Ontogenetic development of inner ear hair cell organization in the New Zealand carpet shark Cephaloscyllium isabellum

Abstract

IntroductionThe inner ear hair cells of fishes can provide insight into the early evolution of vertebrate inner ear structure. Fishes represent some of the first vertebrates to evolve auditory capacity, and the same basic structure, the sensory hair cell, provides the fundament for auditory and vestibular function in jawed vertebrates. Despite holding critical basal position in the evolutionary tree of gnathostomes, relatively little is known about inner ear hair cells in elasmobranchs. Specifically, the extent of plasticity in hair cell organization throughout ontogeny among different sensory epithelia and the degree of variation between species is unknown.MethodsIn this study, we characterized the inner ear hair cells of the New Zealand carpet shark Cephaloscyllium isabellum throughout ontogeny by quantifying macular area, number of hair cells, hair cell density, and hair cell orientations in the inner ear maculae from a range of body sizes.ResultsSimilar to other elasmobranchs and bony fishes, macular area and the number of hair cells increased throughout ontogeny in the otolith organs. The orientations of hair cells within each maculae also was consistent with the limited data on other elasmobranchs. However, contrary to expectation, the macula neglecta did not increase in area or hair cell number throughout ontogeny, and hair cell density did not change with body size in any maculae.DiscussionThese findings suggest there may be variation between elasmobranch species in ontogenetic development of hair cell organization that may be related to hearing capabilities throughout life.

Interspecific Variation in the Inner Ear Maculae of Sharks

“…2007 ; Sauer et al. 2022a , b ). Since the orientation of each HC determines its physiological response to directional stimuli ( Flock and Wersäll 1962 ; Hudspeth and Corey 1977 ), HCs oriented in the dorsal and ventral directions are most sensitive to vertically propagating stimuli.…”

“…1985 ; Sauer et al. 2022a , b ), owing to a continued growth of the inner ear throughout ontogeny. However, comparative datasets spanning a wide range of ecologically and taxonomically diverse species are lacking, and relatively little is known about interspecific variability between maculae in sharks.…”

“…Hair cell density (HCD) in the otoconial organs was estimated using a stereological approach (following Sauer et al. 2022b ), whereby HCs were imaged and counted in three non-overlapping quadrats along the length of each macula (one quadrat each in the rostral, medial, and caudal sections of the maculae).…”

“…In contrast, more recently, Sauer et al. (2022a , b ) characterized variation in HC number, density, and orientation groups throughout ontogeny in Galeorhinus galeus (school shark) ( Sauer et al. 2022a ) and Cephaloscyllium isabellum (New Zealand carpet shark) ( Sauer et al.…”

“…(2022a , b ) characterized variation in HC number, density, and orientation groups throughout ontogeny in Galeorhinus galeus (school shark) ( Sauer et al. 2022a ) and Cephaloscyllium isabellum (New Zealand carpet shark) ( Sauer et al. 2022b ), demonstrating considerable intraspecific variation across all four maculae throughout life in both species.…”