Neurocranial development of the coelacanth and the evolution of the sarcopterygian head

Dutel, Hugo; Galland, Manon; Tafforeau, Paul; Long, John A.; Fagan, Michael J.; Janvier, Philippe; Herrel, Anthony; Santin, Mathieu D.; Clément, Gaël; Herbin, Marc

Abstract

The neurocranium of sarcopterygian fishes was originally divided into an anterior (ethmosphenoid) and posterior (otoccipital) portion by an intracranial joint, and underwent major changes in its overall geometry before fusing into a single unit in lungfishes and early tetrapods. Although the pattern of these changes is well-documented, the developmental mechanisms that underpin variation in the form of the neurocranium and its associated soft tissues during the evolution of sarcopterygian fishes remain poorly understood. The coelacanth Latimeria is the only known living vertebrate that retains an intracranial joint. Despite its importance for understanding neurocranial evolution, the development of the neurocranium of this ovoviviparous fish remains unknown. Here we investigate the ontogeny of the neurocranium and brain in Latimeria chalumnae using conventional and synchrotron X-ray microcomputed tomography as well as magnetic resonance imaging, performed on an extensive growth series for this species. We describe the neurocranium at the earliest developmental stage known for Latimeria, as well as the major changes that the neurocranium undergoes during ontogeny. Changes in the neurocranium are associated with an extreme reduction in the relative size of the brain along with an enlargement of the notochord. The development of the notochord appears to have a major effect on the surrounding cranial components, and might underpin the formation of the intracranial joint. Our results shed light on the interplay between the neurocranium and its adjacent soft tissues during development in Latimeria, and provide insights into the developmental mechanisms that are likely to have underpinned the evolution of neurocranial diversity in sarcopterygian fishes.

Citation

Dutel, H., Galland, M., Tafforeau, P., Long, J. A., Fagan, M. J., Janvier, P., Herrel, A., Santin, M. D., Clément, G., & Herbin, M. (2019). Neurocranial development of the coelacanth and the evolution of the sarcopterygian head. Nature, 569, 556–559. https://doi.org/10.1038/s41586-019-1117-3

• Journal Article Type: Letter
• Acceptance Date: Mar 20, 2019
• Online Publication Date: Apr 17, 2019
• Publication Date: May 23, 2019
• Deposit Date: May 20, 2019
• Publicly Available Date: Apr 18, 2020
• Journal: Nature
• Print ISSN: 0028-0836
• Publisher: Nature Publishing Group
• Peer Reviewed: Peer Reviewed
• Volume: 569
• Pages: 556–559
• DOI: https://doi.org/10.1038/s41586-019-1117-3
• Keywords: Multidisciplinary
• Public URL: https://hull-repository.worktribe.com/output/1811914
• Publisher URL: https://www.nature.com/articles/s41586-019-1117-3
• Additional Information: Received: 15 October 2018; Accepted: 20 March 2019; First Online: 17 April 2019; : The authors declare no competing interests.
• Contract Date: May 20, 2019