Developmental process and homeostasis of whale long bones lacking medullary cavity using the radius of Antarctic minke whales, Balaenoptera bonaerensis.

Abstract

Whales, Earth's largest mammals and live in water, form long bones without marrow cavities. Body size and mechanical stress impact the bone formation and homeostasis, yet the specific developmental processes remain unclear. Here, we demonstrate the histological changes in whale long bones from fetal to mature stages using the radius of Antarctic minke whales in comparison with domestic cats and cattle. Through intramembranous ossification and remodeling, long bones enlarge their diameters and marrow cavities, respectively. It has been demonstrated that relatively small animals, such as cats, develop the radially arranged "primary osteonal bone", whereas larger animals, including cattle, form "laminar bone" initiated by the formation of circumferentially arranged hypercalcified lines during intramembranous ossification. Here, we demonstrated that whales form laminar bones, transitioning from circumferential in the fetus to radial during postnatal growth, and thereafter cortical bones become compact. After maturation, bone remodeling primarily occurs in the lateral and medial regions of long bones, while the bone layers in the cranial-caudal region never undergo complete resorption. As a result, these layers remain as a wire-netting structure composed of thin bone layers, without forming an open medullary cavity. These data suggest that whales enlarge their long bones through laminar bone formation and form long bones without a marrow cavity by regulating bone resorption areas during the developmental process and in maintaining homeostasis.