Heterochrony and developmental modularity of cranial osteogenesis in lipotyphlan mammals.

Daisuke Koyabu,Christoph Pe Zollikofer,Gen Suwa,Marcelo R Sánchez-Villagra,Christian Mitgutsch,Hideki Endo,Sen-Ichi Oda,Motokazu Ando,Kazuhiko Koyasu,Kenneth C Catania

doi:10.1186/2041-9139-2-21

Abstract

BackgroundHere 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.ResultsAn 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).ConclusionsThe 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.

Highlights

We provide the most comprehensive study to date on the cranial ossification sequence in Lipotyphla, the group which includes shrews, moles and hedgehogs
With an extensive series of embryonic specimens from a variety of taxa, we present data on cranial ossification sequences for two species of terrestrial hedgehogs (Erinaceus europaeus and E. amurensis), three species of subterranean mole (Mogera wogura, Condylura cristata, and Scapanus orarius), one terrestrial shrew mole (Urotrichus talpoides), one terrestrial shrew (Suncus murinus), and an aquatic water shrew (Chimarrogale platycephala)
The resolution of sequence data for two moles (Talpa europaea and T. occidentalis) and one shrew species (Cryptotis parva) is much improved compared with the data presented in previous literature [6,42,43]. Using this unique group that encapsulates terrestrial, subterranean and aquatic lifestyles, we examine the evolutionary lability and conservatism of cranial osteogenesis and test the hypothesis that skeletal elements belonging to the same module display coordinated shifts of ossification timing while maintaining the relative sequence within the module

Summary

Introduction

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. One of the major aspects of morphological evolution in the mammalian skull is heterochrony, shifts in the timing and rate of development. Most studies have focused on the physical relationships among functionally- or developmentally-related structures, and there are only a few studies relating developmental timing to the concept of modularity [9,10,11,35]

Objectives

Methods

Results

Discussion

Conclusion