Skip to main content

Advertisement

Log in

Disparate Heterochronic Processes in Baleen Whale Evolution

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

Abstract

Skulls of living baleen whales show distinctive patterns of heterochronic ontogenetic change with implications for mysticete evolution. Here, three baleen whale species are analysed and considered in a heterochronic context. Landmarks show that, during ontogeny, skull morphology changes significantly in the rorqual Balaenoptera borealis and humpback Megaptera novaeangliae (both Balaenopteridae), while the pygmy right whale Caperea marginata (Cetotheriidae: Neobalaeninae) retains an overall juvenile morphology from foetus to adult. Geometric morphometric analyses show that foetal and adult C. marginata are similar, whereas the balaenopterids are more disparate: foetal M. novaeangliae and B. borealis appear in one group, and adult M. novaeangliae and B. borealis are grouped closely. Heterochrony involves paedomorphosis for Caperea, and peramorphosis for the balaenopterids. Heterochrony might cause limited or released developmental constraints, leading to low taxonomic diversity in the single surviving species of neobalaenine, and higher diversity amongst balaenopterids.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Armfield, B. A., George, J. C., Vinyard, C. J., & Thewissen, J. G. M. (2011). Allometric patterns of fetal head growth in mysticetes and odontocetes: Comparison of Balaena mysticetus and Stenella attenuata. Marine Mammal Science, 27(4), 819–827.

    Article  Google Scholar 

  • Armfield, B. A., Zheng, Z., Bajpai, S., Vinyard, C. J., & Thewissen, J. G. M. (2013). Development and evolution of the unique cetacean dentition. PeerJ, 1, e24. doi:10.7717/peerj.24.

    Article  PubMed Central  PubMed  Google Scholar 

  • Bhullar, B.-A. S., Marugán-Lobón, J., Racimo, F., Bever, G. S., Rowe, T. B., Norell, M. A., et al. (2012). Birds have paedomorphic dinosaur skulls. Nature, 487(7406), 223–226.

    Article  CAS  PubMed  Google Scholar 

  • Bininda-Emonds, O. R. P., Jeffrey, J. E., & Richardson, M. K. (2003). Is sequence heterochrony an important evolutionary mechanism in mammals? Journal of Mammalian Evolution, 10(4), 335–361.

    Article  Google Scholar 

  • Bisconti, M. (2012). Comparative osteology and phylogenetic relationships of Miocaperea pulchra, the first fossil pygmy right whale genus and species (Cetacea, Mysticeti, Neobalaenidae). Zoological Journal of the Linnean Society, 166(4), 876–911.

    Article  Google Scholar 

  • Bisconti, M., Lambert, O., & Bosselaers, M. (2013). Taxonomic revision of Isocetus depauwi (Mammalia, Cetacea, Mysticeti) and the phylogenetic relationships of archaic ‘cetothere’ mysticetes. Palaeontology, 56(1), 95–127.

    Article  Google Scholar 

  • Boessenecker, R. W. (2013). Pleistocene survival of an archaic dwarf baleen whale (Mysticeti: Cetotheriidae). Naturwissenschaften, 100(4), 365–371.

    Article  CAS  PubMed  Google Scholar 

  • Brakefield, P. M. (2006). Evo–devo and constraints on selection. Trends in Ecology & Evolution, 21(7), 362–368.

    Article  Google Scholar 

  • Deméré, T. A., McGowen, M. R., Berta, A., & Gatesy, J. (2008). Morphological and molecular evidence for a stepwise evolutionary transition from teeth to baleen in mysticete whales. Systematic Biology, 57(1), 15–37.

    Article  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 

  • Fordyce, R. E. (1980). Whale evolution and Oligocene southern ocean environments. Palaeogeography, Palaeoclimatology, Palaeoecology, 31(2–4), 319–336.

    Article  Google Scholar 

  • Fordyce, R. E., & Marx, F. G. (2013). The pygmy right whale Caperea marginata: The last of the cetotheres. Proceedings of the Royal Society B: Biological Sciences, 280(1753), 1–6.

    Google Scholar 

  • Fortey, R. A., Briggs, D. E. G., & Wills, M. A. (1996). The Cambrian evolutionary ‘explosion’: Decoupling cladogenesis from morphological disparity. Biological Journal of the Linnean Society, 57(1), 13–33.

    Google Scholar 

  • Fortune, S. M. E., Trites, A. W., Perryman, W. L., Moore, M. J., Pettis, H. M., & Lynn, M. S. (2012). Growth and rapid early development of North Atlantic right whales (Eubalaena glacialis). Journal of Mammalogy, 93(5), 1342–1354.

    Article  Google Scholar 

  • Galatius, A. (2010). Paedomorphosis in two small species of toothed whales (Odontoceti): How and why? Biological Journal of the Linnean Society, 99(2), 278–295.

    Article  Google Scholar 

  • Galatius, A., Andersen, M. B. E. R., Haugan, B., Langhoff, H. E., & Jespersen, Å. (2006). Timing of epiphyseal development in the flipper skeleton of the harbour porpoise (Phocoena phocoena) as an indicator of paedomorphosis. Acta Zoologica, 87(1), 77–82.

    Article  Google Scholar 

  • Galatius, A., & Gol’din, P. E. (2011). Geographic variation of skeletal ontogeny and skull shape in the harbour porpoise (Phocoena phocoena). Canadian Journal of Zoology, 89(9), 869–879.

    Article  Google Scholar 

  • Geisler, J. H., McGowen, M. R., Yang, G., & Gatesy, J. (2011). A supermatrix analysis of genomic, morphological, and paleontological data from crown Cetacea. BMC Evolutionary Biology, 11(1), 112. doi:10.1186/1471-2148-11-112.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Goldbogen, J. A., Calambokidis, J., Friedlaender, A. S., Francis, J., DeRuiter, S. L., Stimpert, A. K., et al. (2013). Underwater acrobatics by the world’s largest predator: 360° rolling manoeuvres by lunge-feeding blue whales. Biology Letters, 9(1), 20120986. doi:10.1098/rsbl2012.0986.

    Article  PubMed Central  PubMed  Google Scholar 

  • Goldbogen, J. A., Potvin, J., & Shadwick, R. E. (2010). Skull and buccal cavity allometry increase mass-specific engulfment capacity in fin whales. Proceedings of the Royal Society B: Biological Sciences, 277(1683), 861–868.

    Article  PubMed Central  PubMed  Google Scholar 

  • Gould, S. J. (1977). Ontogeny and phylogeny. Cambridge, MA: The Belknap press of Harvard University Press.

    Google Scholar 

  • Gould, S. J. (2002). The integration of constraint and adaptation (structure and function) in ontogeny and phylogeny: Historical constraints and the evolution of development. In S. J. Gould (Ed.), The structure of evolutionary theory (pp. 1025–1178). Cambridge, MA: The Belknap Press of Harvard University Press.

    Google Scholar 

  • Hampe, O., & Baszio, S. (2010). Relative warps meet cladistics: A contribution to the phylogenetic relationships of baleen whales based on landmark analyses of mysticete crania. Bulletin of Geosciences, 85(2), 199–218.

    Article  Google Scholar 

  • Houben, A. J. P., Bijl, P. K., Pross, J., Bohaty, S. M., Passchier, S., Stickley, C. E., et al. (2013). Reorganization of Southern Ocean plankton ecosystem at the onset of Antarctic glaciation. Science, 340(6130), 341–344.

    Article  CAS  PubMed  Google Scholar 

  • Koyabu, D., Endo, H., Mitgutsch, C., Suwa, G., Catania, K. C., Zollikofer, C. P. E., et al. (2011). Heterochrony and developmental modularity of cranial osteogenesis in lipotyphlan mammals. EvoDevo, 2(1), 1–19.

    Article  Google Scholar 

  • Marx, F. G. (2011). The more the merrier? A large cladistic analysis of mysticetes, and comments on the transition from teeth to baleen. Journal of Mammalian Evolution, 18(2), 77–100.

    Article  Google Scholar 

  • Marx, F. G., Buono, M. R., Fordyce, R. E., & Boessenecker, R. W. (2013). Juvenile morphology: A clue to the origins of the most mysterious of mysticetes? Naturwissenschaften, 100(3), 257–261.

    Article  CAS  PubMed  Google Scholar 

  • Marx, F. G., & Uhen, M. D. (2010). Climate, critters, and cetaceans: Cenozoic drivers of the evolution of modern whales. Science, 327(5968), 993–996.

    Article  CAS  PubMed  Google Scholar 

  • Maynard Smith, J., Burian, R., Kauffman, S., Alberch, P., Campbell, J., Goodwin, B., et al. (1985). Developmental constraints and evolution: A perspective from the Mountain Lake conference on development and evolution. The Quarterly Review of Biology, 60(3), 265–287.

    Article  Google Scholar 

  • McKinney, M. L., & McNamara, K. J. (1991). Heterochrony: The evolution of ontogeny. New York: Plenum Press.

    Book  Google Scholar 

  • McLellan, W. A., Koopman, H. N., Rommel, S. A., Read, A. J., Potter, C. W., Nicolas, J. R., et al. (2002). Ontogenetic allometry and body composition of harbour porpoises (Phocoena phocoena, L.) from the western North Atlantic. Journal of Zoology, 257(4), 457–471.

    Article  Google Scholar 

  • McNamara, K. J. (1986). A guide to the nomenclature of heterochrony. Journal of Paleontology, 60(1), 4–13.

    Google Scholar 

  • McNamara, K. J., & Long, J. A. (2012). The role of heterochrony in dinosaur evolution. In M. K. Brett-Surman, T. R. J. Holtz, & J. O. Farlow (Eds.), The complete dinosaur. Life of the past (2nd ed., pp. 779–802). Indiana: Indian University Press.

    Google Scholar 

  • Mead, J. G., & Fordyce, R. E. (2009). The therian skull: A lexicon with emphasis on the odontocetes. Smithsonian contributions to zoology, 627, 1–248.

    Article  Google Scholar 

  • Mellor, L., Cooper, L. N., Torre, J., & Brownell, R. L, Jr. (2009). Paedomorphic ossification in porpoises with an emphasis on the vaquita (Phocoena sinus). Aquatic Mammals, 35(2), 193–202.

    Article  Google Scholar 

  • Miller, G. S. (1923). The telescoping of the cetacean skull. Smithsonian Miscellaneous Collections, 76(5), 1–71.

    Google Scholar 

  • Murphy, S., & Rogan, E. (2006). External morphology of the short-beaked common dolphin, Delphinus delphis: Growth, allometric relationships and sexual dimorphism. Acta Zoologica, 87(4), 315–329.

    Article  Google Scholar 

  • Nakamura, G., Kato, H., & Fujise, Y. (2012). Relative growth of the skull of the common minke whale Balaenoptera acutorostrata from the North Pacific in comparison to other Balaenoptera species. Mammal Study, 37(2), 105–112.

    Article  Google Scholar 

  • Perrin, W. F. (1975). Variation of spotted and spinner porpoise (Genus Stenella) in the eastern Pacific and Hawaii. Bulletin of the Scripps Institution of Oceanography, University of California, 21, 1–206.

    Google Scholar 

  • Pocock, K. J. (1970). The Emuellidae, a new family of trilobites from the Lower Cambrian of South Australia. Palaeontology, 13(4), 522–562.

    Google Scholar 

  • Pyenson, N. D., Goldbogen, J. A., & Shadwick, R. E. (2013). Mandible allometry in extant and fossil Balaenopteridae (Cetacea: Mammalia): The largest vertebrate skeletal element and its role in rorqual lunge feeding. Biological Journal of the Linnean Society, 108(3), 586–599.

    Article  Google Scholar 

  • Pyenson, N. D., Goldbogen, J. A., Vogl, A. W., Szathmary, G., Drake, R. L., & Shadwick, R. E. (2012). Discovery of a sensory organ that coordinates lunge feeding in rorqual whales. Nature, 485(7399), 498–501.

    Article  CAS  PubMed  Google Scholar 

  • Raff, R. A. (1996). It’s not all heterochrony. In R. A. Raff (Ed.), The shape of life: Genes, development, and the evolution of animal form (pp. 255–291). Chicago: The University of Chicago Press.

    Google Scholar 

  • Read, A. J., & Tolley, K. A. (1997). Postnatal growth and allometry of harbour porpoises from the Bay of Fundy. Canadian Journal of Zoology, 75(1), 122–130.

    Article  Google Scholar 

  • Rice, D. W. (1998). Marine mammals of the world: Systematics and distribution. Lawrence, KS: Society for Marine Mammalogy.

    Google Scholar 

  • Richardson, M. K., & Oelschläger, H. A. (2002). Time, pattern, and heterochrony: A study of hyperphalangy in the dolphin embryo flipper. Evolution & development, 4(6), 435–444.

    Article  Google Scholar 

  • Ridewood, W. G. (1923). Observations on the skull in foetal specimens of whales of the genera Megaptera and Balaenoptera. Philosophical Transactions of the Royal Society of London. Series B Containing Papers of a Biological Character, 211(382–390), 209–272.

    Article  Google Scholar 

  • Rohlf, F. J. (2010). tpsRelw, version 1.11 (software). http://life.bio.sunysb.edu/ee/rohlf/software.html.

  • Rohlf, F. J. (2012). tpsUtil, version 1.55 (software). http://life.bio.sunysb.edu/ee/rohlf/software.html.

  • Rohlf, F. J. (2013). tpsDig, version 2.17 (software). http://life.bio.sunysb.edu/ee/rohlf/software.html.

  • Roston, R. A., Lickorish, D., & Buchholtz, E. A. (2013). Anatomy and age estimation of an early blue whale (Balaenoptera musculus) fetus. The Anatomical Record, 296(4), 709–722.

    PubMed  Google Scholar 

  • Sánchez-Villagra, M. R., Goswami, A., Weisbecker, V., Mock, O., & Kuratani, S. (2008). Conserved relative timing of cranial ossification patterns in early mammalian evolution. Evolution & development, 10(5), 519–530.

    Article  Google Scholar 

  • Seilacher, A. (1970). Arbeitskonzept zur Konstruktions-Morphologie. Lethaia, 3(4), 393–396.

    Article  Google Scholar 

  • Shashikant, C. S., Kim, C. B., Borbély, M. A., Wang, W. C. H., & Ruddle, F. H. (1998). Comparative studies on mammalian Hoxc8 early enhancer sequence reveal a baleen whale-specific deletion of a cis-acting element. Proceedings of the National Academy of Sciences, 95(26), 15446–15451.

    Article  CAS  Google Scholar 

  • Simpson, G. G. (1945). The principles of classification and a classification of mammals. Bulletin of the AMNH; v. 85. Bulletin of the American Museum of Natural History, 85, 1–350.

    Google Scholar 

  • Smith, K. K. (1997). Comparative patterns of craniofacial development in eutherian and metatherian mammals. Evolution, 51(5), 1663–1678.

    Article  Google Scholar 

  • Steeman, M. E., Hebsgaard, M. B., Fordyce, R. E., Ho, S. Y. W., Rabosky, D. L., Nielsen, R., et al. (2009). Radiation of extant cetaceans driven by restructuring of the oceans. Systematic Biology, 58(6), 573–585.

    Article  PubMed Central  PubMed  Google Scholar 

  • Valentine, J. W. (1994). Late Precambrian bilaterians: Grades and clades. Proceedings of the National Academy of Sciences, 91(15), 6751–6757.

    Article  CAS  Google Scholar 

  • Walsh, B. M., & Berta, A. (2011). Occipital ossification of balaenopteroid mysticetes. The Anatomical Record, 294(3), 391–398.

    Article  PubMed  Google Scholar 

  • Winge, H. (1921). A review of the interrelationships of the Cetacea. Smithsonian Miscellaneous Collections, 72(8), 1–97.

    Google Scholar 

  • Yamada, T. K., Chou, L.-S., Chantrapornsyl, S., Adulyanukosol, K., Chakravarti, S. K., Oishi, M., et al. (2006). Middle sized balaenopterid whale specimens (Cetacea: Balaenopteridae) preserved at several institutions in Taiwan, Thailand, and India. Memoirs of the National Science Museum, Tokyo, 44, 1–10.

    Google Scholar 

Download references

Acknowledgments

We thank Kenneth McNamara, Anders Galatius and Oliver Hampe for reviewing the manuscript; Anton van Helden, Tadasu Yamada, Naoki Kohno, Erich Fitzgerald and Karen Roberts for access to collections, allowing photography and discussion during Tsai’s and/or Fordyce’s visits; Robert Boessenecker and Yoshihiro Tanaka for earlier review and comments; Gabriel Aguirre and Felix Marx for discussion; Robert Boessenecker and Felix Marx for providing photographs; Alexander Werth and an anonymous reviewer for their constructive comments. Erich Fitzgerald and Karen Roberts kindly accommodated Tsai in Melbourne. This study is part of Tsai’s PhD thesis, supported by a University of Otago Postgraduate Scholarship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cheng-Hsiu Tsai.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 45 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tsai, CH., Fordyce, R.E. Disparate Heterochronic Processes in Baleen Whale Evolution. Evol Biol 41, 299–307 (2014). https://doi.org/10.1007/s11692-014-9269-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-014-9269-4

Keywords

Navigation