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Published June 30, 2015 | Published + Supplemental Material
Journal Article Open

Self-repairing symmetry in jellyfish through mechanically driven reorganization

Abstract

What happens when an animal is injured and loses important structures? Some animals simply heal the wound, whereas others are able to regenerate lost parts. In this study, we report a previously unidentified strategy of self-repair, where moon jellyfish respond to injuries by reorganizing existing parts, and rebuilding essential body symmetry, without regenerating what is lost. Specifically, in response to arm amputation, the young jellyfish of Aurelia aurita rearrange their remaining arms, recenter their manubria, and rebuild their muscular networks, all completed within 12 hours to 4 days. We call this process symmetrization. We find that symmetrization is not driven by external cues, cell proliferation, cell death, and proceeded even when foreign arms were grafted on. Instead, we find that forces generated by the muscular network are essential. Inhibiting pulsation using muscle relaxants completely, and reversibly, blocked symmetrization. Furthermore, we observed that decreasing pulse frequency using muscle relaxants slowed symmetrization, whereas increasing pulse frequency by lowering the magnesium concentration in seawater accelerated symmetrization. A mathematical model that describes the compressive forces from the muscle contraction, within the context of the elastic response from the mesoglea and the ephyra geometry, can recapitulate the recovery of global symmetry. Thus, self-repair in Aurelia proceeds through the reorganization of existing parts, and is driven by forces generated by its own propulsion machinery. We find evidence for symmetrization across species of jellyfish (Chrysaora pacifica, Mastigias sp., and Cotylorhiza tuberculata).

Additional Information

© 2015 National Academy of Sciences. Freely available online through the PNAS open access option. Edited by Clifford J. Tabin, Harvard Medical School, Boston, MA, and approved May 7, 2015 (received for review February 6, 2015). Published online before print June 15, 2015, doi: 10.1073/pnas.1502497112. We thank the Cabrillo Marine Aquarium and Monterey Bay Aquarium for supplying jellyfish polyps, and especially K. Darrow and W. Patry for their advice on jellyfish nursery. We thank N. Andrew for critical comments that led us to conceiving the pulsation modulation experiment, J. Dabiri for discussions throughout the study, J. Nawroth for pointing us to cactus spines, and E. Meyerowitz for pointing out the importance of viscous ratchet. We thank M. Elowitz, B. Hay, J. H. Cho, C. Frick, H. Nunns, N. Olsman, J. T. Abrams, and B. G. Abrams for suggestions and comments on the manuscript. This work was supported by the National Science Foundation Graduate Research Fellowship Program (to M.J.A.). Author contributions: M.J.A., T.B., and L.G. designed research; M.J.A. and T.B. performed experiments; W.Y. performed the grafting experiments; M.J.A., C.-L.G., and L.G. designed the mathematical model; C.L.G. performed the mathematical modeling; M.J.A., T.B., and L.G. analyzed data; and M.J.A., T.B., and L.G. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1502497112/-/DCSupplemental.

Attached Files

Published - PNAS-2015-Abrams-E3365-73.pdf

Supplemental Material - pnas.1502497112.sm01.mp4

Supplemental Material - pnas.1502497112.sm02.m4v

Supplemental Material - pnas.1502497112.sm03.mp4

Supplemental Material - pnas.1502497112.sm04.m4v

Supplemental Material - pnas.201502497SI.pdf

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