Neuromuscular Correlates to the Evolution of Flapping Flight in Birds

Abstract

The neuromotor pattern (i.e. the onset/offset of muscle contraction within the locomotor cycle) is conserved for some homologous muscles of the tetrapod shoulder but not others in the transition from terrestrial locomotion to flight. Here we test for three shoulder muscles of the European starling (Sturnus vulgaris) to determine whether retention of, or deviation from, a conserved neuromotor pattern can be predicted on the basis of the location of the muscle's motor nucleus within the motor column and the histochemical profile of its constituent muscle fibers. The M. supracoracoideus, the major wing elevator, illustrates a neuromotor pattern that has shifted in its timing within the limb movement cycle. Of the two heads of the triceps, the electrical activity pattern of M. humerotriceps is conserved during the transition, whereas that of the M. scapulotriceps is not. We reacted serial sections of each muscle for myosin adenosine triphosphotase (ATPase), nicotinamide adenine dinucleotide diaphorase (NADH-D), and alpha-glycerophosphate dehydrogenase (alpha-GPD) to characterize all muscles into two fiber types: fast glycolytic (FG) and fast oxidative glycolytic (FOG). We used retrograde axonal tracers to determine the longitudinal distribution and topographical organization of the motoneurons within the motor column in the spinal cord. The histochemical profile of each muscle studied is unique and is statistically different from its homologue in non-avian tetrapods. Compared to non-avian tetrapods, the spatial location of the motor nucleus of the supracoracoideus is conserved. The topology of the two heads of the triceps is fundamentally conserved relative to the other test muscles, but relative to one another there is some spatial segregation which might reflect their respective functional specializations. These data indicate that an evolutionary change in neuromotor pattern can occur without a corresponding topological reorganization of a muscle's motor nucleus within the motor column. Nor can the histochemical profile of homologous muscles be used to predict their neuromotor pattern in the transition from terrestrial locomotion to flight. These findings suggest that evolutionary change in neuromotor outflow relates to altered synaptic input from supraspinal or segmental sources or by alteration of factors intrinsic to individual motoneurons.