Development and Evolution of the Muscles of the Pelvic Fin

Cole, Nicholas J.; Hall, Thomas; Don, Emily K.; Berger, Silke; Boisvert, Catherine A.; Neyt, Christine; Ericsson, Rolf; Joss, Jean; Gurevich, David; Currie, Peter D.

doi:10.1371/journal.pbio.1001168

Cited by 60 publications

(69 citation statements)

References 34 publications

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“…They are the sister group of all other living gnathostomes, and their embryos can be used to gain insight into the development of the last common ancestor of all vertebrates with paired appendages (45,46). During muscle development in chondrichthyans, both appendicular and body wall musculature derive from epithelial extensions of the ventral dermomyotome (47,48). DP312 labeling presented here in Scyliorhinus shows a clean boundary between labeled mesenchyme derived from the DM and unlabeled mesenchyme of presumed lateral plate origin at both fin and interfin levels (Fig.…”

Section: Discussionmentioning

confidence: 99%

Body wall development in lamprey and a new perspective on the origin of vertebrate paired fins

Tulenko

McCauley

MacKenzie

et al. 2013

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

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Classical hypotheses regarding the evolutionary origin of paired appendages propose transformation of precursor structures (gill arches and lateral fin folds) into paired fins. During development, gnathostome paired appendages form as outgrowths of body wall somatopleure, a tissue composed of somatic lateral plate mesoderm (LPM) and overlying ectoderm. In amniotes, LPM contributes connective tissue to abaxial musculature and forms ventrolateral dermis of the interlimb body wall. The phylogenetic distribution of this character is uncertain because lineage analyses of LPM have not been generated in anamniotes. We focus on the evolutionary history of the somatopleure to gain insight into the tissue context in which paired fins first appeared. Lampreys diverged from other vertebrates before the acquisition of paired fins and provide a model for investigating the preappendicular condition. We present vital dye fate maps that suggest the somatopleure is eliminated in lamprey as the LPM is separated from the ectoderm and sequestered to the coelomic linings during myotome extension. We also examine the distribution of postcranial mesoderm in catshark and axolotl. In contrast to lamprey, our findings support an LPM contribution to the trunk body wall of these taxa, which is similar to published data for amniotes. Collectively, these data lead us to hypothesize that a persistent somatopleure in the lateral body wall is a gnathostome synapomorphy, and the redistribution of LPM was a key step in generating the novel developmental module that ultimately produced paired fins. These embryological criteria can refocus arguments on paired fin origins and generate hypotheses testable by comparative studies on the source, sequence, and extent of genetic redeployment.

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Section: Discussionmentioning

confidence: 99%

Body wall development in lamprey and a new perspective on the origin of vertebrate paired fins

Tulenko

McCauley

MacKenzie

et al. 2013

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

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“…The first method was transplantation of labelled tissues, using a modified zebrafish protocol1920 (Fig. 2).…”

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confidence: 99%

Trunk exoskeleton in teleosts is mesodermal in origin

et al. 2013

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The vertebrate mineralized skeleton is known to have first emerged as an exoskeleton that extensively covered the fossil jawless fish. The evolutionary origin of this exoskeleton has long been attributed to the emergence of the neural crest, but experimental evaluation for this is still poor. Here we determine the embryonic origin of scales and fin rays of medaka (teleost trunk exoskeletons) by applying long-term cell labelling methods, and demonstrate that both tissues are mesodermal in origin. Neural crest cells, however, fail to contribute to these tissues. This result suggests that the trunk neural crest has no skeletogenic capability in fish, instead highlighting the dominant role of the mesoderm in the evolution of the trunk skeleton. This further implies that the role of the neural crest in skeletogenesis has been predominant in the cephalic region from the early stage of vertebrate evolution.

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“…Somites anterior to 10 and posterior to 11 do not contribute precursors to pelvic fin muscles 17 . We also found that if the host transplant was not initially placed ventrally enough in the host during the operation then the donor precursors would fail to contribute to the pelvic fin muscles even though the a large portion of the body wall muscle would be made from the donor tissue 17 . It was clear the ventral tip of the extension was the source of the pelvic fin muscle precursors.…”

Section: Examining Pelvic Fin Muscle Formationmentioning

confidence: 97%

Shaping muscle bioarchitecture for the fin to limb transition

Cole

Currie

2012

BioArchitecture

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Our recent paper examined how pelvic fins and their musculature form developmentally and how these mechanisms have evolved within the vertebrate lineage, a process fundamental to the tetrapod transition. The transition from the water onto the land is among one of the most well studied steps in the evolutionary history of vertebrates, yet the genetic basis of this evolutionary transition is little studied and ill-defined. The advent of these terrestrial species resulted in a shift in locomotor strategies from the rhythmic undulating muscles of the fish body to a reliance upon powerful weight bearing muscles of the limbs to generate movement. We demonstrated that the pelvic fin muscles of bony fish are generated by a mechanism that has features of both of limb/fin muscle formation in tetrapods and primitive cartilaginous fish. We hypothesize that the adoption of the fully derived mode of hindlimb muscle formation, was a further modification of the mode of development deployed to generate pelvic fin muscles, a shift in overall muscle bioarchitecture we believe was critical to the success of the tetrapod transition.

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Development and Evolution of the Muscles of the Pelvic Fin

Cited by 60 publications

References 34 publications

Body wall development in lamprey and a new perspective on the origin of vertebrate paired fins

Body wall development in lamprey and a new perspective on the origin of vertebrate paired fins

Trunk exoskeleton in teleosts is mesodermal in origin

Shaping muscle bioarchitecture for the fin to limb transition

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