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The Morphology and Evolution of Chondrichthyan Cranial Muscles: A

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The Morphology and Evolution of Chondrichthyan Cranial Muscles: A The morphology and evolution of chondrichthyan cranial muscles: A digital dissection of the elephantfish Callorhinchus milii and the catshark Scyliorhinus canicula Richard Dearden, Rohan Mansuit, Antoine Cuckovic, Anthony Herrel, Dominique Didier, Paul Tafforeau, Alan Pradel To cite this version: Richard Dearden, Rohan Mansuit, Antoine Cuckovic, Anthony Herrel, Dominique Didier, et al.. The morphology and evolution of chondrichthyan cranial muscles: A digital dissection of the elephantfish Callorhinchus milii and the catshark Scyliorhinus canicula. Journal of Anatomy, Wiley, In press, 10.1111/joa.13362. hal-03103769 HAL Id: hal-03103769 https://hal.archives-ouvertes.fr/hal-03103769 Submitted on 8 Jan 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. bioRxiv preprint doi: https://doi.org/10.1101/2020.07.30.227132; this version posted July 31, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 The morphology and evolution of chondrichthyan cranial muscles: a 2 digital dissection of the elephantfish Callorhinchus milii and the 3 catshark Scyliorhinus canicula. 4 Running title: Cranial muscles of Callorhinchus and Scyliorhinus 5 Richard P. Dearden1, Rohan Mansuit1,2, Antoine Cuckovic3, Anthony Herrel2, Dominique Didier4, 6 Paul Tafforeau5, Alan Pradel1 7 8 1 CR2P, Centre de Recherche en Paléontologie–Paris, Muséum national d’Histoire naturelle, 9 Sorbonne Université, Centre National de la Recherche Scientifique, CP 38, 57 rue Cuvier, F75231 10 Paris cedex 05, France. 11 2 UMR 7179 (MNHN-CNRS) MECADEV, Département Adaptations du Vivant, Muséum National 12 d’Histoire Naturelle, Paris, France 13 3 Université Paris Saclay, 91190 Saint-Aubin, France 14 4Department of Biology, Millersville University, Millersville, PA 17551, USA 15 5 European Synchrotron Radiation Facility, Grenoble, France 16 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.30.227132; this version posted July 31, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 17 Abstract 18 The anatomy of sharks, rays, and chimaeras (chondrichthyans) is crucial to understanding the 19 evolution of the cranial system in vertebrates, due to their position as the sister group to bony fishes 20 (osteichthyans). Strikingly different arrangements of the head in the two constituent chondrichthyan 21 groups – holocephalans and elasmobranchs – have played a pivotal role in the formation of 22 evolutionary hypotheses targeting major cranial structures such as the jaws and pharynx. However, 23 despite the advent of digital dissections as a means of easily visualizing and sharing the results of 24 anatomical studies in three dimensions, information on the musculoskeletal systems of the 25 chondrichthyan head remains largely limited to traditional accounts, many of which are at least a 26 century old. Here we use synchrotron tomography acquire 3D data which we used to carry out a 27 digital dissection of a holocephalan and an elasmobranch widely used as model species: the 28 elephantfish, Callorhinchus milii, and the small-spotted catshark, Scyliorhinus canicula. We 29 describe and figure the skeletal anatomy of the head, labial, mandibular, hyoid, and branchial 30 cartilages in both taxa as well as the muscles of the head and pharynx. We make new observations, 31 particularly regarding the branchial musculature of Callorhinchus, revealing several previously 32 unreported or previously ambiguous structures. Finally, we review what is known about the 33 evolution of chondrichthyan cranial muscles from their fossil record and discuss the implications 34 for muscle homology and evolution, broadly concluding that the holocephalan pharynx is likely 35 derived from a more elasmobranch-like form. This dataset has great potential as a resource, 36 particularly for researchers using these model species for zoological research, functional 37 morphologists requiring models of musculature and skeletons, as well as for palaeontologists 38 seeking comparative models for extinct taxa. 39 Keywords (English): digital dissection, cranial muscles, holocephalan, elasmobranch, 40 Callorhinchus milii, Scyliorhinus canicula 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.30.227132; this version posted July 31, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 41 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.30.227132; this version posted July 31, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 42 Introduction 43 Cartilaginous fishes (Chondrichthyes) comprise only a small fraction of total jawed vertebrate 44 diversity (Nelson et al., 2016) but are key to understanding the evolution of jawed vertebrates. As 45 the sister-group to the more diverse and disparate bony fishes (ray-finned fishes, lobe-finned fishes, 46 and tetrapods) their anatomy and physiology provides a valuable outgroup comparison which, 47 probably incorrectly, has often been held to represent “primitive states” for jawed vertebrates as a 48 whole. The greatly divergent cranial morphologies displayed by the two constituent sister groups of 49 Chondrichthyes – elasmobranchs and holocephalans - have themselves led to much debate, both 50 over chondrichthyan origins and those of jawed vertebrates more broadly. For these reasons, 51 anatomists, embryologists, and physiologists have intensively studied chondrichthyan anatomy over 52 the last two centuries. Recently, tomographic methods have allowed the advent of “digital 53 dissections”, where an organism’s anatomy can be non-destructively visualized and communicated 54 in the form of interactive datasets. These studies have run the gamut of mammals (Cox and Faulkes, 55 2014; Sharp and Trusler, 2015), archosaurs (Klinkhamer et al., 2017; Lautenschlager et al., 2014), 56 lissamphibians (Porro and Richards, 2017), and actinopterygians (Brocklehurst et al., 2019). 57 Although aspects of cartilaginous fish anatomy have been examined (Camp et al., 2017; Denton et 58 al., 2018; Tomita et al., 2018), three-dimensional information on the cranial musculoskeletal system 59 is limited. 60 We aim to address this with a digital dissection of the hard tissues and musculature of two 61 representatives of the Chondrichthyes: Callorhinchus milii Bory de Saint-Vincent 1823, a 62 holocephalan, and Scyliorhinus canicula Linnaeus 1758, an elasmobranch. Callorhinchus milii is a 63 callorhinchid, the sister-group to all other holocephalans (Inoue et al., 2010; Licht et al., 2012) and 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.30.227132; this version posted July 31, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 64 historically one of the best known holocephalans due to its being one of only two species to inhabit 65 shallow, nearshore waters (Didier, 1995). As a result, the musculature of the genus has been 66 described several times (Edgeworth, 1935; Kesteven, 1933; Luther, 1909a; Shann, 1919), most 67 recently with Didier (1995) providing a detailed overview of the anatomy and systematics of 68 holocephalans, including Callorhinchus. Scyliorhinus canicula is a scyliorhinid, a carcharhiniform 69 galeomorph elasmobranch. Because of the accessibility of adults, eggs, and embryos to European 70 researchers (it is abundant in nearshore habitats in the northeastern Atlantic) the species has 71 featured heavily in embryological and physiological studies of chondrichthyans (Coolen et al., 72 2008; de Beer, 1931; Hughes and Ballintijn, 1965; Oulion et al., 2011; Reif, 1980). While accounts 73 exist of its gross anatomy (Allis, 1917; Edgeworth, 1935; Luther, 1909b; Nakaya, 1975; Ridewood, 74 1899; Soares and Carvalho, 2013), detailed and fully illustrated accounts are surprisingly rare in 75 comparison to the similarly common Squalus. 76 Here we use a synchrotron tomographic dataset to provide accounts of anatomy of the cartilages 77 and musculature of the head in Callorhinchus milii and Scyliorhinus canicula. We examine 78 dissection-based reports of muscle anatomy in the light of our reconstructed models. By combining 79 this information with what is known about fossil taxa, we assess scenarios of morphological 80 evolution
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