Abstract
The study of audition in fossil hominins is of great interest given its relationship with intraspecific vocal communication. While the auditory capacities have been studied in early hominins and in the Middle Pleistocene Sima de los Huesos hominins, less is known about the hearing abilities of the Neanderthals. Here, we provide a detailed approach to their auditory capacities. Relying on computerized tomography scans and a comprehensive model from the field of auditory bioengineering, we have established sound power transmission through the outer and middle ear and calculated the occupied bandwidth in Neanderthals. The occupied bandwidth is directly related to the efficiency of the vocal communication system of a species. Our results show that the occupied bandwidth of Neanderthals was greater than the Sima de los Huesos hominins and similar to extant humans, implying that Neanderthals evolved the auditory capacities to support a vocal communication system as efficient as modern human speech.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Data availability
All the technical data regarding the CT scans as well as the measurements of 3D reconstructions necessary to reproduce our work are offered within the manuscript and Supplementary Information. CT scans of fossil material from Krapina are available at the Nespos platform. CT scans of the fossil specimens La Chapelle-aux-Saints 1 and La Quina H5 are the property of Musée de l’Homme (France); that for Amud 1 is the property of Tel Aviv University (Israel); and the fossil specimens from the Sima de los Huesos are property of Junta de Castilla y León (Spain), to whom application must be made for access. Interested readers may contact the authors, who will assist in getting in touch with the relevant institutions. The CT scans and 3D models of recent H. sapiens are available at Morphosource (https://www.morphosource.org/projects/000343670?locale=en).
References
Tattersall, I. The material record and the antiquity of language. Neurosci. Biobehav. Rev. 81, 247–254 (2017).
Albessard-Ball, L. & Balzeau, A. Of tongues and men: a review of morphological evidence for the evolution of language. J. Lang. Evol. 3, 79–89 (2018).
Dediu, D. & Levinson, S. C. Neanderthal language revisited: not only us. Curr. Opin. Behav. Sci. 21, 49–55 (2018).
Bolhuis, J. J., Tattersall, I., Chomsky, N. & Berwick, R. C. How could language have evolved? PLoS Biol. 12, e1001934 (2014).
Arsuaga, J. L. et al. Neandertal roots: cranial and chronological evidence from Sima de los Huesos. Science 344, 1358–1363 (2014).
Arsuaga, J. L. et al. Postcranial morphology of the Middle Pleistocene humans from Sima de los Huesos, Spain. Proc. Natl Acad. Sci. USA 112, 11524–11529 (2015).
Balzeau, A., Holloway, R. L. & Grimaud-Hervé, D. Variations and asymmetries in regional brain surface in the genus Homo. J. Hum. Evol. 62, 696–706 (2012).
Pearce, E., Stringer, C. & Dunbar, R. I. New insights into differences in brain organization between Neandertals and anatomically modern humans. Proc. R. Soc. B 280, 20130168 (2013).
Neubauer, S., Hublin, J. J. & Gunz, P. The evolution of modern human brain shape. Sci. Adv. 4, eaao5961 (2018).
Bruner, E., Manzi, G. & Arsuaga, J. L. Encephalization and allometric trajectories in the genus Homo: evidence from the Neandertal and modern lineages. Proc. Natl Acad. Sci. USA 100, 15335–15340 (2003).
Zollikofer, C. P. E. & Ponce de León, M. S. Pandora’s growing box: inferring the evolution and development of hominin brains from endocasts. Evol. Anthropol. 22, 20–33 (2013).
Balzeau, A., Gilissen, E., Holloway, R. L., Prima, S. & Grimaud-Hervé, D. Variations in size, shape and asymmetries of the third frontal convolution in hominids: paleoneurological implications for hominin evolution and the origin of language. J. Hum. Evol. 76, 116–128 (2014).
Marie, D. et al. Left brain asymmetry of the planum temporale in a nonhominid primate: redefining the origin of brain specialization for language. Cereb. Cortex 28, 1808–1815 (2018).
Martínez, I. et al. Communicative capacities in Middle Pleistocene humans from the Sierra de Atapuerca in Spain. Quat. Int. 295, 94–101 (2013).
Boë, L. J., Heim, J. L., Honda, K. & Maeda, S. The potential Neandertal vowel space was as large as that of modern humans. J. Phon. 30, 465–484 (2002).
de Boer, B. Loss of air sacs improved hominin speech abilities. J. Hum. Evol. 62, 1–6 (2012).
Krause, J. et al. The derived FOXP2 variant of modern humans was shared with Neandertals. Curr. Biol. 17, 1908–1912 (2007).
Quam, R. M., Martínez, I. & Arsuaga, J. L. Reassessment of the La Ferrassie 3 Neandertal ossicular chain. J. Hum. Evol. 64, 250–262 (2013).
Stoessel, A. et al. Morphology and function of Neandertal and modern human ear ossicles. Proc. Natl Acad. Sci. USA 113, 11489–11494 (2016).
Masali, M., Maffei, M. & Borgognini Tarli, S. M. in Circeo 1. The Neandertal Skull: Studies and Documentation (eds Piperno, M. & Scichilone, G.) 321–338 (Instituto Poligrafico e Zecca Dello Stato, 1991).
Quam, R. et al. Early hominin auditory capacities. Sci. Adv. 1, e1500355 (2015).
Martínez, I. et al. Auditory capacities in Middle Pleistocene humans from the Sierra de Atapuerca in Spain. Proc. Natl Acad. Sci. USA 101, 9976–9981 (2004).
Rosowski, J. The effects of external and middle ear filtering on auditory threshold and noise-induced hearing loss. J. Acoust. Soc. Am. 90, 124–135 (1991).
International Telecommunication Union. Recommendation ITU-R SM.443-4, Bandwidth Measurement at Monitoring Stations (SM Series Spectrum Management, 2007).
Shannon, C. E. A mathematical theory of communication. Bell Syst. Tech. J. 27, 379–423 (1948) .
Fano, R. M. The information theory point of view in speech communication. J. Acoust. Soc. Am. 22, 691–696 (1950).
Letowski, T. R. & Scharine, A. A. Correlation Analysis of Speech Intelligibility and Metrics for Speech Transmission (US Army Research Laboratory, 2017).
Skinner, M. W. & Miller, J. D. Amplification bandwidth and intelligibility of speech in quiet and noise for listeners with sensorineural hearing loss. Audiology 22, 253–279 (1983).
Kates, J. M. & Arehart, K. H. Coherence and the speech intelligibility index. J. Acoust. Soc. Am. 117, 2224–2237 (2005).
Methods for Calculation of the Speech Intelligibility Index ANSI/ASA S3.5-1997 (ANSI, reaffirmed 2020).
Meyer, M. et al. Nuclear DNA sequences from the Middle Pleistocene Sima de los Huesos hominins. Nature 531, 504–507 (2016).
Conde-Valverde, M. et al. A revision of the conductive hearing loss in Cranium 4 from the Middle Pleistocene site of Sima de los Huesos (Burgos, Spain). J. Hum. Evol. 135, 102663 (2019).
Fant, C. G. M. Speech Sounds and Features (MIT Press, 1973).
Mitani, J. C., Hunley, K. L. & Murdoch, M. E. Geographic variation in the calls of wild chimpanzees: a reassessment. Am. J. Primatol. 47, 133–151 (1999).
Lieberman, P. On the Origins of Language: An Introduction to the Evolution of Human Speech (Macmillan, 1975).
Maddieson, I. Patterns of Sounds (Cambridge Univ. Press, 1984).
Lameira, A. R., Maddieson, I. & Zuberbühler, K. Primate feedstock for the evolution of consonants. Trends Cogn. Sci. 18, 60–62 (2014).
Caramazza, A., Chialant, D., Capasso, R. & Miceli, G. Separable processing of consonants and vowels. Nature 403, 428–430 (2000).
Owren, M. & Cardillo, G. The relative roles of vowels and consonants in discriminating talker identity versus word meaning. J. Acoust. Soc. Am. 119, 1727–1739 (2006).
Divenyi, P. L., Stark, P. B. & Haupt, K. M. Decline of speech understanding and auditory thresholds in the elderly. J. Acoust. Soc. Am. 118, 1089–1100 (2005).
Weyrich, L. S. et al. Neanderthal behaviour, diet, and disease inferred from ancient DNA in dental calculus. Nature 544, 357–361 (2017).
Krueger, K. L. et al. Anterior dental microwear textures show habitat-driven variability in Neandertal behavior. J. Hum. Evol. 105, 13–23 (2017).
Zilhão, J. et al. Last Interglacial Iberian Neandertals as fisher-hunter-gatherers. Science 367, eaaz7943 (2020).
Heyes, P. J. et al. Selection and use of manganese dioxide by Neanderthals. Sci. Rep. 6, 22159 (2016).
Vallverdú, J. et al. Combustion structures of archaeological level O and Mousterian activity areas with use of fire at the Abric Romaní rockshelter (NE Iberian Peninsula). Quat. Int. 247, 313–324 (2012).
Tuniz, C. et al. Did Neanderthals play music? X‐ray computed micro‐tomography of the Divje babe ‘flute’. Archaeometry 54, 581–590 (2012).
Rendu, W. et al. Evidence supporting an intentional Neandertal burial at La Chapelle-aux-Saints. Proc. Natl Acad. Sci. USA 111, 81–86 (2014).
Radovčić, D., Sršen, A. O., Radovčić, J. & Frayer, D. W. Evidence for Neandertal jewelry: modified white-tailed eagle claws at Krapina. PLoS ONE 10, e0119802 (2015).
Jaubert, J. et al. Early Neanderthal constructions deep in Bruniquel cave in southwestern France. Nature 534, 111–114 (2016).
Hoffmann, D. L., Angelucci, D. E., Villaverde, V., Zapata, J. & Zilhão, J. Symbolic use of marine shells and mineral pigments by Iberian Neandertals 115,000 years ago. Sci. Adv. 4, eaar5255 (2018).
Hoffmann, D. L. et al. U-Th dating of carbonate crusts reveals Neandertal origin of Iberian cave art. Science 359, 912–915 (2018).
Pearce, D. G. & Bonneau, A. Trouble on the dating scene. Nat. Ecol. Evol. 2, 925–926 (2018).
Hoffmann, D. L. et al. Dates for Neanderthal art and symbolic behaviour are reliable. Nat. Ecol. Evol. 2, 1044–1045 (2018).
Carbonell, E. et al. Les premiers comportements funéraires auraient-ils pris place à Atapuerca, il y a 350 000 ans? L'Anthropologie 107, 1–14 (2003).
Rodriguez-Hidalgo, A. et al. Human predatory behavior and the social implications of communal hunting based on evidence from the TD10. 2 bison bone bed at Gran Dolina (Atapuerca, Spain). J. Hum. Evol. 105, 89–122 (2017).
Sala, N. et al. Lethal interpersonal violence in the Middle Pleistocene. PLoS ONE 10, e0126589 (2015).
Gracia, A. et al. Craniosynostosis in the Middle Pleistocene human Cranium 14 from the Sima de los Huesos, Atapuerca, Spain. Proc. Natl Acad. Sci. USA 106, 6573–6578 (2009).
Bonmatí, A. et al. Middle Pleistocene lower back and pelvis from an aged human individual from the Sima de los Huesos site, Spain. Proc. Natl Acad. Sci. USA 107, 18386–18391 (2010).
Rink, W. J., Schwarcz, H. P., Smith, F. H. & Radovĉić, J. ESR ages for Krapina hominids. Nature 378, 24 (1995).
Sankararaman, S., Patterson, N., Li, H., Pääbo, S. & Reich, D. The date of interbreeding between Neandertals and modern humans. PLoS Genet. 8, e1002947 (2012).
Arsuaga, J. L., Martínez, I., Gracia, A., Carretero, J. M. & Carbonell, E. Three new human skulls from the Sima de los Huesos Middle Pleistocene site in Sierra de Atapuerca, Spain. Nature 362, 534–537 (1993).
Pérez, P. J., Gracia, A., Martínez, I. & Arsuaga, J. L. Paleopathological evidence of the cranial remains from the Sima de los Huesos Middle Pleistocene site (Sierra de Atapuerca, Spain). Description and preliminary inferences. J. Hum. Evol. 33, 409–421 (1997).
Quam, R. Temporal Bone Anatomy and the Evolution of Acoustic Capacities in Fossil Humans. PhD thesis, State University of New York (2006).
Wright, C. G. Development of the human external ear. J. Am. Acad. Audiol. 8, 379–382 (1997).
Radovĉić, J., Smith, F., Trinkaus, E. & Wolpoff. M. H. The Krapina Hominids. An Illustrated Catalog of Skeletal Collection (Croatian Natural History Museum, 1988).
Endo, B. & Kimura, T. in The Amud Man and his Cave Site (eds Suzuki, H. & Takai, F.) 231–406 (Univ. Tokyo Press, 1970).
Valladas, H. et al. TL dates for the Neanderthal site of the Amud cave, Israel. J. Archaeol. Sci. 26, 259–268 (1999).
Rink, W. et al. Electron spin resonance (ESR) and thermal ionization mass spectrometric (TIMS) 230Th/234U dating of teeth in Middle Paleolithic layers at Amud Cave, Israel. Geoarchaeology 16, 701–717 (2001).
Boule, M. L’Homme fossile de La Chapelle-aux-Saints. Ann. Paleontol. 6, 111–172 (1911).
Grün, R. & Stringer, C. B. Electron spin resonance dating and the evolution of modern humans. Archaeometry 33, 153–199 (1991).
Martin, H. L'Homme Fossile de La Quina (Gaston Doin, 1923).
Higham, T. et al. The timing and spatiotemporal patterning of Neanderthal disappearance. Nature 512, 306–309 (2014).
Coleman, M. N. & Colbert, M. W. Technical note: CT thresholding protocols for taking measurements on three-dimensional models. Am. J. Phys. Anthropol. 133, 723–725 (2007).
Harris, R. W. Electromechanical analogies in acoustics. Appl. Acoust. 3, 265–281 (1970).
Kringlebotn, M. Network model for the human middle ear. Scand. Audiol. 17, 75–85 (1988).
Rosowski, J. J. in Auditory Computation (eds Hawkins, H. L. et al.) 15–61 (Springer, 1996).
Lampton, M. Transmission matrices in electroacoustics. Acta Acust. United Acust. 39, 239–251 (1978).
Aibara, R., Welsh, J. T., Puria, S. & Goode, R. L. Human middle-ear sound transfer function and cochlear input impedance. Hear. Res. 152, 100–109 (2001).
Radiocommunication Vocabulary ITU-R V.573e4 (International Telecommunication Union, 2007).
Acknowledgements
We thank the following individuals and institutions for providing access to fossils and specimens housed in their care: A. Balzeau (Musée de l’Homme, France) and I. Hershkovitz and J. Abramov (Tel Aviv University, Israel). CT scanning of the SH fossils was carried out at the Laboratorio de Evolución Humana (Burgos, Spain) by R. García and L. Rodríguez. Financial support for this study was provided by the Ministerio de Ciencia, Innovación y Universidades (PGC2018-093925-B-C33) of the Spanish Government. This project forms part of the Bioacústica Evolutiva y Paleoantropología research group of Universidad de Alcalá. M.C.-V. received a predoctoral grant from the Fundación Atapuerca. R.M.Q. received financial support from Binghamton University and the Ginés de los Ríos grant programme from the Universidad de Alcalá. A.D.V. received financial support from Binghamton University and the Fulbright Commission.
Author information
Authors and Affiliations
Contributions
M.C.-V., I.M., R.M.Q. and M.R. designed the research and wrote the article. M.C.-V., A.D.V. and C.L. reconstructed the 3D models for the study and collected data on the 3D models. M.R. and P.J. modelled the hearing results. J.M.B.C., E.C. and J.L.A. provided critical comments and directed the excavation and the research project at the Atapuerca sites.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Peer review information Nature Ecology & Evolution thanks Amelie Beaudet and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data
Extended Data Fig. 1 3D models of the external, middle and inner ear of the Sima de los Huesos fossils.
External auditory canal (green), middle ear cavity (blue), aditus (orange) and mastoid air cells (purple), inner ear (red).
Extended Data Fig. 2 Anatomical variables used to calculate the sound power transmission in the SH and Neanderthal individuals.
VAD = Volume of aditus; VMA = Volume of mastoid air cells; VMEC = Volume of tympanic cavity; LAD = Length of aditus; RAD(exit) = Radius of aditus exit; RAD(entrance) = Radius of aditus entrance; LEAC (Comp) = Complete length of external auditory canal; ATM = Area of tympanic membrane; AEAC = Cross-sectional area of the external auditory canal; AOW = Area of oval window; AFP = Area of stapes footplate; LM/LI = Malleus/incus lever ratio; MM + MI = Mass of malleus + incus; MS = Mass of stapes. ∗LM/LI for SH calculated from the malleus (AT-3746) and the incus (AT-3747) belonging to the temporal bone AT-190721. †MM + MI for SH was calculated from the malleus (AT-3746) and the incus (AT-3747) belonging to the temporal bone AT-190722. The same value has been used for the Neanderthals. ‡MS: the values of Cr. 5 and AT-5518 have been measured directly, and the mean value of both specimens have been used for the rest of the SH and Neanderthal samples.
Extended Data Fig. 3 Sound power transmission (SPT) values and Exact test comparisons for H. sapiens, Neanderthals and SH.
Sound power transmission (SPT) at the entrance to the cochlea relative to P0 = 10−18 W for an incident plane wave intensity of 10−12 W/m2. In bold P < 0.05.
Extended Data Fig. 4 Comparison between values previously published and the present study for the occupied bandwidth and sound power transmission in three SH individuals.
Sound power transmission (SPT) at the entrance to the cochlea relative to P0 = 10−18 W for an incident plane wave intensity of 10−12 W/m2.
Extended Data Fig. 5 Results of the Exact test for the occupied bandwidth and sound power transmission between P. troglodytes and the SH sample.
Previous data for P. troglodytes sample21. Sound power transmission (SPT) at the entrance to the cochlea was calculated relative to P0 = 10−18 W for an incident plane wave intensity of 10−12 W/m2. In bold P < 0.05.
Extended Data Fig. 6 Correlations between the occupied bandwidth and anatomical variables calculated on the pooled modern human, SH and Neanderthal sample.
OBW = Occupied bandwidth; VAD = Volume of aditus; VMA = Volume of mastoid air cells; VMEC = Volume of tympanic cavity; LAD = Length of aditus; RAD(exit) = Radius of aditus exit; RAD(entrance) = Radius of aditus entrance; LEAC (Comp) = Complete length of external auditory canal; ATM = Area of tympanic membrane; AEAC = Cross-sectional area of the external auditory canal; AFP = Area of stapes footplate. In bold P < 0.05.
Extended Data Fig. 7 Results of the Exact test for the anatomical variables in the H. sapiens, SH and Neanderthal samples.
VAD = Volume of aditus; VMA = Volume of mastoid air cells; VMEC = Volume of tympanic cavity; LAD = Length of aditus; RAD(exit) = Radius of aditus exit; RAD(entrance) = Radius of aditus entrance; LEAC (Comp) = Complete length of external auditory canal; ATM = Area of tympanic membrane; AEAC = Cross-sectional area of the external auditory canal; AFP = Area of stapes footplate. In bold P < 0.05.
Extended Data Fig. 8 3D model of the external and middle ear cavities of La QuinaH5 showing the measurement of the variables used to estimate the sound power transmission through the outer and middle ear.
a, Complete 3D model of the ear structures showing the volumes of the mastoid air cells (VMA), of the aditus (VAD) and of the middle ear cavity (VMEC). b, 3D model of the aditus ad antrum showing measurement of the aditus exit (AAD(exit)), length (LAD) and entrance (AAD(entrance)). c, 3D model of the temporal bone and external auditory canal (EAC) showing the measurement of the length of the bony EAC (LEAC). d, 3D model of the EAC showing measurement of the size of the tympanic membrane (RTM1 and RTM2) and cross-section of the EAC (AEAC). e, 3D model of the oval window showing the measurement of the area (AOW). See Extended Data Fig. 9 for measurement definitions.
Supplementary information
Rights and permissions
About this article
Cite this article
Conde-Valverde, M., Martínez, I., Quam, R.M. et al. Neanderthals and Homo sapiens had similar auditory and speech capacities. Nat Ecol Evol 5, 609–615 (2021). https://doi.org/10.1038/s41559-021-01391-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41559-021-01391-6