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The nature of aspidin and the evolutionary origin of bone

Nature Ecology & Evolution volume 2, pages 1501–1506 (2018)Cite this article

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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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References

  1. Donoghue, P. C. J. & Keating, J. N. Early vertebrate evolution. Palaeontology 57, 879–893 (2014).

    Article  Google Scholar 

  2. Donoghue, P. C. J. & Sansom, I. J. Origin and early evolution of vertebrate skeletonization. Microsc. Res. Tech. 59, 352–372 (2002).

    Article  Google Scholar 

  3. Smith, M. M. & Hall, B. K. Development and evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biol. Rev. 65, 277–373 (1990).

    Article  CAS  Google Scholar 

  4. Halstead, L. B. Calcified tissues in the earliest vertebrates. Calcif. Tissue Int. 3, 107–124 (1969).

    Article  CAS  Google Scholar 

  5. Halstead Tarlo, L. B. Psammosteiformes (Agnatha) - A review with descriptions of new material from the Lower Devonian of Poland. I - General part. Palaeontol. Polonica 13, 1–135 (1964).

    Google Scholar 

  6. Halstead, L. B. The heterostracan fishes. Biol. Rev. 48, 279–332 (1973).

    Article  Google Scholar 

  7. Ørvig, T. Histologic studies of ostracoderms, placoderms and fossil elasmobranchs. 6. Hard tissues of Ordovician vertebrates. Zool. Scr. 18, 427–446 (1989).

    Article  Google Scholar 

  8. Denison, R. H. Ordovician vertebrates from western United States. Fieldiana Geol. 16, 131–192 (1967).

    Google Scholar 

  9. Bystrow, A. P. The microstructure of skeleton elements in some vertebrates from Lower Devonian deposits of the USSR. Acta Zool. 40, 59–83 (1959).

    Article  Google Scholar 

  10. Gross, W. Die fische des mittleren Old Red Südlivlands. Palaeont. Abh. 18, 123–156 (1930).

    Google Scholar 

  11. Gross, W. Histologische studien am aussenskelett fossiler agnathen und fische. Palaeontogr. Abt. A 83, 1–60 (1935).

    Google Scholar 

  12. Donoghue, P. C. J. et al. Synchrotron X-ray tomographic microscopy of fossil embryos. Nature 442, 680–683 (2006).

    Article  CAS  Google Scholar 

  13. Tafforeau, P. et al. Applications of X-ray synchrotron microtomography for non-destructive 3D studies of paleontological specimens. Appl. Phys. A 83, 195–202 (2006).

    Article  CAS  Google Scholar 

  14. Rucklin, M. et al. Development of teeth and jaws in the earliest jawed vertebrates. Nature 491, 748–753 (2012).

    Article  Google Scholar 

  15. Sanchez, S., Ahlberg, P. E., Trinajstic, K. M., Mirone, A. & Tafforeau, P. Three-dimensional synchrotron virtual paleohistology: a new insight into the world of fossil bone microstructures. Microsc. Microanal. 18, 1095–1105 (2012).

    Article  CAS  Google Scholar 

  16. Qu, Q., Blom, H., Sanchez, S. & Ahlberg, P. Three-dimensional virtual histology of Silurian osteostracan scales revealed by synchrotron radiation microtomography. J. Morphol. 276, 873–888 (2015).

    Article  Google Scholar 

  17. Keating, J. N. & Donoghue, P. C. J. Histology and affinity of anaspids, and the early evolution of the vertebrate dermal skeleton. Proc. R. Soc. B 283, 20152917 (2016).

    Article  Google Scholar 

  18. Märss, T. A new Late Silurian or Early Devonian thelodont from the Boothia Peninsula, Arctic Canada. Palaeontology 42, 1079–1099 (1999).

    Article  Google Scholar 

  19. Zhu, M. & Janvier, P. The histological structure of the endoskeleton in galeaspids (Galeaspida, Vertebrata). J. Vertebr. Paleontol. 18, 650–654 (1998).

    Article  Google Scholar 

  20. Rohon, J. V. Die obersilurischen Fische von Oesel. II Theil. Selachii, Dipnoi, Ganoidei, Pteraspidae und Cephalaspidae. Mem. Acad. Sci. St Petersbourg 41, 1–124 (1893).

    Google Scholar 

  21. Halstead Tarlo, L. B. Aspidin: the precursor of bone. Nature 199, 46–48 (1963).

    Article  Google Scholar 

  22. Novitskaya, L. I. in Psammosteids (Agnatha, Psammosteidae) of the Devonian of the USSR (eds Obruchev, D. & Mark-Kurik, E.) 257–282 (Geological Institute of the Estonian Academy of Sciences, 1966).

  23. You, L. D., Weinbaum, S., Cowin, S. C. & Schaffler, M. B. Ultrastructure of the osteocyte process and its pericellular matrix. Anat. Rec. A 278, 505–513 (2004).

    Article  Google Scholar 

  24. Höhling, H., Kreilos, R., Neubauer, G. & Boyde, A. Electron microscopy and electron microscopical measurements of collagen mineralization in hard tissues. Z. Zellforsch. Mikrosk. Anat. 122, 36–52 (1971).

    Article  Google Scholar 

  25. Aaron, J. E. Periosteal Sharpey’s fibers: a novel bone matrix regulatory system. Front. Endocrinol. 3, 1–10 (2012).

    Article  Google Scholar 

  26. Moss, M. L. The biology of acellular teleost fish bone. Ann. NY Acad. Sci. 109, 337–350 (1963).

    Article  CAS  Google Scholar 

  27. Petroll, W. M., Cavanagh, H. D. & Jester, J. V. Dynamic three‐dimensional visualization of collagen matrix remodeling and cytoskeletal organization in living corneal fibroblasts. Scanning 26, 1–10 (2004).

    Article  Google Scholar 

  28. Sawhney, R. K. & Howard, J. Slow local movements of collagen fibers by fibroblasts drive the rapid global self-organization of collagen gels. J. Cell Biol. 157, 1083–1092 (2002).

    Article  CAS  Google Scholar 

  29. Sansom, I. J., Haines, P. W., Andreev, P. & Nicoll, R. S. A new pteraspidomorph from the Nibil Formation (Katian, Late Ordovician) of the Canning Basin, Western Australia. J. Vertebr. Paleontol. 33, 764–769 (2013).

    Article  Google Scholar 

  30. Keating, J. N., Marquart, C. L. & Donoghue, P. C. J. Histology of the heterostracan dermal skeleton: insight into the origin of the vertebrate mineralised skeleton. J. Morphol. 276, 657–680 (2015).

    Article  Google Scholar 

  31. Kawasaki, K., Buchanan, A. V. & Weiss, K. M. Biomineralization in humans: making the hard choices in life. Annu. Rev. Genet. 43, 119–142 (2009).

    Article  CAS  Google Scholar 

  32. Huxley-Jones, J., Robertson, D. L. & Boot-Handford, R. P. On the origins of the extracellular matrix in vertebrates. Matrix Biol. 26, 2–11 (2007).

    Article  CAS  Google Scholar 

  33. Kuraku, S., Meyer, A. & Kuratani, S. Timing of genome duplications relative to the origin of the vertebrates: did cyclostomes diverge before or after? Mol. Biol. Evol. 26, 47–59 (2009).

    Article  CAS  Google Scholar 

  34. Holland, P. W., Garcia-Fernàndez, J., Williams, N. A. & Sidow, A. Gene duplications and the origins of vertebrate development. Development 1994, 125–133 (1994).

    Google Scholar 

  35. Smith, J. J. & Keinath, M. C. The sea lamprey meiotic map improves resolution of ancient vertebrate genome duplications. Genome Res. 25, 1081–1090 (2015).

    Article  CAS  Google Scholar 

  36. Smith, J. J. et al. The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evolution. Nat. Genet. 50, 270–277 (2018).

    Article  CAS  Google Scholar 

  37. Donoghue, P. C. J., Graham, A. & Kelsh, R. N. The origin and evolution of the neural crest. BioEssays 30, 530–541 (2008).

    Article  Google Scholar 

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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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Authors and Affiliations

  1. School of Earth Sciences, University of Bristol, Bristol, UK

    Joseph N. Keating, Chloe L. Marquart & Philip C. J. Donoghue

  2. School of Earth and Environmental Sciences, University of Manchester, Manchester, UK

    Joseph N. Keating

  3. Swiss Light Source, Paul Scherrer Institut, Villigen, Switzerland

    Federica Marone

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  1. Joseph N. Keating
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  2. Chloe L. Marquart
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  4. Philip C. J. Donoghue
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Contributions

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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