Skip to main content
SpringerLink
Log in

Timing of ontogenetic changes of two cranial regions in Sotalia guianensis (Delphinidae)

  • Original Investigation
  • Published:
Mammalian Biology Aims and scope Submit manuscript

Abstract

Despite the fact that heterochronic processes seem to be an important process determining morphological evolution of the delphinid skull, previous workers have not found allometric scaling as relevant factor in the differentiation within the genus Sotalia. Here we analyzed the skull ontogeny of the estuarine dolphin S. guianensis and investigate differential growth and shape changes of two cranial regions - the neurocranium and the face – in order to evaluate the relevance of cranial compartmentalization on the ontogeny of this structure. Our results show that, even though both cranial regions stop growing at adulthood, the face has higher initial growth rates than the neurocranium. The rate of shape changes is also different for both regions, with the face showing a initially higher, but rapidly decreasing rate of change, while the neurocranium shows a slow decreasing rate, leading to persistent and localized shape changes throughout adult life, a pattern that could be related to epigenetic regional factors. The pattern of ontogenetic shape change described here is similar to those described for other groups of Delphinidae and also match intra and interspecific variation found within the family, suggesting that mosaic heterochrony could be an important factor in the morphological evolution of this group.

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

Similar content being viewed by others

References

  • Ackermann, R., Cheverud, J.M., 2000. Phenotypic covariance structure in tamarins (genus Saguinus): a comparison of variation patterns using matrix correlation and common principal component analysis. Am. J. Phys. Anthropol. 111, 489.

    Article  CAS  PubMed  Google Scholar 

  • Alberch, P., Gould, S.J., Oster, G., Wake, D.B., 1979. Size and shape in ontogeny and phylogeny. Paleobiology 5, 296–317.

    Article  Google Scholar 

  • Borobia, M., 1989. Distribution and Morphometrics of South American Dolphins of the Genus Sotalia. Macdonald College of McGill University, Montreal, Canada.

    Google Scholar 

  • Borobia, M., Siciliano, S., Lodi, L., Hoek, W., 1991. Distribution of the South American dolphin Sotalia fluviatilis. Canadian Journal of Zoology 69, 1025–1039.

    Article  Google Scholar 

  • Cheverud, J.M., 1982. Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution 36, 499–516.

    Article  PubMed  Google Scholar 

  • David, B., 1990. Mosaic pattern of heterochronies: variation and diversity in Pourtalesiidae (deep-sea echinoids). Evolutionary Biology 24, 297–327.

    Google Scholar 

  • Di Beneditto, A.P.M., Ramos, R.M.A., 2004. Biology of the marine tucuxi (Sotalia fluviatilis) in south-eastern Brazil. J. Mar. Biol. Assoc. U.K. 84, 1245–1250.

    Article  Google Scholar 

  • Dryden, I., 2009. Shapes: Statistical Shape Analysis. R Package Version 1.1-3, http://CRAN.R-project.org/package=shapes.

  • Falconer, D.S., Mackay, T., 1996. An Introduction to Quantitative Genetics. Wiley Press, London.

    Google Scholar 

  • Fettuccia, D.C., da Silva, V.M.F., Simões-Lopes, P.C., 2009. Non-metric characters in two species of Sotalia (Gray, 1866) (Cetacea, Delphinidae). Braz. J. Biol. 69, 907–917.

    Article  CAS  PubMed  Google Scholar 

  • Galatius, A., 2010. Paedomorphosis in two small species of toothed whales (Odontoceti): how and why? Biol. J. Linn. Soc. 99, 278–295.

    Article  Google Scholar 

  • Galatius, A., Gol’din, P.E., 2011. Geographic variation of skeletal ontogeny and skull shape in the harbour porpoise (Phocoena phocoena). Can. J. Zool. 89, 869–879.

    Article  Google Scholar 

  • Galatius, A., Berta, A., Frandsen, M.S., Goodal, R.N.P., 2011. Interspecific variation of ontogeny and skull shape among porpoises (Phocoenidae). J. Morphol. 272, 136–148.

    Article  PubMed  Google Scholar 

  • Geise, L., Borobia, M., 1987. New Brazilian records for Kogia, Pontoporia, Grampus, and Sotalia (Cetacea, Physeteridae, Platanistidae, and Delphinidae). J. Mammal. 68, 873–875.

    Article  Google Scholar 

  • Goswami, A., 2006. Cranial modularity shifts during mammalian evolution. Am. Nat. 168, 270–280.

    Article  PubMed  Google Scholar 

  • Hallgrímsson, B., Lieberman, D.E., Liu, W., Ford-Hutchinson, A.F., Jirik, F.R., 2007. Epigenetic interactions and the structureof phenotypic variation inthe cranium. Evol. Dev. 9, 76–91.

    Article  PubMed  Google Scholar 

  • Klingenberg, C.P., 2009. Morphometric integration and modularity in configurations of landmarks: tools for evaluating a-priori hypotheses. Evol. Dev. 11, 405–421.

    Article  PubMed  PubMed Central  Google Scholar 

  • Loy, A., Tamburelli, A., Carlini, R., Slice, D.E., 2010. Craniometric variation of some Mediterranean and Atlantic populations of Stenella coeruleoalba (Mammalia, Delphinidae): a three-dimensional geometric morphometric analysis. Mar. Mammal Sci.. 27, E65–E78.

    Article  Google Scholar 

  • Macleod, C.D., Reidenberg, J.S., Weller, M., Santos, M.B., Herman, J., Goold, J., Pierce, G.J., 2007. Breaking symmetry: the marine environment, prey size, and the evolution of asymmetry in cetacean skulls. Anat. Rec. 290, 539–545.

    Article  CAS  Google Scholar 

  • Manly, B.F.J., 1997. Randomization, Bootstrap and Monte Carlo Methods in Biology. Chapman and Hall, London, 461 pp.

  • Marroig, G., Cheverud, J.M., 2001. A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of New World monkeys. Evolution 55, 2576–2600.

    Article  CAS  PubMed  Google Scholar 

  • Mitteroecker, P., Bookstein, F., 2008. The evolutionary role of modularity and integration in the hominoid cranium. Evolution 62, 943–958.

    Article  PubMed  Google Scholar 

  • Mitteroecker, P., Gunz, P., Weber, G., Bookstein, F., 2004. Regional dissociated heterochrony in multivariate analysis. Ann. Anat. 186, 463–470.

    Article  CAS  PubMed  Google Scholar 

  • Monteiro-Filho, E.L., Monteiro, L.R., Reis, S.F., 2002. Skull shape and size divergence in dolphins of the genus Sotalia: a tridimensional morphometric analysis. J. Mammal. 83, 125–134.

    Article  Google Scholar 

  • Monteiro-Filho, E.L.A., Filla, G.F., Santos, M.R., Domit, C., Oliveira, L.V., Lima, J.S., 2006. Gênero Sotalia. In: Monteiro-Filho, L.A., Aranha, J.M.R. (orgs.) Revisões em Zoologia I. SEMA/PR, 391 pp.

  • Moore, W.J., 1981. The Mammalian Skull. Cambridge University Press, New York, 369p.

    Google Scholar 

  • Porto, A.G.C., 2009. Evolução da modularidade no crânio de mamíferos. Masters Dissertation. Universidade de São Paulo, São Paulo, Brasil.

    Google Scholar 

  • Porto, A.G.C., Oliveira, F.B., Shirai, L.T., Conto, V., Marroig, G., 2009. The evolution of modularity in the mammalian skull. I. Morphological integration patterns and magnitudes. Evol. Biol. 36, 118–135.

    Google Scholar 

  • R Development Core Team, 2010. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Available at: http://www.R-project.org.

  • Radinsky, L.B., 1981. Evolution of skull shape in carnivores 1. Representative modern carnivores. Biol. J. Linn. Soc. 15, 369–388.

    Article  Google Scholar 

  • Ramos, R.M.A., Rosas, F.C.W., Simões-Lopes, P.C., Zanelatto, R., Dans, S., Crespo, E.A., 2008. Estimativa de idade. In: Monteiro-Filho, E.L.A., Monteiro, K.D.K.A. (Eds.), Biologia Ecologia e Conservação do Boto-Cinza. Páginas & Letras Editora e Gráfica, São Paulo, Brazil, pp. 193–209.

    Google Scholar 

  • Reynolds, W.W., 1977. Skeleton weight allometry in aquatic and terrestrial vertebrates. Hydrobiologia 56, 35–37.

    Article  Google Scholar 

  • Rohlf, F.J., 1998. Onapplications of geometric morphometrics tostudiesofontogeny and phylogeny. Syst. Biol. 47, 147–158.

    Article  CAS  PubMed  Google Scholar 

  • Rohlf, F.J., Corti, M., 2000. Use of two-block partial least-squares to study covariation in shape. Syst. Biol. 49, 740–753.

    Article  CAS  PubMed  Google Scholar 

  • Rohlf, F.J., Slice, D., 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst. Biol. 39, 40–59.

    Google Scholar 

  • Rosas, F.C.W., Barreto, A.S., 2008. Reproduç ão e Crescimento. In: Monteiro-Filho, E.L.A., Monteiro, K.D.K.A. (Eds.), Biologia Ecologia e Conservação do Boto-Cinza. Páginas & Letras Editora e Gráfica, São Paulo, Brazil, pp. 51–65.

    Google Scholar 

  • Rosas, F.C.W., Barreto, A.S., Monteiro-Filho, E.L.A., 2003. Age and growth of the estuarine dolphin (Sotalia guianensis) (Cetacea, Delphinidae) on the Paraná coast, Southern Brazil. Fish. Bull. 101, 377–383.

    Google Scholar 

  • Schluter, D., 1996. Adaptive radiation along genetic lines of least resistance. Evolution 50 (5), 1766–1774.

    Article  PubMed  Google Scholar 

  • Shea, B.T., 1983. Allometry and heterochrony in the African apes. Am. J. Phys. Anthropol. 62, 275–289.

    Article  CAS  PubMed  Google Scholar 

  • Simões-Lopes, P.C., 1988. Ocorrência de uma populaç ão de Sotalia fluviatilis Gervais, 1853 (Cetacea, Delphinidae) no limite sul de sua distribuiç ão, Santa Catarina, Brasil. Biotemas 1, 57–62.

    Google Scholar 

  • Simões-Lopes, P.C., Menezes, M.E., 2008. Morfologia Esqueletal. In: Monteiro-Filho, E.L.A., Monteiro, K.D.K.A. (Eds.), Biologia Ecologia e Conservação do Boto-Cinza. Páginas & Letras Editora e Gráfica, São Paulo, Brazil, pp. 17–38.

    Google Scholar 

  • Steppan, S., 1997. Phylogenetic analysis of phenotypic covariance structure II. Reconstructing matrix evolution. Evolution 51, 587–594.

    PubMed  Google Scholar 

  • Sydney, N.V., Monteiro-Filho, E.L.A., 2011. Efficiency of wear and decalcification technique for estimating the age of estuarine dolphin Sotalia guianensis. J. Biosci. 36, 117–121.

    Article  PubMed  Google Scholar 

  • Thomson, D.H., Richardson, W.J., 1995. Marine mammal sounds. In: Richardson, W.J., Greene Jr., C.R., Malme, C.I., Thomson, D.H. (Eds.), Marine Mammals and Noise. Academic Press, San Diego, pp. 159–204.

    Google Scholar 

  • van der Klaauw, C.J., 1946. Cerebral skull and facial skull. Arch. Neerland. Zool. 8, 16–37.

    Article  Google Scholar 

  • Werth, A.J., 2006. Mandibular and dental variation and the evolution of suction feeding in Odontoceti. J. Mammal. 87, 579–588.

    Article  Google Scholar 

  • Yurick, D.B., Gaskin, D.E., 1988. Asymmetry in the skull of the harbour porpoise Phocoena phocoena (L.) and its relationship to sound production and echolocation. Can. J. Zool. 66, 399–402.

    Article  Google Scholar 

  • Zelditch, M.L., Lundrigan, B.L., Sheets, H.D., Garland Jr., T., 2003. Do precocial mammals develop at a faster rate? A comparison of rates of skull development in Sigmodon fulviventer and Mus musculus domesticus. J. Evol. Biol. 16, 708–720.

    Article  PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Both authors contributed equally.

Authors and Affiliations

  1. Programa de Pós-graduação em Zoologia, Universidade Federal do Paraná, Avenida Coronel Francisco Heráclito dos Santos, 210, 81531-970, Curitiba, PR, Brazil

    Nicolle V. Sydney

  2. Programa de Pós-graduação em Zoologia, Instituto de Biociências da USP, Universidade de São Paulo, Rua do Matão, 321, 05508-900, São Paulo, SP, Brazil

    Fabio A. Machado

  3. Museu Biológico do Instituto Butantan, Avenida Vital Brasil, 1500, 05503-900, São Paulo, SP, Brazil

    Erika Hingst-Zaher

Authors
  1. Nicolle V. Sydney
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fabio A. Machado
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Erika Hingst-Zaher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fabio A. Machado.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sydney, N.V., Machado, F.A. & Hingst-Zaher, E. Timing of ontogenetic changes of two cranial regions in Sotalia guianensis (Delphinidae). Mamm Biol 77, 397–403 (2012). https://doi.org/10.1016/j.mambio.2012.04.007

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.mambio.2012.04.007

Keywords

Search

Navigation