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Neurocranial Development of the Coelacanth and the Evolution of the Sarcopterygian Head Hugo Dutel1,2*, Manon Galland3, Paul Tafforeau4, John A

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Neurocranial Development of the Coelacanth and the Evolution of the Sarcopterygian Head Hugo Dutel1,2*, Manon Galland3, Paul Tafforeau4, John A LETTER https://doi.org/10.1038/s41586-019-1117-3 Neurocranial development of the coelacanth and the evolution of the sarcopterygian head Hugo Dutel1,2*, Manon Galland3, Paul Tafforeau4, John A. Long5, Michael J. Fagan1, Philippe Janvier6, Anthony Herrel7, Mathieu D. Santin8, Gaël Clément6 & Marc Herbin7 The neurocranium of sarcopterygian fishes was originally divided lengthens during prenatal development (Figs. 2, 3, Extended Data into an anterior (ethmosphenoid) and posterior (otoccipital) Fig. 1). The trabeculae extend anteroventrally to the notochord, and portion by an intracranial joint, and underwent major changes in delimit the open hypophyseal fossa. They fuse anteriorly as a narrow its overall geometry before fusing into a single unit in lungfishes trabeculae communis (Fig. 2, Extended Data Figs. 1, 2). Posteriorly, and early tetrapods1. Although the pattern of these changes is the ethmosphenoid portion develops around the anterior notochordal well-documented, the developmental mechanisms that underpin tip in the fetus; in later stages, it lies entirely anterior to the notochord. variation in the form of the neurocranium and its associated soft The notochord penetrates the ethmosphenoid portion at a position tissues during the evolution of sarcopterygian fishes remain poorly posterodorsal to the trabeculae, and terminates posterior to the hypo- understood. The coelacanth Latimeria is the only known living physis, the foramina for the internal carotids, the pituitary vein and the vertebrate that retains an intracranial joint2,3. Despite its importance oculomotor nerve (Fig. 2, Extended Data Figs. 1–3). At this level, the for understanding neurocranial evolution, the development of the neurocranium shows a marked curvature under the cephalic flexure. neurocranium of this ovoviviparous fish remains unknown. Here we This region is similar in topographic terms to the condition that is investigate the ontogeny of the neurocranium and brain in Latimeria observed in other gnathostomes, in which it is interpreted as deriving chalumnae using conventional and synchrotron X-ray micro- from the orbital cartilage5–7. A shallow dorsum sellae separates the computed tomography as well as magnetic resonance imaging, hypophyseal fossa and the large basicranial fenestra. In the otoccipital performed on an extensive growth series for this species. We describe portion, the parachordal plates are widely separated and extend anteri- the neurocranium at the earliest developmental stage known for orly as a short otic shelf. The otic region is shallow and the commissura Latimeria, as well as the major changes that the neurocranium prefacialis is open, as is the metotic fissure in the posterior wall of the undergoes during ontogeny. Changes in the neurocranium are otic capsule (Fig. 2, Extended Data Fig. 1). associated with an extreme reduction in the relative size of the brain The configuration of the neurocranium and brain observed in the fetus along with an enlargement of the notochord. The development of is, to our knowledge, unique among gnathostomes6,7. The endocranial the notochord appears to have a major effect on the surrounding cavity reaches the neurocranial floor in the ethmosphenoid portion, but cranial components, and might underpin the formation of the continues dorsally to the notochordal canal in the otoccipital portion intracranial joint. Our results shed light on the interplay between the (Figs. 2, 3, Extended Data Figs. 1–3). The cerebellum and mesencephalon neurocranium and its adjacent soft tissues during development in straddle the anterior and posterior divisions, and are positioned dorsally Latimeria, and provide insights into the developmental mechanisms to the forebrain and the ethmosphenoid portion. The short pila antotica that are likely to have underpinned the evolution of neurocranial meets the orbital cartilage ventral to the mesencephalon, and the troch- diversity in sarcopterygian fishes. lear nerve emerges above the eyes (Fig. 2, Extended Data Fig. 1). Dorsally, Although the coelacanth Latimeria has been studied extensively since the neurocranium is largely incomplete around the cerebellum and the its discovery 80 years ago4, most aspects of its cranial development mesencephalon, and the taenia marginalis posterior fails to reach the remain unknown2. This lack of knowledge is largely due to the scarcity orbital cartilage. Later during prenatal development, the endocranium of embryonic material and—until recently—the absence of efficient of the ethmosphenoid portion moves dorsally as a narrow internasal non-invasive methods of studying the internal anatomy of these rare septum develops, such that P1 presents a tropibasic neurocranium (Fig. 3, specimens. Here we digitized five specimens of this ovoviviparous spe- Extended Data Figs. 2, 3). The ethmoidal region is proportionally shorter cies that ranged from prenatal to postnatal developmental stages: a in the fetus compared to the adult, because the cavity for the rostral organ small fetus (5 cm total length), a pup with a yolk sac (hereafter referred is not yet formed (Figs. 2, 3, Extended Data Fig. 1). Only from the stage to as P1, 30.5 cm total length), a pup whose yolk sac is resorbed (here- represented by P1 onwards is the cavity for the rostral organ separated after referred to as P2, 35.6 cm total length), a juvenile (42 cm total from the endocranial cavity, which is steeply depressed in its anterior length) and an adult (132 cm total length) (Fig. 1). To the best of our portion (Fig. 3, Extended Data Fig. 3). The expansion of the rostral organ knowledge, these specimens represent the most complete growth series remodels the ethmoid region, and displaces the ethmoidal articulation currently available for this species. from the postnasal wall (in the fetus) to the lateral side of the nasal cap- In the fetus, the neurocranium is already divided into two portions sules (in later stages) (Figs. 2, 3, Extended Data Fig. 1). at the level of the ventral fissure and the intracranial joint (Figs. 1, 2, The reduction in the relative size of the brain (Extended Data Table 1) Extended Data Fig. 1). The individualization of the two divisions of and changes in its shape (Fig. 3, Extended Data Figs. 3, 4) are associated the neurocranium thus occurs earlier, probably during early embry- with a progressive displacement towards the otoccipital portion. In the onic development. The ethmosphenoid portion of the neurocranium fetus (Figs. 2, 3, Extended Data Figs. 1–4), the brain spans the intra- is much narrower and slightly longer than the otoccipital portion, and cranial joint and the telencephalon reaches the nasal capsules. In P1, P2 1School of Engineering and Computer Science, Medical and Biological Engineering Research Group, University of Hull, Hull, UK. 2School of Earth Sciences, University of Bristol, Bristol, UK. 3UMR 7206 (MNHN-CNRS-Université Paris Diderot), Éco-Anthropologie et Ethnobiologie, Département Homme et Environnement, Muséum National d’Histoire Naturelle, Paris, France. 4European Synchrotron Radiation Facility, Grenoble, France. 5College of Science and Engineering, Flinders University, Adelaide, South Australia, Australia. 6UMR 7207 (MNHN-CNRS-Sorbonne Université), CR2P Centre de Recherche en Paléontologie-Paris, Département Origines et Évolution, Muséum National d’Histoire Naturelle, Paris, France. 7UMR 7179 (MNHN-CNRS) MECADEV, Département Adaptations du Vivant, Muséum National d’Histoire Naturelle, Paris, France. 8Inserm U 1127, CNRS UMR 7225, Centre for NeuroImaging Research, ICM (Brain & Spine Institute), Sorbonne University, Paris, France. *e-mail: [email protected] NATURE| www.nature.com/nature RESEARCH LETTER a Fetus Pup 1 a tm ij mes pa oc V23 sc + scc 1 cm 5 cm Pup 2 Juvenile X IV III oro otc V1 5 cm 5 cm II Adult IX VII VI nac otc os fpv c tc 10 cm VIIVII eth.a b os V23 V1 III tc pc IV b Intracranial joint Brain Ethmosphenoid Otoccipital portion VI portion II Branchial eth arches bf nac Nasal hf eth.a capsule otc ds pa oc t Shoulder girdle vf and pectoral n Suspensorium c V23 ce V1 mes Hyoid apparatus Meckel’s cartilage 1 mm rho cf Fig. 1 | The development of the living coelacanth L. chalumnae. die IV a, Growth series gathered for this study (n = 5 specimens). b, Overall fm anterolateral view of the skull of the fetus. III X tel nc and the juvenile (Fig. 3, Extended Data Figs. 3–5), the brain represents II about 11% of the endocranial volume. The telecephalon continues to IX span the intracranial joint but the mesencephalon is restricted to the VIII VII VI ds oc nac c otoccipital portion. The confinement of the brain within the otoccipital h t hp tc portion occurs only during postnatal development (Fig. 3, Extended I 1 mm Data Figs. 3, 4). In the adult (Fig. 3, Extended Data Figs. 3, 4), the entire brain is restricted to the otoccipital portion and represents 1% Otoccipital portion Ethmosphenoid portion Brain Notochord 2,3 of the endocranial volume, as previously reported . In the fetus, the Fig. 2 | The neurocranium of L. chalumnae fetus. a, b, Neurocranium brain is curved ventrally and the cephalic flexure is less pronounced in right lateral (a) and ventral (b) views. c, Right lateral view of the than in other gnathostomes, as the rhombencephalon and the mes- neurocranium virtually cut open along the midsagittal plane. bf, encephalon develop far-dorsal to the forebrain (Figs. 2, 3, Extended basicranial fenestra; ce, cerebellum; cf, cephalic flexure; die, diencephalon; Data Figs. 1–4). This configuration is retained in P1 but not
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