Axial patterning of the chondrichthyan pharyngeal endoskeleton and the origin of the jaw

Classical comparative anatomical hypotheses propose that the upper and lower jaw evolved through modification of dorsal and ventral gill arch skeletal elements, respectively. These hypotheses were based largely on the skeletal anatomy of chondrichthyans (sharks, skates and holocephalans), but remain largely untested from a developmental perspective. Here, I test 1) whether jaws and gill arches ancestrally shared common developmental patterning mechanisms, and 2) whether the mandibular arch might carry anatomical vestiges of an ancestral gill-arch-like condition. To do this, I have used embryos of a cartilaginous fish, the little skate (Leucoraja erinacea), which has retained an ancestral organisation of the jaw and gill arch endoskeleton, and which possesses a reduced gill-like structure (a “pseudobranch”) on the back of the mandibular arch. Using candidate and RNAseq/differential gene expression analysis and mRNA in situ hybridisation, I find broad conservation of dorsoventral patterning mechanisms within pharyngeal arches – embryonic structures which contain the progenitors of the jaw and gill arch skeleton – as well as unique transcriptional features that may underpin distinct jaw and gill arch morphologies. The latter include unique gene expression features of jaw and gill arch muscle progenitors, and of developing gill lamellae. Finally, it has been historically speculated that the chondrichthyan pseudobranch derives from the hyoid (i.e. 2nd pharyngeal) arch. I demonstrate here, by cell lineage tracing, that the pseudobranch is, in fact, mandibular arch derived, that it shares gene expression features with developing gills, and that its supporting spiracular cartilage develops under the influence of a shh-expressing signalling centre, in a manner that parallels that shh-dependent development of branchial rays (i.e. cartilaginous appendages that support the respiratory lamellae of the gill arches). Taken together, this dissertation presents evidence for serial homology of the jaw and gill arch skeleton, and of an ancestral gill-arch nature of the mandibular arch of vertebrates.

Name dc:type.qualificationname

Doctor of Philosophy (PhD)

Level dc:type.qualificationlevel

Doctoral

Grantor dc:publisher.institution

University of Cambridge

Year dc:date.issued

2021

Author dc:creator

• Hirschberger, Marie

Advisor dc:contributor.advisor

• Gillis, J Andrew

• anatomy
• evolution
• vertebrates
• gnathostomes
• development
• chondrichthyans

Licence

• https://apollo8-f-pro.lib.cam.ac.uk/bitstreams/915ccbc9-5548-43c9-b8c3-b9c60b9f9735/download
• https://www.rioxx.net/licenses/all-rights-reserved/

Language dc:language

eng

DOI dc:identifier.doi

https://doi.org/10.17863/CAM.75495

OAI identifier oai:identifier

oai:www.repository.cam.ac.uk:1810/328044