Resegmentation is an ancestral feature of the gnathostome vertebral skeleton

Abstract
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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.

Data availability

Sequencing data have been deposited in GenBank (Uncx4.1 accession number MN478366 and Tbx18 accession number MN478367).CT scan data, including scan parameters and TIFF stacks, have been deposited in the Dryad Digital Repository, doi: 10.5061/dryad.b2rbnzs8s.

The following data sets were generated

1. Criswell KE
2. Gillis JA
(2019) Resegmentation is an ancestral feature of the gnathostome vertebral skeleton
Dryad Digital Repository, doi:10.5061/dryad.b2rbnzs8s.

http://dx.doi.org/10.5061/dryad.b2rbnzs8s

Article and author information

Author details

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.

"This ORCID iD identifies the author of this article:" 0000-0002-4004-0192
Andrew Gillis

Department of Zoology, University of Cambridge, Cambridge, United Kingdom

Competing interests
The authors declare that no competing interests exist.

"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.

Copyright

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.