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Still Connected: Evolutionary implications of the separation of the head from pectoral girdle in tetrapods and their fish relatives

Final Report Summary - GIRDLE EVO-DEVO (Still Connected: Evolutionary implications of the separation of the head from pectoral girdle in tetrapods and their fish relatives)

Still Connected: Evolutionary implications of the separation of the head from pectoral girdle in tetrapods and their fish relatives

Funding Scheme: FP7-MC-IIF

Separation of the shoulders from the head to create a functional neck was an important step in the conquest of land, as it is crucial for land-living vertebrates (tetrapods) to move their heads freely from the body. The primary research objective of the GIRDLE EVO-DEVO project was to discover how the evolution of the functional neck region in tetrapods affected muscle development and connectivity between the head and the shoulder girdle. Did the separation of the head from the shoulder girdle drastically alter the muscles in this region, and their development?

To address this we studied the development of the muscles in the neck region of fish ancestors to the tetrapods including a basal ray-finned fish, the Paddlefish, a basal lobe-finned fish, the Australian lungfish and also basal tetrapod, the Mexican axolotl. Methods used in this project to study neck muscle development included immunohistochemistry, histology and micro-ct scanning.

Our study shows that in all these animals the development of the cucullaris muscle, which connects the back of the head with the shoulder girdle, is delayed relative to all the other muscles of the head, as has been previously described in studies of mouse and chick. It also starts its development close to the insert on the back of the head and then slowly extend towards the shoulder girdle in all species. This indicates an evolutionary conserved mode of development that predates the evolution of a true, functional neck region. In other words, the evolution of this neck, and separation of the head from the shoulder girdle appears to have had little effect on the muscles in this region. This evolutionary conservation during the fish to tetrapod transition may be more extensive than previously expected; the evolution of the tetrapod limb from the fish fin also appears highly conserved in many respects.

We also attempted to study the development and migration of neural crest cells, which have been shown to be important for the development and identity of the muscles in the head and are also important for the cucullaris and other neck muscles in mouse. It is not yet know which population of neural crest cells contributes to the connective tissue and tendons of the cucullaris and when and how this population reaches the shoulder girdle, but previous studies have suggested its origin in the posterior hindbrain. Unfortunately, the high mortality of the embryos of Paddlefish (and the related sturgeon species we subsequently tried: Acipenser ruthenus, A. baeri, A. gueldenstaedtii, A. stellatus, A. sturio) and the very slow development of the Australian lungfish embryos have resulted in ambiguous cell-tracing data. In both Paddlefish and Australian lungfish we find it likely that the neural crest cell population migrates together with the mesoderm, which provides the muscle fibres, but the current data is inconclusive. We are still awaiting data from our collaborators working with the Mexican axolotl.

The microtomography study of various fossil specimens showed, as indicated by the embryological study, that there are few reasons to doubt the hypothesis that the cucullaris muscle is homologous among vertebrates. The first presence of a cucullaris muscle is potentially found in the placoderm lineage.

Significant findings

We conclude that the delayed development of the cucullaris muscle is not correlated with the evolution of a functional neck and that most likely, the neural crest cell contribution to the cucullaris and other neck muscles predates the evolution of a functional neck. The evolution of a functional neck has not affected the development or cell composition of the muscles connecting the head and shoulder girdle or their connective tissue and tendons.

Socio-economic impact

We have presented different aspects of this project during 'Science Uncovered' evenings held at the Natural History Museum, London (2010, 2011). 'Science Uncovered' is a major EU initiative, hosting a Europe-wide festival of science celebrating European Researchers' Night. We also discussed this project during Natural History Museum events such as Nature Live and A-levels. We found a high level of interest in the topic of neck evolution among the public, particularly when they understood that our research was relevant to the evolution of their own necks. Our participation in these events promoted European and UK science to a wide range of the public, including adults, students and children.

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