Muscle development in the shark Scyliorhinus canicula: implications for the evolution of the gnathostome head and paired appendage musculature

Janine M Ziermann,Renata Freitas,Rui Diogo

doi:10.1186/s12983-017-0216-y

Abstract

BackgroundThe 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.ResultsHere 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.ConclusionOur 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.

Highlights

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
Pectoral fin development and muscle differentiation The development of the cephalic and appendicular musculature of S. canicula is summarized in Table 1 and shown in Figs. 1, 2, 3, 4, 5 and 6
Cephalic muscle development occurs following a lateral to ventral myogenic progression, which resemble the process described in osteichthyans such as zebrafish, lungfish, amphibians, and birds [28,29,30,31,32,33, 70, 72]. This pattern is clearer in the branchial arches than in the mandibular and hyoid arches, with the mandibular arch being the only exception: the ventral intermandibularis develops before the other muscles of the first arch, which are more lateral. In both the head and paired appendages of S. canicula, muscles normally develop from their region of origin to their region of insertion, as was previously reported for the cephalic musculature of other osteichthyans [28, 29, 32, 33, 70]

Summary

Introduction

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. Striking similarities were detected between the musculature of chondrichthyans and placoderms, which are fossil representatives of the most basal gnathostomes [7, 8]. This makes them ideal extant models to study the evolution of paired (i.e., pectoral and pelvic) appendage musculature, providing a unique opportunity to investigate the developmental processes involved in the formation of these tissues during early evolution of gnathostomes [9,10,11]. Data from cyclostomes - which are the only extant representatives of agnathans - such as the lamprey are extremely relevant to understand the origin and early evolution of gnathostome morphology [13,14,15,16,17,18,19,20]

Methods

Results

Discussion

Conclusion