Embryonic origin and serial homology of gill arches and paired fins in the skate, Leucoraja erinacea

Victoria Sleight, J Andrew Gillis (Corresponding Author)

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21 Citations (Scopus)
7 Downloads (Pure)

Abstract

Paired fins are a defining feature of the jawed vertebrate body plan, but their evolutionary origin remains unresolved. Gegenbaur proposed that paired fins evolved as gill arch serial homologues, but this hypothesis is now widely discounted, owing largely to the presumed distinct embryonic origins of these structures from mesoderm and neural crest, respectively. Here, we use cell lineage tracing to test the embryonic origin of the pharyngeal and paired fin skeleton in the skate (Leucoraja erinacea). We find that while the jaw and hyoid arch skeleton derive from neural crest, and the pectoral fin skeleton from mesoderm, the gill arches are of dual origin, receiving contributions from both germ layers. We propose that gill arches and paired fins are serially homologous as derivatives of a continuous, dual-origin mesenchyme with common skeletogenic competence, and that this serial homology accounts for their parallel anatomical organization and shared responses to axial patterning signals.
Original languageEnglish
Article numbere60635
Number of pages14
JournaleLife
Volume9
Early online date17 Nov 2020
DOIs
Publication statusPublished - 17 Nov 2020

Bibliographical note

The authors thank Dr. Richard Schneider, Prof. David Sherwood, and the MBL Embryology Course for provision of lab space, Louise Bertrand and Leica Microsystems for microscopy support, the staff of the Marine Resources Center at the MBL for assistance with animal husbandry and Dr. Kate Criswell, Jenaid Rees, Christine Hirschberger and Dr. Kate Rawlinson for helpful discussion. This project benefited from technical advice from Dr. Matt Wayland and use of the Imaging Facility, Department of Zoology, supported by a Sir Isaac Newton Trust Research Grant (18.07ii(c)). This research was supported by a Royal Society University Research Fellowship (UF130182) and grants from the Leverhulme Trust (RPG-2016–373) and the University of Cambridge Sir Isaac Newton Trust (14.23z) to JAG, and by a Junior Research Fellowship from Wolfson College, Cambridge and Whitman Early Career Fellowship from the Marine Biology Laboratory to VAS.

Keywords

  • Leucoraja erinacea
  • Mesoderm
  • Neural crest
  • developmental biology
  • evolutionary biology
  • gill arch
  • little skate
  • paired appendages
  • serial homology

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