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Muscle Development in the Shark Scyliorhinus Canicula: Implications for the Evolution of the Gnathostome Head and Paired Appendage Musculature Janine M

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Muscle Development in the Shark Scyliorhinus Canicula: Implications for the Evolution of the Gnathostome Head and Paired Appendage Musculature Janine M Ziermann et al. Frontiers in Zoology (2017) 14:31 DOI 10.1186/s12983-017-0216-y RESEARCH Open Access Muscle development in the shark Scyliorhinus canicula: implications for the evolution of the gnathostome head and paired appendage musculature Janine M. Ziermann1*, Renata Freitas2,3 and Rui Diogo4 Abstract Background: The origin of jawed vertebrates was marked by profound reconfigurations of the skeleton and muscles of the head and by the acquisition of two sets of paired appendages. Extant cartilaginous fish retained numerous plesiomorphic characters of jawed vertebrates, which include several aspects of their musculature. Therefore, myogenic studies on sharks are essential in yielding clues on the developmental processes involved in the origin of the muscular anatomy. Results: Here we provide a detailed description of the development of specific muscular units integrating the cephalic and appendicular musculature of the shark model, Scyliorhinus canicula. In addition, we analyze the muscle development across gnathostomes by comparing the developmental onset of muscle groups in distinct taxa. Our data reveal that appendicular myogenesis occurs earlier in the pectoral than in the pelvic appendages. Additionally, the pectoral musculature includes muscles that have their primordial developmental origin in the head. This culminates in a tight muscular connection between the pectoral girdle and the cranium, which founds no parallel in the pelvic fins. Moreover, we identified a lateral to ventral pattern of formation of the cephalic muscles, that has been equally documented in osteichthyans but, in contrast with these gnathostomes, the hyoid muscles develop earlier than mandibular muscle in S. canicula. Conclusion: Our analyses reveal considerable differences in the formation of the pectoral and pelvic musculatures in S. canicula, reinforcing the idea that head tissues have contributed to the formation of the pectoral appendages in the common ancestor of extant gnathostomes. In addition, temporal differences in the formation of some cranial muscles between chondrichthyans and osteichthyans might support the hypothesis that the similarity between the musculature of the mandibular arch and of the other pharyngeal arches represents a derived feature of jawed vertebrates. Keywords: Muscles, Cranial, Cucullaris, Head, Pectoral, Pelvic, Fin, Shark, Limb Background feeding to predation in this particular vertebrate lineage The origin of jawed vertebrates (gnathostomes) is un- [1]. These novel morphological features may also have doubtedly one of the major events in the history of life, contributed to the vast radiation of gnathostomes, which as it drastically changed the feeding modes among ver- make up more than 99.9% of all living vertebrates [2]. tebrates [1]. The origin of jaws, paired fins, and the Chondrichthyans such as the sharks are considered to cephalic and appendicular musculature was probably of have morphological characteristics that retained various chief importance for the transition from suspension plesiomorphic gnathostome traits [3, 4]. These cartil- aginous fishes have been around for over 400 million years and are, therefore, amongst the oldest surviving * Correspondence: [email protected] vertebrate groups [5]. Although they have unique fea- 1Department of Anatomy, Howard University College of Medicine, 520 W St NW, Washington, DC 20059, USA tures that evolved in ways distinct from other fishes, Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Ziermann et al. Frontiers in Zoology (2017) 14:31 Page 2 of 17 they possess, for example, the most plesiomorphic paired posterior pharyngeal) arches. Their development also fin structure of modern vertebrates [5]. Therefore, sharks tends to follow a lateral to medial direction. For in- are also relevant for discussions on the development and stance, lateral muscles of one arch tend to differentiate evolution of not only fish muscles but also of the muscles earlier than the more medially and ventral muscles of of vertebrates as a whole [6]. Moreover, striking simi- the same arch. In addition, these muscles normally de- larities were detected between the musculature of chon- velop from their region of origin towards their region of drichthyans and placoderms, which are fossil insertion [28, 32, 33]. It remains unknown, however, if representatives of the most basal gnathostomes [7, 8]. This this temporal and spatial sequence of developmental makes them ideal extant models to study the evolution of events represents the plesiomorphic feature, present in paired (i.e., pectoral and pelvic) appendage musculature, the common ancestor of all gnathostomes. Diogo and providing a unique opportunity to investigate the develop- colleagues suggested that, in general, the developmental mental processes involved in the formation of these tis- order of appearance of the cephalic muscles of amphib- sues during early evolution of gnathostomes [9–11]. ians [28, 29] and zebrafish [34] parallels the evolutionary Sharks, in addition, belong to the living sister group of order of appearance. This is also the case for the ceph- osteichthyans (bony fish + tetrapods), where develop- alic muscles in the head, neck, and limb muscles of pri- mental studies are mostly performed, which makes them mates [35]. Developmental studies on sharks are crucial fundamental models for phylogenetic sampling (e.g., to investigate if such patterns are also seen in chon- [10–12]). Data from cyclostomes - which are the only drichthyans, exploring the conservation of these devel- extant representatives of agnathans - such as the lamprey opmental patterns within gnathostomes, and whether are also extremely relevant to understand the origin and there is a parallelism between ontogeny and phylogeny early evolution of gnathostome morphology [13–20]. in vertebrate muscle development in general. Comparative analyses have provided descriptions of Within the broader analysis of cephalic muscle devel- the musculature of the head, neck, and locomotory ap- opment in vertebrates, special attention has been given pendages across various vertebrate lineages [18, 21–26]. to the puzzling muscle cucullaris, which is deeply related However, little information is available on how and when to one of the most crucial evolutionary events during each of the specific muscles develop in organisms that vertebrate evolutionary history: the evolution of the neck may have retained plesiomorphic gnathostome features, [36]. Recently, Ziermann and colleagues proposed that as with the shark. Currie and colleagues used shark neck evolution was a long, stepwise macroevolutionary models to investigate how the mechanisms that generate event, involving a stage in which an undivided cucullaris appendicular muscles evolved [12, 27]. These authors was connected to the branchial arches and the pectoral confirmed the observations obtained in studies carried girdles [18], followed by its subdivision into the levatores out at the end of the nineteenth century showing that, in arcuum branchialium attaching to the branchial arches sharks, the appendicular musculature is formed by epi- and the protractor pectoralis attaching to the pectoral thelial somitic extensions that penetrate the fin buds girdle, in osteichthyans [18]. Subsequently, there was during development. However, their work was not fo- further differentiation of the protractor pectoralis into cused on providing a detailed description on the devel- various muscles (e.g., trapezius, sternocleidomastoideus) opment of specific muscles, such as those that connect that took place during the evolution of tetrapods, where the pectoral appendages to the skull. The only studies the head became further separated from the trunk [18]. providing details on the development of individual mus- Remarkably, recent analyses of the musculature in placo- cles of sharks were published several decades ago (e.g., derm fossils suggest that the cucullaris might not have cephalic musculature reviewed by Edgeworth [23]), but attached to the pectoral girdle in at least some of the they lack validation with novel methodological ap- members of this extinct group [36]. The comparison of proaches. Therefore, detailed studies on shark muscle the osteichthyans developmental data with the informa- development are required to further explore potential tion obtained via the detailed analyses of the develop- ancient developmental processes involved in the forma- ment of the cucullaris in chondrichthyans may offer tion of the cephalic and appendicular musculature in additional information to discuss the ancestral condition gnathostomes. of the cucullaris and thus the evolution of the neck Several studies suggest a striking conservation of the within gnathostomes. developmental patterning of cephalic muscles, which is Additionally, comprehensive myological analyses in particularly well documented in amphibians [28–31]. shark
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