Letter | Published:

Eocene evolution of whale hearing

Nature volume 430, pages 776778 (12 August 2004) | Download Citation

Subjects

Abstract

The origin of whales (order Cetacea) is one of the best-documented examples of macroevolutionary change in vertebrates1,2,3. As the earliest whales became obligately marine, all of their organ systems adapted to the new environment. The fossil record indicates that this evolutionary transition took less than 15 million years, and that different organ systems followed different evolutionary trajectories. Here we document the evolutionary changes that took place in the sound transmission mechanism of the outer and middle ear in early whales. Sound transmission mechanisms change early on in whale evolution and pass through a stage (in pakicetids) in which hearing in both air and water is unsophisticated. This intermediate stage is soon abandoned and is replaced (in remingtonocetids and protocetids) by a sound transmission mechanism similar to that in modern toothed whales. The mechanism of these fossil whales lacks sophistication, and still retains some of the key elements that land mammals use to hear airborne sound.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    What is a whale? Science 263, 180–181 (1994)

  2. 2.

    & in Secondary Adaptation of Tetrapods to Life in Water (eds Mazin, J. -M. & de Buffrénil, V.) 169–233 (Verlag Dr. Friedrich Pfeil, München, 2001)

  3. 3.

    & The early radiations of Cetacea (Mammalia): Evolutionary pattern and developmental correlations. Annu. Rev. Ecol. Syst. 33, 73–90 (2002)

  4. 4.

    Evolutionary principles of the mammalian middle ear. Adv. Anat. Embryol. Cell Biol. 55, 1–70 (1978)

  5. 5.

    The middle ear of the Archaeoceti. J. Vertebr. Paleontol. 10, 117–127 (1990)

  6. 6.

    in Sensory Abilities of Cetaceans (eds Thomas, J. A. & Kastelein, R. A.) 137–162 (Plenum, New York, 1990)

  7. 7.

    , , & Origin of whales in epicontinental remnant seas: New evidence from the early Eocene of Pakistan. Science 220, 403–406 (1983)

  8. 8.

    & Origin of underwater hearing in whales. Nature 361, 444–445 (1993)

  9. 9.

    , , , & The anatomy of the killer whale middle ear (Orcinus orca). Hear. Res. 133, 61–70 (1999)

  10. 10.

    , & A model of the odontocete middle ear. Hear. Res. 133, 82–97 (1999)

  11. 11.

    , & Modeling whale audiograms: effects of bone mass on high-frequency hearing. Hear. Res. 151, 221–226 (2001)

  12. 12.

    in Handbook of Sensory Physiology (eds Keidel, W. D. & Neff, W. D.) Vol. V/1, 491–517 (Springer, Berlin, 1974)

  13. 13.

    in The Emergence of Whales (ed. Thewissen, J. G. M.) 269–301 (Kluwer Academic/Plenum, New York, 1998)

  14. 14.

    & in The Skull (eds Hanken, J. & Hall, B. K.) 241–302 (Univ. Chicago Press, Chicago, 1993)

  15. 15.

    A new concept of bone conduction. Arch. Otolaryng. 87, 49–54 (1968)

  16. 16.

    Scaling of the mammalian middle ear. Hear. Res. 85, 18–30 (1995)

  17. 17.

    , & What middle ear parameters tell about impedance matching and high-frequency hearing. Hear. Res. 85, 31–44 (1995)

  18. 18.

    The walrus auditory region and the monophyly of pinnipeds. Am. Mus. Novit. 2871, 1–31 (1987)

  19. 19.

    Middle ear structures in fossorial mammals: a comparison with non-fossorial species. J. Zool. 255, 467–486 (2001)

  20. 20.

    in Marine Bio-Acoustics (ed. Tavolga, W. N.) 317–336 (Pergamon, Oxford, 1964)

  21. 21.

    , & Assessment of dolphin (Tursiops truncatus) auditory sensitivity and hearing loss using headphones. J. Acoust. Soc. Am. 109, 1717–1722 (2001)

  22. 22.

    in The Emergence of Whales (ed. Thewissen, J. G. M.) 29–61 (Kluwer Academic/Plenum, New York, 1998)

  23. 23.

    & Terrestrial Mesonychia to aquatic Cetacea: Transformation of the basicranium and evolution of hearing in whales. Univ. Mich. Pap. Paleontol. 31, 1–98 (1999)

  24. 24.

    Hearing in extinct cetaceans as determined by cochlear structure. J. Paleontol. 50, 133–152 (1976)

  25. 25.

    in The Evolutionary Biology of Hearing (eds Webster, D. B., Fay, R. R. & Popper, A. N.) 717–750 (Springer, New York, 1992)

  26. 26.

    et al. Evolution of cetacean osmoregulation. Nature 381, 379–380 (1996)

  27. 27.

    , , , & Vestibular evidence for the evolution of aquatic behaviour in early cetaceans. Nature 417, 163–166 (2002)

  28. 28.

    Land-to-sea transition in early whales: evolution of Eocene Archaeoceti (Cetacea) in relation to skeletal proportions and locomotion of living semiaquatic mammals. Paleobiology 29, 429–454 (2003)

  29. 29.

    & Evolutionarily stable configurations: functional integration and the evolution of phenotypic stability. Evol. Biol. 31, 155–217 (2000)

  30. 30.

    , , & Scaling of the cetacean middle ear. Hear. Res. 133, 71–81 (1999)

Download references

Acknowledgements

We thank E. Blum, K. Grecco and F. Spoor for help with CT scans; W. Lancaster for information about basilosauroid ossicles; M. Filon for artwork; and S. Hemilä, S. Madar, T. Reuter and L. Sundström for commenting on the manuscript. J. Schiebout (Louisiana State University) and H. Baagøe and M. Andersen (Zoological Museum, University of Copenhagen) loaned specimens. The Geological Survey of Pakistan assisted in the collection and loan of some of the fossils. Financial support was provided to J.G.M.T by the National Science Foundation and to S.B. by the Department of Science of Technology of India.

Author information

Affiliations

  1. Department of Anatomy, Northeastern Ohio Universities College of Medicine, Rootstown, Ohio 44272, USA

    • Sirpa Nummela
    •  & J. G. M. Thewissen
  2. Department of Earth Sciences, Indian Institute of Technology, Roorkee 427 667, Uttaranchel, India

    • Sunil Bajpai
  3. Department of Anatomy, Howard University, College of Medicine, Washington DC 20059, USA

    • S. Taseer Hussain
  4. Wadia Institute of Himalayan Geology, Dehradun 248 001, India

    • Kishor Kumar

Authors

  1. Search for Sirpa Nummela in:

  2. Search for J. G. M. Thewissen in:

  3. Search for Sunil Bajpai in:

  4. Search for S. Taseer Hussain in:

  5. Search for Kishor Kumar in:

Competing interests

The authors declare that they have no competing financial interests.

Corresponding author

Correspondence to J. G. M. Thewissen.

Supplementary information

Word documents

  1. 1.

    Supplementary Figure 1

    Rostrolateral view of RUSB 2828, with tympanic.

  2. 2.

    Supplementary Figure 2

    Rostrolateral view of RUSB 2828, without tympanic.

  3. 3.

    Supplementary Figure 3

    Ventral view of RUSB 2828, with tympanic.

  4. 4.

    Supplementary Figure 4

    Ventral view of RUSB 2828, without tympanic.

  5. 5.

    Supplementary Data

    List of specimens studied for this research..

  6. 6.

    Supplementary Methods

    Description of how the drawings in Fig. 1f-g were prepared, and the origin of data presented in Fig. 3.

  7. 7.

    Supplementary Table 1

    Ossicular masses, tympanic membrane and/or tympanic plate areas for those data points of Fig. 3 for which the numerical values have not been published elsewhere.

  8. 8.

    Supplementary Discussion

    Background information for the sound transmission mechanisms in odontocetes and mysticetes, in connection to Fig. 2. Additional information as for the systematic relationships in Fig. 4.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature02720

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.