Morphology and function of Neandertal and modern human ear ossicles

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 41, 2016, Pages 11489-11494

  Stoessel, Alexander ^a   David, Romain ^a   Gunz, Philipp ^a   Schmidt, Tobias ^b   Spoor, Fred ^a,c   Hublin, Jean Jacques ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b JENA UNIVERSITY HOSPITAL   (Germany)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

3D shape; Covariation; Homo; Middle ear

Indexed keywords

ANATOMICAL VARIATION; ANIMAL EXPERIMENT; ARTICLE; AUDITORY OSSICLE; AUDITORY SYSTEM FUNCTION; BRAIN SIZE; COMPARATIVE STUDY; CONTROLLED STUDY; EARDRUM; HEARING ACUITY; HOLOCENE; HOMO NEANDERTHALENSIS; HUMAN; LAST COMMON ANCESTOR; MICRO-COMPUTED TOMOGRAPHY; MIDDLE EAR; MOLECULAR EVOLUTION; MORPHOMETRICS; NONHUMAN; OVAL WINDOW; PLEISTOCENE; PRIORITY JOURNAL; SPECIES DIFFERENTIATION; TEMPORAL BONE; THREE DIMENSIONAL IMAGING; TISSUE STRUCTURE; ANATOMY AND HISTOLOGY; ANIMAL; EVOLUTION; IMAGE PROCESSING; PATHOLOGY; PRINCIPAL COMPONENT ANALYSIS;

ANIMALS; BIOLOGICAL EVOLUTION; EAR OSSICLES; EAR, MIDDLE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; NEANDERTHALS; PRINCIPAL COMPONENT ANALYSIS;

EID: 84991512361     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1605881113     Document Type: Article

References (75)

1. Coleman MN (2009) What do primates hear? A meta-analysis of all known nonhuman primate behavioral audiograms. IntJ Primatol 30(1):55-91.
2. Elder JH (1934) Auditory acuity of the chimpanzee. J Comp Psychol 17(2):157-183.
3. Elder JH (1935) The upper limit of hearing in chimpanzee. Am J Physiol 112(1):109-115.
4. Heffner RS (2004) Primate hearing from a mammalian perspective. AnatRecA Discov Mol Cell Evol Biol 281(1):1111-1122.
5. Kojima S (1990) Comparison of auditory functions in the chimpanzee and human. Folia Primatol (Basel) 55(2):62-72.
6. Kojima S (2003) A Search for the Origins of Human Speech: Auditory and Vocal Functions of the Chimpanzee (Kyoto Univ Academic Press, Kyoto).
7. Quam R, et al. (2012) Studying audition in fossil hominins: A new approach to the evolution of language. Psychology of Language, ed Jackson M (Nova Science Publishers, Hauppauge, NY), pp 47-95.
8. Brown CH, Waser PM (1984) Hearing and communication in blue monkeys (Cercopithecus mitis). Anim Behav 32(1):66-75.
9. Brown CH, Waser PM (1988) Environmental influences on the structure of primate vocalizations. Primate Vocal Communication, eds Todt D, Goedeking P, Symmes D (Springer, Berlin), pp 51-66.
10. Owren MJ, Hopp SL, Sinnott JM, Petersen MR (1988) Absolute auditory thresholds in three Old World monkey species (Cercopithecus aethiops, C. neglectus, Macaca fuscata) and humans (Homo sapiens). J Comp Psychol 102(2):99-107.
11. Coleman MN, Colbert MW (2010) Correlations between auditory structures and hearing sensitivity in non-human primates. J Morphol 271(5):511-532.
12. Quam R, et al. (2015) Early hominin auditory capacities. Sci Adv 1(8):e1500355.
13. Coleman MN, Ross CF (2004) Primate auditory diversity and its influence on hearing performance. Anat Rec A Discov Mol Cell Evol Biol 281(1):1123-1137.
14. Hemilä S, Nummela S, Reuter T (1995) What middle ear parameters tell about impedance matching and high frequency hearing. Hear Res 85(1-2):31-44.
15. Rosowski JJ (2013) Comparative middle ear structure and function in vertebrates. The Middle Ear, eds Puria S, Fay RR, Popper AN (Springer, New York), pp 31-65.
16. Puria S, Peake WT, Rosowski JJ (1997) Sound-pressure measurements in the cochlear vestibule of human-cadaver ears. J Acoust Soc Am 101(5 Pt 1):2754-2770.
17. Quam RM, Coleman MN, Martínez I (2014) Evolution of the auditory ossicles in extant hominids: Metric variation in African apes and humans. J Anat 225(2):167-196.
18. Stoessel A, Gunz P, David R, Spoor F (2016) Comparative anatomy of the middle ear ossicles of extant hominids-Introducing a geometric morphometric protocol. J Hum Evol 91:1-25.
19. Arensburg B, Pap I, Tillier AM, Chech M (1996) The Subalyuk 2 middle ear stapes. IntJ Osteoarchaeol 6(2):185-188.
20. Gómez-Olivencia A, Crevecoeur I, Balzeau A (2015) La Ferrassie 8 Neandertal child reloaded: New remains and re-assessment of the original collection. J Hum Evol 82:107-126.
21. Lisonek P, Trinkaus E (2006) The auditory ossicles. Early Modern Human Evolution in Central Europe: The People of Dolni Vestonice and Pavlov, eds Trinkaus E, Svoboda J (Oxford Univ Press, Oxford), pp 153-155.
22. Maureille B (2002) A lost Neanderthal neonate found. Nature 419(6902):33-34.
23. Ponce de León MS, Zollikofer CP (1999) New evidence from Le Moustier 1: Computerassisted reconstruction and morphometry of the skull. Anat Rec 254(4):474-489.
24. Quam R, Martínez I, Arsuaga JL (2013) Reassessment of the La Ferrassie 3 Neandertal ossicular chain. J Hum Evol 64(4):250-262.
25. Quam R, Rak Y (2008) Auditory ossicles from southwest Asian Mousterian sites. J Hum Evol 54(3):414-433.
26. Beals ME, Frayer DW, Radovcic J, Hill CA (2016) Cochlear labyrinth volume in Krapina Neandertals. J Hum Evol 90:176-182.
27. Braga J, et al. (2015) Disproportionate cochlear length in genus Homo shows a high phylogenetic signal during apes' hearing evolution. PLoS One 10(6):e0127780.
28. Quam RM (2006) Temporal Bone Anatomy and the Evolution of Acoustic Capacities in Fossil Humans (State University of New York at Binghamton Anthropology Department, Binghamton, NY).
29. Gunz P, et al. (2013) Morphological integration of the bony labyrinth and the cranial base in modern humans and Neandertals. Europ Soc Hum Evol 2013:1-4.
30. Harvati K (2003) Quantitative analysis of Neanderthal temporal bone morphology using three-dimensional geometric morphometrics. Am J Phys Anthropol 120(4):323-338.
31. HeldmaierG, Neuweiler G (2004) Vergleichende Tierphysiologie (Springer, Heidelberg).
32. Masali M, Maffei M, Borgognini Tarli S (1991) Application of a morphometric model for the reconstruction of some functional characteristics of external and middle ear in Circeo 1. The Neandertal Skull Circeo 1-Studies and Documentation, eds Piperno M, Scichilone G (Istituto Poligrafico e Zecca dello Stato-Libreria dello Stato, Rome), pp 321-338.
33. Mason MJ (2016) Structure and function of the mammalian middle ear. II. Inferring function from structure. JAnat 228(2):300-312.
34. Nummela S (1995) Scaling of the mammalian middle ear. Hear Res 85(1-2):18-30.
35. Ruff CB, Trinkaus E, Holliday TW (1997) Body mass and encephalization in Pleistocene Homo. Nature 387(6629):173-176.
36. Harvati K, Frost SR, McNulty KP (2004) Neanderthal taxonomy reconsidered: Implications of 3D primate models of intra- and interspecific differences. Proc Natl Acad Sci USA 101(5):1147-1152.
37. Hublin J-J (2009) Out of Africa: Modern human origins special feature: The origin of Neandertals. Proc Natl Acad Sci USA 106(38):16022-16027.
38. Hublin J-J, Spoor F, Braun M, Zonneveld F, Condemi S (1996) A late Neanderthal associated with Upper Palaeolithic artefacts. Nature 381(6579):224-226.
39. Spoor F, Hublin J-J, Braun M, Zonneveld F (2003) The bony labyrinth of Neanderthals. J Hum Evol 44(2):141-165.
40. Rosowski JJ, Ravicz ME, Songer JE (2006) Structures that contribute to middle-ear admittance in chinchilla. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 192(12):1287-1311.
41. Decraemer WF, de La Rochefoucauld O, Funnell WR, Olson ES (2014) Three-dimensional vibration of the malleus and incus in the living gerbil. J Assoc Res Otolaryngol 15(4):483-510.
42. Puria S, Steele C (2010) Tympanic-membrane and malleus-incus-complex co-adaptations for high-frequency hearing in mammals. Hear Res 263(1-2):183-190.
43. Manley GA (1971) Some aspects of the evolution of hearing in vertebrates. Nature 230(5295):506-509.
44. Ruggero MA, Temchin AN (2002) The roles of the external, middle, and inner ears in determining the bandwidth of hearing. Proc Natl Acad Sci USA 99(20):13206-13210.
45. Martínez I, et al. (2004) Auditory capacities in Middle Pleistocene humans from the Sierra de Atapuerca in Spain. Proc Natl Acad Sci USA 101(27):9976-9981.
46. Martínez I, et al. (2013) Communicative capacities in Middle Pleistocene humans from the Sierra de Atapuerca in Spain. Quat Int 295:94-101.
47. Meyer M, et al. (2016) Nuclear DNA sequences from the Middle Pleistocene Sima de los Huesos hominins. Nature 531(7595):504-507.
48. Lockwood CA, Kimbel WH, Lynch JM (2004) Morphometrics and hominoid phylogeny: Support for a chimpanzee-human clade and differentiation among great ape subspecies. Proc Natl Acad Sci USA 101(13):4356-4360.
49. Trinkaus E (2002) The cranial morphology. Portrait of the Artist as a Child. The Gravettian Human Skeleton from the Abrigo Do Lagar Velho and Its Archeological Context, eds Zilhão J, Trinkaus E (Instituto Português de Arqueologia, Lisbon), pp 256-287.
50. Lieberman DE, Ross CF, Ravosa MJ (2000) The primate cranial base: Ontogeny, function, and integration. Am J Phys Anthropol 31(Suppl):117-169.
51. Spoor F (1997) Basicranial architecture and relative brain size of Sts 5 (Australopithecus africanus) and other Plio-Pleistocene hominids. S AfrJ Sci 93:182-186.
52. Bastir M, et al. (2011) Evolution of the base of the brain in highly encephalized human species. Nat Commun 2:5-8.
53. Hublin JJ, Neubauer S, Gunz P (2015) Brain ontogeny and life history in Pleistocene hominins. Philos Trans R Soc Lond B Biol Sci 370(1663):2-140062.
54. Moggi-Cecchi J, Collard M (2002) A fossil stapes from Sterkfontein, South Africa, and the hearing capabilities of early hominids. J Hum Evol 42(3):259-265.
55. Quam RM, et al. (2013) Early hominin auditory ossicles from South Africa. Proc Natl Acad Sci USA 110(22):8847-8851.
56. Rak Y, Clarke RJ (1979) Ear ossicle of Australopithecus robustus. Nature 279(5708):62-63.
57. Castellano S, et al. (2014) Patterns of coding variation in the complete exomes of three Neandertals. Proc Natl Acad Sci USA 111(18):6666-6671.
58. Scheuer L, Black S, Cunningham C (2000) Developmental Juvenile Osteology (Academic, San Diego).
59. Patil S, Ravi B (2005) Voxel-based representation, display and thickness analysis of intricate shapes. Proceedings of the Ninth International Conference on Computer Aided Design and Computer Graphics (IEEE Computer Society Washington, DC), pp 415-422.
60. Good P (2005) Permutation Tests: A Practical Guide to Resampling Methods for Testing Hypotheses (Springer, New York).
61. Mitteroecker P, Gunz P (2009) Advances in geometric morphometrics. Evol Biol 36(2):235-247.
62. Garland T, Jr, Ives AR (2000) Using the past to predict the present: Confidence intervals for regression equations in phylogenetic comparative methods. Am Nat 155(3):346-364.
63. Rohlf FJ (2001) Comparative methods for the analysis of continuous variables: Geometric interpretations. Evolution 55(11):2143-2160.
64. Rohlf FJ (2006) A comment on phylogenetic correction. Evolution 60(7):1509-1515.
65. De Greef D, et al. (2015) Details of human middle ear morphology based on micro-CT imaging of phosphotungstic acid stained samples. J Morphol 276(9):1025-1046.
66. Endicott P, Ho SY, Stringer C (2010) Using genetic evidence to evaluate four palaeoanthropological hypotheses for the timing of Neanderthal and modern human origins. J Hum Evol 59(1):87-95.
67. Higham T, et al. (2011) Precision dating of the Palaeolithic: A new radiocarbon chronology for the Abri Pataud (France), a key Aurignacian sequence. J Hum Evol 61(5):549-563.
68. Valladas H, et al. (1999) TL dates for the Neanderthal site of the Amud Cave, Israel. J Archaeol Sci 26(3):259-268.
69. Henry-Gambier D (2002) Les fossiles de Cro-Magnon (Les Eyzies-de-Tayac, Dordogne). Nouvelles données sur leur position chronologique et leur attribution culturelle. Bull Mém Soc Anthropol Paris 14:89-112.
70. Blackwell B, Schwarcz HP (1986) U-series analyses of the lower travertine at Ehringsdorf, DDR. Quat Res 25(2):21-5-222.
71. Rink WJ, Schwarcz HP, Smith FH, Radovcic (1995) ESR ages for Krapina hominids. Nature 378(6552):24.
72. Raynal JP (1990) Essai de datation directe. La Chapelle-aux-Saints et la Préhistoire en Corrèze, eds Raynal JP, Pautrat Y (La Nef, Bordeaux, France), pp 43-46.
73. Higham T, et al. (2014) The timing and spatiotemporal patterning of Neanderthal disappearance. Nature 512(7514):306-309.
74. Soressi M, Jones HL, Rink WJ, Maureille B, Tillier AM (2007) The Pech-de-l'Azé I Neandertal child: ESR, uranium-series, and AMS 14C dating of its MTA type B context. J Hum Evol 52(4):455-466.
75. Bar-Yosef O (2002) The chronology of the Middle Paleolithic of the Levant. Neandertals and Modern Humans in Western Asia, eds Akazawa T, Aoki K, Bar-Yosef O (Plenum, New York), pp 39-56.