Skip to main content
SpringerLink
Log in

Naming an Innominate: Pelvis and Hindlimbs of Miocene Whales Give an Insight into Evolution and Homology of Cetacean Pelvic Girdle

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Cetaceans have highly transformed pelvic and hindlimb bones as a secondary adaptation to an aquatic lifestyle. Paleontological records of these bones are very scarce, which hampers interpretations of their homology and evolution. Newly found innominates, femora and tibia of Miocene baleen whales of family Cetotheriidae have primitive structure, which makes it possible to compare them with archaeocetes. As a result, a traditional view of a cetacean innominate as containing vestiges of all three pelvic bones and acetabulum is corroborated by new data and interpretations. A part of ischium (possibly, the superior ramus) is reduced in modern whales, but its vestige can sometimes be observed. A developmental mechanism underlying this pattern can hypothetically involve alterations in Pbx1 and Pbx2, Prrx1 and Prrx2, Pit1 or BMP7 expression: the observed anatomy is similar to reported cases of BMP7 mutations, which are combined with previously reported alterations in Shh regulation. Thus, pelvic and hindlimb reduction in modern cetaceans can in some aspects be compared to ‘Mermaid Syndrome’.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abel, O. (1907). Die Morphologie der Hüftrudimente der Cetaceen. Denkschriften der Kaiserlichen Akademie der Wissenschaften, 81, 139–195.

    Google Scholar 

  • Amasaki, H., Ishikawa, H., & Daigo, M. (1988). Developmental changes of the fore-and hind-limbs in the fetuses of the southern minke whale, Balaenoptera acutorostrata. Anatomischer Anzeiger, 169(2), 145–148.

    Google Scholar 

  • Andrews, R. C. (1921). A remarkable case of external hind limbs in a humpback whale. American Museum Novitates, 9, 1–6.

    Google Scholar 

  • Arvy, L. (1979). The abdominal bones of cetaceans. Investigations on Cetacea, 10, 215–227.

    Google Scholar 

  • Bajpai, S., Thewissen, J. G. M., & Sahni, A. (2009). The origin and early evolution of whales: Macroevolution documented on the Indian Subcontinent. Journal of Biosciences, 34(5), 673–686.

    Article  CAS  PubMed  Google Scholar 

  • Benham, W. B. (1937). Fossil Cetacea of New Zealand. IV.Notes on some of the bones of Kekenodon onamata Hector. Transactions of the Royal Society of New Zealand, 67, 15–20.

    Google Scholar 

  • Berzin, A. A. (1971). The sperm whale. Moscow: Pishchevaya Promyshlennost. (in Russian).

    Google Scholar 

  • Bouetel, V., & de Muizon, C. (2006). The anatomy and relationships of Piscobalaena nana (Cetacea, Mysticeti), a Cetotheriidae s.s. from the early Pliocene of Peru. Geodiversitas, 28, 319–395.

    Google Scholar 

  • Capellini, T. D., Handschuh, K., Quintana, L., Ferretti, E., Di Giacomo, G., Fantini, S., et al. (2011). Control of pelvic girdle development by genes of the Pbx family and Emx2. Developmental Dynamics, 240(5), 1173–1189.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fitzgerald, E. M. G. (2010). The morphology and systematics of Mammalodon colliveri (Cetacea: Mysticeti), a toothed mysticete from the Oligocene of Australia. Zoological Journal of the Linnean Society, 158(2), 367–476.

    Article  Google Scholar 

  • Flower, W. H. (1885). An introduction to the osteology of the Mammalia (3rd ed.). London: Macmillan and Co.

    Google Scholar 

  • Fordyce, R. E. (1978). The morphology and systematics of New Zealand Fossil Cetacea. PhD Thesis, University of Canterbury, Christchurch.

  • Fordyce, R. E., Goedert, J. L., Barnes, L. G., & Crowley, B. J. (2000). Pelvic girdle elements of Oligocene and Miocene Mysticeti: Whale hind legs in transition. Journal of Vertebrate Paleontology, 20, 41A.

    Google Scholar 

  • Garrido-Allepuz, C., González-Lamuño, D., & Ros, M. A. (2012). Sirenomelia phenotype in Bmp7;Shh Compound Mutants: A novel experimental model for studies of caudal body malformations. PLoS ONE, 7(9), e44962. doi:10.1371/journal.pone.0044962.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gingerich, P. D., Smith, B. H., & Simons, E. L. (1990). Hind limbs of Basilosaurus isis: Evidence of feet in whales. Science, 229, 154–157.

    Article  Google Scholar 

  • Gol’din, P. E. (2012). Unusual anatomy of a pelvic bone in the harbor porpoise Phocoena phocoena (Cetacea, Phocoenidae). Scientific Notes Of Taurida V.I. Vernadsky National University. Series Biology, Chemistry, 25(4), 21–25 (In Russian).

  • Gol’din, P., Startsev, D., Krakhmalnaya, T. (2013). The anatomy of a late Miocene baleen whale Cetotherium riabinini from Ukraine. Acta Palaeontologica Polonica. doi:http://dx.doi.org/10.4202/app.2012.0107.

  • Gol’din, P., & Zvonok, E. (2013). Basilotritus uheni, a new cetacean (Cetacea, Basilosauridae) from the late Middle Eocene of Eastern Europe. Journal of Paleontology, 87(2), 254–268.

    Article  Google Scholar 

  • Gray, H. (1918). Anatomy of the human body. Philadelphia: Lea & Febiger.

    Google Scholar 

  • Guldberg, G. (1899). Neue Untersuchungen über die Rudimente von Hinterflossen und die Milchdrüsenanlage bei jungen Delphinembryonen. Internationale Monatsschrift für Anatomie und Physiologie, 16, 301–321.

    Google Scholar 

  • Hofstein, I. D. (1965). Materials on fossil cetaceans from the Geological Museum of the USSR Academy of Sciences in Kiev. Paleontologichesky Sbornik Lvovskogo Gosudarstvennogo Universiteta, 1(2), 25–29. [In Russian].

    Google Scholar 

  • Howell, A. B. (1930). Aquatic mammals, their adaptation to life in the water. Illinois: Thomas.

    Google Scholar 

  • Hulbert, R. C, Jr, Petkewich, R. M., Bishop, G. A., Bukry, D., & Aleshire, D. P. (1998). A new middle Eocene protocetid whale (Mammalia: Cetacea: Archaeoceti) and associated biota from Georgia. Journal of Paleontology, 72, 907–927.

    Google Scholar 

  • Itou, J., Kawakami, H., Quach, T., Osterwalder, M., Evans, S. M., Zeller, R., et al. (2012). Islet1 regulates establishment of the posterior hindlimb field upstream of the Hand2-Shh morphoregulatory gene network in mouse embryos. Development, 139(9), 1620–1629.

    Article  CAS  PubMed  Google Scholar 

  • Jena, N., Martín-Seisdedos, C., McCue, P., & Croce, C. M. (1997). BMP7 null mutation in mice: Developmental defects in skeleton, kidney, and eye. Experimental Cell Research, 230(1), 28–37.

    Google Scholar 

  • Kellogg, R. (1936). A review of the Archaeoceti. Carnegie Institute of Washington Publication, 482, 1–366.

    Google Scholar 

  • Krawchuk, D., Weiner, S. J., Chen, Y. T., Lu, B. C., Costantini, F., Behringer, R. R., et al. (2010). Twist1 activity thresholds define multiple functions in limb development. Developmental Biology, 347, 133–146.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kuijper, S., Beverdam, A., Kroon, C., Brouwer, A., Candille, S., Barsh, G., et al. (2005). Genetics of shoulder girdle formation: Roles of Tbx15 and aristaless-like genes. Development, 132, 1601–1610.

    Article  CAS  PubMed  Google Scholar 

  • Lönnberg, E. (1938). Notes on the skeleton of Prodelphinus graffmani Lönnb. Arkiv för zoologi, 30A(20), 1–21.

    Google Scholar 

  • Lucas, F. A. (1900). The pelvic girdle of Zeuglodon, Basilosaurus cetoides (Owen), with notes on other portions of the skeleton. Proceedings of the US Natural Museum, 23, 327–331.

    Article  Google Scholar 

  • Martínez Cáceres, M., de Muizon, C., Lambert, O., Bianucci, G., Salas Gismondi, R., & Urbina Schmidt, M. (2011). A toothed mysticete from the Middle Eocene to Lower Oligocene of the Pisco Basin, Peru: new data on the origin and feeding evolution of Mysticeti. Sixth triennial conference on secondary adaptation of tetrapods to life in water, pp. 56–57.

  • Omura, H. (1978). Preliminary report on morphological study of pelvic bones of the minke whale from the Antarctic. Scientific Reports of the Whales Research Institute, 30, 271–279.

    Google Scholar 

  • Packard, E. L., & Kellogg, R. (1934). A new cetothere from the Miocene Astoria Formation of Newport, Oregon. Contributions to Palaeontology Carnegie Institution of Washington, 447, 3–62.

    Google Scholar 

  • Panman, L., Drenth, T., Tewelscher, P., Zuniga, A., & Zeller, R. (2005). Genetic interaction of Gli3 and Alx4 during limb development. International Journal of Developmental Biology, 49(4), 443–448.

    CAS  PubMed  Google Scholar 

  • Sedmera, D., Misek, I., & Klima, M. (1997). On the development of Cetacean extremities: I. Hind limb rudimentation in the Spotted dolphin (Stenella attenuata). European Journal of Morphology, 35(1), 25–30.

    Article  CAS  PubMed  Google Scholar 

  • Shapiro, M. D., Bell, M. A., & Kingsley, D. M. (2006). Parallel genetic origins of pelvic reduction in vertebrates. Proceedings of the National Academy of Sciences, 103(37), 13753–13758.

    Article  CAS  Google Scholar 

  • Simões-Lopes, P., & Gutstein, C. (2004). Notes on the anatomy, positioning and homology of the pelvic bones in small cetaceans (Cetacea, Delphinidae, Pontoporiidae). Latin American Journal of Aquatic Mammals, 3(2), 157–162.

    Article  Google Scholar 

  • Struthers, J. (1871). Some points in the anatomy of a Great Fin-Whale. Journal of Anatomy and Physiology, 6, 107–124.

    Google Scholar 

  • Struthers, J. (1881). On the bones, articulations, and muscles of the rudimentary hind-limb of the Greenland Right-Whale (Balaena mysticetus). Journal of Anatomy and Physiology, 15, 141–176.

    Google Scholar 

  • ten Berge, D., Brouwer, A., Korving, J., Martin, J. F., & Meijlink, F. (1998). Prx1 and Prx2 in skeletogenesis: Roles in the craniofacial region, inner ear and limbs. Development, 125(19), 3831–3842.

    PubMed  Google Scholar 

  • Thewissen, J. G. M., Cooper, L. N., George, J. C., & Bajpai, S. (2009). From land to water: The origin of whales, dolphins, and porpoises. Evolution: Education and Outreach, 2, 272–288.

  • Thewissen, J. G. M., Cohn, M. J., Stevens, L. S., Bajpai, S., Heyning, J., & Horton, W. E. (2006). Developmental basis for hind-limb loss in dolphins and origin of the cetacean bodyplan. Proceedings of the National Academy of Sciences, 103(22), 8414–8418.

    Google Scholar 

  • Thewissen, J. G. M., & Fish, F. E. (1997). Locomotor evolution in the earliest cetaceans: Functional model, modern analogues, and paleontological evidence. Paleobiology, 23(4), 482–490.

    Google Scholar 

  • Uhen, M. D. (1999). New species of protocetid archaeocete whale, Eocetus wardii (Mammalia: Cetacea) from the middle Eocene of North Carolina. Journal of Paleontology, 73, 512–528.

    Google Scholar 

  • Uhen, M. D. (2004). Form, function, and anatomy of Dorudon atrox (Mammalia, Cetacea): An archaeocete from the middle to late Eocene of Egypt. The University of Michigan Museum of Paleontology Papers on Paleontology, 34, 1–222.

    Google Scholar 

  • Uhen, M. D. (2014). New material of Natchitochia jonesi and a comparison of the innominata and locomotor capabilities of Protocetidae. Marine Mammal Science,. doi:10.1111/mms.12100.

    Google Scholar 

  • Zakin, L., Reversade, B., Kuroda, H., Lyons, K. M., & De Robertis, E. M. (2005). Sirenomelia in Bmp7 and Tsg compound mutant mice: requirement for Bmp signaling in the development of ventral posterior mesoderm. Development, 132(10), 2489–2499.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

I sincerely thank Dmitry Startsev who donated the specimen TNU KB2 for this study and participated in the field research; Karina Vishnyakova, Elena Gladilina, Valentin Serbin, Aleksandr Miroshnichenko and Oksana Demidenko who took part in the field research; Nobumichi Tamura, Vitaly Melnik and Robert Boessenecker who kindly provided their artwork of extinct cetaceans; Manuel Martínez Cáceres for a fruitful discussion, Felix Marx, Mark D. Uhen, Richard C. Hulbert and Varvara Semyonova for providing literature necessary for this study; two anonymous reviewers for comments to the earlier draft of the manuscript and Benedikt Hallgrimsson for the editorial remarks.

Conflict of interest

The author declares that he has no conflict of interest.

Author information

Authors and Affiliations

  1. Taurida National University, 4, Vernadsky Avenue, Simferopol, Crimea, 95007, Ukraine

    Pavel Gol’din

Authors
  1. Pavel Gol’din
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pavel Gol’din.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gol’din, P. Naming an Innominate: Pelvis and Hindlimbs of Miocene Whales Give an Insight into Evolution and Homology of Cetacean Pelvic Girdle. Evol Biol 41, 473–479 (2014). https://doi.org/10.1007/s11692-014-9281-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-014-9281-8

Keywords

Search

Navigation