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Evaluations of bone strength in the evolutionary invasion of land by tetrapods

Periodic Reporting for period 1 - TETRAPODBONES (Evaluations of bone strength in the evolutionary invasion of land by tetrapods)

Reporting period: 2016-08-22 to 2018-08-21

How tetrapods (four-limbed vertebrates with digits) became terrestrial is one of the most transformative yet enigmatic events in the evolution of vertebrate animals. While it is generally accepted that the earliest tetrapods were aquatic, how early stem tetrapods took their first steps onto land is still an active area of enquiry. One of the prevailing theories on the evolution of terrestrial locomotion is that the initial stages resembled the lateral sequence walking gait of extant salamanders. Yet, a recent analysis on the limb mobility of an early stem tetrapod, Ichthyostega, indicated that it was not capable of performing the rotary motions necessary for a lateral sequence walking gait, raising a suspicion that a salamander-like waiting gait was not the earliest form of terrestrial locomotion. We conducted one of the first studies to test the popular ‘salamander walk’ hypothesis, that a salamander-like lateral sequence walk was the first form of terrestrial locomotion, and tests this hypothesis in a novel way. Our overall objective was to build dynamic 3D musculoskeletal models of salamander limbs in order to evaluate the mechanics of a lateral sequence walk and advance knowledge of locomotor aspects related to the water-to-land transition, by adding a new focus on how limb muscles impose stresses on bones. By synthesizing a comprehensive data on musculoskeletal function from a modern analogue to stem tetrapods, important form-function relationships between limb bone morphology and locomotor behaviours can be clarified and serves as a solid foundation in which to develop more accurate models of stem tetrapods in the future. Identifying the ancestral condition for terrestrial locomotion is an important step towards understanding the diversification of all tetrapods thereafter. Moreover, tracing back the evolutionary steps to becoming terrestrial yields powerful insights into the tetrapod body plan, informing how ecological transitions influence functional innovation and how human anatomy is influenced by our ancestry from aquatic tetrapods.
We have integrated muscle anatomy with bone microstructure, geometry, and applied loads to develop one of the most realistic reconstructions of salamander walking to date in order to assess the emergent properties of limb bones in the context of moving on land. A dynamic 3D musculoskeletal model of the forelimb in an adult tiger salamander (Ambystoma tigrinum) was built to simulate limb mechanics during terrestrial walking. The components of this interactive 3D musculoskeletal model included bones, joints, segment masses, and segment moments of inertia that were obtained from salamander cadavers. These data were then integrated with empirical data on the locomotor motions (kinematics) and forces (kinetics) experienced during walking in A. tigrinum. Simulations of the musculoskeletal model indicated that walking was primarily driven by motions at the shoulder and wrist. In addition, simulated muscles generally followed functions presumed in previous research with the exception that novel stabilizing functions were revealed, demonstrating the powerful insights that can be gleaned from such comprehensive computer models. Data were collected and partially processed for creating and analyzing the hindlimb model.

Information on the research have been disseminated at the 2017 Society for Experimental Biology meeting in Gothenburg, Sweden, and an invited seminar to the Palaeobiology group at the University of Bristol that was made accessible to the public through the Palaeocast podcast series. In addition, aspects related to the biomechanics of the evolutionary invasion of land by tetrapods were communicated to the public at the Royal Veterinary College Open Day event through an interactive outreach display. A journal publication on this work is in development, and ~2 others are planned to follow. The Fellow terminated the post early to accept an Assistant Professor faculty position in the U.S.A. at California State University in Long Beach, but this collaboration will continue.
Over twenty musculotendon units were mapped onto the salamander forelimb bones.
Screenshot of our 3D musculoskeletal model of the forelimb in an adult tiger salamander.