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 α-glycerophosphate dehydrogenase (α-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.

Muscle function in avian flight: achieving power and control

“…85% in pigeons) with a smaller component of fast-glycolytic (type IIb) fibres [20,21]. Fibre-type composition of the supracoracoideus, to my knowledge, has not been examined in pigeons, but in the European starling is composed of a greater fraction (68%) of fast-glycolytic versus fastoxidative fibres [22]; whereas, in zebra finches, Anna's hummingbirds [23] and Atlantic puffins [24], the supracoracoideus is exclusively composed of fast-oxidative fibres.…”

Evolution of central pattern generators and rhythmic behaviours

“…The evolution of flight involved changes not only in the morphology and musculature of the forelimbs, but in the pattern of neural activity that drives them [61,62] and in the sensory feedback that they receive [63]. Comparisons of muscle histology in birds suggest further that changes in muscle chemistry also played a role in the evolution of flight movements [61]. Flight behaviour has diverged significantly across birds from the graceful flapping of owls to the rapid movements of hummingbirds [64].…”

Forelimb kinematics and motor patterns of the slider turtle (Trachemys scripta) during swimming and walking: shared and novel strategies for meeting locomotor demands of water and land

“…The idea that new patterns of movement can be achieved while conserving the patterns of muscle activity is commonly described as the neuromotor conservation hypothesis (Peters and Goslow, 1983;Smith, 1994). Despite the drastic diversity in structure and locomotion across vertebrate taxa, remarkably similar patterns of limb muscle activation have been documented across behaviors ranging from sprawling and upright terrestrial locomotion to flight (Peters and Goslow, 1983;Goslow et al, 1989;Dial et al, 1991;Fish, 1996;Goslow et al, 2000). This has led to the hypothesis that patterns of neuromotor control for homologous tetrapod muscles are evolutionarily conserved, despite modifications to the limb muscles and skeleton for different uses (Jenkins and Goslow, 1983;Peters and Goslow, 1983;Smith, 1994).…”