Research ArticleEVOLUTIONARY BIOLOGY

Early hominin auditory capacities

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Science Advances  25 Sep 2015:
Vol. 1, no. 8, e1500355
DOI: 10.1126/sciadv.1500355
  • Fig. 1 Measurements of the middle and outer ear (A to C) and ear ossicles (D).

    (A), (B), (C1), (C2), and (D) are not drawn to the same scale. (A) to (C) are based on the 3D reconstruction of the left side of HTB 1769 (Pan troglodytes), showing the EAC (gray), the middle ear cavity (green), the aditus ad antrum (red), the mastoid antrum and connected mastoid air cells (blue), the inner ear (orange), and the temporal bone (yellow). P1, limit between the mastoid antrum and the connected mastoid air cells with the aditus ad antrum. P2, entrance to the aditus ad antrum from the middle ear cavity. P3, medial edge of the tympanic groove (sulcus tympanicus). P4, cross section perpendicular to the long axis of the EAC that meets the lateral end of the tympanic groove. (A) VMA, volume of the mastoid antrum and connected mastoid air cells, measured dorsal to P1; VMEC, volume of the middle ear cavity, bounded by P2 to P3. (B) LAD, length of the aditus ad antrum, measured as the distance from the center of P1 to the center of P2; AAD1, area of the exit of the aditus ad antrum to the mastoid antrum and connected mastoid air cells; AAD2, area of the entrance to the aditus ad antrum from the middle ear cavity. For modeling purposes, we have calculated the radius (RAD1 and RAD2; not shown), which would correspond to a circle with the given area for the exit (AAD1) and entrance (AAD2). (C1) LEAC, length of the EAC, measured from the most lateral extent of the tympanic groove (defined by P4) to the spina suprameatum. In Pan, the spina suprameatum is replaced by the superior-most point of the porus acusticus externus. (C2) RTM1, half of the measured greater diameter of the tympanic membrane, measured in P3; RTM2, half of the measured lesser diameter (perpendicular to RTM1) of the tympanic membrane, measured in P3; REAC1 and REAC2, half of the measured diameters of the two major perpendicular axes (superoinferior and mediolateral) of the EAC measured at P4. (D) is based on the profiles of the malleus and incus from the temporal bone AT-1907 and the stapes from Cranium 5. LM, functional length of the malleus, measured as the maximum length from the superior border of the lateral process to the inferior-most tip of the manubrium; LI, functional length of the incus, measured from the lateral-most point along the articular facet to the lowest point along the long crus in the rotational axis; AFP, measured area of the footplate of the stapes.

  • Fig. 2 Model results for chimpanzees, modern humans, and early hominins from 0.5 to 5.0 kHz.

    (A) The occupied band is similar in chimpanzees and early hominins, but is shifted toward slightly higher frequencies in the latter. Modern humans show a widened occupied band that is further extended toward higher frequencies. (B) The sound power transmission curves correspond to decibels at the entrance to the cochlea relative to P0 = 10−18 W for an incident plane wave intensity of 10−12 W/m2. The mean value ± 1.0 SD for each frequency position is shown for each group. Points higher along the curve indicate better sound power transmission and heightened auditory sensitivity. Individual results are provided in figs. S5 to S8.

  • Table 1 Measurements and summary statistics for the skeletal variables in chimpanzees and fossil and recent hominins.
    SpeciesVMAVMECLADRAD1RAD2ATMLEAC (Com)AEACLM/LlAFPMM + MIMS
    Volume mastoid air cells cm3Volume tympanic cavity cm3Length of aditus mmRadius of aditus exit mmRadius of aditus entrance mmArea of tympanic membrane mm2Complete length of external ear canal mmCross-sectional area of EAC mm2Malleus/incus lever ratioArea of stapes footplate mm2Mass of malleus + incus mgMass of stapes mg
    Homo sapiens mean ± SD4.43 ± 2.270.46 ± 0.094.4 ± 0.72.4 ± 0.23.0 ± 0.165.1 ± 5.521.0 ± 2.036.4 ± 7.01.26 ± 0.082.92 ± 0.2149.2 ± 4.42.2 ± 0.6
    Homo sapiens range (n)0.52–8.02 (10)0.33–0.62 (10)3.7–6.3 (10)2.0–2.7 (10)2.8–3.2 (10)56.6–74.0 (10)17.7–23.8 (10)26.5–52.0 (10)1.16–1.40 (7)2.51–3.13 (7)41.3–53.0 (8)1.4–3.2 (8)
    Pan troglodytes mean ± SD8.89 ± 4.730.42 ± 0.115.4 ± 0.82.0 ± 0.32.8 ± 0.382.1 ± 8.237.9 ± 2.623.0 ± 4.41.67 ± 0.112.79 ± 0.3942.0 ± 6.21.4 ± 0.5
    Pan troglodytes range (n)2.25–18.73 (11)0.26–0.62 (11)3.6–6.8 (11)1.5–2.4 (11)2.3–3.3 (11)71.0–102.8 (11)34.2–40.8 (11)16.4–30.3 (11)1.52–1.79 (9)2.40–3.48 (7)35.0–53.0 (8)1.0–2.2 (6)
    Cranium 52.150.548.62.93.982.924.626.42.72
    AT-8484.325.559.43.58
    AT-42182.221.651.52.81
    AT-19073.680.765.23.13.974.824.030.21.19
    AT-41035.900.514.82.93.576.825.531.2
    Atapuerca (SH) mean ± SD3.91 ± 1.890.60 ± 0.146.2 ± 2.13.0 ± 0.13.8 ± 0.280.2 ± 4.224.2 ± 1.639.7 ± 14.71.193.04 ± 0.4752.7
    Atapuerca (SH) range (n)2.15–5.90 (5)0.51–0.76 (3)4.8–8.6 (3)2.9–3.1 (3)3.5–3.9 (3)74.8–84.3 (5)21.6–25.5 (5)26.4–59.4 (5)(1)2.72–3.58 (3)(1)
    SK 462.550.436.11.82.762.327.247.62.44
    SK 472.61
    SK 5240.7
    SK 84869.830.047.2
    SK 8792.43
    SKW 18>3.9267.029.838.81.362.42
    SKW 2581>4.5630.056.1
    SK 140030.534.41.92.863.3
    TM 151770.931.739.6
    Paranthropus robustus mean ± SD2.550.46 ± 0.065.21.82.766.6 ± 3.829.7 ± 1.644.5 ± 6.21.362.48 ± 0.09
    Paranthropus robustus range (n)(1)0.42–0.53 (3)4.4–6.1 (2)1.8–1.9 (2)2.70–2.8 (2)62.3–70.9 (5)27.2–31.7 (5)38.8–56.1 (7)(1)2.42–2.61 (4)
    STS 559.428.4
    STS 250.363.161.828.537.0
    STS 71>27.8
    STW 983.430.234.71.12.157.327.42.31
    STW 151>27.043.62.12
    STW 2552.28
    STW 329>1.190.315.61.82.565.139.51.87
    STW 370>27.0
    STW 49955.555.1
    STW 50530.1
    Australopithecus africanus mean ± SD3.430.30 ± 0.065.11.52.6 ± 0.559.8 ± 3.828.6 ± 1.143.8 ± 8.02.15 ± 0.20
    Australopithecus africanus range (n)(1)0.23–0.36 (3)4.7–5.6 (2)1.1–1.8 (2)2.1–3.1 (3)55.5–65.1 (5)27.4–30.1 (4)37.0–55.1 (4)1.87–2.31 (4)
  • Table 2 Results of the Mann-Whitney U test for the anatomical variables.

    Values in bold indicate a significant difference (P < 0.05). Comparisons are limited to those variables with n > 3 for both taxa compared.

    ChimpanzeesAustralopithecusChimpanzeesChimpanzeesModern humansModern humans
    versusversusversusversusversusversus
    Variablemodern humansParanthropusAustralopithecusParanthropusAustralopithecusParanthropus
    VMA0.016
    VMEC0.4260.1260.014
    LAD0.010
    RAD10.003
    RAD20.0430.4560.287
    ATM<0.0010.032<0.001<0.0010.0750.679
    LEAC<0.0010.5560.001<0.0010.0020.001
    AEAC<0.0010.648<0.001<0.0010.0540.014
    LM/LI<0.001
    AFP0.3180.0290.0060.3150.0060.012
    MM + MI0.038
    MS0.059
  • Table 3 Occupied band and sound power transmission values from 0.5 to 5.0 kHz.

    Negative values are in parentheses. Values in bold are means ± SD.

    Occupied bandSound power at the entrance to the cochlea (SPC)*
    LowerUpperSPC atSPC atSPC atSPC atSPC atSPC atSPC atSPC atSPC atSPC at
    limitlimitBandwidth500 Hz1000 Hz1500 Hz2000 Hz2500 Hz3000 Hz3500 Hz4000 Hz4500 Hz5000 Hz
    Speciesn(Hz)(Hz)(Hz)(db)(db)(db)(db)(db)(db)(db)(db)(db)(db)
    Australopithecus africanus (STW 98)1760339026303.113.79.111.113.514.67.0−2.6−13.3−20.5
    Australopithecus africanus (STS 25)1715331026303.314.59.111.212.611.26.70.7−5.4−12.3
    Paranthropus robustus1830341025802.213.49.611.713.914.48.0−2.4−16.9−6.5
    Pooled early hominins mean ± SD3768 ± 583370 ± 532602 ± 262.9± 0.613.9 ± 0.69.3 ± 0.311.3 ± 0.413.3 ± 0.713.4 ± 1.97.2 ± 0.7(1.4) ± 1.9(11.8) ± 5.9(13.1) ± 7.0
    Pooled early hominins range715–8303310–34102580–26302.2–3.313.4–14.59.1–9.611.1–11.712.6–13.911.2–14.66.7–8.0(−2.6)–0.7(−16.9)–(−5.4)(−20.5)–(−6.5)
    Pan troglodytes mean ± SD11570 ± 543015 ± 1222445 ± 1343.8 ± 1.212.9 ± 1.37.1 ± 0.88.4 ± 1.18.2 ± 1.65.9 ± 1.30.2 ± 2.6(7.0) ± 4.8(10.5) ± 5.3(10.7) ± 6.1
    Pan troglodytes range490–6502750–32052185–26351.6–5.810.5–14.45.8–8.96.9–10.15.9–11.23.2–7.4(−3.2)–3.6(−16.6)–(−2.2)(−22.7)–(−3.6)(−17.5)–(−0.6)
    Atapuerca (SH) mean ± SD5791 ± 933969 ± 1663178 ± 2130.8 ± 0.911.7 ± 1.27.9 ± 0.29.0 ± 0.88.8 ± 1.88.6 ± 2.98.3 ± 2.56.4 ± 2.01.1 ± 1.6(−5.2) ± 2.2
    Atapuerca (SH) range715–9303760–41552830–3365(−0.2)–1.99.7–13.07.6–8.07.9–10.26.5–11.55.3–12.95.3–11.14.8–9.8(−1.1)–2.8(−8.5)–(−3.0)
    Homo sapiens mean ± SD10841 ± 954339 ± 3323498 ± 3490.8 ± 1.710.3 ± 1.88.0 ± 0.49.0 ± 0.79.1 ± 1.18.7 ± 1.58.5 ± 1.88.0 ± 1.85.1 ± 3.2(0.9) ± 5.2
    Homo sapiens range720–10653870–49503035–4230(−3.8)–2.15.5–11.87.4–8.57.8–9.96.9–10.55.7–10.44.9–10.55.3–10.4(−1.2)–10.7(−11.5)–4.6

    *Sound power at the entrance to the cochlea relative to P0 = 10−18 W for an incident plane wave intensity of 10−12 W/m2.

    • Table 4 Mann-Whitney U test results for the occupied band and sound power transmission values from 0.5 to 5.0 kHz.

      Values in bold indicate a significant difference (P < 0.05).

      Chimpanzees versus modern humansEarly hominins versus chimpanzeesEarly hominins versus modern humansEarly hominins versus Atapuerca (SH)Atapuerca (SH) versus modern humans
      Band lower limit<0.0010.0050.2170.7860.371
      Band upper limit<0.0010.0050.0070.0360.028
      Bandwidth<0.0010.1260.0070.0360.075
      SPC at 500 Hz<0.0010.1260.0070.0360.594
      SPC at 1000 Hz<0.0010.2250.0070.0360.075
      SPC at 1500 Hz0.0030.0050.0070.0360.254
      SPC at 2000 Hz0.2820.0050.0070.0360.953
      SPC at 2500 Hz0.2510.0050.0070.0360.679
      SPC at 3000 Hz0.0010.0050.0070.0710.679
      SPC at 3500 Hz<0.0010.0050.2170.7860.953
      SPC at 4000 Hz<0.0010.0880.0070.0360.165
      SPC at 4500 Hz<0.0010.7690.0070.0360.013
      SPC at 5000 Hz0.0010.7690.0140.0710.075
    • Table 5 Results of the discriminant function analysis for the sound power transmission values.
      % Correct classification*Homo sapiensPan troglodytesEarly homininsTotal
      Homo sapiens100.0100010
      Pan troglodytes100.0011011
      Early hominins100.00033
      Total100.01011324

      *All specimens were classified with very high posterior probabilities (>0.99).

      Supplementary Materials

      • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/1/8/e1500355/DC1

        Comparative sample composition

        Preservation of early hominin specimens

        CT scanning of modern human, chimpanzee, and fossil hominin specimens

        Model description

        Comparison of present measurements with previous studies

        Fig. S1. Virtual (3D CT) reconstruction of the outer, middle, and inner ears in P. robustus (SK 46).

        Fig. S2. Model results for the effects of intraindividual measurement error on the sound power transmission in two reconstructions of the CSJ 26 H. sapiens individual.

        Fig. S3. Model results for the effects of interindividual measurement error on the sound power transmission in two reconstructions of the HTB 3434 P. troglodytes individual.

        Fig. S4. Block diagram of the analog electrical circuit model based on (30).

        Fig. S5. Model results for sound power transmission in chimpanzees.

        Fig. S6. Model results for sound power transmission in modern humans.

        Fig. S7. Model results for sound power transmission in the early hominins.

        Fig. S8. Model results for sound power transmission in the Middle Pleistocene Atapuerca (SH).

        Fig. S9. Model results for the magnitude of the middle ear gain (|GME|) in modern humans.

        Fig. S10. Model results for the magnitude of the middle ear gain (|GME|) in chimpanzees.

        Fig. S11. Model results for the magnitude of the middle ear gain (|GME|) in early hominins.

        Fig. S12. Model results for the magnitude of the middle ear gain (|GME|) in the Atapuerca (SH) specimens.

        Table S1. Measurements and model results for the influence of intraindividual measurement error.

        Table S2. Measurements and model results for the influence of interindividual measurement error.

        Table S3. Definition of the electrical parameters, their related anatomical variables, the source of the value used, and the sensitivity analysis for frequencies above 2 kHz in the model.

        Table S4. Measurements in the present study compared with those reported previously.

        References (69112)

      • Supplementary Materials

        This PDF file includes:

        • Comparative sample composition
        • Preservation of early hominin specimens
        • CT scanning of modern human, chimpanzee, and fossil hominin specimens
        • Model description
        • Comparison of present measurements with previous studies
        • Fig. S1. Virtual (3D CT) reconstruction of the outer, middle, and inner ears in P. robustus (SK 46).
        • Fig. S2. Model results for the effects of intraindividual measurement error on the sound power transmission in two reconstructions of the CSJ 26 H. sapiens individual.
        • Fig. S3. Model results for the effects of interindividual measurement error on the sound power transmission in two reconstructions of the HTB 3434 P. troglodytes individual.
        • Fig. S4. Block diagram of the analog electrical circuit model based on (30).
        • Fig. S5. Model results for sound power transmission in chimpanzees.
        • Fig. S6. Model results for sound power transmission in modern humans.
        • Fig. S7. Model results for sound power transmission in the early hominins.
        • Fig. S8. Model results for sound power transmission in the Middle Pleistocene Atapuerca (SH).
        • Fig. S9. Model results for the magnitude of the middle ear gain (|GME|) in modern humans.
        • Fig. S10. Model results for the magnitude of the middle ear gain (|GME|) in chimpanzees.
        • Fig. S11. Model results for the magnitude of the middle ear gain (|GME|) in early hominins.
        • Fig. S12. Model results for the magnitude of the middle ear gain (|GME|) in the Atapuerca (SH) specimens.
        • Table S1. Measurements and model results for the influence of intraindividual measurement error.
        • Table S2. Measurements and model results for the influence of interindividual measurement error.
        • Table S3. Definition of the electrical parameters, their related anatomical variables, the source of the value used, and the sensitivity analysis for frequencies above 2 kHz in the model.
        • Table S4. Measurements in the present study compared with those reported previously.
        • References (69–112)

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