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Life history of the stem tetrapod Acanthostega revealed by synchrotron microtomography

Nature volume 537, pages 408–411 (2016)Cite this article

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Abstract

The transition from fish to tetrapod was arguably the most radical series of adaptive shifts in vertebrate evolutionary history. Data are accumulating rapidly for most aspects of these events1,2,3,4,5, but the life histories of the earliest tetrapods remain completely unknown, leaving a major gap in our understanding of these organisms as living animals. Symptomatic of this problem is the unspoken assumption that the largest known Devonian tetrapod fossils represent adult individuals. Here we present the first, to our knowledge, life history data for a Devonian tetrapod, from the Acanthostega mass-death deposit of Stensiö Bjerg, East Greenland6,7. Using propagation phase-contrast synchrotron microtomography (PPC-SRμCT)8 to visualize the histology of humeri (upper arm bones) and infer their growth histories, we show that even the largest individuals from this deposit are juveniles. A long early juvenile stage with unossified limb bones, during which individuals grew to almost final size, was followed by a slow-growing late juvenile stage with ossified limbs that lasted for at least six years in some individuals. The late onset of limb ossification suggests that the juveniles were exclusively aquatic, and the predominance of juveniles in the sample suggests segregated distributions of juveniles and adults at least at certain times. The absolute size at which limb ossification began differs greatly between individuals, suggesting the possibility of sexual dimorphism, adaptive strategies or competition-related size variation.

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Figure 1: Midshaft bone microanatomy and histology of Acanthostega humeri.
Figure 2: Humeral bone development.
Figure 3: Bone skeletochronology.

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Acknowledgements

Beamtime was allocated as inhouse beamtime and thanks to a proposal accepted by the ESRF (EC203, S.S.). This research was supported by an ERC grant (233111, P.E.A.) and a grant from the Vetenskapsrådet (2015-04335, S.S.). The authors thank J. Castanet, J.-S. Steyer, G. Clement, M. Coates, T. Smithson, A. R. Milner, H. Blom, D. Snitting, I. Adameyko, A. Soler, S. Martin and R. R. Schoch for discussions; G. Cuny and B. E. Kramer Lindow for access to the collections housed in the Natural History Museum of Denmark; and M. Lowe for access to the collections of the University Museum of Zoology, Cambridge.

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Authors and Affiliations

  1. Subdepartment of Evolution and Development, Department of Organismal Biology, Science for Life Laboratory and Uppsala University, Evolutionary Biology Centre, Norbyvägen 18A, Uppsala, 752 36, Sweden

    Sophie Sanchez & Per E. Ahlberg

  2. European Synchrotron Radiation Facility, 71 Avenue des Martyrs, CS-40220, Grenoble Cedex, 38043, France

    Sophie Sanchez & Paul Tafforeau

  3. Department of Zoology, University Museum of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK

    Jennifer A. Clack

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Contributions

S.S., P.E.A. and P.T. conceived and designed the project. S.S. and P.T. performed the synchrotron experiments. The localities were excavated by J.A.C. and P.E.A. in 1987. P.T. processed and reconstructed the raw PPC-SRμCT scan data. S.S. segmented the scan data. S.S., P.E.A. and P.T. analysed the data. All authors discussed the interpretations. S.S. and P.E.A. developed the main text. S.S. made the figures and supplementary information. All authors provided a critical review of the manuscript and approved the final draft.

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Correspondence to Sophie Sanchez.

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The authors declare no competing financial interests.

Additional information

Reviewer Information

Nature thanks J. Anderson, N. Fröbisch, R. Schoch and K. Stein for their contribution to the peer review of this work.

The synchrotron data will be made available through the ESRF palaeontology database (http://paleo.esrf.eu).

Extended data figures and tables

Extended Data Figure 1 Three-dimensional models of Acanthostega humeri based on synchrotron microtomography data.

a, NHMD 74756. b, UMZC T.1295. c, MGUH 29019. d, MGUH 29020. From top to bottom: preaxial view, ventral view, postaxial view, dorsal view. Humeri are all oriented with their proximal epiphysis towards the top.

Extended Data Figure 2 Epiphyseal microanatomy and histology of Acanthostega humerus (MGUH 29020).

a, Three-dimentional model in preaxial view, based on synchrotron microtomography data, oriented with the proximal extremity (epiphysis6) towards the top. The black line indicates the virtual thin section illustrated in b. b, Longitudinal virtual thin section (thickness: 50 μm, voxel size: 1.12 μm, same scale bar and orientation as in a) showing the location of the detailed image on the right. The latter shows the marrow processes (mp) formed in the growth plate by endochondral ossification. c, High-resolution virtual thin section (thickness: 50 μm, voxel size: 1.12 μm) from the epiphyseal region showing obvious Liesegang’s rings as remnants of calcified cartilage6 (cc), formed during endochondral ossification. These remnants are entrapped in the trabeculae (t), at the vicinity of the ossification notch6, where the thickness of the periosteal bone (pb) between the mineralization front (mf) and the surface is greatly reduced. The bone is oriented with its surface towards the bottom. Left, longitudinal thin section; right, transverse section.

Extended Data Figure 3 Midshaft bone histology of two Acanthostega humeri (UMZC T.1295 and MGUH 29019).

a, Three-dimensional model of humerus UMZC T.1295 in dorsal view and oriented with the proximal epiphyses6 towards the top. The white circle indicates the midshaft location at which the transverse virtual section was made. The latter (single tomographic slice, voxel size: 0.638 μm) shows the complete bone deposit of cortical bone (c) from the mineralization front (mf) to the surface of the humerus (top). The cortical bone comprises numerous osteocyte lacunae (ol), which are much smaller than the aligned globular cell lacunae (agl) present at the location of the mineralization front. Trabeculae (t) are numerous in the medullary cavity. The red line in the transverse virtual section indicates the location of the next tangential virtual section which details the mineralization front. b, Three-dimensional model of the humerus MGUH 29019 in ventral view showing the high-resolution scanned location. The virtual section shows the humeral cortical histology at the midshaft (single tomographic slice, voxel size: 0.638 μm). As in UMZC T.1295, the cortical bone matrix (cb) is very compact, pierced with small osteocyte lacunae. At this location, its surface (top), although still embedded in the rock matrix, is not well preserved. The red line in the transverse virtual section indicates the location of the next tangential virtual section detailing the cellular structure of the mineralization front.

Extended Data Figure 4 Regions of high-resolution scans.

Skeletochronological observations were done at sub-micrometre resolution in nine homologous regions of the four humeri of Acanthostega. Specimen MGUH 29020 is used here to illustrate the regions providing quantifiable information to calculate annual bone growth rates (Extended Data Table 1). Areas of muscle insertion were avoided when possible. Regions 2, 3 and 9 are non-muscle attachment areas. Regions 7 and 8 are located between two regions of muscle insertions but annual bone growth rates (Extended Data Table 1) were measured only in undisturbed cortical parts exhibiting regular LAG patterns.

Extended Data Figure 5 Humeral midshaft skeletochronology.

All virtual thin sections (voxel size: 0.638 μm) reveal LAGs (black arrows) resulting from the cyclical growth of the cortical deposit (c). They are oriented with the surface of the bone (sb) towards the top and medullary trabeculae (t) downwards. The locations of the thin sections are shown as white dots on the associated 3D models. All 3D models are oriented with their proximal epiphyses6 towards the top. a, Transverse virtual thin section (thickness: 30 μm) showing three LAGs in the cortical bone of the ventral midshaft of the humerus MGUH 29019 (region 7). The inner surface of the cortical bone has been eroded. b, Longitudinal virtual thin section (thickness: 30 μm) showing five LAGs in the cortical bone of the ventral midshaft of MGUH 29020 (region 7). The inner cortical bone is disturbed by a highly vascularised period. LAGs cannot be identified with accuracy in this region. The growth deposits between the LAGs in region 7 are similar in MGUH 29019 and MGUH 29020 (Extended Data Table 1). c, Transverse virtual thin section (thickness: 30 μm) showing two LAGs in the cortical bone of the dorsal midshaft of the specimen MGUH 29019 (region 3). d, Longitudinal virtual thin section (thickness: 50 μm) showing four LAGs in the cortical bone of the dorsal midshaft of UMZC T.1295 (region 3). e, Longitudinal virtual thin section (thickness: 30 μm) showing five LAGs in the cortical bone of the dorsal midshaft of MGUH 29020 (region 3). The growth deposits between the LAGs in region 3 are similar in UMZC T.1295, MGUH 29019 and MGUH 29020 (Extended Data Table 1). Scale bars for virtual thin sections: 0.2 mm. Scale bars for 3D models: 15 mm.

Extended Data Figure 6 Graphic visualizations of bone deposits.

Images are based on the measurements provided in Extended Data Table 1. a, Amount of bone deposited every year—that is, between two LAGs—in the regions of interest (reg.) of the four studied humeri. Except for region 2 (measured in MGUH 29020 and NHMD 74756), all regions show a relatively constant or increasing growth rate during animal development. b, Bone deposition accumulated to form the cortex. Despite a slight variation in values due to growth allometries, the growth rate (illustrated by the slope angle) is relatively constant in all regions of all specimens, meaning that all specimens grew at the same rate.

Extended Data Table 1 Measurements of humeral cyclical growth deposits between LAGs
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Sanchez, S., Tafforeau, P., Clack, J. et al. Life history of the stem tetrapod Acanthostega revealed by synchrotron microtomography. Nature 537, 408–411 (2016). https://doi.org/10.1038/nature19354

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