Nutrient-dependent growth underpinned the Ediacaran transition to large body size

Abstract

Macroscale rangeomorph fossils, with characteristic branching fronds, appear (571 Myr ago) after the Gaskiers glaciation (580 Myr ago). However, biological mechanisms of size growth and potential connections to ocean geochemistry were untested. Using micro-computerized tomography and photographic measurements, alongside mathematical and computer models, we demonstrate that growth of rangeomorph branch internodes declined as their relative surface area decreased. This suggests that frond size and shape were directly responsive to nutrient uptake.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Retrodeformed stem diameter measured from a 3D micro-CT volume rendering of A. abaculus cast ROM 63005.
Figure 2: Sequential stem internode volumes and lengths, from micro-CT and digital photographs of rangeomorph specimens.
Figure 3: Computer simulations of rangeomorph internode size growth.

References

  1. 1.

    Narbonne, G. M. Science 305, 1141–1144 (2004).

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Hoyal Cuthill, J. F. & Conway Morris, S. Proc. Natl Acad. Sci. USA 111, 13122–13126 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Narbonne, G. M. & Gehling, J. G. Geology 31, 27–30 (2003).

    Article  Google Scholar 

  4. 4.

    Pu, J. P. et al. Geology 44, 955–958 (2016).

    CAS  Article  Google Scholar 

  5. 5.

    Butterfield, N. J. Precambrian Res. 173, 201–211 (2009).

    CAS  Article  Google Scholar 

  6. 6.

    Payne, J. L. et al. Proc. Natl Acad. Sci. USA 106, 24–27 (2009).

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Yuan, X., Chen, Z., Xiao, C., Zhou, C. & Hua, H. Nature 470, 390–393 (2011).

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Zhu, S. et al. Nat. Commun. 7, 11500 (2016).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Szathmary, E. & Maynard Smith, J. Nature 374, 227–232 (1995).

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Sperling, E. A., Peterson, K. J. & Laflamme, M. Geobiology 9, 24–33 (2011).

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Narbonne, G. M., Laflamme, M., Greentree, C. & Trusler, P. J. Paleontol. 83, 503–523 (2009).

    Article  Google Scholar 

  12. 12.

    Laflamme, M., Xiao, S. & Kowalewski, M. Proc. Natl Acad. Sci. USA 106, 14438–14443 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Canfield, D. E., Poulton, S. W. & Narbonne, G. M. Science 315, 92–95 (2007).

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Runnegar, B. Alcheringa 6, 223–239 (1982).

    Article  Google Scholar 

  15. 15.

    Garcia Camacho, F. et al. Appl. Microbiol. Biotechnol. 73, 525–532 (2006).

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Mills, D. B. et al. Proc. Natl Acad. Sci. USA 111, 4168–4172 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Budd, G. E. & Jensen, S. Biol. Rev. 92, 446–473 (2017).

    Article  PubMed  Google Scholar 

  18. 18.

    Cavalier-Smith, T. Phil. Trans. R. Soc. B 372, 20151476 (2017).

    Google Scholar 

  19. 19.

    Ghisalberti, M. et al. Curr. Biol. 24, 305–309 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Brasier, M. D. & Antcliffe, J. B. J. Geol. Soc. London 166, 363–384 (2009).

    Article  Google Scholar 

  21. 21.

    Sahoo, S. K. et al. Nature 489, 546–549 (2012).

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Sperling, E. A. et al. Nature 523, 451–454 (2015).

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Niklas, K. J. Ann. Bot 75, 217–227 (1995).

    Article  Google Scholar 

Download references

Acknowledgements

Specimen number ROM 63005 was loaned by the Royal Ontario Museum with the permission of the Rooms Museum, Newfoundland. CT-scanning was conducted by R. Asher at the Cambridge Biotomography Centre. Access to the specimen of Fig. 2d was provided at the South Australian Museum by J. Gehling and M.-A. Binnie, who found this fossil. This research was funded by an ELSI Origins Network (EON) Research Fellowship to J.F.H.C., supported by a grant from the John Templeton Foundation, and Palaeontological Association Research Grant number PA-RG201501 (J.F.H.C.). We thank N. Butterfield, A. Caulton and E. Smith for discussion of the manuscript.

Author information

Affiliations

Authors

Contributions

J.F.H.C. designed and carried out the analysis; J.F.H.C. and S.C.M. co-wrote the paper.

Corresponding author

Correspondence to Jennifer F. Hoyal Cuthill.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Supplementary Information

Supplementary Methods, Supplementary Figures 1–12, Supplementary References

Supplementary Tables

Supplementary Tables 1–5

Supplementary Code

Computer simulation code, MATLAB script in txt format

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hoyal Cuthill, J.F., Conway Morris, S. Nutrient-dependent growth underpinned the Ediacaran transition to large body size. Nat Ecol Evol 1, 1201–1204 (2017). https://doi.org/10.1038/s41559-017-0222-7

Download citation

Further reading