The morphology and evolution of chondrichthyan cranial muscles: A digital dissection of the elephantfish <i>Callorhinchus milii</i> and the catshark <i>Scyliorhinus canicula</i>

Dearden, Richard P.; Mansuit, Rohan; Cuckovic, Antoine; Herrel, Anthony; Didier, Dominique A.; Tafforeau, Paul; Pradel, Alan

doi:10.1111/joa.13362

Cited by 14 publications

(13 citation statements)

References 71 publications

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“…In the holocephalan crown-group, a much smaller posterior mandibular adductor also inserts on the suborbital ridge and preorbital fascia, which in chimaerids is reduced to a small patch of muscle fibers ( 13 , 30 ). It seems likely that there was also a posterior part of the mandibular adductor in Iniopera, which inserted in the bottom part of the orbit ( 30 ). Ventrally delimited fossae on the Meckelian cartilages ( Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Ventrally delimited fossae on the Meckelian cartilages ( Fig. 1 A ) suggest that the mandibular adductor inserted directly on the mandible as in shark-like chondrichthyans, rather than into a tendinous submandibular “sling” like living holocephalans ( 13 , 14 , 30 ). The attachment area of the epaxial muscles on the neurocranial roof is small compared with Callorhinchus ( Fig.…”

Section: Resultsmentioning

confidence: 99%

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Evidence for high-performance suction feeding in the Pennsylvanian stem-group holocephalan Iniopera

Dearden

Herrel

Pradel

2023

Proc. Natl. Acad. Sci. U.S.A.

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The Carboniferous (358.9 to 298.9 Ma) saw the emergence of marine ecosystems dominated by modern vertebrate groups, including abundant stem-group holocephalans (chimaeras and relatives). Compared with the handful of anatomically conservative holocephalan genera alive today—demersal durophages all—these animals were astonishingly morphologically diverse, and bizarre anatomies in groups such as iniopterygians hint at specialized ecological roles foreshadowing those of the later, suction-feeding neopterygians. However, flattened fossils usually obscure these animals’ functional morphologies and how they fitted into these important early ecosystems. Here, we use three-dimensional (3D) methods to show that the musculoskeletal anatomy of the uniquely 3D-preserved iniopterygian Iniopera can be best interpreted as being similar to that of living holocephalans rather than elasmobranchs but that it was mechanically unsuited to durophagy. Rather, Iniopera had a small, anteriorly oriented mouth aperture, expandable pharynx, and strong muscular links among the pectoral girdle, neurocranium, and ventral pharynx consistent with high-performance suction feeding, something exhibited by no living holocephalan and never clearly characterized in any of the extinct members of the holocephalan stem-group. Remarkably, in adapting a distinctly holocephalan anatomy to suction feeding, Iniopera is more comparable to modern tetrapod suction feeders than to the more closely related high-performance suction-feeding elasmobranchs. This raises questions about the assumed role of durophagy in the evolution of holocephalans’ distinctive anatomy and offers a rare glimpse into the breadth of ecological niches filled by holocephalans in a pre-neopterygian world.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Evidence for high-performance suction feeding in the Pennsylvanian stem-group holocephalan Iniopera

Dearden

Herrel

Pradel

2023

Proc. Natl. Acad. Sci. U.S.A.

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“…Prey capture is accomplished by several adaptations in their jaw musculature, and even special modifications in the dentition, as seen in C. plagiosum [ 42 ]. A noticeable trait difference between C. punctatum and S. canicula is the sharp bending of the posterior margin of the lower jaw, which forms the sustentaculum in bamboo shark species, but which is not so prominent in the catshark [ 42 , 43 ]. This is probably a consequence of the specialisation for suction feeding, which is characteristic for Orectolobiformes [ 27 , 28 ].…”

Section: Discussionmentioning

confidence: 99%

“…F.B.). Furthermore, the shape difference of the mandibular apparatus between both species is evident in their adult forms [ 42 , 43 ]. A major difference is also expressed in their early development with the bamboo shark developing at a faster rate than the catshark [ 37 , 44 ].…”

Section: Introductionmentioning

confidence: 99%

Early shape divergence of developmental trajectories in the jaw of galeomorph sharks

et al. 2022

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Background The onset of morphological differences between related groups can be tracked at early stages during embryological development. This is expressed in functional traits that start with minor variations, but eventually diverge to defined specific morphologies. Several processes during this period, like proliferation, remodelling, and apoptosis for instance, can account for the variability observed between related groups. Morphological divergence through development is often associated with the hourglass model, in which early stages display higher variability and reach a conserved point with reduced variability from which divergence occurs again to the final phenotype. Results Here we explored the patterns of developmental shape changes in the lower jaw of two shark species, the bamboo shark (Chiloscyllium punctatum) and the catshark (Scyliorhinus canicula). These two species present marked differences in their foraging behaviour, which is reflected in their adult jaw morphology. By tracing the developmental sequence of the cartilage condensation, we identified the onset of cartilage for both species at around stage 31. Other structures that developed later without a noticeable anlage were the labial cartilages, which appear at around stage 33. We observed that the lower jaw displays striking differences in shape from the earliest moments, without any overlap in shape through the compared stages. Conclusions The differences observed are also reflected in the functional variation in feeding mechanism between both species. Likewise, the trajectory analysis shows that the main differences are in the magnitude of the shape change through time. Both species follow a unique trajectory, which is explained by the timing between stages.

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“…Our work has been greatly aided through reading the historical literature written by the original comparative anatomists and embryologists, much of which appears to have largely been forgotten or overlooked. Such works are treasure stores of much needed anatomical and embryological data that can inform current comparative analyses of different outgroups to bracket evolutionary transitions (Boisvert et al, 2013;Dearden et al, 2021). This will help form hypotheses on evolutionary processes that have shaped the vertebrate skeleton, which can be tested with fossil data that can possess well preserved soft tissues for analyses of the musculature (Trinajstic et al, 2013(Trinajstic et al, , 2018.…”

Section: Discussionmentioning

confidence: 99%

Imaging With the Past: Revealing the Complexity of Chimaeroid Pelvic Musculature Anatomy and Development

et al. 2022

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Chondrichthyans are now widely adopted as models for examining the development and evolution of the stem gnathostome body plan. The fins of some cartilaginous fish are recognized for their plesiomorphic form and mode of muscular development, i.e., epithelial extension. Despite detailed molecular and descriptive examinations of these developmental mechanisms, there has been little contemporary examination of the ontogeny and morphology of the musculature in chondrichthyans including that of the paired fins. This gap represents a need for further examination of the developmental morphology of these appendicular musculatures to gain insight into their evolution in gnathostomes. The elephant shark is a Holocephalan, the sister group of all other chondrichthyans (Holocephali: Callorhinchus milii). Here, we use nano-CT imaging and 3D reconstructions to describe the development of the pelvic musculature of a growth series of elephant shark embryos. We also use historical descriptions from the nineteenth century and traditional dissection methods to describe the adult anatomy. This combined approach, using traditional methods and historical knowledge with modern imaging techniques, has enabled a more thorough examination of the anatomy and development of the pelvic musculature revealing that chimaeroid musculatures are more complex than previously thought. These data, when compared to extant and extinct sister taxa, are essential for interpreting and reconstructing fossil musculatures as well as understanding the evolution of paired fins.

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The morphology and evolution of chondrichthyan cranial muscles: A digital dissection of the elephantfish Callorhinchus milii and the catshark Scyliorhinus canicula

Abstract: The morphology and evolution of chondrichthyan cranial muscles: a digital dissection of the elephantfish Callorhinchus milii and the catshark Scyliorhinus canicula.

Cited by 14 publications

References 71 publications

Evidence for high-performance suction feeding in the Pennsylvanian stem-group holocephalan Iniopera

Evidence for high-performance suction feeding in the Pennsylvanian stem-group holocephalan Iniopera

Early shape divergence of developmental trajectories in the jaw of galeomorph sharks

Imaging With the Past: Revealing the Complexity of Chimaeroid Pelvic Musculature Anatomy and Development

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