Neural development of the zebrafish (Danio rerio) pectoral fin.

The innervation and actuation of limbs have been major areas of research in motor control. Here we describe the innervation of the pectoral fins of the larval zebrafish (Danio rerio) and its ontogeny. Imaging and genetic tools available in this species provide opportunities to add new perspectives to the growing body of work on limbs. We used immunocytological and gross histological techniques with confocal microscopy to characterize the pattern of pectoral fin nerves. We retrogradely labeled fin neurons to describe the distributions of the pectoral fin motor pool in the spinal cord. At 5 days postfertilization, four nerves innervate the pectoral fins. We found that the rostral three nerves enter the fin from the dorsal side of the fin base and service the dorsal and middle fin regions. The fourth nerve enters the fin from the ventral fin base and innervates the ventral region. We found no mediolateral spatial segregation between adductor and abductor cell bodies in the spinal cord. During the larval stage pectoral fins have one adductor and one abductor muscle with an endoskeletal disc between them. As the skeleton and muscles expand and differentiate through postlarval development, there are major changes in fin innervation including extensive elaboration to the developing muscles and concentration of innervation to specific nerves and fin regions. The pattern of larval fin innervation recorded is associated with later muscle subdivision, suggesting that fin muscles may be functionally subdivided before they are morphologically subdivided.

Diversity of pectoral fin structure and function in fishes with labriform propulsion.

Aquatic propulsion generated by the pectoral fins occurs in many groups of perciform fishes, including numerous coral reef families. This study presents a detailed survey of pectoral fin musculoskeletal structure in fishes that use labriform propulsion as the primary mode of swimming over a wide range of speeds. Pectoral fin morphological diversity was surveyed in 12 species that are primarily pectoral swimmers, including members of all labroid families (Labridae, Scaridae, Cichlidae, Pomacentridae, and Embiotocidae) and five additional coral reef fish families. The anatomy of the pectoral fin musculature is described, including muscle origins, insertions, tendons, and muscle masses. Skeletal structures are also described, including fin shape, fin ray morphology, and the structure of the radials and pectoral girdle. Three novel muscle subdivisions, including subdivisions of the abductor superficialis, abductor profundus, and adductor medialis were discovered and are described here. Specific functional roles in fin control are proposed for each of the novel muscle subdivisions. Pectoral muscle masses show broad variation among species, particularly in the adductor profundus, abductor profundus, arrector dorsalis, and abductor superficialis. A previously undescribed system of intraradial ligaments was also discovered in all taxa studied. The morphology of these ligaments and functional ramifications of variation in this connective tissue system are described. Musculoskeletal patterns are interpreted in light of recent analyses of fin behavior and motor control during labriform swimming. Labriform propulsion has apparently evolved independently multiple times in coral reef fishes, providing an excellent system in which to study the evolution of pectoral fin propulsion.

Pectoral fin coordination and gait transitions in steadily swimming juvenile reef fishes.

A common feature of animal locomotion is its organization into gaits with distinct patterns of movement and propulsor use for specific speeds. In terrestrial vertebrates, limb gaits have been extensively studied in diverse taxa and gait transitions have been shown to provide efficient locomotion across a wide range of speeds. In contrast, examination of gaits in fishes has focused on axial gaits and the transition between synchronous paired fin locomotion and axial propulsion. Because many fishes use their pectoral fins as their primary propulsors, we aimed to examine more broadly the use of pectoral fin gaits in locomotion. We used juvenile reef fishes in these experiments because their swimming could be recorded readily across a wide range of Reynolds numbers, which we thought would promote gait diversity. Based on previous work in larval fishes, we hypothesized that juveniles have alternating pectoral fin movements rather than the synchronous, or in-phase, coordination pattern of adults. In flow tank swim studies, we found that juvenile sapphire damselfish Pomacentrus pavo used two fin gaits during steady swimming. Below approximately 3 BL s(-1), P. pavo primarily swam with alternating fin strokes 180 degrees out of phase with one another. At speeds in the range of 3-4 BL s(-1), they performed a gait transition to synchronous fin coordination. Between approximately 4 and 8 BL s(-1), P. pavo primarily beat their fins synchronously. At around 8 BL s(-1) there was another gait transition to body-caudal fin swimming, in which the pectoral fins were tucked against the body. We suggest that the transition from alternating to synchronous fin coordination occurs due to mechanical limits of gait performance rather than to energy efficiency, stability or transitions in hydrodynamic regime. To determine whether this gait transition was species-specific, we surveyed pectoral fin locomotion in juveniles from 11 species in three reef fish families (Pomacentridae, Labridae and Scaridae). We found that this gait transition occurred in every species examined, suggesting that it may be a common behavior of juvenile reef fishes. Greater inclusion of early life history stages in the study of fin-based locomotion should significantly enhance and inform the growing body of work on these behaviors.

Swimming of larval zebrafish: fin-axis coordination and implications for function and neural control.

Adult actinopterygian fishes typically perform steady forward swimming using either their pectoral fins or their body axis as the primary propulsor. In most species, when axial undulation is employed for swimming, the pectoral fins are tucked (i.e. adducted) against the body; conversely, when pectoral fins are beating, the body axis is held straight. In contrast to adults, larval fishes can combine their pectoral fin and body-axis movements during locomotion; however, little is known about how these locomotor modes are coordinated. With this study we provide a detailed analysis of the coordinated fin and axial movements during slow and fast swimming by examining forward locomotion in larval zebrafish (Danio rerio L.). In addition, we describe the musculature that powers pectoral fin movement in larval zebrafish and discuss its functional implications. As larvae, zebrafish alternate their pectoral fins during slow swimming (0.011+/-0.001 mm ms(-1)) in conjunction with axial undulations of the same frequency (18-28 Hz). During fast swimming (0.109+/-0.030 mm ms(-1); 36-67 Hz), the fins are tucked against the body and propulsion occurs by axial undulation alone. We show that during swimming, larval fishes can use a similar limb-axis coordination pattern to that of walking and running salamanders. We suggest that the fin-axis coordination observed in larval zebrafish may be attributed to a primitive neural circuit and that early terrestrial vertebrates may have gained the ability to coordinate limbs and lateral bending by retaining a larval central pattern generator for limb-axis coordination in the adult life history stage.