You are on page 1of 6

Auditory capacities in Middle Pleistocene humans from the Sierra de Atapuerca in Spain

I. Martınez*†‡, M. Rosa§, J.-L. Arsuaga†¶, P. Jarabo§, R. Quam† , C. Lorenzo†**, A. Gracia†, J.-M. Carretero†,††, ´ ´ J.-M. Bermudez de Castro‡‡, and E. Carbonell**
*Departamento de Geologıa, Universidad de Alcala, Edificio de Ciencias, Campus Universitario, 28871 Alcala de Henares, Spain; †Centro de Investigacion ´ ´ ´ ´ (Universidad Complutense de Madrid–Instituto de Salud Carlos III) sobre, Evolucion y Comportamiento Humanos, c Sinesio Delgado 4, 28029 Madrid, Spain; ´ §Departamento de Teorıa de la Senal y Comunicaciones, Universidad de Alcala, Escuela Politecnica, Campus Universitario, 28871 Alcala de Henares, Spain; ´ ˜ ´ ´ ´ ¶Departamento de Paleontologıa, Universidad Complutense de Madrid, Facultad de Ciencias Geologicas, Ciudad Universitaria s n, 28040 Madrid, Spain; ´ ´ ´ Department of Anthropology, State University of New York, Binghamton, NY 13902-6000; **Area de Prehistoria, Universitat Rovira i Virgili, Facultat de ´ ´ Lletres, Placa Imperial Tarraco 1, 43005 Tarragona, Spain; ††Departamento de Ciencias Historicas y Geografıa, Universidad de Burgos, Facultad de ¸ ´ ´ Humanidades y Educacion, 09001 Burgos, Spain; and ‡‡Departamento de Paleobiologıa, Consejo Superior de Investigaciones Cientıficas, ´ Museo Nacional de Ciencias Naturales, c Jose Gutierrez Abascal 2, 28006 Madrid, Spain ´ ´ Contributed by J.-L. Arsuaga, May 20, 2004

Human hearing differs from that of chimpanzees and most other anthropoids in maintaining a relatively high sensitivity from 2 kHz up to 4 kHz, a region that contains relevant acoustic information in spoken language. Knowledge of the auditory capacities in human fossil ancestors could greatly enhance the understanding of when this human pattern emerged during the course of our evolutionary history. Here we use a comprehensive physical model to analyze the influence of skeletal structures on the acoustic filtering of the outer and middle ears in five fossil human specimens from the Middle Pleistocene site of the Sima de los Huesos in the Sierra de Atapuerca of Spain. Our results show that the skeletal anatomy in these hominids is compatible with a human-like pattern of sound power transmission through the outer and middle ear at frequencies up to 5 kHz, suggesting that they already had auditory capacities similar to those of living humans in this frequency range.

K

nowledge about the sensory capabilities of past life forms could greatly enhance our understanding of the adaptations and lifeways in extinct organisms. Audition is the most readily accessible in fossils because it is based primarily in physical properties that can be approached through their skeletal structures (1). Recently, the possibility to analyze auditory capacities in fossil species has been highlighted as one of the major challenges in modern vertebrate paleontology, particularly since the advent of computed tomography (CT)-based analyses (2). The recent publication of a detailed comparison of the human and chimpanzee genomes has highlighted several genes involved with hearing that appear to have undergone adaptive evolutionary changes in the human lineage (3). The authors have suggested that these changes could be related with the acquisition of hearing acuity necessary for understanding spoken language, and they emphasize the importance of further research into hearing differences between humans and chimpanzees (3). At least one of the human genes mentioned as having undergone adaptive evolutionary change (EYA1) is related to the development of the outer and middle ear (4, 5). These results are compatible with the known differences in the anatomical structures of the outer and middle ear in chimpanzees and ourselves (6, 7). As might be expected from these genetic and anatomical data, the empirical studies of chimpanzee hearing capabilities also show clear differences with human hearing. Chimpanzee audiograms (8, 9) show a W-shaped pattern characterized by two peaks of high sensitivity at 1 kHz and 8 kHz, respectively, and a relative loss of sensitivity in the midrange frequencies (between 2 and 4 kHz). Of course, this relative loss does not mean that chimpanzees cannot hear in the midrange frequencies, but rather that they are adapted to hear best at 1 kHz and 8 kHz. It is interesting to note that the species-specific pant-hoots regularly emitted by wild chimpanzees to communicate with conspecifics
9976 –9981 PNAS July 6, 2004 vol. 101 no. 27

over long distances concentrate the acoustic information at 1 kHz (10). At the same time, although human audiograms also show a high sensitivity at 1 kHz, they differ from chimpanzees in lacking the marked relative loss in sensitivity between 2 and 4 kHz, maintaining a relatively high sensitivity within this frequency range (9, 11–13). In this context, knowledge of the auditory capacities in human fossil ancestors could greatly enhance the understanding of when this human pattern emerged during the course of our evolutionary history. A few prior studies have approached this question in fossil hominids, but they should be considered with caution because they are based on simplified physical models relying on only a few anatomical variables (6, 14). To accurately approach the auditory capacities in fossil specimens it is necessary to consider the acoustic and mechanical properties of each component of the outer and middle ears and the way in which they interact (15–17). Although some of these anatomical components are related to soft tissues (e.g., ligaments) that do not preserve in the fossil record, the remaining skeletal structures can provide relevant information about the auditory capacities in fossil specimens. Here we have applied a comprehensive physical model, implemented with its analog electrical circuit, to evaluate the effects of the skeletal anatomy on the acoustic filtering and sound power transmission through the outer and middle ears in five individuals from the Middle Pleistocene site of the Sima de los Huesos (SH) in the Sierra de Atapuerca of Spain. Materials and Methods metric age limit of 350 thousand years (18). They have been argued to be phylogenetically close to the Neandertals and are attributed to the species Homo heidelbergensis (19–21). Among the SH human fossils, there are two adult specimens (Cranium 5 and the isolated left temporal bone AT-84) and one juvenile individual (another isolated left temporal bone labeled AT-421) in which the external and middle ears are exposed, making it possible to directly measure many of the anatomical variables necessary for this study. We have also measured two additional juvenile isolated temporal bones (AT-1907, right, and AT-4103, left) in which the external and middle ears are not exposed. To measure the necessary variables in these individuals, we have relied on their 3D CT reconstructions, using MIMICS 8.0 software (Materialise, Leuven, Belgium). The accuracy of the CT-based measurements in these individuals is guaranteed by the fact that
Abbreviations: CT, computed tomography; SH, Sima de los Huesos.
‡To

Materials. The SH human fossils have a firm minimum radio-

whom correspondence should be addressed. E-mail: imartinezm@isciii.es.

© 2004 by The National Academy of Sciences of the USA

www.pnas.org cgi doi 10.1073 pnas.0403595101

5 76. we have used the average value of the other three SH specimens.2 4.7 3. VAD. 1 A). mm2 LM / LI.98 3.1 3.2 21. 6.4 1. mm LI. we have relied on all of the values obtained in the 3D CT reconstructions for Cranium 5. area of the oval window.1 5.7 2.5 1.4 1.7 2. *The footplate area in AT-84 and AT-421 was estimated as 90% of the area of the oval window (AOW in Table 1).2 52. RAD. We have use the directly measured value of the stapes footplate in Cranium 5 for both AT-1907 and AT-4103. mm ATM. the malleus (AT-3746) and incus (AT-3747) are preserved in the juvenile right isolated temporal bone AT-1907. and AFP are as in Fig.17 0. cm3 VMEC. 23) and the dimensions measured by us in a multiracial modern human sample (see supporting information).2 34.8 1. AEAC.7§ 24.5 1.8 76. 1 A).25 0. REAC1. mm2 cm3 CT 2.9 4.5 3.4 4.9 5. mm AEAC.76 5.8 25. We have used the value from the ear ossicles extracted from AT-1907 for all the SH individuals.2 3.0 2. half of the measured greater diameter of the tympanic membrane measured in the tympanic groove (sulcus tympanicus). we have used the average value of Cranium 5.9 74.1 4.6 5.8 3.8* AT-1907 3.2 1.0‡ 3. Martınez et al.4 3. AT-1907. calculated as the average of RAD1 and RAD2 (Table 1).26 5.2 4.85 0.7 46.51 4. †The value of R TM2 in AT-421 was estimated from the values in the other Atapuerca specimens.0 3. MI.6 4. radius of the entrance to the aditus ad antrum.55 17 4. and AT-4103.9 3.8 2. RAD2.51 4.2 3. LM.2 52. ´ PNAS July 6. Further. the preserved squamous portion represents half of the original EAC.4† Abbreviations are as in Fig.27 0.5 23.8 4. mm RTM1. cm3 LAD.6 51.8 Pan 4.12 VMA. mass of the incus.4 3.7 2.8 AT-4103 6. and the REAC2 can be reliably measured directly.26 5.8 Pan 4.18 0.15 0. half of the measured superoinferior diameter of the external auditory canal at the level of the superior point of the tympanic groove (dotted line 4.7 17. MM.8 AT-84 4.5.0§ AT-4103 5. mm LEAC. RAD1.6 26. cross-sectional area of the external auditory canal calculated as a circle from REAC1 and REAC2 (Table 1). In the SH collection. Original measurements of the outer and middle ears in the SH and Pan individuals Cranium 5 Anatomical variables VMA. RTM1. mm2 mm3 Cranium 5 (CT) 2.2 52.60 6. mm RTM2.3 5. half of the measured anteroposterior diameter (perpendicular to REAC1) of the external auditory canal at the level of the superior point of the tympanic groove.6 2.4 1. 1 and Table 1.95 4.2 5. mm REAC2.3 25. 2004 vol. mm RAD. mg AOW. the measurements taken on a similar 3D CT reconstruction of Cranium 5 were not significantly different from the comparable direct measurements taken on this same specimen (Table 1).9 22. half of the measured greater diameter of the entrance to the aditus ad antrum from the middle ear cavity (dotted line 2. LEAC complete. half of the measured lesser diameter (perpendicular to RTM1) of the tympanic membrane measured in the tympanic groove. mm RAD1.095 0.4 4. Given this agreement.2 52.15 0. 27 9977 ANTHROPOLOGY .5 17.10 0. 14.7 4. 101 no.2 28.05 0. LI. RTM2.4 5. REAC2. Fig. mm2 AFP.0 30. Fig.6* AT-421 4. to complete the measurements related with the cavities of the middle ear and mastoid in AT-84 and AT-421.4 3.8 3.9 24.8 82.02 2.1 Direct AT-84 AT-421 AT-1907 3. VAD.6 3. §We are confident in using the Atapuerca values because the measured masses and general dimensions of the malleus and incus in the Atapuerca hominids are similar to the published modern human masses (22.90 0. mass of the malleus.0 2.2 3.2 52. mm MM M1.60 6.75* 4. ATM.3 5.8 5.5† 14.5 31. AT-1907. 24 –26). mm REAC1.2 20.8 24. mg AFP. as suggested by measurements from Cranium 5 and ref.7 2. allowing us to measure the functional Table 2.5 59. half of the measured lesser diameter (perpendicular to RAD1) of the entrance to the aditus ad antrum from the middle ear cavity.6 4. For the values related with the middle ear cavities and mastoid air cells in AT-84 and AT-421. and AT-4103 (Table 2).Table 1.8 3.75 4. mg MM.2 1.54 8. mm3 LAD. VMEC.6 3. ‡Although AT-421 lacks the tympanic portion of the EAC. *The value of RTM1 in AT-421 was reconstructed from the preserved portion of the tympanic ring. AOW.54 8.5 16. calculated by multiplying the value of LEAC (Table 1) by 1. Values of the outer and middle ear variables used in the physical model Anatomical variables VMA VAD.68 0. †Ref.77 3. LAD.2 3.10 0.8 84. mm MI.7 2.8 2.0 23. to include the cartilaginous portion of the external ear (6. mm RAD2. mm LM.76 5. VMEC.55 16. 1.9 82.40 0.5 1. mm2 LEAC complete. area of the tympanic membrane calculated as an ellipse from RTM1 and RTM2 (Table 1). LEAC.

1073 pnas.org cgi doi 10. AFP. Although our results are not a true audiogram. it is widely recognized that there is a strong correlation between sound power transmission through the outer and middle ear and auditory sensitivity to different frequencies§§ (35–39). It is important to note that only seven of these have an appreciable effect on the model results above 2 kHz (labeled as medium and high in Table 3). ´ . Specifically. we have used the directly measured value of the footplate area in Cranium 5 for the AT-1907 and AT-4103 individuals (Table 2). measured as the maximum length from the superior border of the short process to the inferior-most tip of the manubrium. VMA. Because the area of the oval windows cannot be measured in the 3D CT reconstructions. in the critical region of 4 kHz. we have estimated the footplate area from their exposed oval windows (Table 2). we have modeled two theoretical extreme individuals: (i) a ‘‘human-like’’ chimpanzee. B is based on the profiles of the malleus and incus from the temporal bone AT-1907 and the stapes from Cranium 5. We have measured or accurately estimated in the SH specimens all of the 13 skeletal variables included in the model (Table 2).04 dB for GME is intermediate between those found for the same frequency: 12 dB (27) and 18 dB (33). which has been directly measured for the first time in 11 human cadaver ears by Aibara et al. resistive cochlear input impedance with an average value of 21. Nevertheless. LEAC. measured from its limit with the middle ear (dotted line 2) to its limit with the mastoid antrum (dotted line 1).1 G from 0. To is also well understood that some fundamental aspects of hearing. the 13 skeletal variables in one chimpanzee individual (Pan troglodytes). ‘‘superhuman-like. Because the model requires values for all of the variables. We should highlight one important implication from the way that the human-like chimpanzee individual was constructed. Martınez et al. LAD. measured area of the footplate of the stapes. in fact. 33). Table 3 shows the relationship between the electrical parameters and the anatomical structures. The Physical Model. measured from its limit with the aditus ad antrum (dotted line 1). we have used this empirical value for the cochlear input impedance. volume of the aditus ad antrum. For AT-84 and AT-421. making our human-like chimpanzee.’’ §§It Theoretical Variability in Chimpanzees and Modern Humans. through 3D CT reconstruction. the respective value for modern humans (17. measured from the superior point of the tympanic groove to the spina suprameatum. are determined by properties of the inner ear (34). 1. measured as the mean distance from its limit with the middle ear cavity to the entrance to the mastoid antrum. To evaluate the influence of the skeletal variables on the interspecific difference in the acoustic filtering patterns. LI. We have used modern human values for two skeletal variables (AEAC and MI MM) in which the chimpanzee range of variation is not known (but which seem to have lower values than modern humans) to model the human-like chimpanzee (see supporting information). we are confident the analysis is useful to evaluate the results. The modification we have introduced into the model refers to the cochlear input impedance (Zc). and we have modeled it by using the modern human values (17. The electrical parameters used in the model are associated with anatomical structures of the ear. functional length of the incus measured from the lateral-most point along the articular facet to the lowest point along the long crus. volume of the mastoid antrum and connected mastoid air cells. because the skeletal variables that are modified all have a relatively strong effect on the model (labeled medium or high in Table 3).pnas. 17. 27) for the remaining 17 soft-tissue-related variables. length of the external auditory canal. functional length of the malleus. volume of the middle ear cavity measured from its limit with the aditus ad antrum (dotted line 2) to the edge of the tympanic groove (dotted line 3). Because our study is focused on the frequency range from 2 to 4 kHz. Some of these parameters are related with skeletal structures accessible in fossils. who found a flat. our value of 9978 www. rather than the value provided in the original model (17). For some specific aspects of the study. it is reasonable to conclude that the skeletal differences between humans and chimpanzees can explain an important part of the interspecific differences in their patterns of acoustic filtering in the outer and middle ear. Dotted line 4 marks the level at which the cross-sectional area of the external auditory canal (AEAC) was measured. lengths of these bones in a single individual. and (ii) a ‘‘chimpanzee-like human. 1 and Tables 2 and 3. New York (n 41). To ensure the reliability of our model.Fig. Given that the results for sound power transmission in our chimpanzee individual agree with those of published audiograms for this species (see below). The use of electrical circuits to model sound power transmission through the outer and middle ear is a common practice in auditory research (16. as we have done in the SH specimens.1–5. LM. when constructing these theoretical chimpanzee and modern human individuals. Measurements of the middle and external ear (A) and ear ossicles (B). together with an analysis of the sensitivity of the model above 2 kHz to each variable. 27) has been used for the remaining 17 soft-tissue-related variables that cannot be measured in fossil specimens (Table 3). we have measured (Tables 1 and 2).0403595101 15. which is published on the PNAS web site). we have compared the theoretical middle ear pressure gain (GME) we have obtained for modern humans (see supporting information) with those measured experimentally (27. VAD. Cranium 5 preserves its left stapes (AT-667). whereas others are related with soft tissues that are not preserved in fossil specimens. these skeletal morphology can be used to approach the sound power transmission pattern in closely related fossil human species. 28–32). The definitions and values of the variables used in the model in this study are presented in Fig. Therefore.’’ using values at the extreme of the human variation toward those of chimpanzees (see supporting information). using values at the extreme of the chimpanzee variability toward those of modern humans. A and B are not drawn to the same scale. finding no significant differences. (27).0 kHz. evaluate whether the effects of the intraspecific skeletal variation could result in the chimpanzee and modern human sound power transmission curves overlapping. to estimate the sound power transmission through the outer and middle ears (see supporting information. such as bandwidth limits. Here we have relied on a slightly modified version of the model published by Rosowski (17). we have also measured some variables in the temporal bones from a Spanish Medieval sample (n 30) and in the ear ossicles in a modern multiracial sample housed in Seneca Falls. VMEC. A is based on the CT images of Cranium 5. we have been limited to relying on those skeletal variables whose intra and interspecific variation is known. length of the aditus ad antrum. This use of modern human values has the effect of overestimating the variation of the chimpanzee toward modern humans. Clearly.

*The mass of the tympanic membrane was estimated based on its area.86 3.Table 3. except ZC (cochlear input impedance).65 14. At the same time. ligaments and stapes Functional lengths of the incus and malleus Masses of the incus and malleus Non-articular surface area of the malleus and incus Structural properties of the malleus and incus Mass of the stapes Structural properties of the ossicular joints Area of the stapes footplate Structural properties of the annular ligament Structural properties of the cochlea Measured as LI LM Measured as MI Rosowski (17) Rosowski (17) Rosowski (17) Rosowski (17) MM Measured as AFP Rosowski (17) Aibara et al. Anatomical variables are as in Fig.38 AT-4103 6. medium ( 1 to 3 dB difference).7 4.85 6. their related anatomical variables. and SH individuals at selected frequencies Frequency 3 kHz 4 kHz 5 kHz Modern human 11. incus.32 1. 2 and 3 and Table 4).43 1.67 2. using the values provided by Rosowski (17) and Aibara et al. extrapolating from the values for modern humans provided by Rosowski (17). ´ PNAS July 6.09 AT-421 9.39 12.25 9.46 3.01 Human-like chimpanzee 4. the source of the value used. 101 no. Results and Discussion To evaluate the sound power transmission through the outer and middle ears.31 0. Values of sound power (dB) at the entrance to the cochlea relative to P 10 18 W for an incident plane wave intensity of 10 12 W m2 in the modern human.28 3.87 Cranium 5 4.56 9. (27). Definition of the electrical parameters. Our results in modern humans agree with those published by Rosowski (17) that show two peaks in pressure gain at 1 and 3 kHz (Fig.13 3. Sensitivity has been classified into three broad groupings: low ( 1 dB difference). 2). (27). 27 9979 . and high ( 3 dB difference). we have calculated the sound power at the entrance of the cochlea relative to P0 10 18 W for an incident plane wave intensity of 10 12 W m2 (Figs.49 ANTHROPOLOGY Martınez et al.84 1. (27) All definitions and abbreviations of the electrical parameters follow Rosowski (17). 2004 vol.37 Chimpanzee 2. chimpanzee. and that obtained by increasing and decreasing the individual anatomical variable (A) or electrical parameter (E) by 50% from the respected values reported by Rosowski (17) and Aibara et al.69 Chimpanzee-like modern human 6.74 AT-1907 6.69 1. †The value provided for this variable in Rosowski (17) is infinite and is not included in the sensitivity analysis. (27).43 AT-84 10. which follows Aibara et al. Sensitivity is measured as the difference between the value for sound power at the entrance to the cochlea (in dB).85 2.48 4. our results for the chimpanzee agree with those obtained in audiograms (8. 1 and Table 2. 9) in showing a peak in heightened sensitivity 1 kHz and a steep loss in Table 4. and the sensitivity analysis for frequencies above 2 kHz in the model Related anatomical variables Electrical parameters External ear Two-port network that models the concha horn Two-port network that models the ear canal tube Middle ear Middle ear cavity Definition Concha length Cross-sectional area of wide end Cross-sectional area of narrow end Ear canal length Cross-sectional area of the ear canal CTC CMC RA LA ATM LT1 CT RT LT CT2 RT2 CTS RTS II:IM LMIM RMIM CMIM LSM RJM CJM AFP Inner ear Annular ligament Cochlea CAL RAL ZC Volume of the middle ear cavity Volume of the aditus and mastoid air spaces Surface area of the aditus and mastoid air spaces Length and radius of the aditus Area of the tympanic membrane Mass of the tympanic membrane Structural properties of the tympanic membrane and mallear attachment Value used Rosowski (17) Rosowski (17) Measured as AEAC Measured as LEAC complete Measured as AEAC Measured as VMEC Measured as VAD VMA Rosowski (17) Measured as LAD and RAD Measured as ATM Estimated from ATM* Rosowski (17) Sensitivity ( 2 kHz) High (A) High (A) High (A) High (A) High (A) Low (A) Low (A) Low (E) Low (E) High (A) High (A) Low (E) Low (E) Low (E) Low (E) Medium (E) High (E) Medium (E) High (A) Medium (A) Low (E) Low (E) Low (A) Low (E) Low (E) Medium (A) † High (E) High (E) Tympanic membrane and mallear attachment Malleus.

dashed black line. (27). All individuals have been modeled by using the model defined by Rosowski (17) and the cochlear input impedance (Zc) of Aibara et al. Perez-Gil. Gotherstrom. R. J. Lira. Further. Cuenca. clearly different from chimpanzees in the critical region of 4 kHz. our results suggest that the skeletal characteristics of the outer and middle ear that support the perception of human spoken language were already present in the SH hominids. J. can also be used to validly infer sound power transmission patterns in fossil hominids.A.-L. the region between 2 and 4 kHz also contains relevant acoustic information in human speech (47–49). (27). falling near or within the modern human variation (Fig. Above 3 kHz the chimpanzee curves show a sharp drop in sound power transmission. AT-421. Results from modern human (solid line) and chimpanzee (dashed line) individuals are shown and were obtained by using the model defined by Rosowski (17) and the cochlear input impedance (Zc) of Aibara et al. our analysis shows that the skeletal anatomy of the outer and middle ear in the SH hominids is compatible with a human-like sound power transmission pattern. The CT scans were taken at the Hospital 12 de Octubre (Cranium 5) and the Hospital Ruber Internacional (Chimpanzee. J. M. the first two formant frequencies of the vowels) (45–47). Martı ´n-Loeches. A. At the same time. the frequency range used in telephones reaches up to 4 kHz to ensure the intelligibility of the communication. Table 4 provides the numerical values for the sound power at the entrance to the cochlea at 3. Sound power (dB) at the entrance to the cochlea relative to P0 10 18 W for an incident plane wave intensity of 10 12 W m2. and R. Chimpanzee individual is based on the 3D CT reconstruction. and it has been argued to be represented among the 800. and C. the sound power transmission curves obtained for the SH hominids are clearly separated from the chimpanzee variation in the distinctive region of 4 kHz (from 3 to 5 kHz).8 dB at 4. solid green line.Q. The sound power transmission curves obtained for the SH hominids. the human and chimpanzee curves clearly separate. Although much of the acoustic information in spoken language is concentrated in the region up to 2. solid red line. de los Rı for their ´ ´os valuable help in the elaboration of the present work. was supported by ´ a grant from the Fundacion Atapuerca.pnas.g. It is reasonable to speculate on the relation between the evolution of human hearing and human spoken language (3). modern human. Between 3 and 5 kHz. Sound power (dB) at the entrance to the cochlea relative to P0 10 18 W for an incident plane wave intensity of 10 12 W m2. the distance between the curves that delimit the chimpanzee and human theoretical variation are separated by 10 dB. Bischoff. the immediate implications of our results for the study and reconstruction of the anatomical structures related with speech production in fossil humans have not escaped our notice. From this point of view. de Langues et du Language Program. Ruiz. between 2– 4 kHz. solid magenta line. Thus. We thank J.L. AT-84. Munoz. C.G. theoretical human-like chimpanzee individual. and 5 kHz. we interpret this agreement as evidence that the differences in skeletal anatomy can explain much of the interspecific differences in the sound power transmission between these closely related species and. AT-1907. was supported by a Fulbright full grant and a grant from the Fundacion ´ Duques de Soria. but form part of the Neandertal evolutionary lineage (19–21). The excavations at the Atapuerca sites are funded by the Junta de Castilla y Leon. In addition. Analysis of Neandertal mtDNA suggests that this last common ancestor probably lived at least 500 thousand years 9980 www. 2).Fig. chimpanzee. Spain) attributed to the species Homo antecessor (43. 3. Because the SH hominids are not on the direct evolutionary line that gave rise to our own species.-C.5 kHz (e. A. Keeping in mind the direct relation between the auditory patterns in animals and the sounds they are capable of producing (9. A. AT-1907. AT-4103) in Madrid. it is conceivable that this condition was already present in the last common ancestor of modern humans and Neandertals.org cgi doi 10. the curve of the human-like chimpanzee overlaps the modern human and SH ranges of variation. Linera.-J. reaching a maximum difference of 16..1073 pnas. Greiner. T.0403595101 Fig. Manzi. 3 and Table 4).385 Hz. which is especially relevant. solid black line. 49–53). Ortega. coinciding with that suggested by previous researchers based on audiograms (8. form part of the ´ project Production and Perception of Language in Neandertals (Origines de l’Homme. 2. 9). In fact. Up to 3 kHz. ´ . ˜ M. Esquivel.-A. 44). sensitivity from 2– 4 kHz (Fig. AT-4103. and modern human individuals and their theoretical ranges of variation are shown in Fig. consequently. was supported by a grant from the Fundacion ´ Duques de Soria and the Fundacion Atapuerca. J. whereas the modern human curves maintain higher values for sound power transmission. Martınez et al.000-year-old fossils from the TD6 level at the site of Gran Dolina (Sierra de Atapuerca. Cranium 5. dashed red line. chimpanzee 3D CT. ago (40–42). As mentioned above. given that (as mentioned above) the chimpanzee range of variation toward humans has been overestimated. theoretical chimpanzee-like modern human individual. G. Solid blue line. dasheddotted red line. dashed magenta line. A. G. 3. Centre National de la Recherche Scientifique). J. and the Atapuerca Research and Excavation Team for their work in the field. 4.Q. This work was supported by ´ Ministerio de Ciencia y Tecnologı of the Government of Spain Project ´a BOS2003-08938-C03-01.

Abdelhak. Alonso.. London). & Santos-Sacchi. 40. 219–282. & Graybeal.. Arsuaga. A. NJ). L. (Delft Univ.. J. Carbonell. (2000) Hear. (1934) J. I.. (2002) Proc. Hawke. 52. Honda. Y. 3373. S. pp. Crelin. D.. Rosowski. J. Rosowski. M. Glanowski.. & Mosquera. Thomas. 2. S. L. L. & Murdoch. Acoust.. & Schwartz. Stuhlmann... Shaw. 38.. Krainitzki. M. S. eds. Murphy. 150. S. Oxford). (1997) J. 152. Heim. C. Gracia. Cruaud. 22. & Rosowski. P. H. Am. Vol. M. (1999) in Tratado de Otorrinolaringologı y Cirugı de Cabeza y Cuello. M. Fay. Zwislocki. 34.. & Scichilone. M.. ´ PNAS July 6. Nummela. (1983) in Animal Behaviour. pp. Romanova. 25. 97–133. J. Acad. L. J. Relkin. Vervoort.. Popper. Anthropol. (Springer. R. (1997) Hum. Behav. 51.. R. G. B. USA 99. Soc. S. Vincent. N. & Goodwin. Heffner. Civello. & Jahn. J. 36. Liden. J. (1960) The Structure and Function of the Middle Ear (Univ. eds. O. Martı ´nez. 119–128. 133–151. Gil-Carcedo. & Klatt.. 288–321. A. J. D. 33. J. P. C.. Samson. 66–75. Press. 465–484... Moggi-Cecchi. deBoer. G. Melbourne). Abbott. Comp. Todd. (1999) Am. pp. Kharitonov. A. P. Stone. Evol. Ruggero. 48. (1991) J. Lu. Acoust. R. 47. Puria. & White.. W.. Vallejo. 6. O. & Slater. 114–155. Soc. Onchi. Jahn. M. & Stinson. 490–493. & Borgognini Tarli. 101. Arsuaga. A. A. ´ 19. Martı ´nez. L.. 26. Shamp. (2001) Hear. 62–72. Natl. J. New York). Genet. A. MA). Psychol. H. J. 44. & Peake. R. & Collard. Evol. J. J. 74. Sivian. J. 283–318. Evol. 10. 45. A. 1.. & Fay. 795–801. pp. & Pa¨bo. & Fay.. (1937) J. (Blackwell. M. 42. Primatol. 49. E. M. Krainitzki. E. 321–338. (1993) Nature 362.. M. I. pp. Carbonell. 19–30. R. 275–280. Soc. Phonet. I. Schmitz. S. 1514–1523.. S. (1997) J. Sci.. The Netherlands). Rosowski. Merchant. 30. (2002) J. Rosowski. Hum. T. 534–537. (1999) J. Kringlebotn. G. 5581–5585. 33. W. 23. D. Geisert. 90. 172–247.. Krings. D. (1994) in Comparative Hearing: Mammals. Compain. J. eds. (1988) in Physiology of the Ear. New York).. 18. (1999) J. 15–61. Soc. (2000) Nature 404. S. J. Res. E. ¨a Natl. Rosowski. Fletcher. Acoust. M. Maffei. J. 28. 21. L.. V. J. Genet. McMullen. (1991) in The Circeo 1 Neandertal Skull: Studies and Documentation.. 4. (2002) Auditory Sound Transmission—An Autobiographical Perspective (Erlbaum. J. 13206–13210. D. J. Mahwah. & Bermudez de Castro. & Lorenzo. & Pa¨bo. & Herbert. 13. C. R. 9. Dallos. Cambridge. 43–69. Hawkins. Hum. Kalatzis.. 90. M. NJ). J. L. A. Bermudez de Castro. & Popper. 1–43. Gotherstrom.. (1961) J. H. Rome).. M.. F. Hum. J. 431–457. 34. Archaeol...1. 17. Deller.. Arsuaga. M. Am. J.. 101. Gil-Carcedo. & Popper. Kirikae. S. J. 7. Soc. Mitani. (1992) Acoustic Systems in Biology (Oxford Univ. I. 27. USA 96. 14. et al. Am. Soc. Suarez. J. 32. & Arsuaga. Rosas. G. 50. Press and Trans Pacific Press. Medina. Hunley. R. Zwislocki. Ortega. E.. (2003) Science 302. D. M. 670–687. P.. pp. L. & ˜ Gallego. Acoust. 157–183. A. A. eds. Linn. (Springer. 2. Heilig. S. R. 37. R. 2247–2255. pp. (2003) A Search for the Origins of Human Speech (Kyoto Univ. S. M. Soc.. J. 124–135. 2754–2770. C. 4. Nielsen. 32... 757–766. Acoust. Gracia. C. K. L. & Gil-Carcedo. 29–44. (2002) J... (1996) in The Cochlea. eds. New York). Sci. eds. San Diego). E. Marler. Halliday. Lieberman. Rosowski. J. & Waser. 3–10. & Hansen. Arsuaga. Martı ´nez.. Upper Saddle River. (Singular. ¨a (1997) Cell 90. Am. 20. 55. Carretero. I. Hopkins. Aibara. Mathieu. Evol. Press. Martınez et al. A.. S. Munoz. 75–85. Levi-Acobas. J. Am. eds. H. (1987) Discrete-Time Processing of Speech Signals (Prentice–Hall. (Springer. R. (1994) in Comparative Hearing: Mammals. H. M. 17. A. 33. Proakis. & Santos-Sacchi. Delft. Am. (1991) J.. eds. W. Popper. Stokstad.. 85. 1392–1395. Arsuaga. 10. D.. Gray. Clark. (Academic. (1962) J. Boe. Martı ´ ´nez. 770–771. Tanenbaum. (1990) Folia Primatol. S. Tokyo). Hum. & Viergever. Press. Hum. P. 6. Sci. 2.. C. Brown. R. 30. Welsh. V. eds. 29. 3. A. 47. (1999) Proc. Dallos. Le Merrer. Acad. Schroer. S. (Instituto Poligrafico e Zecca Dello Stato.. Res. P. Descriptive and Surgical (Bounty Books. Acoust. & Heffner. Madrid). J. L. Lieberman.. 8. (1997) Science 276. J. 131–168. Voss. (Editorial Proyectos Medicos. & Trinidad. (1984) The Biology and Evolution of Language (Harvard Univ. C. I. R. 30. 18–30. pp. (Springer. 3017–3023. Kojima. 31. E. pp. E.. F. & Moody. 53. A. 9.. 33. Jahn. M. 17.. (1972) Am. Vol. J. 103–123. R. L. S. J. 11. Lorenzo. Fay. Mol. (1978) in Recent Advances in Primatology. eds. Johnson. 24. 42. (1997) J. J. Puria. Res. Vol. J. Krings. (1996) in Auditory Computation.. O’Brien. 794–805. 12. (2003) J. Oxford). M. A. A. E.. 287–307. J. 27 9981 ANTHROPOLOGY . (1988) Scand. Stoneking. P.. H. H. Bischoff. C. ´a ´a ´ Marco. Acoust. M. pp. 2004 vol. (1991) Zool. (Raven. pp. L. New York). Stevenson. eds. (1973) Speech Sounds and Features (MIT Press. V. Masali. 46... 35. Schmitz. 43. (2003) Science 302. M. 1960–1963. P. C. E. (1983) in Mechanics of Hearing.. 41.. Gracia. MA). (2001) in Physiology of the Ear. ¨ Fant. & Temchin. New York). J. T. J. Am. Martı ´nez.. Cambridge. A... J. Smith. 101 no. P.. Kojima.. Elder. Acoust. K. Audiol. Jackson. J. L. A. A. Soc. 16. Chivers. M. (1995) Hear. 100–109. Ovchinnikov. 5. et al... 106. J. New York). Peake. J. Soc. J.. & Maeda. A. J. (1933) J. 39. Aranburu. A. (1977) Anatomy. 259–265.. K. 15.. Stebbins. I. Kejariwal. R. of Tokyo Press. R. Am. A. 37. W. (1984) Anim.. & Carbonell. & Goode. Piperno. (2002) Eur..