Developmental change in the function of movement systems: transition of the pectoral fins between respiratory and locomotor roles in zebrafish

Abstract

An animal may experience strikingly different functional demands on its body's systems through development. One way of meeting those demands is with temporary, stage-specific adaptations. This strategy requires the animal to develop appropriate morphological states or physiological pathways that address transient functional demands as well as processes that transition morphology, physiology, and function to that of the mature form. Recent research on ray-finned (actinopterygian) fishes is a developmental transition in function of the pectoral fin, thereby providing an opportunity to examine how an organism copes with changes in the roles of its morphology between stages of its life history. As larvae, zebrafish alternate their pectoral fins in coordination with the body axis during slow swimming. The movements of their fins do not appear to contribute to the production of thrust or to stability but instead exchange fluid near the body for cutaneous respiration. The morphology of the larval fin includes a simple stage-specific endoskeletal disc overlaid by fan-shaped adductor and abductor muscles. In contrast, the musculoskeletal system of the mature fin consists of a suite of muscles and bones. Fins are extended laterally during slow swimming of the adult, without the distinct, high-amplitude left-right fin alternation of the larval fin. The morphological and functional transition of the pectoral fin occurs through juvenile development. Early in this period, at about 3 weeks post-fertilization, the gills take over respiratory function, presumably freeing the fins for other roles. Kinematic data suggest that the loss of respiratory function does not lead to a rapid switch in patterns of fin movement but rather that both morphology and movement transition gradually through the juvenile stage of development. Studies relating structure to function often focus on stable systems that are arguably well adapted for the roles they play. Examining how animals navigate transitional periods, when the link of structure to function may be less taut, provides insight both into how animals contend with such change and into the developmental pressures that shape mature form and function.

Fig. 1

Confocal images of the endoskeletal disc and pectoral fin musculature in 5 dpf larval zebrafish. Lateral view confocal slices (B–D) from the same 3D stack. (A) The endoskeletal disc (ED), distal fin membrane (FM), and basal cleithrum (stained in vivo with calcein green). AR is the pectoral fin artery that delimits the endoskeletal disc. (B) Abductor (ABD) and adductor (ADD) musculature in cross-section near their proximal end. The endoskeletal disc that separates would be in the space indicated. Hypaxial musculature (HP) lies medially to the fin. (C) Adductor muscle and a section through the abductor muscles. (D) Extent of the abductor in lateralmost view. Scale bars = 100 μm. Reprinted with permission from Thorsen and Hale (2005).

Fig. 2

Development of pectoral fin position in zebrafish. (A) Through development the pectoral fins transition to a laterally splayed resting position. (B) Change in resting angle of the pectoral fin, plotted against total length of the body and overlayed with changes in the musculoskeletal system. Additionally, general observations on movement of the fins are shown. Circles indicate coordination of the fins with the axis during slow swimming; triangles represent the pattern of slow swimming in adults, when pectoral fins splayed laterally. Reprinted with permission from Thorsen and Hale (2005).

Fig. 3

Typical movements of the pectoral fins and the body axis during slow swimming of larval zebrafish. Fins alternate between the left and right sides and in coordination with axial bending. Note bending of the fin during abduction (e.g., on right side at 40 ms), Scale bar, 1 mm. Reprinted with permission from Green et al. (2011).

Fig. 4

Fin bending and modeling of fluid movement associated with the pectoral fins. (A) Fin movement during abduction and adduction of the pectoral fins demonstrates asymmetry in bending between these phases of movement. (B) Flow modeled in a representation of fin morphology and movement of larval zebrafish. (C) Flow in a manipulated model in which the pectoral fin remains straight as they are abducted and adducted though the fin beat cycle. Fin bending during abductions increases fluid-folding in larval zebrafish, suggesting that it is adapted to support respiratory exchange (Green et al. 2013). Images are an output from modeling performed by M. H. Green and O. Curet in association with Green et al. (2013).

Fig. 5

Slow swimming by a finless larval zebrafish. A full bout of swimming at axial frequencies typical of slow swimming of larval zebrafish with fins. The magnified images of the head illustrate the stability of the finless fish in roll and yaw. Scale bar = 1 mm. Reproduced with permission from Green et al. (2011).

Fig. 6

Typical movement of the pectoral fins during slow axial swimming in a juvenile zebrafish at 35 dpf. The series shows a full, synchronized fin beat cycle at initiation followed by a single fin-stroke on each side of the body. Scale bar = 1 mm.