Cranial muscle development in frogs with different developmental modes: Direct development versus biphasic development

Abstract

Normal development in anurans includes a free swimming larva that goes through metamorphosis to develop into the adult frog. We have investigated cranial muscle development and adult cranial muscle morphology in three different anuran species. Xenopus laevis is obligate aquatic throughout lifetime, Rana(Lithobates) pipiens has an aquatic larvae and a terrestrial adult form, and Eleutherodactylus coqui has direct developing juveniles that hatch from eggs deposited on leaves (terrestrial). The adult morphology shows hardly any differences between the investigated species. Cranial muscle development of E. coqui shows many similarities and only few differences to the development of Rana (Lithobates) and Xenopus. The differences are missing muscles of the branchial arches (which disappear during metamorphosis of biphasic anurans) and a few heterochronic changes. The development of the mandibular arch (adductor mandibulae) and hyoid arch (depressor mandibulae) muscles is similar to that observed in Xenopus and Rana (Lithobates), although the first appearance of these muscles displays a midmetamorphic pattern in E. coqui. We show that the mix of characters observed in E. coqui indicates that the larval stage is not completely lost even without a free swimming larval stage. Cryptic metamorphosis is the process in which morphological changes in the larva/embryo take place that are not as obvious as in normal metamorphosing anurans with a clear biphasic lifestyle. During cryptic metamorphosis, a normal adult frog develops, indicating that the majority of developmental mechanisms towards the functional adult cranial muscles are preserved.

Cephalic muscle development in the Australian lungfish, Neoceratodus forsteri

“…However, the protractor pectoralis always seems to be the lateral portion of the most posterior branchial arch levators. In anurans and caudates, four levatores arcuum branchialium are followed by the dilatator laryngis (Edgeworth, ; Ziermann & Diogo, ; Ziermann & Olsson, ), which is similar to the observations in N. forsteri . Fox () suggests that his levatores arcuum branchialium 5 and 6 include fibers that are homologous to the dilatator laryngis and the cucullaris (protractor pectoralis) muscle.…”

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

“…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]. The only exceptions, within the cephalic muscles analyzed by us, are the coracomandibularis, coracoarcualis and the coracobranchiales , which developed in the head region from their adult region of insertion (mandible, ceratohyal, and branchial arches, respectively) and then extend posteriorly during development towards their adult region of origin (pectoral girdle).…”

“…It remains unknown, however, if this temporal and spatial sequence of developmental events represents the plesiomorphic feature, present in the common ancestor of all gnathostomes. Diogo and colleagues suggested that, in general, the developmental order of appearance of the cephalic muscles of amphibians [28, 29] and zebrafish [34] parallels the evolutionary order of appearance. This is also the case for the cephalic muscles in the head, neck, and limb muscles of primates [35].…”

A new heart for a new head in vertebrate cardiopharyngeal evolution

“…1) derive from the cucullaris, a muscle that probably appeared in early gnathostomes and was found in fossil placoderms 5,6,48,64,65 . Among extant gnathostomes, some of the anatomical and developmental characteristics of the cucullaris are shared with branchiomeric and somite-derived limb, epibranchial and hypobranchial muscles 57,66,67 . Most available data, however, indicate that the cucullaris is a branchiomeric muscle derived from the posterior-most pharyngeal arches, as suggested by Edgeworth 22,68–71 .…”