Development of zebrafish paired and median fin musculature: basis for comparative, developmental, and macroevolutionary studies

Abstract

The model organism Dario rerio (zebrafish) is widely used in evo-devo and comparative studies. Nevertheless, little is known about the development and differentiation of the appendicular musculature in this fish. In this study, we examined the development of the muscles of all five zebrafish fin types (pectoral, pelvic, anal, dorsal and caudal). We describe the development of the muscles of these fins, including some muscles that were never mentioned in the literature, such as the interhypurales of the caudal fin. Interestingly, these caudal muscles are present in early stages but absent in adult zebrafishes. We also compare various stages of zebrafish fin muscle development with the configuration found in other extant fishes, including non-teleostean actinopterygians as well as cartilaginous fishes. The present work thus provides a basis for future developmental, comparative, evolutionary and evo-devo studies and emphasizes the importance of developmental works on muscles for a more comprehensive understanding of the origin, development and evolution of the appendicular appendages of vertebrate animals.

Central and peripheral innervation patterns of defined axial motor units in larval zebrafish

“…Alternatively, it could be that these relatively immature neurons are also waiting for their target muscles to 452 differentiate or mature, since the regions targeted by s'-types are sources of new muscle fibers as larvae 453 grow into adults (Hollway and Currie, 2003;Gurevich et al, 2015). Unfortunately, due to the transient 454 nature of our labeling method, we could not confirm the ultimate target of s'-types, whether new axial or 455 fin musculature (Siomava et al, 2018). 456…”

Cranial or postcranial—Dual origin of the pectoral appendage of vertebrates combining the fin‐fold and gill‐arch theories?

“…Specifically, developmentally and evolutionary, can the pectoral girdle be mainly related to the head—as proposed by Gegenbaur and recently suggested by authors such as Nagashima et al 53 (see Figure 7), Diogo and colleagues, 11‐31 or Gillis and colleagues 6,52 —and the pectoral fin be mainly associated with the trunk, as postulated by the fin‐fold theory accepted by many other researchers? If this is so, and if the pelvic appendage would be mainly related to the trunk—as currently defended by most researchers, including Nagashima et al 53 and Diogo and colleagues, 11 then (a) the pectoral and pelvic girdles would not be serial homologues; (b) the pectoral and pelvic fins could be “developmental” serial homologues; and (c) this would therefore mean that there could be a partial “developmental” serial homology between the pectoral and pelvic appendages as a whole.…”

“…For instance, according to the fin‐fold theory both appendages necessarily appeared evolutionarily at the same time as derivatives of a continuous fin fold, and according to both theories the two appendages should overall be very similar as they would derive from this continuous fold or from similar branchial structures. Instead, the fossil record shows (a) that the pectoral girdle and/or fins seemingly originated earlier in evolution and (b) that in the vast majority of the earlier fishes that did have both of them, these appendages were actually quite different anatomically from each other, particularly their girdle components 7‐32 . Therefore, the main reason why most researchers started to be more receptive about the fin‐fold theory was because of developmental studies, including, more recently, the discovery of shared expression of developmental patterning genes between paired and dorsal median fins 1,33,34 .…”

“…This has led to a major, recurrent problem with both the notion of serial homology and the way the links between the pectoral and pelvic appendages are discussed until today: the fact that these topics were originally not framed within an evolutionary context, but instead within an idealized theoretical “archetype” one. That is, although the idea of such an “ideal polysomeric archetype” has been more and more discredited, the a priori assumption that serial homologues, and that the pectoral and pelvic appendages in particular, were necessarily originally similar continues to be highly influential nowadays 11‐31,43,44 . This a priori assumption neglects the fact that in reality the so‐called “serial homology” between the pectoral and pelvic appendages postulated by authors such as Oken and Owen actually refers to what is now consensually called “evolutionary parallelism,” which is therefore a subset of homoplasy, not of true homology 11,43,44 .…”

Central and peripheral innervation patterns of defined axial motor units in larval zebrafish

“…Fast-twitch units (m-type and ms-type) are more likely to have collaterals and be interconnected. We also propose fast units would be more likely to innervate the equivalent of Renshaw cells in fish, namely V1 interneurons (see Section 4 for details), which have more potent inhibitory inputs to slow units [Color figure can be viewed at wileyonlinelibrary.com] Unfortunately, due to the transient nature of our labeling method, we could not confirm the ultimate target of s'-types, whether new axial or fin musculature(Siomava, Shkil, Voronezhskaya, & Diogo, 2018).Our work also suggests that at larval stages the solution to generating intermediate forces and speeds is to innervate more lateral fast-twitch and slow muscle fibers via ms-type secondary motor neurons. By adulthood, zebrafish have developed axial muscle fibers with intermediate "pink" contractile properties that can be found in the transition from slow to fast-twitch muscle fibers at the horizon-…”