Mechano-chemical regulation of bat wing bones for flight.

ABSTRACT

Distal phalanges in bat wings have been hypothesized to be cartilaginous to allow for flight. We provide new evidence on how bat wing development might facilitate flight though protein-based regulation of bone mineralization and lead to more deflection at phalanx than humerus. Between Pteropus poliocephalus and Pteropus hypomelanus, two large bat species, we detected 112 proteins including 11 associated with mineralization and analyzed their distribution between the wing bones. Here, in contrast to previous reports, we found no cartilage-specific proteins and demonstrate that distal phalanges in bat wings are in fact low density bone that contain collagen I (the main constituent of bone's organic matrix) and proteins associated with mineralization in bone such as osteomodulin, bone-specific protein osteocalcin. The functional relevance of these changes was explored by measuring changes in mineral (crystal sizes, packing and density), material (Young's modulus and hardness) and structural characteristics. Consistent with changes in proteins associated with mineralization, mineral crystal thickness and alignment decreased from humerus to phalanges, and the mineral platelets were less densely packed along the wing length. Crystal thickness was negatively correlated with proteins associated with inhibition of mineralization as well as with two types of small leucine-rich proteoglycans, indicating the mineral growth and maturity is down regulated by these proteins independent of mineral quantity. The Young's modulus decreased across the wing and was significantly correlated with bone mineral density. Thus, the results from two bat species, studied here, demonstrate progressive alterations in bone mineralization occur in concert with the changes in secretion of bone regulatory proteins along the wing length. This altered mineralization together with structural changes serve to lighten the limb bone and optimize biomechanical properties conducive to flight.