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Edgeworth's legacy of cranial muscle development with an analysis of muscles in the ventral gill arch region of batoid fishes (Chondrichthyes: Batoidea)

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Edgeworth's legacy of cranial muscle development with an analysis of muscles in the ventral gill arch region of batoid fishes (Chondrichthyes: Batoidea)

Auteurs : Tsutomu Miyake [Canada] ; John D. Mceachran [États-Unis] ; Brian K. Hall [Canada]

Source :

RBID : ISTEX:E1D734D9834DF9F9313545EF5E38CB8F300847AF

Abstract

A series of studies by Edgeworth demonstrated that cranial muscles of gnathostome fishes are embryologically of somitic origin, originating from the mandibular, hyoid, branchial, epibranchial, and hypobranchial muscle plates. Recent experimental studies using quail‐chick chimeras support Edgeworth's view on the developmental origin of cranial muscles. One of his findings, the existence of the premyogenic condensation constrictor dorsalis in teleost fishes, has also been confirmed by molecular developmental studies. Therefore, developmental mechanisms for patterning of cranial muscles, as described and implicated by Edgeworth, may serve as structural entities or regulatory phenomena responsible for developmental and evolutionary changes. With Edgeworth's and other studies as background, muscles in the ventral gill arch region of batoid fishes are analyzed and compared with those of other gnathostome fishes. The spiracularis is regarded as homologous at least within batoid fishes, but its status within elasmobranchs remains unclear; developmental modifications of the spiracularis proper are evident in some batoid fishes and in several shark groups. The peculiar ventral extension of the spiracularis in electric rays and some stingrays may represent convergence, probably facilitating ventilation and/or feeding in both groups. The evolutionary origin of the “internus” and “externus” remains uncertain, despite the fact that a variety of forms of the constrictor superficiales ventrales in batoid fishes indicates an actual medio‐ventral extension of the “externus.” The intermandibularis is probably present only in electric rays. The “X” muscle occurs only in electric rays and is considered to be Edgeworth's intermandibularis profundus. Its association with the adductor mandibular complex in narkinidid and narcinidid electric rays may relate to its functional role in lower jaw movement. Contrary to common belief, in most batoid fishes as well as some sharks, muscles that originate from the branchial muscle plate and extend medially in the ventral gill arches do exist: the medial extension of the interbranchiales in most batoid fishes and some sharks and the “Y” muscle in the pelagic stingrays Myliobatos and Rhinoptera. The latter is another example of the medial extension of the “internus.” Whether the interbranchiales and “Y” muscle are homologous within elasmobranchs and whether homologous with the obliques ventrales and/or transversi ventrales of osteichthyan fishes await further research. Four hypobranchial muscles are recognized in batoid fishes: the coracomandibularis, coracohyoideus, coracoarcualis, and coracohyomandibularis. The coracohyoideus is discrete from the coracoarcualis; its complete structural separation from the latter occurs in several groups of batoid fishes. The sternohyoideus of osteichthyan fishes is regarded as a partially developed, continuous bundle of muscle whose counterpart in chondrichthyan fishes appears to be the fully developed rectus cervicus in holocephalans and the squaloid shark Isistius. The coracoarculais is, therefore, present structurally and possibly functionally as a discrete muscle only in elasmobranchs. Although the coracohyomandibularis has been regarded as unique in batoid fishes, the first coracobranchialis in the sawshark Pristiophorus may represent the coracohyomandibularis. The conceptual frameworks and results of the development and evolution of cranial muscles presented here emphasize the importance of molecular and experimental embryological studies and integration of these areas with comparative anatomical and functional studies. Edgeworth's contributions remain as a remarkable achievement in muscle biology. © 1992 Wiley‐Liss, Inc.

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DOI: 10.1002/jmor.1052120304

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<div type="abstract" xml:lang="en">A series of studies by Edgeworth demonstrated that cranial muscles of gnathostome fishes are embryologically of somitic origin, originating from the mandibular, hyoid, branchial, epibranchial, and hypobranchial muscle plates. Recent experimental studies using quail‐chick chimeras support Edgeworth's view on the developmental origin of cranial muscles. One of his findings, the existence of the premyogenic condensation constrictor dorsalis in teleost fishes, has also been confirmed by molecular developmental studies. Therefore, developmental mechanisms for patterning of cranial muscles, as described and implicated by Edgeworth, may serve as structural entities or regulatory phenomena responsible for developmental and evolutionary changes. With Edgeworth's and other studies as background, muscles in the ventral gill arch region of batoid fishes are analyzed and compared with those of other gnathostome fishes. The spiracularis is regarded as homologous at least within batoid fishes, but its status within elasmobranchs remains unclear; developmental modifications of the spiracularis proper are evident in some batoid fishes and in several shark groups. The peculiar ventral extension of the spiracularis in electric rays and some stingrays may represent convergence, probably facilitating ventilation and/or feeding in both groups. The evolutionary origin of the “internus” and “externus” remains uncertain, despite the fact that a variety of forms of the constrictor superficiales ventrales in batoid fishes indicates an actual medio‐ventral extension of the “externus.” The intermandibularis is probably present only in electric rays. The “X” muscle occurs only in electric rays and is considered to be Edgeworth's intermandibularis profundus. Its association with the adductor mandibular complex in narkinidid and narcinidid electric rays may relate to its functional role in lower jaw movement. Contrary to common belief, in most batoid fishes as well as some sharks, muscles that originate from the branchial muscle plate and extend medially in the ventral gill arches do exist: the medial extension of the interbranchiales in most batoid fishes and some sharks and the “Y” muscle in the pelagic stingrays Myliobatos and Rhinoptera. The latter is another example of the medial extension of the “internus.” Whether the interbranchiales and “Y” muscle are homologous within elasmobranchs and whether homologous with the obliques ventrales and/or transversi ventrales of osteichthyan fishes await further research. Four hypobranchial muscles are recognized in batoid fishes: the coracomandibularis, coracohyoideus, coracoarcualis, and coracohyomandibularis. The coracohyoideus is discrete from the coracoarcualis; its complete structural separation from the latter occurs in several groups of batoid fishes. The sternohyoideus of osteichthyan fishes is regarded as a partially developed, continuous bundle of muscle whose counterpart in chondrichthyan fishes appears to be the fully developed rectus cervicus in holocephalans and the squaloid shark Isistius. The coracoarculais is, therefore, present structurally and possibly functionally as a discrete muscle only in elasmobranchs. Although the coracohyomandibularis has been regarded as unique in batoid fishes, the first coracobranchialis in the sawshark Pristiophorus may represent the coracohyomandibularis. The conceptual frameworks and results of the development and evolution of cranial muscles presented here emphasize the importance of molecular and experimental embryological studies and integration of these areas with comparative anatomical and functional studies. Edgeworth's contributions remain as a remarkable achievement in muscle biology. © 1992 Wiley‐Liss, Inc.</div>
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