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. J Andrew Gillis
  1. Department of Zoology, University of Cambridge, United Kingdom
  2. Marine Biological Laboratory, United States
Research Article
Cite this article as: eLife 2020;9:e51696 doi: 10.7554/eLife.51696
6 figures, 3 data sets and 3 additional files

Figures

Segmental organization of paraxial mesoderm and the vertebral skeleton in the skate.

(a) Somites of a S24 skate embryo showing (a') trunk (tr), cloacal (c), and tail (tl) somites, delineated with dashed lines. (b) A cleared and stained vertebral column from a skate hatchling, with the trunk to tail transition denoted with an asterisk. (c) µCT scan reconstruction of skate trunk and (d) tail vertebrae, with vertebral elements corresponding to a single body segment color-coded blue or yellow, neural tissue colored green, and blood vessels colored red. Note that in (d), one set of spinal nerves spans two vertebrae. a/v, caudal artery and vein; ca, outer cartilage of vertebral body; ce, centrum; ha, haemal arch; ia, intercalary arch; na, neural arch; nsp, neural spine; sc, spinal cord; sn, set of spinal nerves; tp, transverse process. Scale bars: (a) 400 µm; (a') 100 µm; (b) 500 µm; (c) and (d) 100 µm.

Molecular basis of skate somite rostrocaudal polarity.

Whole-mount mRNA in situ hybridization reveals (a) rostral expression of Tbx18 and (b) caudal expression of Uncx4.1 within skate somites at S22. (c) Hybridization chain reaction (HCR) in situ hybridization on paraffin sections reveals complimentary rostromedial and caudomedial expression of Tbx18 (magenta, c') and Uncx4.1 (green, c"), respectively, in skate somites at S22. Dashed lines indicate somite boundaries. Scale bars: (a) and (b) 100 µm; (c-c") 25 µm.

Skates undergo tetrapod-like resegmentation.

(a) Adjacent CM-DiI- and SpDiOC18-labeled trunk somites in a S24 skate embryo. (b) Sagittal section of the trunk of an embryo 58 days post-injection, showing CM-DiI- and SpDiOC18-labeled cells in the posterior and anterior halves of adjacent vertebrae, consistent with resegmentation. (c, c') CM-DiI-labeled cells and (d, d') SpDiOC18-labeled cells span two vertebrae (each shown with and without DAPI counterstain). Dashed lines indicate somite boundaries in (a) and vertebral boundaries in (b-d). Scale bars for (a) and (b) 100 µm; scale bars for (c-d') 50 µm.

Skate tail vertebrae are duplicated and resegmented.

(a) Adjacent CM-DiI and SpDiOC18 injections in tail somites of a S24 little skate embryo. (b) Sagittal section of the tail of an embryo 117 days post-injection showing CM-DiI- and SpDiOC18-labeled cells in three vertebrae each. Magnified views reveal (c-d) CM-DiI- and (e-f) SpDiOC18-labeled cells spanning vertebral boundaries (images shown with and without DAPI counterstain). Dashed lines indicate somite boundaries in (a) and vertebral boundaries in (b–f). Arrowheads indicate dye-labeled cells. Scale bars for (a and b) 100 µm; scale bars for (c-f') 50 µm.

The cloaca precedes the monospondylous to diplospondylous transition.

(a) CM-DiI labeling of a S24 skate somite (marked with white dashed line) just dorsal to the posterior margin of the cloaca (denoted with yellow dashed line). (b) Sagittal section of an embryo 71 days post-injection, showing two adjacent vertebrae labeled with CM-DiI. (c) Magnified view of two vertebrae showing CM-DiI labeled cells with and (c') without DAPI counterstain. Dashed lines in (b-c) indicate vertebral boundaries. Scale bars for (a) and (c) 100 µm; scale bars for (b) 200 µm.

Resegmentation is ancestral for jawed vertebrates.

(a) Schematic showing the distribution of strict resegmentation on a simplified vertebrate evolutionary tree, and the contribution of two adjacent somites to (b) trunk vertebrae; (c) vertebrae at the trunk-to-tail transition; and (d) tail vertebrae in the skate.

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, https://doi.org/10.5061/dryad.b2rbnzs8s.

The following data sets were generated
  1. 1
    NCBI GenBank
    1. KE Criswell
    2. JA Gillis
    (2020)
    ID MN478366. Nucleotide sequences for Leucoraja erinacea Uncx4.1.
  2. 2
    NCBI GenBank
    1. KE Criswell
    2. JA Gillis
    (2020)
    ID MN478367. Nucleotide sequences for Leucoraja erinacea Tbx18.
  3. 3
    Dryad Digital Repository
    1. KE Criswell
    2. JA Gillis
    (2019)
    Resegmentation is an ancestral feature of the gnathostome vertebral skeleton.
    https://doi.org/10.5061/dryad.b2rbnzs8s

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