The nature of aspidin and the evolutionary origin of bone

Abstract

Bone is the key innovation underpinning the evolution of the vertebrate skeleton, yet its origin is mired by debate over interpretation of the most primitive bone-like tissue, aspidin. This has variously been interpreted as cellular bone, acellular bone, dentine or an intermediate of dentine and bone. The crux of the controversy is the nature of unmineralized spaces pervading the aspidin matrix, which have alternatively been interpreted as having housed cells, cell processes or Sharpey’s fibres. Discriminating between these hypotheses has been hindered by the limits of traditional histological methods. Here, we use synchrotron X-ray tomographic microscopy to reveal the nature of aspidin. We show that the spaces exhibit a linear morphology incompatible with interpretations that they represent voids left by cells or cell processes. Instead, these spaces represent intrinsic collagen fibre bundles that form a scaffold about which mineral was deposited. Aspidin is thus acellular dermal bone. We reject hypotheses that it is a type of dentine, cellular bone or transitional tissue. Our study suggests that the full repertoire of skeletal tissue types was established before the divergence of the earliest known skeletonizing vertebrates, indicating that the corresponding cell types evolved rapidly following the divergence of cyclostomes and gnathostomes.

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Fig. 1: Hypothesis of vertebrate relations based on Keating and Donoghue17.
Fig. 2: Morphology and histology of the heterostracan dermal skeleton.
Fig. 3: Histology of aspidin in phylogenetically disparate heterostracan taxa.
Fig. 4: SrXTM virtual segmentation of aspidin spaces in L. dairydinglensis and T. tesselata.

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Acknowledgements

We thank J. Cunningham (University of Bristol), M. Rucklin (Naturalis, Leiden) and C. Martinez-Perez (University of Valencia) for beamline assistance, E. Bernard (NHM, London) for collections services, and S. Kearns (University of Bristol) for assistance at the Bristol Earth Sciences Microprobe Facility. We thank G. Koentges (University of Warwick) and I. Sansom (University of Birmingham) for discussion. J.N.K. was funded by a NERC Studentship. P.C.J.D. is funded by the NERC (NE/P013678/1, NE/N002067/1 and NE/G016623/1) and BBSRC (BB/N000919/1). C.L.M. completed this work in partial fulfilment of the MSc Palaeobiology at the University of Bristol.

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J.N.K. and P.C.J.D. conceived the project. P.C.J.D. and C.L.M. prepared the histological sections. J.N.K., F.M. and P.C.J.D. collected the tomographic data. J.N.K. and C.L.M. processed the tomographic data. All authors contributed towards data interpretation and writing of the manuscript.

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Correspondence to Joseph N. Keating or Philip C. J. Donoghue.

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Keating, J.N., Marquart, C.L., Marone, F. et al. The nature of aspidin and the evolutionary origin of bone. Nat Ecol Evol 2, 1501–1506 (2018). https://doi.org/10.1038/s41559-018-0624-1

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