the Vaast, which show most of the derived features often considered orientation of the cochlea with respect to the outer and middle ear, throughout growth and development. Several studies have also discussed the question of sexual dimorphism in the cochlea. A * Corresponding author. meta-analysis by Miller (2007) examined 11 studies, including 109 E-mail address: [email protected] (M. Conde-Valverde). https://doi.org/10.1016/j.jhevol.2020.102887 0047-2484/© 2020 Elsevier Ltd. All rights reserved. M. Conde-Valverde, I. Martínez, R. Quam et al. Journal of Human Evolution 148 (2020) 102887 males and 57 females, and found only a single study (Sato et al., The earlier study of the inner ear in Aroeira 3 shows this indi- 1991) which reported significant differences between the sexes in vidual had a largely primitive bony labyrinth, similar to earlier cochlear length. This anomalous result was attributed to the small members of the genus Homo, and lacking the derived Neandertal sample size (6 males and 7 females) used in the Sato et al. (1991) condition in the semicircular canal proportions present in SH study, and Miller (2007) concluded that the cochlea does not (Conde-Valverde et al., 2018). Interestingly, Aroeira 3 shares with show sex differences. More recently, Osipov et al. (2013) analyzed SH a low value of the index of the basal turn of the cochlea, which linear measurements of the bony labyrinth defined by Spoor (1993) was interpreted as evidence for the existence of an Iberian paleo- in 49 males and 45 females. While they found some degree of deme from Marine Isotope Stages 12e11 (Conde-Valverde et al., sexual dimorphism in the semicircular canal dimensions, none of 2018). Although that study only included two variables of the co- the cochlear dimensions examined showed significant differences chlea, the results revealed the significant potential of the cochlea in between males and females. In a more recent study, using the same studies of Middle Pleistocene populations. Thus, a more detailed variables in a sample of 48 females and 50 males representing three analysis of the cochlear dimensions is warranted. We have relied on different populations, Uhl et al. (2020) again found sexual dimor- the 3D reconstruction published in Conde-Valverde et al. (2018), phism in the canals in all three populations (German, Zulu, and and we have measured 12 new cochlear variables compared with Oneota), but the cochlea was sexually dimorphic only in the Oneota that previous study. We have also carried out a new analysis sample. Most recently, however, Braga et al. (2019) demonstrated designed to compare the general proportions of the cochlea in sex-based differences in the torsion of the cochlea in a sample of 50 Aroeira 3 with the SH hominins, Neandertals, recent humans, and females and 44 males. Taken together, these studies indicate the chimpanzees. Our objective is to obtain new information and a importance of considering potential effects of ontogeny and sexual better understanding of the place of this specimen within the dimorphism in studies of taxonomy and phylogeny in hominin context of Middle Pleistocene human evolution in Europe. Given fossils. the close geographic proximity and similar chronology with the SH Within the bony labyrinth, studies of the semicircular canals have fossils, as well as the previously reported similarities in cochlear provided important data and insights into the taxonomy and phy- morphology, we hypothesize Aroeira 3 to show similar cochlear logeny of fossil hominins (Spoor, 1993; Hublin et al., 1996; Spoor dimensions and proportions to the SH fossils and lack the derived et al., 2003; Bouchneb and Crevecoeur, 2009; Gunz et al., 2013; features present in the cochlea of Neandertals and modern humans. Hill et al., 2014; Quam et al., 2016; Li et al., 2017). In general, these studies have shown that the size and proportions of the semicircular 2. Materials and methods canals in living humans are similar to those in Early Pleistocene Homo fossil specimens, suggesting the bony labyrinth morphology We have used the 3D reconstructions published by Conde- in modern humans is largely primitive. At the same time, the Valverde et al. (2018) for Aroeira 3 and those published by semicircular canals in Neandertals show a derived morphology, with Conde-Valverde et al. (2019) for the comparative samples. Tech- absolutely and relatively small anterior and posterior canals and a nical data for the mCT scanning and virtual reconstructions can be larger lateral canal (Hublin et al., 1996; Spoor et al., 2003). The Ne- found in those studies (Conde-Valverde et al., 2019: Table S1). The andertals also show a relatively low placement of the posterior canal, cochlea in Aroeira 3 has been compared with a sample of relative to the plane of the lateral canal (Hublin et al., 1996; Spoor P. troglodytes where we have estimated the sex, one of recent et al., 2003). Interestingly, the absolute and relative sizes of the humans of unknown sex, and two fossil samples. The P. troglodytes semicircular canals in the SH hominins show the derived Neandertal sample includes 10 adult individuals (4 females, 4 males, and 2 of pattern (Quam et al., 2016). Despite being centered on the semi- unknown sex) from the Estacion Biologica de Donana~ (Sevilla, circular canals morphology, these studies also included two vari- Spain). Sex was estimated based on well-known sexual differences ables (cochlear height and width) which allowed to calculate the in the canine size and projection (Dean and Beynon, 1991). The shape index of the cochlear basal turn (COh/w; Spoor, 1993). A low recent humans sample includes 10 adults of unknown sex, 9 of value of this index was considered a population-specificfeatureof them from the mass grave in the Cementerio San Jose (Burgos, the SH hominins (Quam et al., 2016). Spain) and one from the cemetery of Sepulveda (Segovia, Spain). Several recent studies have focused more specifically on the The SH hominin sample includes 6 adult individuals (Cr.4, 7, 8, 12, cochlea and have defined a number of new measurements to 13, and 15; Arsuaga et al., 2014) and 4 subadult individuals (Cr.3, quantify its shape. Some of these studies have found that the AT-421, AT-643, AT-1907; Martínez and Arsuaga, 1997, Martínez cochlear morphology in fossil hominins contains important taxo- et al., 2004). Based on differences in cranial capacity, Poza-Rey nomic and phylogenetic information to differentiate between Af- et al. (2019) assigned Cr.7 and Cr.12 to female individuals and rican apes, Australopithecus africanus, Paranthropus robustus, and Cr.3, Cr.4, Cr.8, Cr.13 and Cr.15 to male individuals. Finally, the early Homo specimens (Braga et al., 2013, 2015, 2017; Beaudet et al., Neandertal sample includes 7 individuals: Amud 1, considered as 2019). In particular, the length of the external border of the cochlea an adult male (Endo and Kimura, 1970); La Chapelle-aux-Saints 1, has been argued to be proportionally longer in the genus Homo attributed to an adult male (Boule, 1911); La Quina H5, considered than in early hominins. At the same time, Beals et al. (2016) found as an adult female (Martin, 1923); La Ferrassie 1, assigned to an that the cochlear volume in the Krapina Neandertals was similar to adult male; La Ferrassie 2, assigned to an adult female (Heim, 1976); that of modern humans but larger than in gorillas and chimpan- La Ferrassie 8, considered a 23 month old individual (Heim, 1982); zees. Most recently, Conde-Valverde et al. (2019) carried out a and Kebara 1, attributed to a 7 month old child (Tillier et al., 2003). detailed study of the cochleae in the SH hominins and defined a The sex assignments for the adult Neandertal specimens include new measurement protocol. That study found that the cochlea in postcranial traits that are considered dimorphic in modern humans the SH fossils shows a mosaic pattern, with some primitive features and represent consensus sex designations. shared with Pan troglodytes, together with other derived features All the cochlear measurements were taken on the 3D model shared with recent humans and Neandertals. That same study using Mimics© v. 18 (Materialise, Leuven, Belgium). We have used found several homoplasies in the cochlear morphology between the same landmarks and standard planes as defined by Conde- recent humans and Neandertals and a derived pattern of cochlear Valverde et al. (2019), and we have measured the following vari- proportions, with a relatively long 1st turn and a very short 3rd turn ables (Fig. 1): length of the 1st turn (L1); length of the 2nd turn (L2); in the latter. length of the 3rd turn (L3); angle of the 3rd turn (A3); number of

2 M. Conde-Valverde, I. Martínez, R. Quam et al. Journal of Human Evolution 148 (2020) 102887

Figure 1. Measurements on the 3D model of the Aroeira 3 cochlea in inferior (a) and lateral (b, c) views. The definition and position of landmarks and standard planes established for measuring the cochlea as in Conde-Valverde et al. (2019). Landmarks: 1 ¼ most lateral point of the round window; 2 ¼ placed at the maximum distance from landmark 1 along the external edge of the basal turn; 3 ¼ midpoint of the basal turn placed on the external edge of the basal turn along the line that joins landmarks 1 and 2; 4 ¼ center point of the cochlea; 5 ¼ apex of the cochlea. Variables: L1 ¼ length of the first turn; L2 ¼ length of the second turn measured; L3 ¼ length of the third turn; A3 ¼ angle of the 3rd turn, used to establish the number of turns (NTs); Sw ¼ width of the cross-section of the1st turn; Sh ¼ height of the cross-section of the 1st turn; ABT ¼ cross-sectional area of the 1st turn. turns (NTs), calculated as number of complete turns þ (A3/360); probabilities for group membership in four defined groups: chim- area of the 1st (basal) turn (ABT); width of the cross-sectional area panzees, recent humans, SH, and Neandertals. All statistical ana- of the 1st turn (Sw); height of the cross-sectional area of the 1st lyses were carried out using the Statistica v. 10 software package. turn (Sh); shape index of the cross-section of the 1st turn (Sw/Sh); cochlear volume (VOL); cochlear thickness (CTh). 3. Results A principal component analysis (PCA) was carried out on the correlation matrix of the variables. To avoid potential effects All measurements of the cochlea in Aroeira 3 are shown in because of size differences, we have used the log-shape trans- Table 1. Most of the values in Aroeira 3 are within one standard formation (Mosimann, 1970; Claude, 2013) for raw variables: L1, L2, deviation (SD) from the P. troglodytes mean, with the exceptions of L3, Sw, Sh, the square root of ABT, the cube root of VOL, and CTh. We NT and CTh, which fall outside the chimpanzee range of variation calculated the geometric mean of all the variables for each indi- and are 2.3 SD below and 2.5 SD above the mean, respectively. vidual and divided each variable by the geometric mean to obtain Compared with the recent human sample, only Sh and Sw/Sh in shape variables. We then calculated the log10 of each of the shape Aroeira 3 fall outside of the range of variation and far from the 0 0 0 variables and included these new variables (labeled as: L1 ,L2,L3, mean (2.1 SD and 3.1 SD, respectively). Aroeira 3 shows values in 3 0 0 Sw’,Sh’, ABT , VOL and CTh’), along with the raw values for NT, in variables that fall near the limit of the Neandertal range of varia- the PCA. A canonical variate analysis (CVA) was also carried out tion, L3 (1.8 SD), NT (1.5 SD), and Sh (1.8 SD), and one variable using the same set of variables for the PCA, assuming equal prior which is outside of the Neandertal range, Sw/Sh (3.9 SD). Finally,

Table 1 Cochlear measurements of Aroeira 3 and comparative samples.

Samples L1 (mm) L2 (mm) L3 (mm) NT Sw (mm) Sh (mm) ABT (mm2) Sw/Sh VOL (mm3) CTh (mm)

Aroeira 3 22.0 12.8 6.8 2.58 1.83 2.26 2.8 0.81 65.0 2.3 P. troglodytes mean ± SD 21.7 ± 1.5 12.1 ± 1.0 6.5 ± 1.2 2.80 ± 0.10 1.69 ± 0.18 2.18 ± 0.13 2.9 ± 0.4 0.78 ± 0.08 59.8 ± 10.3 1.9 ± 0.2 P. troglodytes range (n ¼ 10) 18.8e23.9 10.0e13.1 4.9 e 8.6 2.62 e 2.93 1.50 e 2.00 1.96 e 2.43 2.3 e 3.5 0.66 e 0.95 47.5 e 83.1 1.6 e 2.1 Recent humans mean ± SD 23.5 ± 1.6 12.5 ± 0.8 5.3 ± 1.2 2.55 ± 0.16 1.77 ± 0.16 2.56 ± 0.14 3.6 ± 0.5 0.69 ± 0.04 73.3 ± 10.0 2.4 ± 0.3 Recent humans range (n ¼ 10) 21.2e26.5 11.5e13.5 3.6 e 7.0 2.33 e 2.87 1.50 e 2.05 2.28 e 2.70 2.7 e 4.3 0.64 e 0.77 60.8 e 91.9 2.1 e 3.0 Neandertals mean ± SD 24.1 ± 1.7 13.0 ± 1.0 3.9 ± 1.7 2.37 ± 0.14 1.84 ± 0.13 2.68 ± 0.23 3.6 ± 0.6 0.69 ± 0.03 78.5 ± 14.3 2.2 ± 0.4 Neandertals range (n ¼ 7) 21.6e26.8 11.3e14.2 2.0 e 6.8 2.18 e 2.59 1.67 e 2.07 2.27 e 2.90 2.7 e 4.4 0.65 e 0.74 54.7e102.0 1.7 e 2.8 SH mean ± SD 22.1 ± 1.0 12.2 ± 0.7 5.1 ± 1.1 2.53 ± 0.16 1.72 ± 0.15 2.31 ± 0.21 3.1 ± 0.5 0.74 ± 0.04 60.3 ± 9.3 2.0 ± 0.3 SH range (n ¼ 10) 20.5e23.6 10.9e13.2 3.0 e 6.6 2.25 e 2.81 1.41 e 1.94 1.75 e 2.46 1.9 e 3.7 0.71 e 0.81 44.9 e 71.6 1.7 e 2.4

Abbreviations: L1 ¼ length of the 1st turn; L2 ¼ length of the 2nd turn; L3 ¼ length of the 3rd turn; NT ¼ number of turns; Sw ¼ width of the cross-sectional area of the first turn; Sh ¼ height of the cross-sectional area of the first turn; ABT ¼ area of the 1st turn; Sw/Sh ¼ shape index of the cross-section; VOL ¼ cochlear volume; CTh ¼ cochlear thickness.

3 M. Conde-Valverde, I. Martínez, R. Quam et al. Journal of Human Evolution 148 (2020) 102887

Table 2 of the third turn, the higher NT, the smaller size and more rounded a Results of the principal components analysis. shape of the cross section of the first turn and the small cochlear Variables PC1 PC2 volume, whereas their low values in the cochlear thickness explain

% total variance 57.80 15.98 their low values in PC2. Within the chimpanzees, although there is Eigenvalue 5.20 1.44 no clear difference in the placement of males and females, it seems L10 0.775 0.088 that there is a tendency for males to fall toward the negative ends of 0 L2 0.555 0.394 the PCs and the females toward the positive ends. Nevertheless, a 0 ¡ L3 0.963 0.224 larger sample size would be necessary to reveal any clear pattern of NT ¡0.876 0.223 Sw’ 0.703 0.450 separation between males and females. Sh’ 0.811 0.354 The recent human ellipse overlaps with those of Neandertals ABT0 0.818 0.010 and SH. Along PC1, the sample is split, with half showing positive 0 VOL 0.880 0.148 values and half showing negative values. Along PC2, all specimens CTh’ 0.029 0.908 show positive values because of the high values in the CTh. Abbreviations: L1’ ¼ log-shape of the length of the 1st turn; L2’ ¼ log-shape of the The SH equiprobability ellipse is the only one that overlaps with ’ ¼ ¼ length of the 2nd turn; L3 log-shape of the length of the 3rd turn; NT number of those of all the other groups but falls toward lower values along PC2 turns; Sw’ ¼ log-shape of the width of the cross-sectional area of the first turn; Sh’ ¼ log-shape of the height of the cross-sectional area of the first turn; ABT’ ¼ log- compared with the modern human and Neandertal ellipses, shape of the squared root of area of the 1st turn; VOL’ ¼ log-shape of the cube root of reflecting generally lower values for CTh. In the case of the SH cochlear volume; CTh’ ¼ log-shape of the cochlear thickness; PC ¼ principal hominins, there is no difference in the distribution of specimens component. assigned to males or females. The specimens that fall closest to a Factor loadings >0.7 in bold. Cr.12 (attributed to a female) are Cr.3 and Cr.4 (both attributed to males), whereas the specimens that fall closest to Cr.7 (attributed to the values for Aroeira 3 fall within the SH range, except for Sw/Sh a female) are Cr.15, Cr.13, and Cr.8 (all attributed to males). The (1.8 SD) and L3 (1.6 SD), which are at or slightly above the upper subadult SH individuals are dispersed and distant from one limit, respectively. another. AT-643 is close to the center of the SH equiprobability The PCA yielded only two principal components (PCs) with an ellipse, whereas the other two individuals fall outside of the SH eigenvalue >1, which together explain 73.79% of the total variance ellipse. AT-1907 and AT-421 show the highest values within the SH (Table 2). Variables showing a strong negative correlation with PC1 sample along PC1 and PC2, respectively, because of the low values include L30 and NT. Variables showing a strong positive correlation in the length of their third turn and in the NT in AT-1907 and the with PC1 include L10,Sw’,Sh’, ABT0, and VOL’. In PC2, only CTh’ high value of cochlear thickness in AT-421 (Conde-Valverde et al., shows a strong correlation which is positive. 2019: Table 3). A scatterplot of the individuals along PC1 and PC2 is shown in The Neandertal equiprobability ellipse only overlaps with those Figure 2. Most of the chimpanzees differ from the other samples in of recent humans and SH. Most of the Neandertal specimens showing negative values on both factors. Their low values in PC1 (except La Ferrassie 1 and 2) show high positive values along PC1, are because of the shorter length of the first turn, the longer length because of their lower values of the length of their third turn and

Figure 2. Scatterplot of the first 2 principal components (PC2 vs. PC1) of a PCA of log-shape variables. The 95% confidence ellipses are drawn around the group means for chimpanzees, the Sima de los Huesos (SH) fossils, Neandertals, and recent humans. Individual fossils: Aro3 ¼ Aroeira 3; LCh ¼ La Chapelle aux Saints; LF1 ¼ La Ferrassie 1; LF2 ¼ La Ferrassie 2; LF8 ¼ La Ferrassie 8; LQ5 ¼ La Quina H5; Kb1 ¼ Kebara 1; Am1 ¼ Amud 1.

4 M. Conde-Valverde, I. Martínez, R. Quam et al. Journal of Human Evolution 148 (2020) 102887

Table 3 Results of the canonical variate analysisa.

Group % Correctly classified Chimpanzees Recent humans SH Neandertals

Chimpanzees 100 10 0 0 0 Recent humans 80 0 8 1 1 SH 80 1 (Cr.12) 1 (AT-421) 8 0 Neandertals 71 0 2 (LF1, LF2) 0 5 Total 83.8

Classification Posterior probabilities

Aroeira 3 SH <0.001 0.22 0.77 0.01

Abbreviations: Cr. 12 ¼ Cranium 12; LF1 ¼ La Ferrassie 1; LF2 ¼ La Ferrassie 2. a Assumes equal prior probabilities of group membership. their low NT. There is no obvious difference in the distribution of of the variables used in the present study to discriminate taxo- males and females within the Neandertals, with La Ferrassie 2 nomically between groups. Regarding potential ontogenetic in- (attributed to a female) falling close to La Ferrassie 1 (attributed to a fluences on the cochlea, some differences were seen between adult male) and with La Quina H5 (attributed to a female) falling very and immature Neandertals, with the immature individuals (La close to La Chapelle-aux-Saints (attributed to a male). Interestingly, Ferrassie 8 and Kebara 1) showing less thick cochlea compared with the two infant Neandertal specimens fall very close to one another the adults. This difference is not seen in the SH sample, perhaps and are the only ones in the Neandertal sample to show negative because of the older age at death in the immature SH individuals. In values along PC2, primarily reflecting their low values of cochlear any event, both immature Neandertal individuals were correctly thickness (Conde-Valverde et al., 2019: Table 3), and this could classified in the CVA, indicating that potential ontogenetic factors perhaps be because of their young age at death. do not affect the ability of the variables used in this study to Finally, Aroeira 3 plots within the overlap between the equi- discriminate between groups. probability ellipses of chimpanzees and the SH hominins. Aroeira 3 The results of the present study agree with our initial hypothesis plots within the region of overlap between the equiprobability el- and with the work of Conde-Valverde et al. (2018), which suggested lipses of chimpanzees and the SH hominins. Aroeira 3 shows a a stronger affinity between the cochlea of Aroeira 3 and that of the strong negative value along PC1 compared with most other Homo SH hominins, than with Neandertals or recent humans. Neverthe- specimens because of the lower values of the length of the first less, the similarity found in the present study is mainly based on turn, the size of the cross-section of the first turn, and the cochlear primitive features, while that reported by Conde-Valverde et al. volume, which are similar to those seen in chimpanzees and the SH (2018) was based on a potentially derived feature relative to Ne- hominins (Table 1). The high value of the length of the third turn in andertals and recent humans (low value for the COh/w index). Aroeira 3 also explains its somewhat lower position along PC2, Thus, Aroeira 3 and the SH hominins show a similar cochlear despite showing a similar value of cochlear thickness as in recent morphology that includes primitive traits, along with a shared humans. derived trait that seems to characterize the Iberian paleodeme from The results of the CVA (Table 3) show that all of the chimpanzees MIS 12e11 (Conde-Valverde et al., 2018). Interestingly, while were correctly classified. In the case of the SH hominins, the only Aroeira 3 and the SH hominins show the same combination of adult specimen misclassified (Cr.12) has been assigned to a female, ancestral and derived features in the cochlea, the semicircular ca- but the other adult cranium attributed to a female (Cr.7) was nals in Aroeira 3 show the generalized morphology for the genus correctly classified. Only one of the immature SH individuals (AT- Homo (Conde-Valverde et al., 2018), in contrast to the SH sample 421) was incorrectly classified by the CVA, whereas the remaining which already shows the derived Neandertal pattern of canal pro- three immature individuals were all correctly classified. Among the portions (Quam et al., 2016). This condition reveals a pattern of Neandertals, the two specimens misclassified as recent humans (La mosaic evolution in the inner ear and finds a parallel with the Ferrassie 1, 2) represent a male and female, respectively (Table 3). mosaic pattern established in the cranium and postcranial skeleton The two immature Neandertal individuals were correctly classified in the European Middle Pleistocene fossil record (Arsuaga et al., in the CVA, despite their lower values along PC2 and separation 2014, 2015). Further studies of the cochlea in recent humans, from the adult individuals in the PCA. Finally, Aroeira 3 was clas- relying on the more complete set of variables used here, may sified with the SH hominins with a posterior probability of 0.77. represent another avenue of inquiry into Middle Pleistocene systematics. 4. Discussion and conclusions Declaration of interest The results of the PCA and the CVA revealed that the cochlear morphology of Aroeira 3 is most similar to that of the SH hominins. The authors declare no competing interests. The univariate comparisons indicated that this similarity is pri- marily because of the small size and rounded shape of the cross- Acknowledgments sectional area of the basal turn, and this has been suggested to represent the ancestral morphology for hominins (Conde-Valverde The authors thank the associate editor and the three anonymous et al., 2019). The Aroeira 3 cochlea shares a low NT and a high reviewers for their constructive comments on improving the cochlear thickness with the genus Homo samples, and these two manuscript. Financial support for this study was provided by features have been suggested to represent derived characters in Ministerio de Ciencia, Innovacion y Universidades (PGC2018- Homo relative to chimpanzees (Conde-Valverde et al., 2019). 093925-B-C33) and Universidad de Alcala (CCG2016/EXP-036). Our results of CVA show that the misclassified individuals in the Fieldwork at the Gruta da Aroeira was funded by the Camara^ SH and Neandertal samples included individuals of both sexes, Municipal de and Fundaçao~ para a Ciencia^ e Tecno- which suggests that sexual dimorphism does not affect the ability logia with logistical support by Fabrica de Papel A Renova. M.C.V.

5 M. Conde-Valverde, I. Martínez, R. Quam et al. Journal of Human Evolution 148 (2020) 102887 has received a predoctoral grant from the Fundacion Atapuerca, and hominin cranium from Gruta da Aroeira (Portugal). Proc. Natl. Acad. Sci. USA e R.Q. has been supported by Programa “Gines de los Ríos” (Uni- 114, 3397 3402. https://doi.org/10.1073/pnas.1619040114. Dean, M.C., Beynon, A.D., 1991. Tooth crown heights, tooth wear, sexual dimorphism versidad de Alcala), J.D. by a Ramon y Cajal grant (RYC- 2015- and jaw growth in hominoids. Z. Morphol. Anthropol. 78, 425e440. https:// 17667), and M.S. by a Juan de la Cierva postdoctoral grant (IJCI- www.jstor.org/stable/25757328. 2017-33908). This article is the result of research performed by the Endo, B., Kimura, T., 1970. Postcranial skeleton of the Amud man. In: Suzuki, H., Takai, F. (Eds.), The Amud Man and His Cave Site. University of Tokyo, Tokyo, Evolutionary Bioacoustics Group at the Universidad de Alcala pp. 231e406. (Spain). 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