1. Developmental Biology
  2. Evolutionary Biology
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Resegmentation is an ancestral feature of the gnathostome vertebral skeleton

  1. Katharine E Criswell  Is a corresponding author
  2. Andrew Gillis
  1. University of Cambridge, United Kingdom
Research Article
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Cite this article as: eLife 2020;9:e51696 doi: 10.7554/eLife.51696

Abstract

The vertebral skeleton is a defining feature of vertebrate animals. However, the mode of vertebral segmentation varies considerably between major lineages. In tetrapods, adjacent somite halves recombine to form a single vertebra through the process of 'resegmentation'. In teleost fishes, there is considerable mixing between cells of the anterior and posterior somite halves, without clear resegmentation. To determine whether resegmentation is a tetrapod novelty, or an ancestral feature of jawed vertebrates, we tested the relationship between somites and vertebrae in a cartilaginous fish, the skate (Leucoraja erinacea). Using cell lineage tracing, we show that skate trunk vertebrae arise through tetrapod-like resegmentation, with anterior and posterior halves of each vertebra deriving from adjacent somites. We further show that tail vertebrae also arise through resegmentation, though with a duplication of the number of vertebrae per body segment. These findings resolve axial resegmentation as an ancestral feature of the jawed vertebrate body plan.

Article and author information

Author details

  1. Katharine E Criswell

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    kc518@cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4004-0192
  2. Andrew Gillis

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2062-3777

Funding

Royal Society (NF160762)

  • Katharine E Criswell

Royal Society (UF130182)

  • Andrew Gillis

Marine Biological Laboratory

  • Katharine E Criswell

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experimental work was conducted at the Marine Biological Laboratory in Woods Hole, Massachusetts, USA, in accordance with approved institutional animal care and use (IACUC) protocols (#17-31 and #18-32). All embryological manipulations and euthanasia were performed with use of the anaesthetic Ethyl 3-aminobenzoate methanesulfonate (MS-222 or tricaine) and all efforts were made to minimise suffering.

Reviewing Editor

  1. Pamela C Yelick, Tufts University, United States

Publication history

  1. Received: September 6, 2019
  2. Accepted: February 19, 2020
  3. Accepted Manuscript published: February 24, 2020 (version 1)
  4. Version of Record published: March 10, 2020 (version 2)

Copyright

© 2020, Criswell & Gillis

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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