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Heterochrony and developmental modularity of cranial osteogenesis in lipotyphlan mammals

Daisuke Koyabu12*, Hideki Endo2, Christian Mitgutsch1, Gen Suwa2, Kenneth C Catania3, Christoph PE Zollikofer4, Sen-ichi Oda5, Kazuhiko Koyasu6, Motokazu Ando7 and Marcelo R Sánchez-Villagra1

Author Affiliations

1 Paläontologisches Institut und Museum, Universität Zürich, Karl Schmid-Strasse 4, CH-8006 Zürich, Switzerland

2 The University Museum, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, 113-0033 Tokyo, Japan

3 Department of Biological Sciences, Vanderbilt University, VU Station B, Box 35-1634, Nashville, USA

4 Anthropologisches Institut, Universität Zürich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland

5 Department of Zoology, Okayama University of Science, Ridaichou, Kita-ku, 700-0005 Okayama, Japan

6 The Second Department of Anatomy, School of Dentistry, Aichi-Gakuin University, Kusumotochou 1-100, 464-8650 Nagoya, Japan

7 Faculty of Agriculture, Tokyo University of Agriculture, Funako 1737, 243-0034 Atsugi, Japan

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EvoDevo 2011, 2:21  doi:10.1186/2041-9139-2-21

Published: 1 November 2011



Here we provide the most comprehensive study to date on the cranial ossification sequence in Lipotyphla, the group which includes shrews, moles and hedgehogs. This unique group, which encapsulates diverse ecological modes, such as terrestrial, subterranean, and aquatic lifestyles, is used to examine the evolutionary lability of cranial osteogenesis and to investigate the modularity of development.


An acceleration of developmental timing of the vomeronasal complex has occurred in the common ancestor of moles. However, ossification of the nasal bone has shifted late in the more terrestrial shrew mole. Among the lipotyphlans, sequence heterochrony shows no significant association with modules derived from developmental origins (that is, neural crest cells vs. mesoderm derived parts) or with those derived from ossification modes (that is, dermal vs. endochondral ossification).


The drastic acceleration of vomeronasal development in moles is most likely coupled with the increased importance of the rostrum for digging and its use as a specialized tactile surface, both fossorial adaptations. The late development of the nasal in shrew moles, a condition also displayed by hedgehogs and shrews, is suggested to be the result of an ecological reversal to terrestrial lifestyle and reduced functional importance of the rostrum. As an overall pattern in lipotyphlans, our results reject the hypothesis that ossification sequence heterochrony occurs in modular fashion when considering the developmental patterns of the skull. We suggest that shifts in the cranial ossification sequence are not evolutionarily constrained by developmental origins or mode of ossification.

skull; heterochrony; Eulipotyphla; embryology; ossification; integration; phylogeny; micro CT