Cranial biomechanics in basal urodeles: the Siberian salamander (Salamandrella keyserlingii) and its evolutionary and developmental implications

Zupeng Zhou,Pavel P Skutschas,Jordi Marcé-Nogué,Josep Fortuny

doi:10.1038/s41598-017-10553-1

Abstract

Developmental changes in salamander skulls, before and after metamorphosis, affect the feeding capabilities of these animals. How changes in cranial morphology and tissue properties affect the function of the skull are key to decipher the early evolutionary history of the crown-group of salamanders. Here, 3D cranial biomechanics of the adult Salamandrella keyserlingii were analyzed under different tissue properties and ossification sequences of the cranial skeleton. This helped unravel that: (a) Mechanical properties of tissues (as bone, cartilage or connective tissue) imply a consensus between the stiffness required to perform a function versus the fixation (and displacement) required with the surrounding skeletal elements. (b) Changes on the ossification pattern, producing fontanelles as a result of bone loss or failure to ossify, represent a trend toward simplification potentially helping to distribute stress through the skull, but may also imply a major destabilization of the skull. (c) Bone loss may be originated due to biomechanical optimization and potential reduction of developmental costs. (d) Hynobiids are excellent models for biomechanical reconstruction of extinct early urodeles.

Highlights

Skeletal development of urodeles is mainly influenced by their complex life history: developing morphologically and ecologically distinctive larval and postmetamorphic stages, and undergoing metamorphosis, neoteny or direct development as different developing modes[1,2,3]
The objectives pursued in this study are to (a) describe the feeding biomechanics of the adult Siberian salamander Salamandrella keyserlingii, a small, terrestrial Eurasian hynobiid; (b) discuss the biomechanical patterns that affects the skulls of the crown-group salamanders by comparing with the primitive cryptobranchids and derived groups of salamanders; and (c) discuss the implications of the ossification pattern of the skull roof for feeding biomechanics and its evolutionary and developmental implications
The Siberian salamander, as well as other modern hynobiids[6, 28], retain many cranial morphological features that are widely distributed among more basal Middle Jurassic-Early Cretaceous crown-group taxa

Summary

Introduction

Skeletal development of urodeles (crown-group salamanders) is mainly influenced by their complex life history: developing morphologically and ecologically distinctive larval and postmetamorphic stages, and undergoing metamorphosis, neoteny or direct development as different developing modes[1,2,3]. The objectives pursued in this study are to (a) describe the feeding biomechanics of the adult Siberian salamander Salamandrella keyserlingii, a small, terrestrial Eurasian hynobiid (total length less than 12 cm, but see Kuzmin[25] for size discussion); (b) discuss the biomechanical patterns that affects the skulls of the crown-group salamanders by comparing with the primitive cryptobranchids and derived groups of salamanders (e.g. dicamptodontids); and (c) discuss the implications of the ossification pattern of the skull roof for feeding biomechanics and its evolutionary and developmental implications To achieve these goals, a postmetamorphic skull of S. keyserlingii was digitized and analyzed by 3D Finite Element Analysis (FEA) (Figs 1 and 2). It should be noted that broad cranial fontanelles in different regions of the skull, such as between parietals and frontals, even in large or old adults have been described as covered by connective tissue (collagen)[27]

Methods

Results

Conclusion