Published November 24, 2021 | Version Accepted Version
Journal Article Open

A genetically tractable jellyfish model for systems and evolutionary neuroscience

  • 1. ROR icon California Institute of Technology
  • 2. ROR icon Laboratoire de Biologie du Développement de Villefranche-sur-Mer

Abstract

Jellyfish are radially symmetric organisms without a brain that arose more than 500 million years ago. They achieve organismal behaviors through coordinated interactions between autonomously functioning body parts. Jellyfish neurons have been studied electrophysiologically, but not at the systems level. We introduce Clytia hemisphaerica as a transparent, genetically tractable jellyfish model for systems and evolutionary neuroscience. We generate stable F₁ transgenic lines for cell-type-specific conditional ablation and whole-organism GCaMP imaging. Using these tools and computational analyses, we find that an apparently diffuse network of RFamide-expressing umbrellar neurons is functionally subdivided into a series of spatially localized subassemblies whose synchronous activation controls directional food transfer from the tentacles to the mouth. These data reveal an unanticipated degree of structured neural organization in this species. Clytia affords a platform for systems-level studies of neural function, behavior, and evolution within a clade of marine organisms with growing ecological and economic importance.

Additional Information

© 2021 Elsevier. Received 23 February 2021, Revised 30 August 2021, Accepted 19 October 2021, Available online 24 November 2021. We thank the Marine Resources Center of the MBL (Woods Hole, MA) and J. Malamy for an introduction to Clytia; E. Houliston and R. Copley for Clytia resources and advice; M.D.C. Lamadrid for illustrations; S. Ekker for Tol2 reagents; J. Williams for software; A. Collazo for imaging support; and J. Parker, D. Prober, and Anderson lab members for feedback. We thank the CRBM/Service Aquario (FR 3761; EMBRC-France, managed by ANR-10-INBS-0002) for support. This work was supported by the Caltech Center for Evolutionary Science, the Whitman Center of the MBL, the Life Sciences Research Foundation (to B.W.), NINDS (K99NS119749 to B.W.), and NIMH (K99MH117264 to A.K.). Content is the authors' sole responsibility and not that of NIH. T.M. was supported by ANR (ANR-17-CE13-0016, i-MMEJ) and ASSEMBLE Plus JRA3 (EU Horizon 2020 No. 730984). A.N. was supported by a Scholarship from the Agency of Science, Technology and Research, Singapore. D.J.A. is an Investigator of the Howard Hughes Medical Institute. Author contributions: B.W. and D.J.A. conceived of the project and wrote the manuscript with input from T.M., A.N., A.K., and B.H. B.W., D.J.A., and B.H. designed and performed histology, behavior, and imaging experiments. B.W., D.J.A., and T.M. designed and performed experiments establishing transgenesis. B.W., A.N., and A.K. analyzed the data. A.N. performed NMF/ICA, subspace, and GLM analyses. A.K. generated the neural network models. The authors declare no competing interests. Data and code availability: • Source data reported in this paper will be shared by the lead contact upon request. • Code used for analyses in this paper will be shared by the lead contact upon request. • Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request.

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Additional details

Identifiers

PMCID
PMC8629132
Eprint ID
112062
DOI
10.1016/j.cell.2021.10.021
Resolver ID
CaltechAUTHORS:20201129-234567890

Related works

Funding

European Marine Biological Resource Centre
Agence Nationale pour la Recherche (ANR)
ANR-10-INBS-0002
Caltech Center for Evolutionary Science
Marine Biological Laboratory
Life Sciences Research Foundation
NIH
K99NS119749
NIH
K99MH117264
Agence Nationale pour la Recherche (ANR)
ANR-17-CE13-0016
European Research Council (ERC)
730984
Agency for Science, Technology and Research (A*STAR)
Howard Hughes Medical Institute (HHMI)

Dates

Created
2021-11-29
Created from EPrint's datestamp field
Updated
2023-07-06
Created from EPrint's last_modified field

Caltech Custom Metadata

Caltech groups
Tianqiao and Chrissy Chen Institute for Neuroscience, Division of Biology and Biological Engineering (BBE)