How to make a limb: a new insight using three-dimensional synchrotron palaeohistology

ongoing

Tetrapods, i.e. four-limbed animals, are the only backboned animals to have truly conquered the land, and have achieved worldwide distribution in a wide range of environments. Several fish groups have attempted to colonise terrestrial habitats (e.g. mudskippers among ray-finned fish; lungfish among lobe-finned fish) but only tetrapods were able to initiate a large-scale radiation. What is the key to this success? Our limb skeletons have obviously played a crucial part, by allowing us to walk and support our weight outside of the water, but that is not their only function. For example, at some point during the early evolution of tetrapods, the haematopoietic (blood cell-producing) tissue transferred to the bone marrow; it has been suggested that this protected the production of blood cells from UV radiation and made it more efficient. This extraordinary multifunctionality evolved through successive microanatomical innovations, beginning 400 million years ago. The underlying reasons and processes are still unclear, partly because traditional palaeontological techniques have not been able to uncover the crucial changes in 3D microarchitecture from fin to limb. I will overcome these limitations using a novel cross-disciplinary approach based on state-of-the-art, three-dimensional, tomographic imaging techniques at high resolution. I will combine 3D modelling with virtual simulations of biomechanical stress, evidence of biomarkers and functional genomics to provide the first comprehensive picture of three major steps in the limb evolution: 1) the shaping of our limb into three segments, 2) the origin of blood-cell production in limb bones, and 3) the role of ossified mineralised ends in the exceptional locomotor radiations of tetrapods. This project will illuminate the process by which our limb skeletons became, not just structural props and locomotory levers, but essential powerhouses of cell manufacture without which we cannot survive.