Ultra-high matrix mineralization of sperm whale auditory ossicles facilitates high sound pressure and high-frequency underwater hearing

The auditory ossicles-malleus, incus and stapes-are the smallest bones in mammalian bodies and enable stable sound transmission to the inner ear. Sperm whales are one of the deepest diving aquatic mammals that produce and perceive sounds with extreme loudness greater than 180 dB and frequencies higher than 30 kHz. Therefore, it is of major interest to decipher the microstructural basis for these unparalleled hearing abilities. Using a suite of high-resolution imaging techniques, we reveal that auditory ossicles of sperm whales are highly functional, featuring an ultra-high matrix mineralization that is higher than their teeth. On a micro-morphological and cellular level, this was associated with osteonal structures and osteocyte lacunar occlusions through calcified nanospherites (i.e. micropetrosis), while the bones were characterized by a higher hardness compared to a vertebral bone of the same animals as well as to human auditory ossicles. We propose that the ultra-high mineralization facilitates the unique hearing ability of sperm whales. High matrix mineralization represents an evolutionary conserved or convergent adaptation to middle ear sound transmission.