Article | Published:

Sex-specific pruning of neuronal synapses in Caenorhabditis elegans

Nature volume 533, pages 206211 (12 May 2016) | Download Citation

Abstract

Whether and how neurons that are present in both sexes of the same species can differentiate in a sexually dimorphic manner is not well understood. A comparison of the connectomes of the Caenorhabditis elegans hermaphrodite and male nervous systems reveals the existence of sexually dimorphic synaptic connections between neurons present in both sexes. Here we demonstrate sex-specific functions of these sex-shared neurons and show that many neurons initially form synapses in a hybrid manner in both the male and hermaphrodite pattern before sexual maturation. Sex-specific synapse pruning then results in the sex-specific maintenance of subsets of these connections. Reversal of the sexual identity of either the pre- or postsynaptic neuron alone transforms the patterns of synaptic connectivity to that of the opposite sex. A dimorphically expressed and phylogenetically conserved transcription factor is both necessary and sufficient to determine sex-specific connectivity patterns. Our studies reveal new insights into sex-specific circuit development.

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Acknowledgements

We thank Q. Chen for generating transgenic strains; J. White, J. Sulston and LMB/MRC for sharing their annotated electron microscopy images to D. Hall for curation, and http://www.wormimage.org where these annotated images have been made available by D. Hall; E. Yemini for advice on tracking experiments; S. Cook for help with Elegance software; M. Zhen for communicating unpublished results; P. Sengupta, I. Greenwald and members of the Hobert lab for comments on the manuscript. This work was supported by postdoctoral fellowships from the EMBO and HFSP (to M.O.-S.), the NIH (2R37NS039996) and the HHMI. M.O.-S. is an Awardee of the Weizmann Institute of Science, National Postdoctoral Award Program for Advancing Women in Science.

Author information

Affiliations

  1. Department of Biological Sciences, Columbia University, New York, New York 10027, USA

    • Meital Oren-Suissa
    • , Emily A. Bayer
    •  & Oliver Hobert
  2. Department of Biochemistry and Molecular Biophysics, Columbia University, New York, New York 10032, USA

    • Meital Oren-Suissa
    • , Emily A. Bayer
    •  & Oliver Hobert
  3. Howard Hughes Medical Institute, Columbia University, New York, New York 10027, USA

    • Meital Oren-Suissa
    • , Emily A. Bayer
    •  & Oliver Hobert

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Contributions

M.O.-S. and O.H. designed the experiments. M.O.-S. performed most experiments. E.A.B. quantified the data for PHA-AVG synapses and all iBLINC transgenes, tracked silenced PHB animals and generated driver lines for expression analysis of gpa-6 and flp-18. M.O.-S. and O.H. wrote the paper with input from E.A.B.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Meital Oren-Suissa or Oliver Hobert.

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    Supplementary Tables

    This file contains Supplementary Table 1, which shows Transgenic strains used in this study, and additional references.

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DOI

https://doi.org/10.1038/nature17977

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